Bone morphogenetic proteins prevent bone marrow stromal cell-mediated oligodendroglial differentiation of transplanted adult neural progenitor cells in the injured spinal cord

Stem Cell Research

Volumn 11, Issue 2, 2013, Pages 758-771

  Sandner, Beatrice ^a,c   Rivera, Francisco J ^b   Caioni, Massimiliano ^a   Nicholson, LaShae ^c   Eckstein, Volker ^e   Bogdahn, Ulrich ^a   Aigner, Ludwig ^b   Blesch, Armin ^c,d   Weidner, Norbert ^a,c  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BROMODEOXYCYTIDINE; NOGGIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW STROMAL CELL; CELL DIFFERENTIATION; CERVICAL DORSAL FUNICULUS TRANSECTION; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; STEM CELL TRANSPLANTATION; STROMA CELL; SUBVENTRICULAR ZONE; UPREGULATION;

ANIMALS; BONE MARROW TRANSPLANTATION; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEURAL STEM CELLS; OLIGODENDROGLIA; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; SPINAL CORD INJURIES;

RATTUS;

EID: 84879401334     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.05.003     Document Type: Article

References (78)

1. Akiyama Y., Honmou O., Kato T., Uede T., Hashi K., Kocsis J.D. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp. Neurol. 2001, 167(1):27-39.
2. Alto L.T., Havton L.A., Conner J.M., Hollis Ii E.R., Blesch A., Tuszynski M.H. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat. Neurosci. 2009, 12(9):1106-1113.
3. Ankeny D.P., McTigue D.M., Jakeman L.B. Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats. Exp. Neurol. 2004, 190(1):17-31.
4. Ara J., See J., Mamontov P., Hahn A., Bannerman P., Pleasure D., Grinspan J.B. Bone morphogenetic proteins 4, 6, and 7 are up-regulated in mouse spinal cord during experimental autoimmune encephalomyelitis. J. Neurosci. Res. 2008, 86(1):125-135.
5. Blesch A. Lentiviral and MLV based retroviral vectors for ex vivo and in vivo gene transfer. Methods 2004, 33(2):164-172.
6. Bonaguidi M.A., McGuire T., Hu M., Kan L., Samanta J., Kessler J.A. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 2005, 132(24):5503-5514.
7. 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(1):48-58.
8. Cao Q.L., Howard R.M., Dennison J.B., Whittemore S.R. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp. Neurol. 2002, 177(2):349-359.
9. Caplan A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 2007, 213(2):341-347.
10. Casha S., Yu W.R., Fehlings M.G. Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 2001, 103(1):203-218.
11. 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(12):3204-3214.
12. Cho S.R., Kim Y.R., Kang H.S., Yim S.H., Park C.I., Min Y.H., Lee B.H., Shin J.C., Lim J.B. Functional recovery after the transplantation of neurally differentiated mesenchymal stem cells derived from bone barrow in a rat model of spinal cord injury. Cell Transplant. 2009, 18(12):1359-1368.
13. Colak D., Mori T., Brill M.S., Pfeifer A., Falk S., Deng C., Monteiro R., Mummery C., Sommer L., Gotz M. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J. Neurosci. 2008, 28(2):434-446.
14. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 1997, 3(1):73-76.
15. Enzmann G.U., Benton R.L., Woock J.P., Howard R.M., Tsoulfas P., Whittemore S.R. Consequences of noggin expression by neural stem, glial, and neuronal precursor cells engrafted into the injured spinal cord. Exp. Neurol. 2005, 195(2):293-304.
16. Fuller M.L., DeChant A.K., Rothstein B., Caprariello A., Wang R., Hall A.K., Miller R.H. Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions. Ann. Neurol. 2007, 62(3):288-300.
17. Gage F.H., Ray J., Fisher L.J. Isolation, characterization, and use of stem cells from the CNS. Annu. Rev. Neurosci. 1995, 18:159-192.
18. 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):1-17.
19. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., Affolter M., Vale W.W., Belmonte J.C., Choe S. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 2002, 420(6916):636-642.
20. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., Baban K., Affolter M., Vale W.W., Izpisua Belmonte J.C., Choe S. Structural basis of BMP signaling inhibition by Noggin, a novel twelve-membered cystine knot protein. J. Bone Joint Surg. Am. 2003, 85-A(Suppl. 3):52-58.
21. Gross R.E., Mehler M.F., Mabie P.C., Zang Z., Santschi L., Kessler J.A. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996, 17(4):595-606.
22. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(4):2199-2204.
