Differentiation of neural precursor cell-derived oligodendrocyte progenitor cells following transplantation into normal and injured spinal cords

Differentiation

Volumn 80, Issue 4-5, 2010, Pages 228-240

  Lü, He Zuo ^a,b   Wang, Yan Xia ^a   Zou, Jian ^a   Li, Ying ^a   Fu, Sai Li ^a   Jin, Jian Qiang ^a   Hu, Jian Guo ^a,b   Lu, Pei Hua ^a  

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

^b BENGBU MEDICAL COLLEGE   (China)

Author keywords

Bone morphogenetic proteins; Differentiation; Inflammatory factors; Oligodendrocyte precursor cells; Spinal cord injury; Transplantation

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; NOGGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; STEM CELL; TISSUE HOMOGENATE; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELLS; OLIGODENDROGLIA; RATS; SPINAL CORD INJURIES;

RATTUS;

EID: 78049235500     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2010.09.179     Document Type: Article

References (61)

1. Baumann N., Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 2001, 81:871-927.
2. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999, 285:754-756.
3. Bambakidis N.C., Miller R.H. Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion. Spine J. 2004, 4:16-26.
4. Bonaguidi M.A., McGuire T., Hu M., Kan L., Samanta J., J.A.Kessler LIF BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 2005, 132:5503-5514.
5. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol. Cell. Neurosci. 2003, 24:623-631.
6. Cao Q., Xu X.M., Devries W.H., Enzmann G.U., Ping P., Tsoulfas P., Wood P.M., Bunge M.B., Whittemore S.R. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J. Neurosci. 2005, 25:6947-6957.
7. Chan C.L., Wigley C.B., Berry M. Oligodendrocyte-type 2 astrocyte (O-2A) progenitor cells from neonatal and adult rat optic nerve differ in their responsiveness to platelet-derived growth factor. Brain Res. Dev. Brain Res. 1990, 55:275-282.
8. Chen Y., Balasubramaniyan V., Peng J., Hurlock E.C., Tallquist M., Li J., Lu Q.R. Isolation and culture of rat and mouse oligodendrocyte precursor cells. Nat. Protoc. 2007, 2:1044-1051.
9. Crang A.J., Gilson J.M., Li W.W., Blakemore W.F. The remyelinating potential and in vitro differentiation of MOG-expressing oligodendrocyte precursors isolated from the adult rat CNS. Eur. J. Neurosci. 2004, 20:1445-1460.
10. Cao Q.L., Zhang Y.P., Howard R.M., Walters W.M., Tsoulfas P., Whittemore S.R. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp. Neurol. 2001, 167:48-58.
11. Choi E.W., Shin I.S., Bhang D.H., Lee D.H., Bae B.K., Kang M.S., Kim D.Y., Hwang C.Y., Lee C.W., Youn H.Y. Hormonal change and cytokine mRNA expression in peripheral blood mononuclear cells during the development of canine autoimmune thyroiditis. Clin. Exp. Immunol. 2006, 146:101-108.
12. Cheng X., Wang Y., He Q., Qiu M., Whittemore S.R., Cao Q. Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 2007, 25:3204-3214.
13. Chen D., Zhao M., Mundy G.R. Bone morphogenetic proteins. Growth Factors 2004, 22:233-241.
14. Chen D., Zhao M., Harris S.E., Mi Z. Signal transduction and biological functions of bone morphogenetic proteins. Front Biosci. 2004, 9:349-358.
15. Du Y., Dreyfus C.F. Oligodendrocytes as providers of growth factors. J. Neurosci. Res. 2002, 68:647-654.
16. Domeniconi M., Filbin M.T. Overcoming inhibitors in myelin to promote axonal regeneration. J. Neurol. Sci. 2005, 233:43-47.
17. Durand B., Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 2000, 22:64-71.
18. Dubois C., Manuguerra J.C., Hauttecoeur B., Maze J. Monoclonal antibody A2B5, which detects cell surface antigens, binds to ganglioside GT3 (II3 (NeuAc)3LacCer) and to its 9-O-acetylated derivative. J. Biol. Chem. 1990, 265:2797-2803.
19. Engel U., Wolswijk G. Oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells derived from adult rat spinal cord: in vitro characteristics and response to PDGF, bFGF and NT-3. Glia 1996, 16:16-26.
