Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions

Annals of Neurology

Volumn 62, Issue 3, 2007, Pages 288-300

  Fuller, Molly L ^a   DeChant, Anne K ^a   Rothstein, Brian ^a   Caprariello, Andrew ^a   Wang, Rae ^a   Hall, Alison K ^a   Miller, Robert H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; CORE PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; LYSOPHOSPHATIDYLCHOLINE; MESSENGER RNA; NEUROCAN; NOGGIN; OSTEOGENIC PROTEIN 1; PROTEOCHONDROITIN SULFATE; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEMYELINATION; FEMALE; GENE CONTROL; GLIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURY;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CHONDROITIN SULFATES; DEMYELINATING DISEASES; DNA; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; IMMUNOHISTOCHEMISTRY; LYSOPHOSPHATIDYLCHOLINES; NEUROGLIA; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMAD PROTEINS; SPINAL CORD DISEASES; UP-REGULATION;

EID: 34948825403     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.21179     Document Type: Article

References (49)

1. McKeon RJ, Schreiber RC, Rudge JS, Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 1991;11:3398-3411.
2. Smith GM, Strunz C. Growth factor and cytokine regulation of chondroitin sulfate proteoglycans by astrocytes. Glia 2005;52: 209-218.
3. Jones LL, Margolis RU, Tuszynski MH. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 2003;182:399-411.
4. Woodruff RH, Franklin RJ. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti-galactocerebroside: a comparative study. Glia 1999;25:216-228.
5. Hall AK, Miller RH. Emerging roles for bone morphogenetic proteins in central nervous system glial biology. J Neurosci Res 2004;76:1-8.
6. Liu A, Niswander LA. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev 2005;6: 945-954.
7. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997;390:465-471.
8. Vinals F, Lopez-Rovira T, Rosa JL, Ventura F. Inhibition of PI3K/p70 S6K and p38 MAPK cascades increases osteoblastic differentiation induced by BMP-2. FEBS Lett 2002;510: 99-104.
9. D'Alessandro JS, Wang EA. Bone morphogenetic proteins inhibit proliferation, induce reversible differentiation and prevent cell death in astrocyte lineage cells. Growth Factors 1994;11: 45-52.
10. Gross RE, Mehler MF, Mabie PC, et al. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996;17:595-606.
11. Yanagisawa M, Takizawa T, Ochiai W, et al. Fate alteration of neuroepithelial cells from neurogenesis to astrocytogenesis by bone morphogenetic proteins. Neurosci Res 2001;41:391-396.
12. Lim DA, Tramontin AD, Trevejo JM, et al. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000;28:713-726.
13. Gomes WA, Mehler MF, Kessler JA. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 2003;255:164-177.
14. Mabie PC, Mehler MF, Marmur R, et al. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J Neurosci 1997;17:4112-4120.
15. Zhu G, Mehler MF, Mabie PC, Kessler JA. Developmental changes in progenitor cell responsiveness to cytokines. J Neurosci Res 1999;56:131-145.
16. Nakashima K, Yanagisawa M, Arakawa H, Taga T. Astrocyte differentiation mediated by LIF in cooperation with BMP2. FEBS Lett 1999;457:43-46.
17. Miller RH, Dinsio K, Wang R, et al. Patterning of spinal cord oligodendrocyte development by dorsally derived BMP4. J Neurosci Res 2004;76:9-19.
18. Furuta Y, Piston DW, Hogan BL. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 1997;124:2203-2212.
19. Song Q, Mehler MF, Kessler JA. Bone morphogenetic proteins induce apoptosis and growth factor dependence of cultured sympathoadrenal progenitor cells. Dev Biol 1998;196:119-127.
20. Gomes WA, Kessler JA. Msx-2 and p21 mediate the proapoptotic but not the anti-proliferative effects of BMP4 on cultured sympathetic neuroblasts. Dev Biol 2001;237:212-221.
21. Hollnagel A, Oehlmann V, Heymer J, et al. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 1999;274:19838-19845.
