Autologous Bone Marrow Mononuclear Cells Exert Broad Effects on Short- and Long-Term Biological and Functional Outcomes in Rodents with Intracerebral Hemorrhage

Stem Cells and Development

Volumn 24, Issue 23, 2015, Pages 2756-2766

  Suda, Satoshi ^a   Yang, Bing ^b   Schaar, Krystal ^b   Xi, Xiaopei ^b   Pido, Jennifer ^b   Parsha, Kaushik ^b   Aronowski, Jaroslaw ^b   Savitz, Sean I ^b  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; GELATINASE B; HIGH MOBILITY GROUP B1 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN S100B; AQP4 PROTEIN, RAT; MMP9 PROTEIN, RAT; PROTEIN S 100;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; BONE MARROW DERIVED MONONUCLEAR CELL; BRAIN ATROPHY; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN WATER; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INFLAMMATION; LONG EVANS RAT; MALE; MEMORY DISORDER; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; ANIMAL; AUTOTRANSPLANTATION; BONE MARROW TRANSPLANTATION; CELL CULTURE; CEREBRAL HEMORRHAGE; CYTOLOGY; GENETICS; MEMORY; METABOLISM; MONOCYTE; TRANSPLANTATION;

ANIMALS; AQUAPORIN 4; BONE MARROW TRANSPLANTATION; CELLS, CULTURED; CEREBRAL HEMORRHAGE; MALE; MATRIX METALLOPROTEINASE 9; MEMORY; MONOCYTES; RATS; RATS, LONG-EVANS; S100 PROTEINS; TRANSPLANTATION, AUTOLOGOUS;

EID: 84947421850     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2015.0107     Document Type: Article

References (59)

