Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets

Journal of Neuroscience Research

Volumn 88, Issue 7, 2010, Pages 1394-1405

  Yamane, Junichi ^a   Nakamura, Masaya ^a   Iwanami, Akio ^a,b   Sakaguchi, Masanori ^a   Katoh, Hiroyuki ^a,b   Yamada, Masayuki ^c,d   Momoshima, Suketaka ^a   Miyao, Sachiyo ^a   Ishii, Ken ^a   Tamaoki, Norikazu ^c   Nomura, Tatsuji ^c   Okano, Hirotaka James ^a   Kanemura, Yonehiro ^e   Toyama, Yoshiaki ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION MURAYAMA MEDICAL CENTER   (Japan)

^c CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^d FUJITA HEALTH UNIVERSITY   (Japan)

^e NATIONAL HOSPITAL ORGANIZATION   (Japan)

Author keywords

Common marmoset; Galectin 1; Neural stem progenitor cells; Preclinical study; Spinal cord injury

Indexed keywords

GALECTIN 1; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; EXERCISE RECOVERY; FEMALE; GRIP STRENGTH; HUMAN; IN VITRO STUDY; MARMOSET; MOTOR PERFORMANCE; NERVE FIBER GROWTH; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD INJURY; TREADMILL EXERCISE;

ANIMALS; ASTROCYTES; CALLITHRIX; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; FEMALE; GALECTIN 1; GRAFT SURVIVAL; GREEN FLUORESCENT PROTEINS; NERVE REGENERATION; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; OLIGODENDROGLIA; PARALYSIS; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSFECTION; TREATMENT OUTCOME;

EID: 77952044022     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22322     Document Type: Article

References (64)

