Intravenous multipotent adult progenitor cell therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury

Stem Cells Translational Medicine

Volumn 2, Issue 12, 2013, Pages 953-960

  Bedi, Supinder S ^a   Hetz, Robert ^a,b   Thomas, Chelsea ^a   Smith, Philippa ^a   Olsen, Alex B ^a   Williams, Stephen ^a   Xue, Hasen ^a,b   Aroom, Kevin ^a   Uray, Karen ^a   Hamilton, Jason ^c   Mays, Robert W ^c   Cox Jr , Charles S ^a,b,d  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c ATHERSYS INC   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Adult stem cells; Neuroimmune; Rat model; Stem progenitor cell

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL THERAPY; COGNITION; DENTATE GYRUS; IMMUNOHISTOCHEMISTRY; MICROGLIA; MORRIS WATER MAZE TEST; NONHUMAN; RAT; ROTAROD TEST; SENSORIMOTOR FUNCTION; SPATIAL LEARNING; TRAUMATIC BRAIN INJURY;

ANIMALIA; RATTUS; RODENTIA;

EID: 84888408907     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0100     Document Type: Article

References (36)

1. Loane DJ, Byrnes KR. Role of microglia in neurotrauma. Neurotherapeutics 2010;7: 366-377.
2. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3:23-35.
3. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005;308:1314-1318.
4. Smith HS. Activated microglia in nociception. Pain Physician 2010;13:295-304.
5. Tsuda M, Shigemoto-Mogami Y, Koizumi S et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003;424:778-783.
6. Pineau I, Sun L, Bastien D et al. Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/ MyD88-dependent fashion. Brain Behav Immun 2010;24:540-553.
7. Pineau I, Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: Multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 2007;500:267-285.
8. Harting MT, Jimenez F, Adams SD et al. Acute, regional inflammatory response after traumatic brain injury: Implications for cellular therapy. Surgery 2008;144:803-813.
9. Savitz SI, Misra V, Kasam M et al. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann Neurol 2011;70: 59-69.
10. Cox CS Jr., Baumgartner JE, Harting MT et al. Autologous bone marrow mononuclear cell therapy for severe traumatic brain injury in children. Neurosurgery 2011;68: 588-600.
11. Brenneman M, Sharma S, Harting M et al. Autologous bone marrow mononuclear cells enhance recovery after acute ischemic stroke in young and middle-aged rats. J Cereb Blood Flow Metab 2010;30:140-149.
12. Liu N, Chen R, Du H et al. Expression of IL-10 and TNF-alpha in rats with cerebral infarction after transplantation with mesenchymal stem cells. Cell Mol Immunol 2009;6:207-213.
13. Fischer UM, Harting MT, Jimenez F et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: The pulmonary first-pass effect. Stem Cells Dev 2009;18:683-692.
14. Walker PA, Bedi SS, Shah SK et al. Intravenous multipotent adult progenitor cell therapy after traumatic brain injury: Modulation of the resident microglia population. J Neuroinflammation 2012;9:228.
15. Walker PA, Shah SK, Jimenez F et al. Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: Preserving the blood brain barrier via an interaction with splenocytes. Exp Neurol 2010;225:341-352.
16. Menge T, Zhao Y, Zhao J et al. Mesenchymal stem cells regulate blood-brain barrier integrity through TIMP3 release after traumatic brain injury. Sci Transl Med 2012;4:161ra150.
17. Bedi SS, Walker PA, Shah SK et al. Autologous bone marrow mononuclear cells therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury. J Trauma Acute Care Surg 2013;75:410-416.
18. Lighthall JW. Controlled cortical impact: A new experimental brain injury model. J Neurotrauma 1988;5:1-15.
19. Dixon CE, Bao J, Long DA et al. Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacol Biochem Behav 1996;53:679-686.
20. Budinich CS, Tucker LB, Lowe D et al. Short and long-term motor and behavioral effects of diazoxide and dimethyl sulfoxide administration in the mouse after traumatic brain injury. Pharmacol Biochem Behav 2013;108: 66-73.
21. Morris RG, Garrud P, Rawlins JN et al. Place navigation impaired in rats with hippocampal lesions. Nature 1982;297:681-683.
22. Terry AV Jr. Spatial navigation (water maze) tasks. In: Buccafusco JJ, ed. Methods of Behavior Analysis in Neuroscience. 2nd ed. Boca Raton, FL: CRC Press, 2009.
23. Bannerman DM, Bus T, Taylor A et al. Dissecting spatial knowledge from spatial choice by hippocampal NMDA receptor deletion. Nat Neurosci 2012;15:1153-1159.
24. Sutherland RJ, Whishaw IQ, Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate-or colchicine-induced damage to the hippocampal formation in the rat. Behav Brain Res 1983;7:133-153.
25. Graeber MB. Changing face of microglia. Science 2010;330:783-788.
26. Bedi SS, Smith P, Hetz RA et al. Immunomagnetic enrichment and flow cytometric characterization of mouse microglia. J Neurosci Methods 2013;219:176-182.
27. Gaytan F, Bellido C, Morales C et al. Effects of macrophage depletion at different times after treatment with ethylene dimethane sulfonate (EDS) on the regeneration of Leydig cells in the adult rat. J Androl 1994;15:558-564.
28. Heppner FL, Greter M, Marino D et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005;11:146-152.
29. Belarbi K, Arellano C, Ferguson R et al. Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks. Brain Behav Immun 2012;26:18-23.
30. Belarbi K, Jopson T, Tweedie D et al. TNFalpha protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation 2012;9:23.
31. Gentleman SM, Leclercq PD, Moyes L et al. Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int 2004;146:97-104.
32. Johnson VE, Stewart JE, Begbie FD et al. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 2013;136:28-42.
33. Ramlackhansingh AF, Brooks DJ, Greenwood RJ et al. Inflammation after trauma: Microglial activation and traumatic brain injury. Ann Neurol 2011;70:374-383.
34. Sofroniew MV. Reactive astrocytes in neural repair and protection. Neuroscientist 2005;11:400-407.
35. Xuan A, Long D, Li J et al. Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in betaamyloid rat model of Alzheimer's disease. J Neuroinflammation 2012;9:202.
36. Cusimano M, Biziato D, Brambilla E et al. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012; 135:447-460.