Immunological and regenerative aspects of hepatic mast cells in liver allograft rejection and tolerance

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Nakano, Toshiaki ^a,b   Lai, Chia Yun ^a,b,d   Goto, Shigeru ^a,b,e   Hsu, Li Wen ^a,b   Kawamoto, Seiji ^c   Ono, Kazuhisa ^c   Chen, Kuang Den ^a,b   Lin, Chih Che ^a,b   Chiu, King Wah ^a,b   Wang, Chih Chi ^a,b   Cheng, Yu Fan ^a,b   Chen, Chao Long ^a,b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c HIROSHIMA UNIVERSITY   (Japan)

^d NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^e Iwao Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HISTAMINE; IMMUNOGLOBULIN E RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 9; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; TRYPTASE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPE; CONTROLLED STUDY; GAMMA DELTA T LYMPHOCYTE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IN VITRO STUDY; LIVER GRAFT REJECTION; LIVER REGENERATION; MALE; MAST CELL; MAST CELL DEGRANULATION; MOLECULAR INTERACTION; NONHUMAN; PROTEIN EXPRESSION; RAT; REGULATORY T LYMPHOCYTE; SPLEEN CELL; STEM CELL; ANIMAL; BIOSYNTHESIS; CYTOLOGY; GRAFT REJECTION; IMMUNOLOGY; LIVER CELL; LIVER TRANSPLANTATION; METABOLISM; PHYSIOLOGY; SPLEEN;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; GRAFT REJECTION; HEPATOCYTES; IMMUNE TOLERANCE; INTERLEUKIN-10; INTERLEUKIN-17; LIVER REGENERATION; LIVER TRANSPLANTATION; MAST CELLS; PROTO-ONCOGENE PROTEINS C-KIT; RATS; SPLEEN; STEM CELL FACTOR; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84998714754     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037202     Document Type: Article

References (66)

1. Starzl TE, Marchioro TL, Vonkaulla KN, Hermann G, Brittain RS, et al. (1963) Homotransplantation of the Liver in Humans. Surg Gynecol Obstet 117: 659-676.
2. Calne RY, Rolles K, White DJ, Thiru S, Evans DB, et al. (1979) Cyclosporin A initially as the only immunosuppressant in 34 recipients of cadaveric organs: 32 kidneys, 2 pancreases, and 2 livers. Lancet 2: 1033-1036.
3. Chu Z, Zhang J, Zhao Y, Ji Q, Zhong J, et al. (2010) Influence of immunosuppressive drugs on the development of CD4(+)CD25(high) Foxp3(+) T cells in liver transplant recipients. Transplant Proc 42: 2599-2601.
4. van de Wetering J, Koumoutsakos P, Peeters A, van der Mast BJ, de Kuiper P, et al. (2011) Discontinuation of calcineurin inhibitors treatment allows the development of FOXP3+ regulatory T-cells in patients after kidney transplantation. Clin Transplant 25: 40-46.
5. Shen Z, Song Q, Chen L, Zhong B, Tang S, et al. (2011) Bidirectional immunoregulation of calcineurin inhibitor tacrolimus on FOXP3 transcription? Med Hypotheses 76: 178-180.
6. Denecke C, Reutzel-Selke A, Sawitzki B, Boenisch O, Khalepy Z, et al. (2012 Low-dose cyclosporine mediates donor hyporesponsiveness in a fully mismatched rat kidney transplant model. Transpl Immunol.
7. Koshiba T, Li Y, Takemura M, Wu Y, Sakaguchi S, et al. (2007) Clinical, immunological, and pathological aspects of operational tolerance after pediatric living-donor liver transplantation. Transpl Immunol 17: 94-97.
8. Martinez-Llordella M, Puig-Pey I, Orlando G, Ramoni M, Tisone G, et al. (2007) Multiparameter immune profiling of operational tolerance in liver transplantation. Am J Transplant 7: 309-319.
9. Demetris AJ (1995) Terminology for hepatic allograft rejection. International Working Party. Hepatology 22: 648-654.
10. Batts KP (1999) Acute and chronic hepatic allograft rejection: pathology and classification. Liver Transpl Surg 5: S21-29.
11. O'Keeffe C, Baird AW, Nolan N, McCormick PA (2002) Mast cell hyperplasia in chronic rejection after liver transplantation. Liver Transpl 8: 50-57.
12. Matsunaga Y, Kawasaki H, Terada T (1999) Stromal mast cells and nerve fibers in various chronic liver diseases: relevance to hepatic fibrosis. Am J Gastroenterol 94: 1923-1932.
13. Farrell DJ, Hines JE, Walls AF, Kelly PJ, Bennett MK, et al. (1995) Intrahepatic mast cells in chronic liver diseases. Hepatology 22: 1175-1181.
14. Armbrust T, Batusic D, Ringe B, Ramadori G (1997) Mast cells distribution in human liver disease and experimental rat liver fibrosis. Indications for mast cell participation in development of liver fibrosis. J Hepatol 26: 1042-1054.
