Endometrial regenerative cells as a novel cell therapy attenuate experimental colitis in mice

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Lv, Yongcheng ^a   Xu, Xiaoxi ^b   Zhang, Bai ^a   Zhou, Guangying ^b   Li, Hongyue ^b   Du, Caigan ^c,d   Han, Hongqiu ^a   Wang, Hao ^a,b  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b Department of General Surgery   (China)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Colitis; Endometrial regenerative cells; Mice

Indexed keywords

CD11B ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; DEXTRAN SULFATE; DRINKING WATER; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CD3+ CD25+ T LYMPHOCYTE; CD3+ CD8+ T LYMPHOCYTE; CELL POPULATION; CLINICAL FEATURE; COLON MUCOSA; COLON ULCER; CONTROLLED STUDY; DENDRITIC CELL; DIARRHEA; DISEASE ACTIVITY SCORE; DISEASE SEVERITY; ENDOMETRIAL REGENERATIVE CELL; EXPERIMENTAL COLITIS; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MALE; MENSTRUATION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECTUM HEMORRHAGE; REGULATORY T LYMPHOCYTE; SPLEEN; T LYMPHOCYTE; THERAPY EFFECT; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; CHEMICALLY INDUCED; COLITIS; CYTOLOGY; ENDOMETRIUM; FEMALE; GENETIC TRANSCRIPTION; GENETICS; MESENCHYMAL STROMA CELL;

ANIMALS; COLITIS; CYTOKINES; DEXTRAN SULFATE; ENDOMETRIUM; FEMALE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; TRANSCRIPTION, GENETIC;

EID: 84924918918     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-014-0344-5     Document Type: Article

References (63)

