Axonal growth and connectivity from neural stem cell grafts in models of spinal cord injury

Current Opinion in Neurobiology

Volumn 27, Issue , 2014, Pages 103-109

  Lu, Paul ^a,b   Kadoya, Ken ^b   Tuszynski, Mark H ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; EMBRYONIC STEM CELL; GRAFT SURVIVAL; GRAY MATTER; HUMAN; NERVE FIBER; NERVE FIBER GROWTH; NEURAL STEM CELL TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; SPINAL CORD INJURY; WHITE MATTER; ANIMAL; CYTOLOGY; DISEASE MODEL; NERVE CELL NETWORK; NEURAL STEM CELL; PHYSIOLOGY; PROCEDURES; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; SYNAPSE;

ANIMALS; AXONS; DISEASE MODELS, ANIMAL; HUMANS; NERVE NET; NEURAL STEM CELLS; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; SYNAPSES;

EID: 84897560216     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.03.010     Document Type: Review

References (47)

1. Ramon YC: Degeneration and regeneration of the nerve system 1928, Hafner, New York.
2. Reier P.J. Neural tissue grafts and repair of the injured spinal cord. Neuropathol Appl Neurobiol 1985, 11:81-104.
3. Jakeman L.B., Reier P.J. Axonal projections between fetal spinal cord transplants and the adult rat spinal cord: a neuroanatomical tracing study of local interactions. J Comp Neurol 1991, 307:311-334.
4. Bregman B.S., Coumans J.V., Dai H.N., Kuhn P.L., Lynskey J., McAtee M., Sandhu F. Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury. Prog Brain Res 2002, 137:257-273.
5. Steward O., Zheng B., Banos K., Yee K.M. Response to: Kim et al., "axon regeneration in young adult mice lacking Nogo-A/B." Neuron 38, 187-199. Neuron 2007, 54:191-195.
6. 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.
7. Bonner J.F., Connors T.M., Silverman W.F., Kowalski D.P., Lemay M.A., Fischer I. Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J Neurosci 2011, 31:4675-4686.
8. Li Y., Raisman G. Long axon growth from embryonic neurons transplanted into myelinated tracts of the adult rat spinal cord. Brain Res 1993, 629:115-127.
9. Lowry N., Goderie S.K., Adamo M., Lederman P., Charniga C., Gill J., Silver J., Temple S. Multipotent embryonic spinal cord stem cells expanded by endothelial factors and Shh/RA promote functional recovery after spinal cord injury. Exp Neurol 2008, 209:510-522.
10. Lu P., Jones L.L., Snyder E.Y., Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 2003, 181:115-129.
11. Abematsu M., Tsujimura K., Yamano M., Saito M., Kohno K., Kohyama J., Namihira M., Komiya S., Nakashima K. Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury. J Clin Invest 2010, 120:3255-3266.
12. Lu P., Wang Y., Graham L., McHale K., Gao M., Wu D., Brock J., Blesch A., Rosenzweig E.S., Havton L.A., et al. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 2012, 150:1264-1273.
13. Mu Y., Lee S.W., Gage F.H. Signaling in adult neurogenesis. Curr Opin Neurobiol 2010, 20:416-423.
14. 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.
15. 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, 20:1695-1704.
16. Karimi-Abdolrezaee S., Eftekharpour E., Wang J., Schut D., Fehlings M.G. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 2010, 30:1657-1676.
17. Cusimano M., Biziato D., Brambilla E., Donega M., Alfaro-Cervello C., Snider S., Salani G., Pucci F., Comi G., Garcia-Verdugo J.M., et al. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012, 135:447-460.
18. Wictorin K., Bjorklund A. Axon outgrowth from grafts of human embryonic spinal cord in the lesioned adult rat spinal cord. Neuroreport 1992, 3:1045-1048.
19. Wictorin K., Brundin P., Gustavii B., Lindvall O., Bjorklund A. Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 1990, 347:556-558.
20. Giovanini M.A., Reier P.J., Eskin T.A., Wirth E., Anderson D.K. Characteristics of human fetal spinal cord grafts in the adult rat spinal cord: influences of lesion and grafting conditions. Exp Neurol 1997, 148:523-543.
21. Iwanami A., Kaneko S., Nakamura M., Kanemura Y., Mori H., Kobayashi S., Yamasaki M., Momoshima S., Ishii H., Ando K., et al. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 2005, 80:182-190.
22. Watanabe K., Nakamura M., Iwanami A., Fujita Y., Kanemura Y., Toyama Y., Okano H. Comparison between fetal spinal-cord- and forebrain-derived neural stem/progenitor cells as a source of transplantation for spinal cord injury. Develop Neurosci 2004, 26:275-287.
23. Cummings B.J., Uchida N., Tamaki S.J., Salazar D.L., Hooshmand M., Summers R., Gage F.H., Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci USA 2005, 102:14069-14074.
