A cell population that strongly expresses the CB1 cannabinoid receptor in the ependyma of the rat spinal cord

Journal of Comparative Neurology

Volumn 521, Issue 1, 2013, Pages 233-251

  Garcia Ovejero, Daniel ^a   Arevalo Martin, Angel ^a   Paniagua Torija, Beatriz ^a   Sierra Palomares, Yolanda ^a   Molina Holgado, Eduardo ^a  

^a HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

Author keywords

Ependyma; Neural precursor; Quiescence; Spinal cord injury; Stem cells; Tanycyte

Indexed keywords

CANNABINOID 1 RECEPTOR; CELL MARKER; ENDOCANNABINOID; EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX9; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; CELL POPULATION; CELL PROLIFERATION; EPENDYMA CELL; MALE; MICROGLIA; NERVE CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPINAL CORD; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD15; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEINS; CELL COUNT; EPENDYMA; EXCITATORY AMINO ACID TRANSPORTER 1; FATTY ACID-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERMEDIATE FILAMENT PROTEINS; KI-67 ANTIGEN; LAMINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULE L1; NEUROGLIA; NEURONS; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; SIALIC ACIDS; SOXB1 TRANSCRIPTION FACTORS; SPINAL CORD; SPINAL CORD INJURIES; TUBULIN;

EID: 84870001765     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23184     Document Type: Article

References (93)

