Neuroprotective effects of adipose-derived stem cells against ischemic neuronal damage in the rabbit spinal cord

Journal of the Neurological Sciences

Volumn 317, Issue 1-2, 2012, Pages 40-46

  Chung, Jin Young ^a   Kim, Woosuk ^b   Im, Wooseok ^a   Yoo, Dae Young ^b   Choi, Jung Hoon ^c   Hwang, In Koo ^b   Won, Moo Ho ^c   Chang, In Bok ^d   Cho, Byung Moon ^d   Hwang, Hyung Sik ^d   Moon, Seung Myung ^d  

^a Seoul National University Hospital   (South Korea)

^b Seoul National University   (South Korea)

^c Kangwon National University   (South Korea)

^d Hallym University   (South Korea)

Author keywords

Adipose derived stem cells; Brain derived neurotrophic factor; Neuroprotection; Transient spinal ischemia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY OCCLUSION; ARTICLE; ASTROCYTOSIS; CELL DIFFERENTIATION; CELL ISOLATION; CELL TYPE; CONTROLLED STUDY; HINDLIMB; MALE; MORPHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RABBIT; SPINAL CORD ISCHEMIA; SPINAL CORD LESION; SPINAL CORD VENTRAL HORN;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; MALE; NEURONS; NEUROPROTECTIVE AGENTS; RABBITS; SPINAL CORD ISCHEMIA; STEM CELL TRANSPLANTATION; STEM CELLS; TREATMENT OUTCOME;

EID: 84860271489     PISSN: 0022510X     EISSN: 18785883     Source Type: Journal    
DOI: 10.1016/j.jns.2012.02.035     Document Type: Article

References (53)

