Endogenous proliferation after spinal cord injury in animal models

Stem Cells International

Volumn , Issue , 2012, Pages

  McDonough, Ashley ^a,b   Martínez Cerdeño, Verónica ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PAX7;

ASTROCYTE; CELL FATE; CELL MANIPULATION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTUSION; DISEASE MODEL; EPENDYMA CELL; EXPERIMENTAL ANIMAL; HUMAN; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLIGODENDROCYTE PROGENITOR CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SPINAL CORD COMPRESSION; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; STEM CELL TRANSPLANTATION;

ANIMALIA;

EID: 84872145726     PISSN: None     EISSN: 16879678     Source Type: Journal    
DOI: 10.1155/2012/387513     Document Type: Review

References (132)

1. Beattie M. S., Bresnahan J. C., Komon J., Tovar C. A., Van Meter M., Anderson D. K., Faden A. I., Hsu C. Y., Noble L. J., Salzman S., Young W., Endogenous repair after spinal cord contusion injuries in the rat. Experimental Neurology 1997 148 2 453 463 2-s2.0-0031431557 10.1006/exnr.1997.6695 (Pubitemid 28068841)
2. 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. The Journal of Neuroscience 1996 16 23 7599 7609 2-s2.0-0029860591 (Pubitemid 26389699)
3. Barnabé-Heider F., Göritz C., Sabelström H., Takebayashi H., Pfrieger F. W., Meletis K., Frisén J., Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010 7 4 470 482 2-s2.0-77957331909 10.1016/j.stem.2010.07.014
4. 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. The Journal of Neuroscience 2000 20 6 2218 2228 2-s2.0-0034653399 (Pubitemid 30230075)
5. Bareyre F. M., Neuronal repair and replacement in spinal cord injury. Journal of the Neurological Sciences 2008 265 1-2 63 72 2-s2.0-37849006879 10.1016/j.jns.2007.05.004
6. Gross C. G., Neurogenesis in the adult brain: death of a dogma. Nature Reviews 2000 1 1 67 73 2-s2.0-0034304948
7. Kehl L. J., Fairbanks C. A., Laughlin T. M., Wilcox G. L., Neurogenesis in postnatal rat spinal cord: a study in primary culture. Science 1997 276 5312 586 589 2-s2.0-0030971385 10.1126/science.276.5312.586 (Pubitemid 27193681)
8. Johansson C. B., Momma S., Clarke D. L., Risling M., Lendahl U., Frisén J., Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999 96 1 25 34 2-s2.0-0033534379 10.1016/S0092-8674(00)80956-3 (Pubitemid 29044150)
9. Vaquero J., Ramiro M. J., Oya S., Cabezudo J. M., Ependymal reaction after experimental spinal cord injury. Acta Neurochirurgica 1981 55 3-4 295 302 2-s2.0-0019427808 (Pubitemid 11114859)
10. Vaquero J., Ramiro M. J., Oya S., Manuel Cabezudo J., Ependymal cell proliferation after spinal cord injury. Surgical Neurology 1987 28 5, article 401 2-s2.0-17044460401
11. Bretzner F., Liu J., Currie E., Roskams A. J., Tetzlaff W., Undesired effects of a combinatorial treatment for spinal cord injury-transplantation of olfactory ensheathing cells and BDNF infusion to the red nucleus. European Journal of Neuroscience 2008 28 9 1795 1807 2-s2.0-54849409681 10.1111/j.1460-9568.2008.06462.x
12. Gomes W. A., Mehler M. F., Kessler J. A., Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Developmental Biology 2003 255 1 164 177 2-s2.0-0037333616 10.1016/S0012- 1606(02)00037-4 (Pubitemid 36287148)
13. McTigue D. M., Horner P. J., Stokes B. T., Gage F. H., Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. The Journal of Neuroscience 1998 18 14 5354 5365 2-s2.0-0032528159 (Pubitemid 28311952)
14. Arvanian V. L., Horner P. J., Gage F. H., Mendell L. M., Chronic neurotrophin-3 strengthens synaptic connections to motoneurons in the neonatal rat. The Journal of Neuroscience 2003 23 25 8706 8712 2-s2.0-0141535172 (Pubitemid 37176651)
15. Rong W., Wang J., Liu X., Jiang L., Wei F., Hu X., Han X., Liu Z., Naringin treatment improves functional recovery by increasing BDNF and VEGF expression, inhibiting neuronal apoptosis after spinal cord injury. Neurochemical Research 2012 37 8 1615 1623 2-s2.0-84864376057 10.1007/s11064-012-0756-7
