Aberrant mitochondrial bioenergetics in the cerebral cortex of the Fmr1 knockout mouse model of fragile X syndrome

References

Arrázola, M.S., Andraini, T., Szelechowski, M., Mouledous, L., Arnauné-Pelloquin, L., Davezac, N., Belenguer, P., Rampon, C., and Miquel, M.C. (2018). Mitochondria in developmental and adult neurogenesis. Neurotox. Res. 36, 257–267.10.1007/s12640-018-9942-ySearch in Google Scholar PubMed

Ascano Jr., M., Mukherjee, N., Bandaru, P., Miller, J.B., Nusbaum, J.D., Corcoran, D.L., Langlois, C., Munschauer, M., Dewell, S., Hafner, M., et al. (2012). FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature 492, 382–386.10.1038/nature11737Search in Google Scholar PubMed PubMed Central

Bakker, C.E., Verheij, C., Willemsen, R., der Helm, R., Oerlemans, F., Vermey, M., Bygrave, A., Hoogeveen, A.T., and Ben Oostra, A. (1994). Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell 78, 23–33.10.1016/0092-8674(94)90569-XSearch in Google Scholar

Bechara, E.G., Didiot, M.C., Melko, M., Davidovic, L., Bensaid, M., Martin, P., Castets, M., Pognonec, P., Khandjian, E.W., Moine, H., et al. (2009). A novel function for fragile X mental retardation protein in translational activation. PLoS Biol. 7, e16.10.1371/journal.pbio.1000016Search in Google Scholar PubMed PubMed Central

Bélanger, M., Allaman, I., and Magistretti, P.J. (2011). Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724–738.10.1016/j.cmet.2011.08.016Search in Google Scholar PubMed

Bell, R.M. and Coleman, R.A. (1980). Enzymes of glycerolipid synthesis in eukaryotes. Annu. Rev. Biochem. 49, 459–487.10.1146/annurev.bi.49.070180.002331Search in Google Scholar PubMed

Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T., and Rossignol, R. (2007). Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120, 838–848.10.1242/jcs.03381Search in Google Scholar PubMed

Benard, G., Bellance, N., Jose, C., Melser, S., Nouette-Gaulain, K., and Rossignol, R. (2010). Multi-site control and regulation of mitochondrial energy production. Biochim. Biophys. Acta 1797, 698–709.10.1016/j.bbabio.2010.02.030Search in Google Scholar PubMed

Bonaccorso, C.M., Spatuzza, M., Di Marco, B., Gloria, A., Barrancotto, G., Cupo, A., Musumeci, S.A., D’Antoni, S., Bardoni, B., Catania, M.V. (2015). Fragile X mental retardation protein (FMRP) interacting proteins exhibit different expression patterns during development. Int. J. Dev. Neurosci. 42, 15–23.10.1016/j.ijdevneu.2015.02.004Search in Google Scholar PubMed

Castagnola, S., Delhaye, S., Folci, A., Paquet, A., Brau, F., Duprat, F., Jarjat, M., Grossi, M., Béal, M., Martin, S., et al. (2018). New insights into the role of Cav2 protein family in calcium flux deregulation in Fmr1-KO neurons. Front Mol. Neurosci. 11, 342.10.3389/fnmol.2018.00342Search in Google Scholar PubMed PubMed Central

Castora, F.J. (2018). Mitochondrial function and abnormalities implicated in the pathogenesis of ASD. Prog. Neuropsychopharmacol. Biol. Psychiatry. 92, 83–108.10.1016/j.pnpbp.2018.12.015Search in Google Scholar PubMed

Chowdhury, S.K., Gemin, A., and Singh, G. (2005). High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines. Biochem. Biophys. Res. Commun. 333, 1139–1145.10.1016/j.bbrc.2005.06.017Search in Google Scholar PubMed

Comery, T.A., Harris, J.B., Willems, P.J., Oostra, B.A., Irwin, S.A., Weiler, I.J., and Greenough, W.T. (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. U.S.A. 94, 5401–5404.10.1073/pnas.94.10.5401Search in Google Scholar PubMed PubMed Central

Cui, H., Kong, Y., and Zhang, H. (2012). Oxidative stress, mitochondrial dysfunction, and aging. J. Signal Transduct. 2012, 646354.10.1155/2012/646354Search in Google Scholar PubMed PubMed Central

