[en] Besides the role of mature oligodendrocytes in myelin synthesis during the development of the central nervous system (CNS), the oligodendrocyte lineage also encompasses the largest pool of postnatal proliferating progenitors whose behavior in vivo remains broadly elusive in health and disease. We describe here transgenic models that allow us to track the functions and origins of such cells by using proteolipid protein and 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP) gene promoters to direct oligodendroglial expression of different reporters, in particular the green fluorescent protein (GFP). We emphasize that the CNP-GFP mouse, which targets the entire oligodendroglial lineage from embryonic life to adulthood, provides an outstanding tool to study the in vivo properties of oligodendrocyte progenitor cells in normal and damaged CNS.
Disciplines :
Neurology
Author, co-author :
Belachew, Shibeshih ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie
Yuan, Xiaoqing; National Institutes of Health, Bethesda, USA > National Institute of Child Health and Human Development, > Laboratory of Cellular and Synaptic Neurophysiology
Gallo, Vittorio; National Institutes of Health, Bethesda, USA > National Institute of Child Health and Human Development > Laboratory of Cellular and Synaptic Neurophysiology
Language :
English
Title :
Unraveling Oligodendrocyte Origin and Function by Cell-Specific Transgenesis
Miller RH: Oligodendrocyte origins. Trends Neurosci 1996;19:92-96.
Register B, Ben-Hur T, Dubois-Dalcq M: From neural stem cells to myelinating oligodendrocytes. Mol Cell Neurosci 1999;14:287-300.
Lee JC, Mayer-Proschel M, Rao MS: Gliogenesis in the central nervous system. Glia 2000;30: 105-121.
Sternberger NH, Itoyama Y, Kies MW, Webster H deF: Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat C.N.S. J Neurocytol 1978;7:251-263.
Hartman BK, Agrawal HC, Agrawal D, Kalmbach S: Development and maturation of central nervous system myelin: Comparison of immunohistochemical localization of proteolipid protein and basic protein in myelin and oligodendrocytes. Proc Natl Acad Sci USA 1982;79: 4217-4420.
Kurihara T, Nussbaum JL, Mandel P: 2′,3′-Cyclic nucleotide 3′-phosphohydrolase in brains of mutant mice with deficient myelination. J Neurochem 1970;17:993-997.
Readhead C, Popko B, Takahashi N, Shine HD, Saavedra RA, Sidman RL, Hood L: Expression of a myelin basic protein gene in transgenic shiverer mice: Correction of the dysmyelinating phenotype. Cell 1987;48:703-712.
Turnley AM, Morahan G, Okano H, Bernard O, Mikoshiba K, Allison J, Bartlett PF, Miller JF: Dysmyelination in transgenic mice resulting from expression of class I histocompatibility molecules in oligodendrocytes. Nature 1991; 353:566-569.
Yoshioka T, Feigenbaum L, Jay G: Transgenic mouse model for central nervous system demyelination. Mol CellBiol 1991;11:5479-5486.
Miskimins R, Knapp L, Dewey MJ, Zhang X: Cell and tissue-specific expression of a heterologous gene under control of the myelin basic protein gene promoter in transgenic mice. Brain Res Dev Brain Res 1992;65:217-221.
Gow A, Friedrich VL Jr, Lazzarini RA: Myelin basic protein gene contains separate enhancers for oligodendrocyte and Schwann cell expression. J Cell Biol 1992;119:605-616.
Foran DR, Peterson AC: Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J Neurosci 1992;12:4890-4897.
Jensen NA, Pedersen KM, Celis JE, West MJ: Neurological disturbances, premature lethality, and central myelination deficiency in transgenic mice overexpressing the homeo domain transcription factor Oct-6. J Clin Invest 1998;101: 1292-1299.
Tani M, Fuentes ME, Peterson JW, Trapp BD, Durham SK, Loy JK, Bravo R, Ransohoff RM, Lira SA: Neutrophil infiltration, glial reaction, and neurological disease in transgenic mice expressing the chemokine N51/KC in oligodendrocytes. J Clin Invest 1996;98:529-539.
Taupin V, Renno T, Bourbonnière L, Peterson AC, Rodriguez M, Owens T: Increased severity of experimental autoimmune encephalomyelitis, chronic macrophage/microglial reactivity, and demyelination in transgenic mice producing tumor necrosis factor-alpha in the central nervous system. Eur J Immunol 1997;27:905-913.
Ma W, Ribeiro-da-Silva A, Noel G, Julien JP, Cuello AC: Ectopic substance P and calcitonin gene-related peptide immunoreactive fibres in the spinal cord of transgenic mice over-expressing nerve growth factor. Eur J Neurosci 1995;7: 2021-2035.