16. Ohori Y., Yamamoto S. I., Nagao M., Sugimori M., Yamamoto N., Nakamura K., Nakafuku M., Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. The Journal of Neuroscience 2006 26 46 11948 11960 2-s2.0-33751102129 10.1523/JNEUROSCI.3127-06.2006 (Pubitemid 44772106)
17. Lytle J. M., Chittajallu R., Wrathall J. R., Gallo V., NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 2009 57 3 270 285 2-s2.0-65149090344 10.1002/glia.20755
18. Sellers D. L., Maris D. O., Horner P. J., Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. The Journal of Neuroscience 2009 29 20 6722 6733 2-s2.0-66249132705 10.1523/JNEUROSCI.4538-08.2009
19. Barritt A. W., Davies M., Marchand F., Hartley R., Grist J., Yip P., McMahon S. B., Bradbury E. J., Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. The Journal of Neuroscience 2006 26 42 10856 10867 2-s2.0-33750932815 10.1523/JNEUROSCI.2980-06.2006
20. Bradbury E. J., Moon L. D. F., Popat R. J., King V. R., Bennett G. S., Patel P. N., Fawcett J. W., McMahon S. B., Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002 416 6881 636 640 2-s2.0-0037061426 10.1038/416636a (Pubitemid 34406764)
21. Rowland J. W., Hawryluk G. W., Kwon B., Fehlings M. G., Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurgical Focus 2008 25 5, article E2 2-s2.0-63849340879
22. Ruff R. L., McKerracher L., Selzer M. E., Repair and neurorehabilitation strategies for spinal cord injury. Annals of the New York Academy of Sciences 2008 1142 1 20 2-s2.0-54949105397 10.1196/annals.1444.004
23. Tu J., Liao J., Stoodley M. A., Cunningham A. M., Differentiation of endogenous progenitors in an animal model of post-traumatic syringomyelia. Spine 2010 35 11 1116 1121 2-s2.0-77952427884 10.1097/BRS.0b013e3181ba6ce4
24. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M. E., Rouiller E. M., Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nature Medicine 2006 12 7 790 792 2-s2.0-33745879440 10.1038/nm1436 (Pubitemid 44050068)
25. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M. E., Rouiller E. M., Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates-re-examination and extension of behavioral data. European Journal of Neuroscience 2009 29 5 983 996 2-s2.0-61449199550 10.1111/j.1460-9568.2009.06642.x
26. Spinal Cord Injury Facts and Figures at a Glance 2011 Birgminham, Ala, USA National Spinal Cord Injury Statistical Center
27. Hawryluk G. W., Rowland J., Kwon B. K., Fehlings M. G., Protection and repair of the injured spinal cord: a review of completed, ongoing, and planned clinical trials for acute spinal cord injury. Neurosurgical Focus 2008 25 5, article E14 2-s2.0-63849186608
28. Yamamoto S. I., Yamamoto N., Kitamura T., Nakamura K., Nakafuku M., Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Experimental Neurology 2001 172 1 115 127 2-s2.0-0035214298 10.1006/exnr.2001.7798 (Pubitemid 33141159)
29. Mothe A. J., Tator C. H., Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 2005 131 1 177 187 2-s2.0-12844282237 10.1016/j.neuroscience.2004.10.011 (Pubitemid 40170498)
30. Horky L. L., Galimi F., Gage F. H., Horner P. J., Fate of endogenous stem/progenitor cells following spinal cord injury. Journal of Comparative Neurology 2006 498 4 525 538 2-s2.0-33747157935 10.1002/cne.21065 (Pubitemid 44232692)
31. Yang H., Lu P., McKay H. M., Bernot T., Keirstead H., Steward O., Gage F. H., Edgerton V. R., Tuszynski M. H., Endogenous neurogenesis replaces oligodendrocytes and astrocytes after primate spinal cord injury. The Journal of Neuroscience 2006 26 8 2157 2166 2-s2.0-33645635809 10.1523/JNEUROSCI.4070-05. 2005 (Pubitemid 44699024)
32. Meletis K., Barnabé-Heider F., Carlén M., Evergren E., Tomilin N., Shupliakov O., Frisén J., Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biology 2008 6 7, article e182 2-s2.0-51049112750 10.1371/journal.pbio.0060182