Darnell, J.C., Van Driesche, S.J., Zhang, C., Hung, K.Y., Mele, A., Fraser, C.E., Stone, E.F., Chen, C., Fak, J.J., Chi, S.W., et al. (2011). FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247–261.10.1016/j.cell.2011.06.013Search in Google Scholar PubMed PubMed Central

Davidovic, L., Navratil, V., Bonaccorso, C.M., Catania, M.V., Bardoni, B., and Dumas, M.E. (2011). A metabolomic and systems biology perspective on the brain of the fragile X syndrome mouse model. Genome Res. 21, 2190–2202.10.1101/gr.116764.110Search in Google Scholar PubMed PubMed Central

de Bari, L., Atlante, A., Armeni, T., and Kalapos, M.P. (2019). Synthesis and metabolism of methylglyoxal, S-D-lactoylglutathione and D-lactate in cancer and Alzheimer’s disease. Exploring the crossroad of eternal youth and premature aging. Ageing Res. 53, 100915.10.1016/j.arr.2019.100915Search in Google Scholar

de Diego-Otero, Y., Romero-Zerbo, Y., El Bekay, R., Decara, J., Sanchez, L., Rodriguez-de-Fonseca, F., and Del Arco-Herrera, I. (2009). Alpha-tocopherol protect against oxidative stress in the fragile X knockout mouse: an experimental therapeutic approach for the Fmr1 deficiency. Neuropsycopharmacology 34, 1011–1026.10.1038/npp.2008.152Search in Google Scholar PubMed

De Felipe, J., Marco, P., Fairén, A., and Jones, E.G. (1997). Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb. Cortex 7, 619–634.10.1093/cercor/7.7.619Search in Google Scholar PubMed

De Filippis, B., Valenti, D., de Bari, L., De Rasmo, D., Musto, M., Fabbri, A., Ricceri, L., Fiorentini, C., Laviola, G., and Vacca, R.A. (2015). Mitochondrial free radical overproduction due to respiratory chain impairment in the brain of a mouse model of Rett syndrome: protective effect of CNF1. Free Radic. Biol. Med. 83, 167–177.10.1016/j.freeradbiomed.2015.02.014Search in Google Scholar PubMed

Dockendorff, T.C. and Labrador, M. (2019). The fragile X protein and genome function. Mol. Neurobiol. 56, 711–721.10.1007/s12035-018-1122-9Search in Google Scholar PubMed

El Bekay, R., Romero-Zerbo, Y., Decara, J., Sanchez-Salido, L., Del Arco-Herrera, I., Rodríguez-de Fonseca, F., and de Diego-Otero, Y. (2007). Enhanced markers of oxidative stress, altered antioxidants and NADPH-oxidase activation in brains from Fragile X mental retardation 1-deficient mice, a pathological model for Fragile X syndrome. Eur. J. Neurosci. 26, 3169–3180.10.1111/j.1460-9568.2007.05939.xSearch in Google Scholar PubMed

Ferron, L. (2016). Fragile X mental retardation protein controls ion channel expression and activity. J. Physiol. 594, 5861–5867.10.1113/JP270675Search in Google Scholar PubMed PubMed Central

Gholizadeh, S., Halder, S.K., and Hampson, D.R. (2015). Expression of fragile X mental retardation protein in neurons and glia of the developing and adult mouse brain. Brain Res. 1596, 22–30.10.1016/j.brainres.2014.11.023Search in Google Scholar PubMed

Griffiths, K.K. and Levy, R.J. (2017). Evidence of mitochondrial dysfunction in autism: biochemical links, genetic-based associations, and non-energy-related mechanisms. Oxid. Med. Cell. Longev. 2017, 4314025.10.1155/2017/4314025Search in Google Scholar PubMed PubMed Central

Grilli, M., Summa, M., Salamone, A., Olivero, G., Zappettini, S., Di Prisco, S., Feligioni, M., Usai, C., Pittaluga, A., and Marchi, M. (2012). In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacol. 63, 916–926.10.1016/j.neuropharm.2012.06.049Search in Google Scholar PubMed

Hagerman, R.J., Berry-Kravis, E., Hazlett, H.C., Bailey Jr, D.B., Moine, H., Kooy, R.F., Tassone, F., Gantois, I., Sonenberg, N., Mandel, J.L., et al. (2017). Fragile X syndrome. Nat. Rev. Dis. Primers 3, 17065.10.1038/nrdp.2017.65Search in Google Scholar PubMed

Hroudová, J. and Fišar, Z. (2013). Control mechanisms in mitochondrial oxidative phosphorylation. Neural Regen Res. 8, 363–375.Search in Google Scholar

