Efficacy of the coadministration of granulocyte colony-stimulating factor and stem cell factor in the activation of intrinsic cells after spinal cord injury in mice

Journal of Neurosurgery: Spine

Volumn 13, Issue 4, 2010, Pages 516-523

  Osada, Takahiro ^a   Watanabe, Masahiko ^a   Hasuo, Atsuhiro ^a   Imai, Masaaki ^a   Suyama, Kaori ^a   Sakai, Daisuke ^a   Kawada, Hiroshi ^a   Matsumae, Mitsunori ^a   Mochida, Joji ^a  

^a TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Bone marrow derived cell; Granulocyte colony stimulating factor; Intrinsic cell; Microglia; Oligodendrocyte progenitor cell; Spinal cord injury; Stem cell factor

Indexed keywords

GREEN FLUORESCENT PROTEIN; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; RECOMBINANT STEM CELL FACTOR; DRUG COMBINATION; GRANULOCYTE COLONY STIMULATING FACTOR; LUMINESCENT AGENT; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFICACY; HEMATOPOIETIC STEM CELL; IMMUNOHISTOCHEMISTRY; MOTOR PERFORMANCE; MOUSE; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; RATING SCALE; SPINAL CORD INJURY; TRANSGENIC MOUSE; WHOLE BODY RADIATION; ANIMAL; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL COUNT; CELL PROLIFERATION; COMPARATIVE STUDY; DRUG COMBINATION; DRUG EFFECTS; DRUG POTENTIATION; GENETICS; HINDLIMB; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; MICROGLIA; MOTOR ACTIVITY; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; STEM CELL; TIME;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL COUNT; CELL PROLIFERATION; DRUG COMBINATIONS; DRUG SYNERGISM; GRANULOCYTE COLONY-STIMULATING FACTOR; GREEN FLUORESCENT PROTEINS; HINDLIMB; INJECTIONS, INTRAVENOUS; LUMINESCENT AGENTS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MOTOR ACTIVITY; NEURONS; OLIGODENDROGLIA; PHENOTYPE; SPINAL CORD INJURIES; STEM CELL FACTOR; STEM CELLS; TIME FACTORS;

EID: 77957943588     PISSN: 15475654     EISSN: 15475646     Source Type: Journal    
DOI: 10.3171/2010.4.SPINE09973     Document Type: Article

References (49)

