NG2 proteoglycan expression in the peripheral nervous system: Upregulation following injury and comparison with CNS lesions

Molecular and Cellular Neuroscience

Volumn 25, Issue 4, 2004, Pages 572-584

  Rezajooi, Kia ^a,b   Pavlides, M ^a   Winterbottom, J ^a   Stallcup, W B ^c   Hamlyn, P J ^b   Lieberman, A R ^a   Anderson, P N ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL LONDON HOSPITAL   (United Kingdom)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN S 100; PROTEOGLYCAN; PROTEOGLYCAN NG2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAVEOLA; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDONEURIUM; FEMALE; FIBROBLAST; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE COMPRESSION; NERVE CRUSH; NERVE FIBER REGENERATION; NERVE SPROUTING; NERVE TRANSECTION; NONHUMAN; PERINEURIUM; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; SATELLITE CELL; SCIATIC NERVE; SCIATIC NEUROPATHY; SPINAL CORD INJURY; SPINAL GANGLION; UPREGULATION;

ANIMALS; ANTIGENS; CAVEOLAE; CENTRAL NERVOUS SYSTEM; FEMALE; FIBROBLASTS; GANGLIA, SPINAL; GROWTH CONES; MICE; MICE, INBRED C57BL; MICROVILLI; NERVE REGENERATION; NEURONAL PLASTICITY; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; S100 PROTEINS; SATELLITE CELLS, PERINEURONAL; SCIATIC NEUROPATHY; SPINAL CORD INJURIES; UP-REGULATION;

EID: 1842739600     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.10.009     Document Type: Article

References (48)

