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The role of mycotoxins in neurodegenerative diseases: current state of the art and future perspectives of research

  • Vu Thu Thuy Nguyen , Svenja König , Simone Eggert ORCID logo , Kristina Endres ORCID logo EMAIL logo and Stefan Kins EMAIL logo
Published/Copyright: August 27, 2021

Abstract

Mycotoxins are fungal metabolites that can cause various diseases in humans and animals. The adverse health effects of mycotoxins such as liver failure, immune deficiency, and cancer are well-described. However, growing evidence suggests an additional link between these fungal metabolites and neurodegenerative diseases. Despite the wealth of these initial reports, reliable conclusions are still constrained by limited access to human patients and availability of suitable cell or animal model systems. This review summarizes knowledge on mycotoxins associated with neurodegenerative diseases and the assumed underlying pathophysiological mechanisms. The limitations of the common in vivo and in vitro experiments to identify the role of mycotoxins in neurotoxicity and thereby in neurodegenerative diseases are elucidated and possible future perspectives to further evolve this research field are presented.


Corresponding authors: Kristina Endres, Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg-University Mainz, Untere Zahlbacher Str. 8, D-55131 Mainz, Germany; and Stefan Kins, Department of Human Biology and Human Genetics, University of Kaiserslautern, Erwin-Schrödinger-Straße 13, D-67663 Kaiserslautern, Germany, E-mail: (K. Endres), (S. Kins)
Vu Thu Thuy Nguyen and Svenja König contributed equally to this article.

Funding source: MWG Rhineland-Palatinate

Award Identifier / Grant number: NeurodegX Forschungskolleg

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: All authors were funded by the MWG Rhineland-Palatinate (NeurodegX Forschungskolleg).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Al Shoyaib, A., Archie, S.R., and Karamyan, V.T. (2019). Intraperitoneal route of drug administration: should it be used in experimental animal studies? Pharm. Res. 37: 12, https://doi.org/10.1007/s11095-019-2745-x.Search in Google Scholar PubMed PubMed Central

Alessenko, A.V. and Albi, E. (2020). Exploring sphingolipid implications in neurodegeneration. Front. Neurol. 11: 59–63, doi:https://doi.org/10.3389/fneur.2020.00437.Search in Google Scholar PubMed PubMed Central

Alonso, R., Pisa, D., Fernández-Fernández, A.M., and Carrasco, L. (2018). Infection of fungi and bacteria in brain tissue from elderly persons and patients with Alzheimer’s disease. Front. Aging Neurosci. 10: 159, https://doi.org/10.3389/fnagi.2018.00159.Search in Google Scholar PubMed PubMed Central

Alonso, R., Pisa, D., Fernandez-Fernandez, A.M., Rabano, A., and Carrasco, L. (2017). Fungal infection in neural tissue of patients with amyotrophic lateral sclerosis. Neurobiol. Dis. 108: 249–260, https://doi.org/10.1016/j.nbd.2017.09.001.Search in Google Scholar PubMed

Alonso, R., Pisa, D., Marina, A.I., Morato, E., Rabano, A., Rodal, I., and Carrasco, L. (2015a). Evidence for fungal infection in cerebrospinal fluid and brain tissue from patients with amyotrophic lateral sclerosis. Int. J. Biol. Sci. 11: 546–558, https://doi.org/10.7150/ijbs.11084.Search in Google Scholar PubMed PubMed Central

Alonso, R., Pisa, D., Rábano, A., and Carrasco, L. (2014). Alzheimer’s disease and disseminated mycoses. Eur. J. Clin. Microbiol. Infect. Dis. 33: 1125–1132, https://doi.org/10.1007/s10096-013-2045-z.Search in Google Scholar PubMed

Alonso, R., Pisa, D., Rábano, A., Rodal, I., and Carrasco, L. (2015b). Cerebrospinal fluid from alzheimer’s disease patients contains fungal proteins and DNA. J Alzheimers Dis 47: 873–876, https://doi.org/10.3233/jad-150382.Search in Google Scholar PubMed

Alsayyah, A., Elmazoudy, R., Al-Namshan, M., Al-Jafary, M., and Alaqeel, N. (2019). Chronic neurodegeneration by aflatoxin B1 depends on alterations of brain enzyme activity and immunoexpression of astrocyte in male rats. Ecotoxicol. Environ. Saf. 182: 109407, https://doi.org/10.1016/j.ecoenv.2019.109407.Search in Google Scholar PubMed

Alshannaq, A. and Yu, J.H. (2017). Occurrence, toxicity, and analysis of major mycotoxins in food. Int. J. Environ. Res. Publ. Health 14: 6, doi:https://doi.org/10.3390/ijerph14060632.Search in Google Scholar PubMed PubMed Central

Alston, T.A., Mela, L., and Bright, H.J. (1977). 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase. Proc. Natl. Acad. Sci. U. S. A. 74: 3767–3771, https://doi.org/10.1073/pnas.74.9.3767.Search in Google Scholar PubMed PubMed Central

Anfossi, L., Giovannoli, C., and Baggiani, C. (2016). Mycotoxin detection. Curr. Opin. Biotechnol. 37: 120–126, https://doi.org/10.1016/j.copbio.2015.11.005.Search in Google Scholar PubMed

Ao, Z., Cai, H., Havert, D.J., Wu, Z., Gong, Z., Beggs, J.M., Mackie, K., and Guo, F. (2020). One-stop microfluidic assembly of human brain organoids to model prenatal cannabis exposure. Anal Chem 92: 4630–4638, doi:10.1021/acs.analchem.0c00205.10.1021/acs.analchem.0c00205Search in Google Scholar PubMed

Ardhanareeswaran, K., Mariani, J., Coppola, G., Abyzov, A., and Vaccarino, F.M. (2017). Human induced pluripotent stem cells for modelling neurodevelopmental disorders. Nat. Rev. Neurol. 13: 265–278, https://doi.org/10.1038/nrneurol.2017.45.Search in Google Scholar PubMed PubMed Central

Axelsson, V., Holback, S., Sjogren, M., Gustafsson, H., and Forsby, A. (2006a). Gliotoxin induces caspase-dependent neurite degeneration and calpain-mediated general cytotoxicity in differentiated human neuroblastoma SH-SY5Y cells. Biochem. Biophys. Res. Commun. 345: 1068–1074, https://doi.org/10.1016/j.bbrc.2006.05.019.Search in Google Scholar PubMed

Axelsson, V., Pikkarainen, K., and Forsby, A. (2006b). Glutathione intensifies gliotoxin-induced cytotoxicity in human neuroblastoma SH-SY5Y cells. Cell Biol. Toxicol. 22: 127–136, https://doi.org/10.1007/s10565-006-0048-6.Search in Google Scholar PubMed

Bahey, N.G., Abd Elaziz, H.O., and Gadalla, K.K. (2015). Toxic effect of aflatoxin B1 and the role of recovery on the rat cerebral cortex and hippocampus. Tissue Cell 47: 559–566, https://doi.org/10.1016/j.tice.2015.09.001.Search in Google Scholar PubMed

Banczerowski-Pelyhe, I., Vilagi, I., Detri, L., Doczi, J., Kovacs, F., and Kukorelli, T. (2002). In vivo and in vitro electrophysiological monitoring of rat neocortical activity after dietary fumonisin exposure. Mycopathologia 153: 149–156, https://doi.org/10.1023/a:1014584303427.10.1023/A:1014584303427Search in Google Scholar

Battilani, P., Toscano, P., Van der fels-Klerx, H.J., Moretti, A., Camardo Leggieri, M., Brera, C., Rortais, A., Goumperis, T., and Robinson, T. (2016). Aflatoxin B1 contamination in maize in Europe increases due to climate change. Sci. Rep. 6: 24328, https://doi.org/10.1038/srep24328.Search in Google Scholar PubMed PubMed Central

Beal, M.F., Brouillet, E., Jenkins, B.G., Ferrante, R.J., Kowall, N.W., Miller, J.M., Storey, E., Srivastava, R., Rosen, B.R., and Hyman, B.T. (1993). Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13: 4181–4192, https://doi.org/10.1523/jneurosci.13-10-04181.1993.Search in Google Scholar

Belmadani, A., Tramu, G., Betbeder, A.M., and Creppy, E.E. (1998a). Subchronic effects of ochratoxin A on young adult rat brain and partial prevention by aspartame, a sweetener. Hum. Exp. Toxicol. 17: 380–386, https://doi.org/10.1191/096032798678908981.Search in Google Scholar

Belmadani, A., Tramu, G., Betbeder, A.M., Steyn, P.S., and Creppy, E.E. (1998b). Regional selectivity to ochratoxin A, distribution and cytotoxicity in rat brain. Arch. Toxicol. 72: 656–662, https://doi.org/10.1007/s002040050557.Search in Google Scholar

Benjelloun, N., Charriaut-Marlangue, C., Hantaz-Ambroise, D., Ménard, A., Pierig, R., Alliel, P.M., and Rieger, F. (2002). Induction of cell death in rat brain by a gliotoxic factor from cerebrospinal fluid in multiple sclerosis. Cell. Mol. Biol. 48: 205–212.Search in Google Scholar