Goudreau G, Carpenter S, Beaulieu N, Jolicoeur P: Vacuolar myelopathy in transgenic mice expressing human immunodeficiency virus type 1 proteins under the regulation of the myelin basic protein gene promoter. Nat Med 1996;2:655-661.
Hayes C, Kelly D, Murayama S, Komiyama A, Suzuki K, Popko B: Expression of the neu oncogene under the transcriptional control of the myelin basic protein gene in transgenic mice: Generation of transformed glial cells. J Neurosci Res 1992;31:175-187.
Jensen NA, Pedersen KM, Celis JE, West MJ: Failure of central nervous system myelination in MBP/c-myc transgenic mice: Evidence for c-myc cytotoxicity. Oncogene 1998;16:2123-2129.
Hisahara S, Araki T, Sugiyama F, Yagami Ki, Suzuki M, Abe K, Yamamura K, Miyazaki J, Momoi T, Saruta T, Bernard CC, Okano H, Miura M: Targeted expression of baculovirus p35 caspase inhibitor in oligodendrocytes protects mice against autoimmune-mediated demyelination. EMBO J 2000;19:341-348.
Niwa-Kawakita M, Abramowski V, Kalamarides M, Thomas G, Giovannini M: Targeted expression of Cre recombinase to myelinating cells of the central nervous system in transgenic mice. Genesis 2000;26:127-129.
Nagy A: Cre recombinase: The universal reagent for genome tailoring. Genesis 2000;26: 99-109.
Sauer B: Inducible gene targeting in mice using the Cre/lox system. Methods 1998;14:381-392.
Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC: Green fluorescent protein as a marker for gene expression. Science 1994;263: 802-805.
Tsien RY: The green fluorescent protein. Annu Rev Biochem 1998;67:509-544.
Jordan C, Friedrich V Jr, Dubois-Dalcq M: In situ hybridization analysis of myelin gene transcripts in developing mouse spinal cord. J Neurosci 1989;9:248-257.
Kanfer J, Parenty M, Goujet-Zalc C, Monge M, Bernier L, Campagnoni AT, Dautigny A, Zalc B: Developmental expression of myelin proteolipid, basic protein, and 2′,3′-cyclic nucleotide 3′-phosphodiesterase transcripts in different rat brain regions. J Mol Neurosci 1989;1: 39-46.
Ikenaka K, Kagawa T, Mikoshiba K: Selective expression of DM-20, an alternatively spliced myelin proteolipid protein gene product, in developing nervous system and in nonglial cells. J Neurochem 1992;58:2248-2253.
Timsit SG, Bally-Cuif L, Colman DR, Zalc B: DM-20 mRNA is expressed during the embryonic development of the nervous system of the mouse. J Neurochem 1992;58:1172-1175.
Milner RJ, Lai C, Nave KA, Lenoir D, Ogata J, Sutcliffe JG: Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 1985;42:931-939.
Diehl HJ, Schaich M, Budzinski RM, Stoffel W: Individual exons encode the integral membrane domains of human myelin proteolipid protein. Proc Natl Acad Sci USA 1986;83: 9807-9811.
Gardinier MV, Macklin WB, Diniak AJ, Deininger PL: Characterization of myelin proteolipid mRNAs in normal and jimpy mice. Mol Cell Biol 1986;6:3755-3762.
Willard HF, Riordan JR: Assignment of the gene for myelin proteolipid protein to the X chromosome: Implications for X-linked myelin disorders. Science 1985;230:940-942.
Mattei MG, Alliel PM, Dautigny A, Passage E, Pham-Dinh D, Mattei JF, Jollès P: The gene encoding for the major brain proteolipid (PLP) maps on the q-22 band of the human X chromosome. Hum Genet 1986;72:352-353.
Campagnoni AT, Skoff RP: The pathobiology of myelin mutants reveal novel biological functions of the MBP and PLP genes. Brain Pathol 2001;11:74-91.
Agrawal HC, Burton RM, Fishman MA, Mitchell RF, Prensky AL: Partial characterization of a new myelin protein component. J Neurochem 1972;19:2083-2089.
Trifilieff E, Luu B, Nussbaum JL, Roussel G, Espinosa de los Monteros A, Sabatier JM, Van Rietschoten J: A specific immunological probe for the major myelin proteolipid. Confirmation of a deletion in DM-20. FEBS Lett 1986;198: 235-239.
Nave KA, Lai C, Bloom FE, Milner RJ: Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proc Natl Acad Sci USA 1987;84:5665-5669.