33. McTigue D. M., Wei P., Stokes B. T., Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. The Journal of Neuroscience 2001 21 10 3392 3400 2-s2.0-0035873062 (Pubitemid 32422804)
34. Takahashi M., Arai Y., Kurosawa H., Sueyoshi N., Shirai S., Ependymal cell reactions in spinal cord segments after compression injury in adult rat. Journal of Neuropathology and Experimental Neurology 2003 62 2 185 194 2-s2.0-0037315974 (Pubitemid 36176953)
35. Zai L. J., Yoo S., Wrathall J. R., Increased growth factor expression and cell proliferation after contusive spinal cord injury. Brain Research 2005 1052 2 147 155 2-s2.0-23644450196 10.1016/j.brainres.2005.05.071 (Pubitemid 41116772)
36. Lytle J. M., Wrathall J. R., Glial cell loss, proliferation and replacement in the contused murine spinal cord. European Journal of Neuroscience 2007 25 6 1711 1724 2-s2.0-34047245282 10.1111/j.1460-9568.2007.05390.x (Pubitemid 46549992)
37. Namiki J., Tator C. H., Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. Journal of Neuropathology and Experimental Neurology 1999 58 5 489 498 2-s2.0-0032895971 (Pubitemid 29220742)
38. Wu D., Shibuya S., Miyamoto O., Itano T., Yamamoto T., Increase of NG2-positive cells associated with radial glia following traumatic spinal cord injury in adult rats. Journal of Neurocytology 2005 34 6 459 469 2-s2.0-56249136550 10.1007/s11068-006-8998-4 (Pubitemid 44252077)
39. Eftekharpour E., Karimi-Abdolrezaee S., Fehlings M. G., Current status of experimental cell replacement approaches to spinal cord injury. Neurosurgical Focus 2008 24 3-4, article E18 2-s2.0-42149092238 10.3171/FOC/2008/24/3-4/E17
40. Kwon B. K., Stammers A. M. T., Belanger L. M., Bernardo A., Chan D., Bishop C. M., Slobogean G. P., Zhang H., Umedaly H., Giffin M., Street J., Boyd M. C., Paquette S. J., Fisher C. G., Dvorak M. F., Cerebrospinal fluid inflammatory cytokines and biomarkers of injury severity in acute human spinal cord injury. Journal of Neurotrauma 2010 27 4 669 682 2-s2.0-77951287743 10.1089/neu.2009.1080
41. Stammers A. T., Liu J., Kwon B. K., Expression of inflammatory cytokines following acute spinal cord injury in a rodent model. Journal of Neuroscience Research 2012 90 4 782 790 2-s2.0-84862179426 10.1002/jnr.22820
42. Grossman S. D., Rosenberg L. J., Wrathall J. R., Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Experimental Neurology 2001 168 2 273 282 2-s2.0-0035074297 10.1006/exnr.2001.7628 (Pubitemid 32289763)
43. Davies S. J. A., Shih C. H., Noble M., Mayer-Proschel M., Davies J. E., Proschel C., Transplantation of specific human astrocytes promotes functional recovery after spinal cord injury. PLoS ONE 2011 6 3 2-s2.0-79952284700 10.1371/journal.pone.0017328 e17328
44. Gensel J. C., Tovar C. A., Hamers F. P. T., Deibert R. J., Beattie M. S., Bresnahan J. C., Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. Journal of Neurotrauma 2006 23 1 36 54 2-s2.0-31944432224 10.1089/neu.2006.23.36 (Pubitemid 43191085)
45. Onifer S. M., Rabchevsky A. G., Scheff S. W., Rat models of traumatic spinal cord injury to assess motor recovery. ILAR Journal 2007 48 4 385 395 2-s2.0-36049040405 (Pubitemid 350194370)
46. Basso D. M., Beattie M. S., Bresnahan J. C., Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Experimental Neurology 1996 139 2 244 256 2-s2.0-0030157694 10.1006/exnr.1996.0098 (Pubitemid 26228093)
47. Plemel J. R., Duncan G., Chen K. W. K., Shannon C., Park S., Sparling J. S., Tetzlaff W., A graded forceps crush spinal cord injury model in mice. Journal of Neurotrauma 2008 25 4 350 370 2-s2.0-41449093906 10.1089/neu.2007. 0426 (Pubitemid 351457763)
48. Alvarez-Buylla A., Kohwi M., Nguyen T. M., Merkle F. T., The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harbor Symposia on Quantitative Biology 2008 73 357 365 2-s2.0-66549099504 10.1101/sqb.2008.73.019