1. Broderick J, S Connolly, E Feldmann, D Hanley, C Kase, et al. (2007). Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Stroke 38:2001-2023.
2. Jorgensen HS, H Nakayama, HO Raaschou and TS Olsen. (1995). Intracerebral hemorrhage versus infarction: stroke severity, risk factors, and prognosis. Ann Neurol 38:45-50.
3. Morgenstern LB, JC Hemphill 3rd, C Anderson, K Becker, JP Broderick, et al. (2010). Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 41:2108-2129.
4. Abe K, T Yamashita, S Takizawa, S Kuroda, H Kinouchi, et al. (2012). Stem cell therapy for cerebral ischemia: from basic science to clinical applications. J Cereb Blood Flow Metab 32:1317-1331.
5. Saito H, K Magota, S Zhao, N Kubo, Y Kuge, et al. (2013) 123I-iomazenil single photon emission computed tomography visualizes recovery of neuronal integrity by bone marrow stromal cell therapy in rat infarct brain. Stroke 44:2869-2874.
6. Taguchi A, T Soma, H Tanaka, T Kanda, H Nishimura, et al. (2004). Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114:330-338.
7. Andres RH, N Horie, W Slikker, H Keren-Gill, K Zhan, et al. (2011). Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 134:1777-1789.
8. Savitz SI, V Misra, M Kasam, H Juneja, CS Cox, Jr., et al. (2011). Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann Neurol 70:59-69.
9. Iihoshi S, O Honmou, K Houkin, K Hashi and JD Kocsis. (2004). A therapeutic window for intravenous administration of autologous bone marrow after cerebral ischemia in adult rats. Brain Res 1007:1-9.
10. Lee ST, K Chu, KH Jung, SJ Kim, DH Kim, et al. (2008). Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain 131:616-629.
11. Otero L, M Zurita, C Bonilla, C Aguayo, A Vela, et al. (2011). Late transplantation of allogeneic bone marrow stromal cells improves neurologic deficits subsequent to intracerebral hemorrhage. Cytotherapy 13:562-571.
12. Karki K, RA Knight, Y Han, D Yang, J Zhang, et al. (2009). Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage. Stroke 40:3384-3389.
13. Felberg RA, JC Grotta, AL Shirzadi, R Strong, P Narayana, et al. (2002). Cell death in experimental intracerebral hemorrhage: the black hole model of hemorrhagic damage. Ann Neurol 51:517-524.
14. Yang B, X Xi, J Aronowski and SI Savitz. (2012). Ischemic stroke may activate bone marrow mononuclear cells to enhance recovery after stroke. Stem Cells Dev 21:3332-3340.
15. Brenneman M, S Sharma, MHarting, R Strong, CS Cox, Jr., et al. (2010). Autologous bone marrow mononuclear cells enhance recovery after acute ischemic stroke in young and middle-Aged rats. J Cereb Blood Flow Metab 30:140-149.
16. Yang B, R Strong, S Sharma, M Brenneman, K Mallikarjunarao, et al. (2011). Therapeutic time window and dose response of autologous bone marrow mononuclear cells for ischemic stroke. J Neurosci Res 89:833-839.
17. Yang B, E Migliati, K Parsha, K Schaar, X Xi, et al. (2013). Intra-Arterial delivery is not superior to intravenous delivery of autologous bone marrow mononuclear cells in acute ischemic stroke. Stroke 44:3463-3472.
18. Jung KH, K Chu, SW Jeong, SY Han, ST Lee, et al. (2004). HMG-CoA reductase inhibitor, atorvastatin, promotes sensorimotor recovery, suppressing acute inflammatory reaction after experimental intracerebral hemorrhage. Stroke 35:1744-1749.
19. Keep RF, Y Hua and G Xi. (2012). Brain water content. A misunderstood measurement? Transl Stroke Res 3:263-265.
20. Montoya CP, LJ Campbell-Hope, KD Pemberton and SB Dunnett. (1991). The staircase test: a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods 36:219-228.
21. Schaar KL, MM Brenneman and SI Savitz. (2010). Functional assessments in the rodent stroke model. Exp Transl Stroke Med 2:13.
22. Bouet V, T Freret, J Toutain, D Divoux, M Boulouard, et al. (2007). Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol 203:555-567.
23. MacLellan CL, AM Auriat, SC McGie, RH Yan, HD Huynh, et al. (2006). Gauging recovery after hemorrhagic stroke in rats: implications for cytoprotection studies. J Cereb Blood Flow Metab 26:1031-1042.
24. MacLellan CL, LM Davies, MS Fingas and F Colbourne. (2006). The influence of hypothermia on outcome after intracerebral hemorrhage in rats. Stroke 37:1266-1270.
25. Morris RG, P Garrud, JN Rawlins and J OKeefe. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
26. Thompson HJ, DG LeBold, N Marklund, DM Morales, AP Hagner, et al. (2006). Cognitive evaluation of traumatically brain-injured rats using serial testing in the Morris water maze. Restor Neurol Neurosci 24:109-114.
27. Jolkkonen J, NP Gallagher, K Zilles and J Sivenius. (2003). Behavioral deficits and recovery following transient focal cerebral ischemia in rats: glutamatergic and GABAergic receptor densities. Behav Brain Res 138: 187-200.
28. Ortega FJ, J Jolkkonen, N Mahy and MJ Rodriguez. (2013). Glibenclamide enhances neurogenesis and improves longterm functional recovery after transient focal cerebral ischemia. J Cereb Blood Flow Metab 33:356-364.
29. Masuda T, Y Isobe, N Aihara, F Furuyama, S Misumi, et al. (2007). Increase in neurogenesis and neuroblast migration after a small intracerebral hemorrhage in rats. Neurosci Lett 425:114-119.
30. Savitz SI, M Chopp, R Deans, T Carmichael, D Phinney, et al. (2011). Stem cell therapy as an emerging paradigm for stroke (STEPS) II. Stroke 42:825-829.
