The enigmatic role of mast cells in dominant tolerance

Current Opinion in Organ Transplantation

Volumn 14, Issue 4, 2009, Pages 332-337

  De Vries, Victor C ^a   Pino Lagos, Karina ^a   Elgueta, Raul ^a   Noelle, Randolph J ^a  

^a NORRIS COTTON CANCER CENTER   (United States)

Author keywords

Dominant tolerance; Mast cells; Regulatory T cells

Indexed keywords

CD134 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 4; OX40 LIGAND; PROTEINASE; TRANSFORMING GROWTH FACTOR BETA;

CD4+ T LYMPHOCYTE; CYTOKINE PRODUCTION; IMMUNOLOGICAL TOLERANCE; INFECTION; INFLAMMATION; MAST CELL; MAST CELL DEGRANULATION; MEDIATOR RELEASE; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; TRANSPLANTATION TOLERANCE;

ANIMALS; CELL COMMUNICATION; CELL DEGRANULATION; GRAFT SURVIVAL; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-10; MAST CELLS; ORGAN TRANSPLANTATION; OX40 LIGAND; RECEPTORS, OX40; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HOMOLOGOUS;

EID: 68849093868     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0b013e32832ce87a     Document Type: Review

References (73)

1. Graca L, Chen TC, Le Moine A, et al. Dominant tolerance: activation thresholds for peripheral generation of regulatory T cells. Trends Immunol 2005; 26:130-135. (Pubitemid 40312519)
2. + natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212:8-27.
3. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003; 3:199-210.
4. Boerma M, Fiser WP, Hoyt G, et al. Influence of mast cells on outcome after heterotopic cardiac transplantation in rats. Transpl Int 2007; 20:256-265. (Pubitemid 46246537)
5. Lu LF, Lind EF, Gondek DC, et al. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 2006; 442:997-1002.
6. Gillespie SR, DeMartino RR, Zhu J, et al. IL-10 inhibits Fc epsilon RI expression in mouse mast cells. J Immunol 2004; 172:3181-3188. (Pubitemid 38263709)
7. GomezG, Ramirez CD, Rivera J, et al. TGF-beta 1 inhibits mast cell Fc epsilon RI expression. J Immunol 2005; 174:5987-5993. (Pubitemid 40663785)
8. + regulatory T cells suppress mast cell degranulation and allergic responses through OX40-OX40L interaction. Immunity 2008; 29:771-781. The first study to define the molecules involved in the contact-dependent interaction between Tregs and mast cell. The OX40-OX40L interaction resulted in increased cAMP levels and decreased calcium flux in the mast cells, thereby inhibiting degranulation. This interaction might be impaired in allergies, but on the contrary could play an important role in establishment of tolerance towards an allogeneic transplant.
9. Grimbaldeston MA, Nakae S, Kalesnikoff J, et al. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol 2007; 8:1095-1104. (Pubitemid 47423757)
10. Kashyap M, Bailey DP, Gomez G, et al. TGF-beta1 inhibits late-stage mast cell maturation. Exp Hematol 2005; 33:1281-1291.
11. Kashyap M, Thornton AM, Norton SK, et al. Cutting edge: CD4 T cell-mast cell interactions alter IgE receptor expression and signaling. J Immunol 2008; 180:2039-2043. The authors show a mutual interaction between mast cells and T cells. Mast cells actively recruit both Tregs and Teffs, whereas the Tregs lead to reduced FceRI expression on the mast cells in a contact-dependent manner. Both T-cell subsets were able to induce IgE-mediated cytokine production in the mast cells, thereby showing that T cells can directly impact mast cell responses.
12. Kennedy Norton S, Barnstein B, Brenzovich J, et al. IL-10 suppresses mast cell IgE receptor expression and signaling in vitro and in vivo. J Immunol 2008; 180:2848-2854.
13. + regulatory T cells. Nat Immunol 2003; 4:330-336.
14. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061. (Pubitemid 36222930)
15. + T regulatory cells. Nat Immunol 2003; 4:337-342.
16. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005; 6:331-337.
17. + regulatory t cells for immunologic selftolerance and negative control of immune responses. Annu Rev Immunol 2004; 22:531-562.
18. Shevach EM. Regulatory T cells in autoimmunity. Annu Rev Immunol 2000; 18:423-449.
19. Ehrlich P. Contributions to the theory and practice of histological staining. Leipzig: Leipzig University; 1878.
20. Daeron M. Fc receptor biology. Annu Rev Immunol 1997; 15:203-234.
21. Kinet JP. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu Rev Immunol 1999; 17:931-972. (Pubitemid 29241144)
22. Huang C, Wong GW, Ghildyal N, et al. The tryptase, mouse mast cell protease 7, exhibits anticoagulant activity in vivo and in vitro due to its ability to degrade fibrinogen in the presence of the diverse array of protease inhibitors in plasma. J Biol Chem 1997; 272:31885-31893. (Pubitemid 28013341)