49. Goritz C., Frisen J., Neural stem cells and neurogenesis in the adult. Cell Stem Cell 2012 10 6 657 659
50. Merkle F. T., Alvarez-Buylla A., Neural stem cells in mammalian development. Current Opinion in Cell Biology 2006 18 6 704 709 2-s2.0-33751119584 10.1016/j.ceb.2006.09.008 (Pubitemid 44767726)
51. Merkle F. T., Tramontin A. D., García-Verdugo J. M., Alvarez-Buylla A., Radial glia give rise to adult neural stem cells in the subventricular zone. Proceedings of the National Academy of Sciences of the United States of America 2004 101 50 17528 17532 2-s2.0-10644232285 10.1073/pnas.0407893101 (Pubitemid 39657437)
52. Petit A., Sanders A. D., Kennedy T. E., Tetzlaff W., Glattfelder K. J., Dalley R. A., Puchalski R. B., Jones A. R., Roskams A. J., Adult spinal cord radial glia display a unique progenitor phenotype. PLoS ONE 2011 6 9 e24538 2-s2.0-80052614666 10.1371/journal.pone.0024538
53. Anthony T. E., Klein C., Fishell G., Heintz N., Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 2004 41 6 881 890 2-s2.0-1842527386 10.1016/S0896-6273(04)00140-0 (Pubitemid 38429732)
54. Doetsch F., Caille I., Lim D. A., Garcia-Verdugo J. M., Alvarez-Buylla A., Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999 97 6 703 716 2-s2.0-0033040497 10.1016/S0092-8674(00)80783-7 (Pubitemid 29278045)
55. Garcia A. D. R., Doan N. B., Imura T., Bush T. G., Sofroniew M. V., GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nature Neuroscience 2004 7 11 1233 1241 2-s2.0-7044233126 10.1038/nn1340 (Pubitemid 39426243)
56. Ihrie R. A., Alvarez-Buylla A., Cells in the astroglial lineage are neural stem cells. Cell and Tissue Research 2008 331 1 179 191 2-s2.0-37249065116 10.1007/s00441-007-0461-z (Pubitemid 350265483)
57. Imura T., Kornblum H. I., Sofroniew M. V., The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. The Journal of Neuroscience 2003 23 7 2824 2832 2-s2.0-0344559101 (Pubitemid 36418618)
58. Shihabuddin L. S., Ray J., Gage F. H., FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Experimental Neurology 1997 148 2 577 586 2-s2.0-0031418325 10.1006/exnr.1997.6697 (Pubitemid 28068850)
59. Yamamoto S. I., Nagao M., Sugimori M., Kosako H., Nakatomi H., Yamamoto N., Takebayashi H., Nabeshima Y. I., Kitamura T., Weinmaster G., Nakamura K., Nakafuku M., Transcription factor expression and notch-dependent regulation of neural progenitors in the adult rat spinal cord. The Journal of Neuroscience 2001 21 24 9814 9823 2-s2.0-0035894866 (Pubitemid 34184066)
60. 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. The Journal of Neuroscience 2000 20 23 8727 8735 2-s2.0-0034548865
61. Altman J., Bayer S. A., Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. Journal of Comparative Neurology 1990 301 3 365 381 2-s2.0-0025088801 (Pubitemid 20368500)
62. Bayer S. A., Yackel J. W., Puri P. S., Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 1982 216 4548 890 892 2-s2.0-0019942979 (Pubitemid 12058817)
63. Eriksson P. S., Perfilieva E., Björk-Eriksson T., Alborn A. M., Nordborg C., Peterson D. A., Gage F. H., Neurogenesis in the adult human hippocampus. Nature Medicine 1998 4 11 1313 1317 2-s2.0-0031789814 10.1038/3305 (Pubitemid 28512114)
64. Bruni J. E., Ependymal development, proliferation, and functions: a review. Microscopy Research and Technique 1998 41 1 2 13 2-s2.0-0032053752 (Pubitemid 28160601)
65. Bruni J. E., Reddy K., Ependyma of the central canal of the rat spinal cord: a light and transmission electron microscopic study. Journal of Anatomy 1987 152 55 70 2-s2.0-0023162610 (Pubitemid 17121524)
66. del Bigio M. R., Ependymal cells: biology and pathology. Acta Neuropathologica 2010 119 1 55 73 2-s2.0-77649190846 10.1007/s00401-009-0624-y
67. Smart I. H., Proliferative characteristics of the ependymal layer during the early development of the spinal cord in the mouse. Journal of Anatomy 1972 111 365 380 2-s2.0-0015329592
