Online citations, reference lists, and bibliographies.
← Back to Search

The ErbB2 Gene Is Required For The Development Of Terminally Differentiated Spinal Cord Oligodendrocytes

Song-Kyu Park, R. Miller, I. Krane, T. Vartanian
Published 2001 · Biology, Medicine

Save to my Library
Download PDF
Analyze on Scholarcy
Share
Development of oligodendrocytes and the generation of myelin internodes within the spinal cord depends on regional signals derived from the notochord and axonally derived signals. Neuregulin 1 (NRG)-1, localized in the floor plate as well as in motor and sensory neurons, is necessary for normal oligodendrocyte development. Oligodendrocytes respond to NRGs by activating members of the erbB receptor tyrosine kinase family. Here, we show that erbB2 is not necessary for the early stages of oligodendrocyte precursor development, but is essential for proligodendroblasts to differentiate into galactosylcerebroside-positive (GalC+) oligodendrocytes. In the presence of erbB2, oligodendrocyte development is normal. In the absence of erbB2 (erbB2−/−), however, oligodendrocyte development is halted at the proligodendroblast stage with a >10-fold reduction in the number of GalC+ oligodendrocytes. ErbB2 appears to function in the transition of proligodendroblast to oligodendrocyte by transducing a terminal differentiation signal, since there is no evidence of increased oligodendrocyte death in the absence of erbB2. Furthermore, known survival signals for oligodendrocytes increase oligodendrocyte numbers in the presence of erbB2, but fail to do so in the absence of erbB2. Of the erbB2−/− oligodendrocytes that do differentiate, all fail to ensheath neurites. These data suggest that erbB2 is required for the terminal differentiation of oligodendrocytes and for development of myelin.
This paper references
10.1073/PNAS.75.5.2521
Myelin basic protein demonstrated immunocytochemically in oligodendroglia prior to myelin sheath formation.
N. Sternberger (1978)
10.1523/JNEUROSCI.18-24-10457.1998
The Chemokine Growth-Regulated Oncogene-α Promotes Spinal Cord Oligodendrocyte Precursor Proliferation
S. Robinson (1998)
10.1038/35000219
Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1
M. S. Chen (2000)
10.1523/JNEUROSCI.17-23-09122.1997
Transplanted Oligodendrocyte Progenitor Cells Expressing a Dominant-Negative FGF Receptor Transgene Fail to Migrate In Vivo
D. Osterhout (1997)
Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro.
M. Mayer (1994)
10.1073/PNAS.91.20.9387
Brain neurons and glial cells express Neu differentiation factor/heregulin: a survival factor for astrocytes.
R. Pinkas-Kramarski (1994)
10.1111/j.1749-6632.1991.tb15646.x
Astrocytes and O‐2A Progenitors Migrate Toward Distinct Molecules in a Microchemotaxis Chamber
R. Armstrong (1991)
10.1523/JNEUROSCI.15-09-06124.1995
ARIA is concentrated in nerve terminals at neuromuscular junctions and at other synapses
A. Sandrock (1995)
10.1159/000111414
Progressive remodeling of the oligodendrocyte process arbor during myelinogenesis.
R. Hardy (1996)
10.1073/PNAS.91.24.11626
A role for the acetylcholine receptor-inducing protein ARIA in oligodendrocyte development.
T. Vartanian (1994)
10.1038/39593
Severe neuropathies in mice with targeted mutations in the ErbB3 receptor
D. Riethmacher (1997)
Difference in the morphology of Wallerian degeneration in the central nervous system (CNS) and peripheral nervous system (PNS) and its effect on regeneration.
H. Wisniewski (1983)
10.1097/00005072-198140010-00006
Proliferation of neuroglial cell lines in the degenerating optic nerve of young rats. A radioautographic study.
A. Privat (1981)
10.1016/S0896-6273(00)80898-3
Identification of a Novel Family of Oligodendrocyte Lineage-Specific Basic Helix–Loop–Helix Transcription Factors
Q. Zhou (2000)
10.1074/JBC.C901015199
Ligand Discrimination in Signaling through an ErbB4 Receptor Homodimer*
C. Sweeney (2000)
10.1006/mcne.1998.0733
GGF/Neuregulin Induces a Phenotypic Reversion of Oligodendrocytes
P. Canoll (1999)
10.1128/MCB.18.10.6090
ErbB Tyrosine Kinases and the Two Neuregulin Families Constitute a Ligand-Receptor Network
R. Pinkas-Kramarski (1998)
10.1006/DBIO.1996.0142
Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog.
