Bone marrow-derived mesenchymal stem cell transplantation ameliorates oxidative stress and restores intestinal mucosal permeability in chemically induced colitis in mice

American Journal of Translational Research

Volumn 7, Issue 5, 2015, Pages 891-901

  Sun, Tao ^a   Gao, Guang Zhou ^a   Li, Rong Fu ^a   Li, Xin ^a   Li, Da Wei ^a   Wu, Shan Shan ^a   Yeo, Anthony E T ^b   Jin, Bo ^c  

^a NAVY GENERAL HOSPITAL   (China)

^b The 309th Hospital of People’s Liberation Army ^*  (United States)

^c Department of Gastroenterology The 309th Hospital of People s Liberation Army   (China)

Author keywords

Cell transplantation; Intestinal barrier; Mesenchymal stem cell; Mice; Ulcerative colitis

Indexed keywords

AMINE OXIDASE (COPPER CONTAINING); CD34 ANTIGEN; CD45 ANTIGEN; DEXTRO LACTATE DEHYDROGENASE; HERMES ANTIGEN; MALONALDEHYDE; SUPEROXIDE DISMUTASE; TESTIS DETERMINING FACTOR; THY 1 ANTIGEN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA PERMEABILITY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; ULCERATIVE COLITIS;

MURINAE; MUS;