23. Kanwar S, Kubes P. Ischemia/reperfusion-induced granulocyte influx is a multistep process mediated by mast cells. Microcirculation 1994; 1:175-182.
24. Kauhanen P, Kovanen PT, Reunala T, Lassila R. Effects of skin mast cells on bleeding time and coagulation activation at the site of platelet plug formation. Thromb Haemost 1998; 79:843-847. (Pubitemid 28163865)
25. Mekori YA, Galli SJ. [125I]fibrin deposition occurs at both early and late intervals of IgE-dependent or contact sensitivity reactions elicited in mouse skin. Mast cell-dependent augmentation of fibrin deposition at early intervals in combined IgE-dependent and contact sensitivity reactions. J Immunol 1990; 145:3719-3727.
26. Thomas VA, Wheeless CJ, Stack MS, Johnson DA. Human mast cell tryptase fibrinogenolysis: kinetics, anticoagulation mechanism, and cell adhesion disruption. Biochemistry 1998; 37:2291-2298.
27. Jahanyar J, Koerner MM, Loebe M, et al. The role of mast cells after solid organ transplantation. Transplantation 2008; 85:1365-1371.
28. + T-cell subsets in determining transplantation rejection or tolerance. Immunol Rev 2001; 182:164-179.
29. Godfrey VL, Wilkinson JE, Russell LB. X-linked lymphoreticular disease in the scurfy (sf) mutant mouse. Am J Pathol 1991; 138:1379-1387.
30. Wildin RS, Smyk-Pearson S, Filipovich AH. Clinical and molecular features of the immunodysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. J Med Genet 2002; 39:537-545. (Pubitemid 34864555)
31. Sakaguchi S, Sakaguchi N, Asano M, et al. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155:1151-1164.
32. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998; 188:287-296.
33. Grossman WJ, Verbsky JW, Tollefsen BL, et al. Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 2004; 104:2840-2848. (Pubitemid 39434970)
34. + regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol 2005; 174:1783-1786.
35. Groux H, O'Garra A, Bigler M, et al. A CD4+ T-cell subset inhibits antigenspecific T-cell responses and prevents colitis. Nature 1997; 389:737-742. (Pubitemid 27458961)
36. + CD25- precursors. Am J Transplant 2004; 4:1614-1627.
37. Benson MJ, Pino-Lagos K, Rosemblatt M, Noelle RJ. All-trans retinoic acid mediates enhanced Treg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 2007; 204:1765-1774. (Pubitemid 47236315)
38. Davies JD, Leong LY, Mellor A, et al. T cell suppression in transplantation tolerance through linked recognition. J Immunol 1996; 156:3602-3607. (Pubitemid 26137645)
39. Wise MP, Bemelman F, Cobbold SP, Waldmann H. Linked suppression of skin graft rejection can operate through indirect recognition. J Immunol 1998; 161:5813-5816.
40. Qin SX, Wise M, Cobbold SP, et al. Induction of tolerance in peripheral T cells with monoclonal antibodies. Eur J Immunol 1990; 20:2737-2745.
41. Qin S, Cobbold SP, Pope H, et al. 'Infectious' transplantation tolerance. Science 1993; 259:974-977.
42. Onodera K, Lehmann M, Akalin E, et al. Induction of 'infectious' tolerance to MHC-incompatible cardiac allografts in CD4 monoclonal antibody-treated sensitized rat recipients. J Immunol 1996; 157:1944-1950.
43. Colvin RB, Dvorak HF. Letter: basophils and mast cells in renal allograft rejection. Lancet 1974; 1:212-214.
44. Yousem SA. The potential role of mast cells in lung allograft rejection. Hum Pathol 1997; 28:179-182. (Pubitemid 27069183)
45. Seung LM, Lorincz AL. Incidence of acute renal transplant rejection in atopic individuals. Arch Dermatol 1994; 130:584-588. (Pubitemid 24150936)
46. Ryan JJ, DeSimone S, Klisch G, et al. IL-4 inhibits mouse mast cell Fc epsilonRI expression through a STAT6-dependent mechanism. J Immunol 1998; 161:6915-6923. (Pubitemid 28562238)
47. Barnstein BO, Li G, Wang Z, et al. Stat5 expression is required for IgEmediated mast cell function. J Immunol 2006; 177:3421-3426. (Pubitemid 44277863)
48. Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nat Rev Immunol 2006; 6:218-230. (Pubitemid 43290991)
49. Rivera J,Gilfillan AM. Molecular regulation of mast cell activation. J Allergy Clin Immunol 2006; 117:1214-1225. (Pubitemid 43795719)
50. Zhao W, Gomez G, Yu SH, et al. TGF-beta1 attenuates mediator release and de novo kit expression by human skin mast cells through a Smad-dependent pathway. J Immunol 2008; 181:7263-7272.
51. +CD25 high T-regulatory cells in allergic asthma is subjected to TNFalpha modulation. Allergy 2008; 63:67-74.
52. + regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 2004; 363:608-615.