15. Gaca MD, Pickering JA, Arthur MJ, Benyon RC (1999) Human and rat hepatic stellate cells produce stem cell factor: a possible mechanism for mast cell recruitment in liver fibrosis. J Hepatol 30: 850-858.
16. Yamashiro M, Kouda W, Kono N, Tsuneyama K, Matsui O, et al. (1998) Distribution of intrahepatic mast cells in various hepatobiliary disorders. An immunohistochemical study. Virchows Arch 433: 471-479.
17. Khalil RM, Luz A, Mailhammer R, Moeller J, Mohamed AA, et al. (1996) Schistosoma mansoni infection in mice augments the capacity for interleukin 3 (IL-3) and IL-9 production and concurrently enlarges progenitor pools for mast cells and granulocytes-macrophages. Infect Immun 64: 4960-4966.
18. Lajoie G, Nadasdy T, Laszik Z, Blick KE, Silva FG (1996) Mast cells in acute cellular rejection of human renal allografts. Mod Pathol 9: 1118-1125.
19. Abo-Zenah H, Katsoudas S, Wild G, de Takats D, Shortland J, et al. (2002) Early human renal allograft fibrosis: cellular mediators. Nephron 91: 112-119.
20. Goto E, Honjo S, Yamashita H, Shomori K, Adachi H, et al. (2002) Mast cells in human allografted kidney: correlation with interstitial fibrosis. Clin Transplant 16 Suppl 8: 7-11.
21. Yousem SA (1997) The potential role of mast cells in lung allograft rejection. Hum Pathol 28: 179-182.
22. Li QY, Raza-Ahmad A, MacAulay MA, Lalonde LD, Rowden G, et al. (1992) The relationship of mast cells and their secreted products to the volume of fibrosis in posttransplant hearts. Transplantation 53: 1047-1051.
23. Koskinen PK, Kovanen PT, Lindstedt KA, Lemstrom KB (2001) Mast cells in acute and chronic rejection of rat cardiac allografts-a major source of basic fibroblast growth factor. Transplantation 71: 1741-1747.
24. Lu LF, Lind EF, Gondek DC, Bennett KA, Gleeson MW, et al. (2006) Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442: 997-1002.
25. Boerma M, Fiser WP, Hoyt G, Berry GJ, Joseph L, et al. (2007) Influence of mast cells on outcome after heterotopic cardiac transplantation in rats. Transpl Int 20: 256-265.
26. Kamada N, Davies HS, Roser B (1981) Reversal of transplantation immunity by liver grafting. Nature 292: 840-842.
27. Kamada N, Wight DG (1984) Antigen-specific immunosuppression induced by liver transplantation in the rat. Transplantation 38: 217-221.
28. Kamada N (1985) Transfer of specific immunosuppression of graft rejection using lymph from tolerant liver-grafted rats. Immunology 55: 241-247.
29. Lord R, Kamada N, Kobayashi E, Goto S, Sunagawa M (1995) Isolation of a 40 kDa immunoinhibitory protein induced by rat liver transplantation. Transpl Immunol 3: 174-179.
30. Andrzejewski W, Brolsch C (1982) Postoperative reactions of rats after orthotopic liver transplantation: a model for the human response? A histological and biochemical study. Eur Surg Res 14: 428-439.
31. Bearman SI (1997) Use of stem cell factor to mobilize hematopoietic progenitors. Curr Opin Hematol 4: 157-162.
32. Zhang W, Wu K, He W, Gao Y, Huang W, et al. (2010) Transforming growth factor beta 1 plays an important role in inducing CD4(+)CD25(+)forhead box P3(+) regulatory T cells by mast cells. Clin Exp Immunol 161: 490-496.
33. Roark CL, Simonian PL, Fontenot AP, Born WK, O'Brien RL (2008) gammadelta T cells: an important source of IL-17. Curr Opin Immunol 20: 353-357.
34. O'Brien RL, Roark CL, Born WK (2009) IL-17-producing gammadelta T cells. Eur J Immunol 39: 662-666.
35. Do JS, Fink PJ, Li L, Spolski R, Robinson J, et al. (2010) Cutting edge: spontaneous development of IL-17-producing gamma delta T cells in the thymus occurs via a TGF-beta 1-dependent mechanism. J Immunol 184: 1675-1679.
36. Paton WD (1951) Compound 48/80: a potent histamine liberator. Br J Pharmacol Chemother 6: 499-508.
37. Zaruba MM, Theiss HD, Vallaster M, Mehl U, Brunner S, et al. (2009) Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell 4: 313-323.
38. Yovchev MI, Grozdanov PN, Joseph B, Gupta S, Dabeva MD (2007) Novel hepatic progenitor cell surface markers in the adult rat liver. Hepatology 45: 139-149.
39. Yoon SM, Gerasimidou D, Kuwahara R, Hytiroglou P, Yoo JE, et al. (2011) Epithelial cell adhesion molecule (EpCAM) marks hepatocytes newly derived from stem/progenitor cells in humans. Hepatology 53: 964-973.
40. Fiegel HC, Park JJ, Lioznov MV, Martin A, Jaeschke-Melli S, et al. (2003) Characterization of cell types during rat liver development. Hepatology 37: 148-154.
