Activation of dendritic-like cells and neural stem/progenitor cells in injured spinal cord by GM-CSF

Neuroscience Research

Volumn 64, Issue 1, 2009, Pages 96-103

  Hayashi, Kaori ^a   Ohta, Shigeki ^a   Kawakami, Yutaka ^a   Toda, Masahiro ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Dendritic cells; Immune cells; Neural stem cells; Regeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFICACY; DRUG MECHANISM; FEMALE; LOCOMOTION; MACROPHAGE; MICROGLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD INJURY;

ANIMALS; ANTIGENS, CD11C; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED BALB C; MICROGLIA; MOTOR ACTIVITY; NEUROGENESIS; NEURONS; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; STEM CELLS;

EID: 64249102516     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2009.01.018     Document Type: Article

References (61)

1. Azari M.F., Profyris C., Le Grande M.R., Lopes E.C., Hirst J., Petratos S., and Cheema S.S. Effects of intraperitoneal injection of Rofecoxib in a mouse model of ALS. Eur. J. Neurol. 12 5 (2005) 357-364
2. Bagley C.J., Woodcock J.M., Guthridge M.A., Stomski F.C., and Lopez A.F. Structural and functional hot spots in cytokine receptors. Int. J. Hematol. 73 3 (2001) 299-307
3. Barde Y.A. Trophic factors and neuronal survival. Neuron 2 6 (1989) 1525-1534
4. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12 1 (1995) 1-21
5. Batchelor P.E., Liberatore G.T., Wong J.Y., Porritt M.J., Frerichs F., Donnan G.A., and Howells D.W. Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J. Neurosci. 19 5 (1999) 1708-1716
6. Bouhy D., Malgrange B., Multon S., Poirrier A.L., Scholtes F., Schoenen J., and Franzen R. Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J. 20 8 (2006) 1239-1241
7. Chitnis S., Mondal D., and Agrawal K.C. Zidovudine (AZT) treatment suppresses granulocyte-monocyte colony stimulating factor receptor type alpha (GM-CSFR alpha) gene expression in murine bone marrow cells. Life Sci. 71 8 (2002) 967-978
8. Cummings B.J., Uchida N., Tamaki S.J., Salazar D.L., Hooshmand M., Summers R., Gage F.H., and Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. U.S.A. 102 39 (2005) 14069-14074
9. Dame J.B., Christensen R.D., and Juul S.E. The distribution of granulocyte-macrophage colony-stimulating factor and its receptor in the developing human fetus. Pediatr. Res. 46 4 (1999) 358-366
10. Eide F.F., Lowenstein D.H., and Reichardt L.F. Neurotrophins and their receptors-current concepts and implications for neurologic disease. Exp. Neurol. 121 2 (1993) 200-214
11. Elkabes S., DiCicco-Bloom E.M., and Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci. 16 8 (1996) 2508-2521
12. Fischer H.G., and Reichmann G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J. Immunol. 166 4 (2001) 2717-2726
13. Franzen R., Bouhy D., and Schoenen J. Nervous system injury: focus on the inflammatory cytokine 'granulocyte-macrophage colony stimulating factor'. Neurosci. Lett. 361 1-3 (2004) 76-78
14. Friedman B., Kleinfeld D., Ip N.Y., Verge V.M., Moulton R., Boland P., Zlotchenko E., Lindsay R.M., and Liu L. BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15 2 (1995) 1044-1056
15. Frisén J., Johansson C.B., Török C., Risling M., and Lendahl U. Rapid, widespread, and longlasting induction of nestin contribute to the generation of glial scar tissue after CNS injury. J. Cell Biol. 131 2 (1995) 453-464
16. Ha Y., Kim Y.S., Cho J.M., Yoon S.H., Park S.R., Yoon D.H., Kim E.Y., and Park H.C. Role of granulocyte-macrophage colony-stimulating factor in preventing apoptosis and improving functional outcome in experimental spinal cord contusion injury. J. Neurosurg. Spine 2 1 (2005) 55-61
17. Hauben E., Gothilf A., Cohen A., Butovsky O., Nevo U., Smirnov I., Yoles E., Akselrod S., and Schwartz M. Vaccination with dendritic cells pulsed with peptides of myelin basic protein promotes functional recovery from spinal cord injury. J. Neurosci. 23 25 (2003) 8808-8819
18. Hauben E., Nevo U., Yoles E., Moalem G., Agranov E., Mor F., Akselrod S., Neeman M., Cohen I.R., and Schwartz M. Autoimmune T cells as potential neuroprotective therapy for spinal cord injury. Lancet 355 9200 (2000) 286-287
19. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., and Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20 6 (2000) 2218-2228
20. Huang X., Choi J.K., Park S.R., Ha Y., Park H., Yoon S.H., Park H.C., Park J.O., and Choi B.H. GM-CSF inhibits apoptosis of neural cells via regulating the expression of apoptosis-related proteins. Neurosci. Res. 58 1 (2007) 50-57
21. Imai F., Suzuki H., Oda J., Ninomiya T., Ono K., Sano H., and Sawada M. Neuroprotective effect of exogenous microglia in global brain ischemia. J. Cereb. Blood Flow Metab. 27 3 (2007) 488-500
22. Johansson C.B., Lothian C., Molin M., Okano H., and Lendahl U. Nestin enhancer requirements for expression in normal and injured adults CNS. J. Neurosci. Res. 69 6 (2002) 784-794
23. Kannan Y., Moriyama M., Sugano T., Yamate J., Kuwamura M., Kagaya A., and Kiso Y. Neurotrophic action of interleukin 3 and granulocyte-macrophage colony-stimulating factor on murine sympathetic neurons. Neuroimmunomodulation 8 3 (2000) 132-141
24. Kawaguchi A., Miyata T., Sawamoto K., Takashita N., Murayama A., Akamatsu W., Ogawa M., Okabe M., Tano Y., Goldman S.A., and Okano H. Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol. Cell Neurosci. 17 2 (2001) 259-273
25. Lazarov-Spiegler O., Solomon A.S., and Schwartz M. Peripheral nerve-stimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24 3 (1998) 329-337
26. Lendahl U., Zimmerman L.B., and Mackay R.D. CNS stem cell express a new class of intermediate filament protein. Cell 66 4 (1990) 713-729
27. Lindsay R.M., Wiegand S.J., Altar C.A., and DiStefano P.S. Neurotrophic factors: from molecule to man. Trends Neurosci. 17 5 (1994) 182-190
28. Lu P., Jones L.L., Snyder E.Y., and Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol. 181 2 (2003) 115-129
29. Marusich M.F., Furneaux H.M., Henion P.D., and Weston J.A. Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol. 25 2 (1994) 143-155
30. Metcalf D. The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature 339 6219 (1989) 27-30
31. Mikami Y., Okano H., Sakaguchi M., Nakamura M., Shimazaki T., Okano H.J., Kawakami Y., Toyama Y., and Toda M. 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. J. Neurosci. Res. 76 4 (2004) 453-465
32. Mikami Y., Toda M., Watanabe M., Nakamura M., Toyama Y., and Kawakami Y. A simple and reliable behavioral analysis of locomotor function after spinal cord injury in mice. Technical note. J. Neurosurg. 97 Suppl. 1 (2002) 142-147
33. Miwa T., Furukawa S., Nakajima K., Furukawa Y., and Kohsaka S. Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia. J. Neurosci. Res. 50 6 (1997) 1023-1029
34. Nakagawa T., Suga S., Kawase T., and Toda M. Intracarotid injection of granulocyte-macrophage colony-stimulating factor induces neuroprotection in a rat transient middle cerebral artery occlusion model. Brain Res. 1089 1 (2006) 179-185
35. Nakajima K., Honda S., Tohyama Y., Imai Y., Kohsaka S., and Kurihara T. Neurotrophin secretion from cultured microglia. J. Neurosci. Res. 65 4 (2001) 322-331
36. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T., and Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110 4 (2002) 429-441
37. Nemunaitis J., Rosenfeld C.S., Ash R., Freedman M.H., Deeg H.J., Appelbaum F., Singer J.W., Flomenberg N., Dalton W., Elfenbein G.J., et al. Phase III randomized, double-blind placebo-controlled trial of rhGM-CSF following allogeneic bone marrow transplantation. Bone Marrow Transplant. 15 6 (1995) 949-954
38. Ohori Y., Yamamoto S., Nagao M., Sugimori M., Yamamoto N., Nakamura K., and Nakafuku M. Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J. Neurosci. 26 46 (2006) 11948-11960
39. Ohta S., Gregg C., and Weiss S. Pituitary adenylate cyclase-activating polypeptide regulates forebrain neural stem cells and neurogenesis in vitro and in vivo. J. Neurosci. Res. 84 6 (2006) 1177-1186
40. Okano H. Stem cell biology of the central nervous system. J. Neurosci. Res. 69 6 (2002) 698-707
