Mesenchymal stem cells alleviate bacteria-induced liver injury in mice by inducing regulatory dendritic cells

Hepatology

Volumn 59, Issue 2, 2014, Pages 671-682

  Zhang, Yi ^a,d   Cai, Wei ^a   Huang, Qingrong ^a   Gu, Yuting ^a   Shi, Yufang ^a   Huang, Jiefang ^a   Zhao, Fang ^a   Liu, Qiang ^a   Wei, Xunbin ^b   Jin, Min ^a   Wu, Changping ^c   Xie, Qing ^a   Wan, Bing ^a   Zhang, Yanyun ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c SOOCHOW UNIVERSITY   (China)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL THERAPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; FULMINANT HEPATIC FAILURE; HELPER CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC INFILTRATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; REGULATORY T LYMPHOCYTE; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; GRAM-POSITIVE BACTERIAL INFECTIONS; LIPOPOLYSACCHARIDES; LIVER; LIVER FAILURE, ACUTE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; PROPIONIBACTERIUM ACNES; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84893644558     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26670     Document Type: Article

References (38)

1. Yoneyama H, Harada A, Imai T, Baba M, Yoshie O, Zhang Y, et al. Pivotal role of TARC, a CC chemokine, in bacteria-induced fulminant hepatic failure in mice. J Clin Invest 1998;102:1933-1941.
2. Hoofnagle JH, Carithers RL Jr, Shapiro C, Ascher N. Fulminant hepatic failure: summary of a workshop. Hepatology 1995;21:240-252.
3. Moniaux N, Song H, Darnaud M, Garbin K, Gigou M, Mitchell C, et al. Human hepatocarcinoma-intestine-pancreas/pancreatitis-associated protein cures fas-induced acute liver failure in mice by attenuating free-radical damage in injured livers. Hepatology 2011;53:618-627.
4. Nemes B, Gelley F, Piros L, Zadori G, Gorog D, Fehervari I, et al. The impact of Milan criteria on liver transplantation for hepatocellular carcinoma: first 15 years' experience of the Hungarian Liver Transplant Program. Transplant Proc 2011;43:1272-1274.
5. Shi Y, Hu G, Su J, Li W, Chen Q, Shou P, et al. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res 2010;20:510-518.
6. Pileggi A. Mesenchymal stem cells for the treatment of diabetes. Diabetes 2012;61:1355-1356.
7. Papadopoulou A, Yiangou M, Athanasiou E, Zogas N, Kaloyannidis P, Batsis I, et al. Mesenchymal stem cells are conditionally therapeutic in preclinical models of rheumatoid arthritis. Ann Rheum Dis 2012;71:1733-1740.
8. Li W, Ren G, Huang Y, Su J, Han Y, Li J, et al. Mesenchymal stem cells: a double-edged sword in regulating immune responses. Cell Death Differ 2012;19:1505-1513.
9. Aquino JB, Bolontrade MF, Garcia MG, Podhajcer OL, Mazzolini G. Mesenchymal stem cells as therapeutic tools and gene carriers in liver fibrosis and hepatocellular carcinoma. Gene Ther 2010;17:692-708.
10. Adler HS, Steinbrink K. Tolerogenic dendritic cells in health and disease: friend and foe! Eur J Dermatol 2007;17:476-491.
11. Liu X, Qu X, Chen Y, Liao L, Cheng K, Shao C, et al. Mesenchymal stem/stromal cells induce the generation of novel IL-10-dependent regulatory dendritic cells by SOCS3 activation. J Immunol 2012;189:1182-1192.
12. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 2006;177:2080-2087.
13. Yoneyama H, Narumi S, Zhang Y, Murai M, Baggiolini M, Lanzavecchia A, et al. Pivotal role of dendritic cell-derived CXCL10 in the retention of T helper cell 1 lymphocytes in secondary lymph nodes. J Exp Med 2002;195:1257-1266.
14. Yoneyama H, Matsuno K, Zhang Y, Murai M, Itakura M, Ishikawa S, et al. Regulation by chemokines of circulating dendritic cell precursors, and the formation of portal tract-associated lymphoid tissue, in a granulomatous liver disease. J Exp Med 2001;193:35-49.
15. Zhang Y, Yoneyama H, Wang Y, Ishikawa S, Hashimoto S, Gao JL, et al. Mobilization of dendritic cell precursors into the circulation by administration of MIP-1alpha in mice. J Natl Cancer Inst 2004;96:201-209.
