Development of a middle cerebral artery occlusion model in the nonhuman primate and a safety study of i.v. infusion of human mesenchymal stem cells

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Sasaki, Masanori ^a,b,c   Honmou, Osamu ^a,b,c   Radtke, Christine ^a,b,d   Kocsis, Jeffery D ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CHLOROCEBUS; COLLATERAL CIRCULATION; CONTROLLED STUDY; FEMALE; FUNCTIONAL STATUS; HEMIPLEGIA; MALE; MESENCHYMAL STEM CELL; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR PERFORMANCE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; VENOUS STASIS; ANIMAL; CELL TRANSPLANTATION; CERCOPITHECUS; DISEASE MODEL; HUMAN; INTRAVENOUS DRUG ADMINISTRATION; MIDDLE CEREBRAL ARTERY; PATHOLOGY; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIMATE;

ANIMALIA; CERCOPITHECUS AETHIOPS; PRIMATES; RODENTIA; SYLVIA;

ANIMALS; ARTERIAL OCCLUSIVE DISEASES; CELL TRANSPLANTATION; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFUSIONS, INTRAVENOUS; MAGNETIC RESONANCE IMAGING; MALE; MESENCHYMAL STEM CELLS; MIDDLE CEREBRAL ARTERY; PRIMATES;

EID: 80055060432     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026577     Document Type: Article

References (54)