N. Pringle (1996)
Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin.
M. Sliwkowski (1994)
10.1523/JNEUROSCI.16-19-06107.1996
Axonal Interactions Regulate Schwann Cell Apoptosis in Developing Peripheral Nerve: Neuregulin Receptors and the Role of Neuregulins
J. Grinspan (1996)
10.1523/JNEUROSCI.18-12-04627.1998
Purification and Characterization of Adult Oligodendrocyte Precursor Cells from the Rat Optic Nerve
J. Shi (1998)
10.1016/S0896-6273(00)00087-8
Evidence that Axon-Derived Neuregulin Promotes Oligodendrocyte Survival in the Developing Rat Optic Nerve
P. Fernández (2000)
10.1002/JNR.490340102
Differential myelinogenic capacity of specific developmental stages of the oligodendrocyte lineage upon transplantation into hypomyelinating hosts
A. Warrington (1993)
10.1016/0012-1606(81)90477-2
Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system.
I. Sommer (1981)
10.1002/j.1460-2075.1996.tb00603.x
Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions.
R. Pinkas-Kramarski (1996)
10.1016/0022-510X(92)90160-M
Delayed wallerian degeneration in the central nervous system of Ola mice: an ultrastructural study
S. Ludwin (1992)
10.1038/35052073
Untangling the ErbB signalling network
Y. Yarden (2001)
ErbB2 is essential in oligodendrocyte development | Park et al
(1257)
Difference in the morphology of Wallerian degeneration in the central nervous system (CNS) and peripheral nervous system (PNS) and its effect on regeneration.
Wísniewski Hm (1983)
10.1083/JCB.146.6.1365
Rat Optic Nerve Oligodendrocytes Develop in the Absence of Viable Retinal Ganglion Cell Axons
H. Ueda (1999)
10.1387/IJDB.9654007
Cell number control and timing in animal development: the oligodendrocyte cell lineage.
M. Raff (1998)
10.1002/(SICI)1098-1136(199903)26:1<22::AID-GLIA3>3.0.CO;2-M
Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration
P. Simpson (1999)
10.1038/379174A0
Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor
J. Trachtenberg (1996)
10.1016/0736-5748(88)90005-6
Experimental modifications of postnatal differentiation and fate of glial cells related to axo-glial relationships
J. Valat (1988)
10.1016/0896-6273(95)90244-9
Differential expression of ARIA isoforms in the rat brain
G. Corfas (1995)
10.1038/303390A0
A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium
M. Raff (1983)
10.1523/JNEUROSCI.11-08-02477.1991
Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord
B. C. Warf (1991)
10.1083/JCB.147.1.77
Erbb4 Signaling in the Mammary Gland Is Required for Lobuloalveolar Development and Stat5 Activation during Lactation
F. E. Jones (1999)
Early development and dispersal of oligodendrocyte precursors in the embryonic chick spinal cord.
K. Ono (1995)
10.1523/JNEUROSCI.16-06-02064.1996
Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons
J. Burne (1996)
10.1093/emboj/16.7.1647
ErbB‐2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling
D. Graus-Porta (1997)
10.1007/BF02284808
Glial cells in transected optic nerves of immature rats. I. An analysis of individual cells by intracellular dye-injection
A. Butt (1996)
10.1046/J.1529-8027.2000.005002119.X
A Dual Role of erbB2 in Myelination and in Expansion of the Schwann Cell Precursor Pool
A. Garratt (2000)
10.1016/0896-6273(90)90216-3
Two proliferative stages of the oligodendrocyte lineage (A2B5+O4- and O4+GaIC-) under different mitogenic control
A. Gard (1990)
Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell.
M. Noble (1988)
10.1161/01.RES.84.12.1380
Neuregulin signaling in the heart. Dynamic targeting of erbB4 to caveolar microdomains in cardiac myocytes.
Y. Zhao (1999)
10.1007/BF02284809
Glial cells in transected optic nerves of immature rats. II. An immunohistochemical study
A. Butt (1996)
10.1038/378386A0
Multiple essential functions of neuregulin in development
Dirk Meyer (1995)
10.1038/274812A0
Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture
M. Raff (1978)
10.1073/PNAS.87.16.6368
Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells.