Huber, K.M., Gallagher, S.M., Warren, S.T., and Bear, M.F. (2002). Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. U.S.A. 99, 7746–7750.10.1073/pnas.122205699Search in Google Scholar PubMed PubMed Central

Khalfallah, O., Jarjat, M., Davidovic, L., Nottet, N., Cestèle, S., Mantegazza, M., and Bardoni, B. (2017). Depletion of the fragile X mental retardation protein in embryonic stem cells alters the kinetics of neurogenesis. Stem Cells 35, 374–385.10.1002/stem.2505Search in Google Scholar PubMed

Manente, A.G., Valenti, D., Pinton, G., Jithesh, P.V., Daga, A., Rossi, L., Gray, S.G., O’Byrne, K.J., Fennell, D.A., Vacca, R.A., et al. (2013). Estrogen receptor β activation impairs mitochondrial oxidative metabolism and affects malignant mesothelioma cell growth in vitro and in vivo. Oncogenesis 2, e72.10.1038/oncsis.2013.32Search in Google Scholar PubMed PubMed Central

Maurin, T., Zongaro, S., and Bardoni, B. (2014). Fragile X Syndrome: from molecular pathology to therapy. Neurosci. Biobehav. Rev. 46, 242–255.10.1016/j.neubiorev.2014.01.006Search in Google Scholar PubMed

Maurin, T., Lebrigand, K., Castagnola, S., Paquet, A., Jarjat, M., Popa, A., Grossi, M., Rage, F., and Bardoni, B. (2018). HITS-CLIP in various brain areas reveals new targets and new modalities of RNA binding by fragile X mental retardation protein. Nucleic Acids Res. 46, 6344–6355.10.1093/nar/gky267Search in Google Scholar PubMed PubMed Central

Mrácek, T., Pecinová, A., Vrbacký, M., Drahota, Z., and Houstek, J. (2009). High efficiency of ROS production by glycerophosphate dehydrogenase in mammalian mitochondria. Arch. Biochem. Biophys. 481, 30–36.10.1016/j.abb.2008.10.011Search in Google Scholar

Mráček, T., Drahota, Z., and Houštěk, J. (2013). The function and the role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues. Biochim. Biophys. Acta. 1827, 401–410.10.1016/j.bbabio.2012.11.014Search in Google Scholar

Musumeci, S.A., Bosco, P., Calabrese, G., Bakker, C., De Sarro, G.B., Elia, M., Ferri, R., and Oostra, B.A. (2000). Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 41, 19–23.10.1111/j.1528-1157.2000.tb01499.xSearch in Google Scholar

Orlando, R., Borro, M., Motolese, M., Molinaro, G., Scaccianoce, S., Caruso, A., di Nuzzo, L., Caraci, F., Matrisciano, F., Pittaluga, A., et al. (2014). Levels of the Rab GDP dissociation inhibitor (GDI) are altered in the prenatal restrain stress mouse model of schizophrenia and are differentially regulated by the mGlu2/3 receptor agonists, LY379268 and LY354740. Neuropharmacology 86, 133–144.10.1016/j.neuropharm.2014.07.009Search in Google Scholar

Pieretti, M., Zhang, F., Fu, Y.H., Warren, S.T., Oostra, B.A., Caskey, C.T., and Nelson, D.L. (1991). Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66, 817–822.10.1016/0092-8674(91)90125-ISearch in Google Scholar

Qin, M., Kang, J., and Smith, C.B. (2002). Increased rates of cerebral glucose metabolism in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. U.S.A. 99, 15758–15763.10.1073/pnas.242377399Search in Google Scholar PubMed PubMed Central

Richter, J.D. and Coller, J. (2015). Pausing on polyribosomes: make way for elongation in translational control. Cell 163, 292–300.10.1016/j.cell.2015.09.041Search in Google Scholar PubMed PubMed Central

Rose, S., Bennuri, S.C., Wynne, R., Melnyk, S., James, S.J., and Frye, R.E. (2017). Mitochondrial and redox abnormalities in autism lymphoblastoid cells: a sibling control study. FASEB J. 31, 904–909.10.1096/fj.201601004RSearch in Google Scholar PubMed PubMed Central

Santos, A.R., Kanellopoulos, A.K., and Bagni, C. (2014). Learning and behavioral deficits associated with the absence of the fragile X mental retardation protein: what a fly and mouse model can teach us. Learn Mem. 21, 543–555.10.1101/lm.035956.114Search in Google Scholar PubMed PubMed Central