1. Li Y, Chen J, Chen XG, Wang L, Gautam SC, et al. (2002) Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59: 514-523.
2. Iihoshi S, Honmou O, Houkin K, Hashi K, Kocsis JD, (2004) A therapeutic window for intravenous administration of autologous bone marrow after cerebral ischemia in adult rats. Brain Res 1007: 1-9.
3. Nomura T, Honmou O, Harada K, Houkin K, Hamada H, et al. (2005) 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: 161-169.
4. Chen J, Chopp M, (2006) Neurorestorative treatment of stroke: cell and pharmacological approaches. NeuroRx 3: 466-473.
5. Chopp M, Li Y, (2006) Transplantation of bone marrow stromal cells for treatment of central nervous system diseases. Adv Exp Med Biol 585: 49-64.
6. Honma T, Honmou O, Iihoshi S, Harada K, Houkin K, et al. (2006) Intravenous infusion of immortalized human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Exp Neurol 199: 56-66.
7. Li Y, McIntosh K, Chen J, Zhang C, Gao Q, et al. (2006) Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp Neurol 198: 313-325.
8. Liu H, Honmou O, Harada K, Nakamura K, Houkin K, et al. (2006) Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 129: 2734-2745.
9. Shen LH, Li Y, Chen J, Cui Y, Zhang C, et al. (2007) One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke 38: 2150-2156.
10. Shen LH, Li Y, Chen J, Zacharek K, Gao Q, et al. (2007) Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 27: 6-13.
11. Omori Y, Honmou O, Harada K, Suzuki J, Houkin K, et al. (2008) Optimization of a therapeutic protocol for intravenous injection of human mesenchymal stem cells after cerebral ischemia in adult rats. Brain Res 1236: 30-38.
12. Onda T, Honmou O, Harada K, Houkin K, Hamada H, et al. (2008) Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 28: 329-340.
13. Pavlichenko N, Sokolova I, Vijde S, Shvedova E, Alexandrov G, et al. (2008) Mesenchymal stem cells transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res 1233: 203-213.
14. Li Y, Chopp M, (2009) Marrow stromal cell transplantation in stroke and traumatic brain injury. Neurosci Lett 456: 120-123.
15. Zhang J, Li Y, Zhang ZG, Lu M, Borneman J, et al. (2009) Bone marrow stromal cells increase oligodendrogenesis after stroke. J Cereb Blood Flow Metab 29: 1166-1174.
16. Liu Z, Li Y, Zhang ZG, Cui X, Cui Y, et al. (2010) Bone marrow stromal cells enhance inter- and intracortical axonal connections after ischemic stroke in adult rats. J Cereb Blood Flow Metab pp. 1288-95.
17. Zacharek A, Shehadah A, Chen J, Cui X, Roberts C, et al. (2010) Comparison of bone marrow stromal cells derived from stroke and normal rats for stroke treatment. Stroke 41: 524-530.
18. Stroke Therapy Academic Industry Roundtable (STAIR) (1999) Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30: 2752-2758.
19. Furuichi Y, Maeda M, Moriguchi A, Sawamoto T, Kawamura A, et al. (2003) Tacrolimus, a potential neuroprotective agent, ameliorates ischemic brain damage and neurologic deficits after focal cerebral ischemia in nonhuman primates. J Cereb Blood Flow Metab 23: 1183-1194.
20. Virley D, Hadingham SJ, Roberts JC, Farnfield B, Elliott H, et al. (2004) A new primate model of focal stroke: endothelin-1-induced middle cerebral artery occlusion and reperfusion in the common marmoset. J Cereb Blood Flow Metab 24: 24-41.
21. de Crespigny AJ, D'Arceuil HE, Maynard KI, Maynard KI, He J, et al. (2005) Acute studies of a new primate model of reversible middle cerebral artery occlusion. J Stroke Cerebrovasc Dis 14: 80-87.
22. Roitberg BZ, Mangubat E, Chen EY, Sugaya K, Thulborn KR, et al. (2006) Survival and early differentiation of human neural stem cells transplanted in a nonhuman primate model of stroke. J Neurosurg 105: 96-102.
23. West GA, Golshani KJ, Doyle KP, Lessov NS, Hobbs TR, et al. (2009) A new model of cortical stroke in the rhesus macaque. J Cereb Blood Flow Metab 29: 1175-1186.
24. Jones TH, Morawetz RB, Crowell RM, Marcoux FW, FitzGibbon SJ, et al. (1981) Thresholds of focal cerebral ischemia in awake monkeys. J Neurosurg 54: 773-782.
25. Rink C, Christoforidis G, Abduljalil A, Kontzialis M, Bergdall V, et al. (2008) Minimally invasive neuroradiologic model of preclinical transient middle cerebral artery occlusion in canines. Proc Natl Acad Sci U S A 105: 14100-14105.
26. Sasaki M, Honmou O, Kocsis JD, (2009) A rat middle cerebral artery occlusion model and intravenous cellular delivery. Methods Mol Biol 549: 187-195.
27. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, et al. (2009) Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40: 2244-2250.
28. Courtine G, Bunge MB, Fawcett JW, Grossman RG, Kaas JH, et al. (2007) Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat Med 13: 561-566.
29. Roitberg B, Khan N, Tuccar E, Kompoliti K, Chu Y, et al. (2003) Chronic ischemic stroke model in cynomolgus monkeys: behavioral, neuroimaging and anatomical study. Neurol Res 25: 68-78.
30. Fukuda S, del Zoppo G, (2003) Models of focal cerebral ischemia in the nonhuman primate. ILAR J 44: 96-104.
31. Imai H, Konno K, Nakamura M, Shimizu T, Kubota C, et al. (2006) A new model of focal cerebral ischemia in the miniature pig. J Neurosurg 104: 123-132.
32. Boltze J, Förschler A, Nitzsche B, Waldmin D, Hoffmann A, et al. (2008) Permanent middle cerebral artery occlusion in sheep: a novel large animal model of focal cerebral ischemia. J Cereb Blood Flow Metab 28: 1951-1964.
33. Rasmussen P, (2009) The evolution and role of endovascular therapy for the treatment of intracranial atherosclerotic disease. J Neuroimaging 19 (Suppl. 1): 30S-34S.
34. Longa E, Weinstein P, Carlson S, Cummins R, (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91.
35. Kalfas I, Little J, (1988) Postoperative hemorrhage: a survey of 4992 intracranial procedures. Neurosurgery 23: 343-347.
36. Chen X, Li Y, Wang L, Katakowski M, Zhang L, et al. (2002) Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22: 275-279.
37. Parr AM, Tator CH, Keating A, (2007) Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 40: 609-619.
38. Sasaki M, Radtke C, Tan AM, Zhao P, Hamada H, et al. (2009) BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. J Neurosci 29: 14932-14941.
39. Shen LH, Li Y, Chen J, Zhang J, Vanquri P, et al. (2006) Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience 137: 393-399.
40. Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, et al. (2008) Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A 105: 14638-14643.
41. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, et al. (2009) Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 57: 1192-203.
42. Kurozumi K, Nakamura K, Tamiya T, Kawano Y, Kobune M, et al. (2004) BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol Ther 9: 189-197.
43. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, et al. (2006) 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: 1495-1504.
44. Miki Y, Nonoguchi N, Ikeda N, Coffin R, Kuroiwa T, et al. (2007) Vascular endothelial growth factor gene-transferred bone marrow stromal cells engineered with a herpes simplex virus type 1 vector can improve neurological deficits and reduce infarction volume in rat brain ischemia. Neurosurgery 61: 586-594.
45. Toyama K, Honmou O, Harada K, Suzuki J, Houkin K, et al. (2009) Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp Neurol 216: 47-55.
46. Bang OY, Lee JS, Lee PH, Lee G, (2005) Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 57: 874-882.
47. Honmou O, Houkin K, Matsunaga T, Niitsu Y, Ishiai S, et al. (2011) Intravenous administration of auto serum-expanded autologous mesenchymal stem cells derived from bone marrow into stroke patients. Brain Jun;134 (Pt 6): 1790-807.
48. Suárez-Monteagudo C, Hernández-Ramírez P, Alvarez-González L, García-Maeso I, de la Cuétara-Bernal K, et al. (2009) Autologous bone marrow stem cell neurotransplantation in stroke patients. An open study. Restor Neurol Neurosci 27: 151-161.
49. Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, et al. (2010) A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 28: 1099-1106.
50. Isakova IA, Baker K, Dufour J, Gaupp D, Phinney DG, (2006) Preclinical evaluation of adult stem cell engraftment and toxicity in the CNS of rhesus macaques. Mol Ther 13: 1173-1184.
51. Isakova IA, Baker K, DuTreil M, Dufour J, Gaupp D, et al. (2007) Age- and dose-related effects on MSC engraftment levels and anatomical distribution in the central nervous systems of nonhuman primates: identification of novel MSC subpopulations that respond to guidance cues in brain. Stem Cells 25: 3261-3270.
52. Kobune M, Kawano Y, Ito Y, Chiba H, Nakamura K, et al. (2003) Telomerized human multipotent mesenchymal cells can differentiate into hematopoietic and cobblestone area-supporting cells. Exp Hematol 31: 715-722.
53. Radtke C, Akiyama Y, Brokaw J, Lankford KL, Wewetzer K, et al. (2004) Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB J 18: 335-337.
54. Kataoka Y, Kalanithi PS, Grantz H, Schwartz ML, Saper C, et al. (2010) Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J Comp Neurol 518: 277-291.