Basophils Trigger Fibroblast Activation in Cardiac Allograft Fibrosis Development

American Journal of Transplantation

Volumn 16, Issue 9, 2016, Pages 2574-2588

  Schiechl, G ^a   Hermann, F J ^a   Rodriguez Gomez, M ^a   Kutzi, S ^a   Schmidbauer, K ^a   Talke, Y ^a   Neumayer, S ^a   Goebel, N ^a   Renner, K ^a   Bruhl H ^a   Karasuyama, H ^b   Obata Ninomiya, K ^b   Utpatel, K ^a   Evert, M ^a   Hirt, S W ^a   Geissler, E K ^a   Fichtner Feigl, S ^a,c   Mack, M ^a,c  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

basic (laboratory) research science; fibrosis; heart (allograft) function dysfunction; heart transplantation cardiology; immune regulation; immunobiology; immunosuppression immune modulation; rejection: chronic; signaling signaling pathways

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; ENPP3 PROTEIN; FIBRONECTIN; IMMUNOGLOBULIN E RECEPTOR; INTERLEUKIN 13; INTERLEUKIN 3; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; MACROPHAGE DERIVED CHEMOKINE; PROTEIN; SCLEROPROTEIN; THYMIC STROMAL LYMPHOPOIETIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

ACUTE GRAFT REJECTION; ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOPHIL; CARDIAC ALLOGRAFT FIBROSIS; CARDIAC GRAFT REJECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL INFILTRATION; CELL SUSPENSION; FEMALE; FIBROSING ALVEOLITIS; FLOW CYTOMETRY; GENE EXPRESSION; GRAFT RECIPIENT; HEART FIBROBLAST; HEART GRAFT; HEART MUSCLE BIOPSY; HEART MUSCLE FIBROSIS; HEART TRANSPLANTATION; HETEROTOPIC TRANSPLANTATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; ISOGRAFT; LEUKOCYTE; MAST CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN CELL; T CELL DEPLETION; VASCULAR SMOOTH MUSCLE CELL;

EID: 84984628688     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13764     Document Type: Article

References (68)

