The Ectoenzyme E-NPP3 Negatively Regulates ATP-Dependent Chronic Allergic Responses by Basophils and Mast Cells

Immunity

Volumn 42, Issue 2, 2015, Pages 279-293

  Tsai, Shih Han ^a,b   Kinoshita, Makoto ^a,b   Kusu, Takashi ^a,b   Kayama, Hisako ^a,b   Okumura, Ryu ^a,b   Ikeda, Kayo ^a,b   Shimada, Yosuke ^a,b   Takeda, Akira ^a   Yoshikawa, Soichiro ^c   Obata Ninomiya, Kazushige ^c   Kurashima, Yosuke ^b,d   Sato, Shintaro ^b,d   Umemoto, Eiji ^a,b   Kiyono, Hiroshi ^b,d   Karasuyama, Hajime ^b,c   Takeda, Kiyoshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ECTO NUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE 3; FC EPSILON RECEPTOR I; FC RECEPTOR; IMMUNOGLOBULIN E; INTERLEUKIN 4; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; NUCLEOTIDE PYROPHOSPHATASE; PHOSPHODIESTERASE III; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG; E-NPP3 PROTEIN, MOUSE; IMMUNOGLOBULIN E RECEPTOR; INORGANIC PYROPHOSPHATASE; NITROBENZENE DERIVATIVE; P2RX7 PROTEIN, MOUSE; PHOSPHODIESTERASE; SMALL INTERFERING RNA;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; AUTOCRINE EFFECT; BASOPHIL; BONE MARROW CELL; CELL ACTIVATION; CHRONIC DISEASE; CHRONIC INFLAMMATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME REPRESSION; EOSINOPHIL; EOSINOPHIL COUNT; GENE TARGETING; HEMATOPOIETIC CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMEDIATE TYPE HYPERSENSITIVITY; IMMUNOGLOBULIN BLOOD LEVEL; LYMPHOCYTE COUNT; MAST CELL; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PASSIVE SKIN ANAPHYLAXIS; PRIORITY JOURNAL; SKIN ALLERGY; TH2 CELL; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CONTACT DERMATITIS; CYTOLOGY; DIARRHEA; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RNA INTERFERENCE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTHMA; BASOPHILS; DERMATITIS, CONTACT; DIARRHEA; IMMUNOGLOBULIN E; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PASSIVE CUTANEOUS ANAPHYLAXIS; PHOSPHORIC DIESTER HYDROLASES; PYROPHOSPHATASES; RECEPTORS, IGE; RECEPTORS, PURINERGIC P2X7; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRINITROBENZENES;

EID: 84923040707     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.01.015     Document Type: Article

References (42)

