G-csf as an adjunctive therapy with umbilical cord blood cell transplantation for traumatic brain injury

Cell Transplantation

Volumn 24, Issue 3, 2015, Pages 447-457

  De La Peña, Ike ^a   Sanberg, Paul R ^a   Acosta, Sandra ^a   Lin, Shinn Zong ^b,c,d   Borlongan, Cesar V ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Granulocyte colony stimulating factor (G CSF); Neuroinflammation; Stem cells; Traumatic brain injury (TBI)

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; NEUROPROTECTIVE AGENT;

ADULT STEM CELL; AMNION CELL; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; BLOOD CELL; BONE MARROW STROMA CELL; BRAIN EDEMA; BYSTANDER EFFECT; CELL DEATH; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; DRUG INDICATION; DRUG MECHANISM; DRUG SAFETY; DRUG USE; GRANULOCYTE PRECURSOR; HUMAN; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NERVE REGENERATION; NEUROPROTECTION; NEUTROPHIL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RECOMBINANT DNA TECHNOLOGY; STEM CELL MOBILIZATION; STEM CELL TRANSPLANTATION; THERAPY EFFECT; TRAUMATIC BRAIN INJURY; UMBILICAL CORD BLOOD; ANIMAL; BIOLOGICAL THERAPY; BRAIN INJURIES; CYTOLOGY; FETUS BLOOD; STEM CELL;

ANIMALS; BRAIN INJURIES; CELL- AND TISSUE-BASED THERAPY; FETAL BLOOD; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84927137441     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368915X686913     Document Type: Article

References (134)

1. Acosta, S. A.; Franzese, N.; Staples, M.; Weinbren, N. L.; Babilonia, M.; Patel, J.; Merchant, N.; Simancas, A. J.; Slakter, A.; Caputo, M.; Patel, M.; Franyuti, G.; Franzblau, M. H.; Suarez, L.; Gonzales-Portillo, C.; Diamandis, T.; Shinozuka, K.; Tajiri, N.; Sanberg, P. R.; Kaneko, Y.; Miller, L. W.; Borlongan, C. V. Human umbilical cord for transplantation therapy in myocardial infarction. J. Stem Cell Res. Ther. 1 Suppl 4:S004-005; 2013.
2. Acosta, S. A.; Tajiri, N.; Shinozuka, K.; Ishikawa, H.; Sanberg, P. R.; Sanchez-Ramos, J.; Song, S.; Kaneko, Y.; Borlongan, C. V. Combination therapy of human umbilical cord blood cells and granulocyte colony stimulating factor reduces histopathological and motor impairments in an experimental model of chronic traumatic brain injury. PLos One 9(3):e90953; 2014.
3. Arciniegas, D. B.; Anderson, A. C.; Topkoff, J.; McAllister, T. W. Mild traumatic brain injury: A neuropsychiatric approach to diagnosis, evaluation, and treatment. Neuropsychiatr. Dis. Treat. 1(4): 311–327; 2005.
4. Azouvi, P.; Vallat-Azouvi, C.; Belmont, A. Cognitive deficits after traumatic coma. Prog. Brain Res. 177: 89–110; 2009.
5. Balseanu, A. T.; Buga, A. M.; Catalin, B.; Wagner, D. C.; Boltze, J.; Zagrean, A. M.; Reymann, K.; Schaebitz, W.; Popa-Wagner, A. Multimodal approaches for regenerative stroke therapies: Combination of granulocyte colonystimulating factor with bone marrow mesenchymal stem cells is not superior to G-CSF alone. Front. Aging Neurosci. 6:130; 2014.
6. Bao-Guo, X. Cell biology and clinical promise of G-CSF: Immunomodulation and neuroprotection. J. Cell. Mol. Med. 11(6): 1272–1290;2007.
7. Beekman, R.; Valkhof, M. G.; Sanders, M. A.; van Strien, P. M.; Haanstra, J. R.; Broeders, L.; Geertsma-Kleinekoort, W. M.; Veerman, A. J.; Valk, P. J.; Verhaak, R. G.; Löwenberg, B.; Touw, I. P. Sequential gain of mutations in severe congenital neutropenia progressing to acute myeloid leukemia. Blood 119(22):5071–5077; 2012.
8. Bensinger, W.; Singer, J.; Appelbaum, F.; Lilleby, K.; Longin, K.; Rowley, S.; Clarke, E.; Clift, R.; Hansen, J.; Shields, T.; Storb, R.; Weaver, P.; Weiden, P.; Bucker, C. D. Autologous transplantation with peripheral blood progenitor mononuclear cells collected after administration of recombinant granulocyte stimulating factor. Blood 81:3158–3163;1993.
9. Blumbergs, P. C.; Jones, N. R.; North, J. B. Diffuse axonal injury in head trauma. J. Neurol. Neurosurg. Psychiatry 52: 838–841;1989.
10. Bodine, D. M.; Seidel, N. E.; Gale, M. S.; Nienhuis, A. W.; Orlic, D. Efficient retrovirus transduction of mouse pluripotent hematopoietic stem cells mobilized into the peripheral blood by treatment with granulocyte colony-stimulating factor and stem cell factor. Blood 84(5):1482–1491;1994.