1. Mitchell RN. Graft vascular disease: Immune response meets the vessel wall. Annu Rev Pathol 2009; 4: 19–47.
2. Weber KT, Sun Y, Tyagi SC, Cleutjens JP. Collagen network of the myocardium: Function, structural remodeling and regulatory mechanisms. J Mol Cell Cardiol 1994; 26: 279–292.
3. Booth AJ, Bishop DK. TGF-beta, IL-6, IL-17 and CTGF direct multiple pathologies of chronic cardiac allograft rejection. Immunotherapy 2010; 2: 511–520.
4. Duffield JS, Lupher M, Thannickal VJ, Wynn TA. Host responses in tissue repair and fibrosis. Annu Rev Pathol 2013; 8: 241–276.
5. Kong P, Christia P, Frangogiannis NG. The pathogenesis of cardiac fibrosis. Cell Mol Life Sci 2014; 71: 549–574.
6. Reich B, Schmidbauer K, Rodriguez Gomez M, et al. Fibrocytes develop outside the kidney but contribute to renal fibrosis in a mouse model. Kidney Int 2013; 84: 78–89.
7. LeBleu VS, Taduri G, O'Connell J, et al. Origin and function of myofibroblasts in kidney fibrosis. Nat Med 2013; 19: 1047–1053.
8. Zeisberg EM, Tarnavski O, Zeisberg M, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007; 13: 952–961.
9. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008; 214: 199–210.
10. Hinz B, Phan SH, Thannickal VJ, et al. Recent developments in myofibroblast biology: Paradigms for connective tissue remodeling. Am J Pathol 2012; 180: 1340–1355.
11. Tay SS, Plain KM, Bishop GA. Role of IL-4 and Th2 responses in allograft rejection and tolerance. Curr Opin Organ Transplant 2009; 14: 16–22.
12. Ma B, Blackburn MR, Lee CG, et al. Adenosine metabolism and murine strain-specific IL-4-induced inflammation, emphysema, and fibrosis. J Clin Invest 2006; 116: 1274–1283.
13. Kanellakis P, Ditiatkovski M, Kostolias G, Bobik A. A pro-fibrotic role for interleukin-4 in cardiac pressure overload. Cardiovasc Res 2012; 95: 77–85.
14. Atamas SP, Luzina IG, Dai H, Wilt SG, White B. Synergy between CD40 ligation and IL-4 on fibroblast proliferation involves IL-4 receptor signaling. J Immunol 2002; 168: 1139–1145.
15. Postlethwaite AE, Holness MA, Katai H, Raghow R. Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J Clin Invest 1992; 90: 1479–1485.
16. Todd NW, Luzina IG, Atamas SP. Molecular and cellular mechanisms of pulmonary fibrosis. Fibrogenesis Tissue Repair 2012; 5: 11.
17. Buonocore S, Flamand V, Goldman M, Braun MY. Bone marrow-derived immature dendritic cells prime in vivo alloreactive T cells for interleukin-4-dependent rejection of major histocompatibility complex class II antigen-disparate cardiac allograft. Transplantation 2003; 75: 407–413.
18. Goldman M, Le Moine A, Braun M, Flamand V, Abramowicz D. A role for eosinophils in transplant rejection. Trends Immunol 2001; 22: 247–251.
19. Souza PP, Palmqvist P, Lundberg P, et al. Interleukin-4 and interleukin-13 inhibit the expression of leukemia inhibitory factor and interleukin-11 in fibroblasts. Mol Immunol 2012; 49: 601–610.
20. Sempowski GD, Beckmann MP, Derdak S, Phipps RP. Subsets of murine lung fibroblasts express membrane-bound and soluble IL-4 receptors. Role of IL-4 in enhancing fibroblast proliferation and collagen synthesis. J Immunol 1994; 152: 3606–3614.
21. Doucet C, Brouty-Boyé D, Pottin-Clémenceau C, Canonica GW, Jasmin C, Azzarone B. Interleukin (IL) 4 and IL-13 act on human lung fibroblasts. Implication in asthma. J Clin Invest 1998; 101: 2129–2139.
22. Schiechl G, Brunner SM, Kesselring R, et al. Inhibition of innate co-receptor TREM-1 signaling reduces CD4(+) T cell activation and prolongs cardiac allograft survival. Am J Transplant 2013; 13: 1168–1180.
23. Booth AJ, Wood SC, Cornett AM, et al. Recipient-derived EDA fibronectin promotes cardiac allograft fibrosis. J Pathol 2012; 226: 609–618.
24. Bishop DK, Li W, Chan SY, Ensley RD, Shelby J, Eichwald EJ. Helper T lymphocyte unresponsiveness to cardiac allografts following transient depletion of CD4-positive cells. Implications for cellular and humoral responses. Transplantation 1994; 58: 576–584.
25. Haynes R, Harden P, Judge P, et al. Alemtuzumab-based induction treatment versus basiliximab-based induction treatment in kidney transplantation (the 3C Study): A randomised trial. Lancet 2014; 384: 1684–1690.
26. Kwun J, Oh BC, Gibby AC, et al. Patterns of de novo allo B cells and antibody formation in chronic cardiac allograft rejection after alemtuzumab treatment. Am J Transplant 2012; 12: 2641–2651.
27. Niedermeier M, Reich B, Rodriguez Gomez M, et al. CD4+ T cells control the differentiation of Gr1+ monocytes into fibrocytes. Proc Natl Acad Sci U S A 2009; 106: 17892–17897.
28. Yoshimoto T, Yasuda K, Tanaka H, et al. Basophils contribute to T(H)2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol 2009; 10: 706–712.
29. Gomez MR, Talke Y, Hofmann C, et al. Basophils control T-cell responses and limit disease activity in experimental murine colitis. Mucosal Immunol 2014; 7: 188–199.
30. van Panhuys N, Prout M, Forbes E, Min B, Paul WE, Le Gros G. Basophils are the major producers of IL-4 during primary helminth infection. J Immunol 2011; 186: 2719–2728.
31. Nakashima C, Otsuka A, Kitoh A, et al. Basophils regulate the recruitment of eosinophils in a murine model of irritant contact dermatitis. J Allergy Clin Immunol 2014; 134: 100–107.
32. Hasegawa T, Visovatti SH, Hyman MC, Hayasaki T, Pinsky DJ. Heterotopic vascularized murine cardiac transplantation to study graft arteriopathy. Nat Protoc 2007; 2: 471–480.
33. Yamaguchi M, Hirai K, Komiya A, et al. Regulation of mouse mast cell surface Fc epsilon RI expression by dexamethasone. Int Immunol 2001; 13: 843–851.