1. Dalal J, Gandy K, Domen J: Role of mesenchymal stem cell therapy in Crohn's disease. Pediatr Res 2012, 71:445-451.
2. Ye L, Cao Q, Cheng J: Review of inflammatory bowel disease in China. ScientificWorldJournal 2013, 2013:296470.
3. Ponder A, Long MD: A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin Epidemiol 2013, 5:237-247.
4. Baumgart DC, Carding SR: Inflammatory bowel disease: cause and immunobiology. Lancet 2007, 369:1627-1640.
5. Kornbluth A, Sachar DB, Practice Parameters Committee of the American College of G: Ulcerative colitis practice guidelines in adults: American College Of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol 2010, 105:501-523. quiz 524.
6. Toruner M, Loftus EV Jr, Harmsen WS, Zinsmeister AR, Orenstein R, Sandborn WJ, Colombel JF, Egan LJ: Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 2008, 134:929-936.
7. Naganuma M, Kunisaki R, Yoshimura N, Takeuchi Y, Watanabe M: A prospective analysis of the incidence of and risk factors for opportunistic infections in patients with inflammatory bowel disease. J Gastroenterol 2013, 48:595-600.
8. Sternthal MB, Murphy SJ, George J, Kornbluth A, Lichtiger S, Present DH: Adverse events associated with the use of cyclosporine in patients with inflammatory bowel disease. Am J Gastroenterol 2008, 103:937-943.
9. Singh UP, Singh NP, Singh B, Mishra MK, Nagarkatti M, Nagarkatti PS, Singh SR: Stem cells as potential therapeutic targets for inflammatory bowel disease. Front Biosci (Schol Ed) 2010, 2:993-1008.
10. Larsen S, Lewis ID: Potential therapeutic applications of mesenchymal stromal cells. Pathology 2011, 43:592-604.
11. Luo Q, Zhang C, Song G: Research progresses of paracrine effect of bone marrow derived mesenchymal stem cells on wound healing. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 2012, 29:999-1002.
12. Xu X, Zhu F, Zhang M, Zeng D, Luo D, Liu G, Cui W, Wang S, Guo W, Xing W, Liang H, Li L, Fu X, Jiang J, Huang H: Stromal cell-derived factor-1 enhances wound healing through recruiting bone marrow-derived mesenchymal stem cells to the wound area and promoting neovascularization. Cells Tissues Organs 2013, 197:103-113.
13. He XW, He XS, Lian L, Wu XJ, Lan P: Systemic infusion of bone marrow-derived mesenchymal stem cells for treatment of experimental colitis in mice. Dig Dis Sci 2012, 57:3136-3144.
14. De Miguel MP, Fuentes-Julian S, Blazquez-Martinez A, Pascual CY, Aller MA, Arias J, Arnalich-Montiel F: Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr Mol Med 2012, 12:574-591.
15. Molendijk I, Duijvestein M, van der Meulen-de Jong AE, van Deen WK, Swets M, Hommes DW, Verspaget HW: Immunomodulatory effects of mesenchymal stromal cells in Crohn's disease. J Allergy (Cairo) 2012, 2012:187408.
16. Soleymaninejadian E, Pramanik K, Samadian E: Immunomodulatory properties of mesenchymal stem cells: cytokines and factors. Am J Reprod Immunol 2012, 67:1-8.
17. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O: HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003, 31:890-896.
18. Li M, Ikehara S: Bone-marrow-derived mesenchymal stem cells for organ repair. Stem Cells Int 2013, 2013:132642.
19. Hayashi Y, Tsuji S, Tsujii M, Nishida T, Ishii S, Iijima H, Nakamura T, Eguchi H, Miyoshi E, Hayashi N, 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.
20. Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW, Thebaud B, Riordan NH: Endometrial regenerative cells: a novel stem cell population. J Transl Med 2007, 5:57.
21. Murphy MP, Wang H, Patel AN, Kambhampati S, Angle N, Chan K, Marleau AM, Pyszniak A, Carrier E, Ichim TE, Riordan NH: Allogeneic endometrial regenerative cells: an "Off the shelf solution" for critical limb ischemia? J Transl Med 2008, 6:45.
22. Borlongan CV, Kaneko Y, Maki M, Yu SJ, Ali M, Allickson JG, Sanberg CD, Kuzmin-Nichols N, Sanberg PR: Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev 2010, 19:439-452.