11. Boltze, J.; Reich, D. M.; Hau, S.; Reymann, K. G.; Strassburger, M.; Lobsien, D.; Wagner, D. C.; Kamprad, M.; Stahl, T. Assessment of neuroprotective effects of human umbilical cord blood mononuclear cell subpopulations in vitro and in vivo. Cell Transplant. 21(4):723–37; 2012.
12. Borlongan, C. V. Bone marrow stem cell mobilization in stroke: A ‘bonehead’ may be good after all! Leukemia 25: 1674–1686; 2011.
13. Brain Trauma Foundation; American Association of Neurological Surgeons; Congress of Neurological Surgeons; Joint Section on Neurotrauma and Critical Care, AANS/CNS, Carney, N. A. Guidelines for the management of severe traumatic brain injury. Methods J. Neurotrauma 24 Suppl 1: S3–6; 2007.
14. Brasure, M.; Lamberty, G. J.; Sayer, N. A.; Nelson, N. W.; Macdonald, R.; Ouellette, J.; Wilt, T. J. Participation after multidisciplinary rehabilitation for moderate to severe traumatic brain injury in adults: A systematic review. Arch. Phys. Med. Rehabil. 94(7):1398–420; 2013.
15. Bronchud, M. H.; Scarffe, J. H.; Thatcher, N.; Crowther, D.; Souza, L. M.; Alton, N. K.; Testa, N. G.; Dexter, T. M. Phase I/II study of recombinant human granulocyte colony-stimulating factor in patients receiving intensive chemotherapy for small cell lung cancer. Br. J. Cancer 56:809–813;1987.
16. Chen, S. J.; Chang, C. M.; Tsai, S. K.; Chang, Y. L.; Chou, S. J.; Huang, S. S.; Tai, L. K.; Chen, Y. C.; Ku, H. H.; Li, H. Y.; Chiou, S. H. Functional improvement of focal cerebral ischemia injury by subdural transplantation of induced pluripotent stem cells with fibrin glue. Stem Cells Dev. 19:1757–67; 2010.
17. Copeland, N.; Harris, D.; Gaballa, M. A. Human umbilical cord blood stem cells, myocardial infarction and stroke. Clin. Med. 9(4):342–5; 2009.
18. Corrigan, J. D.; Selassie, A. W.; Orman, J. A. The epidemiology of traumatic brain injury. J. Head Trauma Rehabil. 25:72–80;2010.
19. Crawford, J.; Ozer, H.; Stoller, R.; Johnson, D.; Lyman, G.; Tabbara, I. Reduction by granulocyte colony-stimulating factor of fever and neutropenia induced by chemotherapy in patients with small-cell lung cancer. N. Engl. J. Med. 325: 164–70; 1991.
20. Dale, D. C.; Bonilla, M. A.; Davis, M. W.; Nakanishi, A. M.; Hammond, W. P.; Kutzberg, J.; Wang, W.; Jakubowski, A.; Winton, E.; Lalezari, P.; Robinson, W.; Glaspy, J. A.; Emerson, S.; Gabrilove, J.; Vincent, M.; Boxer, L. A. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood 81:2496–501; 1993.
21. Dawn, B.; Sanganalmath, S. K.; Bolli, R. G-CSF-induced mobilization of bone marrow stem cells and cardiac repair. In: Molineux, G.; Foote, M.; Arvedson, T. eds. Twenty years of G-CSF, milestones in drug therapy. Basel, Switzerland: Springer Basel AG; 2012:435–455.
22. De Luca, E.; Sheridan, W. P.; Watson, D.; Szer, J.; Begley, C. G. Prior chemotherapy does not prevent effective mobilisation by G-CSF of peripheral blood progenitor cells. Br. J. Cancer 66:893–899;1992.
23. dela Peña, I.; Sanberg, P. R.; Acosta, S.; Tajiri, N.; Lin, S. Z.; Borlongan, C. V. Stem cells and G-CSF for treating neuroinflammation in traumatic brain injury: Aging as a comorbidity factor. J. Neurosurg. Sci. 58(3):145–149; 2014.
24. Demetri, G. D., Griffin, J. D. Granulocyte colony-stimulating factor and its receptor. Blood 78: 2791–2808;1991.
25. Diederich, K.; Sevimli, S.; Dörr, H.; Kösters, E.; Hoppen, M.; Lewejohann, L.; Klocke, R.; Minnerup, J.; Knecht, S.; Nikol, S.; Sachser, N.; Schneider, A.; Gorji, A.; Sommer, C.; Schäbitz, W. R. The role of granulocyte-colony stimulating factor (G-CSF) in the healthy brain. A characterization of G-CSF-deficient mice. J. Neurosci. 29(37):11572–11581; 2009.
26. Dong, F.; Larner, A. C. Activation of Akt kinase by granulocyte colony-stimulating factor (G-CSF): Evidence for the role of tyrosine kinase activity distinct from the Janus kinases. Blood 98:1656–1662; 2000.
27. Duhrsen, U.; Villeval, J.; Boyd, J.; Kannourakis, G.; Morstyn, G.; Metcalf, D. Effects of recombinant human granulocyte colony-stimulating factor on hematopoietic progenitor cells in cancer patients. Blood 72:2074–2081; 1988.
28. England, T. J.; Abaei, M.; Auer, D. P.; Lowe, J.; Jones, D. R.; Sare, G.; Walker, M.; Bath, P. M. Granulocyte-colony stimulating factor for mobilizing bone marrow stem cells in subacute stroke: The stem cell trial of recovery enhancement after stroke 2 randomized controlled trial. Stroke 43: 405–11; 2012.