1. Y. Kuniyoshi, K. Koja, K. Miyagi, M. Shimoji, T. Uezu, and K. Arakaki Prevention of postoperative paraplegia during thoracoabdominal aortic surgery Ann Thorac Surg 76 2003 1477 1484 (Pubitemid 37378297)
2. T.A. Sandson, and J.H. Friedman Spinal cord infarction: report of 8 cases and review of the literature Medicine 68 1989 282 292 (Pubitemid 19251932)
3. R. Lin, G. Roseborough, Y. Dong, G.M. Williams, and C. Wei DNA damage and repair system in spinal cord ischemia J Vasc Surg 37 2003 847 858 (Pubitemid 36373375)
4. I. Hwang, J.C. Lee, K.Y. Yoo, J.H. Cho, J.Y. Jung, and T.C. Kang Transient ischemia-induced changes of excitatory amino acid carrier 1 in the ventral horn of the lumbar spinal cord in rabbits Neurol Res 29 2007 310 316 (Pubitemid 46802370)
5. G.J. Wu, W.F. Chen, C.S. Sung, Y.H. Jean, C.M. Shih, and C.Y. Shyu Preventive effects of intrathecal methylprednisolone administration on spinal cord ischemia in rats: the role of excitatory amino acid metabolizing systems Neuroscience 147 2007 294 303
6. F. Chronidou, E. Apostolakis, I. Papapostolou, K. Grintzalis, C.D. Georgiou, and E.N. Koletsis Beneficial effect of the oxygen free radical scavenger amifostine (WR-2721) on spinal cord ischemia/reperfusion injury in rabbits J Cardiothorac Surg 4 2009 50
7. H.L. Dong, Y. Zhang, B.X. Su, Z.H. Zhu, Q.H. Gu, and H.F. Sang Limb remote ischemic preconditioning protects the spinal cord from ischemia-reperfusion injury: a newly identified nonneuronal but reactive oxygen species-dependent pathway Anesthesiology 112 2010 881 891
8. C. Guven, A.O. Borcek, B. Cemil, G. Kurt, Z. Yildirim, and N.L. Ucankus Neuroprotective effects of infliximab in experimental spinal cord ischemic injury J Clin Neurosci 17 2010 1563 1567
9. F. Locatelli, A. Bersano, E. Ballabio, S. Lanfranconi, D. Papadimitriou, and S. Strazzer Stem cell therapy in stroke Cell Mol Life Sci 66 2009 757 772
10. L. Wechsler, D. Steindler, C. Borlongan, M. Chopp, S. Savitz, and R. Deans Stem Cell Therapies as an Emerging Paradigm in Stroke (STEPS): bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke Stroke 40 2009 510 515
11. J. Gimble, and F. Guilak Adipose-derived adult stem cells: isolation, characterization, and differentiation potential Cytotherapy 5 2003 362 369 (Pubitemid 37369023)
12. V. Planat-Benard, J.S. Silvestre, B. Cousin, M. Andre, M. Nibbelink, and R. Tamarat Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives Circulation 109 2004 656 663 (Pubitemid 38198874)
13. J.K. Fraser, I. Wulur, Z. Alfonso, and M.H. Hedrick Fat tissue: an underappreciated source of stem cells for biotechnology Trends Biotechnol 24 2006 150 154
14. Y. Ikegame, K. Yamashita, S. Hayashi, H. Mizuno, M. Tawada, and F. You Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy Cytotherapy 13 2011 675 685
15. T. Nomura, O. Honmou, K. Harada, K. Houkin, H. Hamada, and J.D. Kocsis I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat Neuroscience 136 2005 161 169 (Pubitemid 41483844)
16. T. Honma, O. Honmou, S. Iihoshi, K. Harada, K. Houkin, and H. Hamada Intravenous infusion of immortalized human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat Exp Neurol 199 2006 56 66
17. Y. Horita, O. Honmou, K. Harada, K. Houkin, H. Hamada, and J.D. Kocsis Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat J Neurosci Res 84 2006 1495 1504 (Pubitemid 44683142)
18. + cells derived from human umbilical cord blood in rats with cerebral ischemia Chin Med J (Engl) 119 2006 1744 1748
19. S.K. Kang, D.H. Lee, Y.C. Bae, H.K. Kim, S.Y. Baik, and J.S. Jung Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats Exp Neurol 183 2003 355 366 (Pubitemid 37205078)
20. X. Wei, Z. Du, L. Zhao, D. Feng, G. Wei, and Y. He IFATS collection: the conditioned media of adipose stromal cells protect against hypoxia-ischemia- induced brain damage in neonatal rats Stem Cells 27 2009 478 488
21. Y.C. Yang, B.S. Liu, C.C. Shen, C.H. Lin, M.T. Chiao, and H.C. Cheng Transplantation of adipose tissue-derived stem cells for treatment of focal cerebral ischemia Curr Neurovasc Res 8 2011 1 13
22. J.H. Choi, J.Y. Chung, D.Y. Yoo, I.K. Hwang, K.Y. Yoo, C.H. Lee, B.C. Yan, J.O. Ahn, H.Y. Youn, and M.H. Won Cell proliferation and neuroblast differentiation in the rat dentate gyrus after intrathecal treatment with adipose-derived mesenchymal stem cells Cell Mol Neurobiol 31 2011 1271 1280
23. T. Kiyoshima, S. Fukuda, M. Matsumoto, Y. Iida, S. Oka, and K. Nakakimura Lack of evidence for apoptosis as a cause of delayed onset paraplegia after spinal cord ischemia in rabbits Anesth Analg 96 2003 839 846 (Pubitemid 36245578)
24. H.J. Habisch, M. Janowski, D. Binder, M. Kuzma-Kozakiewicz, A. Widmann, and A. Habich Intrathecal application of neuroectodermally converted stem cells into a mouse model of ALS: limited intraparenchymal migration and survival narrows therapeutic effects J Neural Transm 114 2007 1395 1406 (Pubitemid 350112275)
25. T.P. Jacobs, O. Kempski, D. McKinley, A.J. Dutka, J.M. Hallenbeck, and G. Feuerstein Blood flow and vascular permeability during motor dysfunction in a rabbit model of spinal cord ischemia Stroke 23 1992 367 373
26. Y. Huang, K. Xie, J. Li, N. Xu, G. Gong, and G. Wang Beneficial effects of hydrogen gas against spinal cord ischemia-reperfusion injury in rabbits Brain Res 1378 2011 125 136
27. W.M. Moore Jr., and L.H. Hollier The influence of severity of spinal cord ischemia in the etiology of delayed-onset paraplegia Ann Surg 213 1991 427 431
