Perineuronal oligodendrocytes in health and disease: the journey so far

References

Arai, N., Umitsu, R., Komori, T., Hayashi, M., Kurata, K., Nagata, J., Tamagawa, K., Mizutani, T., Oda, M., and Morimatsu, Y. (2003). Peculiar form of cerebral microdysgenesis characterized by white matter neurons with perineuronal and perivascular glial satellitosis: a study using a variety of human autopsied brains. Pathol. Int. 53, 345–352.10.1046/j.1440-1827.2003.01480.xSuche in Google Scholar

Barron, K.D., Marciano, F.F., Amundson, R., and Mankes, R. (1990). Perineuronal glial responses after axotomy of central and peripheral axons. A comparison. Brain Res. 523, 219–229.10.1016/0006-8993(90)91490-8Suche in Google Scholar

Battefeld, A., Klooster, J., and Kole, M.H. (2016). Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity. Nat. Commun. 7, 11298.10.1038/ncomms11298Suche in Google Scholar PubMed PubMed Central

Baumann, N. and Pham-Dinh, D. (2001). Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 81, 871–927.10.1152/physrev.2001.81.2.871Suche in Google Scholar PubMed

Bernstein, H.G., Keilhoff, G., Bukowska, A., Ziegeler, A., Funke, S., Dobrowolny, H., Kanakis, D., Bogerts, B., and Lendeckel, U. (2004). ADAM (a disintegrin and metalloprotease) 12 is expressed in rat and human brain and localized to oligodendrocytes. J. Neurosci. Res. 75, 353–360.10.1002/jnr.10858Suche in Google Scholar PubMed

Bernstein, H.G., Smalla, K.H., Dürrschmidt, D., Keilhoff, G., Dobrowolny, H., Steiner, J., Schmitt, A., Kreutz, M.R., and Bogerts, B. (2012). Increased density of prohibitin-immunoreactive oligodendrocytes in the dorsolateral prefrontal white matter of subjects with schizophrenia suggests extraneuronal roles for the protein in the disease. Neuromol. Med. 14, 270–280.10.1007/s12017-012-8185-ySuche in Google Scholar PubMed

Bernstein, H.G., Tausch, A., Wagner, R., Steiner, J., Seeleke, P., Walter, M., Dobrowolny, H., and Bogerts, B. (2013). Disruption of glutamate-glutamine-GABA cycle significantly impacts on suicidal behaviour: survey of the literature and own findings on glutamine synthetase. CNS Neurol. Disord. Drug Targets 12, 900–913.10.2174/18715273113129990091Suche in Google Scholar PubMed

Bernstein, H.G., Bannier, J., Meyer-Lotz, G., Steiner, J., Keilhoff, G., Dobrowolny, H., Walter, M., and Bogerts, B. (2014). Distribution of immunoreactive glutamine synthetase in the adult human and mouse brain. Qualitative and quantitative observations with special emphasis on extra-astroglial protein localization. J. Chem. Neuroanat. 61–62, 33–50.10.1016/j.jchemneu.2014.07.003Suche in Google Scholar PubMed

Bernstein, H.G., Meyer-Lotz, G., Dobrowolny, H., Bannier, J., Steiner, J., Walter, M., and Bogerts, B. (2015a). Reduced density of glutamine synthetase immunoreactive astrocytes in different cortical areas in major depression but not in bipolar I disorder. Front. Cell. Neurosci. 9, 273.10.3389/fncel.2015.00273Suche in Google Scholar PubMed PubMed Central

Bernstein, H.G., Steiner, J., Guest, P.C., Dobrowolny, H., and Bogerts, B. (2015b). Glial cells as key players in schizophrenia pathology: recent insights and concepts of therapy. Schizophr. Res. 161, 4–18.10.1016/j.schres.2014.03.035Suche in Google Scholar PubMed