24. Yan J., Xu L., Welsh A.M., Hatfield G., Hazel T., Johe K., Koliatsos V.E. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med 2007, 4:e39.
25. Cowan C.A., Klimanskaya I., McMahon J., Atienza J., Witmyer J., Zucker J.P., Wang S., Morton C.C., McMahon A.P., Powers D., et al. Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 2004, 350:1353-1356.
26. Zhao J., Sun W., Cho H.M., Ouyang H., Li W., Lin Y., Do J., Zhang L., Ding S., Liu Y., et al. Integration and long distance axonal regeneration in the central nervous system from transplanted primitive neural stem cells. J Biol Chem 2013, 288:164-168.
27. van Gorp S., Leerink M., Kakinohana O., Platoshyn O., Santucci C., Galik J., Joosten E.A., Hruska-Plochan M., Goldberg D., Marsala S., et al. Amelioration of motor/sensory dysfunction and spasticity in a rat model of acute lumbar spinal cord injury by human neural stem cell transplantation. Stem Cell Res Ther 2013, 4:57.
28. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
29. Tsuji O., Miura K., Okada Y., Fujiyoshi K., Mukaino M., Nagoshi N., Kitamura K., Kumagai G., Nishino M., Tomisato S., et al. Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proc Natl Acad Sci USA 2010, 107:12704-12709.
30. Nori S., Okada Y., Yasuda A., Tsuji O., Takahashi Y., Kobayashi Y., Fujiyoshi K., Koike M., Uchiyama Y., Ikeda E., et al. Grafted human-induced pluripotent stem-cell-derived neurospheres promote motor functional recovery after spinal cord injury in mice. Proc Natl Acad Sci USA 2011, 108:16825-16830.
31. Fujimoto Y., Abematsu M., Falk A., Tsujimura K., Sanosaka T., Juliandi B., Semi K., Namihira M., Komiya S., Smith A., et al. Treatment of a mouse model of spinal cord injury by transplantation of human induced pluripotent stem cell-derived long-term self-renewing neuroepithelial-like stem cells. Stem Cells 2012, 30:1163-1173.
32. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 1999, 5:1410-1412.
33. Sharp J., Frame J., Siegenthaler M., Nistor G., Keirstead H.S. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants improve recovery after cervical spinal cord injury. Stem Cells 2010, 28:152-163.
34. Liu S., Qu Y., Stewart T.J., Howard M.J., Chakrabortty S., Holekamp T.F., McDonald J.W. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci USA 2000, 97:6126-6131.
35. 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.
36. Kaiser J. Embryonic stem cells. Researchers mull impact of Geron's sudden exit from field. Science 2011, 334:1043.
37. Iwashita Y., Kawaguchi S., Murata M. Restoration of function by replacement of spinal cord segments in the rat. Nature 1994, 367:167-170.
38. Bregman B.S., McAtee M., Dai H.N., Kuhn P.L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp Neurol 1997, 148:475-494.
39. White T.E., Lane M.A., Sandhu M.S., O'Steen B.E., Fuller D.D., Reier P.J. Neuronal progenitor transplantation and respiratory outcomes following upper cervical spinal cord injury in adult rats. Exp Neurol 2010, 225:231-236.
40. Coumans J.V., Lin T.T., Dai H.N., MacArthur L., McAtee M., Nash C., Bregman B.S. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J Neurosci 2001, 21:9334-9344.
41. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr Opin Neurobiol 2010, 20:510-518.
42. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 2010, 13:1075-1081.
43. Blackmore M.G., Wang Z., Lerch J.K., Motti D., Zhang Y.P., Shields C.B., Lee J.K., Goldberg J.L., Lemmon V.P., Bixby J.L. Kruppel-like Factor 7 engineered for transcriptional activation promotes axon regeneration in the adult corticospinal tract. Proc Natl Acad Sci USA 2012, 109:7517-7522.
44. Lu P., Blesch A., Graham L., Wang Y., Samara R., Banos K., Haringer V., Havton L., Weishaupt N., Bennett D., et al. Motor axonal regeneration after partial and complete spinal cord transection. J Neurosci 2012, 32:8208-8218.
45. Gao M., Lu P., Bednark B., Lynam D., Conner J.M., Sakamoto J., Tuszynski M.H. Templated agarose scaffolds for the support of motor axon regeneration into sites of complete spinal cord transection. Biomaterials 2013, 34:1529-1536.
46. Canty A.J., Murphy M. Molecular mechanisms of axon guidance in the developing corticospinal tract. Prog Neurobiol 2008, 85:214-235.
47. Vinay L., Brocard F., Clarac F., Norreel J.C., Pearlstein E., Pflieger J.F. Development of posture and locomotion: an interplay of endogenously generated activities and neurotrophic actions by descending pathways. Brain Res Brain Res Rev 2002, 40:118-129.