EID: 84936771995     PISSN: None     EISSN: 19438141     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. [1] Ahuja V and Tandon RK. Inflammatory bowel disease in the Asia-Pacific area: a comparison with developed countries and regional differ ences. J Dig Dis 2010; 11: 134-147.
2. [2] Loftus EV Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental infuences. Gastroenterology 2004; 126: 1504-1517.
3. [3] Abreu MT and Sparrow MP. Translational research in inflammatory bowel disease. Mt Sinai J Med 2006; 73: 1067-1073.
4. [4] Hendrickson BA, Gokhale R and Cho JH. Clinical aspects and pathophysiology of inflammatory bowel disease. Clin Microbiol Rev 2002; 15: 79-94.
5. [5] Danese S and Fiocchi C. Ulcerative colitis. N Engl J Med 2011; 365: 1713-1725.
6. [6] Rosenberg LN and Peppercorn MA. Efficacy and safety of drugs for ulcerative colitis. Expert Opin Drug Saf 2010; 9: 573-592.
7. [7] Drakos PE, Nagler A and Or R. Case of Crohn’s disease in bone marrow transplantation. Am J Hematol 1993; 43: 157-158.
8. [8] Matsumoto T, Okamoto R, Yajima T, Mori T, Okamoto S, Ikeda Y, Mukai M, Yamazaki M, Os-hima S, Tsuchiya K, Nakamura T, Kanai T, Okano H, Inazawa J, Hibi T and Watanabe M. Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. Gastroenterology 2005; 128: 1851-1867.
9. [9] Clerici M, Cassinotti A, Onida F, Trabattoni D, Annaloro C, Della Volpe A, Rainone V, Lissoni F, Duca P, Sampietro G, Fociani P, Vago G, Foschi D, Ardizzone S, Deliliers GL and Porro GB. Im-munomodulatory effects of unselected haematopoietic stem cells autotransplantation in refractory Crohn’s disease. Dig Liver Dis 2011; 43: 946-952.
10. [10] Komori M, Tsuji S, Tsujii M, Murata H, Iijima H, Yasumaru M, Nishida T, Irie T, Kawano S and Hori M. Involvement of bone marrow-derived cells in healing of experimental colitis in rats. Wound Repair Regen 2005; 13: 109-118.
11. 11[] Zhang J, Gong JF, Zhang W, Zhu WM and Li JS. Effects of transplanted bone marrow mesen- chymal stem cells on the irradiated intestine of mice. J Biomed Sci 2008; 15: 585-594.
12. [12] Khalil PN, Weiler V, Nelson PJ, Khalil MN, Moosmann S, Mutschler WE, Siebeck M and Huss R. Nonmyeloablative stem cell therapy enhances microcirculation and tissue regeneration in murine inflammatory bowel disease. Gastroenterology 2007; 132: 944-954.
13. [13] Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y and Le AD. Mesenchymal stem cells derived from human gingiva are capable of immunomodulato- ry functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 2009; 183: 7787-7798.
14. [14] Hayashi Y, Tsuji S, Tsujii M, Nishida T, Ishii S, Iijima H, Nakamura T, Eguchi H, Miyoshi E, Hayashi N and Kawano S. Topical implantation of mesenchymal stem cells has beneficial effects on healing of experimental colitis in rats. J Pharmacol Exp Ther 2008; 326: 523-531.
15. [15] Nasef A, Ashammakhi N and Fouillard L. Im-munomodulatory effect of mesenchymal stro-mal cells: possible mechanisms. Regen Med 2008; 3: 531-546.
16. [16] Tanaka F, Tominaga K, Ochi M, Tanigawa T, Watanabe T, Fujiwara Y, Ohta K, Oshitani N, Hi-guchi K and Arakawa T. Exogenous administration of mesenchymal stem cells ameliorates dextran sulfate sodium-induced colitis via anti-inflammatory action in damaged tissue in rats. Life Sci 2008; 83: 771-779.
17. [17] Jena G, Trivedi PP and Sandala B. Oxidative stress in ulcerative colitis: an old concept but a new concern. Free Radic Res 2012; 46: 1339-1345.
18. [18] Shen ZY, Zhang J, Song HL and Zheng WP. Bone-marrow mesenchymal stem cells reduce rat intestinal ischemia-reperfusion injury, ZO-1 downregulation and tight junction disruption via a TNF-alpha-regulated mechanism. World J Gastroenterol 2013; 19: 3583-3595.
19. [19] Jiang H, Qu L, Li Y, Gu L, Shi Y, Zhang J, Zhu W and Li J. Bone marrow mesenchymal stem cells reduce intestinal ischemia/reperfusion injuries in rats. J Surg Res 2011; 168: 127-134.
20. [20] Yabana T, Arimura Y, Tanaka H, Goto A, Hoso-kawa M, Nagaishi K, Yamashita K, Yamamoto H, Adachi Y, Sasaki Y, Isobe M, Fujimiya M, Imai K and Shinomura Y. Enhancing epithelial en-graftment of rat mesenchymal stem cells restores epithelial barrier integrity. J Pathol 2009; 218: 350-359.
21. [21] He XW, He XS, Lian L, Wu XJ and Lan P. Systemic infusion of bone marrow-derived mesen-chymal stem cells for treatment of experimental colitis in mice. Dig Dis Sci 2012; 57: 3136-3144.