Black, J.E., Kodish, I.M., Grossman, A.W., Klintsova, A.Y., Orlovskaya, D., Vostrikov, V., Uranova, N., and Greenough, W.T. (2004). Pathology of layer V pyramidal neurons in the prefrontal cortex of patients with schizophrenia. Am. J. Psychiatry 161, 742–744.10.1176/appi.ajp.161.4.742Suche in Google Scholar

Brownson, R.H. (1955). Perineuronal satellite cells in the motor cortex of aging brains. J. Neuropathol. Exp. Neurol. 14, 424–432.Suche in Google Scholar

Carlton, W.W. (1966). Response of mice to the chelating agents sodium diethyldithiocarbamate, alpha-benzoinoxime, and biscyclohexanone oxaldihydrazone. Toxicol. Appl. Pharmacol. 8, 512–552.10.1016/0041-008X(66)90062-7Suche in Google Scholar

Chabas, D., Baranzini, S.E., Mitchell, D., Bernard, C.C., Rittling, S.R., Denhardt, D.T., Sobel, R.A., Lock, C., Karpuj, M., Pedotti, R., et al. (2001). The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294, 1731–1735.10.1100/tsw.2002.326Suche in Google Scholar

D’Amelio, F., Eng, L.F., and Gibbs, M.A. (1990). Glutamine synthetase immunoreactivity is present in oligodendroglia of various regions of the central nervous system. Glia 3, 335–341.10.1002/glia.440030504Suche in Google Scholar

Del Río Hortega, P. (1928). Tercera aportación al conocimiento morfológico e interpretación funcional de la oligodendroglía. Mem. Real Soc. Esp. Hist. Nat. 14, 5–122.Suche in Google Scholar

Del Río Hortega, P. (1942). La neuroglía normal. Conceptos de neurogliona y angiogliona. Arch. Histol. Norm. Patol. 1, 5–71.Suche in Google Scholar

Devon, R.M. (1990). Comparison of oligodendrocytes grown in neocortex and spinal cord aggregate cultures. Brain Res. 429, 289–294.10.1016/0165-3806(87)90109-XSuche in Google Scholar

Eisenbarth, G.S., Walsh, F.S., and Nirenberg, M. (1979). Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. U.S.A. 76, 4913–4917.10.1073/pnas.76.10.4913Suche in Google Scholar PubMed PubMed Central

Faber-Zuschratter, H., Hüttmann, K., Steinhäuser, C., Becker, A., Schramm, J., Okafo, U., Shanley, D., and Yilmazer-Hanke, D.M. (2009). Ultrastructural and functional characterization of satellitosis in the human lateral amygdala associated with Ammon’s horn sclerosis. Acta Neuropathol. 117, 545–555.10.1007/s00401-009-0504-5Suche in Google Scholar PubMed

Falkai, P., Steiner, J., Malchow, B., Shariati, J., Knaus, A., Bernstein, H.G., Schneider-Axmann, T., Kraus, T., Hasan, A., Bogerts, B., et al. (2016a). Oligodendrocyte and interneuron density in hippocampal subfields in schizophrenia and association of oligodendrocyte number with cognitive deficits. Front. Cell. Neurosci. 10, 78.10.3389/fncel.2016.00078Suche in Google Scholar PubMed PubMed Central

Falkai, P., Malchow, B., Wetzestein, K., Nowastowski, V., Bernstein, H.G., Steiner, J., Schneider-Axmann, T., Kraus, T., Hasan, A., Bogerts, B., et al. (2016b). Decreased oligodendrocyte and neuron number in anterior hippocampal areas and the entire hippocampus in schizophrenia: a stereological postmortem study. Schizophr. Bull. 42(Suppl. 1), S4–S12.10.1093/schbul/sbv157Suche in Google Scholar PubMed PubMed Central

Farkas, N., Lendeckel, U., Dobrowolny, H., Funke, S., Steiner, J., Keilhoff, G., Schmitt, A., Bogerts, B., and Bernstein, H.G. (2010). Reduced density of ADAM 12-immunoreactive oligodendrocytes in the anterior cingulate white matter of patients with schizophrenia. World J. Biol. Psychiatry 11, 556–566.10.3109/15622970903497936Suche in Google Scholar PubMed

