Mast cells participate in allograft rejection: can IL-37 play an inhibitory role?

Inflammation Research

Volumn 67, Issue 9, 2018, Pages 747-755

  Conti, Pio ^a   Caraffa, Alessandro ^b   Ronconi, Gianpaolo ^c   Kritas, Spiros K ^d   Mastrangelo, Filiberto ^e   Tettamanti, Lucia ^f   Frydas, Ilias ^d   Theoharides, Theoharis C ^g  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

^d ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^e UNIVERSITY OF FOGGIA   (Italy)

^f UNIVERSITY OF INSUBRIA   (Italy)

^g TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chemokine; Cytokine; Inflammation; Macrophage; Mast cell; Rejection

Indexed keywords

IMMUNOGLOBULIN E; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 33; INTERLEUKIN 37; MYELOID DIFFERENTIATION FACTOR 88; CYTOKINE;

ADAPTIVE IMMUNITY; ALLERGIC ASTHMA; ANAPHYLAXIS; CELL ACTIVATION; CROSS LINKING; CYTOKINE RELEASE; GRAFT REJECTION; HUMAN; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; MACROPHAGE CELL LINE; MALIGNANT NEOPLASM; MAST CELL; NEUTROPHIL CHEMOTAXIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; TLR SIGNALING; ALLOGRAFT; ANIMAL; IMMUNOLOGY;

ALLOGRAFTS; ANIMALS; CYTOKINES; GRAFT REJECTION; HUMANS; IMMUNITY, INNATE; MAST CELLS;

EID: 85049232450     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-018-1166-3     Document Type: Review

References (83)