1. Basso DM, Beattie MS, Bresnahan JC: A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21, 1995
2. Basso DM, Beattie MS, Bresnahan JC: Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256, 1996
3. Bomstein Y, Marder JB, Vitner K, Smirnov I, Lisaey G, Butovsky O, et al: Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J Neuroimmunol 142:10-16, 2003 (Pubitemid 38368584)
4. Bouhy D, Malgrange B, Multon S, Poirrier AL, Scholtes F, Schoenen J, et al: Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J 20:1239-1241, 2006
5. Buss A, Schwab ME: Sequential loss of myelin proteins during Wallerian degeneration in the rat spinal cord. Glia 42: 424-432, 2003
6. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J: Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-683, 1997 (Pubitemid 28016354)
7. Dhandapani KM, Wade FM, Wakade C, Mahesh VB, Brann DW: Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappaB. J Neurochem 95:9-19, 2005 (Pubitemid 41384421)
8. Dougherty KD, Dreyfus CF, Black IB: Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 7 (6 Pt B):574-585, 2000
9. Franzen R, Schoenen J, Leprince P, Joosten E, Moonen G, Martin D: Effects of macrophage transplantation in the injured adult rat spinal cord: a combined immunocytochemical and biochemical study. J Neurosci Res 51:316-327, 1998 (Pubitemid 28078463)
10. Gibson CL, Bath PM, Murphy SP: G-CSF reduces infarct volume and improves functional outcome after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 25:431-439, 2005
11. Hess DA, Levac KD, Karanu FN, Rosu-Myles M, White MJ, Gallacher L, et al: Functional analysis of human hematopoietic repopulating cells mobilized with granulocyte colony-stimulating factor alone versus granulocyte colony-stimulating factor in combination with stem cell factor. Blood 100:869-878, 2002 (Pubitemid 34832612)
12. Ikeda O, Murakami M, Ino H, Yamazaki M, Nemoto T, Koda M, et al: Acute up-regulation of brain-derived neurotrophic factor expression resulting from experimentally induced injury in the rat spinal cord. Acta Neuropathol 102:239-245, 2001 (Pubitemid 32816144)
13. Imai M, Watanabe M, Suyama K, Osada T, Sakai D, Kawada H, et al: Delayed accumulation of activated macrophages and inhibition of remyelination after spinal cord injury in an adult rodent model. J Neurosurg Spine 8:58-66, 2008
14. Inoue T, Kawaguchi S, Kurisu K: Spontaneous regeneration of the pyramidal tract after transection in young rats. Neurosci Lett 247:151-154, 1998 (Pubitemid 28240119)
15. Jin K, Mao XO, Sun Y, Xie L, Greenberg DA: Stem cell factor stimulates neurogenesis in vitro and in vivo. J Clin Invest 110:311-319, 2002 (Pubitemid 34847963)
16. Jung KH, Chu K, Lee ST, Kang L, Kim SU, Kim M, et al: GCSF protects human cerebral hybrid neurons against in vitro ischemia. Neurosci Lett 394:168-173, 2006 (Pubitemid 43144844)
17. Jung KH, Chu K, Lee ST, Kim SJ, Sinn DI, Kim SU, et al: Granulocyte colony-stimulating factor stimulates neurogenesis via vascular endothelial growth factor with STAT activation. Brain Res 1073-1074:190-201, 2006
18. Kanellakis P, Slater NJ, Du XJ, Bobik A, Curtis DJ: Granulocyte colony-stimulating factor and stem cell factor improve endogenous repair after myocardial infarction. Cardiovasc Res 70:117-125, 2006
19. Kawada H, Fujita J, Kinjo K, Matsuzaki Y, Tsuma M, Miyat ake H, et al: Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood 104:3581-3587, 2004 (Pubitemid 39564430)
20. Kawada H, Takizawa S, Takanashi T, Morita Y, Fujita J, Fukuda K, et al: Administration of hematopoietic cytokines in the subacute phase after cerebral infarction is effective for functional recovery facilitating proliferation of intrinsic neural stem/progenitor cells and transition of bone marrow-derived neuronal cells. Circulation 113:701-710, 2006
21. Koda M, Nishio Y, Kamada T, Someya Y, Okawa A, Mori C, et al: Granulocyte colony-stimulating factor (G-CSF) mobilizes bone marrow-derived cells into injured spinal cord and promotes functional recovery after compression-induced spinal cord injury in mice. Brain Res 1149:223-231, 2007 (Pubitemid 46659901)
22. Komine-Kobayashi M, Zhang N, Liu M, Tanaka R, Hara H, Osaka A, et al: Neuroprotective effect of recombinant human granulocyte colony-stimulating factor in transient focal ischemia of mice. J Cereb Blood Flow Metab 26:402-413, 2006
