Home LiteratureArticle Details
PMID: 9852583 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The chemokine growth-regulated oncogene-alpha promotes spinal cord oligodendrocyte precursor proliferation.

Robinson S, Tani M, Strieter RM, Ransohoff RM, Miller RH

Abstract

Chemokines, (chemotactic cytokines) are a family of regulatory molecules involved in modulating inflammatory responses. Here we demonstrate that the chemokine growth-regulated oncogene-alpha (GRO-alpha) is a potent promoter of oligodendrocyte precursor proliferation. The proliferative response of immature spinal cord oligodendrocyte precursors to their major mitogen, platelet derived growth factor (PDGF), is dramatically enhanced by GRO-alpha present in spinal cord conditioned medium. One source of GRO-alpha is a subset of spinal cord astrocytes. Cultures of astrocytes contain GRO-alpha mRNA and protein and secrete biologically active concentrations of GRO-alpha. In postnatal spinal cord white matter the location of GRO-alpha-immunoreactive cells is developmentally regulated: GRO-alpha+ cells first appear in ventral and later in dorsal spinal cord white matter. These results suggest that localized proliferation of oligodendrocytes is mediated by synergy between PDGF and GRO-alpha.

MeSH Terms
Animals Astrocytes/chemistry,metabolism Cell Division/drug effects Cells, Cultured Chemokine CXCL1 Chemokines, CXC/metabolism,pharmacology Chemotactic Factors/metabolism,pharmacology Culture Media, Conditioned/pharmacology Dose-Response Relationship, Drug Drug Synergism Gangliosides/analysis Gene Expression Regulation, Developmental Growth Substances/metabolism,pharmacology Intercellular Signaling Peptides and Proteins Oligodendroglia/cytology,drug effects Platelet-Derived Growth Factor/pharmacology RNA, Messenger/analysis Rats Spinal Cord/cytology Stem Cells/cytology,drug effects
Chemicals
Chemokine CXCL1 Chemokines, CXC Chemotactic Factors Culture Media, Conditioned Cxcl1 protein, rat Gangliosides Growth Substances Intercellular Signaling Peptides and Proteins Platelet-Derived Growth Factor RNA, Messenger ganglioside A2B5
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Robinson S
Department of Neurosurgery, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106, USA.
Tani M
Strieter R M
Ransohoff R M
Miller R H
References (51)
51 references, click to expand
  1. Differential myelinogenic capacity of specific developmental stages of the oligodendrocyte lineage upon transplantation into hypomyelinating hosts.
    J Neurosci Res. 1993 Jan;34(1):1-13 PMID: 7678656
  2. Recombinant human adenovirus with rat MIP-2 gene insertion causes prolonged PMN recruitment to the murine brain.
    Eur J Neurosci. 1996 Sep;8(9):1803-11 PMID: 8921271
  3. Neutrophil infiltration, glial reaction, and neurological disease in transgenic mice expressing the chemokine N51/KC in oligodendrocytes.
    J Clin Invest. 1996 Jul 15;98(2):529-39 PMID: 8755666
  4. Human chemokines: an update.
    Annu Rev Immunol. 1997;15:675-705 PMID: 9143704
  5. Separation of melanoma growth stimulatory activity and human type-alpha transforming growth factor.
    Methods Enzymol. 1987;146:112-26 PMID: 3479673
  6. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6368-72 PMID: 2201028
  7. Radially oriented astrocytes in the normal adult rat spinal cord.
    Brain Res. 1987 Feb 17;403(2):385-8 PMID: 2435373
  8. IL-1 and TNF-alpha induction of IL-8 and monocyte chemotactic and activating factor (MCAF) mRNA expression in a human astrocytoma cell line.
    Immunology. 1991 Sep;74(1):60-7 PMID: 1937574
  9. Interleukin-8 is produced in neoplastic and infectious diseases of the human central nervous system.
    Cancer Res. 1992 Aug 15;52(16):4297-305 PMID: 1643627
  10. Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis.
    Am J Pathol. 1997 Feb;150(2):617-30 PMID: 9033275
  11. Multiple sclerosis. Oligodendrocyte survival and proliferation in an active established lesion.
    Lab Invest. 1981 Dec;45(6):534-46 PMID: 7321526
  12. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium.
    Nature. 1983 Jun 2-8;303(5916):390-6 PMID: 6304520
  13. Neuroglial population in the spinal white matter of neonatal and early postnatal rats: an autoradiographic study of numbers of neuroglia and changes in their proliferative activity.
    Anat Rec. 1971 Oct;171(2):283-91 PMID: 5113431
  14. Mouse astrocytes respond to the chemokines MCP-1 and KC, but reverse transcriptase-polymerase chain reaction does not detect mRNA for the KC or new MCP-1 receptor.
    J Neurosci Res. 1996 Aug 15;45(4):382-91 PMID: 8872898
  15. Chemokines and leukocyte traffic.
    Nature. 1998 Apr 9;392(6676):565-8 PMID: 9560152
  16. The platelet-derived growth factor-inducible KC gene encodes a secretory protein related to platelet alpha-granule proteins.
    J Biol Chem. 1989 Mar 5;264(7):4133-7 PMID: 2917992
  17. Spinal cord oligodendrocytes develop from a limited number of migratory highly proliferative precursors.
    J Neurosci Res. 1997 Oct 15;50(2):157-68 PMID: 9373026
  18. PDGF A chain homodimers drive proliferation of bipotential (O-2A) glial progenitor cells in the developing rat optic nerve.
    EMBO J. 1989 Apr;8(4):1049-56 PMID: 2545439
  19. Environmental enhancement of growth factor-mediated oligodendrocyte precursor proliferation.