23. Hofstetter C.P., Holmstrom N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 2005, 8(3):346-353.
24. Horky L.L., Galimi F., Gage F.H., Horner P.J. Fate of endogenous stem/progenitor cells following spinal cord injury. J. Comp. Neurol. 2006, 498(4):525-538.
25. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 2000, 20(6):2218-2228.
26. Kakulas B.A. A review of the neuropathology of human spinal cord injury with emphasis on special features. J. Spinal Cord Med. 1999, 22(2):119-124.
27. Karimi-Abdolrezaee S., Eftekharpour E., Wang J., Morshead C.M., Fehlings M.G. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 2006, 26(13):3377-3389.
28. Keating A. Mesenchymal stromal cells. Curr. Opin. Hematol. 2006, 13(6):419-425.
29. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295(5556):868-872.
30. Lu P., Jones L.L., Tuszynski M.H. BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp. Neurol. 2005, 191(2):344-360.
31. Lu P., Jones L.L., Tuszynski M.H. Axon regeneration through scars and into sites of chronic spinal cord injury. Exp. Neurol. 2007, 203(1):8-21.
32. 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(11):4112-4120.
33. Mabie P.C., Mehler M.F., Kessler J.A. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J. Neurosci. 1999, 19(16):7077-7088.
34. 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(4):1471-1479.
35. 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. 2001, 21(10):3392-3400.
36. Miyagi M., Mikawa S., Sato T., Hasegawa T., Kobayashi S., Matsuyama Y., Sato K. BMP2, BMP4, noggin, BMPRIA, BMPRIB, and BMPRII are differentially expressed in the adult rat spinal cord. Neuroscience 2012, 203:12-26.
37. Nakashima K., Takizawa T., Ochiai W., Yanagisawa M., Hisatsune T., Nakafuku M., Miyazono K., Kishimoto T., Kageyama R., Taga T. BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(10):5868-5873.
38. Nashmi R., Fehlings M.G. Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 2001, 104(1):235-251.
39. Nashmi R., Fehlings M.G. Mechanisms of axonal dysfunction after spinal cord injury: with an emphasis on the role of voltage-gated potassium channels. Brain Res. Brain Res. Rev. 2001, 38(1-2):165-191.
40. Neuhuber B., Timothy Himes B., Shumsky J.S., Gallo G., Fischer I. Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res. 2005, 1035(1):73-85.
41. Parr A.M., Kulbatski I., Tator C.H. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J. Neurotrauma 2007, 24(5):835-845.
42. Pfeifer A., Ikawa M., Dayn Y., Verma I.M. Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(4):2140-2145.
43. Pfeifer K., Vroemen M., Blesch A., Weidner N. Adult neural progenitor cells provide a permissive guiding substrate for corticospinal axon growth following spinal cord injury. Eur. J. Neurosci. 2004, 20(7):1695-1704.
44. Pfeifer K., Vroemen M., Caioni M., Aigner L., Bogdahn U., Weidner N. Autologous adult rodent neural progenitor cell transplantation represents a feasible strategy to promote structural repair in the chronically injured spinal cord. Regen. Med. 2006, 1(2):255-266.
45. Rivera F.J., Couillard-Despres S., Pedre X., Ploetz S., Caioni M., Lois C., Bogdahn U., Aigner L. Mesenchymal stem cells instruct oligodendrogenic fate decision on adult neural stem cells. Stem Cells 2006.
46. Rivera F.J., Kandasamy M., Couillard-Despres S., Caioni M., Sanchez R., Huber C., Weidner N., Bogdahn U., Aigner L. Oligodendrogenesis of adult neural progenitors: differential effects of ciliary neurotrophic factor and mesenchymal stem cell derived factors. J. Neurochem. 2008, 107(3):832-843.
47. Rivera F.J., Siebzehnrubl F.A., Kandasamy M., Couillard-Despres S., Caioni M., Poehler A.M., Berninger B., Sandner B., Bogdahn U., Goetz M., Bluemcke I., Weidner N., Aigner L. Mesenchymal stem cells promote oligodendroglial differentiation in hippocampal slice cultures. Cell. Physiol. Biochem. 2009, 24(3-4):317-324.
48. Rivera F.J., Steffenhagen C., Kremer D., Kandasamy M., Sandner B., Couillard-Despres S., Weidner N., Kury P., Aigner L. Deciphering the oligodendrogenic program of neural progenitors: cell intrinsic and extrinsic regulators. Stem Cells Dev. 2010, 19(5):595-606.
49. Samanta J., Kessler J.A. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 2004, 131(17):4131-4142.
50. Scolding N., Franklin R., Stevens S., Heldin C.H., Compston A., Newcombe J. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 1998, 121(Pt 12):2221-2228.
