Oligodendrocyte myelin glycoprotein (OMgp): evolution, structure and function

The oligodendrocyte myelin glycoprotein (OMgp) is a glycosylphosphatidylinositol-anchored protein expressed by neurons and oligodendrocytes in the central nervous system (CNS). Although the precise function of OMgp is yet to be determined in vivo, recent in vitro studies suggested roles for this protein in both the developing and adult central nervous system. In vitro experiments demonstrated the participation of OMgp in growth cone collapse and inhibition of neurite outgrowth through its interaction with NgR, the receptor for Nogo. This function requires its leucine-rich repeat domain, a highly conserved region in OMgp during mammal evolution. OMgp leucine-rich repeat domain is also implicated in the inhibition of cell proliferation. Based on its developmental expression, localization and structure, OMgp may also be involved in the formation and maintenance of myelin sheaths. Cell proliferation, neuronal sprouting and myelination are crucial processes involved in brain development and regeneration after injury. Here, we review the information available on the structure and evolution of OMgp, summarize its tissue expression and discuss its putative role(s) during the development and in adult CNS.

[1]  T. Johns,et al.  Myelin oligodendrocyte glycoprotein: a novel candidate autoantigen in multiple sclerosis , 1997, Journal of Molecular Medicine.

[2]  M. Schwab,et al.  Systemic Deletion of the Myelin-Associated Outgrowth Inhibitor Nogo-A Improves Regenerative and Plastic Responses after Spinal Cord Injury , 2003, Neuron.

[3]  J. Gulcher,et al.  The OMgp gene, a second growth suppressor within the NF1 gene , 1998, Oncogene.

[4]  R. Coffin,et al.  The Nogo receptor, its ligands and axonal regeneration in the spinal cord; A review , 2002, Journal of neurocytology.

[5]  K. Kullander,et al.  Mechanisms and functions of eph and ephrin signalling , 2002, Nature Reviews Molecular Cell Biology.

[6]  E. Bongarzone Induction of Oligodendrocyte Fate During the Formation of the Vertebrate Neural Tube , 2002, Neurochemical Research.

[7]  B. Tang,et al.  Nogos and the Nogo‐66 receptor: Factors inhibiting CNS neuron regeneration , 2002, Journal of neuroscience research.

[8]  P. Thibault,et al.  Oligodendrocyte‐myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth , 2002, Journal of neurochemistry.

[9]  T. Waehneldt,et al.  Phylogeny of Myelin Proteins , 1990, Annals of the New York Academy of Sciences.

[10]  Robert H Miller Regulation of oligodendrocyte development in the vertebrate CNS , 2002, Progress in Neurobiology.

[11]  B. Zalc,et al.  Origins of Vertebrate Success , 2000, Science.

[12]  M. Poo,et al.  A p75NTR and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein , 2002, Nature Neuroscience.

[13]  J. Mandel,et al.  Monogenic causes of X-linked mental retardation , 2001, Nature Reviews Genetics.

[14]  O. Steward,et al.  Lack of Enhanced Spinal Regeneration in Nogo-Deficient Mice , 2003, Neuron.

[15]  Michael Klinger,et al.  A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family 1 , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  M. Schwab,et al.  Growth of regenerating goldfish axons is inhibited by rat oligodendrocytes and CNS myelin but not but not by goldfish optic nerve tract oligodendrocytelike cells and fish CNS myelin , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  M. Schachner,et al.  Crucial Role for the Myelin‐associated Glycoprotein in the Maintenance of Axon‐Myelin Integrity , 1995, The European journal of neuroscience.

[18]  Margaret Robertson,et al.  The neurofibromatosis type 1 gene encodes a protein related to GAP , 1990, Cell.

[19]  D. Ledbetter,et al.  The human homolog of murine Evi-2 lies between two von Recklinghausen neurofibromatosis translocations. , 1990, Genomics.

[20]  A. Fournier,et al.  Repulsive factors and axon regeneration in the CNS , 2001, Current Opinion in Neurobiology.

[21]  L. Hood,et al.  The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system , 1989, Journal of Molecular Evolution.

[22]  M. Noble,et al.  Platelet‐derived growth factor is mitogenic for O‐2Aadult progenitor cells , 1991, Glia.

[23]  T. Waehneldt,et al.  Major Central Nervous System Myelin Glycoprotein of the African Lungfish (Protopterus dolloi) Cross‐Reacts with Myelin Proteolipid Protein Antibodies, Indicating a Close Phylogenetic Relationship with Amphibians , 1986, Journal of neurochemistry.

