Implantation of Dendritic Cells in Injured Adult Spinal Cord Results in Activation of Endogenous Neural Stem/Progenitor Cells Leading to De Novo Neurogenesis and Functional Recovery

Journal of Neuroscience Research

Volumn 76, Issue 4, 2004, Pages 453-465

  Mikami, Yuji ^a   Okano, Hideyuki ^a   Sakaguchi, Masanori ^a   Nakamura, Masaya ^a   Shimazaki, Takuya ^a   Okano, Hirotaka James ^a   Kawakami, Yutaka ^a   Toyama, Yoshiaki ^a   Toda, Masahiro ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Dendritic cells; Neural stem cells; Neurogenesis; Regeneration; Spinal cord injury

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION;

ANIMALS; BEHAVIOR, ANIMAL; BIOTIN; BROMODEOXYURIDINE; CELL COUNT; CELL SURVIVAL; DENDRITIC CELLS; DEXTRANS; EMBRYO; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTERMEDIATE FILAMENT PROTEINS; LOCOMOTION; LUMINESCENT PROTEINS; MACROPHAGE-1 ANTIGEN; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NERVE GROWTH FACTORS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONS; NEUROTROPHIN 3; PHOSPHOPYRUVATE HYDRATASE; RECOVERY OF FUNCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPINAL CORD INJURIES; STEM CELLS; TIME FACTORS;

EID: 2342564525     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20086     Document Type: Article

References (70)

1. Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K, Akira S. 2000. Cutting edge: cell surface expression and lipopolysaccharide signaling via the toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J Immunol 164: 3471-3475.
2. Alvarez-Buylla A, Garcia-Verdugo JM. 2002. Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
3. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
4. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
5. Barres BA. 2003. What is a glial cell? Glia 43:4-5.
6. Basso DM, Beattie MS, Bresnahan JC. 1995. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
7. Brosamle C, Huber AB, Fiedler M, Skerra A, Schwab ME. 2000. Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J Neurosci 20:8061-8068.
8. Capela A, Temple S. 2002. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
9. Cheng H, Cao Y, Olson L. 1996. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273:510-513.
10. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
11. De Smedt T, Pajak B, Muraille E, Lespagnard L, Heinen E, De Baetselier P, Urbain J, Leo O, Moser M. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J Exp Med 184:1413-1424.
12. DiCicco-Bloom E, Friedman WJ, Black IB. 1993. NT-3 stimulates sympathetic neuroblast proliferation by promoting precursor survival. Neuron 11:1101-1111.
13. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
14. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang K, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin M. 2002. Myelin-associated glycoprotein interacts with the Nogo 66 receptor to inhibit neurite outgrowth. Neuron 35:283-290.
15. Dougherty KD, Dreyfus CF, Black IB. 2000. Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 7:574-585.
16. Ekdahl CT, Mohapel P, Elmer E, Lindvall O. 2001. Caspase inhibitors increase short-term survival of progenitor-cell progeny in the adult rat dentate gyrus following status epilepticus. Eur J Neurosci 14:937-945.
17. Elkabes S, Peng L, Black IB. 1998. Lipopolysaccharide differentially regulates microglial trk receptor and neurotrophin expression. J Neurosci Res. 54:117-122.
18. Filbin MT. 1995. Myelin-associated glycoprotein: a role in myelination and in the inhibition of axonal regeneration? Curr Opin Neurobiol 5:588-595.
19. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang L, Yamaguchi M, Kettenmann H, Kempermann G. 2003. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23:373-382.
20. Frisén J, Johansson CB, Török C, Risling M, Lendahl U. 1995. B. Rapid, widespread and long lasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol 131:453-464.
21. Fukao T, Tanabe M, Terauchi Y, Ota T, Matsuda S, Asano T, Kadowaki T, Takeuchi T, Koyasu S. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol 3:875-881.
22. Ghosh A, Greenberg ME. 1995. Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
23. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. 1997. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17:5560-5572.
24. Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M. 2000a. Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 20: 6421-6430.
25. Hauben E, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Akselrod S, Neeman M, Cohen IR, Schwartz M. 2000b. Autoimmune T cells as potential neuroprotective therapy for spinal cord injury. Lancet 355:286-287.
26. Hauben E, Ibarra A, Mizrahi T, Barouch R, Agranov E, Schwartz M. 2001a. Posttraumatic therapeutic vaccination with modified myelin self-antigen prevents complete paralysis while avoiding autoimmune disease. J Clin Invest 108:591-599.
27. Hauben E, Ibarra A, Mizrahi T, Barouch R, Agranov E, Schwartz M. 2001b. Vaccination with a Nogo-A-derived peptide after incomplete spinal-cord injury promotes recovery via a T-cell-mediated neuroprotective response: comparison with other myelin antigens. Proc Natl Acad Sci USA 98:15173-15178.
28. Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR. 2000. Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains. Amsterdam: Elsevier Science BV. p 29-63.
29. 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.
30. Imura T, Kornblum HI, Sofroniew MV. 2003. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 23:2824-2832.
31. Johansson CB, Lothian C, Molin M, Okano H, Lendahl U. 2002. Nestin enhancer requirements for expression in normal and injured adult CNS. J Neurosci Res 69:784-794.
32. 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.
33. Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman SA, Okano H. 2001. Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17:259-273.
34. Kempermann G, Gage FH. 1999. New nerve cells for the adult brain. Sci Am 280:48-53.
35. Kiehn O, Butt SJ. 2003. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70:347-361.
36. Kokaia Z, Lindvall O. 2003. Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 13:127-132.
37. Larsson E, Mandel RJ, Klein RL, Muzyczka N, Lindvall O, Kokaia Z. 2002. Suppression of insult-induced neurogenesis in adult rat brain by brain-derived neurotrophic factor. Exp Neurol 177:1-8.
38. Lazarov-Spiegler O, Solomon AS, Schwartz M, Schwartzberg LS. 1998. Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24:329-337.
39. Liu J, Solway K, Messing RO, Sharp FR. 1998. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-7778.
40. Marusich MF, Furneaux HM, Henion P, Weston JA. 1994. Hu neuronal proteins are expressed in proliferating neurogenic cells. J Neurobiol 25:143-155.
41. Mikami Y, Toda M, Watanabe M, Nakamura M, Toyama Y, Kawakami Y. 2002. A simple and reliable behavioral analysis of locomotor function after spinal cord injury in mice. Technical note. J Neurosurg 97:142-147.
42. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D. 1994. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
43. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT. 1994. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
44. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
45. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino, T, Nakafuku M. 2002. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-441.
46. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS. 2003. Difference in cytokine gene expression profile between acutely and chronically injured adult rat spinal cord. Exp Neurol 184:313-325.
47. Namiki J, Tator CH, Namiki K. 1999. Cell proliferation and nestin expression in the ependyma of the adult rat spinal cord after injury. J Neuropathol Exp Neurol 58:489-498.
48. 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.
49. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 1997. "Green mice" as a source of ubiquitous green cells. FEBS Lett 407:313-319.
50. Okada S, Nakamura M, Mikami Y, Shimazaki T, Mihara M, Ohsugi Y, Iwamoto Y, Yoshizaki K, Kishimoto T, Toyama Y, Okano H. 2003. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J Neurosci Res (in press).
51. Okano H. 2002. The stem cell biology of the central nervous system. J Neurosci Res 69:698-707.
52. Okano HJ, Darnell RB. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
53. 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.
54. Olson L. 2002. Medicine: clearing a path for nerve growth. Nature 416: 589-590.
55. Pearson H. 2003. In search of a miracle. Nature 423:112-113.
56. Rabchevsky AG, Streit WJ. 1997. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 47:34-48.
57. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M. 1998. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821.
58. Reddy SM, Hsiao KH, Abernethy VE, Fan H, Longacre A, Lieberthal W, Rauch J, Koh JS, Levine JS. 2002. Phagocytosis of apoptotic cells by macrophages induces novel signaling events leading to cytokine-independent survival and inhibition of proliferation: activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J Immunol 169:702-713.
59. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
60. 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.
61. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. 2001. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412:736-739.
62. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA. 2000. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6:271-278.
63. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME. 1994. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
64. Schwab ME. 1990. Myelin-associated inhibitors of neurite growth. Exp Neurol 109:2-5.
65. Schwartz M, Moalem G, Leibowitz-Amit R, Cohen IR. 1999. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22:295-299.
66. Shihabuddin LS, Homer 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.
67. Taupin P, Ray J, Fischer WH, Suhr ST, Hakansson K, Grubb A, Gage FH. 2000. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28:385-397.
68. Temple S, Alvarez-Buylla A. 1999. Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9:135-141.
69. Thallmair M, Metz GA, Z'Graggen WJ, Raineteau O, Kartje GL, Schwab ME. 1998. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1:124-131.
70. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa K, Miyata T, Okano H, Hori M, Matsumoto M. 2001. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32:1890-1896.