20. Faulkner J., Keirstead H.S. Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transplant Immunol. 2005, 15:131-142.
21. Fu S.L., Hu J.G., Li Y., Wang Y.X., Jin J.Q., Xui X.M., Lu P.H. A simplified method for generating oligodendrocyte progenitor cells from neural precursor cells isolated from the E16 rat spinal cord. Acta Neurobiol. Exp. (Wars) 2007, 67:367-377.
22. Fu S.L., Ma Z.W., Yin L., Iannotti C., Lu P.H., Xu X.M. Region-specific growth properties and trophic requirements of brain- and spinal cord-derived rat embryonic neural precursor cells. Neuroscience 2005, 135:851-862.
23. Fields R.D. Oligodendrocytes changing the rules: action potentials in glia and oligodendrocytes controlling action potentials. Neuroscientist 2008, 14:540-543.
24. Feldhaus B., Dietzel I.D., Heumann R., Berger R. Effects of interferon-gamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors. J. Soc. Gynecol. Invest. 2004, 11:89-96.
25. Gao F.B., Apperly J., Raff M. Cell-intrinsic timers and thyroid hormone regulate the probability of cell-cycle withdrawal and differentiation of oligodendrocyte precursor cells. Dev. Biol. 1998, 197:54-66.
26. Glaser T., Perez-Bouza A., Klein K., Brustle O. Generation of purified oligodendrocyte progenitors from embryonic stem cells. Faseb J. 2005, 19:112-114.
27. Grinspan J.B., Edell E., Carpio D.F., Beesley J.S., Lavy L., Pleasure D., Golden J.A. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J. Neurobiol. 2000, 43:1-17.
28. Hill C.E., Proschel C., Noble M., Mayer-Proschel M., Gensel J.C., Beattie M.S., Bresnahan J.C. Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: survival, differentiation, and effects on lesion environment and axonal regeneration. Exp. Neurol. 2004, 190:289-310.
29. Heaton M.B., Swanson D.J., Paiva M. Neurotrophic activity in embryonic chick brain: early appearance and differential regional distribution. Dev. Neurosci. 1993, 15:1-9.
30. Hampton D.W., Asher R.A., Kondo T., Steeves J.D., Ramer M.S., Fawcett J.W. A potential role for bone morphogenetic protein signalling in glial cell fate determination following adult central nervous system injury in vivo. Eur. J. Neurosci. 2007, 26:3024-3035.
31. Hu J.G., Fu S.L., Zhang K.H., Li Y., Yin L., Lu P.H., Xu X.M. Differential gene expression in neural stem cells and oligodendrocyte precursor cells: a cDNA microarray analysis. J. Neurosci. Res. 2004, 78:637-646.
32. Kim B.G., Hwang D.H., Lee S.I., Kim E.J., Kim S.U. Stem cell-based cell therapy for spinal cord injury. Cell Transplant 2007, 16:355-364.
33. Kang S.M., Cho M.S., Seo H., Yoon C.J., Oh S.K., Choi Y.M., Kim D.W. Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells 2007, 25:419-424.
34. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 2005, 25:4694-4705.
35. Kondo T., Raff M.C. A role for Noggin in the development of oligodendrocyte precursor cells. Dev. Biol. 2004, 267:242-251.
36. Lu H.Z., Wang Y.X., Li Y., Fu S.L., Hang Q., Lu P.H. Proliferation and differentiation of oligodendrocyte progenitor cells induced from rat embryonic neural precursor cells followed by flow cytometry. Cytometry A. 2008.
37. Louis J.C., Magal E., Muir D., Manthorpe M., Varon S. CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J. Neurosci. Res. 1992, 31:193-204.
38. Lepore A.C., Fischer I. Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Exp. Neurol. 2005, 194:230-242.
39. Liu N., Han S., Lu P.H., Xu X.M. Upregulation of annexins I, II, and V after traumatic spinal cord injury in adult rats. J. Neurosci. Res. 2004, 77:391-401.
40. McKerracher L., Winton M.J. Nogo on the go. Neuron 2002, 36:345-348.
41. Mabie P.C., Mehler M.F., Marmur R., Papavasiliou A., Song Q., Kessler J.A. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 1997, 17:4112-4120.
