The inhibitory effect of mesenchymal stem cell on blood-brain barrier disruption following intracerebral hemorrhage in rats: Contribution of TSG-6

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Chen, Min ^a   Li, Xifeng ^a   Zhang, Xin ^a   He, Xuying ^a   Lai, Lingfeng ^a   Liu, Yanchao ^b   Zhu, Guohui ^a   Li, Wei ^a   Li, Hui ^a   Fang, Qinrui ^a   Wang, Zequn ^a   Duan, Chuanzhi ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b THE FIRST PEOPLE S HOSPITAL OF FOSHAN   (China)

Author keywords

Blood brain barrier; Inducible nitric oxide synthase; Intracerebral hemorrhage; Mesenchymal stem cell; Nuclear factor B; Peroxynitrite; TNF stimulated gene protein 6

Indexed keywords

CLAUDIN 5; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PROTEIN ZO1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA STIMULATED GENE 6; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CYTOKINE; PEROXYNITROUS ACID; TNFAIP6 PROTEIN, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BEHAVIOR CHANGE; BLOOD BRAIN BARRIER; BLOOD BRAIN BARRIER LEAKAGE; BRAIN DISEASE; BRAIN EDEMA; BRAIN HEMORRHAGE; CONTROLLED STUDY; INFLAMMATION; MACROPHAGE; MALE; MEMBRANE DAMAGE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROGLIA; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; RAT; TREATMENT OUTCOME; ANIMAL; BRAIN; DISEASE MODEL; GENE EXPRESSION REGULATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; CELL ADHESION MOLECULES; CEREBRAL HEMORRHAGE; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; MALE; MATRIX METALLOPROTEINASE 9; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NITRIC OXIDE SYNTHASE TYPE II; PEROXYNITROUS ACID; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84926685116     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0284-x     Document Type: Article

References (66)