34. Anyan WK, Seki T, Kumagai T, et al. Basophil depletion downregulates Schistosoma mansoni egg-induced granuloma formation. Parasitol Int 2013; 62: 508–513.
35. Brunner SM, Schiechl G, Falk W, Schlitt HJ, Geissler EK, Fichtner-Feigl S. Interleukin-33 prolongs allograft survival during chronic cardiac rejection. Transpl Int 2011; 24: 1027–1039.
36. McCulloch RS, Ashwell MS, O'Nan AT, Mente PL. Identification of stable normalization genes for quantitative real-time PCR in porcine articular cartilage. J Anim Sci Biotechnol 2012; 3: 36.
37. Franz M, Grün K, Richter P, et al. Extra cellular matrix remodelling after heterotopic rat heart transplantation: Gene expression profiling and involvement of ED-A+ fibronectin, alpha-smooth muscle actin and B+ tenascin-C in chronic cardiac allograft rejection. Histochem Cell Biol 2010; 134: 503–517.
38. Franz M, Berndt A, Grün K, et al. Expression of extra domain A containing fibronectin in chronic cardiac allograft rejection. J Heart Lung Transplant 2011; 30: 86–94.
39. Booth AJ, Grabauskiene S, Wood SC, Lu G, Burrell BE, Bishop DK. IL-6 promotes cardiac graft rejection mediated by CD4+ cells. J Immunol 2011; 187: 5764–5771.
40. Diaz JA, Booth AJ, Lu G, Wood SC, Pinsky DJ, Bishop DK. Critical role for IL-6 in hypertrophy and fibrosis in chronic cardiac allograft rejection. Am J Transplant 2009; 9: 1773–1783.
41. Pierce EM, Carpenter K, Jakubzick C, et al. Idiopathic pulmonary fibrosis fibroblasts migrate and proliferate to CC chemokine ligand 21. Eur Respir J 2007; 29: 1082–1093.
42. Piccotti JR, Li K, Chan SY, Eichwald EJ, Bishop DK. Cytokine regulation of chronic cardiac allograft rejection: Evidence against a role for Th1 in the disease process. Transplantation 1999; 67: 1548–1555.
43. Ugajin T, Kojima T, Mukai K, et al. Basophils preferentially express mouse Mast Cell Protease 11 among the mast cell tryptase family in contrast to mast cells. J Leukoc Biol 2009; 86: 1417–1425.
44. Liang G, Barker T, Xie Z, Charles N, Rivera J, Druey KM. Naive T cells sense the cysteine protease allergen papain through protease-activated receptor 2 and propel TH2 immunity. J Allergy Clin Immunol 2012; 129: 1377–1386.e1313.
45. Siracusa MC, Saenz SA, Wojno ED, et al. Thymic stromal lymphopoietin-mediated extramedullary hematopoiesis promotes allergic inflammation. Immunity 2013; 39: 1158–1170.
46. Voehringer D. Basophil modulation by cytokine instruction. Eur J Immunol 2012; 42: 2544–2550.
47. Denzel A, Maus UA, Rodriguez Gomez M, et al. Basophils enhance immunological memory responses. Nat Immunol 2008; 9: 733–742.
48. Mack M, Rosenkranz AR. Basophils and mast cells in renal injury. Kidney Int 2009; 76: 1142–1147.
49. Obata K, Mukai K, Tsujimura Y, et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 2007; 110: 913–920.
50. Valent P, Besemer J, Muhm M, Majdic O, Lechner K, Bettelheim P. Interleukin 3 activates human blood basophils via high-affinity binding sites. Proc Natl Acad Sci U S A 1989; 86: 5542–5546.
51. Ohmori K, Luo Y, Jia Y, et al. IL-3 induces basophil expansion in vivo by directing granulocyte-monocyte progenitors to differentiate into basophil lineage-restricted progenitors in the bone marrow and by increasing the number of basophil/mast cell progenitors in the spleen. J Immunol 2009; 182: 2835–2841.
52. Bühring HJ, Streble A, Valent P. The basophil-specific ectoenzyme E-NPP3 (CD203c) as a marker for cell activation and allergy diagnosis. Int Arch Allergy Immunol 2004; 133: 317–329.
53. Eisen HJ, Tuzcu EM, Dorent R, et al. Everolimus for the prevention of allograft rejection and vasculopathy in cardiac-transplant recipients. N Engl J Med 2003; 349: 847–858.
54. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002; 3: 349–363.
55. Wynn TA. Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 2004; 4: 583–594.
56. Wick G, Grundtman C, Mayerl C, et al. The immunology of fibrosis. Annu Rev Immunol 2013; 31: 107–135.
57. Wynn TA, Cheever AW, Jankovic D, et al. An IL-12-based vaccination method for preventing fibrosis induced by schistosome infection. Nature 1995; 376: 594–596.
58. Epelman S, Lavine KJ, Beaudin AE, et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014; 40: 91–104.
59. Jenkins SJ, Ruckerl D, Cook PC, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011; 332: 1284–1288.
60. Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 2006; 12: 99–106.
61. Lee CG, Homer RJ, Zhu Z, et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). J Exp Med 2001; 194: 809–821.
62. Seder RA, Paul WE, Dvorak AM, et al. Mouse splenic and bone marrow cell populations that express high-affinity Fc epsilon receptors and produce interleukin 4 are highly enriched in basophils. Proc Natl Acad Sci U S A 1991; 88: 2835–2839.
63. Min B, Prout M, Hu-Li J, et al. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 2004; 200: 507–517.
64. Obata-Ninomiya K, Ishiwata K, Tsutsui H, et al. The skin is an important bulwark of acquired immunity against intestinal helminths. J Exp Med 2013; 210: 2583–2595.
65. Mack M, Yanagita M. Origin of myofibroblasts and cellular events triggering fibrosis. Kidney Int 2015; 87: 297–307.
66. Kendall RT, Feghali-Bostwick CA. Fibroblasts in fibrosis: Novel roles and mediators. Front Pharmacol 2014; 5: 123.
67. Lin SL, Kisseleva T, Brenner DA, Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 2008; 173: 1617–1627.
68. Shinde AV, Frangogiannis NG. Fibroblasts in myocardial infarction: A role in inflammation and repair. J Mol Cell Cardiol 2014; 70: 74–82.