42. McDonald J.W. Repairing the damaged spinal cord. Sci. Am. 1999, 281:64-73.
43. McDonald J.W. Repairing the damaged spinal cord: from stem cells to activity-based restoration therapies. Clin. Neurosurg. 2004, 51:207-227.
44. McDonald J.W., Howard M.J. Repairing the damaged spinal cord: a summary of our early success with embryonic stem cell transplantation and remyelination. Prog. Brain Res. 2002, 137:299-309.
45. Marano J.E., Sun D., Zama A.M., Young W., Uzumcu M. Orthotopic transplantation of neonatal GFP rat ovary as experimental model to study ovarian development and toxicology. Reprod. Toxicol. 2008, 26:191-196.
46. Matsuura I., Taniguchi J., Hata K., Saeki N., Yamashita T. BMP inhibition enhances axonal growth and functional recovery after spinal cord injury. J. Neurochem. 2008, 105:1471-1479.
47. Miyazono K., Maeda S., Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005, 16:251-263.
48. Noble M., Barnett S.C., Bogler O., Land H., Wolswijk G., Wren D. Control of division and differentiation in oligodendrocyte-type-2 astrocyte progenitor cells. Ciba Found. Symp. 1990, 150:227-243. discussion 244-229.
49. Okano H., Ogawa Y., Nakamura M., Kaneko S., Iwanami A., Toyama Y. Transplantation of neural stem cells into the spinal cord after injury. Semin. Cell Dev. Biol. 2003, 14:191-198.
50. Power J., Mayer-Proschel M., Smith J., Noble M. Oligodendrocyte precursor cells from different brain regions express divergent properties consistent with the differing time courses of myelination in these regions. Dev. Biol. 2002, 245:362-375.
51. Pringle N.P., Mudhar H.S., Collarini E.J., Richardson W.D. 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, 115:535-551.
52. Pera M.F., Andrade J., Houssami S., Reubinoff B., Trounson A., Stanley E.G., Ward-van Oostwaard D., Mummery, C. Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J. Cell Sci. 2004, 117:1269-1280.
53. Raff M.C., Miller R.H., Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983, 303:390-396.
54. Rauch M.F., Hynes S.R., Bertram J., Redmond A., Robinson R., Williams C., Xu H., Madri J.A., Lavik E.B. Engineering angiogenesis following spinal cord injury: a coculture of neural progenitor and endothelial cells in a degradable polymer implant leads to an increase in vessel density and formation of the blood-spinal cord barrier. Eur. J. Neurosci 2009, 29:132-145.
55. Ricci-Vitiani L., Casalbore P., Petrucci G., Lauretti L., Montano N., Larocca L.M., Falchetti M.L., Lombardi D.G., Gerevini V.D., Cenciarelli C., D'Alessandris Q.G., Fernandez E., De Maria R., Maira G., Peschle C., Parati E., Pallini R. Influence of local environment on the differentiation of neural stem cells engrafted onto the injured spinal cord. Neurol. Res. 2006, 28:488-492.
56. Rengachary S.S. Bone morphogenetic proteins: basic concepts. Neurosurg. Focus 2002, 13:e2.
57. Smith R.G., McManaman J., Appel S.H. Trophic effects of skeletal muscle extracts on ventral spinal cord neurons in vitro: separation of a protein with morphologic activity from proteins with cholinergic activity. J. Cell. Biol. 1985, 101:1608-1621.
58. See J., Zhang X., Eraydin N., Mun S.B., Mamontov P., Golden J.A., Grinspan J.B. Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol. Cell Neurosci. 2004, 26:481-492.
59. Setoguchi T., Yone K., Matsuoka E., Takenouchi H., Nakashima K., Sakou T., Komiya S., Izumo S. Traumatic injury-induced BMP7 expression in the adult rat spinal cord. Brain Res. 2001, 921:219-225.
60. Xu, L., Xu, C.J., Lu, H.Z., Wang, Y.X., Li, Y., Lu, P.H., 2010. Long-term fate of allogeneic neural stem cells following transplantation into injured spinal cord, Stem Cell Rev, 6 121-136.
61. Xiao, Q., Du, Y., Wu, W., Yip, H.K., 2010. Bone morphogenetic proteins mediate cellular response and, together with Noggin, regulate astrocyte differentiation after spinal cord injury. Exp. Neurol., 221 353-366.