1. Butcher K, Laidlaw J. Current intracerebral haemorrhage management. J Clin Neurosci. 2003;10:158-67.
2. Xi G, Keep RF, Hoff JT. Erythrocytes and delayed brain edema formation following intracerebral hemorrhage in rats. J Neurosurg. 1998;89:991-6.
3. Yang GY, Betz AL, Chenevert TL, Brunberg JA, Hoff JT. Experimental intracerebral hemorrhage: relationship between brain edema, blood flow, and blood-brain barrier permeability in rats. J Neurosurg. 1994;81:93-102.
4. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37:13-25.
5. Kim KS. Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol. 2008;6:625-34.
6. Chu H, Ding H, Tang Y, Dong Q. Erythropoietin protects against hemorrhagic blood-brain barrier disruption through the effects of aquaporin-4. Lab Invest. 2014;94:1042-53.
7. Wang T, Chen X, Wang Z, Zhang M, Meng H, Gao Y, et al. Poloxamer-188 can attenuate blood-brain barrier damage to exert neuroprotective effect in mice intracerebral hemorrhage model. J Mol Neurosci. 2014;55:240-50.
8. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87:1620-4.
9. Ding R, Chen Y, Yang S, Deng X, Fu Z, Feng L, et al. Blood-brain barrier disruption induced by hemoglobin in vivo: involvement of up-regulation of nitric oxide synthase and peroxynitrite formation. Brain Res. 2014;1571:25-38.
10. Marcus JS, Karackattu SL, Fleegal MA, Sumners C. Cytokine-stimulated inducible nitric oxide synthase expression in astroglia: role of Erk mitogen-activated protein kinase and NF-kappaB. Glia. 2003;41:152-60.
11. Candolfi M, Jaita G, Zaldivar V, Zarate S, Pisera D, Seilicovich A. Tumor necrosis factor-alpha-induced nitric oxide restrains the apoptotic response of anterior pituitary cells. Neuroendocrinology. 2004;80:83-91.
12. Chang CC, Wang YH, Chern CM, Liou KT, Hou YC, Peng YT, et al. Prodigiosin inhibits gp91(phox) and iNOS expression to protect mice against the oxidative/nitrosative brain injury induced by hypoxia-ischemia. Toxicol Appl Pharmacol. 2011;257:137-47.
13. Qayyum I, Zubrow AB, Ashraf QM, Kubin J, Delivoria-Papadopoulos M, Mishra OP. Nitration as a mechanism of Na+, K + -ATPase modification during hypoxia in the cerebral cortex of the guinea pig fetus. Neurochem Res. 2001;26:1163-9.
14. Cassina A, Radi R. Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys. 1996;328:309-16.
15. Wang W, Sawicki G, Schulz R. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc Res. 2002;53:165-74.
16. Suofu Y, Clark J, Broderick J, Wagner KR, Tomsick T, Sa Y, et al. Peroxynitrite decomposition catalyst prevents matrix metalloproteinase activation and neurovascular injury after prolonged cerebral ischemia in rats. J Neurochem. 2010;115:1266-76.
17. Li J, Zhang L, Xin J, Jiang L, Li J, Zhang T, et al. Immediate intraportal transplantation of human bone marrow mesenchymal stem cells prevents death from fulminant hepatic failure in pigs. Hepatology. 2012;56:1044-52.
18. Shi LL, Liu FP, Wang DW. Transplantation of human umbilical cord blood mesenchymal stem cells improves survival rates in a rat model of acute hepatic necrosis. Am J Med Sci. 2011;342:212-7.
19. Liu L, Yu Y, Hou Y, Chai J, Duan H, Chu W, et al. Human umbilical cord mesenchymal stem cells transplantation promotes cutaneous wound healing of severe burned rats. PLoS One. 2014;9:e88348.
20. Zhang R, Liu Y, Yan K, Chen L, Chen XR, Li P, et al. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J Neuroinflammation. 2013;10:106.
21. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell. 2009;5:54-63.
22. Wu HJ, Yiu WH, Li RX, Wong DW, Leung JC, Chan LY, et al. Mesenchymal stem cells modulatealbumin-induced renal tubular inflammation and fibrosis. PLoS One. 2014;9:e90883.
23. Oh JY, Roddy GW, Choi H, Lee RH, Ylostalo JH, Rosa RJ, et al. Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. Proc Natl Acad Sci U S A. 2010;107:16875-80.
24. Liu Y, Zhang R, Yan K, Chen F, Huang W, Lv B, et al. Mesenchymal stem cells inhibit lipopolysaccharide-induced inflammatory responses of BV2 microglial cells through TSG-6. J Neuroinflammation. 2014;11:135.
25. Jung Y, Kim SH, Kim YH, Kim SH. The effects of dynamic and three-dimensional environments on chondrogenic differentiation of bone marrow stromal cells. Biomed Mater. 2009;4:55009.
26. Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke. 1990;21:801-7.
27. Garbuzova-Davis S, Willing AE, Zigova T, Saporta S, Justen EB, Lane JC, et al. Intravenous administration of human umbilical cord blood cells in a mouse model of amyotrophic lateral sclerosis: distribution, migration, and differentiation. J Hematother Stem Cell Res. 2003;12:255-70.
28. Ke K, Rui Y, Li L, Zheng H, Xu W, Tan X, et al. Upregulation of EHD2 after intracerebral hemorrhage in adult rats. J Mol Neurosci. 2014;54:171-80.
29. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke. 2001;32:1005-11.
30. Song EC, Chu K, Jeong SW, Jung KH, Kim SH, Kim M, et al. Hyperglycemia exacerbates brain edema and perihematomal cell death after intracerebral hemorrhage. Stroke. 2003;34:2215-20.
31. Khan M, Sakakima H, Dhammu TS, Shunmugavel A, Im YB, Gilg AG, et al. S-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats. J Neuroinflammation. 2011;8:78.
32. Yang S, Chen Y, Deng X, Jiang W, Li B, Fu Z, et al. Hemoglobin-induced nitric oxide synthase overexpression and nitric oxide production contribute to blood-brain barrier disruption in the rat. J Mol Neurosci. 2013;51:352-63.