[24]  Marc Tessier-Lavigne,et al.  Conservation and divergence of axon guidance mechanisms , 1999, Current Opinion in Neurobiology.

[25]  M. Schwab,et al.  Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors , 1995, Nature.

[26]  J. Silver,et al.  Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  F. Castro Chemotropic Molecules: Guides for Axonal Pathfinding and Cell Migration During CNS Development , 2003 .

[28]  B. Sommer,et al.  Characterization of two novel proteins, NgRH1 and NgRH2, structurally and biochemically homologous to the Nogo‐66 receptor , 2003, Journal of neurochemistry.

[29]  J. Friedman Epidemiology of neurofibromatosis type 1. , 1999, American journal of medical genetics.

[30]  D. Mikol,et al.  A phosphatidylinositol-linked peanut agglutinin-binding glycoprotein in central nervous system myelin and on oligodendrocytes , 1988, The Journal of cell biology.

[31]  B. Kobe,et al.  The leucine-rich repeat as a protein recognition motif. , 2001, Current opinion in structural biology.

[32]  M. Weaver,et al.  NF1 microdeletion breakpoints are clustered at flanking repetitive sequences. , 2000, Human molecular genetics.

[33]  M. Giovannini,et al.  Mouse models of human cancer consortium symposium on nervous system tumors. , 2003, Cancer research.

[34]  H. Hameister,et al.  Molecular characterization and gene content of breakpoint boundaries in patients with neurofibromatosis type 1 with 17q11.2 microdeletions. , 2001, American journal of human genetics.

[35]  M. Schwab,et al.  Patterns of Nogo mRNA and Protein Expression in the Developing and Adult Rat and After CNS Lesions , 2002, The Journal of Neuroscience.

[36]  A. Fournier,et al.  Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration , 2001, Nature.

[37]  M. Schwab,et al.  Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber outgrowth , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  V. Gallo,et al.  Cyclin-Dependent Kinase-2 Controls Oligodendrocyte Progenitor Cell Cycle Progression and Is Downregulated in Adult Oligodendrocyte Progenitors , 2002, The Journal of Neuroscience.

[39]  Y. Barde,et al.  The neurotrophin receptor p75NTR: novel functions and implications for diseases of the nervous system , 2002, Nature Neuroscience.

[40]  J. Gulcher,et al.  Expression of the Oligodendrocyte‐Myelin Glycoprotein by Neurons in the Mouse Central Nervous System , 1998, Journal of neurochemistry.

[41]  J. Roder,et al.  Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function , 1989, Neuron.

[42]  M. Schwab,et al.  Genomic structure and functional characterisation of the promoters of human and mouse nogo/rtn4. , 2003, Journal of molecular biology.

[43]  D. Horn,et al.  A common set of at least 11 functional genes is lost in the majority of NF1 patients with gross deletions. , 2000, Genomics.

[44]  J. Taylor,et al.  Identification of Nogo-66 receptor (NgR) and homologous genes in fish. , 2004, Molecular biology and evolution.

[45]  M. Tessier-Lavigne,et al.  Neuropilins as Semaphorin Receptors , 2002 .

[46]  S. Ozonoff,et al.  Cognitive impairment in neurofibromatosis type 1. , 1999, American journal of medical genetics.

[47]  W. Burke,et al.  Large de novo DNA deletion in a patient with sporadic neurofibromatosis 1, mental retardation, and dysmorphism. , 1992, Journal of medical genetics.

[48]  D. Lowy,et al.  Neurofibromin can inhibit Ras-dependent growth by a mechanism independent of its GTPase-accelerating function , 1994, Molecular and cellular biology.

[49]  D. Cooper,et al.  Gross deletions of the neurofibromatosis type 1 (NF1) gene are predominantly of maternal origin and commonly associated with a learning disability, dysmorphic features and developmental delay , 1998, Human Genetics.

[50]  A. Aguayo,et al.  Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. , 1981, Science.

[51]  T. Yamashita,et al.  The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho , 2002, The Journal of cell biology.

[52]  A. Goffinet,et al.  Reelin and brain development , 2003, Nature Reviews Neuroscience.

[53]  T. Johns,et al.  Regulation of myelin oligodendrocyte glycoprotein in different species throughout development. , 1997, Developmental neuroscience.

[54]  M. Raff,et al.  Clonal analysis of oligodendrocyte development in culture: Evidence for a developmental clock that counts cell divisions , 1986, Cell.

[55]  R. Wiggins,et al.  Structural characterization of myelin‐associated glycoprotein gene core promoter , 1997, Journal of neuroscience research.