1. Adrian EK Jr, Walker BE. 1962. Incorporation of thymidine-H3 by cells in normal and injured mouse spinal cord. J Neuropathol Exp Neurol 21: 597-609.
2. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I. 2005. The endocannabinoid system drives neural progenitor proliferation. FASEB J 19: 1704-1706.
3. Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I. 2006. The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J Neurosci 26: 1551-1561.
4. Aguado T, Romero E, Monory K, Palazuelos J, Sendtner M, Marsicano G, Lutz B, Guzman M, Galve-Roperh I. 2007. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem 282: 23892-23898.
5. Alfaro-Cervello C, Soriano-Navarro M, Mirzadeh Z, Alvarez-Buylla A, Garcia-Verdugo JM. 2012. Biciliated ependymal cell proliferation contributes to spinal cord growth. J Comp Neurol [Epub ahead of print].
6. Arevalo-Martin A, Garcia-Ovejero D, Rubio-Araiz A, Gomez O, Molina-Holgado F, Molina-Holgado E. 2007. Cannabinoids modulate Olig2 and polysialylated neural cell adhesion molecule expression in the subventricular zone of post-natal rats through cannabinoid receptor 1 and cannabinoid receptor 2. Eur J Neurosci 26: 1548-1559.
7. Barber RP, Vaughn JE, Roberts E. 1982. The cytoarchitecture of GABAergic neurons in rat spinal cord. Brain Res 238: 305-328.
8. Barcia C, Sanderson NS, Barrett RJ, Wawrowsky K, Kroeger KM, Puntel M, Liu C, Castro MG, Lowenstein PR. 2008. T cells' immunological synapses induce polarization of brain astrocytes in vivo and in vitro: a novel astrocyte response mechanism to cellular injury. PLoS ONE 3: e2977.
9. Barnabé-Heider F, Göritz C, Sabelström H, Takebayashi H, Pfrieger FW, Meletis K, Frisén J. 2010. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7: 470-482.
10. Ben-Hur T, Rogister B, Murray K, Rougon G, Dubois-Dalcq M. 1998. Growth and fate of PSA-NCAM+ precursors of the postnatal brain. J Neurosci 18: 5777-5788.
11. Bjugn R, Haugland HK, Flood PR. 1988. Ultrastructure of the mouse spinal cord ependyma. J Anat 160: 117-125.
12. Bruni JE. 1998. Ependymal development, proliferation, and functions: a review. Microsc Res Tech 41: 2-13.
13. Bruni JE, Reddy K. 1987. Ependyma of the central canal of the rat spinal cord: a light and transmission electron microscopic study. J Anat 152: 55-70.
14. Bruni JE, Del Bigio MR, Clattenburg RE. 1985. Ependyma: normal and pathological. A review of the literature. Brain Res 356: 1-19.
15. Carrier EJ, Kearn CS, Barkmeier AJ, Breese NM, Yang W, Nithipatikom K, Pfister SL, Campbell WB, Hillard CJ. 2004. Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism. Mol Pharmacol 65: 999-1007.
16. Cizkova D, Nagyova M, Slovinska L, Novotna I, Radonak J, Cizek M, Mechirova E, Tomori Z, Hlucilova J, Motlik J, Sulla I, Vanicky I. 2009. Response of ependymal progenitors to spinal cord injury or enhanced physical activity in adult rat. Cell Mol Neurobiol 29: 999-1013.
17. Doetsch F. 2003. The glial identity of neural stem cells. Nat Neurosci 6: 1127-1134.
18. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-5061.
19. Dromard C, Guillon H, Rigau V, Ripoll C, Sabourin JC, Perrin FE, Scamps F, Bozza S, Sabatier P, Lonjon N, Duffau H, Vachiery-Lahaye F, Prieto M, Tran Van Ba C, Deleyrolle L, Boularan A, Langley K, Gaviria M, Privat A, Hugnot JP, Bauchet L. 2008. Adult human spinal cord harbors neural precursor cells that generate neurons and glial cells in vitro. J Neurosci Res 86: 1916-1926.
20. Farquhar-Smith WP, Egertova M, Bradbury EJ, McMahon SB, Rice AS, Elphick MR. 2000. Cannabinoid CB(1) receptor expression in rat spinal cord. Mol Cell Neurosci 15: 510-521.
21. Fox N, Damjanov I, Knowles BB, Solter D. 1983. Immunohistochemical localization of the mouse stage-specific embryonic antigen 1 in human tissues and tumors. Cancer Res 43: 669-678.
22. Frisen J, Johansson CB, Torok C, Risling M, Lendahl U. 1995. Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131: 453-464.
23. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. 2006. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26: 8609-8621.
24. Garcia-Ovejero D, Arevalo-Martin A, Petrosino S, Docagne F, Hagen C, Bisogno T, Watanabe M, Guaza C, Di Marzo V, Molina-Holgado E. 2009. The endocannabinoid system is modulated in response to spinal cord injury in rats. Neurobiol Dis 33: 57-71.
25. Goncalves MB, Suetterlin P, Yip P, Molina-Holgado F, Walker DJ, Oudin MJ, Zentar MP, Pollard S, Yanez-Munoz RJ, Williams G, Walsh FS, Pangalos MN, Doherty P. 2008. A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol Cell Neurosci 38: 526-536.
26. Gotz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6: 777-788.
27. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
28. Hamilton LK, Truong MKV, Bednarczyk MR, Aumont A, Fernandes KJL. 2009. Cellular organization of the central canal ependymal zone, a niche of latent neural stem cells in the adult mammalian spinal cord. Neuroscience 164: 1044-1056.
29. Haubst N, Georges-Labouesse E, De Arcangelis A, Mayer U, Gotz M. 2006. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133: 3245-3254.