41. Gassel HJ, Engemann R, Thiede A, Hamelmann H (1987) Replacement of donor Kupffer cells by recipient cells after orthotopic rat liver transplantation. Transplant Proc 19: 351-353.
42. Gouw AS, Houthoff HJ, Huitema S, Beelen JM, Gips CH, et al. (1987) Expression of major histocompatibility complex antigens and replacement of donor cells by recipient ones in human liver grafts. Transplantation 43: 291-296.
43. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, et al. (1999) Bone marrow as a potential source of hepatic oval cells. Science 284: 1168-1170.
44. Theise ND, Nimmakayalu M, Gardner R, Illei PB, Morgan G, et al. (2000) Liver from bone marrow in humans. Hepatology 32: 11-16.
45. Theise ND, Badve S, Saxena R, Henegariu O, Sell S, et al. (2000) Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31: 235-240.
46. Wu T, Cieply K, Nalesnik MA, Randhawa PS, Sonzogni A, et al. (2003) Minimal evidence of transdifferentiation from recipient bone marrow to parenchymal cells in regenerating and long-surviving human allografts. Am J Transplant 3: 1173-1181.
47. Romagnani S (2006) Regulation of the T cell response. Clin Exp Allergy 36: 1357-1366.
48. Cao Y, Zhao J, Lei Z, Shen S, Liu C, et al. (2008) Local accumulation of FOXP3+ regulatory T cells: evidence for an immune evasion mechanism in patients with large condylomata acuminata. J Immunol 180: 7681-7686.
49. Li J, Lai X, Liao W, He Y, Liu Y, et al. (2011) The dynamic changes of Th17/Treg cytokines in rat liver transplant rejection and tolerance. Int Immunopharmacol 11: 962-967.
50. Girardi M (2006) Immunosurveillance and immunoregulation by gammadelta T cells. J Invest Dermatol 126: 25-31.
51. Nakano T, Kawamoto S, Lai CY, Sasaki T, Aki T, et al. (2004) Liver transplantation-induced antihistone H1 autoantibodies suppress mixed lymphocyte reaction. Transplantation 77: 1595-1603.
52. Nakano T, Goto S, Lai CY, Hsu LW, Kao YH, et al. (2007) Experimental and clinical significance of antinuclear antibodies in liver transplantation. Transplantation 83: 1122-1125.
53. Nakano T, Goto S, Lai CY, Hsu LW, Ono K, et al. (2007) Impact of vaccine therapy using nuclear histone H1 on allograft survival in experimental organ transplantation. Transpl Immunol 17: 147-152.
54. Nakano T, Goto S, Lai CY, Hsu LW, Wong JL, et al. (2008) Involvement of autoimmunity against nuclear histone H1 in liver transplantation tolerance. Transpl Immunol 19: 87-92.
55. Parseghian MH, Luhrs KA (2006) Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 84: 589-604.
56. Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5: 331-342.
57. Hershko AY, Suzuki R, Charles N, Alvarez-Errico D, Sargent JL, et al. (2011) Mast cell interleukin-2 production contributes to suppression of chronic allergic dermatitis. Immunity 35: 562-571.
58. Yang Z, Zhang B, Li D, Lv M, Huang C, et al. (2010) Mast cells mobilize myeloid-derived suppressor cells and Treg cells in tumor microenvironment via IL-17 pathway in murine hepatocarcinoma model. PLoS One 5: e8922.
59. Truta-Feles K, Lagadari M, Lehmann K, Berod L, Cubillos S, et al. (2010) Histamine modulates gammadelta-T lymphocyte migration and cytotoxicity, via Gi and Gs protein-coupled signalling pathways. Br J Pharmacol 161: 1291-1300.
60. Ren X, Hogaboam C, Carpenter A, Colletti L (2003) Stem cell factor restores hepatocyte proliferation in IL-6 knockout mice following 70% hepatectomy. J Clin Invest 112: 1407-1418.
61. Hu B, Colletti LM (2008) Stem cell factor and c-kit are involved in hepatic recovery after acetaminophen-induced liver injury in mice. Am J Physiol Gastrointest Liver Physiol 295: G45-G53.
62. Ren X, Hu B, Colletti L (2008) Stem cell factor and its receptor, c-kit, are important for hepatocyte proliferation in wild-type and tumor necrosis factor receptor-1 knockout mice after 70% hepatectomy. Surgery 143: 790-802.
63. Michalopoulos GK (2007) Liver regeneration. J Cell Physiol 213: 286-300.
64. Kamada N, Calne RY (1979) Orthotopic liver transplantation in the rat. Technique using cuff for portal vein anastomosis and biliary drainage. Transplantation 28: 47-50.
65. Huang B, Lei Z, Zhang GM, Li D, Song C, et al. (2008) SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood 112: 1269-1279.
66. Tateno C, Takai-Kajihara K, Yamasaki C, Sato H, Yoshizato K (2000) Heterogeneity of growth potential of adult rat hepatocytes in vitro. Hepatology 31: 65-74.