Simons R, Alon N, Riordan JR: Human myelin DM-20 proteolipid protein deletion defined by cDNA sequence. Biochem Biophys Res Commun 1987;146:666-671.
Bongarzone ER, Campagnoni CW, Kampf K, Jacobs EC, Handley VW, Schonmann V, Campagnoni AT: Identification of a new exon in the myelin proteolipid protein gene encoding novel protein isoforms that are restricted to the somata of oligodendrocytes and neurons. J Neurosci 1999;19:8349-8357.
Nave KA, Lemke G: Induction of the myelin proteolipid protein (PLP) gene in C6 glioblastoma cells: Functional analysis of the PLP promotor. J Neurosci 1991;11:3060-3069.
Cook JL, Irias-Donaghey S, Deininger PL: Regulation of rodent myelin proteolipid protein gene expression. Neurosci Lett 1992;137:56-60.
Berndt JA, Kim JG, Hudson LD: Identification of cis-regulatory elements in the myelin proteolipid protein (PLP) gene. J Biol Chem 1992;267:14730-14737.
Wight PA, Duchala CS, Readhead C, Macklin WB: A myelin proteolipid protein-LacZ fusion protein is developmentally regulated and targeted to the myelin membrane in transgenic mice. J Cell Biol 1993;123:443-454.
Spassky N, Goujet-Zalc C, Parmantier E, Olivier C, Martinez S, Ivanova A, Ikenaka K, Macklin W, Cerruti I, Zalc B, Thomas JL: Multiple restricted origin of oligodendrocytes. J Neurosci 1998;18:8331-8343.
Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB: Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 2000;218:259-274.
Vogel US, Thompson RJ: Molecular structure, localization, and possible functions of the myelin-associated enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase. J Neurochem 1988;50: 1667-1677.
Sprinkle TJ: 2′,3′-Cyclic nucleotide 3′-phosphodiesterase, an oligodendrocyte-Schwann cell and myelin-associated enzyme of the nervous system. Crit Rev Neurobiol 1989;4:235-301.
Scherer SS, Braun PE, Grinspan J, Collarini E, Wang DY, Kamholz J: Differential regulation of the 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene during oligodendrocyte development. Neuron 1994;12:1363-1375.
Monoh K, Kurihara T, Sakimura K, Takahashi Y: Structure of mouse 2′,3′-cyclic-nucleotide 3′-phosphodiesterase gene. Biochem Biophys Res Commun 1989;165:1213-1220.
Kurihara T, Monoh K, Sakimura K, Takahashi Y: Alternative splicing of mouse brain 2′,3′-cyclic-nucleotide 3′-phosphodiesterase mRNA. Biochem Biophys Res Commun 1990;170: 1074-1081.
Douglas AJ, Thompson RJ: Structure of the myelin membrane enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase: Evidence for two human mRNAs. Biochem Soc Trans 1993;21: 295-297.
Gravel M, DeAngelis D, Braun PE: Molecular cloning and characterization of rat brain 2′,3′-cyclic nucleotide 3′-phosphodiesterase isoform 2. J Neurosci Res 1994;38:243-247.
O'Neill RC, Minuk J, Cox ME, Braun PE, Gravel M: CNP2 mRNA directs synthesis of both CNP1 and CNP2 polypeptides. J Neurosci Res 1997;50:248-257.
Gravel M, Di Polo A, Valera PB, Braun PE: Four-kilobase sequence of the mouse CNP gene directs spatial and temporal expression of lacZ in transgenic mice. J Neurosci Res 1998; 53:393-404.
Chandross KJ, Cohen RI, Paras P Jr, Gravel M, Braun PE, Hudson LD: Identification and characterization of early glial progenitors using a transgenic selection strategy. J Neurosci 1999;19:759-774.
Yuan X, Chittajallu R, Gallo V: In vivo identification, characterization and FACS purification of oligodendrocyte lineage cells using a CNP-GFP transgenic mouse model. Abstr Soc Neurosci Meet (Ref N 1496) 2001.
Richardson WD, Smith HK, Sun T, Pringle NP, Hall A, Woodruff R: Oligodendrocyte lineage and the motor neuron connection. Glia 2000;29:136-142.
Spassky N, Olivier C, Perez-Villegas E, Goujet-Zalc C, Martinez S, Thomas Jl, Zalc B: Single or multiple oligodendroglial lineages: A controversy. Glia 2000;29:143-148.
Pringle NP, Richardson WD: A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 1993;117:525-533.
Pringle NP, Yu WP, Guthrie S, Roelink H, Lumsden A, Peterson AC, Richardson WD: Determination of neuroepithelial cell fate: Induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev Biol 1996;177:30-42.