23. Lee J, Kuroda S, Shichinohe H, Ikeda J, Seki T, Hida K, et al: Migration and differentiation of nuclear fluorescence-labeled bone marrow stromal cells after transplantation into cerebral infarct and spinal cord injury in mice. Neuropathology 23:169-180, 2003 (Pubitemid 37210130)
24. Lytle JM, Vicini S, Wrathall JR: Phenotypic changes in NG2+ cells after spinal cord injury. J Neurotrauma 23:1726-1738, 2006 (Pubitemid 46034447)
25. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB: Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp Neurol 169:239-254, 2001 (Pubitemid 32524420)
26. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, et al: Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5:1410-1412, 1999
27. Nakajima K, Kohsaka S: Functional roles of microglia in the brain. Neurosci Res 17:187-203, 1993
28. Nakajima K, Kohsaka S: Functional roles of microglia in the central nervous system. Hum Cell 11:141-155, 1998
29. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS: Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 184:313-325, 2003 (Pubitemid 37444041)
30. Nishio Y, Koda M, Kamada T, Someya Y, Kadota R, Mannoji C, et al: Granulocyte colony-stimulating factor attenuates neuronal death and promotes functional recovery after spinal cord injury in mice. J Neuropathol Exp Neurol 66:724-731, 2007 (Pubitemid 47344251)
31. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, Nakamura M, et al: 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, 2002 (Pubitemid 34984709)
32. Parr AM, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, et al: Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155:760-770, 2008
33. Perry VH, Brown MC, Gordon S: The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J Exp Med 165:1218-1223, 1987
34. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT: Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365, 1999 (Pubitemid 29382826)
35. Prewitt CM, Niesman IR, Kane CJ, Houlé JD: Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 148:433-443, 1997 (Pubitemid 28068839)
36. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, et al: Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821, 1998 (Pubitemid 28331023)
37. Schäbitz WR, Kollmar R, Schwaninger M, Juettler E, Bardutzky J, Schölzke MN, et al: Neuroprotective effect of granulocyte colony-stimulating factor after focal cerebral ischemia. Stroke 34:745-751, 2003 (Pubitemid 36307405)
38. Shyu WC, Lin SZ, Yang HI, Tzeng YS, Pang CY, Yen PS, et al: Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 110:1847-1854, 2004
39. Suyama K, Watanabe M, Sakai D, Osada T, Imai M, Mochida J: Nkx2.2 expression in differentiation of oligodendrocyte precursor cells and inhibitory factors for differentiation of oligodendrocytes after traumatic spinal cord injury. J Neurotrauma 24:1013-1025, 2007 (Pubitemid 47015435)
40. Teng YD, Lavik EB, Qu X, Park KI, Ourednik J, Zurakowski D, et al: Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci U S A 99:3024-3029, 2002 (Pubitemid 34240579)
41. Toth ZE, Leker RR, Shahar T, Pastorino S, Szalayova I, Asemenew B, et al: The combination of granulocyte colony-stimulating factor and stem cell factor significantly increases the number of bone marrow-derived endothelial cells in brains of mice following cerebral ischemia. Blood 111:5544-5552, 2008
42. Tripathi R, McTigue DM: Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia 55:698-711, 2007 (Pubitemid 46663023)
43. Urdzíková L, Jendelová P, Glogarová K, Burian M, Hájek M, Syková E: Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J Neurotrauma 23:1379-1391, 2006
44. Vroemen M, Aigner L, Winkler J, Weidner N: Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur J Neurosci 18:743-751, 2003 (Pubitemid 37059685)
45. Watanabe M, Toyama Y, Nishiyama A: Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69:826-836, 2002 (Pubitemid 34984700)
46. Watanabe T, Yamamoto T, Abe Y, Saito N, Kumagai T, Kayama H: Differential activation of microglia after experimental spinal cord injury. J Neurotrauma 16:255-265, 1999 (Pubitemid 29141142)
47. Zhao LR, Navalitloha Y, Singhal S, Mehta J, Piao CS, Guo WP, et al: Hematopoietic growth factors pass through the bloodbrain barrier in intact rats. Exp Neurol 204:569-573, 2007 (Pubitemid 46497044)
48. Zhang SC, Fedoroff S: Cellular localization of stem cell factor and c-kit receptor in the mouse nervous system. J Neurosci Res 47:1-15, 1997
49. Zhang SC, Fedoroff S: Modulation of microglia by stem cell factor. J Neurosci Res 53:29-37, 1998 (Pubitemid 28308979)