1. Abraham S.N., St John A.L. Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 2010, 10:440-452.
2. Bischoff S.C., Sellge G., Lorentz A., Sebald W., Raab R., Manns M.P. IL-4 enhances proliferation and mediator release in mature human mast cells. Proc. Natl. Acad. Sci. USA 1999, 96:8080-8085.
3. Bollen M., Gijsbers R., Ceulemans H., Stalmans W., Stefan C. Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit. Rev. Biochem. Mol. Biol. 2000, 35:393-432.
4. Brandt E.B., Strait R.T., Hershko D., Wang Q., Muntel E.E., Scribner T.A., Zimmermann N., Finkelman F.D., Rothenberg M.E. Mast cells are required for experimental oral allergen-induced diarrhea. J.Clin. Invest. 2003, 112:1666-1677.
5. Bühring H.J., Seiffert M., Giesert C., Marxer A., Kanz L., Valent P., Sano K. The basophil activation marker defined by antibody 97A6 is identical to the ectonucleotide pyrophosphatase/phosphodiesterase 3. Blood 2001, 97:3303-3305.
6. Bühring H.J., 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.
7. Corriden R., Insel P.A. Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci. Signal. 2010, 3:re1.
8. Deaglio S., Dwyer K.M., Gao W., Friedman D., Usheva A., Erat A., Chen J.F., Enjyoji K., Linden J., Oukka M., et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory Tcells mediates immune suppression. J.Exp. Med. 2007, 204:1257-1265.
9. Denlinger L.C., Manthei D.M., Seibold M.A., Ahn K., Bleecker E., Boushey H.A., Calhoun W.J., Castro M., Chinchili V.M., Fahy J.V., et al. P2X7-regulated protection from exacerbations and loss of control is independent of asthma maintenance therapy. Am. J. Respir. Crit. Care Med. 2013, 187:28-33. NHLBI Asthma Clinical Research Network Investigators.
10. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., Park D., Woodson R.I., Ostankovich M., Sharma P., et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
11. Friedman D.J., Künzli B.M., A-Rahim Y.I., Sevigny J., Berberat P.O., Enjyoji K., Csizmadia E., Friess H., Robson S.C. From the Cover: CD39 deletion exacerbates experimental murine colitis and human polymorphisms increase susceptibility to inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 2009, 106:16788-16793.
12. Ghannadan M., Hauswirth A.W., Schernthaner G.H., Müller M.R., Klepetko W., Schatzl G., Sperr W.R., Bühring H.J., Valent P. Detection of novel CD antigens on the surface of human mast cells and basophils. Int. Arch. Allergy Immunol. 2002, 127:299-307.
13. Gould H.J., Sutton B.J. IgE in allergy and asthma today. Nat. Rev. Immunol. 2008, 8:205-217.
14. Hessle L., Johnson K.A., Anderson H.C., Narisawa S., Sali A., Goding J.W., Terkeltaub R., Millan J.L. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc. Natl. Acad. Sci. USA 2002, 99:9445-9449.
15. Idzko M., Hammad H., van Nimwegen M., Kool M., Willart M.A., Muskens F., Hoogsteden H.C., Luttmann W., Ferrari D., Di Virgilio F., et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat. Med. 2007, 13:913-919.
16. Idzko M., Ferrari D., Eltzschig H.K. Nucleotide signalling during inflammation. Nature 2014, 509:310-317.
17. Junger W.G. Immune cell regulation by autocrine purinergic signalling. Nat. Rev. Immunol. 2011, 11:201-212.
18. Kanda H., Newton R., Klein R., Morita Y., Gunn M.D., Rosen S.D. Autotaxin, an ectoenzyme that produces lysophosphatidic acid, promotes the entry of lymphocytes into secondary lymphoid organs. Nat. Immunol. 2008, 9:415-423.
19. Karasuyama H., Mukai K., Tsujimura Y., Obata K. Newly discovered roles for basophils: a neglected minority gains new respect. Nat. Rev. Immunol. 2009, 9:9-13.
20. Karasuyama H., Mukai K., Obata K., Tsujimura Y., Wada T. Nonredundant roles of basophils in immunity. Annu. Rev. Immunol. 2011, 29:45-69.
21. Kawamura T., Ogawa Y., Nakamura Y., Nakamizo S., Ohta Y., Nakano H., Kabashima K., Katayama I., Koizumi S., Kodama T., et al. Severe dermatitis with loss of epidermal Langerhans cells in human and mouse zinc deficiency. J.Clin. Invest. 2012, 122:722-732.
22. Kurashima Y., Amiya T., Nochi T., Fujisawa K., Haraguchi T., Iba H., Tsutsui H., Sato S., Nakajima S., Iijima H., et al. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat. Commun. 2012, 3:1034.