29. Fabrizio, K. S.; Keltner, N. L. Traumatic brain injury in operation enduring freedom/operation Iraqi freedom: A primer. Nurs. Clin. North Am. 45(4): 569–80; 2010.
30. Faul, M.; Xu, L.; Wald, M. M.; Coronado, V. G. Traumatic brain injury in the United States: Emergency department visits, hospitalizations and deaths. Atlanta (GA): Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010.
31. Fesli, A.; Sari, A.; Yilmaz, N.; Comelekoglu, U.; Tasdelen, B. Enhancement of nerve healing with the combined use of amniotic membrane and granulocyte-colony-stimulating factor. J. Plast. Reconstr. Aesthet. Surg. 67(6):837–843; 2014.
32. Gennarelli, T. A. Mechanisms of brain injury. J. Emerg. Med. 11: 5–11; 1993.
33. Giustini, A.; Pistarini, C.; Pisoni, C. Traumatic and nontraumatic brain injury. Handb. Clin. Neurol. 110:401–409; 2013.
34. Globus, M. Y.; Alonso, O.; Dietrich, W. D.; Busto, R.; Ginsberg, M. D. Glutamate release and free radical production following brain injury: Effects of posttraumatic hypothermia. J. Neurochem. 65(4):1704–11; 1995.
35. Gorin, N. C.; Isnard, F.; Garderet, L.; Ikhlef, S.; Corm, S.; Quesnel, B.; Legrand, O.; Cachanado, M.; Rousseau, A.; Laporte, J. P. Administration of alemtuzumab and G-CSF to adults with relapsed or refractory acute lymphoblastic leukemia: Results of a phase II study. Eur. J. Haematol. 91(4):315–321; 2013.
36. Graham, D. I.; McIntosh, T. K.; Maxwell, W. L.; Nicoll, J. A. Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 59: 641–651; 2000.
37. Guo, X.; Bu, X.; Jiang, J.; Cheng, P.; Yan, Z. Enhanced neuroprotective effects of co-administration of G-CSF with simvastatin on intracerebral hemorrhage in rats. Turk. Neurosurg. 22(6):732–739; 2012.
38. Han, J. L.; Blank, T.; Schwab, S.; Kollmar, R. Inhibited glutamate release by granulocyte-colony stimulating factor after experimental stroke. Neurosci. Lett. 432:167–169; 2008.
39. Hanazono, Y.; Hosoi, T.; Kuwaki, T.; Matsuki, S.; Miyazono, K.; Miyagawa, K.; Takaku, F. Structural analysis of the receptors for granulocyte colony-stimulating factor on neutrophils. Exp. Hematol. 18:1097–1103; 1990.
40. Harris, O. A.; Muh, C. R.; Surles, M. C.; Pan, Y.; Rozycki, G.; Macleod, J.; Easley, K. Discrete cerebral hypothermia in the management of traumatic brain injury. J. Neurosurg. 110:1256–1264; 2009.
41. Henning, R. J.; Shariff, M.; Eadula, U.; Alvarado, F.; Vasko, M.; Sanberg, P. R.; Sanberg, C. D.; Delostia, V. Human cord blood mononuclear cells decrease cytokines and inflammatory cells in acute myocardial infarction. Stem Cells Dev. 17(6):1207–1219; 2008.
42. Hernandez-Ontiveros, D. G.; Tajiri, N.; Acosta, S.; Giunta, B.; Tan, J.; Borlongan, C. V. Microglia activation as a biomarker for traumatic brain injury. Front. Neurol. 4:30; 2013.
43. Huang, H. Y.; Chen, L.; Sanberg, P. R. Clinical achievements, obstacles, falsehoods, and future directions of cellbased neurorestoratology. Cell Transplant. 21(1):S3–S11; 2012.
44. Hunter, M. G.; Avalos, B. R. Phosphatidylinositol 3- kinase and SH2-containing inositol phosphatase (SHIP) are recruited by distinct positive and negative growth-regulatory domains in the granulocyte colony-stimulating factor receptor. J. Immunol. 160:4979–4987; 1998.
45. Ilic, D.; Miere, C.; Lazic, E. Umbilical cord blood cells: Clinical trials in non-hematological disorders. Brit. Med. Bull. 102:43–57; 2012.
46. Iskander, A.; Knight, R. A.; Zhang, Z. G.; Ewing, J. R.; Shankar, A.; Varma, N. R.; Bagher-Ebadian, H.; Ali, M. M.; Arbab, A. S.; Janic, B. Intravenous administration of human umbilical cord blood-derived AC133+ endothelial progenitor cells in rat stroke model reduces infarct volume: Magnetic resonance imaging and histological findings. Stem Cells Transl. Med. 2:703–714; 2013.
47. Kadota, R.; Koda, M.; Kawabe, J.; Hashimoto, M.; Nishio, Y.; Mannoji, C.; Miyashita, T.; Furuya, T.; Okawa, A.; Takahashi, K.; Yamazaki, M. Granulocyte colony-stimulating factor (G-CSF) protects oligodendrocyte and promotes hindlimb functional recovery after spinal cord injury in rats. PLoS One 7(11):e50391; 2012.