31. Bedi SS, PA Walker, SK Shah, F Jimenez, CP Thomas, et al. (2013). Autologous bone marrow mononuclear cells therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury. J Trauma Acute Care Surg 75:410-416.
32. Maruichi K, S Kuroda, Y Chiba, M Hokari, H Shichinohe, et al. (2009). Transplanted bone marrow stromal cells improves cognitive dysfunction due to diffuse axonal injury in rats. Neuropathology 29:422-432.
33. Ramos AB, A Vasconcelos-Dos-Santos, SA Lopes de Souza, PH Rosado-de-Castro, LM Barbosa da Fonseca, et al. (2013). Bone-marrow mononuclear cells reduce neurodegeneration in hippocampal CA1 layer after transient global ischemia in rats. Brain Res 1522:1-11.
34. Aronowski J and CE Hall. (2005). New horizons for primary intracerebral hemorrhage treatment: experience from preclinical studies. Neurol Res 27:268-279.
35. Zhao XSG, H Zhang, S-M Ting, S Song, N Gonzales and J Aronowski. (2014). Polymorphonuclear neutrophil in brain parenchyma after experimental intracerebral hemorrhage. Transl Stroke Res 5:554-561.
36. Leal MM, ZS Costa-Ferro, BS Souza, CM Azevedo, TM Carvalho, CM Kaneto, et al. (2014). Early transplantation of bonemarrowmononuclear cells promotes neuroprotection and modulation of inflammation after status epilepticus in mice by paracrine mechanisms. Neurochem Res 39:259-268.
37. Xi G, RF Keep and JT Hoff. (2006). Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5:53-63.
38. Hua Y, T Schallert, RF Keep, J Wu, JT Hoff, et al. (2002). Behavioral tests after intracerebral hemorrhage in the rat. Stroke 33:2478-2484.
39. Borlongan CV, JG Lind, O Dillon-Carter, G Yu, M Hadman, et al. (2004). Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats. Brain Res 1010:108-116.
40. Badaut J, F Lasbennes, PJ Magistretti and L Regli. (2002). Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab 22:367-378.
41. Tang G, Y Liu, Z Zhang, Y Lu, Y Wang, et al. (2014). Mesenchymal stem cells maintain blood-brain barrier integrity by inhibiting aquaporin-4 up-regulation after cerebral ischemia. Stem Cells 32:3150-3162.
42. Yamashita T, T Kamiya, K Deguchi, T Inaba, H Zhang, et al. (2009). Dissociation and protection of the neurovascular unit after thrombolysis and reperfusion in ischemic rat brain. J Cereb Blood Flow Metab 29:715-725.
43. Ohnishi M, H Katsuki, C Fukutomi, M Takahashi, M Motomura, et al. (2011). HMGB1 inhibitor glycyrrhizin attenuates intracerebral hemorrhage-induced injury in rats. Neuropharmacology 61:975-980.
44. Hayakawa K, J Qiu and EH Lo. (2010). Biphasic actions of HMGB1 signaling in inflammation and recovery after stroke. Ann N Y Acad Sci 1207:50-57.
45. Mori T, J Tan, GW Arendash, N Koyama, Y Nojima, et al. (2008). Overexpression of human S100B exacerbates brain damage and periinfarct gliosis after permanent focal ischemia. Stroke 39:2114-2121.
46. Delgado P, J Alvarez Sabin, E Santamarina, CA Molina, M Quintana, et al. (2006). Plasma S100B level after acute spontaneous intracerebral hemorrhage. Stroke 37:2837-2839.
47. Shen J, L Xie, X Mao, Y Zhou, R Zhan, et al. (2008). Neurogenesis after primary intracerebral hemorrhage in adult human brain. J Cereb Blood Flow Metab 28:1460-1468.
48. Wiltrout C, B Lang, Y Yan, RJ Dempsey and R Vemuganti. (2007). Repairing brain after stroke: a review on postischemic neurogenesis. Neurochem Int 50:1028-1041.
49. Shen LH, Y Li and M Chopp. (2010). Astrocytic endogenous glial cell derived neurotrophic factor production is enhanced by bone marrow stromal cell transplantation in the ischemic boundary zone after stroke in adult rats. Glia 58:1074-1081.
50. Fujita Y, M Ihara, T Ushiki, H Hirai, S Kizaka-Kondoh, et al. (2010). Early protective effect of bone marrow mononuclear cells against ischemic white matter damage through augmentation of cerebral blood flow. Stroke 41:2938-2943.
51. Wang J, X Fu, C Jiang, L Yu, M Wang, et al. (2014). Bone marrow mononuclear cell transplantation promotes therapeutic angiogenesis via upregulation of the VEGFVEGFR2 signaling pathway in a rat model of vascular dementia. Behav Brain Res 265:171-180.
52. Raval Z and DW Losordo. (2013). Cell therapy of peripheral arterial disease: from experimental findings to clinical trials. Circ Res 112:1288-1302.
53. Stroke Therapy Academic Industry Roundtable (STAIR). (1999) Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30:2752-2758.
54. Kamiya N, M Ueda, H Igarashi, Y Nishiyama, S Suda, et al. (2008). Intra-Arterial transplantation of bone marrow mononuclear cells immediately after reperfusion decreases brain injury after focal ischemia in rats. Life Sci 83:433-437.
55. Fisher M, G Feuerstein, DW Howells, PD Hurn, TA Kent, et al. (2009). Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40:2244-2250.
56. Nakano-Doi A, T Nakagomi, M Fujikawa, N Nakagomi, S Kubo, S Lu, et al. (2010). Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells 28:1292-1302.
57. Balseanu AT, AM Buga, B Catalin, DC Wagner, J Boltze, et al. (2014). 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.
58. Popa-Wagner A, AM Buga, TR Doeppner and DM Hermann. (2014). Stem cell therapies in preclinical models of stroke associated with aging. Front Cell Neurosci 8:347.
59. Li ZM, ZT Zhang, CJ Guo, FY Geng, F Qiang and LX Wang. (2013). Autologous bone marrow mononuclear cell implantation for intracerebral hemorrhage-A prospective clinical observation. Clin Neurol Neurosurg 115:72-76.