    Mol Cell Neurosci. 1996;8(1):38-52 PMID: 8923454
  20. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan.
    J Neurosci. 1987 Sep;7(9):2737-44 PMID: 3305800
  21. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell.
    Nature. 1988 Jun 9;333(6173):560-2 PMID: 3287176
  22. Trophic effects of interleukin-4, -7 and -8 on hippocampal neuronal cultures: potential involvement of glial-derived factors.
    Brain Res. 1993 Jan 8;600(1):49-55 PMID: 8422590
  23. Distribution of phosphoprotein p19 in rat brain during ontogeny: stage-specific expression in neurons and glia.
    Brain Res Dev Brain Res. 1991 Jun 21;60(2):205-18 PMID: 1893566
  24. PDGF A-chain gene is expressed by mammalian neurons during development and in maturity.
    Cell. 1991 Jan 11;64(1):209-16 PMID: 1986867
  25. 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 Feb;117(2):525-33 PMID: 8330523
  26. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system.
    Cell. 1988 Apr 22;53(2):309-19 PMID: 2834067
  27. Localization of 9E3/CEF-4 in avian tissues: expression is absent in Rous sarcoma virus-induced tumors but is stimulated by injury.
    J Cell Biol. 1990 Mar;110(3):581-95 PMID: 2155240
  28. Comparative analysis of the human macrophage inflammatory protein family of cytokines (chemokines) on proliferation of human myeloid progenitor cells. Interacting effects involving suppression, synergistic suppression, and blocking of suppression.
    J Immunol. 1993 Apr 15;150(8 Pt 1):3448-58 PMID: 7682242
  29. Identification of three related human GRO genes encoding cytokine functions.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7732-6 PMID: 2217207
  30. Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral midline region in the embryonic rat spinal cord.
    Development. 1993 Jun;118(2):563-73 PMID: 8223279
  31. Glial cell mitogens bFGF and PDGF differentially regulate development of O4+GalC- oligodendrocyte progenitors.
    Dev Biol. 1993 Oct;159(2):618-30 PMID: 8405684
  32. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord.
    J Neurosci. 1991 Aug;11(8):2477-88 PMID: 1869925
  33. Region-specific appearance of myelin constituents in the developing rat spinal cord.
    J Neurocytol. 1989 Apr;18(2):161-9 PMID: 2471819
  34. Multiple sclerosis: remyelination of nascent lesions.
    Ann Neurol. 1993 Feb;33(2):137-51 PMID: 8434875
  35. Constitutive overexpression of a growth-regulated gene in transformed Chinese hamster and human cells.
    Proc Natl Acad Sci U S A. 1987 Oct;84(20):7188-92 PMID: 2890161
  36. Chemokines.
    Blood. 1997 Aug 1;90(3):909-28 PMID: 9242519
  37. Molecular cloning of gene sequences regulated by platelet-derived growth factor.
    Cell. 1983 Jul;33(3):939-47 PMID: 6872001
  38. An NF-kappa B-like transcription factor mediates IL-1/TNF-alpha induction of gro in human fibroblasts.
    J Immunol. 1991 Jul 15;147(2):520-7 PMID: 1906501
  39. C-X-C and C-C chemokines are expressed in the cerebrospinal fluid in bacterial meningitis and mediate chemotactic activity on peripheral blood-derived polymorphonuclear and mononuclear cells in vitro.
    J Immunol. 1997 Feb 15;158(4):1956-64 PMID: 9029138
  40. Melanoma growth stimulatory activity: isolation from human melanoma tumors and characterization of tissue distribution.
    J Cell Biochem. 1988 Feb;36(2):185-98 PMID: 3356754
  41. Molecular characterization and chromosomal mapping of melanoma growth stimulatory activity, a growth factor structurally related to beta-thromboglobulin.
    EMBO J. 1988 Jul;7(7):2025-33 PMID: 2970963
  42. Oligodendrocyte population dynamics and the role of PDGF in vivo.
    Neuron. 1998 May;20(5):869-82 PMID: 9620692
  43. Channeling of developing rat corticospinal tract axons by myelin-associated neurite growth inhibitors.
    J Neurosci. 1991 Mar;11(3):709-21 PMID: 1705967
  44. Distribution and differentiation of A2B5+ glial precursors in the developing rat spinal cord.
    J Neurosci Res. 1994 Feb 1;37(2):219-35 PMID: 8151730
  45. Two proliferative stages of the oligodendrocyte lineage (A2B5+O4- and O4+GalC-) under different mitogenic control.
    Neuron. 1990 Nov;5(5):615-25 PMID: 2223090
  46. FGF modulates the PDGF-driven pathway of oligodendrocyte development.
    Neuron. 1990 Nov;5(5):603-14 PMID: 2171589
  47. Induction of oligodendrocyte proliferation and remyelination after chronic demyelination. Relevance to multiple sclerosis.
    Lab Invest. 1988 Oct;59(4):467-76 PMID: 2459499
  48. The role of CXC chemokines as regulators of angiogenesis.
    Shock. 1995 Sep;4(3):155-60 PMID: 8574748
  49. Cytokine-induced neutrophil chemoattractant mRNA expressed in cerebral ischemia.
    Neurosci Lett. 1993 Dec 24;164(1-2):125-8 PMID: 8152586
  50. The CXC chemokines, IL-8 and IP-10, regulate angiogenic activity in idiopathic pulmonary fibrosis.
    J Immunol. 1997 Aug 1;159(3):1437-43 PMID: 9233641
  51. PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage.
    Development. 1992 Jun;115(2):535-51 PMID: 1425339
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1998-12-15
Pages
10457-63
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793357
Subset
IM
Grants
NINDS NIH HHS · R01 NS036674 · United States
NINDS NIH HHS · R37 NS036674 · United States
NINDS NIH HHS · NS 36674 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com