41. Okano H., Kaneko S., Okada S., Iwanami A., Nakamura M., and Toyama Y. Regeneration-based therapies for spinal cord injuries. Neurochem. Int. 51 2-4 (2007) 68-73
42. Okano H.J., and Darnell R.B. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17 9 (1997) 3024-3037
43. Park H.C., Shim Y.S., Ha Y., Yoon S.H., Park S.R., Choi B.H., and Park H.S. Treatment of complete spinal cord injury patients by autologous bone marrow cell transplantation and administration of granulocyte-macrophage colony stimulating factor. Tissue Eng. 11 5-6 (2005) 913-922
44. Prewitt C.M., Niesman I.R., Kane C.J., and Houle J.D. Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp. Neurol. 148 2 (1997) 433-443
45. Rabchevsky A.G., and Streit W.J. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J. Neurosci. Res. 47 1 (1997) 34-48
46. Rapalino O., Lazarov-Spiegler O., Agranov E., Velan G.J., Yoles E., Fraidakis M., Solomon A., Gepstein R., Katz A., Belkin M., Hadani M., and Schwartz M. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 4 7 (1998) 814-821
47. Rahpenymai Y., Hietala M.A., Wilhelmsson U., Fotheringham A., Davies I., Nilsson A.K., Zwirner J., Wetsel R.A., Gerard C., Penkny M., and Pekna M. Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J. 25 (2006) 1364-1374
48. Re F., Belyanskaya S.L., Riese R.J., Cipriani B., Fischer F.R., Granucci F., Ricciardi-Castagnoli P., Brosnan C., Stern L.J., Strominger J.L., and Santambrogio L. Granulocyte-macrophage colony-stimulating factor induces an expression program in neonatal microglia that primes them for antigen presentation. J. Immunol. 169 5 (2002) 2264-2273
49. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 5052 (1992) 1707-1710
50. Rowe J.M., Andersen J.W., Mazza J.J., Bennett J.M., Paietta E., Hayes F.A., Oette D., Cassileth P.A., Stadtmauer E.A., and Wiernik P.H. A randomized placebo-controlled phase III study of granulocyte-macrophage colony-stimulating factor in adult patients (> 55 to 70 years of age) with acute myelogenous leukemia: a study of the Eastern Cooperative Oncology Group (E1490). Blood 86 2 (1995) 457-462
51. Santambrogio L., Belyanskaya S.L., Fischer F.R., Cipriani B., Brosnan C.F., Ricciardi-Castagnoli P., Stern L.J., Strominger J.L., and Riese R. Developmental plasticity of CNS microglia. Proc. Natl. Acad. Sci. U.S.A. 98 11 (2001) 6295-6300
52. Sawada M., Itoh Y., Suzumura A., and Marunouchi T. Expression of cytokine receptors in cultured neuronal and glial cells. Neurosci. Lett. 160 2 (1993) 131-134
53. Schabitz W.R., Kruger C., Pitzer C., Weber D., Laage R., Gassler N., Aronowski J., Mier W., Kirsch F., Dittgen T., Bach A., Sommer C., and Schneider A. A neuroprotective function for the hematopoietic protein granulocyte-macrophage colony stimulating factor (GM-CSF). J. Cereb. Blood Flow Metab. 28 1 (2008) 29-43
54. Schermer C., and Humpel C. Granulocyte macrophage-colony stimulating factor activates microglia in rat cortex organotypic brain slices. Neurosci. Lett. 328 2 (2002) 180-184
55. Schwartz M., and Yoles E. Macrophages and dendritic cells treatment of spinal cord injury: from the bench to the clinic. Acta Neurochir. Suppl. 93 (2005) 147-150
56. Stoll G., and Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog. Neurobiol. 58 3 (1999) 233-247
57. Thoenen H. The changing scene of neurotrophic factors. Trends Neurosci. 14 5 (1991) 165-170
58. Thuret S., Moon L.D., and Gage F.H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7 8 (2006) 628-643
59. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., and Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16 23 (1996) 7599-7609
60. Yaguchi M., Ohta S., Toyama Y., Kawakami Y., and Toda M. Functional recovery after spinal cord injury in mice through activation of microglia and dendritic cells after IL-12 administration. J. Neurosci. Res. 86 9 (2008) 1972-1980
61. Yoon S.H., Shim Y.S., Park Y.H., Chung J.K., Nam J.H., Kim M.O., Park H.C., Park S.R., Min B.H., Kim E.Y., Choi B.H., Park H., and Ha Y. Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage-colony stimulating factor (GM-CSF): phase I/II clinical trial. Stem Cells 25 8 (2007) 2066-2073