48. Kaneko, Y.; Tajiri, N.; Yu, S.; Hayashi, T.; Stahl, C. E.; Bae, E.; Mestre, H.; Franzese, N.; Rodrigues, A. Jr.; Rodrigues, M. C.; Ishikawa, H.; Shinozuka, K.; Hethorn, W.; Weinbren, N.; Glover, L. E.; Tan, J.; Achyuta, A. H.; van Loveren, H.; Sanberg, P. R.; Shivsankar, S.; Borlongan, C. V. Nestin overexpression precedes caspase-3 upregulation in rats exposed to controlled cortical impact traumatic brain injury. Cell Med. 4(2):55–63; 2012.
49. Kawada, H.; Takizawa, S.; Takanashi, T.; Morita, Y.; Fujita, J.; Fukuda, K.; Takagi, S.; Okano, H.; Ando, K.; Hotta, T. 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.
50. Kokjohn, T. A.; Maarouf, C. L.; Daugs, I. D.; Hunter, J. M.; Whiteside, C. M.; Malek-Ahmadi, M.; Rodriguez, E.; Kalback, W.; Jacobson, S. A.; Sabbagh, M. N.; Beach, T. G.; Roher, A. E. Neurochemical profile of dementia pugilistica. J. Neurotrauma 30(11):981–997; 2013.
51. Komine-Kobayashi, M.; Zhang, N.; Liu, M.; Tanaka, R.; Hara, H.; Osaka, A.; Mochizuki, H.; Mizuno, Y.; Urabe, T. Neuroprotective effect of recombinant human granulocyte colony-stimulating factor in transient focal ischemia of mice. J. Cereb. Blood Flow Metab. 26:402–413; 2006.
52. Kumar, A.; Loane, D. J. Neuroinflammation after traumatic brain injury: Opportunities for therapeutic intervention. Brain Behav. Immun. 26(8):1191–1201; 2012.
53. Lee, E. J.; Choi, E. K.; Kang, S. K.; Kim, G. H.; Park, J. Y.; Kang, H. J.; Lee, S. W.; Kim, K. H.; Kwon, J. S.; Lee, K. H.; Ahn, Y.; Lee, H. J.; Cho, H. J.; Choi, S. J.; Oh, W. I.; Park, Y. B.; Kim, H. S. N-cadherin determines individual variations in the therapeutic efficacy of human umbilical cord blood-derived mesenchymal stem cells in a rat model of myocardial infarction. Mol. Ther. 20(1): 155–67; 2012.
54. Lemoli, R. M.; Rosti, G.; Visani, G.; Gherlinzoni, F.; Miggiano, M. C.; Fortuna, A.; Zinzani, P.; Tura, S. Concomitant and sequential administration of recombinant human granulocyte colony-stimulating factor and recombinant human interleukin-3 to accelerate hematopoietic recovery after autologous bone marrow transplantation for malignant lymphoma. J. Clin. Oncol. 14(11):3018–3025; 1996.
55. Li, T.; Ma, Q.; Ning, M.; Zhao, Y.; Hou, Y. Cotransplantation of human umbilical cord-derived mesenchymal stem cells and umbilical cord blood-derived CD34+cells in a rabbit model of myocardial infarction. Mol. Cell. Biochem. 387(1–2): 91–100; 2014.
56. Lieschke, G. J.; Grail, D.; Hodgson, G.; Metcalf, D.; Stanley, E.; Cheers, C.; Fowler, K. J.; Basu, S.; Zhan, Y. F.; Dunn, A. R. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84:1737–1746; 1994.
57. Lindvall, O.; Brundin, P.; Widner, H.; Rehncrona, S.; Gustavii, B.; Frackowiak, R.; Leenders, K. L.; Sawle, G.; Rothwell, J. C.; Marsden, C. D.; Bjorklund, A. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson’s disease. Science 247:574–557; 1990.
58. Liu, Y. P.; Lang, B. T.; Baskaya, M. K.; Dempsey, R. J.; Vemuganti, R. The potential of neural stem cells to repair stroke-induced brain damage. Acta. Neurophatol. 117:469–480; 2009.
59. Lu, J.; Gary, K. W.; Neimeier, J. P.; Ward, J.; Lapane, K. L. Randomized controlled trials in adult traumatic brain injury. Brain Inj. 26:1523–1548; 2012.
60. Luo, J.; Zhang, H. T.; Jiang, X. D.; Xue, S.; Ke, Y. Q. Combination of bone marrow stromal cell transplantation with mobilization by granulocyte-colony stimulating factor promotes functional recovery after spinal cord transection. Acta. Neurochir. (Wien). 151(11):1483–1492; 2009.
61. Maas, A. I.; Stocchetti, N.; Bullock, R. Moderate and severe traumatic brain injury in adults. Lancet Neurol. 7: 728–741; 2008.
62. Mahmood, A.; Lu, D.; Lu, M.; Chopp, M. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 53:697–702, discussion 702–703; 2003.
63. Mahmood, A.; Lu, D.; Qu, C.; Goussev, A.; Chopp, M. Long-term recovery after bone marrow stromal cell treatment of traumatic brain injury in rats. J. Neurosurg. 104: 272–277; 2006.
64. Marshall, L. Head injury: Recent past, present, and future. Neurosurgery 47:546–561; 2000.
65. McAllister, T. W. Neurobiological consequences of traumatic brain injury. Dialogues Clin. Neurosci. 13:287–300; 2011.
66. McIntosh, T. K.; Smith, D. H.; Garde, E. Therapeutic approaches for the prevention of secondary brain injury. Eur. J. Anaesthesiol. 13:291–309; 1996.