30. Hegyi Z, Kis G, Hollo K, Ledent C, Antal M. 2009. Neuronal and glial localization of the cannabinoid-1 receptor in the superficial spinal dorsal horn of the rodent spinal cord. Eur J Neurosci 30: 251-262.
31. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC. 1991. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11: 563-583.
32. Horky LL, Galimi F, Gage FH, Horner PJ. 2006. Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 498: 525-538.
33. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH. 2000. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20: 2218-2228.
34. Hutton SR, Pevny LH. 2011. SOX2 expression levels distinguish between neural progenitor populations of the developing dorsal telencephalon. Dev Biol 352: 40-47.
35. Imura T, Nakano I, Kornblum HI, Sofroniew MV. 2006. Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 53: 277-293.
36. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, Zhang X. 2005. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 115: 3104-3116.
37. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, Childs J, Greenberg DA. 2004. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 66: 204-208.
38. 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.
39. Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, Sasaki T, Patton B, Mattson MP, Hirschi KK, Dickinson ME, ffrench-Constant C. 2010. Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30: 9771-9781.
40. Kelly TK, Karsten SL, Geschwind DH, Kornblum HI. 2009. Cell lineage and regional identity of cultured spinal cord neural stem cells and comparison to brain-derived neural stem cells. PLoS ONE 4: e4213.
41. Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F. 2007. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25: 2146-2157.
42. Kohno K. 1969. Electron microscopic studies on Reissner's fiber and the ependymal cells in the spinal cord of the rat. Z Zellforsch Mikrosk Anat 94: 565-573.
43. Komitova M, Eriksson PS. 2004. Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369: 24-27.
44. Lendahl U, Zimmerman LB, McKay RD. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
45. Liu RH, Morassutti DJ, Whittemore SR, Sosnowski JS, Magnuson DS. 1999. Electrophysiological properties of mitogen-expanded adult rat spinal cord and subventricular zone neural precursor cells. Exp Neurol 158: 143-154.
46. Marichal N, Garcia G, Radmilovich M, Trujillo-Cenoz O, Russo RE. 2009. Enigmatic central canal contacting cells: immature neurons in "standby mode"? J Neurosci 29: 10010-10024.
47. Matthews MA, St Onge MF, Faciane CL. 1979. An electron microscopic analysis of abnormal ependymal cell proliferation and envelopment of sprouting axons following spinal cord transection in the rat. Acta Neuropathol 45: 27-36.
48. McTigue DM, Wei P, Stokes BT. 2001. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 21: 3392-3400.
49. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J. 2008. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6: e182.
50. Mercier F, Kitasako JT, Hatton GI. 2002. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol 451: 170-188.
51. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3: 265-278.
52. Molina-Holgado F, Rubio-Araiz A, Garcia-Ovejero D, Williams RJ, Moore JD, Arevalo-Martin A, Gomez-Torres O, Molina-Holgado E. 2007. CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur J Neurosci 25: 629-634.
53. Mulder J, Zilberter M, Pasquare SJ, Alpar A, Schulte G, Ferreira SG, Kofalvi A, Martin-Moreno AM, Keimpema E, Tanila H, Watanabe M, Mackie K, Hortobagyi T, de Ceballos ML, Harkany T. 2011. Molecular reorganization of endocannabinoid signalling in Alzheimer's disease. Brain 134( Pt 4): 1041-1060.
54. Nakayama Y, Kohno K. 1974. Number and polarity of the ependymal cilia in the central canal of some vertebrates. J Neurocytol 3: 449-458.
55. Nyilas R, Gregg LC, Mackie K, Watanabe M, Zimmer A, Hohmann AG, Katona I. 2009. Molecular architecture of endocannabinoid signaling at nociceptive synapses mediating analgesia. Eur J Neurosci 29: 1964-1978.
56. Oakley BR. 1992. Gamma-tubulin: the microtubule organizer? Trends Cell Biol 2: 1-5.
57. Obermair F-J, Fiorelli R, Schroeter A, Beyeler S, Blatti C, Zoerner B, Thallmair M. 2010. A novel classification of quiescent and transit amplifying adult neural stem cells by surface and metabolic markers permits a defined simultaneous isolation. Stem Cell Res 5: 131-143.
58. Ohori Y, Yamamoto Si, Nagao M, Sugimori M, Yamamoto N, Nakamura K, Nakafuku M. 2006. Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J Neurosci 26: 11948-11960.
59. Ong WY, Mackie K. 1999. A light and electron microscopic study of the CB1 cannabinoid receptor in the primate spinal cord. J Neurocytol 28: 39-45.
60. Pacher P, Batkai S, Kunos G. 2006. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58: 389-462.
61. Palazuelos J, Aguado T, Egia A, Mechoulam R, Guzman M, Galve-Roperh I. 2006. Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 20: 2405-2407.
62. Pfenninger CV, Steinhoff C, Hertwig F, Nuber UA. 2011. Prospectively isolated CD133/CD24-positive ependymal cells from the adult spinal cord and lateral ventricle wall differ in their long-term in vitro self-renewal and in vivo gene expression. Glia 59: 68-81.
