Critical Role for Mast Cells in Interleukin-1β-Driven Skin Inflammation Associated with an Activating Mutation in the Nlrp3 Protein

Immunity

Volumn 37, Issue 1, 2012, Pages 85-95

  Nakamura, Yuumi ^a   Franchi, Luigi ^a   Kambe, Naotomo ^b   Meng, Guangxun ^c   Strober, Warren ^d   Núñez, Gabriel ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; POLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; FEMALE; GENE MUTATION; HISTOPATHOLOGY; MAST CELL; MICROFLORA; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN INFLAMMATION;

ANIMALS; CARRIER PROTEINS; CASPASE 1; DERMATITIS; FEMALE; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; SKIN DISEASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84864313288     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.04.013     Document Type: Article

References (46)

1. Agostini L., Martinon F., Burns K., McDermott M.F., Hawkins P.N., Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 2004, 20:319-325.
2. Aksentijevich I., Nowak M., Mallah M., Chae J.J., Watford W.T., Hofmann S.R., Stein L., Russo R., Goldsmith D., Dent P., et al. De novo CIAS1 mutations, cytokine activation, and evidence for genetic heterogeneity in patients with neonatal-onset multisystem inflammatory disease (NOMID): a new member of the expanding family of pyrin-associated autoinflammatory diseases. Arthritis Rheum. 2002, 46:3340-3348.
3. Aksentijevich I., D Putnam C., Remmers E.F., Mueller J.L., Le J., Kolodner R.D., Moak Z., Chuang M., Austin F., Goldbach-Mansky R., et al. The clinical continuum of cryopyrinopathies: novel CIAS1 mutations in North American patients and a new cryopyrin model. Arthritis Rheum. 2007, 56:1273-1285.
4. Arend W.P., Palmer G., Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 2008, 223:20-38.
5. Bauernfeind F.G., Horvath G., Stutz A., Alnemri E.S., MacDonald K., Speert D., Fernandes-Alnemri T., Wu J., Monks B.G., Fitzgerald K.A., et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 2009, 183:787-791.
6. Brydges S.D., Mueller J.L., McGeough M.D., Pena C.A., Misaghi A., Gandhi C., Putnam C.D., Boyle D.L., Firestein G.S., Horner A.A., et al. Inflammasome-mediated disease animal models reveal roles for innate but not adaptive immunity. Immunity 2009, 30:875-887.
7. Chae J.J., Wood G., Masters S.L., Richard K., Park G., Smith B.J., Kastner D.L. The B30.2 domain of pyrin, the familial Mediterranean fever protein, interacts directly with caspase-1 to modulate IL-1beta production. Proc. Natl. Acad. Sci. USA 2006, 103:9982-9987.
8. Chae J.J., Cho Y.H., Lee G.S., Cheng J., Liu P.P., Feigenbaum L., Katz S.I., Kastner D.L. Gain-of-function Pyrin mutations induce NLRP3 protein-independent interleukin-1β activation and severe autoinflammation in mice. Immunity 2011, 34:755-768.
9. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
10. Dowds T.A., Masumoto J., Zhu L., Inohara N., Núñez G. Cryopyrin-induced interleukin 1beta secretion in monocytic cells: enhanced activity of disease-associated mutants and requirement for ASC. J. Biol. Chem. 2004, 279:21924-21928.
11. Ebrahimi-Fakhari D., Wahlster L., Mackensen F., Blank N. Clinical manifestations and longterm followup of a patient with CINCA/NOMID syndrome. J. Rheumatol. 2010, 37:2196-2197.
12. Echtenacher B., Männel D.N., Hültner L. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 1996, 381:75-77.
13. Federico G., Rigante D., Pugliese A.L., Ranno O., Catania S., Stabile A. Etanercept induces improvement of arthropathy in chronic infantile neurological cutaneous articular (CINCA) syndrome. Scand. J. Rheumatol. 2003, 32:312-314.
14. Franchi L., Kanneganti T.D., Dubyak G.R., Núñez G. Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 2007, 282:18810-18818.
15. Franchi L., Eigenbrod T., Muñoz-Planillo R., Nuñez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 2009, 10:241-247.
16. Franchi L., Eigenbrod T., Núñez G. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J. Immunol. 2009, 183:792-796.
17. Franchi L., Warner N., Viani K., Nuñez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 2009, 227:106-128.
18. Franchi L., Muñoz-Planillo R., Reimer T., Eigenbrod T., Núñez G. Inflammasomes as microbial sensors. Eur. J. Immunol. 2010, 40:611-615.
19. Fujisawa A., Kambe N., Saito M., Nishikomori R., Tanizaki H., Kanazawa N., Adachi S., Heike T., Sagara J., Suda T., et al. Disease-associated mutations in CIAS1 induce cathepsin B-dependent rapid cell death of human THP-1 monocytic cells. Blood 2007, 109:2903-2911.
20. Galli S.J., Grimbaldeston M., Tsai M. Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nat. Rev. Immunol. 2008, 8:478-486.
21. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 2009, 15:1170-1178.
22. Goldbach-Mansky R., Dailey N.J., Canna S.W., Gelabert A., Jones J., Rubin B.I., Kim H.J., Brewer C., Zalewski C., Wiggs E., et al. Neonatal-onset multisystem inflammatory disease responsive to interleukin-1beta inhibition. N. Engl. J. Med. 2006, 355:581-592.
23. Gordon J.R., Galli S.J. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature 1990, 346:274-276.
