Critical involvement of Rho GTPase activity in the efficient transplantation of neural stem cells into the injured spinal cord

Molecular Brain

Volumn 2, Issue 1, 2009, Pages

  Numano, Fujiki ^a,b   Inoue, Akihiro ^a   Enomoto, Mitsuhiro ^b   Shinomiya, Kenichi ^b   Okawa, Atsushi ^b   Okabe, Shigeo ^a,c  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CDC42; RAC PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 2; STAUROSPORINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LINEAGE; CELL MIGRATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; GENETIC MANIPULATION; IMMUNOHISTOCHEMISTRY; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; TREATMENT OUTCOME; ADENOVIRUS; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; NEURAL STEM CELL; PATHOLOGY; SPINAL CORD; SPRAGUE DAWLEY RAT; STEM CELL TRANSPLANTATION; TRANSPLANTATION; VIROLOGY;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; FIBROBLAST GROWTH FACTOR 2; MUTATION; NEURAL STEM CELLS; RAC GTP-BINDING PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RHO GTP-BINDING PROTEINS; SPINAL CORD; SPINAL CORD INJURIES; STAUROSPORINE; STEM CELL TRANSPLANTATION;

EID: 72849150898     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-2-37     Document Type: Article

References (58)

1. Mammalian neural stem cells. FH Gage, Science 2000 287 1433 1438 10.1126/science.287.5457.1433 10688783
2. Stem cell biology and neurodegenerative disease. RD McKay, Philos Trans R Soc Lond B Biol Sci 2004 359 851 856 15293812 10.1098/rstb.2004.1472 (Pubitemid 38673752)
3. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. KK Johe TG Hazel T Muller MM Dugich-Djordjevic RD McKay, Genes Dev 1996 10 3129 3140 10.1101/gad.10.24.3129 8985182
4. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. S Okabe K Forsberg-Nilsson AC Spiro M Segal RD McKay, Mech Dev 1996 59 89 102 10.1016/0925-4773(96)00572-2 8892235
5. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. O Brustle KN Jones RD Learish K Karram K Choudhary OD Wiestler ID Duncan RD McKay, Science 1999 285 754 756 10.1126/science.285.5428.754 10427001
6. Stem cell therapy for human neurodegenerative disorders-how to make it work. O Lindvall Z Kokaia A Martinez-Serrano, Nat Med 2004 10 Suppl 42 50 10.1038/nm1064 15272269
7. Rodent models for treatment of spinal cord injury: research trends and progress toward useful repair. ES Rosenzweig JW McDonald, Curr Opin Neurol 2004 17 121 131 10.1097/00019052-200404000-00007 15021237
8. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. JW McDonald XZ Liu Y Qu S Liu SK Mickey D Turetsky DI Gottlieb DW Choi, Nat Med 1999 5 1410 1412 10.1038/70986 10581084
9. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. Y Ogawa K Sawamoto T Miyata S Miyao M Watanabe M Nakamura BS Bregman M Koike Y Uchiyama Y Toyama H Okano, J Neurosci Res 2002 69 925 933 10.1002/jnr.10341 12205685
10. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. Q Cao XM Xu WH Devries GU Enzmann P Ping P Tsoulfas PM Wood MB Bunge SR Whittemore, J Neurosci 2005 25 6947 6957 10.1523/JNEUROSCI.1065-05.2005 16049170
11. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. HS Keirstead G Nistor G Bernal M Totoiu F Cloutier K Sharp O Steward, J Neurosci 2005 25 4694 4705 10.1523/JNEUROSCI.0311-05.2005 15888645
12. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. QL Cao YP Zhang RM Howard WM Walters P Tsoulfas SR Whittemore, Exp Neurol 2001 167 48 58 10.1006/exnr.2000. 7536 11161592
13. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. MS Beattie, Trends Mol Med 2004 10 580 583 10.1016/j.molmed.2004.10.006 15567326
14. Rho GTPases and the actin cytoskeleton. A Hall, Science 1998 279 509 514 10.1126/science.279.5350.509 9438836
15. Rho and Rac take center stage. K Burridge K Wennerberg, Cell 2004 116 167 179 10.1016/S0092-8674(04)00003-0 14744429
16. The small GTP-binding protein Cdc42 is required for nerve growth factor withdrawal-induced neuronal death. CE Bazenet MA Mota LL Rubin, Proc Natl Acad Sci USA 1998 95 3984 3989 9520479 10.1073/pnas.95.7.3984 (Pubitemid 28173240)