Herndon, R.M., Price, D.L., and Weiner, L.P. (1977). Regeneration of oligodendroglia during recovery from demyelinating disease. Science 195, 693–694.10.1126/science.190678Suche in Google Scholar

Hiroishi, S. and Lee, C.C. (1936). Origin of senile plaques. Arch. Neurol. Psychol. 35, 827–838.10.1001/archneurpsyc.1936.02260040135009Suche in Google Scholar

Hof, P.R., Haroutunian, V., Friedrich, V.L., Jr., Byne, W., Buitron, C., Perl, D.P., and Davis, K.L. (2003). Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biol. Psychiatry 53, 1075–1085.10.1016/S0006-3223(03)00237-3Suche in Google Scholar

Kim, S. and Webster, M.J. (2010). Correlation analysis between genome-wide expression profiles and cytoarchitectural abnormalities in the prefrontal cortex of psychiatric disorders. Mol. Psychiatry 15, 326–336.10.1038/mp.2008.99Suche in Google Scholar

King, J.S. (1968). Perineuronal glial cells and processes in the rabbit neocortex. Anat. Rec. 161, 111–123.10.1002/ar.1091610112Suche in Google Scholar

Kolomeets, N.S. and Uranova, N.A. (2018). Reduced oligodendrocyte density in layer 5 of the prefrontal cortex in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 269, 379–86.10.1007/s00406-018-0888-0Suche in Google Scholar

Kuznetsova, V.I. (1979). Pathomorphology of the brains of schizophrenic patients treated with psychotropic drugs (concerning drug pathomorphosis). Zh. Nevropatol. Psikhiatr. SS Korsakova 79, 929–933.Suche in Google Scholar

Lendeckel, U., Wolke, C., Bernstein, H.G., and Keilhoff, G. (2015). Effects of nitric oxide synthase deficiency on a disintegrin and metalloproteinase domain-containing protein 12 expression in mouse brain samples. Mol. Med. Rep. 12, 2253–2262.10.3892/mmr.2015.3643Suche in Google Scholar

Levine, S.M. and Torres, M.V. (1993). Satellite oligodendrocytes and myelin are displaced in the cortex of the reeler mouse. Brain Res. Dev. Brain Res. 75, 279–284.10.1016/0165-3806(93)90032-6Suche in Google Scholar

Lin, W.L., Lewis, J., Yen, S.H., Hutton, M., and Dickson, D.W. (2003). Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation. Am. J. Pathol. 162, 213–218.10.1016/S0002-9440(10)63812-6Suche in Google Scholar

Ludwin, S.K. (1978). Central nervous system demyelination and remyelination in the mouse. An ultrastructural study of cuprizone toxicity. Lab. Invest. 39, 597–612.Suche in Google Scholar

Ludwin, S.K. (1979). The perineuronal satellite oligodendrocyte. A role in remyelination. Acta Neuropathol. 47, 49–53.10.1007/BF00698272Suche in Google Scholar PubMed

Ludwin, S.K. (1984). The function of perineuronal satellite oligodendrocytes: an immunohistochemical study. Neuropathol. Appl. Neurobiol. 10, 143–149.10.1111/j.1365-2990.1984.tb00345.xSuche in Google Scholar PubMed

Luse, S.A. (1960). The ultrastructure of normal and abnormal oligodendroglia. Anat. Rec. 138, 461–492.10.1002/ar.1091380406Suche in Google Scholar PubMed

Minagar, A., Barnett, M.H., Benedict, R.H., Pelletier, D., Pirko, I., Sahraian, M.A., Frohman, E., and Zivadinov, R. (2013). The thalamus and multiple sclerosis: modern views on pathologic, imaging, and clinical aspects. Neurology 80, 210–219.10.1212/WNL.0b013e31827b910bSuche in Google Scholar PubMed PubMed Central