24. Grimbaldeston M.A., Chen C.C., Piliponsky A.M., Tsai M., Tam S.Y., Galli S.J. Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am. J. Pathol. 2005, 167:835-848.
25. Gunduz Z., Dursun I., Aróstegui J.I., Yagüe J., Dusunsel R., Poyrazoglu H.M., Gurgoze M.K., Yikilmaz A. A fatal Turkish case of CINCA-NOMID syndrome due to the novel Val-351-Leu CIAS1 gene mutation. Rheumatol. Int. 2008, 28:379-383.
26. Hasegawa M., Osaka T., Tawaratsumida K., Yamazaki T., Tada H., Chen G.Y., Tsuneda S., Núñez G., Inohara N. Transitions in oral and intestinal microflora composition and innate immune receptor-dependent stimulation during mouse development. Infect. Immun. 2010, 78:639-650.
27. Hoffman H.M., Mueller J.L., Broide D.H., Wanderer A.A., Kolodner R.D. Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nat. Genet. 2001, 29:301-305.
28. Hoffman H.M., Rosengren S., Boyle D.L., Cho J.Y., Nayar J., Mueller J.L., Anderson J.P., Wanderer A.A., Firestein G.S. Prevention of cold-associated acute inflammation in familial cold autoinflammatory syndrome by interleukin-1 receptor antagonist. Lancet 2004, 364:1779-1785.
29. Hoffman H.M., Throne M.L., Amar N.J., Sebai M., Kivitz A.J., Kavanaugh A., Weinstein S.P., Belomestnov P., Yancopoulos G.D., Stahl N., Mellis S.J. Efficacy and safety of rilonacept (interleukin-1 Trap) in patients with cryopyrin-associated periodic syndromes: results from two sequential placebo-controlled studies. Arthritis Rheum. 2008, 58:2443-2452.
30. Kallinich T., Hoffman H.M., Roth J., Keitzer R. The clinical course of a child with CINCA/NOMID syndrome improved during and after treatment with thalidomide. Scand. J. Rheumatol. 2005, 34:246-249.
31. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
32. Lachmann H.J., Kone-Paut I., Kuemmerle-Deschner J.B., Leslie K.S., Hachulla E., Quartier P., Gitton X., Widmer A., Patel N., Hawkins P.N. Use of canakinumab in the cryopyrin-associated periodic syndrome. N. Engl. J. Med. 2009, 360:2416-2425. Canakinumab in CAPS Study Group.
33. Matsubara T., Hasegawa M., Shiraishi M., Hoffman H.M., Ichiyama T., Tanaka T., Ueda H., Ishihara T., Furukawa S. A severe case of chronic infantile neurologic, cutaneous, articular syndrome treated with biologic agents. Arthritis Rheum. 2006, 54:2314-2320.
34. Matsuda H., Watanabe N., Geba G.P., Sperl J., Tsudzuki M., Hiroi J., Matsumoto M., Ushio H., Saito S., Askenase P.W., Ra C. Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int. Immunol. 1997, 9:461-466.
35. Maurer M., Lopez Kostka S., Siebenhaar F., Moelle K., Metz M., Knop J., von Stebut E. Skin mast cells control T cell-dependent host defense in Leishmania major infections. FASEB J. 2006, 20:2460-2467.
36. Meng G., Zhang F., Fuss I., Kitani A., Strober W. A mutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses. Immunity 2009, 30:860-874.
37. Mousli M., Bronner C., Landry Y., Bockaert J., Rouot B. Direct activation of GTP-binding regulatory proteins (G-proteins) by substance P and compound 48/80. FEBS Lett. 1990, 259:260-262.
38. Nakamura Y., Kambe N., Saito M., Nishikomori R., Kim Y.G., Murakami M., Núñez G., Matsue H. Mast cells mediate neutrophil recruitment and vascular leakage through the NLRP3 inflammasome in histamine-independent urticaria. J. Exp. Med. 2009, 206:1037-1046.
39. Neven B., Callebaut I., Prieur A.M., Feldmann J., Bodemer C., Lepore L., Derfalvi B., Benjaponpitak S., Vesely R., Sauvain M.J., et al. Molecular basis of the spectral expression of CIAS1 mutations associated with phagocytic cell-mediated autoinflammatory disorders CINCA/NOMID, MWS, and FCU. Blood 2004, 103:2809-2815.
40. Papin S., Cuenin S., Agostini L., Martinon F., Werner S., Beer H.D., Grütter C., Grütter M., Tschopp J. The SPRY domain of Pyrin, mutated in familial Mediterranean fever patients, interacts with inflammasome components and inhibits proIL-1beta processing. Cell Death Differ. 2007, 14:1457-1466.
41. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
42. Suto H., Nakae S., Kakurai M., Sedgwick J.D., Tsai M., Galli S.J. Mast cell-associated TNF promotes dendritic cell migration. J. Immunol. 2006, 176:4102-4112.
43. Theoharides T.C., Donelan J.M., Papadopoulou N., Cao J., Kempuraj D., Conti P. Mast cells as targets of corticotropin-releasing factor and related peptides. Trends Pharmacol. Sci. 2004, 25:563-568.
44. Willingham S.B., Bergstralh D.T., O'Connor W., Morrison A.C., Taxman D.J., Duncan J.A., Barnoy S., Venkatesan M.M., Flavell R.A., Deshmukh M., et al. Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2007, 2:147-159.
45. Yamada N., Matsushima H., Tagaya Y., Shimada S., Katz S.I. Generation of a large number of connective tissue type mast cells by culture of murine fetal skin cells. J. Invest. Dermatol. 2003, 121:1425-1432.
46. Zhu G.F., Chancellor-Freeland C., Berman A.S., Kage R., Leeman S.E., Beller D.I., Black P.H. Endogenous substance P mediates cold water stress-induced increase in interleukin-6 secretion from peritoneal macrophages. J. Neurosci. 1996, 16:3745-3752.