Roles of ES cell-derived gliogenic neural stem/progenitor cells in functional recovery after spinal cord injury

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Kumagai, Gentaro ^a,b   Okada, Yohei ^a,c   Yamane, Junichi ^a   Nagoshi, Narihito ^a   Kitamura, Kazuya ^a   Mukaino, Masahiko ^a   Tsuji, Osahiko ^a   Fujiyoshi, Kanehiro ^a   Katoh, Hiroyuki ^a   Okada, Seiji ^d   Shibata, Shinsuke ^a   Matsuzaki, Yumi ^a   Toh, Satoshi ^b   Toyama, Yoshiaki ^a   Nakamura, Masaya ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; FUNCTIONAL STATUS; IN VITRO STUDY; LOCOMOTION; MOUSE; NERVE FIBER GROWTH; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; REMYELINIZATION; SPINAL CORD INJURY; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; CELL TRANSPLANTATION; CYTOLOGY; DISEASE MODEL; METABOLISM; METHODOLOGY; NEOVASCULARIZATION (PATHOLOGY); NERVE CELL; NERVE FIBER; PATHOLOGY; PATHOPHYSIOLOGY; STEM CELL; STEM CELL TRANSPLANTATION;

RODENTIA;

ANIMALS; AXONS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; FEMALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NEURONS; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 70450195049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007706     Document Type: Article

References (50)

1. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, et al. (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.
2. Iwanami A, Kaneko S, Nakamura M, Kanemura Y, Mori H, et al. (2005) Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 80: 182-190.
3. Okada S, Ishii K, Yamane J, Iwanami A, Ikegami T, et al. (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.
4. Hofstetter CP, Holmstrom NA, Lilja JA, Schweinhardt P, Hao J, et al. (2005) Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8: 346-353.
5. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, et al. (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.
6. Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, et al. (2004) Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 7: 1003-1009.
7. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, et al. (1999) Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5: 1410-1412.
8. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, et al. (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25: 4694-4705.
9. Okada Y, Shimazaki T, Sobue G, Okano H (2004) Retinoic-acid-concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev Biol 275: 124-142.
10. Okada Y, Matsumoto A, Shimazaki T, Enoki R, Koizumi A, et al. (2008) Spatio-Temporal Recapitulation of Central Nervous System Development By Murine ES Cell-Derived Neural Stem/Progenitor Cells. Stem Cells.
11. Zhao H, Doyle TC, Coquoz O, Kalish F, Rice BW, et al. (2005) Emission spectra of bioluminescent reporters and interaction with mammalian tissue determine the sensitivity of detection in vivo. J Biomed Opt 10: 41210.
12. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90.
13. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24: 372-376.
14. Wang X, Rosol M, Ge S, Peterson D, McNamara G, et al. (2003) Dynamic tracking of human hematopoietic stem cell engraftment using in vivo bioluminescence imaging. Blood 102: 3478-3482.
15. Contag CH, Bachmann MH (2002) Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng 4: 235-260.
16. Bregman BS (1987) Spinal cord transplants permit the growth of serotonergic axons across the site of neonatal spinal cord transection. Brain Res 431: 265-279.
17. Saruhashi Y, Young W, Perkins R (1996) The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp Neurol 139: 203-213.
18. Ramon-Cueto A, Plant GW, Avila J, Bunge MB (1998) Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 18: 3803-3815.
19. Kaneko S, Iwanami A, Nakamura M, Kishino A, Kikuchi K, et al. (2006) A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat Med 12: 1380-1389.
20. Kobayashi NR, Fan DP, Giehl KM, Bedard AM, Wiegand SJ, et al. (1997) BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Talpha1-tubulin mRNA expression, and promote axonal regeneration. J Neurosci 17: 9583-9595.
21. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, et al. (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23: 635-659.
22. Coutts M, Keirstead HS (2007) Stem cells for the treatment of spinal cord injury. Exp Neurol.
23. Temple S (2001) The development of neural stem cells. Nature 414: 112-117.
24. Fan G, Martinowich K, Chin MH, He F, Fouse SD, et al. (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAKSTAT signaling. Development 132: 3345-3356.
25. Shimozaki K, Namihira M, Nakashima K, Taga T (2005) Stage- and site-specific DNA demethylation during neural cell development from embryonic stem cells. J Neurochem 93: 432-439.
26. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, et al. (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758.
27. Winkler C, Fricker RA, Gates MA, Olsson M, Hammang JP, et al. (1998) Incorporation and glial differentiation of mouse EGF-responsive neural progenitor cells after transplantation into the embryonic rat brain. Mol Cell Neurosci 11: 99-116.
28. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, et al. (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.
29. Hill CE, Proschel C, Noble M, Mayer-Proschel M, Gensel JC, et al. (2004) Acute transplantation of glial-restricted precursor cells into spinal cord contusion injuries: survival, differentiation, and effects on lesion environment and axonal regeneration. Exp Neurol 190: 289-310.
30. Cao Q, Xu XM, Devries WH, Enzmann GU, Ping P, et al. (2005) Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J Neurosci 25: 6947-6957.
31. Davies JE, Huang C, Proschel C, Noble M, Mayer-Proschel M, et al. (2006) Astrocytes derived from glial-restricted precursors promote spinal cord repair. J Biol 5: 7.
32. Baehr M, Bunge RP (1990) Growth of adult rat retinal ganglion cell neurites on astrocytes. Glia 3: 293-300.
33. Noble M, Fok-Seang J, Cohen J (1984) Glia are a unique substrate for the in vitro growth of central nervous system neurons. J Neurosci 4: 1892-1903.
34. Tang X, Davies JE, Davies SJ (2003) Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 71: 427-444.
35. Bundesen LQ, Scheel TA, Bregman BS, Kromer LF (2003) Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J Neurosci 23: 7789-7800.
36. De Winter F, Oudega M, Lankhorst AJ, Hamers FP, Blits B, et al. (2002) Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp Neurol 175: 61-75.
37. Moreau-Fauvarque C, Kumanogoh A, Camand E, Jaillard C, Barbin G, et al. (2003) The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 23: 9229-9239.
38. Berry M, Maxwell WL, Logan A, Mathewson A, McConnell P, et al. (1983) Deposition of scar tissue in the central nervous system. Acta Neurochir Suppl (Wien) 32: 31-53.
39. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki T, et al. (2006) Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12: 829-834.
40. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, et al. (2008) Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 105: 3581-3586.
41. Blondel O, Collin C, McCarran WJ, Zhu S, Zamostiano R, et al. (2000) A glia-derived signal regulating neuronal differentiation. J Neurosci 20: 8012-8020.
42. Gallo V, Bertolotto A (1990) Extracellular matrix of cultured glial cells: selective expression of chondroitin 4-sulfate by type-2 astrocytes and their progenitors. Exp Cell Res 187: 211-223.
43. 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.
44. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, et al. (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148: 453-463.
45. Mense SM, Sengupta A, Zhou M, Lan C, Bentsman G, et al. (2006) Gene expression profiling reveals the profound upregulation of hypoxia-responsive genes in primary human astrocytes. Physiol Genomics 25: 435-449.
46. Yoshida H, Imaizumi T, Tanji K, Matsumiya T, Sakaki H, et al. (2002) Platelet-activating factor enhances the expression of vascular endothelial growth factor in normal human astrocytes. Brain Res 944: 65-72.
47. Liu S, Qu Y, Stewart TJ, Howard MJ, Chakrabortty S, et al. (2000) Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci U S A 97: 6126-6131.
48. Hooper M, Hardy K, Handyside A, Hunter S, Monk M (1987) HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 326: 292-295.
49. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE, Jr. (2003) Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 20: 179-193.
50. Rice BW, Cable MD, Nelson MB (2001) In vivo imaging of light-emitting probes. J Biomed Opt 6: 432-440.