Bennett, J.W. and Klich, M. (2003). Mycotoxins. Clin. Microbiol. Rev. 16: 497–516, https://doi.org/10.1128/cmr.16.3.497-516.2003.Search in Google Scholar

Berntsen, H.F., Bogen, I.L., Wigestrand, M.B., Fonnum, F., Walaas, S.I., and Moldes-Anaya, A. (2017). The fungal neurotoxin penitrem A induces the production of reactive oxygen species in human neutrophils at submicromolar concentrations. Toxicology 392: 64–70, https://doi.org/10.1016/j.tox.2017.10.008.Search in Google Scholar

Berntsen, H.F., Wigestrand, M.B., Bogen, I.L., Fonnum, F., Walaas, S.I., and Moldes-Anaya, A. (2013). Mechanisms of penitrem-induced cerebellar granule neuron death in vitro: possible involvement of GABAA receptors and oxidative processes. Neurotoxicology 35: 129–136, https://doi.org/10.1016/j.neuro.2013.01.004.Search in Google Scholar

Bhandari, N., He, Q., and Sharma, R.P. (2001). Gender-related differences in subacute fumonisin B1 hepatotoxicity in BALB/c mice. Toxicology 165: 195–204, https://doi.org/10.1016/s0300-483x(01)00449-8.Search in Google Scholar

Bhat, P.V., Anand, T., Mohan Manu, T., and Khanum, F. (2018). Restorative effect of L-dopa treatment against Ochratoxin A induced neurotoxicity. Neurochem. Int. 118: 252–263, https://doi.org/10.1016/j.neuint.2018.04.003.Search in Google Scholar

Bhat, P.V., Pandareesh, M., Khanum, F., and Tamatam, A. (2016). Cytotoxic effects of ochratoxin A in neuro-2a cells: role of oxidative stress evidenced by N-acetylcysteine. Front. Microbiol. 7: 1142, https://doi.org/10.3389/fmicb.2016.01142.Search in Google Scholar

Bonsi, P., Augusti-Tocco, G., Palmery, M., and Giorgi, M. (1999). Aflatoxin B1 is an inhibitor of cyclic nucleotide phosphodiesterase activity. Gen. Pharmacol. 32: 615–619, https://doi.org/10.1016/s0306-3623(98)00282-1.Search in Google Scholar

Boyd, K.E., Fitzpatrick, D.W., Wilson, J.R., and Wilson, L.M. (1988). Effect of T-2 toxin on brain biogenic monoamines in rats and chickens. Can. J. Vet. Res. 52: 181–185, https://doi.org/10.1086/269136.Search in Google Scholar

Bradford, H.F., Norris, P.J., and Smith, C.C. (1990). Changes in transmitter release patterns in vitro induced by tremorgenic mycotoxins. J. Environ. Pathol. Toxicol. Oncol. 10: 17–30, https://doi.org/10.1016/0263-8231(90)90003-h.Search in Google Scholar

Brand, B., Stoye, N.M., Guilherme, M.D.S., Nguyen, V.T.T., Baumgaertner, J.C., Schuffler, A., Thines, E., and Endres, K. (2019). Identification of patulin from Penicillium coprobium as a toxin for enteric neurons. Molecules 24: 15, doi:https://doi.org/10.3390/molecules24152776.Search in Google Scholar

Bredesen, D.E. (2016). Inhalational Alzheimer’s disease: an unrecognized - and treatable - epidemic. Aging 8: 304–313, https://doi.org/10.18632/aging.100896.Search in Google Scholar

Brouillet, E., Hantraye, P., Dolan, R., Leroy-Willig, A., Bottlaender, M., Isacson, O., Maziere, M., Ferrante, R., and Beal, M. (1993a). Chronic administration of 3-nitropropionic acid induced selective striatal degeneration and abnormal choreiform movements in monkeys. Soc. Neurosci. Abstr.: 409.Search in Google Scholar

Brouillet, E., Jenkins, B.G., Hyman, B.T., Ferrante, R.J., Kowall, N.W., Srivastava, R., Roy, D.S., Rosen, B.R., and Beal, M.F. (1993b). Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J. Neurochem. 60: 356–359, https://doi.org/10.1111/j.1471-4159.1993.tb05859.x.Search in Google Scholar

Brouillet, E., Hantraye, P., Ferrante, R.J., Dolan, R., Leroy-Willig, A., Kowall, N.W., and Beal, M.F. (1995). Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc. Natl. Acad. Sci. U. S. A. 92: 7105–7109, https://doi.org/10.1073/pnas.92.15.7105.Search in Google Scholar

Bullerman, L.B. (1979). Significance of mycotoxins to food safety and human health. J. Food Protect. 42: 65–86, https://doi.org/10.4315/0362-028x-42.1.65.Search in Google Scholar

Bunge, I., Dirheimer, G., and Roschenthaler, R. (1978). In vivo and in vitro inhibition of protein synthesis in Bacillus stearothermophilus by ochratoxin A. Biochem. Biophys. Res. Commun. 83: 398–405, https://doi.org/10.1016/0006-291x(78)91004-5.Search in Google Scholar

Castanedo-Vazquez, D., Bosque-Varela, P., Sainz-Pelayo, A., and Riancho, J. (2019). Infectious agents and amyotrophic lateral sclerosis: another piece of the puzzle of motor neuron degeneration. J. Neurol. 266: 27–36, https://doi.org/10.1007/s00415-018-8919-3.Search in Google Scholar

Chaudhary, M. and Rao, P.V. (2010). Brain oxidative stress after dermal and subcutaneous exposure of T-2 toxin in mice. Food Chem. Toxicol. 48: 3436–3442, https://doi.org/10.1016/j.fct.2010.09.018.Search in Google Scholar

Coulombe, R.A.Jr. and Sharma, R.P. (1985). Effect of repeated dietary exposure of aflatoxin B1 on brain biogenic amines and metabolites in the rat. Toxicol. Appl. Pharmacol. 80: 496–501, https://doi.org/10.1016/0041-008x(85)90394-1.Search in Google Scholar

Creppy, E.E., Chakor, K., Fisher, M.J., and Dirheimer, G. (1990). The myocotoxin ochratoxin A is a substrate for phenylalanine hydroxylase in isolated rat hepatocytes and in vivo. Arch. Toxicol. 64: 279–284, https://doi.org/10.1007/bf01972987.Search in Google Scholar PubMed

Creppy, E.E., Kern, D., Steyn, P.S., Vleggaar, R., Roschenthaler, R., and Dirheimer, G. (1983). Comparative study of the effect of ochratoxin A analogues on yeast aminoacyl-tRNA synthetases and on the growth and protein synthesis of hepatoma cells. Toxicol. Lett. 19: 217–224, https://doi.org/10.1016/0378-4274(83)90122-4.Search in Google Scholar

da Silva, A.S., Santurio, J.M., Roza, L.F., Bottari, N.B., Galli, G.M., Morsch, V.M., Schetinger, M.R.C., Baldissera, M.D., Stefani, L.M., Radavelli, W.M., et al.. (2017). Aflatoxins produced by Aspergillus parasiticus present in the diet of quails increase the activities of cholinesterase and adenosine deaminase. Microb. Pathog. 107: 309–312, https://doi.org/10.1016/j.micpath.2017.03.041.Search in Google Scholar

Dalziel, J.E., Finch, S.C., and Dunlop, J. (2005). The fungal neurotoxin lolitrem B inhibits the function of human large conductance calcium-activated potassium channels. Toxicol. Lett. 155: 421–426, https://doi.org/10.1016/j.toxlet.2004.11.011.Search in Google Scholar

Daviaud, N., Garbayo, E., Lautram, N., Franconi, F., Lemaire, L., Perez-Pinzon, M., and Montero-Menei, C.N. (2014). Modeling nigrostriatal degeneration in organotypic cultures, a new ex vivo model of Parkinson’s disease. Neuroscience 256: 10–22, https://doi.org/10.1016/j.neuroscience.2013.10.021.Search in Google Scholar

de Melo, F.T., De Oliveira, I.M., Greggio, S., Dacosta, J.C., Guecheva, T.N., Saffi, J., Henriques, J.A., and Rosa, R.M. (2012). DNA damage in organs of mice treated acutely with patulin, a known mycotoxin. Food Chem. Toxicol. 50: 3548–3555, https://doi.org/10.1016/j.fct.2011.12.022.Search in Google Scholar

Delibas, N., Altuntas, I., Yonden, Z., and Ozcelik, N. (2003). Ochratoxin A reduces NMDA receptor subunits 2A and 2B concentrations in rat hippocampus: partial protective effect of melatonin. Hum. Exp. Toxicol. 22: 335–339, https://doi.org/10.1191/0960327103ht357oa.Search in Google Scholar

Desai, K., Sullards, M.C., Allegood, J., Wang, E., Schmelz, E.M., Hartl, M., Humpf, H.U., Liotta, D.C., Peng, Q., and Merrill, A.H.Jr. (2002). Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis. Biochim. Biophys. Acta 1585: 188–192, https://doi.org/10.1016/s1388-1981(02)00340-2.Search in Google Scholar

Doi, K. and Uetsuka, K. (2011). Mechanisms of mycotoxin-induced neurotoxicity through oxidative stress-associated pathways. Int. J. Mol. Sci. 12: 5213–5237, https://doi.org/10.3390/ijms12085213.Search in Google Scholar PubMed PubMed Central