O. Bögler (1990)
10.1038/sj.onc.1201466
Differential expression of NDF/neuregulin receptors ErbB-3 and ErbB-4 and involvement in inhibition of neuronal differentiation
R. Pinkas-Kramarski (1997)
10.1038/333562A0
Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture
M. Raff (1988)
10.1002/CNE.901760204
Neuroglial reactions secondary to wallerian degeneration in the optic nerve of the postnatal rat: Ultrastructural and quantitative study
J. Fulcrand (1977)
10.1016/S0896-6273(00)81176-9
Regulation of Neuregulin Signaling by PSD-95 Interacting with ErbB4 at CNS Synapses
Y. Z. Huang (2000)
10.1038/361258a0
Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons
B. Barres (1993)
10.1083/JCB.109.6.3411
PDGF and intracellular signaling in the timing of oligodendrocyte differentiation
I. Hart (1989)
10.1038/328155A0
Evidence for migration of oligodendrocyte–type-2 astrocyte progenitor cells into the developing rat optic nerve
R. K. Small (1987)
10.1016/s0021-9258(17)46636-1
Characterization of a breast cancer cell differentiation factor that specifically activates the HER4/p180erbB4 receptor.
J. M. Culouscou (1993)
10.1002/(SICI)1521-1878(199801)20:1<41::AID-BIES7>3.0.CO;2-V
Specificity within the EGF family/ErbB receptor family signaling network
D. Riese (1998)
10.1016/S0896-6273(00)80779-5
Rescue of the Cardiac Defect in ErbB2 Mutant Mice Reveals Essential Roles of ErbB2 in Peripheral Nervous System Development
J. Morris (1999)
10.1002/(SICI)1098-1136(20000115)29:2<104::AID-GLIA2>3.0.CO;2-2
Role of neuregulins in glial cell development
K. Adlkofer (2000)
ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice.
S. Erickson (1997)
10.1146/ANNUREV.NEURO.20.1.429
ARIA: a neuromuscular junction neuregulin.
G. Fischbach (1997)
10.1083/JCB.137.1.211
Axonal Neuregulin Signals Cells of the Oligodendrocyte Lineage through Activation of HER4 and Schwann Cells through HER2 and HER3
T. Vartanian (1997)
10.1016/0092-8674(94)90150-3
Glial growth factor restricts mammalian neural crest stem cells to a glial fate
N. Shah (1994)
10.1038/373158A0
Neuregulins are concentrated at nerve-muscle synapses and activate ACh–receptor gene expression
S. Jo (1995)
10.1016/0896-6273(95)90147-7
Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat schwann cell precursors
Z. Dong (1995)
10.1006/mcne.1998.0676
The Neuregulin Precursor proARIA Is Processed to ARIA after Expression on the Cell Surface by a Protein Kinase C-Enhanced Mechanism
J. Loeb (1998)
10.1038/30012
Requirement of ErbB2 for signalling by interleukin-6 in prostate carcinoma cells
Y. Qiu (1998)
10.1073/PNAS.92.5.1431
Axon-induced mitogenesis of human Schwann cells involves heregulin and p185erbB2.
T. Morrissey (1995)
10.1016/S0896-6273(00)80873-9
Cysteine-Rich Domain Isoforms of the Neuregulin-1 Gene Are Required for Maintenance of Peripheral Synapses
Deon Wolpowitz (2000)
10.1002/(SICI)1098-1136(20000115)29:2<175::AID-GLIA11>3.0.CO;2-F
NI‐35/250/nogo‐a: A neurite growth inhibitor restricting structural plasticity and regeneration of nerve fibers in the adult vertebrate CNS
C. Bandtlow (2000)
10.1126/SCIENCE.276.5312.599
Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo.
A. Sandrock (1997)
10.1016/0092-8674(94)90564-9
A neu acquaintance for ErbB3 and ErbB4: A role for receptor heterodimerization in growth signaling
K. Carraway (1994)
10.1016/0306-4522(91)90435-Q
Delayed response to denervation in muscles of C57BL/Ola mice
M. Brown (1991)
10.1073/PNAS.90.14.6820
Even in culture, oligodendrocytes myelinate solely axons.
C. Lubetzki (1993)
10.1016/S0896-6273(00)80897-1
Sonic Hedgehog–Regulated Oligodendrocyte Lineage Genes Encoding bHLH Proteins in the Mammalian Central Nervous System
Q.Richard Lu (2000)
10.1083/JCB.134.3.757
Induction of neuronal apoptosis by camptothecin, an inhibitor of DNA topoisomerase-I: evidence for cell cycle-independent toxicity
E. Morris (1996)
10.1007/BF01148596
Effects of neonatal transection on glial cell development in the rat optic nerve: evidence that the oligodendrocyte-type 2 astrocyte cell lineage depends on axons for its survival
S. David (1984)
10.1038/366473A0
Heregulin induces tyrosine phosphorylation of HER4/p180erbB4
G. Plowman (1993)
10.1002/NEU.480230912
Cell death in the oligodendrocyte lineage.