1. Dinarello CA, Conti P, Mier JW. Effects of human interleukin-1 on natural killer cell activity: is fever a host defense mechanism for tumor killing? Yale J Biol Med. 1986;59(2):97–106
2. Netea MG, Nold-Petry CA, Nold MF, et al. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood. 2009;113(10):2324–35. 10.1182/blood-2008-03-146720
3. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood. 1996;87(6):2095–147
4. de Mooij CEM, Netea MG, van der Velden WJFM, Blijlevens NMA. Targeting the interleukin-1 pathway in patients with hematological. disorders Blood. 2017;129(24):3155–64. 10.1182/blood-2016-12-754994
5. Berda-Haddad Y, Robert S, Salers P, et al. Sterile inflammation of endothelial cell-derived apoptotic bodies is mediated by interleukin-1α. Proc Natl Acad Sci USA. 2011;108(51):20684–9. 10.1073/pnas.1116848108
6. Chen F, Date H. Update on ischemia-reperfusion injury in lung transplantation. Curr Opin Organ Transplant. 2015;20(5):515–20
7. Liu XL, Zhao X, Wang C, Gao SJ, Tan YH. Decitabine treatment for acute myeloid leukemia relapse after allogeneic hematopoietic stem cell transplantation. J Biol Regul Homeost Agents. 2017;31(1):171–5
8. Bharat A, Mohanakumar T. Immune responses to tissue-restricted nonmajor histocompatibility complex antigens in allograft. rejection. J Immunol Res. 2017;2017:6312514. 10.1155/2017/6312514
9. Qiao LW, Qu QS, Jiang X. Evaluation of tolerance and safety of conversion from mycophenolate mofetil to enteric-coated mycophenolic acid in renal transplant recipients. J Biol Regul Homeost Agents. 2017;31(1):141–6
10. Krams SM, Ascher NL, Martinez OM. New immunologic insights into mechanisms of allograft rejection. Gastroenterol Clin North Am. 1993;22(2):381–400
11. Hall BM. Cells T. Soldiers and Spies—the surveillance and control of effector T cells by regulatory T cells. Clin J Am Soc Nephrol. 2015;10(11):2050–64
12. Alegre ML, Florquin S, Goldman M. Cellular mechanisms underlying acute graft rejection: time for reassessment. Curr Opin Immunol. 2007;19(5):563–8
13. Galli SJ, Gaudenzio N. Human mast cells as antigen-presenting cells: when is this role important in vivo? J Allergy Clin Immunol. 2017. 10.1016/j.jaci.2017.05.029 (epub ahead of print)
14. Jahanyar J, Koerner MM, Loebe M, Youker KA, Torre-Amione G, Noon GP. The role of mast cells after solid organ transplantation. Transplantation. 2008;85(10):1365–71
15. Zegarska J, Paczek L, Pawlowska M, et al. Quantitative gene expression of TGF-beta1, TNF-alpha, IL-1beta, and IL-6 in the renal artery wall of chronically rejected human renal allografts. Transplant Proc. 2002;34(8):3176–9
16. Seto T, Kamijo S, Wada Y, et al. Upregulation of the apoptosis-related inflammasome in cardiac allograft rejection. J Heart Lung Transplant. 2010;29(3):352–9. 10.1016/j.healun.2009.09.008
17. Teppo AM, Honkanen E, Ahonen J, Grönhagen-Riska C. Does increased urinary interleukin-1 receptor antagonist/interleukin-1beta ratio indicate good prognosis in renal transplant. recipients? Transplantation. 1998;66(8):1009–14
18. Theoharides TC, Kempuraj D, Tagen M, Conti P, Kalogeromitros D. Differential release of mast cell mediators and the pathogenesis of inflammation. Immunol Rev. 2007;217:65–78
19. Toniato E, Frydas I, Robuffo I, et al. Activation and inhibition of adaptive immune response mediated by mast cells. J Biol Regul Homeost Agents. 2017;31(3):543–8
20. Zhang B, Alysandratos KD, Angelidou A, et al. Human mast cell degranulation and preformed TNF secretion require mitochondrial translocation to exocytosis sites: relevance to atopic dermatitis. J Allergy Clin Immunol. 2011;127(6):1522–31.e8. 10.1016/j.jaci.2011.02.005
21. Conti P, Caraffa Al, Kritas SK, et al. Mast cell, pro-inflammatory and anti-inflammatory: Jekyll and Hyde, the story continues. J Biol Regul Homeost Agents. 2017;31(2):263–7
22. Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as “tunable” effector and immunoregulatory cells: recent advances. Annu Rev Immunol. 2005;23:749–86
23. Theoharides TC, Stewart JM, Tsilioni I. Tolerability and benefit of a tetramethoxyluteolin-containing skin lotion. Int J Immunopathol Pharmacol. 2017;30(2):146–51. 10.1177/0394632017707610
24. Ranjan S, Goihl A, Kohli S, et al. Activated protein C protects from GvHD via PAR2/PAR3 signalling in regulatory T-cells. Nat Commun. 2017;8(1):311. 10.1038/s41467-017-00169-4
25. Siracusa MC, Kim BS, Spergel JM, Artis D. Basophils and allergic inflammation. J Allergy Clin Immunol. 2013;132(4):789–801. 10.1016/j.jaci.2013.07.046
26. Taracanova A, Alevizos M, Karagkouni A, et al. SP and IL-33 together markedly enhance TNF synthesis and secretion from human mast cells mediated by the interaction of their receptors. Proc Natl Acad Sci USA. 2017;114(20):E4002–9. 10.1073/pnas.1524845114
27. Conti P, Caraffa A, Ronconi G, Kritas SK, Mastrangelo F, Tettamanti L, Theoharides TC. Impact of mast cells in mucosal immunity of intestinal inflammation: inhibitory effect of IL-37. Eur J Pharmacol. 2017 10.1016/j.ejphar.2017.09.044 (epub ahead of print)
28. + T cells and ILC2 cells in primary and secondary immunity to Strongyloides venezuelensis. Infect Immun 2017;85(5). 10.1128/IAI.00053-17
29. Presta I, Guadagno E, Di Vito A, et al. Innate immunity may play a role in growth and relapse of chordoid meningioma. Int J Immunopathol Pharmacol. 2017. 10.1177/0394632017730241
30. Amaral RC, Barbeiro DF, Koike MK, et al. Cytokine and chemokine levels in the heart tissue of aged rats following severe acute pancreatitis. Eur J Inflamm. 2017;2:102–6
31. Félix NM, Goy-Thollot I, Walton RS, et al. Garlic tablet supplementation reduces lipopolysaccharide-induced TNF-alpha production by peripheral blood mononuclear cells. Eur J Inflamm. 2016;3:190–5
32. Caraffa A, Spinas E, Kritas SK, et al. Endocrinology of the skin: intradermal neuroimmune network, a new frontier. J Biol Regul Homeost Agents. 2016;30(2):339–43
33. Mack M, Rosenkranz AR. Basophils and mast cells in renal injury. Kidney Int. 2009;76(11):1142–7
34. Conti P, Ronconi G, Caraffa A, Lessiani G, Duraisamy K. IL-37 a New IL-1 family member emerges as a key suppressor of asthma mediated by mast cells. Immunol Invest. 2017;46(3):239–50. 10.1080/08820139.2016.1250220
35. + regulatory T cells. Blood. 2013;122(22):3659–65. 10.1182/blood-2013-08-519157
36. Jungraithmayr W. The putative role of mast cells in lung transplantation. Am J Transplant. 2015;15(3):594–600. 10.1111/ajt.13126. (review)
37. Nourshargh S, Alon R. Leukocyte migration into inflamed tissues. Immunity. 2014;41(5):694–707. 10.1016/j.immuni.2014.10.008
38. Franzese O, Mascali A, Capria A, Castagnola V, Paganizza L, Di Daniele N. Regulatory T cells in the immunodiagnosis and outcome of kidney allograft rejection. Clin Dev Immunol. 2013;2013:852395. 10.1155/2013/852395
39. Su C, Yang T, Wu Z, Zhong J, Huang Y, Huang T, Zheng E. Differentiation of T-helper cells in distinct phases of atopic dermatitis involves Th1/Th2 and Th17/Treg. Eur J Inflamm. 2017;1:46–52
40. Conti P, Pang X, Boucher W, et al. Impact of Rantes and MCP-1 chemokines on in vivo basophilic cell recruitment in rat skin injection model and their role in modifying the protein and mRNA levels for histidine decarboxylase. Blood. 1997;89(11):4120–7
41. Mekori YA, Baram D. Heterotypic adhesion-induced mast cell activation: biologic relevance in the inflammatory context. Mol Immunol. 2002;38(16–18):1363–7
42. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis. Annu Rev Immunol. 2009;27:165–97. 10.1146/annurev.immunol.021908.132620