Domijan, A.M. (2012). Fumonisin B(1): a neurotoxic mycotoxin. Arh. Hig. Rada. Toksikol. 63: 531–544, https://doi.org/10.2478/10004-1254-63-2012-2239.Search in Google Scholar PubMed

Domijan, A.M. and Abramov, A.Y. (2011). Fumonisin B1 inhibits mitochondrial respiration and deregulates calcium homeostasis--implication to mechanism of cell toxicity. Int. J. Biochem. Cell Biol. 43: 897–904, https://doi.org/10.1016/j.biocel.2011.03.003.Search in Google Scholar PubMed

Domijan, A.M., Kovac, S., and Abramov, A.Y. (2012). Impact of fumonisin B1 on glutamate toxicity and low magnesium-induced seizure activity in neuronal primary culture. Neuroscience 202: 10–16, https://doi.org/10.1016/j.neuroscience.2011.12.005.Search in Google Scholar

Egbunike, G.N. and Ikegwuonu, F.I. (1984). Effect of aflatoxicosis on acetylcholinesterase activity in the brain and adenohypophysis of the male rat. Neurosci. Lett. 52: 171–174, https://doi.org/10.1016/0304-3940(84)90369-0.Search in Google Scholar

Eiser, A.R. (2017). Why does Finland have the highest dementia mortality rate? Environmental factors may be generalizable. Brain Res. 1671: 14–17, https://doi.org/10.1016/j.brainres.2017.06.032.Search in Google Scholar PubMed

Escher, B.I., Hackermüller, J., Polte, T., Scholz, S., Aigner, A., Altenburger, R., Böhme, A., Bopp, S.K., Brack, W., and Busch, W., et al.. (2016). From the exposome to mechanistic understanding of chemical-induced adverse effects. Environ. Int 99: 97–106, doi:10.1016/j.envint.2016.11.029.10.1016/j.envint.2016.11.029Search in Google Scholar PubMed PubMed Central

Eskola, M., Elliott, C.T., Hajslova, J., Steiner, D., and Krska, R. (2020a). Towards a dietary-exposome assessment of chemicals in food: an update on the chronic health risks for the European consumer. Crit. Rev. Food Sci. Nutr. 60: 1890–1911, https://doi.org/10.1080/10408398.2019.1612320.Search in Google Scholar PubMed

Eskola, M., Kos, G., Elliott, C.T., Hajslova, J., Mayar, S., and Krska, R. (2020b). Worldwide contamination of food-crops with mycotoxins: validity of the widely cited ’FAO estimate’ of 25. Crit. Rev. Food Sci. Nutr. 60: 2773–2789, https://doi.org/10.1080/10408398.2019.1658570.Search in Google Scholar PubMed

Ferrante, R.J. (1993). Striatal pathology of impaired mitochondrial metabolism in primnates profiles Huntington’s disease. Soc. Neurosci. Abstr. 19: 408.Search in Google Scholar

Ferrante, R.J. (2009). Mouse models of Huntington’s disease and methodological considerations for therapeutic trials. Biochim. Biophys. Acta 1792: 506–520, https://doi.org/10.1016/j.bbadis.2009.04.001.Search in Google Scholar PubMed PubMed Central

Foran, E. and Trotti, D. (2009). Glutamate transporters and the excitotoxic path to motor neuron degeneration in amyotrophic lateral sclerosis. Antioxidants Redox Signal. 11: 1587–1602, https://doi.org/10.1089/ars.2009.2444.Search in Google Scholar PubMed PubMed Central

Freese, C., Reinhardt, S., Hefner, G., Unger, R.E., Kirkpatrick, C.J., and Endres, K. (2014). A novel blood-brain barrier co-culture system for drug targeting of Alzheimer’s disease: establishment by using acitretin as a model drug. PloS One 9: e91003, https://doi.org/10.1371/journal.pone.0091003.Search in Google Scholar PubMed PubMed Central

French, P.W., Ludowyke, R.I., and Guillemin, G.J. (2019). Fungal-contaminated grass and well water and sporadic amyotrophic lateral sclerosis. Neural Regen. Res. 14: 1490–1493, https://doi.org/10.4103/1673-5374.255959.Search in Google Scholar PubMed PubMed Central

Gabrielson, K.L., Hogue, B.A., Bohr, V.A., Cardounel, A.J., Nakajima, W., Kofler, J., Zweier, J.L., Rodriguez, E.R., Martin, L.J., De Souza-Pinto, N.C., et al.. (2001). Mitochondrial toxin 3-nitropropionic acid induces cardiac and neurotoxicity differentially in mice. Am. J. Pathol. 159: 1507–1520, https://doi.org/10.1016/s0002-9440(10)62536-9.Search in Google Scholar

Gajęcka, M., Stopa, E., Tarasiuk, M., Zielonka, L., and Gajęcki, M. (2013). The expression of type-1 and type-2 nitric oxide synthase in selected tissues of the gastrointestinal tract during mixed mycotoxicosis. Toxins 5: 2281–2292, https://doi.org/10.3390/toxins5112281.Search in Google Scholar PubMed PubMed Central

Galvano, F., Campisi, A., Russo, A., Galvano, G., Palumbo, M., Renis, M., Barcellona, M.L., Perez-Polo, J.R., and Vanella, A. (2002). DNA damage in astrocytes exposed to fumonisin B1. Neurochem. Res. 27: 345–351, https://doi.org/10.1023/a:1014971515377.10.1023/A:1014971515377Search in Google Scholar

Gelineau-Van Waes, J., Starr, L., Maddox, J., Aleman, F., Voss, K.A., Wilberding, J., and Riley, R.T. (2005). Maternal fumonisin exposure and risk for neural tube defects: mechanisms in an in vivo mouse model. Birth Defects Res. A Clin. Mol. Teratol. 73: 487–497, https://doi.org/10.1002/bdra.20148.Search in Google Scholar PubMed

Gerding, J., Ali, N., Schwartzbord, J., Cramer, B., Brown, D.L., Degen, G.H., and Humpf, H.U. (2015). A comparative study of the human urinary mycotoxin excretion patterns in Bangladesh, Germany, and Haiti using a rapid and sensitive LC-MS/MS approach. Mycotoxin Res. 31: 127–136, https://doi.org/10.1007/s12550-015-0223-9.Search in Google Scholar PubMed

Giussani, P., Prinetti, A., and Tringali, C. (2021). The role of Sphingolipids in myelination and myelin stability and their involvement in childhood and adult demyelinating disorders. J. Neurochem. 156: 403–414, https://doi.org/10.1111/jnc.15133.Search in Google Scholar PubMed

Goers, L., Freemont, P., and Polizzi, K.M. (2014). Co-culture systems and technologies: taking synthetic biology to the next level. J. R. Soc. Interface 11: 96, doi:https://doi.org/10.1098/rsif.2014.0065.Search in Google Scholar PubMed PubMed Central

Graham, M.L. and Prescott, M.J. (2015). The multifactorial role of the 3Rs in shifting the harm-benefit analysis in animal models of disease. Eur. J. Pharmacol. 759: 19–29, https://doi.org/10.1016/j.ejphar.2015.03.040.Search in Google Scholar PubMed PubMed Central

Guo, P., Liu, A., Huang, D., Wu, Q., Fatima, Z., Tao, Y., Cheng, G., Wang, X., and Yuan, Z. (2018). Brain damage and neurological symptoms induced by T-2 toxin in rat brain. Toxicol. Lett. 286: 96–107, https://doi.org/10.1016/j.toxlet.2018.01.012.Search in Google Scholar PubMed

Haley, R.W. (2003a). Excess incidence of ALS in young Gulf War veterans. Neurology 61: 750, https://doi.org/10.1212/wnl.61.6.750.Search in Google Scholar PubMed

Haley, R.W. (2003b). Gulf war syndrome: narrowing the possibilities. Lancet Neurol. 2: 272–273, https://doi.org/10.1016/s1474-4422(03)00376-4.Search in Google Scholar

Han, N., Luo, R., Liu, J., Guo, T., Feng, J., and Peng, X. (2020). Transcriptomic and proteomic analysis reveals mechanisms of patulin-induced cell toxicity in human embryonic kidney cells. Toxins 12: 11, doi:https://doi.org/10.3390/toxins12110681.Search in Google Scholar

Hanley, A.B., Mcbride, J., Oehlschlager, S., and Opara, E. (1999). Use of a flow cell bioreactor as a chronic toxicity model system. Toxicol. Vitro 13: 847–851, https://doi.org/10.1016/s0887-2333(99)00053-3.Search in Google Scholar

Harel, R. and Futerman, A.H. (1993). Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J. Biol. Chem. 268: 14476–14481, https://doi.org/10.1016/s0021-9258(19)85263-8.Search in Google Scholar

Heidtmann-Bemvenuti, R., Mendes, G.L., Scaglioni, P.T., Badiale-Furlong, E., and Souza-Soares, L.A. (2011). Biochemistry and metabolism of mycotoxins: a review. Afr. J. Food Sci. 5: 861–869, doi:https://doi.org/10.5897/ajfsx11.009.Search in Google Scholar