68. Rehermann M. I., Marichal N., Russo R. E., Trujillo-Cenóz O., Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. Journal of Comparative Neurology 2009 515 2 197 214 2-s2.0-67650325146 10.1002/cne.22061
69. Dervan A. G., Roberts B. L., Reaction of spinal cord central canal cells to cord transection and their contribution to cord regeneration. Journal of Comparative Neurology 2003 458 3 293 306 2-s2.0-0037424672 10.1002/cne.10594 (Pubitemid 36297917)
70. Bruni J. E., del Bigio M. R., Clattenburg R. E., Ependyma: normal and pathological: a review of the literature. Brain Research 1985 356 1 1 19 2-s2.0-0022049532 (Pubitemid 15088958)
71. Marichal N., García G., Radmilovich M., Trujillo-Cenóz O., Russo R. E., Enigmatic central canal contacting cells: immature neurons in "standby mode"? The Journal of Neuroscience 2009 29 32 10010 10024 2-s2.0-68849116786 10.1523/JNEUROSCI.6183-08.2009
72. Russo R. E., Fernández A., Reali C., Radmilovich M., Trujillo-Cenóz O., Functional and molecular clues reveal precursor-like cells and immature neurones in the turtle spinal cord. Journal of Physiology 2004 560 831 838 2-s2.0-8844229516 10.1113/jphysiol.2004.072405 (Pubitemid 39530121)
73. Russo R. E., Reali C., Radmilovich M., Fernández A., Trujillo-Cenóz O., Connexin 43 delimits functional domains of neurogenic precursors in the spinal cord. The Journal of Neuroscience 2008 28 13 3298 3309 2-s2.0-41549088486 10.1523/JNEUROSCI.5736-07.2008 (Pubitemid 351469315)
74. Noctor S. C., Flint A. C., Weissman T. A., Wong W. S., Clinton B. K., Kriegstein A. R., Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. The Journal of Neuroscience 2002 22 8 3161 3173 2-s2.0-0037092422 (Pubitemid 35379204)
75. Trujillo-Cenóz O., Fernández A., Radmilovich M., Reali C., Russo R. E., Cytological organization of the central gelatinosa in the turtle spinal corel. Journal of Comparative Neurology 2007 502 2 291 308 2-s2.0-34247110921 10.1002/cne.21306 (Pubitemid 46595400)
76. Rehermann M. I., Santiñaque F. F., López-Carro B., Russo R. E., Trujillo-Cenóz O., Cell proliferation and cytoarchitectural remodeling during spinal cord reconnection in the fresh-water turtle Trachemys dorbignyi. Cell and Tissue Research 2011 344 3 415 433 2-s2.0-79958287448 10.1007/s00441-011-1173-y
77. McHedlishvili L., Epperlein H. H., Telzerow A., Tanaka E. M., A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors. Development 2007 134 11 2083 2093 2-s2.0-34250891912 10.1242/dev.02852 (Pubitemid 46979795)
78. Ma D. K., Bonaguidi M. A., Ming G. L., Song H., Adult neural stem cells in the mammalian central nervous system. Cell Research 2009 19 6 672 682 2-s2.0-67649908864 10.1038/cr.2009.56
79. Martínez-Cerdeño V., Cunningham C. L., Camacho J., Antczak J. L., Prakash A. N., Cziep M. E., Walker A. I., Noctor S. C., Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS ONE 2012 7 1 e30178 2-s2.0-84855825323 10.1371/journal.pone.0030178
80. Noctor S. C., Martínez-Cerdeño V., Kriegstein A. R., Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. Journal of Comparative Neurology 2008 508 1 28 44 2-s2.0-42149188826 10.1002/cne.21669 (Pubitemid 351532566)
81. Noctor S. C., Martinez-Cerdeño V., Ivic L., Kriegstein A. R., Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neuroscience 2004 7 2 136 144 2-s2.0-1642458489 10.1038/nn1172 (Pubitemid 38129789)
82. Noctor S. C., Flint A. C., Weissman T. A., Dammerman R. S., Kriegstein A. R., Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001 409 6821 714 720 2-s2.0-0035825670 10.1038/35055553 (Pubitemid 32144516)
83. Yoo S., Wrathall J. R., Mixed primary culture and clonal analysis provide evidence that NG2 proteoglycan-expressing cells after spinal cord injury are glial progenitors. Developmental Neurobiology 2007 67 7 860 874 2-s2.0-34447574996 10.1002/dneu.20369 (Pubitemid 47066917)