Timsit S, Martinez S, Allinquant B, Peyron F, Puelles L, Zalc B: Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J Neurosci 1995;15:1012-1024.
Yu WP, Collarini EJ, Pringle NP, Richardson WD: Embryonic expression of myelin genes: Evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 1994;12:1353-1362.
Hardy RJ, Friedrich VL Jr: Oligodendrocyte progenitors are generated throughout the embryonic mouse brain, but differentiate in restricted foci. Development 1996;122:2059-2069.
Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, Richardson WD: Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 1998;20:869-882.
Fruttiger M, Karlsson L, Hall AC, Abramsson A, Calver AR, Boström H, Willetts K, Bertold CH, Heath JK, Betsholtz C, Richardson WD: Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 1999;126:457-467.
Briscoe J, Ericson J: The specification of neuronal identity by graded sonic hedgehog signalling. Semin Cell Dev Biol 1999;10:353-362.
Briscoe J, Pierani A, Jessell TM, Ericson J: A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 2000;101:435-445.
Orentas DM, Hayes JE, Dyer KL, Miller RH: Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 1999;126:2419-2429.
Poncet C, Soula C, Trousse F, Kan P, Hirsinger E, Pourquié O, Duprat AM, Cochard P: Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: Effects of notochord and floor plate grafts, and of sonic hedgehog. Mech Dev 1996;60:13-32.
Sussel L, Marin O, Kimura S, Rubenstein JL: Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: Evidence for a transformation of the pallidum into the striatum. Development 1999;126:3359-3370.
Nery S, Wichterle H, Fishell G: Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 2001; 128:527-540.
Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH: Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000;25:317-329.
Zhou Q, Wang S, Anderson DJ: Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000;25:331-343.
Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y: Dynamic expression of basic helix-loop-helix Olig family members: Implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 2000;99:143-148.
Kondo T, Raff M: Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 2000;289:1754-1757.
Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A: Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 1994;12:11-24.
Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman SA, Okano H: Nestin-EGFP transgenic mice: Visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 2001;17:259-273.
Malatesta P, Hartfuss E, Gotz M: Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000;127:5253-5263.
Wegner M: Expression of transcription factors during oligodendroglial development. Microsc Res Tech 2001;52:746-752.
Gallo V, Ghiani CA: Glutamate receptors in glia: New cells, new inputs and new functions. Trends Pharmacol Sci 2000;21:252-258.
Ghiani C, Gallo V: Inhibition of cyclin E-cyclin-dependent kinase 2 complex formation and activity is associated with cell cycle arrest and withdrawal in oligodendrocyte progenitor cells. J Neurosci 2001;21:1274-1282.
Levine JM, Reynolds R, Fawcett JW: The oligodendrocyte precursor cell in health and disease. Trends Neurosci 2001;24:39-47.
Chittajallu R, Yuan X, McBain CJ, Gallo V: Electrophysiological characterization of oligodendrocyte cells in a CNP-GFP transgenic mouse model. Abstr Soc Neurosci Meet (Ref N 2727) 2001.
Dawson MR, Levine JM, Reynolds R: NG2-expressing cells in the central nervous system: Are they oligodendroglial progenitors? J Neurosci Res 2000;61:471-479.
Levine JM, Stincone F, Lee YS: Development and differentiation of glial precursor cells in the rat cerebellum. Glia 1993;7:307-321.
Nishiyama A, Yu M, Drazba JA, Tuohy VK: Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. J Neurosci Res 1997;48:299-312.
Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH: Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000;20:2218-2228.
Ong WY, Levine JM: A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience 1999;92:83-95.
Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M: Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 1999;26:84-91.
Bergles DE, Roberts JD, Somogyi P, Jahr CE: Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 2000;405:187-191.
Araque A, Carmignoto G, Haydon P: Dynamic signaling between astrocytes and neurons. Annu Rev Physiol 2001;63:795-813.
Haydon PG: GLIA: Listening and talking to the synapse. Nat Rev Neurosci 2001;2:185-193.
Ullian EM, Sapperstein SK, Christopherson KS, Barres BA: Control of synapse number by glia. Science 2001;291:657-661.
Oliet SHR, Piet R, Poulain DA: Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 2001;292:923-926.
Iino M, Goto K, Kakegawa W, Okado H, Sudo M, Ishiuchi S, Miwa A, Takayasu Y, Saito I, Tsuzuki K, Ozawa S: Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science 2001;292:926-929.
Gallo V, Chittajallu R: Unwrapping glial cells from the synapse: What lies inside? Science 2001;292:872-873.
Mathis C, Hindelang C, LeMeur M, Borrelli E: A transgenic mouse model for inducible and reversible dysmyelination. J Neurosci 2000;20: 7698-7705.