Helms, H.C., Abbott, N.J., Burek, M., Cecchelli, R., Couraud, P.O., Deli, M.A., Forster, C., Galla, H.J., Romero, I.A., Shusta, E.V., et al.. (2016). In vitro models of the blood-brain barrier: an overview of commonly used brain endothelial cell culture models and guidelines for their use. J. Cerebr. Blood Flow Metabol. 36: 862–890, https://doi.org/10.1177/0271678x16630991.Search in Google Scholar

Hirsch, C. and Schildknecht, S. (2019). In vitro research reproducibility: keeping up high standards. Front. Pharmacol. 10: 1484, https://doi.org/10.3389/fphar.2019.01484.Search in Google Scholar

Hotujac, L., Muftic, R.H., and Filipovic, N. (1976). Verruculogen: a new substance for decreasing of GABA levels in CNS. Pharmacology 14: 297–300, https://doi.org/10.1159/000136608.Search in Google Scholar

IARC (2012). Monographs on the evaluation of carcinogenic risks to humans: chemical agents and related occupations. A review of human carcinogens. International Agency for Research on Cancer, Lyon.Search in Google Scholar

Ikegwuonu, F.I. (1983). The neurotoxicity of aflatoxin B1 in the rat. Toxicology 28: 247–259, https://doi.org/10.1016/0300-483x(83)90121-x.Search in Google Scholar

Ismaiel, A.A. and Papenbrock, J. (2015). Mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture 5: 492–537, https://doi.org/10.3390/agriculture5030492.Search in Google Scholar

Israel, M.A., Yuan, S.H., Bardy, C., Reyna, S.M., Mu, Y., Herrera, C., Hefferan, M.P., Van Gorp, S., Nazor, K.L., Boscolo, F.S., et al.. (2012). Probing sporadic and familial Alzheimer’s disease using induced pluripotent stem cells. Nature 482: 216–220, https://doi.org/10.1038/nature10821.Search in Google Scholar

Janik, E., Niemcewicz, M., Ceremuga, M., Stela, M., Saluk-Bijak, J., Siadkowski, A., and Bijak, M. (2020). Molecular aspects of mycotoxins - a serious problem for human health. Int. J. Mol. Sci. 21: 21, https://doi.org/10.3390/ijms21218187.Search in Google Scholar

Jayasekara, S., Drown, D.B., Coulombe, R.A.Jr., and Sharma, R.P. (1989). Alteration of biogenic amines in mouse brain regions by alkylating agents. I. Effects of aflatoxin B1 on brain monoamines concentrations and activities of metabolizing enzymes. Arch. Environ. Contam. Toxicol. 18: 396–403, https://doi.org/10.1007/bf01062364.Search in Google Scholar

Jo, J., Xiao, Y., Sun, A.X., Cukuroglu, E., Tran, H.D., Goke, J., Tan, Z.Y., Saw, T.Y., Tan, C.P., Lokman, H., et al.. (2016). Midbrain-like organoids from human pluripotent stem cells contain functional dopaminergic and neuromelanin-producing neurons. Cell Stem Cell 19: 248–257, https://doi.org/10.1016/j.stem.2016.07.005.Search in Google Scholar

Kadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M., and Sasai, Y. (2013). Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc. Natl. Acad. Sci. U. S. A. 110: 20284–20289, https://doi.org/10.1073/pnas.1315710110.Search in Google Scholar

Kellerman, T.S., Marasas, W.F., Thiel, P.G., Gelderblom, W.C., Cawood, M., and Coetzer, J.A. (1990). Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. Onderstepoort J. Vet. Res. 57: 269–275.Search in Google Scholar

Kimbrough, T.D., Llewellyn, G.C., and Weekley, L.B. (1992). The effect of aflatoxin B1 exposure on serotonin metabolism: response to a tryptophan load. Metab. Brain Dis. 7: 175–182, https://doi.org/10.1007/bf01000244.Search in Google Scholar

Kodsi, M.H. and Swerdlow, N.R. (1997). Mitochondrial toxin 3-nitropropionic acid produces startle reflex abnormalities and striatal damage in rats that model some features of Huntington’s disease. Neurosci. Lett. 231: 103–107, https://doi.org/10.1016/s0304-3940(97)00482-5.Search in Google Scholar

Kovacic, S., Pepeljnjak, S., Petrinec, Z., and Klaric, M.S. (2009). Fumonisin B1 neurotoxicity in young carp (Cyprinus carpio L.). Arh. Hig. Rada. Toksikol. 60: 419–426.10.2478/10004-1254-60-2009-1974Search in Google Scholar PubMed

Kovalevich, J. and Langford, D. (2013). Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology. Methods Mol. Biol. 1078: 9–21, https://doi.org/10.1007/978-1-62703-640-5_2.Search in Google Scholar PubMed PubMed Central

Koziolek, M., Alcaro, S., Augustijns, P., Basit, A.W., Grimm, M., Hens, B., Hoad, C.L., Jedamzik, P., Madla, C.M., Maliepaard, M., et al.. (2019). The mechanisms of pharmacokinetic food-drug interactions – a perspective from the UNGAP group. Eur. J. Pharmaceut. Sci. 134: 31–59, https://doi.org/10.1016/j.ejps.2019.04.003.Search in Google Scholar PubMed

Kunkanjanawan, T., Noisa, P., and Parnpai, R. (2011). Modeling neurological disorders by human induced pluripotent stem cells. J. Biomed. Biotechnol. 2011: 350131, https://doi.org/10.1155/2011/350131.Search in Google Scholar

Kwon, O.S., Sandberg, J.A., and Slikker, W.Jr. (1997a). Effects of fumonisin B1 treatment on blood-brain barrier transfer in developing rats. Neurotoxicol. Teratol. 19: 151–155, https://doi.org/10.1016/s0892-0362(96)00217-6.Search in Google Scholar

Kwon, O.S., Schmued, L.C., and Slikker, W.Jr. (1997b). Fumonisin B1 in developing rats alters brain sphinganine levels and myelination. Neurotoxicology 18: 571–579.Search in Google Scholar

Kwon, O.S., Slikker, W.Jr., and Davies, D.L. (2000). Biochemical and morphological effects of fumonisin B(1) on primary cultures of rat cerebrum. Neurotoxicol. Teratol. 22: 565–572, https://doi.org/10.1016/s0892-0362(00)00082-9.Search in Google Scholar

Liew, W.-P.-P. and Mohd-Redzwan, S. (2018). Mycotoxin: its impact on gut health and microbiota. Front. Cell. Infect. Microbiol. 8: 60, https://doi.org/10.3389/fcimb.2018.00060.Search in Google Scholar PubMed PubMed Central

Lorenz, N., Danicke, S., Edler, L., Gottschalk, C., Lassek, E., Marko, D., Rychlik, M., and Mally, A. (2019). A critical evaluation of health risk assessment of modified mycotoxins with a special focus on zearalenone. Mycotoxin Res. 35: 27–46, https://doi.org/10.1007/s12550-018-0328-z.Search in Google Scholar PubMed PubMed Central

Lu, H.X., Levis, H., Melhem, N., and Parker, T. (2008). Toxin-produced Purkinje cell death: a model for neural stem cell transplantation studies. Brain Res. 1207: 207–213, https://doi.org/10.1016/j.brainres.2008.02.034.Search in Google Scholar PubMed

Ludolph, A., Seelig, M., Ludolph, A., Novitt, P., Allen, C., Spencer, P., and Sabri, M. (1992). 3-Nitropropionic acid decreases cellular energy levels and causes neuronal degeneration in cortical explants. Neurodegeneration 1: 21–28.Search in Google Scholar

Malekinejad, H., Aghazadeh-Attari, J., Rezabakhsh, A., Sattari, M., and Ghasemsoltani-Momtaz, B. (2015). Neurotoxicity of mycotoxins produced in vitro by Penicillium roqueforti isolated from maize and grass silage. Hum. Exp. Toxicol. 34: 997–1005, https://doi.org/10.1177/0960327114565493.Search in Google Scholar PubMed

Mao, Z., Choo, Y.S., and Lesort, M. (2006). Cystamine and cysteamine prevent 3-NP-induced mitochondrial depolarization of Huntington’s disease knock-in striatal cells. Eur. J. Neurosci. 23: 1701–1710, https://doi.org/10.1111/j.1460-9568.2006.04686.x.Search in Google Scholar PubMed

Marasas, W.F., Kellerman, T.S., Gelderblom, W.C., Coetzer, J.A., Thiel, P.G., and Van Der Lugt, J.J. (1988). Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort J. Vet. Res. 55: 197–203.Search in Google Scholar

Marquardt, R.R. and Frohlich, A.A. (1992). A review of recent advances in understanding ochratoxicosis. J. Anim. Sci. 70: 3968–3988, https://doi.org/10.2527/1992.70123968x.Search in Google Scholar PubMed

Martins, C., Vidal, A., De Boevre, M., De Saeger, S., Nunes, C., Torres, D., Goios, A., Lopes, C., Assunção, R., and Alvito, P. (2019). Exposure assessment of Portuguese population to multiple mycotoxins: the human biomonitoring approach. Int. J. Hyg Environ. Health 222: 913–925, https://doi.org/10.1016/j.ijheh.2019.06.010.Search in Google Scholar PubMed

Matossian, M.K. (1991). Poisons of the past. J. Interdiscipl. Hist. 22: 170–175.Search in Google Scholar

