Restoration of intrahepatic regulatory T cells through MMP-9/13-dependent activation of TGF-β is critical for immune homeostasis following acute liver injury

Journal of Molecular Cell Biology

Volumn 5, Issue 6, 2013, Pages 369-379

  Lu, Ling ^a   Feng, Min ^b   Gu, Jia ^a   Xia, Zanxian ^c   Zhang, Hongjun ^d   Zheng, Sujun ^e   Duan, Zhongping ^e   Hu, Richard ^f   Wang, Julie ^d   Shi, Wei ^d   Ji, Cheng ^d   Shen, Yi ^g   Chen, Guihua ^h   Zheng, Song Guo ^g,i   Han, Yuan Ping ^j  

^a NANJING MEDICAL UNIVERSITY   (China)

^b MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e CAPITAL MEDICAL UNIVERSITY   (China)

^f OLIVE VIEW UCLA MEDICAL CENTER   (United States)

^g PENN STATE COLLEGE OF MEDICINE   (United States)

^h SUN YAT SEN UNIVERSITY   (China)

ⁱ Key Laboratory of Arrhythmias of Ministry of Education   (China)

^j SICHUAN UNIVERSITY   (China)

more..

Author keywords

Hepatic stellate cells; IL 1; Liver injury; Matrix metalloproteinase; Regulatory T cells; TGF ; Wound healing

Indexed keywords

CASPASE 3; COLLAGENASE 3; GELATINASE B; HELIOS; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL REGENERATION; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVATION; HEALING; HOMEOSTASIS; IMMUNE SYSTEM; IMMUNOREGULATION; INFLAMMATION; KUPFFER CELL; LIVER INJURY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; STELLATE CELL; TISSUE INJURY; TISSUE REPAIR; WOUND HEALING;

HEPATIC STELLATE CELLS; IL-1; LIVER INJURY; MATRIX METALLOPROTEINASE; REGULATORY T CELLS; TGF-Β; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DRUG-INDUCED LIVER INJURY; FLOW CYTOMETRY; HOMEOSTASIS; LIVER; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 9; MICE; MICE, TRANSGENIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84890361099     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjt042     Document Type: Article

References (41)