Mori, S. and LeBlond, C.P. (1970). Electron-microscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J. Comp. Neurol. 139, 1–30.10.1002/cne.901390102Suche in Google Scholar PubMed

Morita, T., Shimada, A., Ohama, E., Umemura, T., and Fukuda, S. (1999). Oligodendroglial vacuolar degeneration in the bilateral motor cortices and astrocytosis in epileptic beagle dogs. J. Vet. Med. Sci. 61, 107–111.10.1292/jvms.61.107Suche in Google Scholar PubMed

Nasrabady, S.E., Rizvi, B., Goldman, J.E., and Brickman, A.M. (2018). White matter changes in Alzheimer’s disease: a focus on myelin and oligodendrocytes. Acta Neuropathol. Commun. 6, 22.10.1186/s40478-018-0515-3Suche in Google Scholar PubMed PubMed Central

Newcombe, J., Uddin, A., Dove, R., Patel, B., Turski, L., Nishizawa, Y., and Smith, T. (2008). Glutamate receptor expression in multiple sclerosis lesions. Brain Pathol. 18, 52–61.10.1111/j.1750-3639.2007.00101.xSuche in Google Scholar PubMed PubMed Central

Ogawa, Y. and Kojima, T. (1983). Some observations on the morphological characteristics of oligodendrocytes in the mesencephalic nucleus of the trigeminal nerve of the cat as revealed by reduced silver impregnation method. Okajiams Folia Anat. 60, 147–160.10.2535/ofaj1936.60.2-3_147Suche in Google Scholar PubMed

Penfield, W. (1930). A further modification of Del Rio-Hortega’s method of staining oligodendroglia. Am. J. Pathol. 6, 445–448.Suche in Google Scholar

Pérez-Cerdá, F., Sánchez-Gómez, M.V., and Matute, C. (2015). Pío del Río Hortega and the discovery of the oligodendrocytes. Front. Neuroanat. 9, 92.10.3389/fnana.2015.00092Suche in Google Scholar PubMed PubMed Central

Petito, C.K. (1986). Transformation of postischemic perineuronal glial cells. I. Electron microscopic studies. J. Cereb. Blood Flow Metab. 6, 616–624.10.1038/jcbfm.1986.109Suche in Google Scholar PubMed

Philips, T. and Rothstein, J.D. (2017). Oligodendroglia: metabolic supporters of neurons. J. Clin. Invest. 127, 3271–3280.10.1172/JCI90610Suche in Google Scholar

Rajkowska, G. and Miguel-Hidalgo, J.J. (2007). Gliogenesis and glial pathology in depression. CNS Neurol. Disord. Drug Targets 6, 219–233.10.2174/187152707780619326Suche in Google Scholar

Schmitt, A., Steyskal, C., Bernstein, H.G., Schneider-Axman, T., Parlapani, E., Schaeffer, E.L., Gattaz, W.F., Bogerts, B., Schmitz, C., and Falkai, P. (2009). Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathol. 117, 395–407.10.1007/s00401-008-0430-ySuche in Google Scholar

Schroeter, M.L., Abdul-Khaliq, H., Sacher, J., Steiner, J., Blasig, I.E., and Mueller, K. (2010). Mood disorders are glial disorders: evidence from in vivo studies. Cardiovasc. Psychiatry Neurol. 2010, 780645.10.1155/2010/780645Suche in Google Scholar

Seifert, G. and Steinhäuser, C. (2018). Heterogeneity and function of hippocampal macroglia. Cell Tissue Res. 373, 653–670.10.1007/s00441-017-2746-1Suche in Google Scholar

Selemon, L.D., Rajkowska, G., and Goldman-Rakic, P.S. (1995). Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch. Gen. Psychiatry 52, 805–818.10.1001/archpsyc.1995.03950220015005Suche in Google Scholar

Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., and Van Hoesen, G.W. (2001). Prefrontal cortex in humans and apes: a comparative study of area 10. Am. J. Phys. Antropol. 114, 224–241.10.1002/1096-8644(200103)114:3<224::AID-AJPA1022>3.0.CO;2-ISuche in Google Scholar