McGeer, P.L. and McGeer, E.G. (2008). Glial reactions in Parkinson’s disease. Mov. Disord. 23: 474–483, https://doi.org/10.1002/mds.21751.Search in Google Scholar

McMillan, A., Renaud, J.B., Burgess, K.M.N., Orimadegun, A.E., Akinyinka, O.O., Allen, S.J., Miller, J.D., Reid, G., and Sumarah, M.W. (2018). Aflatoxin exposure in Nigerian children with severe acute malnutrition. Food Chem. Toxicol. 111: 356–362, https://doi.org/10.1016/j.fct.2017.11.030.Search in Google Scholar

Mehrzad, J., Hosseinkhani, S., and Malvandi, A.M. (2018). Human microglial cells undergo proapoptotic induction and inflammatory activation upon in vitro exposure to a naturally occurring level of aflatoxin B1. Neuroimmunomodulation 25: 176–183, https://doi.org/10.1159/000493528.Search in Google Scholar

Mehrzad, J., Malvandi, A.M., Alipour, M., and Hosseinkhani, S. (2017). Environmentally relevant level of aflatoxin B1 elicits toxic pro-inflammatory response in murine CNS-derived cells. Toxicol. Lett. 279: 96–106, https://doi.org/10.1016/j.toxlet.2017.07.902.Search in Google Scholar

Ménard, A., Amouri, R., Dobránsky, T., Charriaut-Marlangue, C., Pierig, R., Cifuentes-Diaz, C., Ghandour, S., Belliveau, J., Gascan, H., Hentati, F., et al.. (1998). A gliotoxic factor and multiple sclerosis. J. Neurol. Sci. 154: 209–221, https://doi.org/10.1016/s0022-510x(97)00231-1.Search in Google Scholar

Merrill, A.H.Jr., Wang, E., Vales, T.R., Smith, E.R., Schroeder, J.J., Menaldino, D.S., Alexander, C., Crane, H.M., Xia, J., Liotta, D.C., et al.. (1996). Fumonisin toxicity and sphingolipid biosynthesis. Adv. Exp. Med. Biol. 392: 297–306, https://doi.org/10.1007/978-1-4899-1379-1_25.Search in Google Scholar

Mobio, T.A., Anane, R., Baudrimont, I., Carratu, M.R., Shier, T.W., Dano, S.D., Ueno, Y., and Creppy, E.E. (2000a). Epigenetic properties of fumonisin B(1): cell cycle arrest and DNA base modification in C6 glioma cells. Toxicol. Appl. Pharmacol. 164: 91–96, https://doi.org/10.1006/taap.2000.8893.Search in Google Scholar

Mobio, T.A., Baudrimont, I., Sanni, A., Shier, T.W., Saboureau, D., Dano, S.D., Ueno, Y., Steyn, P.S., and Creppy, E.E. (2000b). Prevention by vitamin E of DNA fragmentation and apoptosis induced by fumonisin B1 in C6 glioma cells. Arch. Toxicol. 74: 112–119, https://doi.org/10.1007/s002040050661.Search in Google Scholar

Mobio, T.A., Tavan, E., Baudrimont, I., Anane, R., Carratu, M.R., Sanni, A., Gbeassor, M.F., Shier, T.W., Narbonne, J.F., and Creppy, E.E. (2003). Comparative study of the toxic effects of fumonisin B1 in rat C6 glioma cells and p53-null mouse embryo fibroblasts. Toxicology 183: 65–75, https://doi.org/10.1016/s0300-483x(02)00441-9.Search in Google Scholar

Moldes-Anaya, A.S., Fonnum, F., Eriksen, G.S., Rundberget, T., Walaas, S.I., and Wigestrand, M.B. (2011). In vitro neuropharmacological evaluation of penitrem-induced tremorgenic syndromes: importance of the GABAergic system. Neurochem. Int. 59: 1074–1081, https://doi.org/10.1016/j.neuint.2011.08.014.Search in Google Scholar PubMed

Monnet-Tschudi, F., Zurich, M.G., Sorg, O., Matthieu, J.M., Honegger, P., and Schilter, B. (1999). The naturally occurring food mycotoxin fumonisin B1 impairs myelin formation in aggregating brain cell culture. Neurotoxicology 20: 41–48.Search in Google Scholar

Monzel, A.S., Smits, L.M., Hemmer, K., Hachi, S., Moreno, E.L., Van Wuellen, T., Jarazo, J., Walter, J., Bruggemann, I., Boussaad, I., et al.. (2017). Derivation of human midbrain-specific organoids from neuroepithelial stem cells. Stem Cell Rep. 8: 1144–1154, https://doi.org/10.1016/j.stemcr.2017.03.010.Search in Google Scholar

Muguruma, K., Nishiyama, A., Kawakami, H., Hashimoto, K., and Sasai, Y. (2015). Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep. 10: 537–550, https://doi.org/10.1016/j.celrep.2014.12.051.Search in Google Scholar

Mullbacher, A., Waring, P., Tiwari-Palni, U., and Eichner, R.D. (1986). Structural relationship of epipolythiodioxopiperazines and their immunomodulating activity. Mol. Immunol. 23: 231–235, https://doi.org/10.1016/0161-5890(86)90047-7.Search in Google Scholar

Myburg, R.B., Needhi, N., and Chuturgoon, A.A. (2009). The ultrastructural effects and immunolocalisation of fumonisin B1 on cultured oesophageal cancer cells (SNO). South Afr. J. Sci. 105: 217–222.10.4102/sajs.v105i5/6.94Search in Google Scholar

Newberne, P.M. and Butler, W.H. (1969). Acute and chronic effects of aflatoxin on the liver of domestic and laboratory animals: a review. Canc. Res. 29: 236–250.Search in Google Scholar

Niaz, K., Shah, S.Z.A., Khan, F., and Bule, M. (2020). Ochratoxin A-induced genotoxic and epigenetic mechanisms lead to Alzheimer disease: its modulation with strategies. Environ. Sci. Pollut. Res. Int. 27: 44673–44700, https://doi.org/10.1007/s11356-020-08991-y.Search in Google Scholar PubMed

Norris, P.J., Smith, C.C., De Belleroche, J., Bradford, H.F., Mantle, P.G., Thomas, A.J., and Penny, R.H. (1980). Actions of tremorgenic fungal toxins on neurotransmitter release. J. Neurochem. 34: 33–42, https://doi.org/10.1111/j.1471-4159.1980.tb04618.x.Search in Google Scholar PubMed

Oncu Kaya, E.M., Korkmaz, O.T., Yeniceli Ugur, D., Sener, E., Tuncel, A.N., and Tuncel, M. (2019). Determination of Ochratoxin-A in the brain microdialysates and plasma of awake, freely moving rats using ultra high performance liquid chromatography fluorescence detection method. J. Chromatogr. B Ana. Technol. Biomed. Life Sci. 1125: 121700, https://doi.org/10.1016/j.jchromb.2019.06.027.Search in Google Scholar PubMed

Oskarsson, B., Horton, D.K., and Mitsumoto, H. (2015). Potential environmental factors in amyotrophic lateral sclerosis. Neurol. Clin. 33: 877–888, https://doi.org/10.1016/j.ncl.2015.07.009.Search in Google Scholar PubMed PubMed Central

Osuchowski, M.F., Edwards, G.L., and Sharma, R.P. (2005). Fumonisin B1-induced neurodegeneration in mice after intracerebroventricular infusion is concurrent with disruption of sphingolipid metabolism and activation of proinflammatory signaling. Neurotoxicology 26: 211–221, https://doi.org/10.1016/j.neuro.2004.10.001.Search in Google Scholar PubMed

Osuchowski, M.F. and Sharma, R.P. (2005). Fumonisin B1 induces necrotic cell death in BV-2 cells and murine cultured astrocytes and is antiproliferative in BV-2 cells while N2A cells and primary cortical neurons are resistant. Neurotoxicology 26: 981–992, https://doi.org/10.1016/j.neuro.2005.05.001.Search in Google Scholar PubMed

Oyelami, O.A., Maxwell, S.M., Adelusola, K.A., Aladekoma, T.A., and Oyelese, A.O. (1995). Aflatoxins in the autopsy brain tissue of children in Nigeria. Mycopathologia 132: 35–38, https://doi.org/10.1007/bf01138602.Search in Google Scholar

Ozone, C., Suga, H., Eiraku, M., Kadoshima, T., Yonemura, S., Takata, N., Oiso, Y., Tsuji, T., and Sasai, Y. (2016). Functional anterior pituitary generated in self-organizing culture of human embryonic stem cells. Nat. Commun. 7: 10351, https://doi.org/10.1038/ncomms10351.Search in Google Scholar

Pal, S., Singh, N., and Ansari, K.M. (2017). Toxicological effects of patulin mycotoxin on the mammalian system: an overview. Toxicol. Res. 6: 764–771, https://doi.org/10.1039/c7tx00138j.Search in Google Scholar

Palfi, S., Ferrante, R.J., Brouillet, E., Beal, M.F., Dolan, R., Guyot, M.C., Peschanski, M., and Hantraye, P. (1996). Chronic 3-nitropropionic acid treatment in baboons replicates the cognitive and motor deficits of Huntington’s disease. J. Neurosci. 16: 3019–3025, https://doi.org/10.1523/jneurosci.16-09-03019.1996.Search in Google Scholar