84. Zai L. J., Wrathall J. R., Cell proliferation and replacement following contusive spinal cord injury. Glia 2005 50 3 247 257 2-s2.0-20044362061 10.1002/glia.20176 (Pubitemid 40769854)
85. + cells after spinal cord injury. Journal of Neurotrauma 2006 23 12 1726 1738 2-s2.0-33845948003 10.1089/neu.2006.23.1726 (Pubitemid 46034447)
86. Horner P. J., Thallmair M., Gage F. H., Defining the NG2-expressing cell of the adult CNS. Journal of Neurocytology 2002 31 6-7 469 480 2-s2.0-54249146500 (Pubitemid 37378259)
87. Diers-Fenger M., Kirchhoff F., Kettenmann H., Levine J. M., Trotter J., AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia. Glia 2001 34 3 213 228 2-s2.0-0035009839 10.1002/glia.1055 (Pubitemid 32477384)
88. Sellers D. L., Horner P. J., Instructive niches: environmental instructions that confound NG2 proteoglycan expression and the fate-restriction of CNS progenitors. Journal of Anatomy 2005 207 6 727 734 2-s2.0-29644437679 10.1111/j.1469-7580.2005.00480.x (Pubitemid 43019732)
89. Berry M., Hubbard P., Butt A. M., Cytology and lineage of NG2-positive glia. Journal of Neurocytology 2002 31 6-7 457 467 2-s2.0-54249160983 (Pubitemid 37378258)
90. Schnapp E., Kragl M., Rubin L., Tanaka E. M., Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 2005 132 14 3243 3253 2-s2.0-23844489401 10.1242/dev.01906 (Pubitemid 41167152)
91. Reimer M. M., Kuscha V., Wyatt C., Sörensen I., Frank R. E., Knüwer M., Becker T., Becker C. G., Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. The Journal of Neuroscience 2009 29 48 15073 15082 2-s2.0-72849151554 10.1523/JNEUROSCI.4748-09.2009
92. Egar M., Simpson S. B., Singer M., The growth and differentiation of the regenerating spinal cord of the lizard, Anolis carolinensis. Journal of Morphology 1970 131 2 131 151 2-s2.0-0014802727
93. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., Van Heyningen V., Jessell T. M., Briscoe J., Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 1997 90 1 169 180 2-s2.0-0031458813 10.1016/S0092-8674(00)80323-2 (Pubitemid 28009428)
94. Genethliou N., Panayiotou E., Panayi H., Orford M., Mean R., Lapathitis G., Malas S., Spatially distinct functions of PAX6 and NKX2.2 during gliogenesis in the ventral spinal cord. Biochemical and Biophysical Research Communications 2009 382 1 69 73 2-s2.0-63349102675 10.1016/j.bbrc.2009.02.134
95. Sun T., Pringle N. P., Hardy A. P., Richardson W. D., Smith H. K., Pax6 influences the time and site of origin of glial precursors in the ventral neural tube. Molecular and Cellular Neurosciences 1998 12 4-5 228 239 2-s2.0-0031761287 10.1006/mcne.1998.0711 (Pubitemid 28536076)
96. Henley B. M., McDermott K. W., The expression of neuroepithelial cell fate determinants in rat spinal cord development. Journal of Molecular Neuroscience 2010 42 1 28 34 2-s2.0-77955171731 10.1007/s12031-010-9339-8
97. Bel-Vialar S., Medevielle F., Pituello F., The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord. Developmental Biology 2007 305 2 659 673 2-s2.0-34247618823 10.1016/j.ydbio. 2007.02.012 (Pubitemid 46686604)
98. Alaynick W. A., Jessell T. M., Pfaff S. L., Snapshot: spinal cord development. Cell 2011 146 1 178.e1 178.e1 2-s2.0-79960004405 10.1016/j.cell.2011.06.038
99. Tanabe Y., Jessell T. M., Diversity and pattern in the developing spinal cord. Science 1996 274 5290 1115 1123 2-s2.0-0029860502 10.1126/science.274. 5290.1115 (Pubitemid 26389267)
100. Tochitani S., Hayashizaki Y., Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation. Biochemical and Biophysical Research Communications 2008 372 4 691 696 2-s2.0-45449092537 10.1016/j.bbrc.2008.05.127
101. Cui Y.-F., Xu J. C., Hargus G., Jakovcevski I., Schachner M., Bernreuther C., Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery after spinal cord injury in mice. PLoS ONE 2011 6 3 2-s2.0-79952802524 10.1371/journal.pone.0017126 e17126