43. Piccinni MP, Maggi E, Romagnani S. Environmental factors favoring the allergen-specific Th2 response in allergic subjects. Ann NY Acad Sci. 2000;917:844–52
44. + T cells in inflammatory bowel disease. J Biol Regul Homeost Agents. 2017;31(2):279–87
45. Jungraithmayr W. The putative role of mast cells in lung transplantation. Am J Transplant. 2015;15(3):594–600. 10.1111/ajt.13126
46. Theoharides TC, Conti P. Mast cells: the Jekyll and Hyde of tumor growth. Trends Immunol. 2004;25(5):235–41
47. Grimbaldeston MA, Nakae S, Kalesnikoff J, Tsai M, Galli SJ. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol. 2007;8(10):1095–104
48. Lu L, Lee WC, Takayama T, et al. Genetic engineering of dendritic cells to express immunosuppressive molecules [viral IL-10, TGF-beta, and CTLA4Ig. J Leukoc Biol. 1999;66(2):293–96
49. Itoh S, Nakae S, Velotta JB, et al. The role of recipient mast cells in acute and chronic cardiac allograft rejection in C57BL/6-KitW-sh/W-sh mice. J Heart Lung Transplant. 2010;29(4):401–9
50. Rakhmilevich AL, North RJ, Dye ES. Evidence inconsistent with a role for tumor necrosis factor in tumor allograft rejection. Transplantation. 1993;55(1):182–6
51. Rojas-Zuleta WG, Sanchez E. IL-9: function, sources, and detection. Methods Mol Biol. 2017;1585:21–35. 10.1007/978-1-4939-6877-0_2
52. Weigt SS, Palchevskiy V, Belperio JA. Inflammasomes and IL-1 biology in the pathogenesis of allograft dysfunction. J Clin Invest. 2017;127(6):2022–9. 10.1172/JCI93537
53. Tsampalieros A, Knoll GA, Molnar AO, Fergusson N, Fergusson DA. Corticosteroid use and growth after pediatric solid organ transplantation: a systematic review and meta-analysis. Transplantation. 2017;101(4):694–703. 10.1097/TP.0000000000001320
54. Tsipotis E, Gupta NR, Raman G, Zintzaras E, Jaber BL. Bioavailability, efficacy and safety of generic immunosuppressive drugs for kidney transplantation: a systematic review and meta-analysis. Am J Nephrol. 2016;44(3):206–18. 10.1159/000449020
55. Fruhwald F, Lassner D, Fruhwald S, Gross UM, Dapunt O, Schultheiss HP. Immunosuppressive treatment in fulminant myocarditis and gene expression pattern associated with, but no histological confirmation of giant cell myocarditis. ESC Heart Fail. 2017;4(2):190–2. 10.1002/ehf2.12130
56. Zhou J, Wang J, Gu M-Y, et al. Effect of dexamethasone on TLR4 and MyD88 expression in monocytes of patients with tuberculous meningitis. Eur J Inflamm. 2017;2:107–12
57. Bach JF. Immunosuppressive therapy of autoimmune diseases. Immunol Today. 1993;14(6):322–6
58. Yapici Ü, Kers J, Bemelman FJ, et al. Interleukin-17 positive cells accumulate in renal allografts during acute rejection and are independent predictors of worse graft outcome. Transpl Int. 2011;24(10):1008–17. 10.1111/j.1432-2277.2011.01302.x
59. DeBenedette MA, Wen T, Bachmann MF, et al. Analysis of 4-1BB ligand [4-1BBL-deficient mice and of mice lacking both 4-1BBL and CD28 reveals a role for 4-1BBL in skin allograft rejection and in the cytotoxic T cell response to influenza virus. J Immunol. 1999;163(9):4833–41
60. Zhang WF, Li ZT, Fang JJ, et al. Expression and clinical significance of rhubarb on serum amylase and TNF-alpha of rat model of acute pancreatitis. J Biol Regul Homeost Agents. 2017;31(3):753–60
61. Zweifel M, Matozan K, Dahinden C, Schaffner T, Mohacsi P. Eotaxin/CCL11 levels correlate with myocardial fibrosis and mast cell density in native and transplanted rat hearts. Transplant Proc. 2010;42(7):2763–6. 10.1016/j.transproceed.2010.05.152
62. Baan CC, Kannegieter NM, Felipe CR, Tedesco Silva H Jr. Targeting JAK/STAT signaling to prevent rejection after kidney transplantation: a reappraisal. Transplantation. 2016;100(9):1833–9. 10.1097/TP.0000000000001226
63. Norrby K. Tumor-bearing depresses distant mast-cell-mediated mitogenesis. Acta Pathol Microbiol Immunol Scand A. 1984;92(6):395–400
