Platelets expressing IgG receptor FcγRIIA/CD32A determine the severity of experimental anaphylaxis

Science Immunology

Volumn 3, Issue 22, 2018, Pages

  Beutier, Héloïse ^a,b,c   Hechler, Béatrice ^d   Godon, Ophélie ^a,b   Wang, Yu ^a,b,e   Gillis, Caitlin M ^a,b,c   De Chaisemartin, Luc ^b,f   Gouel Chéron, Aurélie ^a,b,f   Magnenat, Stéphanie ^d   Macdonald, Lynn E ^g   Murphy, Andrew J ^g   Chollet Martin, Sylvie ^b,f   Longrois, Dan ^f,h   Gachet, Christian ^d   Bruhns, Pierre ^a,b,f   Jönsson, Friederike ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f BICHAT HOSPITAL   (France)

^g REGENERON PHARMACEUTICALS INC   (United States)

^h Service de Pneumologie A Département hospitalo universitaire FIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR IIA; IMMUNOGLOBULIN G RECEPTOR; IMMUNOGLOBULIN RECEPTOR; UNCLASSIFIED DRUG; FC RECEPTOR; FCGR2A PROTEIN, HUMAN; IMMUNOGLOBULIN G; SEROTONIN;

ANAPHYLAXIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DEPLETION; DISEASE SEVERITY; HUMAN; HYPOTHERMIA; LEUKOCYTE ACTIVATION; MOUSE; NONHUMAN; PLATELET COUNT; PLATELET DEPLETION; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTHEMIA; 129 MOUSE; ANIMAL; BLOOD; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SEVERITY OF ILLNESS INDEX; THROMBOCYTOSIS; TRANSGENIC MOUSE;

ANAPHYLAXIS; ANIMALS; BLOOD PLATELETS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOGLOBULIN G; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PLATELET ACTIVATION; PLATELET COUNT; RECEPTORS, IGG; SEROTONIN; SEVERITY OF ILLNESS INDEX; THROMBOCYTOSIS;

EID: 85048798531     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aan5997     Document Type: Article

References (46)