B. Barres (1992)
ErbB2 is essential in oligodendrocyte development | Park et al. 1257
Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral midline region in the embryonic rat spinal cord.
E. Noll (1993)
10.1523/JNEUROSCI.20-20-07622.2000
Akt-Mediated Survival of Oligodendrocytes Induced by Neuregulins
A. Flores (2000)
10.1128/MCB.15.10.5770
The cellular response to neuregulins is governed by complex interactions of the erbB receptor family.
D. Riese (1995)
10.1002/JNR.490370208
Distribution and differentiation of A2B5+ glial precursors in the developing rat spinal cord
J. Fok-Seang (1994)
10.1073/PNAS.95.12.6809
ErbB2 expression increases the spectrum and potency of ligand-mediated signal transduction through ErbB4.
L. Wang (1998)
10.1038/344871A0
Role of myelin Po protein as a homophilic adhesion molecule
M. Filbin (1990)
10.1073/PNAS.96.2.731
Failure of spinal cord oligodendrocyte development in mice lacking neuregulin.
T. Vartanian (1999)
10.1016/S0896-6273(00)80515-2
Notch Receptor Activation Inhibits Oligodendrocyte Differentiation
S. Wang (1998)
10.1101/GAD.12.19.3074
Synapse-specific and neuregulin-induced transcription require an ets site that binds GABPalpha/GABPbeta.
L. Fromm (1998)
10.1111/j.1460-9568.1995.tb01159.x
Persistence of Neuromuscular Junctions after Axotomy in Mice with Slow Wallerian Degeneration (C57BL/Wlds)
R. Ribchester (1995)
10.1016/0896-6273(94)90450-2
Embryonic expression of myelin genes: Evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube
Wei-ping Yu (1994)
Neuregulin signaling in the heart
Y. Y. Zhao (1999)
10.1016/0896-6273(90)90215-2
FGF modulates the PDGF-driven pathway of oligodendrocyte development
R. McKinnon (1990)
Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors.
D. M. Orentas (1999)
10.1016/S0896-6273(00)80155-5
GGF/Neuregulin Is a Neuronal Signal That Promotes the Proliferation and Survival and Inhibits the Differentiation of Oligodendrocyte Progenitors
P. Canoll (1996)
10.1523/JNEUROSCI.15-02-01012.1995
Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression
S. Timsit (1995)
10.1038/35000226
Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein
T. Grandpre (2000)
10.1016/0959-4388(95)80065-4
Neuregulins and their receptors
K. Carraway (1995)
10.1016/0092-8674(92)90531-G
Cell death and control of cell survival in the oligodendrocyte lineage
B. Barres (1992)
10.1083/JCB.147.6.1123
Axonal Control of Oligodendrocyte Development
B. Barres (1999)
10.1097/00000478-198912000-00004
Immunoproliferative small-intestinal disease. An immunohistochemical study.
P. Isaacson (1989)
10.1002/(SICI)1097-4547(19971201)50:5<755::AID-JNR12>3.0.CO;2-0
Effect of neu differentiation factor isoforms on neonatal oligodendrocyte function
T. Raabe (1997)
10.1038/378394A0
Requirement for neuregulin receptor erbB2 in neural and cardiac development
Kuo-Fen Lee (1995)
10.1523/JNEUROSCI.09-07-02327.1989
Macrophage function during Wallerian degeneration of rat optic nerve: clearance of degenerating myelin and Ia expression
G. Stoll (1989)



This paper is referenced by
10.1101/GAD.215802
Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10.
C. Stolt (2002)
10.3389/fphar.2016.00327
Understanding the Impact of ErbB Activating Events and Signal Transduction on Antigen Processing and Presentation: MHC Expression as a Model
A. Kersh (2016)
10.1016/j.ijdevneu.2008.05.003
A correlative light and electron microscopic study of postnatal myelination in the murine corpus callosum
A. Vincze (2008)
Role of miRNAs in Oligodendrocyte Development
H. Budde (2010)
10.1007/978-3-319-04843-7_9
HER-2 involvement in osteosarcoma.