51. 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(4):481-492.
52. See J.M., Grinspan J.B. Sending mixed signals: bone morphogenetic protein in myelination and demyelination. J. Neuropathol. Exp. Neurol. 2009, 68(6):595-604.
53. 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(1-2):219-225.
54. Setoguchi T., Nakashima K., Takizawa T., Yanagisawa M., Ochiai W., Okabe M., Yone K., Komiya S., Taga T. Treatment of spinal cord injury by transplantation of fetal neural precursor cells engineered to express BMP inhibitor. Exp. Neurol. 2004, 189(1):33-44.
55. Shibuya S., Miyamoto O., Auer R.N., Itano T., Mori S., Norimatsu H. Embryonic intermediate filament, nestin, expression following traumatic spinal cord injury in adult rats. Neuroscience 2002, 114(4):905-916.
56. Shihabuddin L.S., Ray J., Gage F.H. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp. Neurol. 1997, 148(2):577-586.
57. Shihabuddin L.S., Horner P.J., Ray J., Gage F.H. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 2000, 20(23):8727-8735.
58. Siegenthaler M.M., Tu M.K., Keirstead H.S. The extent of myelin pathology differs following contusion and transection spinal cord injury. J. Neurotrauma 2007, 24(10):1631-1646.
59. Sim F.J., Zhao C., Penderis J., Franklin R.J. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. 2002, 22(7):2451-2459.
60. Steffenhagen C., Dechant F.X., Oberbauer E., Furtner T., Weidner N., Kury P., Aigner L., Rivera F.J. Mesenchymal stem cells prime proliferating adult neural progenitors toward an oligodendrocyte fate. Stem Cells Dev. 2012, 21(11):1838-1851.
61. Suhonen J.O., Peterson D.A., Ray J., Gage F.H. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 1996, 383(6601):624-627.
62. Taylor L., Jones L., Tuszynski M.H., Blesch A. Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 2006, 26(38):9713-9721.
63. Uccelli A., Zappia E., Benvenuto F., Frassoni F., Mancardi G. Stem cells in inflammatory demyelinating disorders: a dual role for immunosuppression and neuroprotection. Expert. Opin. Biol. Ther. 2006, 6(1):17-22.
64. Uccelli A., Pistoia V., Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression?. Trends Immunol. 2007, 28(5):219-226.
65. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 2008, 8:726-736.
66. Vroemen M., Aigner L., Winkler J., Weidner N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur. J. Neurosci. 2003, 18(4):743-751.
67. Vroemen M., Weidner N., Blesch A. Loss of gene expression in lentivirus- and retrovirus-transduced neural progenitor cells is correlated to migration and differentiation in the adult spinal cord. Exp. Neurol. 2005, 195(1):127-139.
68. Wachs F.P., Couillard-Despres S., Engelhardt M., Wilhelm D., Ploetz S., Vroemen M., Kaesbauer J., Uyanik G., Klucken J., Karl C., Tebbing J., Svendsen C., Weidner N., Kuhn H.G., Winkler J., Aigner L. High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest. 2003, 83(7):949-962.
69. Weidner N., Blesch A., Grill R.J., Tuszynski M.H. Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J. Comp. Neurol. 1999, 413(4):495-506.
70. Weidner N., Ner A., Salimi N., Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(6):3513-3518.
71. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 1996, 16(23):7599-7609.
72. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 1998, 18(2):601-609.
73. Wright K.T., Masri W.E., Osman A., Roberts S., Trivedi J., Ashton B.A., Johnson W.E. The cell culture expansion of bone marrow stromal cells from humans with spinal cord injury: implications for future cell transplantation therapy. Spinal Cord 2008, 46:811-817.
74. Xiao Q., Du Y., Wu W., Yip H.K. Bone morphogenetic proteins mediate cellular response and, together with Noggin, regulate astrocyte differentiation after spinal cord injury. Exp. Neurol. 2010, 221(2):353-366.
75. Xu Y., Kitada M., Yamaguchi M., Dezawa M., Ide C. Increase in bFGF-responsive neural progenitor population following contusion injury of the adult rodent spinal cord. Neurosci. Lett. 2006, 397(3):174-179.
76. Yamamoto S., Yamamoto N., Kitamura T., Nakamura K., Nakafuku M. Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp. Neurol. 2001, 172(1):115-127.
77. Zai L.J., Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005, 50(3):247-257.
78. Zurita M., Vaquero J. Bone marrow stromal cells can achieve cure of chronic paraplegic rats: functional and morphological outcome one year after transplantation. Neurosci. Lett. 2006, 402(1-2):51-56.