23. Kurashima Y., Amiya T., Fujisawa K., Shibata N., Suzuki Y., Kogure Y., Hashimoto E., Otsuka A., Kabashima K., Sato S., et al. The enzyme Cyp26b1 mediates inhibition of mast cell activation by fibroblasts to maintain skin-barrier homeostasis. Immunity 2014, 40:530-541.
24. Manthei D.M., Jackson D.J., Evans M.D., Gangnon R.E., Tisler C.J., Gern J.E., Lemanske R.F., Denlinger L.C. Protection from asthma in a high-risk birth cohort by attenuated P2X(7) function. J.Allergy Clin. Immunol. 2012, 130:496-502.
25. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., Lee W.P., Weinrauch Y., Monack D.M., Dixit V.M. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006, 440:228-232.
26. Mizumoto N., Kumamoto T., Robson S.C., Sévigny J., Matsue H., Enjyoji K., Takashima A. CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat. Med. 2002, 8:358-365.
27. Mukai K., Matsuoka K., Taya C., Suzuki H., Yokozeki H., Nishioka K., Hirokawa K., Etori M., Yamashita M., Kubota T., et al. Basophils play a critical role in the development of IgE-mediated chronic allergic inflammation independently of Tcells and mast cells. Immunity 2005, 23:191-202.
28. Müller T., Vieira R.P., Grimm M., Dürk T., Cicko S., Zeiser R., Jakob T., Martin S.F., Blumenthal B., Sorichter S., et al. A potential role for P2X7R in allergic airway inflammation in mice and humans. Am. J. Respir. Cell Mol. Biol. 2011, 44:456-464.
29. Obata K., Mukai K., Tsujimura Y., Ishiwata K., Kawano Y., Minegishi Y., Watanabe N., Karasuyama H. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 2007, 110:913-920.
30. Okawa A., Nakamura I., Goto S., Moriya H., Nakamura Y., Ikegawa S. Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat. Genet. 1998, 19:271-273.
31. Schetinger M.R., Morsch V.M., Bonan C.D., Wyse A.T. NTPDase and 5'-nucleotidase activities in physiological and disease conditions: new perspectives for human health. Biofactors 2007, 31:77-98.
32. Shiratori M., Tozaki-Saitoh H., Yoshitake M., Tsuda M., Inoue K. P2X7 receptor activation induces CXCL2 production in microglia through NFAT and PKC/MAPK pathways. J.Neurochem. 2010, 114:810-819.
33. Stefan C., Jansen S., Bollen M. NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem. Sci. 2005, 30:542-550.
34. Sudo N., Tanaka K., Koga Y., Okumura Y., Kubo C., Nomoto K. Extracellular ATP activates mast cells via a mechanism that is different from the activation induced by the cross-linking of Fc receptors. J.Immunol. 1996, 156:3970-3979.
35. Swanson K.D., Reigh C., Landreth G.E. ATP-stimulated activation of the mitogen-activated protein kinases through ionotrophic P2X2 purinoreceptors in PC12 cells. Difference in purinoreceptor sensitivity in two PC12 cell lines. J.Biol. Chem. 1998, 273:19965-19971.
36. Umemoto E., Hayasaka H., Bai Z., Cai L., Yonekura S., Peng X., Takeda A., Tohya K., Miyasaka M. Novel regulators of lymphocyte trafficking across high endothelial venules. Crit. Rev. Immunol. 2011, 31:147-169.
37. van Meeteren L.A., Ruurs P., Stortelers C., Bouwman P., van Rooijen M.A., Pradère J.P., Pettit T.R., Wakelam M.J., Saulnier-Blache J.S., Mummery C.L., et al. Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol. 2006, 26:5015-5022.
38. Voehringer D. Protective and pathological roles of mast cells and basophils. Nat. Rev. Immunol. 2013, 13:362-375.
39. Wakahara K., Van V.Q., Baba N., Bégin P., Rubio M., Delespesse G., Sarfati M. Basophils are recruited to inflamed lungs and exacerbate memory Th2 responses in mice and humans. Allergy 2013, 68:180-189.
40. Wang L., Sikora J., Hu L., Shen X., Grygorczyk R., Schwarz W. ATP release from mast cells by physical stimulation: a putative early step in activation of acupuncture points. Evid. Based Complement. Alternat. Med. 2013, 2013:350949.
41. Weber F.C., Esser P.R., Müller T., Ganesan J., Pellegatti P., Simon M.M., Zeiser R., Idzko M., Jakob T., Martin S.F. Lack of the purinergic receptor P2X(7) results in resistance to contact hypersensitivity. J.Exp. Med. 2010, 207:2609-2619.
42. Yegutkin G.G. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 2008, 1783:673-694.