23. Bockeria L, Bogin V, Bockeria O, Le T, Alekyan B, Woods EJ, Brown AA, Ichim TE, Patel AN: Endometrial regenerative cells for treatment of heart failure: a new stem cell enters the clinic. J Transl Med 2013, 11:56.
24. Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, Mori T, Miyado K, Ikegami Y, Cui C, Kiyono T, Kyo S, Shimizu T, Okano T, Sakamoto M, Ogawa S, Umezawa A: Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells 2008, 26:1695-1704.
25. Kihara N, de la Fuente SG, Fujino K, Takahashi T, Pappas TN, Mantyh CR: Vanilloid receptor-1 containing primary sensory neurones mediate dextran sulphate sodium induced colitis in rats. Gut 2003, 52:713-719.
26. Chidlow JH Jr, Langston W, Greer JJ, Ostanin D, Abdelbaqi M, Houghton J, Senthilkumar A, Shukla D, Mazar AP, Grisham MB, Kevil CG: Differential angiogenic regulation of experimental colitis. Am J Pathol 2006, 169:2014-2030.
27. Liang Y, Hou X, Cui Q, Kang TB, Fu JH, Zhang LJ, Luo RZ, He JH, Zeng YX, Yang HX: Skp2 expression unfavorably impacts survival in resectable esophageal squamous cell carcinoma. J Transl Med 2012, 10:73.
28. Zhong Z, Patel AN, Ichim TE, Riordan NH, Wang H, Min WP, Woods EJ, Reid M, Mansilla E, Marin GH, Drago H, Murphy MP, Minev B: Feasibility investigation of allogeneic endometrial regenerative cells. J Transl Med 2009, 7:15.
29. Neurath MF: Cytokines in inflammatory bowel disease. Nat Rev Immunol 2014, 14:329-342.
30. Al-Hassi HO, Mann ER, Sanchez B, English NR, Peake ST, Landy J, Man R, Urdaci M, Hart AL, Fernandez-Salazar L, Lee GH, Garrote JA, Arranz E, Margolles A, Stagg AJ, Knight SC, Bernardo D: Altered human gut dendritic cell properties in ulcerative colitis are reversed by Lactobacillus plantarum extracellular encrypted peptide STp. Mol Nutr Food Res 2014, 58:1132-1143.
31. Kim MG, Kim SH, Noh H, Ko YS, Lee HY, Jo SK, Cho WY, Kim HK: CD11c(+) cells partially mediate the renoprotective effect induced by bone marrow-derived mesenchymal stem cells. PLoS One 2013, 8:e72544.
32. Choi YS, Jeong JA, Lim DS: Mesenchymal stem cell-mediated immature dendritic cells induce regulatory T cell-based immunosuppressive effect. Immunol Invest 2012, 41:214-229.
33. Chiesa S, Morbelli S, Morando S, Massollo M, Marini C, Bertoni A, Frassoni F, Bartolome ST, Sambuceti G, Traggiai E, Uccelli A: Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci U S A 2011, 108:17384-17389.
34. Drakes ML, Blanchard TG, Czinn SJ: Colon lamina propria dendritic cells induce a proinflammatory cytokine response in lamina propria T cells in the SCID mouse model of colitis. J Leukoc Biol 2005, 78:1291-1300.
35. Himmel ME, Yao Y, Orban PC, Steiner TS, Levings MK: Regulatory T-cell therapy for inflammatory bowel disease: more questions than answers. Immunology 2012, 136:115-122.
36. Coombes JL, Robinson NJ, Maloy KJ, Uhlig HH, Powrie F: Regulatory T cells and intestinal homeostasis. Immunol Rev 2005, 204:184-194.
37. Maloy KJ, Antonelli LR, Lefevre M, Powrie F: Cure of innate intestinal immune pathology by CD4+CD25+ regulatory T cells. Immunol Lett 2005, 97:189-192.
38. Himmel ME, Hardenberg G, Piccirillo CA, Steiner TS, Levings MK: The role of T-regulatory cells and Toll-like receptors in the pathogenesis of human inflammatory bowel disease. Immunology 2008, 125:145-153.
39. Muller S, Lory J, Corazza N, Griffiths GM, Z'Graggen K, Mazzucchelli L, Kappeler A, Mueller C: Activated CD4+ and CD8+ cytotoxic cells are present in increased numbers in the intestinal mucosa from patients with active inflammatory bowel disease. Am J Pathol 1998, 152:261-268.
40. Westendorf AM, Fleissner D, Deppenmeier S, Gruber AD, Bruder D, Hansen W, Liblau R, Buer J: Autoimmune-mediated intestinal inflammation-impact and regulation of antigen-specific CD8+ T cells. Gastroenterology 2006, 131:510-524.
41. Nancey S, Holvoet S, Graber I, Joubert G, Philippe D, Martin S, Nicolas JF, Desreumaux P, Flourie B, Kaiserlian D: CD8+ cytotoxic T cells induce relapsing colitis in normal mice. Gastroenterology 2006, 131:485-496.