Shen, M., Wang, F., Li, M., Sah, N., Stockton, M.E., Tidei, J.J., Gao, Y., Korabelnikov, T., Kannan, S., Vevea, J.D., et al. (2019). Reduced mitochondrial fusion and Huntingtin levels contribute to impaired dendritic maturation and behavioral deficits in Fmr1-mutant mice. Nat. Neurosci. 2, 386–400.10.1038/s41593-019-0338-ySearch in Google Scholar PubMed PubMed Central

Shul, J.A. and Warren, S.T. (2015). Single-nucleotide mutations in FMR1 reveal novel functions and regulatory mechanisms of the fragile X syndrome protein FMRP. J. Exp. Neurosci. 9(Suppl. 2), 35–41.10.4137/JEN.S25524Search in Google Scholar

Tabet, R., Moutin, E., Becker, J.A., Heintz, D., Fouillen, L., Flatter, E., Krężel, W., Alunni, V., Koebel, P., Dembélé, D., et al. (2016). Fragile X Mental Retardation Protein (FMRP) controls diacylglycerol kinase activity in neurons. Proc. Natl. Acad. Sci. U.S.A. 113, E3619–E3628.10.1073/pnas.1522631113Search in Google Scholar PubMed PubMed Central

Tang, B., Wang, T., Wan, H., Han, L., Qin, X., Zhang, Y., Wang, J., Yu, C., Berton, F., Francesconi, W., et al. (2015). Fmr1 deficiency promotes age-dependent alterations in the cortical synaptic proteome. Proc. Natl. Acad. Sci. U.S.A. 112, 4697–4706.10.1073/pnas.1502258112Search in Google Scholar PubMed PubMed Central

Till, S.M. (2010). The developmental roles of FMRP. Biochem. Soc. Trans. 38, 507–510.10.1042/BST0380507Search in Google Scholar PubMed

Vacca, R.A., Bawari, S., Valenti, D., Tewari, D., Nabavi, S.F., Shirooie, S., Sah, A.N., Volpicella, M., Braidy, N., Nabavi, S.M. (2019). Down syndrome: neurobiological alterations and therapeutic targets. Neurosci. Biobehav. Rev. 98, 234–255.10.1016/j.neubiorev.2019.01.001Search in Google Scholar PubMed

Valenti, D., de Bari, L., De Filippis, B., Henrion-Caude, A., and Vacca, R.A. (2014a). Mitochondrial dysfunction as a central actor in intellectual disability-related diseases: an overview of Down syndrome, autism, Fragile X and Rett syndrome. Neurosci. Biobehav. Rev. 46, 202–217.10.1016/j.neubiorev.2014.01.012Search in Google Scholar PubMed

Valenti, D., de Bari, L., De Filippis, B., Ricceri, L., and Vacca, R.A. (2014b). Preservation of mitochondrial functional integrity in mitochondria isolated from small cryopreserved mouse brain areas. Anal. Biochem. 444, 25–31.10.1016/j.ab.2013.08.030Search in Google Scholar PubMed

Valenti, D., Vacca, R.A., and de Bari, L. (2015). 3-Bromopyruvate induces rapid human prostate cancer cell death by affecting cell energy metabolism, GSH pool and the glyoxalase system. J. Bioenerg. Biomembr. 47, 493–506.10.1007/s10863-015-9631-ySearch in Google Scholar PubMed

Valenti, D., Rossi, L., Marzulli, D., Bellomo, F., De Rasmo, D., Signorile, A., and Vacca, R.A. (2017). Inhibition of Drp1-mediated mitochondrial fission improves mitochondrial dynamics and bioenergetics stimulating neurogenesis in hippocampal progenitor cells from a Down syndrome mouse model. Biochim. Biophys. Acta Mol. Basis Dis. 1863, 3117–3127.10.1016/j.bbadis.2017.09.014Search in Google Scholar PubMed

Weisz, E.D., Towheed, A., Monyak, R.E., Toth, M.S., Wallace, D.C., and Jongens, T.A. (2018). Loss of Drosophila FMRP leads to alterations in energy metabolism and mitochondrial function. Hum. Mol. Genet. 27, 95–106.10.1093/hmg/ddx387Search in Google Scholar PubMed PubMed Central

Yin, F., Boveris, A., and Cadenas, E. (2014). Mitochondrial energy metabolism and redox signaling in brain aging and neurodegeneration. Antioxid. Redox Signal. 20, 353–371.10.1089/ars.2012.4774Search in Google Scholar PubMed PubMed Central