16. Xiao Y, Xu J, Mao C, Jin M, Wu Q, Zou J, et al. 18Beta-glycyrrhetinic acid ameliorates acute Propionibacterium acnes-induced liver injury through inhibition of macrophage inflammatory protein-1alpha. J Biol Chem 2010;285:1128-1137.
17. Hattori T, Saban DR, Emami-Naeini P, Chauhan SK, Funaki T, Ueno H, et al. Donor-derived, tolerogenic dendritic cells suppress immune rejection in the indirect allosensitization-dominant setting of corneal transplantation. J Leukoc Biol 2012;91:621-627.
18. Grangette C. Bifidobacteria and subsets of dendritic cells: friendly players in immune regulation! Gut 2012;61:331-332.
19. Yen JH, Kocieda VP, Jing H, Ganea D. Prostaglandin E2 induces matrix metalloproteinase 9 expression in dendritic cells through two independent signaling pathways leading to activator protein 1 (AP-1) activation. J Biol Chem 2011;286:38913-38923.
20. Caparros E, Munoz P, Sierra-Filardi E, Serrano-Gomez D, Puig-Kroger A, Rodriguez-Fernandez JL, et al. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 2006;107:3950-3958.
21. Chamberlain J, Yamagami T, Colletti E, Theise ND, Desai J, Frias A, et al. Efficient generation of human hepatocytes by the intrahepatic delivery of clonal human mesenchymal stem cells in fetal sheep. Hepatology 2007;46:1935-1945.
22. Sato K, Yamashita N, Baba M, Matsuyama T. Regulatory dendritic cells protect mice from murine acute graft-versus-host disease and leukemia relapse. Immunity 2003;18:367-379.
23. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 2002;23:445-449.
24. Menges M, Rossner S, Voigtlander C, Schindler H, Kukutsch NA, Bogdan C, et al. Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J Exp Med 2002;195:15-21.
25. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001;2:725-731.
26. Matta BM, Raimondi G, Rosborough BR, Sumpter TL, Thomson AW. IL-27 production and STAT3-dependent upregulation of B7-H1 mediate immune regulatory functions of liver plasmacytoid dendritic cells. J Immunol 2012;188:5227-5237.
27. Popov A, Abdullah Z, Wickenhauser C, Saric T, Driesen J, Hanisch FG, et al. Indoleamine 2, 3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. J Clin Invest 2006;116:3160-3170.
28. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-βeta and retinoic acid-dependent mechanism. J Exp Med 2007;204:1757-1764.
29. Takagi H, Fukaya T, Eizumi K, Sato Y, Sato K, Shibazaki A, et al. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 2011;35:958-971.
30. Li YP, Paczesny S, Lauret E, Poirault S, Bordigoni P, Mekhloufi F, et al. Human mesenchymal stem cells license adult CD34+ hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway. J Immunol 2008;180:1598-1608.
31. Bendelac A, Bonneville M, Kearney JF. Autoreactivity by design: innate B and T lymphocytes. Nat Rev Immunol 2001;1:177-186.
32. Ochsenbein AF, Pinschewer DD, Odermatt B, Ciurea A, Hengartner H, Zinkernagel RM. Correlation of T cell independence of antibody responses with antigen dose reaching secondary lymphoid organs: implications for splenectomized patients and vaccine design. J Immunol 2000;164:6296-6302.
33. Schmidt LM, Belvisi MG, Bode KA, Bauer J, Schmidt C, Suchy MT, et al. Bronchial epithelial cell-derived prostaglandin E2 dampens the reactivity of dendritic cells. J Immunol 2011;186:2095-2105.
34. Harizi H, Gualde N. Pivotal role of PGE2 and IL-10 in the cross-regulation of dendritic cell-derived inflammatory mediators. Cell Mol Immunol 2006;3:271-277.
35. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol 2009;37:1445-1453.
36. Zhang QZ, Su WR, Shi SH, Wilder-Smith P, Xiang AP, Wong A, et al. Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 2010;28:1856-1868.
37. van Poll D, Parekkadan B, Cho CH, Berthiaume F, Nahmias Y, Tilles AW, et al. Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 2008;47:1634-1643.
38. Peng L, Xie DY, Lin BL, Liu J, Zhu HP, Xie C, et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes. Hepatology 2011;54:820-828.