53. + T cells and interleukin-10 in birch pollen-allergic patients and nonallergic controls. Clin Exp Allergy 2007; 37:1127-1136.
54. Depinay N, Hacini F, Beghdadi W, et al. Mast cell-dependent down-regulation of antigen-specific immune responses by mosquito bites. J Immunol 2006; 176:4141-4146. (Pubitemid 44264393)
55. Vocks E, Stander K, Rakoski J, Ring J. Suppression of immediate-type hypersensitivity elicitation in the skin prick test by ultraviolet B irradiation. Photodermatol Photoimmunol Photomed 1999; 15:236-240.
56. Hart PH, Grimbaldeston MA, Swift GJ, et al. Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J Exp Med 1998; 187:2045-2053.
57. Fujita T, Kambe N, Uchiyama T, Hori T. Type I interferons attenuate T cell activating functions of human mast cells by decreasing TNF-alpha production and OX40 ligand expression while increasing IL-10 production. J Clin Immunol 2006; 26:512-518. (Pubitemid 44764261)
58. Halak BK, Maguire HC Jr, Lattime EC. Tumor-induced interleukin-10 inhibits type 1 immune responses directed at a tumor antigen as well as a nontumor antigen present at the tumor site. Cancer Res 1999; 59:911-917.
59. Wasiuk A, de Vries VC, Hartmann K, et al. Mast cells as regulators of adaptive immunity to tumours. Clin Exp Immunol 2009; 155:140-146.
60. Galinsky DS, Nechushtan H. Mast cells and cancer: no longer just basic science. Crit Rev Oncol Hematol 2008; 68:115-130.
61. Barr ML, Carey JN, Nishanian GP, et al. Addition of a mast cell stabilizing compound to organ preservation solutions decreases lung reperfusion injury. J Thorac Cardiovasc Surg 1998; 115:631-636; discussion 636-637.
62. Facoetti A, Fallarini S, Miserere S, et al. Histochemical study of cardiac mast cells degranulation and collagen deposition: interaction with the catecholaminergic system in the rat. Eur J Histochem 2006; 50:133-140.
63. Li QY, Raza-Ahmad A, MacAulay MA, et al. The relationship of mast cells and their secreted products to the volume of fibrosis in posttransplant hearts. Transplantation 1992; 53:1047-1051.
64. Zweifel M, Hirsiger H, Matozan K, et al. Mast cells in ongoing acute rejection: increase in number and expression of a different phenotype in rat heart transplants. Transplantation 2002; 73:1707-1716. (Pubitemid 34655244)
65. Aune TM, Golden HW, McGrath KM. Inhibitors of serotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo. J Immunol 1994; 153:489-498.
66. + T cells in vitro. J Immunol 1996; 156:310-315.
67. Leon-Ponte M, Ahern GP, O'Connell PJ. Serotonin provides an accessory signal to enhance T-cell activation by signaling through the 5-HT7 receptor. Blood 2007; 109:3139-3146. (Pubitemid 46572497)
68. Nakae S, Suto H, Iikura M, et al. Mast cells enhance T cell activation: importance of mast cell costimulatory molecules and secreted TNF. J Immunol 2006; 176:2238-2248. (Pubitemid 43201671)
69. Nakano N, Nishiyama C, Yagita H, et al. Notch signaling confers antigenpresenting cell functions on mast cells. J Allergy Clin Immunol 2009; 123:74-81. The authors defined a pathway that makes mast cells bona fide antigen-presenting cells. Notch signaling induced upregulation of both MHC-II and OX40L on the mast cells. Coculture of T cells with these mast cells resulted in proliferation and skewing to a Th2 phenotype.
70. Singh N. Novel immune regulatory pathways and their role in immune reconstitution syndrome in organ transplant recipients with invasive mycoses. Eur J Clin Microbiol Infect Dis 2008; 27:403-408. (Pubitemid 351713067)
71. Barczyk M, Mysliwiec M, Kalinowski M, et al. Mast cells tryptase in patients after renal transplantation. Transplant Proc 2008; 40:3437-3439.
72. Musch W, Wege AK, Mannel DN, Hehlgans T. Generation and characterization of alpha-chymase-Cre transgenic mice. Genesis 2008; 46:163-166. Both Musch et al. [72•] and Scholten et al. [73•] developed mast cell-specific creexpressing mice. Mast cell-deficient mice, such as theWv/Wv andWsh/Wsh, which are based on mutation in the cKit gene have many known and unknown variables that could alter the results, Therefore, these mice will prove to be invaluable to specifically address the role of mast cells and their mediators in inflammation and dominant tolerance. (Pubitemid 351554745)
73. •] developed mast cell-specific Creexpressing mice. As reconstitution of mast cell deficient mice has many known and unknown variables that could alter the results, these mice will prove to be invaluable to specifically address the role of mast cells in inflammation and dominant tolerance.