Paradells, S., Rocamonde, B., Llinares, C., Herranz-Perez, V., Jimenez, M., Garcia-Verdugo, J.M., Zipancic, I., Soria, J.M., and Garcia-Esparza, M.A. (2015). Neurotoxic effects of ochratoxin A on the subventricular zone of adult mouse brain. J. Appl. Toxicol. 35: 737–751, https://doi.org/10.1002/jat.3061.Search in Google Scholar

Park, I.H., Zhao, R., West, J.A., Yabuuchi, A., Huo, H., Ince, T.A., Lerou, P.H., Lensch, M.W., and Daley, G.Q. (2008). Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451: 141–146, https://doi.org/10.1038/nature06534.Search in Google Scholar

Park, S., Lee, J.Y., You, S., Song, G., and Lim, W. (2020). Neurotoxic effects of aflatoxin B1 on human astrocytes in vitro and on glial cell development in zebrafish in vivo. J. Hazard Mater. 386: 121639, https://doi.org/10.1016/j.jhazmat.2019.121639.Search in Google Scholar

Park, S., Lim, W., You, S., and Song, G. (2019). Ochratoxin A exerts neurotoxicity in human astrocytes through mitochondria-dependent apoptosis and intracellular calcium overload. Toxicol. Lett. 313: 42–49, https://doi.org/10.1016/j.toxlet.2019.05.021.Search in Google Scholar

Penney, J., Ralvenius, W.T., and Tsai, L.H. (2020). Modeling Alzheimer’s disease with iPSC-derived brain cells. Mol. Psychiatr. 25: 148–167, https://doi.org/10.1038/s41380-019-0468-3.Search in Google Scholar

Pestka, J.J., Clark, E.S., Schwartz-Zimmermann, H.E., and Berthiller, F. (2017). Sex is a determinant for deoxynivalenol metabolism and elimination in the mouse. Toxins 9, https://doi.org/10.3390/toxins9080240.Search in Google Scholar

Peterson, D.W., Bradfor, H.F., and Mantle, P.G. (1982). Actions of a tremorgenic mycotoxin on amino acid transmitter release in vivo. Biochem. Pharmacol. 31: 2807–2810, https://doi.org/10.1016/0006-2952(82)90137-x.Search in Google Scholar

Pierig, R., Belliveau, J., Amouri, R., Ménard, A., and Rieger, F. (2002). Association of a gliotoxic activity with active multiple sclerosis in US patients. Cell. Mol. Biol. 48: 199–203.Search in Google Scholar

Pisa, D., Alonso, R., Rábano, A., Rodal, I., and Carrasco, L. (2015). Different brain regions are infected with fungi in alzheimer’s disease. Sci. Rep. 5: 15015, https://doi.org/10.1038/srep15015.Search in Google Scholar PubMed PubMed Central

Porter, J.K., Voss, K.A., Bacon, C.W., and Norred, W.P. (1990). Effects of Fusarium moniliforme and corn associated with equine leukoencephalomalacia on rat neurotransmitters and metabolites. Proc. Soc. Exp. Biol. Med. 194: 265–269, https://doi.org/10.3181/00379727-194-43089.Search in Google Scholar PubMed

Porter, J.K., Voss, K.A., Chamberlain, W.J., Bacon, C.W., and Norred, W.P. (1993). Neurotransmitters in rats fed fumonisin B1. Proc. Soc. Exp. Biol. Med. 202: 360–364, https://doi.org/10.3181/00379727-202-43547.Search in Google Scholar PubMed

Prelusky, D.B., Trenholm, H.L., and Savard, M.E. (1994). Pharmacokinetic fate of 14C-labelled fumonisin B1 in swine. Nat. Toxins 2: 73–80, https://doi.org/10.1002/nt.2620020205.Search in Google Scholar PubMed

Purzycki, C.B. and Shain, D.H. (2010). Fungal toxins and multiple sclerosis: a compelling connection. Brain Res. Bull. 82: 4–6, https://doi.org/10.1016/j.brainresbull.2010.02.012.Search in Google Scholar PubMed

Qian, X., Nguyen, H.N., Song, M.M., Hadiono, C., Ogden, S.C., Hammack, C., Yao, B., Hamersky, G.R., Jacob, F., Zhong, C., et al.. (2016). Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165: 1238–1254, https://doi.org/10.1016/j.cell.2016.04.032.Search in Google Scholar PubMed PubMed Central

Qureshi, H., Hamid, S.S., Ali, S.S., Anwar, J., Siddiqui, A.A., and Khan, N.A. (2015). Cytotoxic effects of aflatoxin B1 on human brain microvascular endothelial cells of the blood-brain barrier. Med. Mycol. 53: 409–416, https://doi.org/10.1093/mmy/myv010.Search in Google Scholar PubMed

Reddy, P., Guthridge, K., Vassiliadis, S., Hemsworth, J., Hettiarachchige, I., Spangenberg, G., and Rochfort, S. (2019). Tremorgenic mycotoxins: structure diversity and biological activity. Toxins 11, https://doi.org/10.3390/toxins11050302.Search in Google Scholar PubMed PubMed Central

Reinhardt, P., Glatza, M., Hemmer, K., Tsytsyura, Y., Thiel, C.S., Hoing, S., Moritz, S., Parga, J.A., Wagner, L., Bruder, J.M., et al.. (2013). Derivation and expansion using only small molecules of human neural progenitors for neurodegenerative disease modeling. PloS One 8: e59252, https://doi.org/10.1371/journal.pone.0059252.Search in Google Scholar PubMed PubMed Central

Richard, S.A., Manaphraim, N.Y.B., and Kortei, N.K. (2020). The novel neurotoxic and neuroimmunotoxic capabilities of aflatoxin B1 on the nervous system: a review. Adv. Biosci. Clin. Med. 8: 1–8.10.7575/aiac.abcmed.v.8n.3p.1Search in Google Scholar

Rieger, F., Amouri, R., Benjelloun, N., Cifuentes-Diaz, C., LYON-Caen, O., Hantaz-Ambroise, D., Dobransky, T., Perron, H., and Gemy, C. (1996). Gliotoxic factor and multiple sclerosis. Comptes Rendus Acad. Sci. III 319: 343–350.Search in Google Scholar

Rodríguez-Carrasco, Y., Moltó, J.C., Mañes, J., and Berrada, H. (2014). Exposure assessment approach through mycotoxin/creatinine ratio evaluation in urine by GC-MS/MS. Food Chem. Toxicol. 72: 69–75, https://doi.org/10.1016/j.fct.2014.07.014.Search in Google Scholar PubMed

Roque, P.J. and Costa, L.G. (2017). Co-culture of neurons and microglia. Curr. Protoc. Toxicol. 74: 11.24.1–11.24.17, doi:https://doi.org/10.1002/cptx.32.Search in Google Scholar PubMed PubMed Central

Rosenstein, R.E., Chuluyan, H.E., and Cardinali, D.P. (1990). Presynaptic effects of gamma-aminobutyric acid on norepinephrine release and uptake in rat pineal gland. J. Neural Transm. Gen. Sect. 82: 131–140, https://doi.org/10.1007/bf01245169.Search in Google Scholar

Ross, P.F., Ledet, A.E., Owens, D.L., Rice, L.G., Nelson, H.A., Osweiler, G.D., and Wilson, T.M. (1993). Experimental equine leukoencephalomalacia, toxic hepatosis, and encephalopathy caused by corn naturally contaminated with fumonisins. J. Vet. Diagn. Invest. 5: 69–74, https://doi.org/10.1177/104063879300500115.Search in Google Scholar PubMed

Roy, J., Minotti, S., Dong, L., Figlewicz, D.A., and Durham, H.D. (1998). Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18: 9673–9684, https://doi.org/10.1523/jneurosci.18-23-09673.1998.Search in Google Scholar

Rumora, L. and Grubisić, T.Z. (2009). A journey through mitogen-activated protein kinase and ochratoxin A interactions. Arh. Hig. Rada. Toksikol. 60: 449–456, https://doi.org/10.2478/10004-1254-60-2009-1969.Search in Google Scholar PubMed

Sabater-Vilar, M., Maas, R.F., De Bosschere, H., Ducatelle, R., and Fink-Gremmels, J. (2004). Patulin produced by an Aspergillus clavatus isolated from feed containing malting residues associated with a lethal neurotoxicosis in cattle. Mycopathologia 158: 419–426, https://doi.org/10.1007/s11046-005-2877-x.Search in Google Scholar PubMed

Sadler, T.W., Merrill, A.H., Stevens, V.L., Sullards, M.C., Wang, E., and Wang, P. (2002). Prevention of fumonisin B1-induced neural tube defects by folic acid. Teratology 66: 169–176, https://doi.org/10.1002/tera.10089.Search in Google Scholar PubMed

Sakaguchi, H., Kadoshima, T., Soen, M., Narii, N., Ishida, Y., Ohgushi, M., Takahashi, J., Eiraku, M., and Sasai, Y. (2015). Generation of functional hippocampal neurons from self-organizing human embryonic stem cell-derived dorsomedial telencephalic tissue. Nat. Commun. 6: 8896, https://doi.org/10.1038/ncomms9896.Search in Google Scholar PubMed PubMed Central