Sigaard, R.K., Kjaer, M., and Pakkenberg, B.C. (2016). Development of cell populations in the brain white matter of young children. Cereb Cortex 26, 89–95.10.1093/cercor/bhu178Suche in Google Scholar

Stefanits, H., Czech, T., Patarala, E., Baumgartner, C., Derhasching, N., Slana, A., and Kovacs, G.G. (2012). Prominent oligodendroglial response in surgical specimens of patients with temporal lobe epilepsy. Clin. Neuropathol. 31, 409–417.10.5414/NP300536Suche in Google Scholar

Steiner, J., Sarnyai, Z., Westphal, S., Gos, T., Bernstein, H.G., Bogerts, B., and Keilhoff, G. (2011). Protective effects of haloperidol and clozapine on energy-deprived OLN-93 oligodendrocytes. Eur. Arch. Psychiatry Clin. Neurosci. 261, 477–482.10.1007/s00406-011-0197-3Suche in Google Scholar

Szuchet, S. and Seeger, M.A. (2003). Oligodendrocyte phenotypical and morphological heterogeneity: a reexamination of old concepts in view of new findings. Adv. Mol. Cell Biol. 31, 53–73.10.1016/S1569-2558(03)31002-1Suche in Google Scholar

Szuchet, S., Plachetzki, D.C., and Eaton, K.S. (2001). Oligodendrocyte transmembrane protein: a novel member of the glutamate-binding protein subfamily. Biochem. Biophys. Res. Commun. 283, 900–907.10.1006/bbrc.2001.4859Suche in Google Scholar

Szuchet, S., Nielsen, J.A., Lovas, G., Domowicz, M.S., de Velasco, J.M., Maric, D., and Hudson, L.D. (2011). The genetic signature of perineuronal oligodendrocytes reveals their unique phenotype. Eur. J. Neurosci. 34, 1906–1922.10.1111/j.1460-9568.2011.07922.xSuche in Google Scholar

Takasaki, C., Yamasaki, M., Uchigashima, M., Konno, K., Yanagawa, Y., and Watanabe, M. (2010). Cytochemical and cytological properties of perineuronal oligodendrocytes in the mouse cortex. Eur. J. Neurosci. 32, 1326–1336.10.1111/j.1460-9568.2010.07377.xSuche in Google Scholar

Taniike, M., Mohri, I., Eguchi, N., Beuckmann, C.T., Suzuki, K., and Urade, Y. (2002). Perineuronal oligodendrocytes protect against neuronal apoptosis through the production of lipocalin-type prostaglandin D synthase in a genetic demyelinating model. J. Neurosci. 22, 4885–4896.10.1523/JNEUROSCI.22-12-04885.2002Suche in Google Scholar

Uranova, N.A., Vostrikov, V.M., Orlovskaya, D.D., and Rachmanova, V.I. (2004). Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr. Res. 67, 269–275.10.1016/S0920-9964(03)00181-6Suche in Google Scholar

Uranova, N.A., Vostrikov, V.M., Vikhreva, O.V., Zimina, I.S., Kolomeets, N.S., and Orlovskaya, D.D. (2017). The role of oligodendrocyte pathology in schizophrenia. Int. J. Neuropsychopharmacol. 10, 537–545.10.1017/S1461145707007626Suche in Google Scholar PubMed

van Landeghem, F.K., Weiss, T., and von Deimling, A. (2007). Expression of PACAP and glutamate transporter proteins in satellite oligodendrocytes of the human CNS. Regul. Pept. 142, 52–59.10.1016/j.regpep.2007.01.008Suche in Google Scholar PubMed

Verkhratsky, A. and Butt, A., eds. (2013). Glial Physiology and Pathophysiology. Chapter V. Oligodendrocytes (Hoboken, NJ: Wiley-Blackwell), pp. 245–319. ISBN-10: 0470978538.10.1002/9781118402061Suche in Google Scholar