1. Anderson P.N., Nadim W., Turmaine M. Schwann cell migration through freeze-killed peripheral nerve grafts without accompanying axons. Acta Neuropathol. Berl. 82:1991;193-199.
2. Bavetta S., Hamlyn P.J., Burnstock G., Lieberman A.R., Anderson P.N. The effects of FK506 on dorsal column axons following spinal cord injury in adult rats: neuroprotection and local regeneration. Exp. Neurol. 158:1999;382-393.
3. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., Gallo V. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 161:2003;169-186.
4. Burg M.A., Tillet E., Timpl R., Stallcup W.B. Binding of the NG2 proteoglycan to type VI collagen and other extracellular matrix molecules. J. Biol. Chem. 271:1996;26110-26116.
5. Burg M.A., Grako K.A., Stallcup W.B. Expression of the NG2 proteoglycan enhances the growth and metastatic properties of melanoma cells. J. Cell. Physiol. 177:1998;299-312.
6. Butt A.M., Berry M. Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J. Neurosci. Res. 59:2000;477-488.
7. Butt A.M., Duncan A., Hornby M.F., Kirvell S.L., Hunter A., Levine J.M., Berry M. Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia. 26:1999;84-91.
8. Dawson M.R., Levine J.M., Reynolds R. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J. Neurosci. Res. 61:2000;471-479.
9. Di Bello I.C., Dawson M.R., Levine J.M., Reynolds R. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J. Neurocytol. 28:1999;365-381.
10. Dou C.L., Levine J.M. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci. 14:1994;7616-7628.
11. Fang X., Burg M.A., Barritt D., Dahlin Huppe K., Nishiyama A., Stallcup W.B. Cytoskeletal reorganization induced by engagement of the NG2 proteoglycan leads to cell spreading and migration. Mol. Biol. Cell. 10:1999;3373-3387.
12. Fidler P.S., Schuette K., Asher R.A., Dobbertin A., Thornton S.R., Calle Patino Y., Muir E., Levine J.M., Geller H.M., Rogers J.H., Faissner A., Fawcett J.W. Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J. Neurosci. 19:1999;8778-8788.
13. Garrigues H.J., Lark M.W., Lara S., Hellstrom I., Hellstrom K.E., Wight T.N. The melanoma proteoglycan: restricted expression on microspikes, a specific microdomain of the cell surface. J. Cell Biol. 103:1986;1699-1710.
14. Hillenbrand R., Molthagen M., Montag D., Schachner M. The close homologue of the neural adhesion molecule L1, CHL1: patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur. J. Neurosci. 11:1999;813-826.
15. Holtz A., Nystrom B., Gerdin B., Olsson Y. Neuropathological changes and neurological function after spinal cord compression in the rat. J. Neurotrauma. 7:1990;155-167.
16. Jones L.L., Yamaguchi Y., Stallcup W.B., Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22:2002;2792-2803.
17. Keirstead H.S., Levine J.M., Blakemore W.F. Response of the oligodendrocyte progenitor cell population, defined by NG2 labelling to demyelination of the adult spinal cord. Glia. 22:1998;161-170.
18. Levine J.M. Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci. 14:1994;4716-4730.
19. Levine J.M., Enquist L.W., Card J.P. Reactions of oligodendrocyte precursor cells to alpha herpesvirus infection of the central nervous system. Glia. 23:1998;316-328.
20. Levine J.M., Reynolds R., Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24:2001;39-47.
21. Martin S., Levine A.K., Chen Z.J., Ughrin Y., Levine J.M. Deposition of the NG2 proteoglycan at nodes of Ranvier in the peripheral nervous system. J. Neurosci. 21:2001;8119-8128.
22. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1994;1-28.
23. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 21:2001;3392-3400.
24. Morgenstern D.A., Asher R.A., Levine J.M., Fawcett J.W. Expression of the chondroitin sulphate proteoglycan in normal and regenerating sciatic nerve. Soc. Neurosci. Abstr. 25:1999;1264.
25. Neumann S., Woolf C.J. Regeneration of dorsal column fibres into and beyond the lesion site following adult spinal cord injury. Neuron. 23:1999;83-91.
26. Nishiyama A. Glial progenitor cells in normal and pathological states. Keio J. Med. 47:1998;205-208.
27. Nishiyama A., Dahlin K.J., Prince J.T., Johnstone S.R., Stallcup W.B. The primary structure of NG2, a novel membrane-spanning proteoglycan. J. Cell Biol. 114:1991;359-371.
28. Nishiyama A., Chang A., Trapp B.D. NG2-positive glial cells: a novel glial cell population in the adult brain. J. Neuropathol. Exp. Neurol. 58:1999;1113-1124.
29. Nystrom B., Berglund J.E. Spinal cord restitution following compression injuries in rats. Acta Neurol. Scand. 78:1988;467-472.
30. Nystrom B., Berglund J.E., Bergquist E. Methodological analysis of an experimental spinal cord compression model in the rat. Acta Neurol. Scand. 78:1988;460-466.
31. Ong W.Y., Levine J.M. A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. NeuroReport. 92:1999;83-95.
32. Ozerdem U., Grako K.A., Dahlin-Huppe K., Monosov E., Stallcup W.B. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev. Dyn. 222:2001;218-227.
33. Ozerdem U., Monosov E., Stallcup W.B. NG2 proteoglycan expression by pericytes in pathological microvasculature. Microvasc. Res. 63:2002;129-134.
34. Palay S.L., Chan-Palay V. Cerebellar Cortex: Cytology and Organization. 1974;Springer-Verlag, Berlin.
35. Ramer M.S., Bisby M.A. Differences in sympathetic innervation of mouse DRG following proximal or distal nerve lesions. Exp. Neurol. 152:1989;197-207.
36. Schneider S., Bosse F., D'Urso D., Muller H., Sereda M.W., Nave K., Niehaus A., Kempf T., Schnolzer M., Trotter J. The AN2 protein is a novel marker for the Schwann cell lineage expressed by immature and nonmyelinating Schwann cells. J. Neurosci. 21:2001;920-933.
37. Shinder V., Govrin-Lippmann R., Cohen S., Belenky M., Ilin P., Fried K., Wilkinson H.A., Devor M. Structural basis of sympathetic-sensory coupling in rat and human dorsal root ganglia following peripheral nerve injury. J. Neurocytol. 28:1999;743-761.
38. Siironen J., Collan Y.L., Roytta M. Axonal reinnervation does not influence Schwann cell proliferation after rat sciatic nerve transection. Brain Res. 654:1994;303-311.
39. Stallcup W.B., Dahlin-Huppe K. Chondroitin sulfate and cytoplasmic domain-dependent membrane targeting of the NG2 proteoglycan promotes retraction fiber formation and cell polarization. J. Cell Sci. 114:2001;2315-2325.
40. Stallcup W.B., Dahlin K., Healy P. Interaction of the NG2 chondroitin sulfate proteoglycan with type VI collagen. J. Cell Biol. 111:1990;3177-3188.
41. Tang X., Davies J.E., Davies S.J. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 71:2003;427-444.
42. Tillet E., Ruggiero F., Nishiyama A., Stallcup W.B. The membrane-spanning proteoglycan NG2 binds to collagens V and VI through the central nonglobular domain of its core protein. J. Biol. Chem. 272:1997;10769-10776.
43. Ughrin Y.M., Chen Z.J., Levine J.M. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J. Neurosci. 23:2003;175-186.
44. Wilson S.S., Baetge E.E., Stallcup W.B. Antisera specific for cell lines with mixed neuronal and glial properties. Dev. Biol. 83:1981;146-153.
45. Woodham P., Anderson P.N., Nadim W., Turmaine M. Satellite cells surrounding axotomised rat dorsal root ganglion cells increase expression of a GFAP-like protein. Neurosci. Lett. 98:1989;8-12.
46. Zhang Y., Winterbottom J.K., Schachner M., Lieberman A.R., Anderson P.N. Tenascin-C expression and axonal sprouting following injury to the spinal dorsal columns in the adult rat. J. Neurosci. Res. 49:1997;433-450.
47. Zhang Y., Tohyama K., Winterbottom J.K., Haque N.S., Schachner M., Lieberman A.R., Anderson P.N. Correlation between putative inhibitory molecules at the dorsal root entry zone and failure of dorsal root axonal regeneration. Mol. Cell. Neurosci. 17:2001;444-459.
48. Zuo J., Hernandez Y.J., Muir D. Chondroitin sulfate proteoglycan with neuriteinhibiting activity is up-regulated following peripheral nerve injury. J. Neurobiol. 34:1998;41-54.