1. R. T. Strait, A. Mahler, S. Hogan, M. Khodoun, A. Shibuya, F. D. Finkelman, Ingested allergens must be absorbed systemically to induce systemic anaphylaxis. J. Allergy Clin. Immunol. 127, 982-989.e1 (2011).
2. J. Kalesnikoff, S. J. Galli, New developments in mast cell biology. Nat. Immunol. 9, 1215-1223 (2008).
3. S. J. Galli, Pathogenesis and management of anaphylaxis: Current status and future challenges. J. Allergy Clin. Immunol. 115, 571-574 (2005).
4. F. D. Finkelman, M. E. Rothenberg, E. B. Brandt, S. C. Morris, R. T. Strait, Molecular mechanisms of anaphylaxis: Lessons from studies with murine models. J. Allergy Clin. Immunol. 115, 449-457 (2005).
5. H. Karasuyama, K. Mukai, Y. Tsujimura, K. Obata, Newly discovered roles for basophils: A neglected minority gains new respect. Nat. Rev. Immunol. 9, 9-13 (2009).
6. γRs to disease with evidence from human polymorphisms and transgenic animal studies. Front. Immunol. 5, 254 (2014).
7. F. D. Finkelman, M. V. Khodoun, R. Strait, Human IgE-independent systemic anaphylaxis. J. Allergy Clin. Immunol. 137, 1674-1680 (2016).
8. P. Vadas, M. Gold, B. Perelman, G. M. Liss, G. Lack, T. Blyth, F. E. R. Simons, K. J. Simons, D. Cass, J. Yeung, Platelet-activating factor, PAF acetylhydrolase, and severe anaphylaxis. N. Engl. J. Med. 358, 28-35 (2008).
9. R. T. Strait, S. C. Morris, M. Yang, X.-W. Qu, F. D. Finkelman, Pathways of anaphylaxis in the mouse. J. Allergy Clin. Immunol. 109, 658-668 (2002).
10. F. Jönsson, D. A. Mancardi, Y. Kita, H. Karasuyama, B. Iannascoli, N. Van Rooijen, T. Shimizu, M. Daëron, P. Bruhns, Mouse and human neutrophils induce anaphylaxis. J. Clin. Invest. 121, 1484-1496 (2011).
11. C. M. Gillis, F. Jönsson, D. A. Mancardi, N. Tu, H. Beutier, N. Van Rooijen, L. E. Macdonald, A. J. Murphy, P. Bruhns, Mechanisms of anaphylaxis in human low-affinity IgG receptor locus knock-in mice. J. Allergy Clin. Immunol. 139, 1253-1265. e14 (2017).
12. F. Jönsson, D. A. Mancardi, M. Albanesi, P. Bruhns, Neutrophils in local and systemic antibody-dependent inflammatory and anaphylactic reactions. J. Leukoc. Biol. 94, 643-656 (2013).
13. P. Bruhns, Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119, 5640-5649 (2012).
14. F. Jönsson, D. A. Mancardi, W. Zhao, Y. Kita, B. Iannascoli, H. Khun, N. van Rooijen, T. Shimizu, L. B. Schwartz, M. Daëron, P. Bruhns, Human FcγRIIA induces anaphylactic and allergic reactions. Blood 119, 2533-2544 (2012).
15. P. Bruhns, F. Jönsson, Mouse and human FcR effector functions. Immunol. Rev. 268, 25-51 (2015).
16. G. Majno, G. E. Palade, Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: An electron microscopic study. J. Biophys. Biochem. Cytol. 11, 571-605 (1961).
17. N. Cloutier, A. Paré, R. W. Farndale, H. R. Schumacher, P. A. Nigrovic, S. Lacroix, E. Boilard, Platelets can enhance vascular permeability. Blood 120, 1334-1343 (2012).
18. S. W. Watts, S. F. Morrison, R. P. Davis, S. M. Barman, Serotonin and blood pressure regulation. Pharmacol. Rev. 64, 359-388 (2012).
19. F. Lechin, B. van der Dijs, B. Orozco, M. Lechin, A. E. Lechin, Increased levels of free serotonin in plasma of symptomatic asthmatic patients. Ann. Allergy Asthma Immunol. 77, 245-253 (1996).
20. P. Smith, D. J. DiLillo, S. Bournazos, F. Li, J. V. Ravetch, Mouse model recapitulating human Fcγ receptor structural and functional diversity. Proc. Natl. Acad. Sci. U.S.A. 109, 6181-6186 (2012).
21. J. Li, D. E. van der Wal, G. Zhu, M. Xu, I. Yougbare, L. Ma, B. Vadasz, N. Carrim, R. Grozovsky, M. Ruan, L. Zhu, Q. Zeng, L. Tao, Z.-M. Zhai, J. Peng, M. Hou, V. Leytin, J. Freedman, K. M. Hoffmeister, H. Ni, Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat. Commun. 6, 7737 (2015).
22. C. Léon, K. Evert, F. Dombrowski, F. Pertuy, A. Eckly, P. Laeuffer, C. Gachet, A. Greinacher, Romiplostim administration shows reduced megakaryocyte response-capacity and increased myelofibrosis in a mouse model of MYH9-RD. Blood 119, 3333-3341 (2012).
23. B. K. Koe, A. Weissman, p-Chlorophenylalanine: A specific depletor of brain serotonin. J. Pharmacol. Exp. Ther. 154, 499-516 (1966).
24. C. Gao, B. Boylan, J. Fang, D. A. Wilcox, D. K. Newman, P. J. Newman, Heparin promotes platelet responsiveness by potentiating αIIbβ3-mediated outside-in signaling. Blood 117, 4946-4952 (2011).
25. N. Bermejo, J. L. Guéant, E. Mata, P. Gérard, D. A. Moneret-Vautrin, M. C. Laxenaire, Platelet serotonin is a mediator potentially involved in anaphylactic reaction to neuromuscular blocking drugs. Br. J. Anaesth. 70, 322-325 (1993).
26. T. Meyer, L. Robles-Carrillo, T. Robson, F. Langer, H. Desai, M. Davila, M. Amaya, J. L. Francis, A. Amirkhosravi, Bevacizumab immune complexes activate platelets and induce thrombosis in FCGR2A transgenic mice. J. Thromb. Haemost. 7, 171-181 (2009).