Sava, V., Reunova, O., Velasquez, A., Harbison, R., and Sanchez-Ramos, J. (2006a). Acute neurotoxic effects of the fungal metabolite ochratoxin-A. Neurotoxicology 27: 82–92, https://doi.org/10.1016/j.neuro.2005.07.004.Search in Google Scholar PubMed

Sava, V., Reunova, O., Velasquez, A., and Sanchez-Ramos, J. (2006b). Can low level exposure to ochratoxin-A cause parkinsonism? J. Neurol. Sci. 249: 68–75, https://doi.org/10.1016/j.jns.2006.06.006.Search in Google Scholar PubMed

Sava, V., Velasquez, A., Song, S., and Sanchez-Ramos, J. (2007). Adult hippocampal neural stem/progenitor cells in vitro are vulnerable to the mycotoxin ochratoxin-A. Toxicol. Sci. 98: 187–197, https://doi.org/10.1093/toxsci/kfm093.Search in Google Scholar PubMed

Scafuri, B., Varriale, A., Facchiano, A., D’auria, S., Raggi, M.E., and Marabotti, A. (2017). Binding of mycotoxins to proteins involved in neuronal plasticity: a combined in silico/wet investigation. Sci. Rep. 7: 15156, https://doi.org/10.1038/s41598-017-15148-4.Search in Google Scholar PubMed PubMed Central

Schwarz, A., Rapaport, E., Hirschberg, K., and Futerman, A.H. (1995). A regulatory role for sphingolipids in neuronal growth. Inhibition of sphingolipid synthesis and degradation have opposite effects on axonal branching. J. Biol. Chem. 270: 10990–10998, https://doi.org/10.1074/jbc.270.18.10990.Search in Google Scholar PubMed

Scofield, M.D., Korutla, L., Jackson, T.G., Kalivas, P.W., and Mackler, S.A. (2012). Nucleus Accumbens 1, a pox virus and zinc finger/Bric-a-brac tramtrack broad protein binds to TAR DNA-binding protein 43 and has a potential role in amyotrophic lateral sclerosis. Neuroscience 227: 44–54, https://doi.org/10.1016/j.neuroscience.2012.09.043.Search in Google Scholar PubMed PubMed Central

Sehata, S., Kiyosawa, N., Makino, T., Atsumi, F., Ito, K., Yamoto, T., Teranishi, M., Baba, Y., Uetsuka, K., Nakayama, H., et al.. (2004). Morphological and microarray analysis of T-2 toxin-induced rat fetal brain lesion. Food Chem. Toxicol. 42: 1727–1736, https://doi.org/10.1016/j.fct.2004.06.006.Search in Google Scholar PubMed

Shephard, G.S., Van Der Westhuizen, L., and Sewram, V. (2007). Biomarkers of exposure to fumonisin mycotoxins: a review. Food Addit. Contam. 24: 1196–1201, https://doi.org/10.1080/02652030701513818.Search in Google Scholar PubMed

Shi, Y., Sun, L., Wang, M., Liu, J., Zhong, S., Li, R., Li, P., Guo, L., Fang, A., Chen, R., et al.. (2020). Vascularized human cortical organoids (vOrganoids) model cortical development in vivo. PLoS Biol. 18: e3000705, https://doi.org/10.1371/journal.pbio.3000705.Search in Google Scholar PubMed PubMed Central

Shifrin, V.I. and Anderson, P. (1999). Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem. 274: 13985–13992, https://doi.org/10.1074/jbc.274.20.13985.Search in Google Scholar PubMed

Shimada, T. and Guengerich, F.P. (1989). Evidence for cytochrome P-450nf, the nifedipine oxidase, being the principal enzyme involved in the bioactivation of aflatoxins in human liver. Proc. Natl. Acad. Sci. U. S. A. 86: 462–465, https://doi.org/10.1073/pnas.86.2.462.Search in Google Scholar PubMed PubMed Central

Slanzi, A., Iannoto, G., Rossi, B., Zenaro, E., and Constantin, G. (2020). In vitro models of neurodegenerative diseases. Front Cell Dev. Biol. 8: 328, https://doi.org/10.3389/fcell.2020.00328.Search in Google Scholar PubMed PubMed Central

Smits, L.M., Reinhardt, L., Reinhardt, P., Glatza, M., Monzel, A.S., Stanslowsky, N., Rosato-Siri, M.D., Zanon, A., Antony, P.M., Bellmann, J., et al.. (2019). Modeling Parkinson’s disease in midbrain-like organoids. NPJ Parkinsons Dis. 5: 5, https://doi.org/10.1038/s41531-019-0078-4.Search in Google Scholar PubMed PubMed Central

Song, E., Su, C., Fu, J., Xia, X., Yang, S., Xiao, C., Lu, B., Chen, H., Sun, Z., Wu, S., et al.. (2014). Selenium supplementation shows protective effects against patulin-induced brain damage in mice via increases in GSH-related enzyme activity and expression. Life Sci. 109: 37–43, https://doi.org/10.1016/j.lfs.2014.05.022.Search in Google Scholar PubMed

Souto, N.S., Claudia Monteiro Braga, A., Lutchemeyer De Freitas, M., Rechia Fighera, M., Royes, L.F.F., Schneider Oliveira, M., and Furian, A.F. (2018). Aflatoxin B1 reduces non-enzymatic antioxidant defenses and increases protein kinase C activation in the cerebral cortex of young rats. Nutr. Neurosci. 21: 268–275, https://doi.org/10.1080/1028415x.2017.1278837.Search in Google Scholar PubMed

Souto, P., Jager, A.V., Tonin, F.G., Petta, T., DI Gregório, M.C., Cossalter, A.M., Pinton, P., Oswald, I.P., Rottinghaus, G.E., and Oliveira, C.A.F. (2017). Determination of fumonisin B(1) levels in body fluids and hair from piglets fed fumonisin B(1)-contaminated diets. Food Chem. Toxicol. 108: 1–9, https://doi.org/10.1016/j.fct.2017.07.036.Search in Google Scholar PubMed

Souza, C.F., Baldissera, M.D., Zeppenfeld, C.C., Descovi, S., Stefani, L.M., Baldisserotto, B., and Da Silva, A.S. (2019). Oxidative stress mediated the inhibition of cerebral creatine kinase activity in silver catfish fed with aflatoxin B1-contaminated diet. Fish Physiol. Biochem. 45: 63–70, https://doi.org/10.1007/s10695-018-0534-9.Search in Google Scholar PubMed

Spencer Smith, J., Paul Williams, W., and Windham, G.L. (2019). Aflatoxin in maize: a review of the early literature from “moldy-corn toxicosis” to the genetics of aflatoxin accumulation resistance. Mycotoxin Res. 35: 111–128, https://doi.org/10.1007/s12550-018-00340-w.Search in Google Scholar PubMed

Speth, C., Kupfahl, C., Pfaller, K., Hagleitner, M., Deutinger, M., Wurzner, R., Mohsenipour, I., Lass-Florl, C., and Rambach, G. (2011). Gliotoxin as putative virulence factor and immunotherapeutic target in a cell culture model of cerebral aspergillosis. Mol. Immunol. 48: 2122–2129, https://doi.org/10.1016/j.molimm.2011.07.005.Search in Google Scholar PubMed

Stockmann-Juvala, H., Mikkola, J., Naarala, J., Loikkanen, J., Elovaara, E., and Savolainen, K. (2004a). Fumonisin B1-induced toxicity and oxidative damage in U-118MG glioblastoma cells. Toxicology 202: 173–183, https://doi.org/10.1016/j.tox.2004.05.002.Search in Google Scholar PubMed

Stockmann-Juvala, H., Mikkola, J., Naarala, J., Loikkanen, J., Elovaara, E., and Savolainen, K. (2004b). Oxidative stress induced by fumonisin B1 in continuous human and rodent neural cell cultures. Free Radic. Res. 38: 933–942, https://doi.org/10.1080/10715760412331273205.Search in Google Scholar PubMed

Stockmann-Juvala, H., Naarala, J., Loikkanen, J., Vahakangas, K., and Savolainen, K. (2006). Fumonisin B1-induced apoptosis in neuroblastoma, glioblastoma and hypothalamic cell lines. Toxicology 225: 234–241, https://doi.org/10.1016/j.tox.2006.06.006.Search in Google Scholar

Sweeney, M.J. and Dobson, A.D. (1998). Mycotoxin production by Aspergillus, Fusarium and Penicillium species. Int. J. Food Microbiol. 43: 141–158, https://doi.org/10.1016/s0168-1605(98)00112-3.Search in Google Scholar

Talley, S.M., Coley, P.D., and Kursar, T.A. (2002). The effects of weather on fungal abundance and richness among 25 communities in the Intermountain West. BMC Ecol. 2: 7, https://doi.org/10.1186/1472-6785-2-7.Search in Google Scholar

Thuvander, A., Wikman, C., and Gadhasson, I. (1999). In vitro exposure of human lymphocytes to trichothecenes: individual variation in sensitivity and effects of combined exposure on lymphocyte function. Food Chem. Toxicol. 37: 639–648, https://doi.org/10.1016/s0278-6915(99)00038-1.Search in Google Scholar