[56]  M. Schwab,et al.  Nogo-A, a Potent Inhibitor of Neurite Outgrowth and Regeneration , 2000, Biological chemistry.

[57]  Marco Domeniconi,et al.  Myelin-Associated Glycoprotein Interacts with the Nogo66 Receptor to Inhibit Neurite Outgrowth , 2002, Neuron.

[58]  M. Schwab,et al.  Identification and Characterization of a Bovine Neurite Growth Inhibitor (bNI-220)* , 1998, The Journal of Biological Chemistry.

[59]  T. Hirata,et al.  Expression of Nogo protein by growing axons in the developing nervous system. , 2002, Brain research. Molecular brain research.

[60]  R. Prinjha,et al.  Neurobiology: Inhibitor of neurite outgrowth in humans , 2000, Nature.

[61]  Jean-Antoine Girault,et al.  Development of nodes of Ranvier , 2002, Current Opinion in Neurobiology.

[62]  A. Campagnoni Molecular Biology of Myelin Proteins from the Central Nervous System , 1988, Journal of neurochemistry.

[63]  A. Mitsudome,et al.  X-Linked mental retardation and epilepsy: pathogenetic significance of ARX mutations , 2003, Brain and Development.

[64]  M. Schwab,et al.  Reevaluation of the growth-permissive substrate properties of goldfish optic nerve myelin and myelin proteins , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  M. Schwab,et al.  Bovine CNS Myelin Contains Neurite Growth-Inhibitory Activity Associated with Chondroitin Sulfate Proteoglycans , 1999, The Journal of Neuroscience.

[66]  A. Davies,et al.  Regulation of neuronal survival and death by extracellular signals during development , 2003, The EMBO journal.

[67]  M. Filbin,et al.  Myelin-Associated Glycoprotein Inhibits Axonal Regeneration from a Variety of Neurons via Interaction with a Sialoglycoprotein , 1996, Molecular and Cellular Neuroscience.

[68]  S. B. Kater,et al.  Myelin‐associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse , 1996, Journal of neuroscience research.

[69]  T. Yamashita,et al.  The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI , 2003, Nature Neuroscience.

[70]  Axel Benner,et al.  Further characterization of the autism susceptibility locus AUTS1 on chromosome 7q. , 2001, Human molecular genetics.

[71]  M. L. Le Beau,et al.  Structure and chromosomal localization of the gene for the oligodendrocyte-myelin glycoprotein , 1990, The Journal of cell biology.

[72]  F. Collins,et al.  Neurofibromatosis Type 1: Beyond Positional Cloning , 1993 .

[73]  P. O'Connell,et al.  Identification and characterization of transcripts from the neurofibromatosis 1 region: the sequence and genomic structure of EVI2 and mapping of other transcripts. , 1990, Genomics.

[74]  M. Schachner,et al.  Multiple functions of the myelin‐associated glycoprotein MAG (siglec‐4a) in formation and maintenance of myelin , 2000, Glia.

[75]  Fumio Nakamura,et al.  Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein , 2000, Nature.

[76]  P. Caroni,et al.  Central nervous system regeneration: oligodendrocytes and myelin as non-permissive substrates for neurite growth. , 1988, Progress in brain research.

[77]  P. Vourc'h,et al.  The oligodendrocyte-myelin glycoprotein gene is highly expressed during the late stages of myelination in the rat central nervous system. , 2003, Brain research. Developmental brain research.

[78]  Y. Lim,et al.  Growth Factors Stimulate Tyrosine Dephosphorylation of p75 and Its Dissociation from the SH2 Domain of Grb2* , 1997, The Journal of Biological Chemistry.

[79]  M. Hemling,et al.  Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM M-proteins in patients with neuropathy. , 1987, The Journal of biological chemistry.

[80]  M. Tessier-Lavigne,et al.  Neuropilins as Semaphorin receptors: in vivo functions in neuronal cell migration and axon guidance. , 2002, Advances in experimental medicine and biology.

[81]  A. Espinosa-Jeffrey,et al.  Tumor necrosis factor modulates transcription of myelin basic protein gene through nuclear factor kappa B in a human oligodendroglioma cell line , 2002, International Journal of Developmental Neuroscience.

[82]  M. Filbin,et al.  A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration , 1994, Neuron.

[83]  A. Kajava Structural diversity of leucine-rich repeat proteins. , 1998, Journal of molecular biology.

[84]  B. Allwardt,et al.  The oligodendrocyte-myelin glycoprotein of mouse: primary structure and gene structure. , 1993, Genomics.