67. Metcalf, D. The colony-stimulating factors and cancer. Nat. Rev. Cancer 10:425–434; 2010.
68. Meuer, K.; Pitzer, C.; Teismann, P.; Krüger, C.; Göricke, B.; Laage, R.; Lingor, P.; Peters, K.; Schlachetzki, J. C.; Kobayashi, K.; Dietz, G. P.; Weber, D.; Ferger, B.; Schäbitz, W. R.; Bach, A.; Schulz, J. B.; Bähr, M.; Schneider, A.; Weishaupt, J. H. Granulocyte-colony stimulating factor is neuroprotective in a model of Parkinson’s disease. J. Neurochem. 97:675–686; 2006.
69. Minnerup, J.; Sevimli, S.; Schabitz, W. R. Granulocytecolony stimulating factor for stroke treatment: Mechanisms of action and efficacy in preclinical studies. Exp. Transl. Stroke Med. 1:2; 2009.
70. Morikawa, K.; Morikawa, S.; Nakamura, M.; Miyawaki, T. Characterization of granulocyte colony-stimulating factor receptor expressed on human lymphocytes. Br. J. Haematol. 118:296–304; 2002.
71. Mueller, B. K.; Mueller, R.; Schoemaker, H. Stimulating neuroregeneration as a therapeutic drug approach for traumatic brain injury. Br. J. Pharmacol. 157(5):675–685; 2009.
72. Narayan, R. K.; Michel, M. E.; Ansell, B.; Baethmann, A.; Biegon, A.; Bracken, M. B.; Bullock, M. R.; Choi, S. C.; Clifton, G. L.; Contant, C. F.; Coplin, W. M.; Dietrich, W. D.; Ghajar, J.; Grady, S. M.; Grossman, R. G.; Hall, E. D.; Heetderks, W.; Hovda, D. A.; Jallo, J.; Katz, R. L.; Knoller, N.; Kochanek, P. M.; Maas, A. I.; Majde, J.; Marion, D. W.; Marmarou, A.; Marshall, L. F.; McIntosh, T. K.; Miller, E.; Mohberg, N.; Muizelaar, J. P.; Pitts, L. H.; Quinn, P.; Riesenfeld, G.; Robertson, C. S.; Strauss, K. I.; Teasdale, G.; Temkin, N.; Tuma, R.; Wade, C.; Walker, M. D.; Weinrich, M.; Whyte, J.; Wilberger, J.; Young, A. B.; Yurkewicz, L. Clinical trials in head injury. J. Neurotrauma 19:503–557; 2002.
73. Nemetz, P. N.; Leibson, C.; Naessens, J. M.; Beard, M.; Kokmen, E.; Annegers, J. F.; Kurland, L. T. Traumatic brain injury and time to onset of Alzheimer’s disease: A populationbased study. Am. J. Epidemiol. 149(1):32–40; 1999.
74. Newman, M. B.; Davis, C. D.; Kuzmin-Nichols, N.; Sanberg, P. R. Human umbilical cord blood (HUCB) cells for central nervous system repair. Neurotox. Res. 5(5):355–368; 2003.
75. Newman, M. B.; Misiuta, I.; Willing, A. E.; Zigova, T.; Karl, R. C.; Borlongan, C. V.; Sanberg, P. R. Tumorigenicity issues of embryonic carcinoma-derived stem cells: Relevance to surgical trials using NT2 and hNT neural cells. Stem Cells Dev. 14:29–43; 2005.
76. Nishio, Y.; Koda, M.; Kamada, T.; Someya, Y.; Kadota, R.; Mannoji, C.; Miyashita, T.; Okada, S.; Okawa, A.; Moriya, H.; Yamazaki, M. Granulocyte colony-stimulating factor attenuates neuronal death and promotes functional recovery after spinal cord injury in mice. J. Neuropathol. Exp. Neurol. 66(8):724–731; 2007.
77. Piao, C. S.; Li, B.; Zhang, L. J.; Zhao, L. R. Stem cell factor and granulocyte colony-stimulating factor promote neuronal lineage commitment of neural stem cells. Differentiation 83(1):17–25; 2012.
78. Pimentel-Coelho, P. M.; Rosado-de Castro, P. H.; Barbosa da Fonseca, L. M.; Otero, R. M. Umbilical cord blood mononuclear cell transplantation for neonatal hypoxicischemic encephalophaty. Pediatr. Res. 71:464–473; 2012.
79. Platzer, E.; Welte, K.; Gabrilove, J. L.; Lu, L.; Harris, P.; Mertelsmann, R.; Moore, M. A. S. Biological activities of a human pluripotent hematopoietic colony stimulating factor on normal and leukemic cells. J. Exp. Med. 162:1788–1801; 1985.
80. Popa-Wagner, A.; Stöcker, K.; Balseanu, A. T.; Rogalewski, A.; Diederich, K.; Minnerup, J.; Margaritescu, C.; Schäbitz, W. R. Effects of granulocyte-colony stimulating factor after stroke in aged rats. Stroke 41(5): 1027–31; 2010.
81. Prakash, A.; Medhi, B.; Chopra, K. Granulocyte colony stimulating factor (GCSF) improves memory and neurobehavior in an amyloid-induced experimental model of Alzheimer’s disease. Pharmacol. Biochem. Behav. 110:46–57; 2013.