1. Amariglio N, Hirshberg A, Scheithauer BW, Cohen Y, Loewenthal R, Trakhtenbrot L, Paz N, Koren-Michowitz M, Waldman D, Leider-Trejo L, Toren A, Constantini S, Rechavi G. 2009. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 6:e1000029.
2. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, Hoffman RM. 2005. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A 102:17734-17738. (Pubitemid 41803566)
3. Amoh Y, Li L, Katsuoka K, Hoffman RM. 2008. Multipotent hair follicle stem cells promote repair of spinal cord injury and recovery of walking function. Cell Cycle 7:1865-1869. (Pubitemid 351988753)
4. Arnhold S, Klein H, Semkova I, Addicks K, Schraermeyer U. 2004. Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space. Invest Ophthalmol Vis Sci 45:4251-4255. (Pubitemid 39564646)
5. Campbell EM, Hope TJ. 2005. Gene therapy progress and prospects: viral trafficking during infection. Gene Ther 12:1353-1359.
6. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR. 2001. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167:48-58. (Pubitemid 32066408)
7. Chung S, Shin BS, Hwang M, Lardaro T, Kang UJ, Isacson O, Kim KS. 2006. Neural precursors derived from embryonic stem cells, but not those from fetal ventral mesencephalon, maintain the potential to differentiate into dopaminergic neurons after expansion in vitro. Stem Cells 24:1583-1593. (Pubitemid 44464676)
8. Consiglio A, Gritti A, Dolcetta D, Follenzi A, Bordignon C, Gage FH, Vescovi AL, Naldini L. 2004. Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc Natl Acad Sci U S A 101:14835-14840. (Pubitemid 39410761)
9. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, Gage FH, Anderson AJ. 2005. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102:14069-14074. (Pubitemid 41377704)
10. David S, Lacroix S. 2003. Molecular approaches to spinal cord repair. Annu Rev Neurosci 26:411-440. (Pubitemid 37064940)
11. Englund U, Ericson C, Rosenblad C, Mandel RJ, Trono D, Wictorin K, Lundberg C. 2000. The use of a recombinant lentiviral vector for ex vivo gene transfer into the rat CNS. Neuroreport 11:3973-3977. (Pubitemid 32038787)
12. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L. 2002. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 99:2199-2204. (Pubitemid 34169038)
13. Horie H, Inagaki Y, Sohma Y, Nozawa R, Okawa K, Hasegawa M, Muramatsu N, Kawano H, Horie M, Koyama H, Sakai I, Takeshita K, Kowada Y, Takano M, Kadoya T. 1999. Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J Neurosci 19:9964-9974. (Pubitemid 30226668)
14. Horner PJ, Gage FH. 2000. Regenerating the damaged central nervous system. Nature 407:963-970.
15. Ishibashi S, Sakaguchi M, Kuroiwa T, Yamasaki M, Kanemura Y, Shizuko I, Shimazaki T, Onodera M, Okano H, Mizusawa H. 2004. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 78:215-223. (Pubitemid 39313794)
16. Ishibashi S, Kuroiwa T, Sakaguchi M, Sun L, Kadoya T, Okano H, Mizusawa H. 2007. Galectin-1 regulates neurogenesis in the subventricular zone and promotes functional recovery after stroke. Exp Neurol 207:302-313. (Pubitemid 47440093)
17. Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, Kobayashi S, Yamasaki M, Momoshima S, Ishii H, Ando K, Tanioka Y, Tamaoki N, Nomura T, Toyama Y, Okano H. 2005a. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 80:182-190. (Pubitemid 40676302)
18. Iwanami A, Yamane J, Katoh H, Nakamura M, Momoshima S, Ishii H, Tanioka Y, Tamaoki N, Nomura T, Toyama Y, Okano H. 2005b. Establishment of graded spinal cord injury model in a nonhuman primate: the common marmoset. J Neurosci Res 80:172-181. (Pubitemid 40676301)
19. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34. (Pubitemid 29044150)
20. Kajitani K, Nomaru H, Ifuku M, Yutsudo N, Dan Y, Miura T, Tsuchimoto D, Sakumi K, Kadoya T, Horie H, Poirier F, Noda M, Nakabeppu Y. 2009. Galectin-1 promotes basal and kainate-induced proliferation of neural progenitors in the dentate gyrus of adult mouse hippocampus. Cell Death Differ 16:417-427.
21. Kanemura Y, Mori H, Kobayashi S, Islam O, Kodama E, Yamamoto A, Nakanishi Y, Arita N, Yamasaki M, Okano H, Hara M, Miyake J. 2002. Evaluation of in vitro proliferative activity of human fetal neural stem/progenitor cells using indirect measurements of viable cells based on cellular metabolic activity. J Neurosci Res 69:869-879. (Pubitemid 34984704)
22. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. 2005. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705. (Pubitemid 40664118)
23. Koda M, Murakami M, Ino H, Yoshinaga K, Ikeda O, Hashimoto M, Yamazaki M, Nakayama C, Moriya H. 2002. Brain-derived neurotrophic factor suppresses delayed apoptosis of oligodendrocytes after spinal cord injury in rats. J Neurotrauma 19:777-785. (Pubitemid 34761339)
24. Li L, Mignone J, Yang M, Matic M, Penman S, Enikolopov G, Hoffman RM. 2003. Nestin expression in hair follicle sheath progenitor cells. Proc Natl Acad Sci U S A 100:9958-9961. (Pubitemid 37087050)
25. Li X, Xu J, Bai Y, Wang X, Dai X, Liu Y, Zhang J, Zou J, Shen L, Li L. 2005. Isolation and characterization of neural stem cells from human fetal striatum. Biochem Biophys Res Commun 326:425-434. (Pubitemid 39593564)
26. Li Y, Field PM, Raisman G. 1997. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000-2002. (Pubitemid 27449143)
27. Mahanthappa NK, Cooper DN, Barondes SH, Schwarting GA. 1994. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 120:1373-1384.
28. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW. 1999. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5:1410-1412.
29. Metz GA, Curt A, van de Meent H, Klusman I, Schwab ME, Dietz V. 2000. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 17:1-17. (Pubitemid 30075612)
30. Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita K, Nakagawa M, Koyanagi M, Tanabe K, Ohnuki M, Ogawa D, Ikeda E, Okano H, Yamanaka S. 2009. Variation in the safety of inducedpluripotent stem cell lines. Nat Biotechnol [July 9 E-pub ahead of print].
31. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. 1998. Development of a self-inactivating lentivirus vector. J Virol 72:8150-8157.
32. Moiseeva EP, Williams B, Goodall AH, Samani NJ. 2003. Galectin-1 interacts with beta-1 subunit of integrin. Biochem Biophys Res Commun 310:1010-1016. (Pubitemid 37188723)
33. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90. (Pubitemid 34044921)
34. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS. 2003. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 184:313-325. (Pubitemid 37444041)
35. Nakamura M, Okano H, Toyama Y, Dai HN, Finn TP, Bregman BS. 2005. Transplantation of embryonic spinal cord-derived neurospheres support growth of supraspinal projections and functional recovery after spinal cord injury in the neonatal rat. J Neurosci Res 81:457-468. (Pubitemid 41297383)
36. Namiki J, Kojima A, Tator CH. 2000. Effect of brain-derived neurotrophic factor, nerve growth factor, and neurotrophin-3 on functional recovery and regeneration after spinal cord injury in adult rats. J Neurotrauma 17:1219-1231.
37. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, Nakamura M, Bregman BS, Koike M, Uchiyama Y, Toyama Y, Okano H. 2002. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 69:925-933. (Pubitemid 34984709)
38. Ohta K, Fujimura Y, Nakamura M, Watanabe M, Yato Y. 1999. Experimental study on MRI evaluation of the course of cervical spinal cord injury. Spinal Cord 37:580-584. (Pubitemid 29385203)
39. Okada S, Ishii K, Yamane J, Iwanami A, Ikegami T, Katoh H, Iwamoto Y, Nakamura M, Miyoshi H, Okano HJ, Contag CH, Toyama Y, Okano H. 2005. In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J 19:1839-1841.
40. Okano H. 2002a. Neural stem cells: progression of basic research and perspective for clinical application. Keio J Med 51:115-128.
41. Okano H. 2002b. Stem cell biology of the central nervous system. J Neurosci Res 69:698-707. (Pubitemid 34984686)
42. Okano HJ, Darnell RB. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
43. Okano H, Ogawa Y, Nakamura M, Kaneko S, Iwanami A, Toyama Y. 2003. Transplantation of neural stem cells into the spinal cord after injury. Semin Cell Dev Biol 14:191-198. (Pubitemid 38160914)
44. Olson L. 2002. Medicine: clearing a path for nerve growth. Nature 416:589-590. (Pubitemid 34406740)
45. Outenreath RL, Jones AL. 1992. Influence of an endogenous lectin substrate on cultured dorsal root ganglion cells. J Neurocytol 21:788-795.
46. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. 1995. Apoptosis of T cells mediated by galectin-1. Nature 378:736-739.
47. Perillo NL, Marcus ME, Baum LG. 1998. Galectins: versatile modulators of cell adhesion, cell proliferation, and cell death. J Mol Med 76:402-412.
48. Puche AC, Poirier F, Hair M, Bartlett PF, Key B. 1996. Role of galectin-1 in the developing mouse olfactory system. Dev Biol 179:274-287. (Pubitemid 26363263)
49. Rabinovich GA, Alonso CR, Sotomayor CE, Durand S, Bocco JL, Riera CM. 2000a. Molecular mechanisms implicated in galectin-1-induced apoptosis: activation of the AP-1 transcription factor and downregulation of Bcl-2. Cell Death Differ 7:747-753. (Pubitemid 30599255)
50. Rabinovich GA, Sotomayor CE, Riera CM, Bianco I, Correa SG. 2000b. Evidence of a role for galectin-1 in acute inflammation. Eur J Immunol 30:1331-1339. (Pubitemid 30311962)
51. Rabinovich GA, Baum LG, Tinari N, Paganelli R, Natoli C, Liu FT, Iacobelli S. 2002. Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol 23:313-320.
52. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. 2002. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298:597-600.
53. Reynolds BA, Weiss S. 1996. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13. (Pubitemid 26150042)
54. Sakaguchi M, Shingo T, Shimazaki T, Okano HJ, Shiwa M, Ishibashi S, Oguro H, Ninomiya M, Kadoya T, Horie H, Shibuya A, Mizusawa H, Poirier F, Nakauchi H, Sawamoto K, Okano H. 2006. A carbohydratebinding protein, galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci U S A 103:7112-7117.
55. Schwab ME. 2002. Repairing the injured spinal cord. Science 295:1029-1031.
56. Silva WA Jr, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL, Santos AR, Zago MA. 2003. The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 21:661-669. (Pubitemid 37329159)
57. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
58. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676. (Pubitemid 44233629)
59. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. 2004. Defining the epithelial stem cell niche in skin. Science 303:359-363. (Pubitemid 38095773)
60. Vas V, Fajka-Boja R, Ion G, Dudics V, Monostori E, Uher F. 2005. Biphasic effect of recombinant galectin-1 on the growth and death of early hematopoietic cells. Stem Cells 23:279-287. (Pubitemid 40239522)
61. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, Soldner F, Broccoli V, Constantine-Paton M, Isacson O, Jaenisch R. 2008. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A 105:5856-5861. (Pubitemid 351758462)
62. Widenfalk J, Lundstromer K, Jubran M, Brene S, Olson L. 2001. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21:3457-3475. (Pubitemid 32422810)
63. Yoshizaki T, Inaji M, Kouike H, Shimazaki T, Sawamoto K, Ando K, Date I, Kobayashi K, Suhara T, Uchiyama Y, Okano H. 2004. Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells. Neurosci Lett 363:33-37. (Pubitemid 38659556)
64. Young LS, Searle PF, Onion D, Mautner V. 2006. Viral gene therapy strategies: from basic science to clinical application. J Pathol 208:299-318. (Pubitemid 43126122)