27. D. Cox, S. W. Kerrigan, S. P. Watson, Platelets and the innate immune system: Mechanisms of bacterial-induced platelet activation. J. Thromb. Haemost. 9, 1097-1107 (2011).
28. S. E. McKenzie, B. S. Sachais, Advances in the pathophysiology and treatment of heparin-induced thrombocytopenia. Curr. Opin. Hematol. 21, 380-387 (2014).
29. M. Stolla, L. Stefanini, P. André, T. D. Ouellette, M. P. Reilly, S. E. McKenzie, W. Bergmeier, CalDAG-GEFI deficiency protects mice in a novel model of FcγRIIA-mediated thrombosis and thrombocytopenia. Blood 118, 1113-1120 (2011).
30. A. Gros, V. Syvannarath, L. Lamrani, V. Ollivier, S. Loyau, T. Goerge, B. Nieswandt, M. Jandrot-Perrus, B. Ho-Tin-Noé, Single platelets seal neutrophil-induced vascular breaches via GPVI during immune-complex-mediated inflammation in mice. Blood 126, 1017-1026 (2015).
31. M. Inui, K. Tazawa, Y. Kishi, T. Takai, Platelets convert peripheral blood circulating monocytes to regulatory cells via immunoglobulin G and activating-type Fcγ receptors. BMC Immunol. 16, 20 (2015).
32. J. Chen, J. A. López, Interactions of platelets with subendothelium and endothelium. Microcirculation 12, 235-246 (2005).
33. S. R. Clark, A. C. Ma, S. A. Tavener, B. McDonald, Z. Goodarzi, M. M. Kelly, K. D. Patel, S. Chakrabarti, E. McAvoy, G. D. Sinclair, E. M. Keys, E. Allen-Vercoe, R. DeVinney, C. J. Doig, F. H. Y. Green, P. Kubes, Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13, 463-469 (2007).
34. A. Caudrillier, K. Kessenbrock, B. M. Gilliss, J. X. Nguyen, M. B. Marques, M. Monestier, P. Toy, Z. Werb, M. R. Looney, Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J. Clin. Invest. 122, 2661-2671 (2012).
35. V. Sreeramkumar, J. M. Adrover, I. Ballesteros, M. I. Cuartero, J. Rossaint, I. Bilbao, M. Nácher, C. Pitaval, I. Radovanovic, Y. Fukui, R. P. McEver, M.-D. Filippi, I. Lizasoain, J. Ruiz-Cabello, A. Zarbock, M. A. Moro, A. Hidalgo, Neutrophils scan for activated platelets to initiate inflammation. Science 346, 1234-1238 (2014).
36. I. H. Choi, T. Y. Ha, D. G. Lee, J. S. Park, J. H. Lee, Y. M. Park, H. K. Lee, Occurrence of disseminated intravascular coagulation (DIC) in active systemic anaphylaxis: Role of platelet-activating factor. Clin. Exp. Immunol. 100, 390-394 (1995).
37. A. Gouel-Chéron, L. de Chaisemartin, F. Jönsson, P. Nicaise-Roland, V. Granger, A. Sabahov, M. T. Guinnepain, S. Chollet-Martin, P. Bruhns, C. Neukirch, D. Longrois; NASA study group, Low end-tidal CO2 as a real-time severity marker of intra-anaesthetic acute hypersensitivity reactions. Br. J. Anaesth. 119, 908-917 (2017).
38. J. Ring, K. Messmer, Incidence and severity of anaphylactoid reactions to colloid volume substitutes. Lancet 309, 466-469 (1977).
39. P. M. Mertes, P. M. Mertes, J. M. Malinovsky, L. Jouffroy; Working Group of the SFAR and SFA, W. Aberer, I. Terreehorst, K. Brockow, P. Demoly; ENDA; EAACI Interest Group on Drug Allergy, Reducing the risk of anaphylaxis during anesthesia: 2011 updated guidelines for clinical practice. J. Investig. Allergol. Clin. Immunol. 21, 442-453 (2011).
40. A. Gouel-Chéron, A. Harpan, P.-M. Mertes, D. Longrois, Management of anaphylactic shock in the operating room. Presse Med. 45, 774-783 (2016).
41. F. E. R. Simons, L. R. F. Ardusso, V. Dimov, M. Ebisawa, Y. M. El-Gamal, R. F. Lockey, M. Sanchez-Borges, G. E. Senna, A. Sheikh, B. Y. Thong, M. Worm; World Allergy Organization, World allergy organization anaphylaxis guidelines: 2013 update of the evidence base. Int. Arch. Allergy Immunol. 162, 193-204 (2013).
42. F. E. R. Simons, M. Ebisawa, M. Sanchez-Borges, B. Y. Thong, M. Worm, L. Kase Tanno, R. F. Lockey, Y. M. El-Gamal, S. G. A. Brown, H.-S. Park, A. Sheikh, 2015 update of the evidence base: World allergy organization anaphylaxis guidelines. World Allergy Organ. J. 8, 80 (2015).
43. D. Longrois, C. Lejus, I. Constant, M. Bruyère, P.-M. Mertes, Traitement des réactions anaphylactiques survenant en cours d'anesthésie et en particulier du choc anaphylactique. Ann. Fr. Anesth. Reanim. 30, 312-322 (2011).
44. C. M. Gillis, P. P. Zenatti, D. A. Mancardi, H. Beutier, L. Fiette, L. E. Macdonald, A. J. Murphy, S. Celli, P. Bousso, F. Jönsson, P. Bruhns, In vivo effector functions of high-affinity mouse IgG receptor FcRI in disease and therapy models. J. Autoimmun. 80, 95-102 (2016).
45. S. E. McKenzie, S. M. Taylor, P. Malladi, H. Yuhan, D. L. Cassel, P. Chien, E. Schwartz, A. D. Schreiber, S. Surrey, M. P. Reilly, The role of the human Fc receptor FcγRIIA in the immune clearance of platelets: A transgenic mouse model. J. Immunol. 162, 4311-4318 (1999).
46. J.-P. Cazenave, P. Ohlmann, D. Cassel, A. Eckly, B. Hechler, C. Gachet, Preparation of washed platelet suspensions from human and rodent blood. Methods Mol. Biol. 272, 13-28 (2004).