64. Cross KS, el-Sanadiki MN, Murray JJ, Mikat EM, McCann RL, Hagen PO. Mast cell infiltration: a possible mechanism for vein graft vasospasm. Surgery. 1988;104(2):171–7
65. Nold MF, Nold-Petry CA, Zepp JA, Palmer BE, Bufler P, Dinarello CA. IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol. 2010;1 1(11):1014–22. 10.1038/ni.1944
66. Carinci F, Lessiani G, Spinas E, et al. Mast cell and cancer with special emphasis on il-37 an anti-inflammatory and inhibitor of innate immunity: new frontiers. J Biol Regul Homeost Agents. 2016;30(4):945–950
67. Boraschi D, Lucchesi D, Hainzl S, et al. IL-37: a new anti-inflammatory cytokine of the IL-1 family. Eur Cytokine Netw. 2011;22(3):127–47. 10.1684/ecn.2011.0288
68. Bednarczyk M, Muc-Wierzgoń M, Walkiewicz K, Kokot T, Fatyga E, Mazurek U. Profile of gene expression of TLR-signaling pathways in colorectal cancer tissues. Int J Immunopathol Pharmacol. 2017;30(3):322–6. 10.1177/0394632017716048
69. Kulka M, Alexopoulou L, Flavell RA, Metcalfe DD. Activation of mast cells by double-stranded RNA: evidence for activation through toll-like receptor 3. J Allergy Clin Immunol. 2004;114(1):174–82
70. Guo J, Liang W, Li J, Long J. Knockdown of FSTL1 inhibits oxLDL-induced inflammation responses through the TLR4/MyD88/NF-κB and MAPK pathway. Biochem Biophys Res Commun. 2016;478(4):1528–33. 10.1016/j.bbrc.2016.08.138
71. Aragona SE, Amori P, Mereghetti G, Lotti J, Lotti T. Chronic inflammation therapy combined with low dose cytokines in the treatment of chronic ulcers of lower limbs. J Biol Regul Homeost Agents. 2017;31(2 Suppl. 2):193–200
72. Li XC. The significance of non-T-cell pathways in graft rejection: implications for transplant tolerance. Transplantation. 2010;90(10):1043–7
73. Zhan Q, Zeng Q, Song R, et al. IL-37 suppresses MyD88-mediated inflammatory responses in human aortic valve interstitial cells. Mol Med. 2017; 10.2119/molmed.2017.00022 (epub ahead of print)
74. Nakanishi K, Yoshimoto T, Tsutsui H, Okamura H. Interleukin-18 is a unique cytokine that stimulates both Th1 and Th2 responses depending on its cytokine milieu. Cytokine Growth Factor Rev. 2001;12(1):53–72
75. Dinarello CA. Interleukin-18 and the pathogenesis of inflammatory diseases. Semin Nephrol. 2007;27(1):98–114
76. Luo Y, Cai X, Liu S, et al. Suppression of antigen-specific adaptive immunity by IL-37 via induction of tolerogenic dendritic cells. Proc Natl Acad Sci USA. 2014;111(42):15178–83. 10.1073/pnas.1416714111
77. Chiavaroli A, Recinella L, Ferrante C, et al. Crocus sativus, Serenoa repens and Pinus massoniana extracts modulate inflammatory response in isolated rat prostate challenged with LPS. J Biol Regul Homeost Agents. 2017;31(3):531–41
78. Li J, Zhai Y, Ao L, Hui H, Fullerton DA, Dinarello CA, Meng X. Interleukin-37 suppresses the inflammatory response to protect cardiac function in old endotoxemic mice. Cytokine. 2017;95:55–63. 10.1016/j.cyto.2017.02.008
79. Chen WY, Li LC, Yang JL. Emerging roles of IL-33/ST2 axis in renal diseases. Int J Mol Sci. 2017;18(4). 10.3390/ijms18040783
80. Scarpioni R, Ricardi M, Albertazzi V. Secondary amyloidosis in autoinflammatory diseases and the role of inflammation in renal damage. World J Nephrol. 2016;5(1):66–75. 10.5527/wjn.v5.i1.66
81. Nickeleit V, Andreoni K. Inflammatory cells in renal allografts. Front Biosci. 2008;13:6202–13 (review)
82. Hügle T. Beyond allergy: the role of mast cells in fibrosis. Swiss Med Wkly. 2014;144:w13999. 10.4414/smw.2014.13999 (eCollection 2014)
83. Conti P, Carinci F, Caraffa A, Ronconi G, Lessiani G, Theoharides TC. Link between mast cells and bacteria: antimicrobial defense, function and regulation by cytokines. Med Hypotheses. 2017;106:10–4. 10.1016/j.mehy.2017.06.018