82. Reilly, P. L. Brain injury: The pathophysiology of the first hours. “Talk and Die revisited.” J. Clin. Neurosci. 8:398–403; 2001.
83. Sakowitz, O. W.; Schardt, C.; Neher, M.; Stover, J. F.; Unterberg, A. W.; Kiening, K. L. Granulocyte colonystimulating factor does not affect contusion size, brain edema or cerebrospinal fluid glutamate concentrations in rats following controlled cortical impact. Acta Neurochir. Suppl. 96:139–143; 2006.
84. Sanberg, P. R.; Eve, D. J.; Cruz, L. E.; Borlongan, C. V. Neurological disorders and the potential role for stem cells as a therapy. Br. Med. Bull. 101:163–181; 2012.
85. Sanberg, P. R.; Eve, D. J.; Metcalf, C.; Borlongan, C. V. Advantages and challenges of alternative sources of adultderived stem cells for brain repair in stroke. Prog. Brain Res. 201:99–117; 2012.
86. Sanberg, P. R.; Willing, A. E.; Garbuzova-Davis, S.; Saporta, S.; Liu, G.; Sanberg, C. D.; Bickford, P. C. Umbilical cord blood-derived stem cells and brain repair. Ann. N. Y. Acad. Sci. 1049:67–83; 2005.
87. Sanchez-Ramos, J.; Cimino, C.; Avila, R.; Rowe, A.; Chen, R.; Whelan, G.; Lin, X.; Cao, C.; Ashok, R. Pilot study of granulocyte-colony stimulating factor for treatment of Alzheimer’s disease. J. Alzheimers Dis. 31(4): 843–55; 2012.
88. Sanchez-Ramos, J.; Song, S.; Sava, V.; Catlow, B.; Lin, X.; Mori, T.; Cao, C.; Arendash, G. W. Granulocyte colony stimulating factor decreases brain amyloid burden and reverses cognitive impairment in Alzheimer’s mice. Neuroscience 163:55–72; 2009.
89. Sandestig, A.; Romner, B.; Grände, P. O. Therapeutic hypothermia in children and adults with severe traumatic brain injury. Ther. Hypothermia Temp. Manag. 4(1): 10–20; 2014.
90. Sandoe, J.; Eggan, K. Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 16(7):780–789; 2013.
91. Sanganalmath, S. K.; Abdel-Latif, A.; Bolli, R.; Xuan, Y. T.; Dawn, B. Hematopoietic cytokines for cardiac repair: Mobilization of bone marrow cells and beyond. Basic Res. Cardiol. 106(5):709–733; 2011.
92. Schabitz, W. R.; Kollmar, R.; Schwaninger, M.; Juettler, E.; Bardutzky, J.; Scholzke, M. N.; Sommer, C.; Schwab, S. Neuroprotective effect of granulocyte colony-stimulating factor after focal cerebral ischemia. Stroke 34:745–751; 2003.
93. Schabitz, W. R.; Laage, R.; Vogt, G.; Koch, W.; Kollmar, R.; Schwab, S.; Schneider, D.; Hamann, G. F.; Rosenkranz, M.; Veltkamp, R.; Fiebach, J. B.; Hacke, W.; Grotta, J. C.; Fisher, M.; Schneider, A. AXIS: A trial of intravenous granulocyte colony-stimulating factor in acute ischemic stroke. Stroke 41:2545–2551; 2010.
94. Schneider, A.; Kuhn, H. G.; Schabitz, W. R. A role for G-CSF (granulocyte colony stimulating factor) in the central nervous system. Cell Cycle 4:1753–1757; 2005.
95. Schneider, A.; Kruger, C.; Steigleder, T.; Weber, D.; Pitzer, C.; Laage, R.; Aronowski, J.; Maurer, M. H.; Gassler, N.; Mier, W.; Hasselblatt, M.; Kollmar, R.; Schwab, S.; Sommer, C.; Bach, A.; Kuhn, H. G.; Schabitz, W. R. The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J. Clin. Invest. 115:2083–2098; 2005.
96. Shahaduzzaman, M.; Golden, J. E.; Green, S.; Gronda, A. E.; Adrien, E.; Ahmed, A.; Sanberg, P. R.; Bickford, P. C.; Gemma, C.; Willing, A. E. A single administration of human umbilical cord blood T cells produces long-lasting effects in the aging hippocampus. Age (Dordr) 35:2071–2087; 2013.
97. Shao, C.; Roberts, K. N.; Markesbery, W. R.; Scheff, S. W.; Lovell, M. A. Oxidative stress in head trauma imaging. Free Radic. Biol. Med. 41:77–85; 2006.
98. Sheridan, W. P.; Begley, C. G.; Juttner, C. A.; Szer, J.; To, L. B.; Maher, D.; McGrath, K. M.; Morstyn, G.; Fox, R. M. Effect of peripheral-blood progenitor cells mobilised by filgrastim (G-CSF) on platelet recovery after high-dose chemotherapy. Lancet 339:640–644; 1992.
99. Sheridan, W. P.; Morstyn, G.; Wolf, M.; Dodds, A.; Lusk, J.; Maher, D.; Layton, J. E.; Green, M. D.; Souza, L.; Fox, R. M. Granulocyte colony stimulating factor and neutrophil recovery after high-dose chemotherapy and autologous bone marrow transplantation. Lancet 2:891–895; 1989.