1. Akimova, T., Beier, U.H., Wang, L., et al. (2011). Helios expression is a marker of T cell activation and proliferation. PLoS One 6, e24226.
2. + regulatory T cells in immune tolerance. Annu. Rev. Immunol. 30, 733-758.
3. + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886.
4. + regulatory T cells by production of retinoic acid. J. Immunol. 190, 2009-2016.
5. Friedman, S.L. (2008). Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88, 125-172.
6. Gieling, R.G., Wallace, K., and Han, Y.P. (2009). Interleukin-1 participates in the progression from liver injury to fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G1324-G1331.
7. Gorelik, L., and Flavell, R.A. (2000). Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12, 171-181.
8. Han, Y.P., Zhou, L., Wang, J., et al. (2004). Essential role of matrix metalloproteinases in interleukin-1-induced myofibroblastic activation of hepatic stellate cell in collagen. J. Biol. Chem. 279, 4820-4828.
9. Han, Y.P., Yan, C., Zhou, L., et al. (2007). A matrix metalloproteinase-9 activation cascade by hepatic stellate cells in trans-differentiation in the threedimensional extracellular matrix. J. Biol. Chem. 282, 12928-12939.
10. Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061.
11. + regulatory T cells are not mirror images of each other. Trends Immunol. 29, 429-435.
12. Ichikawa, S., Mucida, D., Tyznik, A.J., et al. (2011). Hepatic stellate cells function as regulatory bystanders. J. Immunol. 186, 5549-5555.
13. + T helper cells. Cell 126, 1121-1133.
14. Kida, Y., Xia, Z., Zheng, S., et al. (2011). Interleukin-1 as an injury signal mobilizes retinyl esters in hepatic stellate cells through down regulation of lecithin retinol acyltransferase. PLoS One 6, e26644.
15. Lemire, J.M., Archer, D.C., Beck, L., et al. (1995). Immunosuppressive actions of 1,25-dihydroxyvitamin D3: preferential inhibition of Th1 functions. J. Nutr. 125, 1704S-1708S.
16. Liu, F., Liu, J., Weng, D., et al. (2010). CD4+CD25+Foxp3+ regulatory T cells depletion mayattenuate the development of silica-induced lung fibrosis in mice. PLoS One 5, e15404.
17. + T cells. J. Exp. Med. 205, 1381-1393.
18. Lu, L., Zhou, X., Wang, J., et al. (2010). Characterization of protective human CD4CD25 FOXP3 regulatory T cells generated with IL-2, TGF-beta and retinoic acid. PLoS One 5, e15150.
19. Mangan, P.R., Harrington, L.E., O'Quinn, D.B., et al. (2006). Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441, 231-234.
20. Namba, K., Kitaichi, N., Nishida, T., et al. (2002). Induction of regulatory T cells by the immunomodulating cytokines alpha-melanocyte- stimulating hormone and transforming growth factor-beta2. J. Leukoc. Biol. 72, 946-952.
21. Ormandy, L.A., Hillemann, T., Wedemeyer, H., et al. (2005). Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res. 65, 2457-2464.
22. Qin, L., and Han, Y.P. (2011). Epigenetic repression of matrix metalloproteinases in myofibroblastic hepatic stellate cells through histone deacetylases 4: implication in tissue fibrosis. Am. J. Pathol. 177, 1915-1928.
23. Roncarolo, M.G., and Levings, M.K. (2000). The role of different subsets of T regulatory cells in controlling autoimmunity. Curr. Opin. Immunol. 12, 676-683.
24. Rudensky, A.Y., Gavin, M., and Zheng, Y. (2006). FOXP3 and NFAT: partners in tolerance. Cell 126, 253-256.
25. Sakaguchi, S., Sakaguchi, N., Asano, M., et al. (1995). Immunologic selftolerance maintained by activated T cells expressing IL-2 receptor alphachains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164.
26. + T regulatory cells. J. Immunol. 184, 3433-3441.
27. Tiegs, G., and Lohse, A.W. (2010). Immune tolerance: what is unique about the liver. J. Autoimmun. 34, 1-6.
28. Veldhoen, M., Hocking, R.J., Atkins, C.J., et al. (2006). TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189.
29. Wang, G., Zhong, A., Wang, S., et al. (2010). Retinoic acid attenuates acute heart rejection by increasing regulatory T cell and repressing differentiation of Th17 cell in the presence of TGF-beta. Transpl. Int. 23, 986-997.
30. + regulatory T cells protect against T cell-mediated fulminant hepatitis in a TGF-beta-dependent manner in mice. J. Immunol. 181, 7221-7229.
31. + regulatory T cells and inhibits development of Th17 cells by enhancing TGF-beta-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J. Immunol. 181, 2277-2284.
32. Yan, C., Zhou, L., and Han, Y.P. (2008). Contribution of hepatic stellate cells and matrix metalloproteinase 9 in acute liver failure. Liver Int. 28, 959-971.
33. + regulatory T-cells in the liver of patients with hepatocellular carcinoma. J. Hepatol. 45, 254-262.
34. Yang, X.O., Nurieva, R., Martinez, G.J., et al. (2008). Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29, 44-56.
35. - precursors. J. Immunol. 169, 4183-4189.
36. +CD252 cells to develop suppressive activity: the role of IL-2, TGF-beta, and IL-10. J. Immunol. 172, 5213-5221.
37. + regulatory T cells generated ex vivo with IL-2 and TGF-beta suppress a stimulatory graft-versus-host disease with a lupus-like syndrome. J. Immunol. 172, 1531-1539.
38. + regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6. J. Immunol. 180, 7112-7116.
39. Zhou, L., Fu, J.L., Lu, Y.Y., et al. (2010a). Regulatory T cells are associated with post-cryoablation prognosis in patients with hepatitis B virus-related hepatocellular carcinoma. J. Gastroenterol. 45, 968-978.
40. Zhou, X., Kong, N., Wang, J., et al. (2010b). Cutting edge: all-trans retinoic acid sustains the stability and function of natural regulatory T cells in an inflammatory milieu. J. Immunol. 185, 2675-2679.
41. Zou, W. (2006). Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6, 295-307.