102. Krencik R., Weick J. P., Liu Y., Zhang Z. J., Zhang S. C., Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nature Biotechnology 2011 29 6 528 534 2-s2.0-79958128131 10.1038/nbt.1877
103. Menei P., Montero-Menei C., Whittemore S. R., Bunge R. P., Bartlett Bunge M., Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. European Journal of Neuroscience 1998 10 2 607 621 2-s2.0-0031814388 10.1046/j.1460-9568.1998.00071. x (Pubitemid 28325484)
104. Obermair F. J., Schröter A., Thallmair M., Endogenous neural progenitor cells as therapeutic target after spinal cord injury. Physiology 2008 23 5 296 304 2-s2.0-57049088552 10.1152/physiol.00017.2008
105. Nakamura M., Tsuji O., Bregman B. S., Toyama Y., Okano H., Mimicking the neurotrophic factor profile of embryonic spinal cord controls the differentiation potential of spinal progenitors into neuronal cells. PLoS ONE 2011 6 6 2-s2.0-79959241226 10.1371/journal.pone.0020717 e20717
106. Giménez Y Ribotta M., Orsal D., Feraboli-Lohnherr D., Privat A., Recovery of locomotion following transplantation of monoaminergic neurons in the spinal cord of paraplegic rats. Annals of the New York Academy of Sciences 1998 860 393 411 2-s2.0-0032416310 10.1111/j.1749-6632.1998.tb09064.x (Pubitemid 29045985)
107. Lepore A. C., Fischer I., Lineage-restricted neural precursors survive, migrate, and differentiate following transplantation into the injured adult spinal cord. Experimental Neurology 2005 194 1 230 242 2-s2.0-19344365362 10.1016/j.expneurol.2005.02.020 (Pubitemid 40719758)
108. 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. The Journal of Neuroscience 2011 31 12 4675 4686 2-s2.0-79953015414 10.1523/JNEUROSCI.4130-10.2011
109. 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. Proceedings of the National Academy of Sciences of the United States of America 2005 102 39 14069 14074 2-s2.0-25444455637 10.1073/pnas.0507063102 (Pubitemid 41377704)
110. Feraboli-Lohnherr D., Orsal D., Yakovleff A., Giménez Y Ribotta M., Privat A., Recovery of locomotor activity in the adult chronic spinal rat after sublesional transplantation of embryonic nervous cells: specific role of serotonergic neurons. Experimental Brain Research 1997 113 3 443 454 2-s2.0-0030889982 10.1007/PL00005597 (Pubitemid 27140268)
111. Lee H., Al Shamy G., Elkabetz Y., Schofield C. M., Harrsion N. L., Panagiotakos G., Socci N. D., Tabar V., Studera L., Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 2007 25 8 1931 1939 2-s2.0-34547858511 10.1634/stemcells.2007-0097 (Pubitemid 47258171)
112. Davies J. E., Huang C., Proschel C., Noble M., Mayer-Proschel M., Davies S. J. A., Astrocytes derived from glial-restricted precursors promote spinal cord repair. Journal of Biology 2006 5 3, article 7 2-s2.0-33746914843 10.1186/jbiol35
113. Faulkner J., Keirstead H. S., Human embryonic stem cell-derived oligodendrocyte progenitors for the treatment of spinal cord injury. Transplant Immunology 2005 15 2 131 142 2-s2.0-30444459785 10.1016/j.trim.2005.09.007 (Pubitemid 43075333)
114. Glass J. D., Boulis N. M., Johe K., Rutkove S. B., Federici T., Polak M., Kelly C., Feldman E. L., Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells 2012 30 6 1144 1151 2-s2.0-84864184427 10.1002/stem.1079
115. Mazzini L., Mareschi K., Ferrero I., Miglioretti M., Stecco A., Servo S., Carriero A., Monaco F., Fagioli F., Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study. Cytotherapy 2012 14 1 56 60 2-s2.0-83755188611 10.3109/14653249.2011.613929
116. Chen L., Chen D., Xi H., Wang Q., Liu Y., Zhang F., Wang H., Ren Y., Xiao J., Wang Y., Huang H., Olfactory ensheathing cell neurorestorotherapy for amyotrophic lateral sclerosis patients: benefits from multiple transplantations. Cell Transplantation 2012 21 supplement 1 S65 S77 2-s2.0-84855330877 http://dx.doi.org/10.3727/096368912X633789
117. McCall J., Weidner N., Blesch A., Neurotrophic factors in combinatorial approaches for spinal cord regeneration. Cell and Tissue Research 2012 349 1 27 37 2-s2.0-84859905286 10.1007/s00441-012-1388-6