22. Setoguchi T, Yone K, Matsuoka E, et al. Traumatic injury-induced BMP7 expression in the adult rat spinal cord. Brain Res 2001;921:219-225.
23. Chen J, Leong SY, Schachner M. Differential expression of cell fate determinants in neurons and glial cells of adult mouse spinal cord after compression injury. Eur J Neurosci 2005;22: 1895-1906.
24. Davies SJ, Fitch MT, Memberg SP, et al. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997;390:680-683.
25. Smith GM, Rutishauser U, Silver J, Miller RH. Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev Biol 1990;138:377.
26. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002;30:e36.
27. Grinspan JB, Edell E, Carpio DF, et al. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol 2000;43:1-17.
28. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999;49:377-391.
29. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev 2004;5:146-156.
30. Wang Y, Chang CF, Morales M, et al. Bone morphogenetic protein-6 reduces ischemia-induced brain damage in rats. Stroke 2001;32:2170-2178.
31. Mehler MF, Mabie PC, Zhang D, Kessler JA. Bone morphogenetic proteins in the nervous system. Trends Neurosci 1997; 20:309-317.
32. Tang X, Davies JE, Davies SJ. 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 2003;71:427-444.
33. Israsena N, Kessler JA. Msx2 and p21(CIP1/WAF1) mediate the proapoptotic effects of bone morphogenetic protein-4 on ventricular zone progenitor cells. J Neurosci Res 2002;69: 803-809.
34. Pekny M, Johansson CB, Eliasson C, et al. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol 1999;145:503-514.
35. Menet V, Gimenez y Ribotta M, Chauvet N, et al. Inactivation of the glial fibrillary acidic protein gene, but not that of vimentin, improves neuronal survival and neurite growth by modifying adhesion molecule expression. J Neurosci 2001;21: 6147-6158.
36. Menet V, Gimenez YRM, Sandillon F, Privat A. GFAP null astrocytes are a favorable substrate for neuronal survival and neurite growth. Glia 2000;31:267-272.
37. Smith GM, Hale JH. Macrophage/microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J Neurosci 1997; 17:9624-9633.
38. Sobel RA, Ahmed AS. White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis. J Neuropathol Exp Neurol 2001;60: 1198-1207.
39. Lemons ML, Sandy JD, Anderson DK, Howland DR. Intact aggrecan and fragments generated by both aggrecanse and metalloproteinase-like activities are present in the developing and adult rat spinal cold and their relative abundance is altered by injury. J Neurosci 2001;21:4772-4781.
40. Asher RA, Morgenstern DA, Fidler PS, et al. Neurocan is up-regulated in injured brain and in cytokine-treated astrocytes. J Neurosci 2000;20:2427-2438.
41. John GR, Shankar SL, Shafit-Zagardo B, et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 2002;8: 1115-1121.
42. Milev P, Friedlander DR, Sakurai T, et al. Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J Cell Biol 1994;127:1703-1715.
43. Snyder SE, Li J, Schauwecker PE, et al. Comparison of RPTP zeta/beta, phosphacan, and trkB mRNA expression in the developing and adult rat nervous system and induction of RPTP zeta/beta and phosphacan mRNA following brain injury. Brain Res 1996;40:79-96.
44. Hayashi N, Miyata S, Yamada M, et al. Neuronal expression of the chondroitin sulfate proteoglycans receptor-type protein-tyrosine phosphatase beta and phosphacan. Neuroscience 2005; 131:331-348.
45. Harroch S, Furtado GC, Brueck W, et al. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat Genet 2002;32:411-414.
46. Levine JM, Reynolds R, Fawcett JW. The oligodendrocyte precursor cell in health and disease. Trends Neurosci 2001;24: 39-47.
47. Ligon KL, Fancy SP, Franklin RJ, Rowitch DH. Olig gene function in CNS development and disease. Glia 2006;54: 1-10.
48. Mycko MP, Papoian R, Boschert U, et al. Microarray gene expression profiling of chronic active and inactive lesions in multiple sclerosis. Clin Neurol Neurosurg 2004;106:223-229.
49. Lock C, Hermans G, Pedotti R, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002;8:500-508.