Vijayan, V.K., Zhou, S.S., Russell, M.J., Geddes, J., Ellis, J., and Cotman, C.W. (1993). Perineuronal satellitosis in the human hippocampal formation. Hippocampus 3, 239–250.10.1002/hipo.450030215Suche in Google Scholar PubMed

Vostrikov, V.M. and Uranova, N.A. (2016). [A possible relationship between disturbed interhemispheric asymmetry and a decrease in perineuronal oligodendrocytes in schizophrenia]. Zh. Nevrol. Psikhiatr. Im S S Korsakova 116, 70–73.10.17116/jnevro20161168170-73Suche in Google Scholar PubMed

Vostrikov, V.M. and Uranova, N.A. (2018). [Deficit of oligodendrocytes in the frontal cortex in schizophrenia]. Zh. Nevrol. Psikhiatr. Im S S Korsakova 118, 100–103.10.17116/jnevro201811851100Suche in Google Scholar PubMed

Vostrikov, V.M., Uranova, N.A., Rakhmanova, V.I., and Orlovskaya, D.D. (2004). Lowered oligodendroglial cell density in the prefrontal cortex in schizophrenia. Zh. Nevrol. Psikhiatr. Im S S Korsakova 104, 47–51.Suche in Google Scholar

Vostrikov, V.M., Uranova, N.A., and Orlovskaya, D.D. (2007). Deficit of perineuronal oligodendrocytes in the prefrontal cortex in schizophrenia and mood disorders. Schizophr. Res. 94, 273–280.10.1016/j.schres.2007.04.014Suche in Google Scholar PubMed

Vostrikov, V.M., Artiukhova, O.A., Kholmova, M.A., Samodorov, A.V., and Uranova, N.A. (2013). The spatial organization of oligodendrocytes and pyramidal neurons in the frontal limbic cortex of patients with schizophrenia and healthy people: a computer morphometric study. Zh. Nevrol. Psikhiatr. Im S S Korsakova 113, 67–70.Suche in Google Scholar

Vostrikov, M.V., Kolomeets, N.S., and Uranova, N.A. (2014). Deficit of perineuronal oligodendrocytes in the inferior parietal lobule is associated with lack of insight in schizophrenia. Eur. J. Psychiatry 28, 114–123.10.4321/S0213-61632014000200005Suche in Google Scholar

Weider, M., Wegener, A., Schmitt, C., Küspert, M., Hillgärtner, S., Bösl, M.R., Hermans-Borgmeyer, I., Nait-Oumesmar, B., and Wegner, M.E. (2015). Elevated in vivo levels of a single transcription factor directly convert satellite glia into oligodendrocyte-like cells. PLoS Genet. 11, e1005008.10.1371/journal.pgen.1005008Suche in Google Scholar PubMed PubMed Central

Wilson, C. and Terry, A.V., Jr. (2010). Neurodevelopmental animal models of schizophrenia: role in novel drug discovery and development. Clin. Schizophr. Rel. Psych. 4, 124–137.10.3371/CSRP.4.2.4Suche in Google Scholar PubMed PubMed Central

Wilson, H.C., Onischke, C., and Raine, C.S. (2003). Human oligodendrocyte precursor cells in vitro: phenotypic analysis and differential response to growth factors. Glia 44, 153–165.10.1002/glia.10280Suche in Google Scholar PubMed

Yamazaki, Y., Hozumi, Y., Kaneko, K., and Fujii, S. (2018). Modulatory effects of perineuronal oligodendrocytes on neuronal activity in the rat hippocampus. Neurochem. Res. 43, 18–31.10.1007/s11064-017-2278-9Suche in Google Scholar PubMed

Zhou, P., Qian, L., D’Aurelio, M., Cho, S., Wang, G., Manfredi, G., Pickel, V., and Iadecola, C. (2012). Prohibitin reduces mitochondrial free radical production and protects brain cells from different injury modalities. J. Neurosci. 32, 583–592.10.1523/JNEUROSCI.2849-11.2012Suche in Google Scholar PubMed PubMed Central