Oligodendrocyte precursor cells differentially expressing Nogo-A but not MAG are more permissive to neurite outgrowth than mature oligodendrocytes

Experimental Neurology

Volumn 217, Issue 1, 2009, Pages 184-196

  Ma, Zhengwen ^a,c   Cao, Qilin ^a   Zhang, Liqun ^a   Hu, Jianguo ^b   Howard, Russell M ^a   Lu, Peihua ^c   Whittemore, Scott R ^a   Xu, Xiao Ming ^a,b,c  

^a University of Louisville School of Medicine   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

MAG; Myelin inhibitors; Neurite outgrowth; Nogo A; OPC

Indexed keywords

MYELIN ASSOCIATED GLYCOPROTEIN; PROTEIN NOGO A;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; NEURITE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; STEM CELL;

ANALYSIS OF VARIANCE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; FIBROBLAST GROWTH FACTOR 2; GANGLIA, SPINAL; GANGLIOSIDES; MYELIN BASIC PROTEINS; MYELIN PROTEINS; NEURITES; NEURONS; OLIGODENDROGLIA; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SPINAL CORD; STEM CELLS; TIME FACTORS;

EID: 64249124962     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.02.006     Document Type: Article

References (54)

1. Bamber N.I., Li H., Lu X., Oudega M., Aebischer P., and Xu X.M. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 13 (2001) 257-268
2. Baumann N., and Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 81 (2001) 871-927
3. Cai J., Qi Y., Hu X., Tan M., Liu Z., Zhang J., Li Q., Sander M., and Qiu M. Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45 (2005) 41-53
4. Cao Q., Xu X.M., Devries W.H., Enzmann G.U., Ping P., Tsoulfas P., Wood P.M., Bunge M.B., and Whittemore S.R. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J. Neurosci. 25 (2005) 6947-6957
5. Chau C.H., Shum D.K.Y., and Xu X.M. Combinatorial strategies towards spinal cord repair: enhancement of the Schwann cell bridge and modification of the graft-host interface. Preclinica 2 (2004) 409-415
6. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ R., and Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403 (2000) 434-439
7. Domeniconi M., and Filbin M.T. Overcoming inhibitors in myelin to promote axonal regeneration. J. Neurol. Sci. 233 (2005) 43-47
8. Domeniconi M., Cao Z., Spencer T., Sivasankaran R., Wang K.C., Nikulina E., Kimura N., Cai H., Deng K., Gao Y., He Z., and Filbin M.T. Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35 (2002) 283-290
9. Fournier A.E., and Strittmatter S.M. Repulsive factors and axonal regeneration in the CNS. Curr. Opin. Neurobiol. 11 (2001) 89-94
10. Fournier A.E., GrandPre T., and Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409 (2001) 341-346
11. Fraher J.P. Axon-glial relationships in early CNS-PNS transitional zone development: an ultrastructural study. J. Neurocytol. 26 (1997) 41-52
12. Gianino S., Stein S.A., Li H., Lu X.B., Biesiada E., Ulas J., and Xu X.M. Postnatal growth of corticospinal axons in the spinal cord of developing mice. Dev. Brain Res. 112 (1999) 189-204
13. Goldberg J.L., Vargas M.E., Wang J.T., Mandemakers W., Oster S.F., Sretavan D.W., and Barres B.A. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J. Neurosci. 24 (2004) 4989-4999
14. GrandPre T., Nakamura F., Vartanian T., and Strittmatter S.M. Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 403 (2000) 439-444
15. Hata K., Fujitani M., Yasuda Y., Doya H., Saito T., Yamagishi S., Mueller B.K., and Yamashita T. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J. Cell. Biol. 173 (2006) 47-58
16. Huang J.K., Phillips G.R., Roth A.D., Pedraza L., Shan W., Belkaid W., Mi S., Fex-Svenningsen A., Florens L., Yates III J.R., and Colman D.R. Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310 (2005) 1813-1817
17. Kottis V., Thibault P., Mikol D., Xiao Z.C., Zhang R., Dergham P., and Braun P.E. Oligodendrocyte-myelin glycoprotein (OMpg) is an inhibitor of neurite outgrowth. J. Neurochem. 82 (2002) 1566-1569
18. Kullander K., Croll S.D., Zimmer M., Pan L., McClain J., Hughes V., Zabski S., DeChiara T.M., Klein R., Yancopoulos G.D., and Gale N.W. Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev. 15 (2001) 877-888
19. Lee J.C., Mayer-Proschel M., and Rao M.S. Gliogenesis in the central nervous system. Glia 30 (2000) 105-121
20. Levine J.M., Reynolds R., and Fawcett J.W. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24 (2001) 39-47
21. Liu B.P., Fournier A., GrandPre T., and Strittmatter S.M. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 297 (2002) 1190-1193
22. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., and Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109 (2002) 75-86
23. Manitt C., Wang D., Kennedy T.E., and Howland D.R. Positioned to inhibit: netrin-1 and netrin receptor expression after spinal cord injury. J. Neurosci. Res. 84 (2006) 1808-1820