28. W. Wisselink, P. Patetsios, T.F. Panetta, J.A. Ramirez, W. Rodino, and J.D. Kirwin Medium molecular weight pentastarch reduces reperfusion injury by decreasing capillary leak in an animal model of spinal cord ischemia J Vasc Surg 27 1998 109 116 (Pubitemid 28081166)
29. I.K. Hwang, K.Y. Yoo, H. Li, O.K. Park, C.H. Lee, and J.H. Choi Indole-3-propionic acid attenuates neuronal damage and oxidative stress in the ischemic hippocampus J Neurosci Res 87 2009 2126 2137
30. P.A. Zuk, M. Zhu, H. Mizuno, J. Huang, J.W. Futrell, and A.J. Katz Multilineage cells from human adipose tissue: implications for cell-based therapies Tissue Eng 7 2001 211 228 (Pubitemid 32295155)
31. P.A. Zuk, M. Zhu, P. Ashjian, D.A. De Ugarte, J.I. Huang, and H. Mizuno Human adipose tissue is a source of multipotent stem cells Mol Biol Cell 13 2002 4279 4295 (Pubitemid 35471185)
32. T.G. Ebrahimian, F. Pouzoulet, C. Squiban, V. Buard, M. Andre, and B. Cousin Cell therapy based on adipose tissue-derived stromal cells promotes physiological and pathological wound healing Arterioscler Thromb Vasc Biol 29 2009 503 510
33. B.T. Estes, B.O. Diekman, J.M. Gimble, and F. Guilak Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype Nat Protoc 5 2010 1294 1311
34. L. de Girolamo, E. Arrigoni, D. Stanco, S. Lopa, A. Di Giancamillo, and A. Addis Role of autologous rabbit adipose-derived stem cells in the early phases of the repairing process of critical bone defects J Orthop Res 29 2011 100 108
35. A.C. Lepore, A. Bakshi, S.A. Swanger, M.S. Rao, and I. Fischer Neural precursor cells can be delivered into the injured cervical spinal cord by intrathecal injection at the lumbar cord Brain Res 1045 2005 206 216 (Pubitemid 40725237)
36. A. Bakshi, A.L. Barshinger, S.A. Swanger, V. Madhavani, J.S. Shumsky, and B. Neuhuber Lumbar puncture delivery of bone marrow stromal cells in spinal cord contusion: a novel method for minimally invasive cell transplantation J Neurotrauma 23 2006 55 65 (Pubitemid 43191086)
37. H. Kim, H.Y. Kim, M.R. Choi, S. Hwang, K.H. Nam, and H.C. Kim Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice Neurosci Lett 468 2010 190 194
38. J. Chen, Y. Li, L. Wang, Z. Zhang, D. Lu, and M. Lu Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats Stroke 32 2001 1005 1011 (Pubitemid 32285175)
39. D.C. Hess, W.D. Hill, A. Martin-Studdard, J. Carroll, J. Brailer, and J. Carothers Bone marrow as a source of endothelial cells and NeuN-expressing cells after stroke Stroke 33 2002 1362 1368 (Pubitemid 34517061)
40. Z.G. Zhang, L. Zhang, Q. Jiang, and M. Chopp Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse Circ Res 90 2002 284 288 (Pubitemid 34633929)
41. J.M. Kim, S.T. Lee, K. Chu, K.H. Jung, E.C. Song, and S.J. Kim Systemic transplantation of human adipose stem cells attenuated cerebral inflammation and degeneration in a hemorrhagic stroke model Brain Res 1183 2007 43 50 (Pubitemid 350103784)
42. C.K. Petito, S. Morgello, J.C. Felix, and M.L. Lesser The two patterns of reactive astrogliosis in postischemic rat brain J Cereb Blood Flow Metab 10 1990 850 859 (Pubitemid 20345226)
43. R.P. Kraig, C.D. Lascola, and A. Caggiano Glial response to brain ischemia H. Kettenmann, B. Ransom, Neuroglia 1995 Oxford Press New York 964 976
44. S.H. Choi, D.Y. Lee, S.U. Kim, and B.K. Jin Thrombin-induced oxidative stress contributes to the death of hippocampal neurons in vivo: role of microglial NADPH oxidase J Neurosci 25 2005 4082 4090
45. N. Tateishi, T. Mori, Y. Kagamiishi, S. Satoh, N. Katsube, and E. Morikawa Astrocytic activation and delayed infarct expansion after permanent focal ischemia in rats. Part II: suppression of astrocytic activation by a novel agent (R)-(-)-2-propyloctanoic acid (ONO-2506) leads to mitigation of delayed infarct expansion and early improvement of neurologic deficits J Cereb Blood Flow Metab 22 2002 723 734 (Pubitemid 34596465)
46. T. Mori, N. Tateishi, Y. Kagamiishi, T. Shimoda, S. Satoh, and S. Ono Attenuation of a delayed increase in the extracellular glutamate level in the peri-infarct area following focal cerebral ischemia by a novel agent ONO-2506 Neurochem Int 45 2004 381 387 (Pubitemid 38625628)
47. M. Chopp, and Y. Li Treatment of neural injury with marrow stromal cells Lancet Neurol 1 2002 92 100 (Pubitemid 37163494)
48. K. Kurozumi, K. Nakamura, T. Tamiya, Y. Kawano, K. Ishii, and M. Kobune Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model Mol Ther 11 2005 96 104 (Pubitemid 40012003)
49. D.F. Kalbermatten, D. Schaakxs, P.J. Kingham, and M. Wiberg Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat Cell Tissue Res 344 2011 251 260
50. T. Lopatina, N. Kalinina, M. Karagyaur, D. Stambolsky, K. Rubina, and A. Revischin Adipose-derived stem cells stimulate regeneration of peripheral nerves: BDNF secreted by these cells promotes nerve healing and axon growth de novo PLoS One 6 2011 e17899
51. Y.C. Lin, T.L. Ko, Y.H. Shih, M.Y. Lin, T.W. Fu, and H.S. Hsiao Human umbilical mesenchymal stem cells promote recovery after ischemic stroke Stroke 42 2011 2045 2053
52. I. Kiprianova, T.M. Freiman, S. Desiderato, S. Schwab, R. Galmbacher, and F. Gillardon Brain-derived neurotrophic factor prevents neuronal death and glial activation after global ischemia in the rat J Neurosci Res 56 1999 21 27 (Pubitemid 29190612)
53. Q. Shi, P. Zhang, J. Zhang, X. Chen, H. Lu, and Y. Tian Adenovirus-mediated brain-derived neurotrophic factor expression regulated by hypoxia response element protects brain from injury of transient middle cerebral artery occlusion in mice Neurosci Lett 465 2009 220 225