17. Role of apoptosis signal-regulating kinase in regulation of the c-Jun N-terminal kinase pathway and apoptosis in sympathetic neurons. T Kanamoto M Mota K Takeda LL Rubin K Miyazono H Ichijo CE Bazenet, Mol Cell Biol 2000 20 196 204 10594022 10.1128/MCB.20.1.196-204.2000
18. Activation of Rac GTPase by p75 is necessary for c-jun N-terminal kinase-mediated apoptosis. AW Harrington JY Kim SO Yoon, J Neurosci 2002 22 156 166 11756498
19. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. CI Dubreuil MJ Winton L McKerracher, J Cell Biol 2003 162 233 243 12860969 10.1083/jcb.200301080 (Pubitemid 36928837)
20. Migration and differentiation of neural progenitor cells from two different regions of embryonic central nervous system after transplantation into the intact spinal cord. M Enomoto K Shinomiya S Okabe, Eur J Neurosci 2003 17 1223 1232 10.1046/j.1460-9568.2003.02555.x 12670310
21. Rho kinase inhibition enhances axonal regeneration in the injured CNS. AE Fournier BT Takizawa SM Strittmatter, J Neurosci 2003 23 1416 1423 12598630
22. Inhibition of Rac GTPase triggers a c-Jun- and Bim-dependent mitochondrial apoptotic cascade in cerebellar granule neurons. SS Le FA Loucks H Udo S Richardson-Burns RA Phelps RJ Bouchard H Barth K Aktories KL Tyler ER Kandel KA Heidenreich DA Linseman, J Neurochem 2005 94 1025 1039 16092944 10.1111/j.1471-4159.2005.03252.x (Pubitemid 41170590)
23. Antibody against single-stranded DNA detects both programmed cell death and drug-induced apoptosis. I Naruse H Keino Y Kawarada, Histochemistry 1994 101 73 78 10.1007/BF00315834 7517929
24. Role of tumor necrosis factor-alpha in neuronal and glial apoptosis after spinal cord injury. YB Lee TY Yune SY Baik YH Shin S Du H Rhim EB Lee YC Kim ML Shin GJ Markelonis TH Oh, Exp Neurol 2000 166 190 195 10.1006/exnr.2000.7494 11031095
25. Control of synaptic strength by glial TNFalpha. EC Beattie D Stellwagen W Morishita JC Bresnahan BK Ha M Von Zastrow MS Beattie RC Malenka, Science 2002 295 2282 2285 10.1126/science.1067859 11910117
26. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. DD Pearse FC Pereira AE Marcillo ML Bates YA Berrocal MT Filbin MB Bunge, Nat Med 2004 10 610 616 10.1038/nm1056 15156204
27. Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. M Nakamura RA Houghtling L MacArthur BM Bayer BS Bregman, Exp Neurol 2003 184 313 25 10.1016/S0014-4886(03)00361-3 14637102
28. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. AE Fournier T GrandPre SM Strittmatter, Nature 2001 409 341 346 10.1038/35053072 11201742
29. p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. KC Wang JA Kim R Sivasankaran R Segal Z He, Nature 2002 420 74 78 10.1038/nature01176 12422217
30. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. S Mi X Lee Z Shao G Thill B Ji J Relton M Levesque N Allaire S Perrin B Sands T Crowell RL Cate JM McCoy RB Pepinsky, Nat Neurosci 2004 7 221 228 10.1038/nn1188 14966521
31. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. T Yamashita KL Tucker YA Barde, Neuron 1999 24 585 593 10.1016/S0896-6273(00)81114-9 10595511
32. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. T Yamashita M Tohyama, Nat Neurosci 2003 6 461 467 12692556
33. The role of the Rho GTPases in neuronal development. EE Govek SE Newey L Van Aelst, Genes Dev 2005 19 1 49 10.1101/gad.1256405 15630019
34. Rho and Rac take center stage. K Burridge K Wennerberg, Cell 2004 116 167 79 10.1016/S0092-8674(04)00003-0 14744429
35. Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. K Jalink WH Moolenaar, J Cell Biol 1992 118 411 419 1321160 10.1083/jcb.118.2.411
36. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. K Jalink EJ van Corven T Hengeveld N Morii S Narumiya WH Moolenaar, J Cell Biol 1994 126 801 810 8045941 10.1083/jcb.126.3.801 (Pubitemid 24241391)
37. Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. S Srinivasan F Wang S Glavas A Ott F Hofmann K Aktories D Kalman HR Bourne, J Cell Biol 2003 160 375 385 12551955 10.1083/jcb.200208179 (Pubitemid 36182728)
38. Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement. AT Sasaki C Chun K Takeda RA Firtel, J Cell Biol 2004 167 505 518 15534002 10.1083/jcb.200406177 (Pubitemid 39489058)
39. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. ES Ang Jr TF Haydar V Gluncic P Rakic, J Neurosci 2003 23 5805 5815 12843285
40. Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. D Tanaka Y Nakaya Y Yanagawa K Obata F Murakami, Development 2003 130 5803 5813 10.1242/dev.00825 14534141
41. Direct visualization of cell movement in the embryonic olfactory bulb using green fluorescent protein transgenic mice: evidence for rapid tangential migration of neural cell precursors. K Yamamoto M Yamaguchi S Okabe, Neurosci Res 2005 51 199 214 10.1016/j.neures.2004.11.003 15681037
42. Chondroitinase ABC combined with neural stem/progenitor cell transplantationenhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. T Ikegami M Nakamura J Yamane H Katoh S Okada A Iwanami K Watanabe K Ishii F Kato H Fujita T Takahashi HJ Okano Y Toyama H Okano, Eur J Neurosci 2005 22 3036 46 10.1111/j.1460-9568. 2005.04492.x 16367770
43. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. M Kerschensteiner ME Schwab JW Lichtman T Misgeld, Nat Med 2005 11 572 577 10.1038/nm1229 15821747
44. In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. S Okada K Ishii J Yamane A Iwanami T Ikegami H Katoh Y Iwamoto M Nakamura H Miyoshi HJ Okano CH Contag Y Toyama H Okano, FASEB J 2005 19 1839 1841 16141363
45. Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. FC Yang SJ Atkinson Y Gu JB Borneo AW Roberts Y Zheng J Pennington DA Williams, Proc Natl Acad Sci USA 2001 98 5614 5618 11320224 10.1073/pnas.101546898 (Pubitemid 32435690)
46. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Y Gu MD Filippi JA Cancelas JE Siefring EP Williams AC Jasti CE Harris AW Lee R Prabhakar SJ Atkinson DJ Kwiatkowski DA Williams, Science 2003 302 445 449 10.1126/science.1088485 14564009
47. Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. JA Cancelas AW Lee R Prabhakar KF Stringer Y Zheng DA Williams, Nat Med 2005 11 886 891 10.1038/nm1274 16025125
48. Stem cell depletion through epidermal deletion of Rac1. SA Benitah M Frye M Glogauer FM Watt, Science 2005 309 933 935 10.1126/science.1113579 16081735
49. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. R Sordella W Jiang GC Chen M Curto J Settleman, Cell 2003 113 147 158 10.1016/S0092-8674(03)00271-X 12705864
50. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. R McBeath DM Pirone CM Nelson K Bhadriraju CS Chen, Dev Cell 2004 6 483 495 10.1016/S1534-5807(04)00075-9 15068789
51. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. QL Cao YP Zhang RM Howard WM Walters P Tsoulfas SR Whittemore, Exp Neurol 2001 167 48 58 10.1006/exnr.2000. 7536 11161592
52. Ciliary neurotrophic factor may activate mature astrocytes via binding with the leukemia inhibitory factor receptor. C Monville M Coulpier L Conti C De-Fraja P Dreyfus C Fages D Riche M Tardy E Cattaneo M Peschanski, Mol Cell Neurosci 2001 17 373 84 10.1006/mcne.2000.0926 11178874
53. Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. S Okada M Nakamura H Katoh T Miyao T Shimazaki K Ishii J Yamane A Yoshimura Y Iwamoto Y Toyama H Okano, Nat Med 2006 12 829 34 10.1038/nm1425 16783372
54. Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. RB Tripathi DM McTigue, J Comp Neurol 2008 510 129 44 10.1002/cne.21787 18615534
55. Notch signaling in the mammalian central nervous system: insights from mouse mutants. K Yoon N Gaiano, Nat Neurosci 2005 8 709 15 10.1038/nn1475 15917835
56. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. JE Bottenstein GH Sato, Proc Natl Acad Sci USA 1979 76 514 517 284369 10.1073/pnas.76.1.514
57. Cell death in adult neural stem cells. E Sleeper C Tamm J Frisén B Zhivotovsky S Orrenius S Ceccatelli, Cell Death Differ 2002 9 1377 8 10.1038/sj.cdd.4401127 12478475
58. Efficient selection for high-expression transfectants with a novel eukaryotic vector. H Niwa K Yamamura J Miyazaki, Gene 1991 108 193 199 10.1016/0378-1119(91)90434-D 1660837