24. Mayer-Proschel M., Kalyani A.J., Mujtaba T., and Rao M.S. Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19 (1997) 773-785
25. McGee A.W., and Strittmatter S.M. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci. 26 (2003) 193-198
26. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., and Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13 (1994) 805-811
27. Mingorance A., Fontana X., Sole M., Burgaya F., Urena J.M., Teng F.Y., Tang B.L., Hunt D., Anderson P.N., Bethea J.R., Schwab M.E., Soriano E., and del Rio J.A. Regulation of Nogo and Nogo receptor during the development of the entorhino-hippocampal pathway and after adult hippocampal lesions. Mol. Cell. Neurosci. 26 (2004) 34-49
28. Moreau-Fauvarque C., Kumanogoh A., Camand E., Jaillard C., Barbin G., Boquet I., Love C., Jones E.Y., Kikutani H., Lubetzki C., Dusart I., and Chedotal A. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J. Neurosci. 23 (2003) 9229-9239
29. Mujtaba T., Piper D.R., Kalyani A., Groves A.K., Lucero M.T., and Rao M.S. Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev. Biol. 214 (1999) 113-127
30. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., and Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13 (1994) 757-767
31. O'Brien D., Dockery P., McDermott K., and Fraher J.P. The ventral motoneurone axon bundle in the CNS-a cordone system?. J. Neurocytol. 27 (1998) 247-258
32. O'Neill P., Whalley K., and Ferretti P. Nogo and Nogo-66 receptor in human and chick: implications for development and regeneration. Dev. Dyn. 231 (2004) 109-121
33. Oertle T., van der Haar M.E., Bandtlow C.E., Robeva A., Burfeind P., Buss A., Huber A.B., Simonen M., Schnell L., Brosamle C., Kaupmann K., Vallon R., and Schwab M.E. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 23 (2003) 5393-5406
34. Oudega M., and Xu X.M. Schwann cell transplantation for repair of the adult spinal cord. J. Neurotrauma. 23 (2006) 453-467
35. Peters A., Palay S., and Webster H.D. The Fine Structure of the Nervous System: The Neuron and Supporting Cells (1991), Oxford Univ. Press, Oxford
36. Prinjha R., Moore S.E., Vinson M., Blake S., Morrow R., Christie G., Michalovich D., Simmons D.L., and Walsh F.S. Inhibitor of neurite outgrowth in humans. Nature 403 (2000) 383-384
37. Qi Y., Cai J., Wu Y., Wu R., Lee J., Fu H., Rao M., Sussel L., Rubenstein J., and Qiu M. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128 (2001) 2723-2733
38. Rao M.S., and Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol. 188 (1997) 48-63
39. Rao M.S., Noble M., and Mayer-Proschel M. A tripotential glial precursor cell is present in the developing spinal cord. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3996-4001
40. Schnell L., and Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343 (1990) 269-272
41. Schwab M.E., and Caroni P. Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J. Neurosci. 8 (1988) 2381-2393
42. Spencer T., Domeniconi M., Cao Z., and Filbin M.T. New roles for old proteins in adult CNS axonal regeneration. Curr. Opin. Neurobiol. 13 (2003) 133-139
43. Stebbins J.W., Jaffe H., Fales H.M., and Moller J.R. Determination of a native proteolytic site in myelin-associated glycoprotein. Biochemistry 36 (1997) 2221-2226
44. Trapp B.D. Myelin-associated glycoprotein. Location and potential functions. Ann. N. Y. Acad. Sci. 605 (1990) 29-43
45. Vactor D.V. Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8 (1998) 80-86
46. Venkatesh K., Chivatakarn O., Lee H., Joshi P.S., Kantor D.B., Newman B.A., Mage R., Rader C., and Giger R.J. The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J. Neurosci. 25 (2005) 808-822
47. Wang K.C., Kim J.A., Sivasankaran R., Segal R., and He Z. p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420 (2002) 74-78
48. Wang K.C., Koprivica V., Kim J.A., Sivasankaran R., Guo Y., Neve R.L., and He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417 (2002) 941-944
49. Wang X., Chun S.J., Treloar H., Vartanian T., Greer C.A., and Strittmatter S.M. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22 (2002) 5505-5515
50. Winslow J.W., Moran P., Valverde J., Shih A., Yuan J.Q., Wong S.C., Tsai S.P., Goddard A., Henzel W.J., Hefti F., et al. Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14 (1995) 973-981
51. Wong S.T., Henley J.R., Kanning K.C., Huang K.H., Bothwell M., and Poo M.M. A p75 (NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5 (2002) 1302-1308
52. Wood P.M., and Williams A.K. Oligodendrocyte proliferation and CNS myelination in cultures containing dissociated embryonic neuroglia and dorsal root ganglion neurons. Dev. Brain Res. 12 (1984) 225-241
53. Xu X.M., Chen A., Guenard V., Kleitman N., and Bunge M.B. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 26 (1997) 1-16
54. Yiu G., and He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7 (2006) 617-627