Tsunoda, M., Dugyala, R.R., and Sharma, R.P. (1998). Fumonisin B1-induced increases in neurotransmitter metabolite levels in different brain regions of BALB/c mice. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 120: 457–465, https://doi.org/10.1016/s0742-8413(98)10061-0.Search in Google Scholar

van der Merwe, K.J., Steyn, P.S., Fourie, L., Scott, D.B., and Theron, J.J. (1965). Ochratoxin A, a toxic metabolite produced by Aspergillus ochraceus Wilh. Nature 205: 1112–1113, https://doi.org/10.1038/2051112a0.Search in Google Scholar PubMed

Venkataraman, P., Krishnamoorthy, G., Selvakumar, K., and Arunakaran, J. (2009). Oxidative stress alters creatine kinase system in serum and brain regions of polychlorinated biphenyl (Aroclor 1254)-exposed rats: protective role of melatonin. Basic Clin. Pharmacol. Toxicol. 105: 92–97, https://doi.org/10.1111/j.1742-7843.2009.00406.x.Search in Google Scholar PubMed

Vidal, A., Claeys, L., Mengelers, M., Vanhoorne, V., Vervaet, C., Huybrechts, B., DE Saeger, S., and DE Boevre, M. (2018). Humans significantly metabolize and excrete the mycotoxin deoxynivalenol and its modified form deoxynivalenol-3-glucoside within 24 hours. Sci. Rep. 8: 5255, https://doi.org/10.1038/s41598-018-23526-9.Search in Google Scholar PubMed PubMed Central

Vigasova, D., Nemergut, M., Liskova, B., and Damborsky, J. (2021). Multi-pathogen infections and Alzheimer’s disease. Microb. Cell Factories 20: 25, https://doi.org/10.1186/s12934-021-01520-7.Search in Google Scholar PubMed PubMed Central

Vogel, D.Y., Kooij, G., Heijnen, P.D., Breur, M., Peferoen, L.A., Van Der Valk, P., De Vries, H.E., Amor, S., and Dijkstra, C.D. (2015). GM-CSF promotes migration of human monocytes across the blood brain barrier. Eur. J. Immunol. 45: 1808–1819, https://doi.org/10.1002/eji.201444960.Search in Google Scholar PubMed

von Tobel, J.S., Antinori, P., Zurich, M.G., Rosset, R., Aschner, M., Gluck, F., Scherl, A., and Monnet-Tschudi, F. (2014). Repeated exposure to Ochratoxin A generates a neuroinflammatory response, characterized by neurodegenerative M1 microglial phenotype. Neurotoxicology 44: 61–70, https://doi.org/10.1016/j.neuro.2014.04.005.Search in Google Scholar

Vudathala, D.K., Prelusky, D.B., Ayroud, M., Trenholm, H.L., and Miller, J.D. (1994). Pharmacokinetic fate and pathological effects of 14C-fumonisin B1 in laying hens. Nat. Toxins 2: 81–88, https://doi.org/10.1002/nt.2620020206.Search in Google Scholar

Wang, E., Norred, W.P., Bacon, C.W., Riley, R.T., and Merrill, A.H.Jr. (1991). Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J. Biol. Chem. 266: 14486–14490, https://doi.org/10.1016/s0021-9258(18)98712-0.Search in Google Scholar

Wang, J., Fitzpatrick, D.W., and Wilson, J.R. (1998a). Effect of T-2 toxin on blood-brain barrier permeability monoamine oxidase activity and protein synthesis in rats. Food Chem. Toxicol. 36: 955–961, https://doi.org/10.1016/s0278-6915(98)00079-9.Search in Google Scholar

Wang, J., Fitzpatrick, D.W., and Wilson, J.R. (1998b). Effects of the trichothecene mycotoxin T-2 toxin on neurotransmitters and metabolites in discrete areas of the rat brain. Food Chem. Toxicol. 36: 947–953, https://doi.org/10.1016/s0278-6915(98)00078-7.Search in Google Scholar

Wang, Y., Gallagher, E., Jorgensen, C., Troendle, E.P., Hu, D., Searson, P.C., and Ulmschneider, M.B. (2019). An experimentally validated approach to calculate the blood-brain barrier permeability of small molecules. Sci. Rep. 9: 6117, https://doi.org/10.1038/s41598-019-42272-0.Search in Google Scholar

Wang, Y., Wang, L., Zhu, Y., and Qin, J. (2018). Human brain organoid-on-a-chip to model prenatal nicotine exposure. Lab Chip 18: 851–860, https://doi.org/10.1039/c7lc01084b.Search in Google Scholar

Waring, P., Eichner, R.D., and Mullbacher, A. (1988). The chemistry and biology of the immunomodulating agent gliotoxin and related epipolythiodioxopiperazines. Med. Res. Rev. 8: 499–524, https://doi.org/10.1002/med.2610080404.Search in Google Scholar

Wild, C.P., Jiang, Y.Z., Sabbioni, G., Chapot, B., and Montesano, R. (1990). Evaluation of methods for quantitation of aflatoxin-albumin adducts and their application to human exposure assessment. Canc. Res. 50: 245–251.Search in Google Scholar

Wilson, B.J., Hoekman, T., and Dettbarn, W.D. (1972). Effects of a fungus tremorgenic toxin (penitrem A) on transmission in rat phrenic nerve-diaphragm preparations. Brain Res. 40: 540–544, https://doi.org/10.1016/0006-8993(72)90159-x.Search in Google Scholar

Wilson, T.M., Ross, P.F., Rice, L.G., Osweiler, G.D., Nelson, H.A., Owens, D.L., Plattner, R.D., Reggiardo, C., Noon, T.H., and Pickrell, J.W. (1990). Fumonisin B1 levels associated with an epizootic of equine leukoencephalomalacia. J. Vet. Diagn. Invest. 2: 213–216, https://doi.org/10.1177/104063879000200311.Search in Google Scholar PubMed

Xicoy, H., Wieringa, B., and Martens, G.J. (2017). The SH-SY5Y cell line in Parkinson’s disease research: a systematic review. Mol. Neurodegener. 12: 10, https://doi.org/10.1186/s13024-017-0149-0.Search in Google Scholar PubMed PubMed Central

Yagi, T., Ito, D., Okada, Y., Akamatsu, W., Nihei, Y., Yoshizaki, T., Yamanaka, S., Okano, H., and Suzuki, N. (2011). Modeling familial Alzheimer’s disease with induced pluripotent stem cells. Hum. Mol. Genet. 20: 4530–4539, https://doi.org/10.1093/hmg/ddr394.Search in Google Scholar PubMed

Yoon, S., Cong, W.T., Bang, Y., Lee, S.N., Yoon, C.S., Kwack, S.J., Kang, T.S., Lee, K.Y., Choi, J.K., and Choi, H.J. (2009). Proteome response to ochratoxin A-induced apoptotic cell death in mouse hippocampal HT22 cells. Neurotoxicology 30: 666–676, https://doi.org/10.1016/j.neuro.2009.04.013.Search in Google Scholar PubMed

Zain, M.E. (2011). Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc. 15: 129–144, https://doi.org/10.1016/j.jscs.2010.06.006.Search in Google Scholar

Zhang, J., You, L., Wu, W., Wang, X., Chrienova, Z., Nepovimova, E., Wu, Q., and Kuca, K. (2020). The neurotoxicity of trichothecenes T-2 toxin and deoxynivalenol (DON): current status and future perspectives. Food Chem. Toxicol. 145: 111676, https://doi.org/10.1016/j.fct.2020.111676.Search in Google Scholar PubMed

Zhang, X., Boesch-Saadatmandi, C., Lou, Y., Wolffram, S., Huebbe, P., and Rimbach, G. (2009). Ochratoxin A induces apoptosis in neuronal cells. Genes Nutr. 4: 41–48, https://doi.org/10.1007/s12263-008-0109-y.Search in Google Scholar PubMed PubMed Central

Zhu, P. and Wang, L. (2017). Passive and active droplet generation with microfluidics: a review. Lab Chip 17: 34–75, https://doi.org/10.1039/c6lc01018k.Search in Google Scholar PubMed

Zilinskas, R.A. (1997). Iraq’s biological weapons: the past as future? J. Am. Med. Assoc. 278: 418–424, https://doi.org/10.1001/jama.1997.03550050080037.Search in Google Scholar

Zurich, M.G. and Honegger, P. (2011). Ochratoxin A at nanomolar concentration perturbs the homeostasis of neural stem cells in highly differentiated but not in immature three-dimensional brain cell cultures. Toxicol. Lett. 205: 203–208, https://doi.org/10.1016/j.toxlet.2011.06.007.Search in Google Scholar PubMed

Zurich, M.G., Lengacher, S., Braissant, O., Monnet-Tschudi, F., Pellerin, L., and Honegger, P. (2005). Unusual astrocyte reactivity caused by the food mycotoxin ochratoxin A in aggregating rat brain cell cultures. Neuroscience 134: 771–782, https://doi.org/10.1016/j.neuroscience.2005.04.030.Search in Google Scholar PubMed

Received: 2021-04-01
Accepted: 2021-08-16
Published Online: 2021-08-27
Published in Print: 2022-01-26

© 2021 Walter de Gruyter GmbH, Berlin/Boston

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