100. Shim, W.; Mehta, A.; Lim, S. Y.; Zhang, G.; Lim, C. H.; Chua, T.; Wong, P. G-CSF for stem cell therapy in acute myocardial infarction: Friend or foe? Cardiovasc. Res. 89(1):20–30; 2011.
101. Shimoda, K.; Feng, J.; Murakami, H.; Nagata, S.; Watling, D.; Rogers, N. C.; Stark, G. R.; Kerr, I. M.; Ihle, J. N. Jak1 plays an essential role for receptor phosphorylation and Stat activation in response to granulocyte colony-stimulating factor. Blood 90:597–604; 1997.
102. Shimoda, K.; Okamura, S.; Harada, N.; Kondo, S.; Okamura, T.; Niho, Y. Identification of a functional receptor for granulocyte colony-stimulating factor on platelets. J. Clin. Invest. 91:1310–1313; 1993.
103. Shyu, W. C.; Lin, S. Z.; Lee, C. C.; Liu, D. D.; Li, H. Granulocyte colony-stimulating factor for acute ischemic stroke: A randomized controlled trial. CMAJ 174:927–33; 2006.
104. Shyu, W. C.; Lin, S. Z.; Yang, H. I.; Tzeng, Y. S.; Pang, C. Y.; Yen, P. S.; Li, H. Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 110:1847–1854; 2004.
105. Solaroglu, I.; Cahill, J.; Tsubokawa, T.; Beskonakli, E.; Zhang, J. H. Granulocyte colony-stimulating factor protects the brain against experimental stroke via inhibition of apoptosis and inflammation. Neurol. Res. 31(2):167–172; 2009.
106. Solaroglu, I.; Tsubokawa, T.; Cahill, J.; Zhang, J. H. Antiapoptotic effect of granulocyte-colony stimulating factor after focal cerebral ischemia in the rat. Neuroscience 143: 965–974; 2006.
107. Sprigg, N.; Bath, P. M.; Zhao, L.; Willmot, M. R.; Gray, L. J.; Walker, M. F.; Dennis, M. S.; Russell, N. Granulocytecolony- stimulating factor mobilizes bone marrow stem cells in patients with subacute ischemic stroke: The Stem cell Trial of recovery enhancement after Stroke (STEMS) pilot randomized, controlled trial (ISRCTN 16784092). Stroke 37: 2979–83; 2006.
108. Stachura, D. L.; Svoboda, O.; Campbell, C. A.; Espín- Palazón, R.; Lau, R. P.; Zon, L. I.; Bartunek, P.; Traver, D. The zebrafish granulocyte colony stimulating factors (Gcsfs): Two paralogous cytokines and their roles in hematopoietic development and maintenance. Blood 122(24): 3918–3928; 2013.
109. Tajiri, N.; Acosta, S. A.; Shahaduzzaman, M. D.; Ishikawa, H.; Shinozuka, K.; Pabon, M.; Hernandez-Ontiveros, D.; Kim, D. W.; Metcalf, C.; Staples, M.; Dailey, T.; Vasconcellos, J.; Franyuti, G.; Gould, L.; Patel, N.; Cooper, D.; Kaneko, Y.; Borlongan, C. V.; Bickford, P. C. Intravenous transplants of human adipose-derived stem cell protect the brain from traumatic brain injury-induced neurodegeneration and motor and cognitive and cognitive impairments: Cell graft biodistribution and soluble factors in young and aged rats. J. Neurosci. 34(1):313–316; 2014.
110. Takahashi, H.; Yamazaki, M.; Okawa, A.; Sakuma, T.; Kato, K.; Hashimoto, M.; Hayashi, K.; Furuya, T.; Fujiyoshi, T.; Kawabe, J.; Yamauchi, T.; Mannoji, C.; Miyashita, T.; Kadota, R.; Hashimoto, M.; Ito, Y.; Takahashi, K.; Koda, M. Neuroprotective therapy using granulocyte colony-stimulating factor for acute spinal cord injury: A phase I/IIa clinical trial. Eur. Spine J. 21(12): 2580–2587; 2012.
111. Taylor, K. M.; Jagannath, S.; Spitzer, G.; Spinolo, J. A.; Tucker, S. L.; Fogel, B.; Cabanillas, F. F.; Hagemeister, F. B.; Souza, L. M. Recombinant human granulocyte colony stimulating factor hastens granulocyte recovery after high-dose chemotherapy and autologous bone marrow transplantation in Hodgkin’s disease. J. Clin. Oncol. 7:1791–1799; 1989.
112. Temkin, N. R.; Anderson, G. D.; Winn, H. R.; Ellenbogen, R. G.; Britz, G. W.; Schuster, J.; Lucas, T.; Newell, D. W.; Mansfield, P. N.; Machamer, J. E.; Barber, J.; Dikmen, S. S. Magnesium sulfate for neuroprotection after traumatic brain injury: A randomised controlled trial. Lancet Neurol. 6: 29–38; 2007.
113. Thurman, D.; Guerrero, J. Trends in hospitalization traumatic brain injury. JAMA 282:954–957; 1999.
114. Tian, S. S.; Lamb, P.; Seidel, H. M.; Stein, R. B.; Rosen, J. Rapid activation of the STAT3 transcription factor by granulocyte colony-stimulating factor. Blood 84:1760–1764; 1994.
115. Toth, Z. E.; Leker, R. R.; Shahar, T.; Pastorino, S.; Szalayova, I.; Asemenew, B.; Key, S.; Parmelee, A.; Mayer, B.; Nemeth, K.; Bratincsák, A.; Mezey, E. 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.