42. Lotfinegad P, Shamsasenjan K, Movassaghpour A, Majidi J, Baradaran B: Immunomodulatory nature and site specific affinity of mesenchymal stem cells: a hope in cell therapy. Adv Pharm Bull 2014, 4:5-13.
43. Torres MI, Rios A: Current view of the immunopathogenesis in inflammatory bowel disease and its implications for therapy. World J Gastroenterol 2008, 14:1972-1980.
44. Muzes G, Molnar B, Tulassay Z, Sipos F: Changes of the cytokine profile in inflammatory bowel diseases. World J Gastroenterol 2012, 18:5848-5861.
45. Sanchez-Munoz F, Dominguez-Lopez A, Yamamoto-Furusho JK: Role of cytokines in inflammatory bowel disease. World J Gastroenterol 2008, 14:4280-4288.
46. Doorn J, Moll G, Le Blanc K, van Blitterswijk C, de Boer J: Therapeutic applications of mesenchymal stromal cells: paracrine effects and potential improvements. Tissue Eng Part B Rev 2012, 18:101-115.
47. Smith KA: Interleukin-2: inception, impact, and implications. Science 1988, 240:1169-1176.
48. Parekkadan B, Milwid JM: Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 2010, 12:87-117.
49. Mok PL, Leong CF, Cheong SK: Cellular mechanisms of emerging applications of mesenchymal stem cells. Malays J Pathol 2013, 35:17-32.
50. Apostolaki M, Armaka M, Victoratos P, Kollias G: Cellular mechanisms of TNF function in models of inflammation and autoimmunity. Curr Dir Autoimmun 2010, 11:1-26.
51. Lv R, Qiao W, Wu Z, Wang Y, Dai S, Liu Q, Zheng X: Tumor necrosis factor alpha blocking agents as treatment for ulcerative colitis intolerant or refractory to conventional medical therapy: a meta-analysis. PLoS One 2014, 9:e86692.
52. Chen LL, Wang XH, Cui Y, Lian GH, Zhang J, Ouyang CH, Lu FG: Therapeutic effects of four strains of probiotics on experimental colitis in mice. World J Gastroenterol 2009, 15:321-327.
53. Macdonald TT: Viral vectors expressing immunoregulatory cytokines to treat inflammatory bowel disease. Gut 1998, 42:460-461.
54. Xiong J, Lin YH, Bi LH, Wang JD, Bai Y, Liu SD: Effects of interleukin-4 or interleukin-10 gene therapy on trinitrobenzenesulfonic acid-induced murine colitis. BMC Gastroenterol 2013, 13:165.
55. Iijima H, Takahashi I, Kishi D, Kim JK, Kawano S, Hori M, Kiyono H: Alteration of interleukin 4 production results in the inhibition of T helper type 2 cell-dominated inflammatory bowel disease in T cell receptor alpha chain-deficient mice. J Exp Med 1999, 190:607-615.
56. Iyer SS, Cheng G: Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol 2012, 32:23-63.
57. Ranatunga DC, Ramakrishnan A, Uprety P, Wang F, Zhang H, Margolick JB, Brayton C, Bream JH: A protective role for human IL-10-expressing CD4+ T cells in colitis. J Immunol 2012, 189:1243-1252.
58. Dorronsoro A, Fernandez-Rueda J, Fechter K, Ferrin I, Salcedo JM, Jakobsson E, Trigueros C: Human Mesenchymal Stromal Cell-Mediated Immunoregulation: Mechanisms of Action and Clinical Applications. Bone Marrow Res 2013, 2013:203643.
59. Shi Y, Su J, Roberts AI, Shou P, Rabson AB, Ren G: How mesenchymal stem cells interact with tissue immune responses. Trends Immunol 2012, 33:136-143.
60. Khalil PN, Weiler V, Nelson PJ, Khalil MN, Moosmann S, Mutschler WE, Siebeck M, Huss R: Nonmyeloablative stem cell therapy enhances microcirculation and tissue regeneration in murine inflammatory bowel disease. Gastroenterology 2007, 132:944-954.
61. Kim HS, Shin TH, Lee BC, Yu KR, Seo Y, Lee S, Seo MS, Hong IS, Choi SW, Seo KW, Nunez G, Park JH, Kang KS: Human umbilical cord blood mesenchymal stem cells reduce colitis in mice by activating NOD2 signaling to COX2. Gastroenterology 2013, 145:1392-1403. e1391-1398.
62. Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, Lin CP, Wohlgemuth R: Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 2008, 14:181-187.
63. Ge W, Jiang J, Baroja ML, Arp J, Zassoko R, Liu W, Bartholomew A, Garcia B, Wang H: Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am J Transplant 2009, 9:1760-1772.