22. [22] Song C and Li G. CXCR4 and matrix metallopro-teinase-2 are involved in mesenchymal stro-mal cell homing and engraftment to tumors. Cytotherapy 2011; 13: 549-561.
23. [23] Chen X, McClurg A, Zhou GQ, McCaigue M, Armstrong MA and Li G. Chondrogenic differentiation alters the immunosuppressive property of bone marrow-derived mesenchymal stem cells, and the effect is partially due to the up-regulated expression of B7 molecules. Stem Cells 2007; 25: 364-370.
24. [24] Kihara N, de la Fuente SG, Fujino K, Takahashi T, Pappas TN and Mantyh CR. Vanilloid recep- tor-1 containing primary sensory neurones mediate dextran sulphate sodium induced colitis in rats. Gut 2003; 52: 713-719.
25. [25] Murano M, Maemura K, Hirata I, Toshina K, Ni-shikawa T, Hamamoto N, Sasaki S, Saitoh O and Katsu K. Therapeutic effect of intracoloni-cally administered nuclear factor kappa B (p65) antisense oligonucleotide on mouse dextran sulphate sodium (DSS)-induced colitis. Clin Exp Immunol 2000; 120: 51-58.
26. [26] Randhawa PK, Singh K, Singh N and Jaggi AS. A review on chemical-induced inflammatory bowel disease models in rodents. Korean J Physiol Pharmacol 2014; 18: 279-288.
27. [27] Dominici M, Le Blanc K, Mueller I, Slaper-Cor-tenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D and Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317.
28. [28] Ren G, Chen X, Dong F, Li W, Ren X, Zhang Y and Shi Y. Concise review: mesenchymal stem cells and translational medicine: emerging issues. Stem Cells Transl Med 2012; 1: 51-58.
29. [29] Jackson WM, Nesti LJ and Tuan RS. Concise review: clinical translation of wound healing therapies based on mesenchymal stem cells. Stem Cells Transl Med 2012; 1: 44-50.
30. [30] Ricart E. Current status of mesenchymal stem cell therapy and bone marrow transplantation in IBD. Dig Dis 2012; 30: 387-391.
31. 31[] Scaldaferri F, Pizzoferrato M, Gerardi V, Lope-tuso L and Gasbarrini A. The gut barrier: new acquisitions and therapeutic approaches. J Clin Gastroenterol 2012; 46 Suppl: S12-17.
32. [32] Hermiston ML, Wong MH and Gordon JI. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev 1996; 10: 985-996.
33. [33] Dogan A, Wang ZD and Spencer J. E-cadherin expression in intestinal epithelium. J Clin Pathol 1995; 48: 143-146.
34. [34] Murray MJ, Barbose JJ and Cobb CF. Serum D(-)-lactate levels as a predictor of acute intestinal ischemia in a rat model. J Surg Res 1993; 54: 507-509.
35. [35] Luk GD, Bayless TM and Baylin SB. Diamine oxidase (histaminase). A circulating marker for rat intestinal mucosal maturation and integrity. J Clin Invest 1980; 66: 66-70.
36. [36] Song WB, Lv YH, Zhang ZS, Li YN, Xiao LP, Yu XP, Wang YY, Ji HL and Ma L. Soluble intercellular adhesion molecule-1, D-lactate and di-amine oxidase in patients with inflammatory bowel disease. World J Gastroenterol 2009; 15: 3916-3919.
37. [37] Garg S, Wang W, Prabath BG, Boerma M, Wang J, Zhou D and Hauer-Jensen M. Bone marrow transplantation helps restore the intestinal mucosal barrier after total body irradiation in mice. Radiat Res 2014; 181: 229-239.
38. [38] Baghaban Eslaminejad M and Malakooty Poor E. Mesenchymal stem cells as a potent cell source for articular cartilage regeneration. World J Stem Cells 2014; 6: 344-354.
39. [39] Rezaie A, Parker RD and Abdollahi M. Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause? Dig Dis Sci 2007; 52: 2015-2021.
40. [40] Lykkesfeldt J. Malondialdehyde as biomarker of oxidative damage to lipids caused by smoking. Clin Chim Acta 2007; 380: 50-58.
41. [41] Del Rio D, Stewart AJ and Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 2005; 15: 316-328.
42. [42] Lih-Brody L, Powell SR, Collier KP, Reddy GM, Cerchia R, Kahn E, Weissman GS, Katz S, Floyd RA, McKinley MJ, Fisher SE and Mullin GE. Increased oxidative stress and decreased anti-oxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 1996; 41: 2078-2086.
43. [43] Miller AF. Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 2012; 586: 585-595.
44. [44] Semedo P, Correa-Costa M, Antonio Cenedeze M, Maria Avancini Costa Malheiros D, Antonia dosReis M, Shimizu MH, Seguro AC, Pacheco-Silva A and Saraiva Camara NO. Mesenchymal stem cells attenuate renal fbrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 2009; 27: 3063-3073.