116. Tsuji, T.; Nishimura-Morita, Y.; Watanabe, Y.; Hirano, D.; Nakanishi, S.; Mori, K. J.; Yatsunami, K. A murine stromal cell line promotes the expansion of CD34high+-primitive progenitor cells isolated from human umbilical cord blood in combination with human cytokines. Growth Factors 16(3):225–240; 1999.
117. Twamley, E. W.; Jak, A. J.; Dellis, D. C.; Bondi, M. W.; Lohr, J. B. Cognitive symptom management and rehabilitation therapy (CogSMART) for veterans with traumatic brain injury: Pilot randomized controlled trial. J. Rehab. Res. Dev. 51(1):59–70; 2014.
118. Urdziková, L.; Likavčanová-Mašínová, K.; Vaněček, V.; Růžičkam, J.; Sedým, J.; Syková, E.; Jendelová, P. Flt3 ligand synergizes with granulocyte-colony-stimulating factor in bone marrow mobilization to improve functional outcome after spinal cord injury in the rat. Cytotherapy 13(9):1090–104; 2011.
119. Verina, T.; Fatemi, A.; Johnston, M. V.; Comi, A. M. Pluripotent possibilities: Human umbilical cord blood cell treatment after neonatal brain injury. Pediatr. Neurol. 48(5): 346–54; 2013.
120. Walker, P. A.; Harting, M. T.; Baumgartner, J. E.; Fletcher, S.; Strobel, N.; Cox, C. S. Jr. Modern approaches to pediatric brain injury therapy. J. Trauma 67 Suppl 2:S120–127; 2009.
121. Walker, P. A.; Shah, S. K.; Jimenez, F.; Aroom, K. R.; Harting, M. T.; Cox, C. S. Jr. Bone marrow-derived stromal cell therapy for traumatic brain injury is neuroprotective via stimulation of non-neurologic organ systems. Surgery 152: 790–793; 2012.
122. Ward, A. C.; Loeb, D. M.; Soede-Bobok, A. A.; Touw, I. P.; Friedman, A. D. Regulation of granulopoiesis by transcription factors and cytokine signals. Leukemia 14:973–990; 2000.
123. Welte, K. Discovery of G-CSF and early clinical studies. In: Molineux, G.; Foote, M.; Arvedson, T. eds. Twenty years of G-CSF, milestones in drug therapy. Basel, Switzerland: Springer Basel AG; 2012:15–24.
124. Werner, C.; Engelhard, K. Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99:4–9; 2007.
125. Willing, A. E.; Vendrame, M.; Mallery, J.; Cassady, C. J.; Davis, C. D.; Sanchez-Ramos, J.; Sanberg, P. R. Mobilized peripheral blood cells administered intravenously produce functional recovery in stroke. Cell Transplant. 12: 449–454; 2003.
126. Wong, D.; Dahm, J.; Ponsford, J. Factor structure of the depression anxiety stress scales in individuals with traumatic brain injury. Brain Inj. 27:1377–1382; 2013.
127. Wong, J. C.; Hazrati, L. N. Parkinson’s disease, Parkinsonism, and traumatic brain injury. Crit. Rev. Clin. Lab. Sci. 50(4–5):103–106; 2013.
128. Woodlock, T.; Morganti-Kossmann, M. C. The role of markers of inflammation in traumatic brain injury. Front. Neurol. 4:18; 2013.
129. Yang, D. Y.; Chen, Y. J.; Wang, M. F.; Pan, H. C.; Chen, S. Y.; Cheng, F. C. Granulocyte colony-stimulating factor enhances cellular proliferation and motor function recovery on rats subjected to traumatic brain injury. Neurol. Res. 32(10):1041–1049; 2010.
130. Yang, M.; Wei, X.; Li, J.; Heine, L. A.; Rosenwasser, R.; Iacovitti, L. Changes in host blood factors and brain glia accompanying the functional recovery after systemic administration of bone marrow stem cells in ischemic stroke rats. Cell Transplant. 19:1073–1084; 2010.
131. Yu, G.; Borlongan, C. V.; Stahl, C. E.; Yu, S. J.; Bae, E.; Yang, T.; Zhou, J.; Li, Y.; Xiong, W.; Qin, L.; Zhou, B. Transplantation of human umbilical cord blood cells for the repair of myocardial infarction. Med. Sci. Monit. 14(10):RA163–172; 2008.
132. Zhang, X. M.; Du, F.; Yang, D.; Wang, R.; Yu, C.; Huang, X. N.; Hu, H. Y.; Liu, W.; Fu, J. Granulocyte colony-stimulating factor increases the therapeutic efficacy of bone marrow mononuclear cell transplantation in cerebral ischemia in mice. BMC Neurosci. 12:61; 2011.
133. Zhang, Y. B.; Li, S. X.; Chen, X. P.; Yang, L.; Zhang, Y. G.; Liu, R.; Tao, L. Y. Autophagy is activated and might protect neurons from degeneration after traumatic brain injury. Neurosci. Bull. 24:143–149; 2008.
134. Zhao, L. R.; Piao, C. S.; Murikinati, S. R.; Gonzalez- Toledo, M. E. The role of stem cell factor and granulocytecolony stimulating factor in treatment of stroke. Recent Pat. CNS Drug Discov. 8(1):2–12; 2013.