118. Arnett H. A., Mason J., Marino M., Suzuki K., Matsushima G. K., Ting J. P. Y., TNF α promotes proliferation of oligodendrocyte progenitors and remyelination. Nature Neuroscience 2001 4 11 1116 1122 2-s2.0-0035705454 10.1038/nn738 (Pubitemid 34116557)
119. Bond A. M., Bhalala O. G., Kessler J. A., The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Developmental Neurobiology 2012 72 7 1068 1084 2-s2.0-68549104117 10.1002/dneu.22022
120. Hofstetter C. P., Holmström N. A. V., Lilja J. A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S. N., Frisén J., Olson L., Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nature Neuroscience 2005 8 3 346 353 2-s2.0-20044370811 10.1038/nn1405 (Pubitemid 40300192)
121. Uchida Y., Nakano S. I., Gomi F., Takahashi H., Differential regulation of basic helix-loop-helix factors Mash1 and Olig2 by β -amyloid accelerates both differentiation and death of cultured neural stem/progenitor cells. Journal of Biological Chemistry 2007 282 27 19700 19709 2-s2.0-34547093895 10.1074/jbc.M703099200 (Pubitemid 47100101)
122. Kallur T., Gisler R., Lindvall O., Kokaia Z., Pax6 promotes neurogenesis in human neural stem cells. Molecular and Cellular Neuroscience 2008 38 4 616 628 2-s2.0-47749138860 10.1016/j.mcn.2008.05.010
123. Sebastián-Serrano A., Sandonis A., Cardozo M., Rodríguez-Tornos F. M., Bovolenta P., Nieto M., Palphax6 expression in postmitotic neurons mediates the growth of axons in response to SFRP1. PLoS ONE 2012 7 2 e31590 2-s2.0-84862760328 10.1371/journal.pone.0031590
124. Chmielnicki E., Benraiss A., Economides A. N., Goldman S. A., Adenovirally expressed noggin and brian-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. The Journal of Neuroscience 2004 24 9 2133 2142 2-s2.0-1542376943 10.1523/JNEUROSCI.1554-03.2004 (Pubitemid 38314545)
125. Bergen J. M., Park I. K., Horner P. J., Pun S. H., Nonviral approaches for neuronal delivery of nucleic acids. Pharmaceutical Research 2008 25 5 983 998 2-s2.0-42049114012 10.1007/s11095-007-9439-5
126. Kwon E. J., Lasiene J., Jacobson B. E., Park I. K., Horner P. J., Pun S. H., Targeted nonviral delivery vehicles to neural progenitor cells in the mouse subventricular zone. Biomaterials 2010 31 8 2417 2424 2-s2.0-74449086252 10.1016/j.biomaterials.2009.11.086
127. Harper M. M., Grozdanic S. D., Blits B., Kuehn M. H., Zamzow D., Buss J. E., Kardon R. H., Sakaguchi D. S., Transplantation of BDNF-secreting mesenchymal stem cells provides neuroprotection in chronically hypertensive rat eyes. Investigative Ophthalmology and Visual Science 2011 52 7 4506 4515 2-s2.0-80052369665 10.1167/iovs.11-7346
128. Sasaki M., Radtke C., Tan A. M., Zhao P., Hamada H., Houkin K., Honmou O., Kocsis J. D., BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. The Journal of Neuroscience 2009 29 47 14932 14941 2-s2.0-72449122797 10.1523/JNEUROSCI.2769-09.2009
129. Davies J. E., Pröschel C., Zhang N., Noble M., Mayer-Pröschel M., Davies S. J. A., Transplanted astrocytes derived from BMP- or CNTF-treated
130. Ke Y., Chi L., Xu R., Luo C., Gozal D., Liu R., Early response of endogenous adult neural progenitor cells to acute spinal cord injury in mice. Stem Cells 2006 24 4 1011 1019 2-s2.0-33745500882 10.1634/stemcells.2005-0249 (Pubitemid 44464734)
131. Murray K. C., Nakae A., Stephens M. J., Rank M., D'Amico J., Harvey P. J., Li X., Harris R. L. W., Ballou E. W., Anelli R., Heckman C. J., Mashimo T., Vavrek R., Sanelli L., Gorassini M. A., Bennett D. J., Fouad K., Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-H T2C receptors. Nature Medicine 2010 16 6 694 700 2-s2.0-77953229364 10.1038/nm.2160
132. Keirstead H. S., Levine J. M., Blakemore W. F., Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 1998 22 2 161 170 2-s2.0-0032534610 (Pubitemid 28084388)