[85]  S. Strittmatter,et al.  Axon Regeneration in Young Adult Mice Lacking Nogo-A/B , 2003, Neuron.

[86]  B. Dickson Molecular Mechanisms of Axon Guidance , 2002, Science.

[87]  M. Schachner,et al.  Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS , 1995, Neuron.

[88]  T. Manabe,et al.  Mice Deficient in Nervous System-specific Carbohydrate Epitope HNK-1 Exhibit Impaired Synaptic Plasticity and Spatial Learning* , 2002, The Journal of Biological Chemistry.

[89]  Zhigang He,et al.  Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth , 2002, Nature.

[90]  A. Fournier,et al.  Truncated Soluble Nogo Receptor Binds Nogo-66 and Blocks Inhibition of Axon Growth by Myelin , 2002, The Journal of Neuroscience.

[91]  C. Barthélémy,et al.  Molecular analysis of the oligodendrocyte myelin glycoprotein gene in autistic disorder , 2003, Neuroscience Letters.

[92]  Martin E. Schwab,et al.  Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1 , 2000, Nature.

[93]  A. Püschel The function of neuropilin/plexin complexes. , 2002, Advances in experimental medicine and biology.

[94]  C. Barthélémy,et al.  Association study of the NF1 gene and autistic disorder. , 1999, American journal of medical genetics.

[95]  S. Gupta Deficiency of monoclonal antibody-defined NK Cells (HNK-1+) in primary immunodeficiency disorders. , 1982, Immunology Letters.

[96]  M. Yutsudo,et al.  Link of a new type of apoptosis-inducing gene ASY/Nogo-B to human cancer , 2001, Oncogene.

[97]  J. Gulcher,et al.  The oligodendrocyte-myelin glycoprotein belongs to a distinct family of proteins and contains the HNK-1 carbohydrate , 1990, The Journal of cell biology.

[98]  T. Yamashita,et al.  Neurotrophin Binding to the p75 Receptor Modulates Rho Activity and Axonal Outgrowth , 1999, Neuron.

[99]  L. Spiryda Myelin protein zero and membrane adhesion , 1998, Journal of neuroscience research.

[100]  M. Yoshida,et al.  Parallel Evolution and Coexpression of the Proteolipid Proteins and Protein Zero in Vertebrate Myelin , 1996, Neuron.

[101]  A. Fournier,et al.  Myelin-Associated Glycoprotein as a Functional Ligand for the Nogo-66 Receptor , 2002, Science.

[102]  R. Quarles Myelin sheaths: glycoproteins involved in their formation, maintenance and degeneration , 2002, Cellular and Molecular Life Sciences CMLS.

[103]  M. Raff,et al.  Two molecularly distinct intracellular pathways to oligodendrocyte differentiation: role of a p53 family protein , 2001, The EMBO journal.

[104]  G. Elgar,et al.  Genomic characterization of the Neurofibromatosis Type 1 gene of Fugu rubripes. , 1998, Gene.

[105]  F. McCormick,et al.  Ras signaling and NF1. , 1995, Current opinion in genetics & development.

[106]  R. Tenconi,et al.  NF1 microdeletion syndrome: refined FISH characterization of sporadic and familial deletions with locus-specific probes. , 2000, American journal of human genetics.

[107]  Y. Ushio,et al.  Neuronal cell migration for the developmental formation of the mammalian striatum , 2003, Brain Research Reviews.

[108]  P. O'Connell,et al.  The gene encoding the oligodendrocyte-myelin glycoprotein is embedded within the neurofibromatosis type 1 gene , 1991, Molecular and cellular biology.

[109]  M. Wullimann,et al.  Readiness of Zebrafish Brain Neurons to Regenerate a Spinal Axon Correlates with Differential Expression of Specific Cell Recognition Molecules , 1998, The Journal of Neuroscience.

[110]  L. Mckerracher,et al.  Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth , 1994, Neuron.

[111]  P. Caroni,et al.  Antibody against myelin associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter , 1988, Neuron.

[112]  P. Vourc'h,et al.  Oligodendrocyte myelin glycoprotein growth inhibition function requires its conserved leucine‐rich repeat domain, not its glycosylphosphatidyl‐inositol anchor , 2003, Journal of neurochemistry.

[113]  R. Segal,et al.  p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp , 2002, Nature.

[114]  F. Cambi,et al.  Down-Regulation of the Retinoblastoma Protein (Rb) Is Associated with Rat Oligodendrocyte Differentiation , 2002, Molecular and Cellular Neuroscience.