63. Rafols JA, Goshgarian HG. 1985. Spinal tanycytes in the adult rat: a correlative Golgi gold-toning study. Anat Rec 211: 75-86.
64. Rakic P. 1998. Radial glial cells: scaffolding for brain construction. In: Ransom BKH, editor. Neuroglia. New York: Oxford University Press. p 746-763.
65. Rameshwar P, Petit A, Sanders AD, Kennedy TE, Tetzlaff W, Glattfelder KJ, Dalley RA, Puchalski RB, Jones AR, Roskams AJ. 2011. Adult spinal cord radial glia display a unique progenitor phenotype. PLoS ONE 6: e24538.
66. Ramon y Cajal S. 1899, 1904. Textura del sistema nervioso del hombre y de los vertebrados. Madrid: Moya.
67. Rougon G, Dubois C, Buckley N, Magnani JL, Zollinger W. 1986. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J Cell Biol 103( 6 Pt 1): 2429-2437.
68. Rubio-Araiz A, Arevalo-Martin A, Gomez-Torres O, Navarro-Galve B, Garcia-Ovejero D, Suetterlin P, Sanchez-Heras E, Molina-Holgado E, Molina-Holgado F. 2008. The endocannabinoid system modulates a transient TNF pathway that induces neural stem cell proliferation. Mol Cell Neurosci 38: 374-380.
69. Rueda D, Navarro B, Martinez-Serrano A, Guzman M, Galve-Roperh I. 2002. The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J Biol Chem 277: 46645-46650.
70. Sabourin J-C, Ackema KB, Ohayon D, Guichet P-O, Perrin FE, Garces A, Ripoll C, Charité J, Simonneau L, Kettenmann H, Zine A, Privat A, Valmier J, Pattyn A, Hugnot J-P. 2009. A mesenchymal-like ZEB1+Niche harbors dorsal radial glial fibrillary acidic protein-positive stem cells in the spinal cord. Stem Cells 27: 2722-2733.
71. Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV, Booth S, Gao B, Cheah KS, Lovell-Badge R, Briscoe J. 2010. SOX9 induces and maintains neural stem cells. Nat Neurosci 13: 1181-1189.
72. Schmitz C, Hof PR. 2005. Design-based stereology in neuroscience. Neuroscience 130: 813-831.
73. Seitz R, Lohler J, Schwendemann G. 1981. Ependyma and meninges of the spinal cord of the mouse. A light-and electron-microscopic study. Cell Tissue Res 220: 61-72.
74. Ševc J, Daxnerová Z, Miklošová M. 2009. Role of radial glia in transformation of the primitive lumen to the central canal in the developing rat spinal cord. Cell Mol Neurobiol 29: 927-936.
75. Ševc J, Daxnerová Z, Haňová V, Koval' J. 2011. Novel observations on the origin of ependymal cells in the ventricular zone of the rat spinal cord. Acta Histochem 113: 156-162.
76. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. 2008. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3: 289-300.
77. Shihabuddin LS, Ray J, Gage FH. 1997. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148: 577-586.
78. Shihabuddin LS, Horner PJ, Ray J, Gage FH. 2000. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 20: 8727-8735.
79. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M. 2010. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7: 483-495.
80. Solter D, Knowles BB. 1978. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci U S A 75: 5565-5569.
81. Stoeckel M-E, Uhl-Bronner S, Hugel S, Veinante P, Klein M-J, Mutterer J, Freund-Mercier M-J, Schlichter RM. 2003. Cerebrospinal fluid-contacting neurons in the rat spinal cord, a γ-aminobutyric acidergic system expressing the P2X2 subunit of purinergic receptors, PSA-NCAM, and GAP-43 immunoreactivities: light and electron microscopic study. J Comp Neurol 457: 159-174.
82. Sturrock RR. 1981. An electron microscopic study of the development of the ependyma of the central canal of the mouse spinal cord. J Anat 132( Pt 1): 119-136.
83. Suarez J, Romero-Zerbo SY, Rivera P, Bermudez-Silva FJ, Perez J, De Fonseca FR, Fernandez-Llebrez P. 2010. Endocannabinoid system in the adult rat circumventricular areas: an immunohistochemical study. J Comp Neurol 518: 3065-3085.
84. Suh H, Consiglio A, Ray J, Sawai T, D'Amour KA, Gage FH. 2007. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1: 515-528.
85. Taupin P. 2007. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53: 198-214.
86. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3: 279-288.
87. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83: 393-411.
88. Uchigashima M, Narushima M, Fukaya M, Katona I, Kano M, Watanabe M. 2007. Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27: 3663-3676.
89. Vigh B, Manzano e Silva MJ, Frank CL, Vincze C, Czirok SJ, Szabo A, Lukats A, Szel A. 2004. The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. Histol Histopathol 19: 607-628.
90. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N. 2003. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 23: 1398-1405.
91. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. 1996. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599-7609.
92. Yamamoto S-I, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M. 2001. Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol 172: 115-127.
93. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M. 2006. Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26: 4740-4751.