J. Gill (2014)
10.1016/j.mcn.2014.02.006
LINGO-1 regulates oligodendrocyte differentiation by inhibiting ErbB2 translocation and activation in lipid rafts
X. Lee (2014)
Damage and Repair in Experimental Cortical Demyelination
Enrique Garea Rodríguez (2010)
10.2183/pjab.87.415
Increased numbers of oligodendrocyte lineage cells in the optic nerves of cerebroside sulfotransferase knockout mice
Hitoshi Kajigaya (2011)
10.1002/glia.10284
Paranodal transverse bands are required for maintenance but not initiation of Nav1.6 sodium channel clustering in CNS optic nerve axons
M. Rasband (2003)
10.1007/s00795-010-0524-1
Detailed DARPP-32 expression profiles in postmortem brains from patients with schizophrenia: an immunohistochemical study
Y. Kunii (2010)
FUNCTIONAL ANALYSES OF THE CHEMOKINE RECEPTOR CXCR2 IN THE NORMAL AND DEMYELINATED ADULT CENTRAL NERVOUS SYSTEM
D. Padovani-Claudio (2006)
10.1146/annurev-med-050715-104400
Mechanisms and Medicines for Remyelination.
M. Bothwell (2017)
10.1007/s00018-008-7440-8
The epidermal growth factor receptor family: Biology driving targeted therapeutics
M. Wieduwilt (2008)
10.1016/J.BRAINRESREV.2005.11.006
Neuregulins: Versatile growth and differentiation factors in nervous system development and human disease
R. M. Esper (2006)
10.1111/ejn.12268
Dysregulation of the neuregulin‐1–ErbB network modulates endogenous oligodendrocyte differentiation and preservation after spinal cord injury
M. Gauthier (2013)
10.1016/j.neuron.2008.06.028
Neuregulin-1/ErbB Signaling Serves Distinct Functions in Myelination of the Peripheral and Central Nervous System
Bastian G Brinkmann (2008)
10.1111/j.1460-9568.2005.04225.x
Expression of zonula occludens‐1 (ZO‐1) and the transcription factor ZO‐1‐associated nucleic acid‐binding protein (ZONAB)–MsY3 in glial cells and colocalization at oligodendrocyte and astrocyte gap junctions in mouse brain
Mihai C. Penes (2005)
10.1002/glia.20042
CD44 overexpression by oligodendrocytes: A novel mouse model of inflammation‐independent demyelination and dysmyelination
Therese M F Tuohy (2004)
Role of ErbB2 and ErbB4 in Cancer Growth, Prognosis and as Targets for Immunotherapy
M. Hollmén (2010)
10.1002/glia.10275
erbB3 is dispensable for oligodendrocyte development in vitro and in vivo
Johannes Schmucker (2003)
10.1016/J.GENE.2005.10.018
Epidermal growth factor receptor (EGFR) signaling in cancer.
N. Normanno (2006)
Role of integrins and neuregulins in axoglial interaction in central nervous system myelination
Ana Cristina Nunes Lopes da Fonseca (2015)
10.1242/jcs.02799
Characterization of a neural-specific splicing form of the human neuregulin 3 gene involved in oligodendrocyte survival
Christelle Carteron (2006)
10.1002/glia.23306
Vitamin C promotes oligodendrocytes generation and remyelination
Yu’e Guo (2018)
10.1159/000111119
Neuregulin-1: A Potential Endogenous Protector in Perinatal Brain White Matter Damage
O. Dammann (2007)
10.1016/S0014-4827(02)00102-7
Neuregulins: functions, forms, and signaling strategies.
D. Falls (2003)
10.1016/j.conb.2006.08.008
Axonal regulation of myelination by neuregulin 1
K. Nave (2006)
10.1523/JNEUROSCI.23-03-00883.2003
Fibroblast Growth Factor Receptor 3 Signaling Regulates the Onset of Oligodendrocyte Terminal Differentiation
L. Oh (2003)
10.1001/jama.1950.02920160084027
Multiple sclerosis and demyelinating diseases
M. Freedman (2006)
KATRI KÖNINKI HER-2 Positive Breast Cancer
Katri Köninki (2010)
10.1007/978-1-4419-7104-3_16
Biology of Demyelinating Diseases
D. Pham-Dinh (2011)
10.1007/s00401-009-0601-5
Oligodendrocytes: biology and pathology
M. Bradl (2009)
See more
Semantic Scholar Logo Some data provided by SemanticScholar