33. Bethea JR, Castro M, Keane RW, Lee TT, Dietrich WD, Yezierski RP. Traumatic spinal cord injury induces nuclear factor-kappaB activation. J Neurosci. 1998;18:3251-60.
34. Genovese T, Mazzon E, Esposito E, Muia C, Di Paola R, Bramanti P, et al. Beneficial effects of FeTSPP, a peroxynitrite decomposition catalyst, in a mouse model of spinal cord injury. Free Radic Biol Med. 2007;43:763-80.
35. Shlosberg D, Benifla M, Kaufer D, Friedman A. Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol. 2010;6:393-403.
36. Muijsers RB, Folkerts G, Henricks PA, Sadeghi-Hashjin G, Nijkamp FP. Peroxynitrite: a two-faced metabolite of nitric oxide. Life Sci. 1997;60:1833-45.
37. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87:315-424.
38. Arima H, Wang JG, Huang Y, Heeley E, Skulina C, Parsons MW, et al. Significance of perihematomal edema in acute intracerebral hemorrhage: the INTERACT trial. Neurology. 2009;73:1963-8.
39. Chen HY, Chen TY, Lee MY, Chen ST, Hsu YS, Kuo YL, et al. Melatonin decreases neurovascular oxidative/nitrosative damage and protects against early increases in the blood-brain barrier permeability after transient focal cerebral ischemia in mice. J Pineal Res. 2006;41:175-82.
40. Parathath SR, Parathath S, Tsirka SE. Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice. J Cell Sci. 2006;119:339-49.
41. Phares TW, Fabis MJ, Brimer CM, Kean RB, Hooper DC. A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-alpha is neither necessary nor sufficient. J Immunol. 2007;178:7334-43.
42. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, et al. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol. 2003;161:653-60.
43. Zhang GS, Tian Y, Huang JY, Tao RR, Liao MH, Lu YM, et al. The gamma-secretase blocker DAPT reduces the permeability of the blood-brain barrier by decreasing the ubiquitination and degradation of occludin during permanent brain ischemia. CNS Neurosci Ther. 2013;19:53-60.
44. Anderson JM, Fanning AS, Lapierre L, Van Itallie CM. Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem Soc Trans. 1995;23:470-5.
45. Gursoy-Ozdemir Y, Can A, Dalkara T. Reperfusion-induced oxidative/nitrative injury to neurovascular unit after focal cerebral ischemia. Stroke. 2004;35:1449-53.
46. Wang J, Tsirka SE. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain. 2005;128:1622-33.
47. Wang J, Dore S. Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2007;27:894-908.
48. Seyfried D, Ding J, Han Y, Li Y, Chen J, Chopp M. Effects of intravenous administration of human bone marrow stromal cells after intracerebral hemorrhage in rats. J Neurosurg. 2006;104:313-8.
49. Wang SP, Wang ZH, Peng DY, Li SM, Wang H, Wang XH. Therapeutic effect of mesenchymal stem cells in rats with intracerebral hemorrhage: reduced apoptosis and enhanced neuroprotection. Mol Med Rep. 2012;6:848-54.
50. Bao XJ, Liu FY, Lu S, Han Q, Feng M, Wei JJ, et al. Transplantation of Flk-1+ human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and anti-inflammatory and angiogenesis effects in an intracerebral hemorrhage rat model. Int J Mol Med. 2013;31:1087-96.
51. Liao W, Zhong J, Yu J, Xie J, Liu Y, Du L, et al. Therapeutic benefit of human umbilical cord derived mesenchymal stromal cells in intracerebral hemorrhage rat: implications of anti-inflammation and angiogenesis. Cell Physiol Biochem. 2009;24:307-16.
52. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15:42-9.
53. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103:4619-21.
54. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008;111:1327-33.
55. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815-22.
56. Milner CM, Higman VA, Day AJ. TSG-6: a pluripotent inflammatory mediator? Biochem Soc Trans. 2006;34:446-50.
57. Getting SJ, Mahoney DJ, Cao T, Rugg MS, Fries E, Milner CM, et al. The link module from human TSG-6 inhibits neutrophil migration in a hyaluronan- and inter-alpha -inhibitor-independent manner. J Biol Chem. 2002;277:51068-76.
58. Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ. Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Blood. 2011;118:330-8.
59. Zhao X, Zhang Y, Strong R, Zhang J, Grotta JC, Aronowski J. Distinct patterns of intracerebral hemorrhage-induced alterations in NF-kappaB subunit, iNOS, and COX-2 expression. J Neurochem. 2007;101:652-63.
60. Bowie A, O'Neill LA. Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol. 2000;59:13-23.
61. Bredt DS. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res. 1999;31:577-96.
62. Ohtaki H, Funahashi H, Dohi K, Oguro T, Horai R, Asano M, et al. Suppression of oxidative neuronal damage after transient middle cerebral artery occlusion in mice lacking interleukin-1. Neurosci Res. 2003;45:313-24.
63. Walford GA, Moussignac RL, Scribner AW, Loscalzo J, Leopold JA. Hypoxia potentiates nitric oxide-mediated apoptosis in endothelial cells via peroxynitrite-induced activation of mitochondria-dependent and -independent pathways. J Biol Chem. 2004;279:4425-32.
64. Yokoo H, Chiba S, Tomita K, Takashina M, Sagara H, Yagisita S, et al. Neurodegenerative evidence in mice brains with cecal ligation and puncture-induced sepsis: preventive effect of the free radical scavenger edaravone. PLoS One. 2012;7:e51539.
65. Luth HJ, Munch G, Arendt T. Aberrant expression of NOS isoforms in Alzheimer's disease is structurally related to nitrotyrosine formation. Brain Res. 2002;953:135-43.
66. Murphy G, Willenbrock F, Crabbe T, O'Shea M, Ward R, Atkinson S, et al. Regulation of matrix metalloproteinase activity. Ann N Y Acad Sci. 1994;732:31-41.