Allergen induces the migration of platelets to lung tissue in allergic asthma

American Journal of Respiratory and Critical Care Medicine

Volumn 177, Issue 6, 2008, Pages 604-612

  Pitchford, Simon C ^a,b,d   Momi, Stefania ^a   Baglioni, Stefano ^c   Casali, Lucio ^a   Giannini, Silvia ^a   Rossi, Roberta ^a   Page, Clive P ^b   Gresele, Paolo ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c Ospedale Silvestrini   (Italy)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Allergen; Chemotaxis; Fc RI; IgE; Inflammation; Platelets

Indexed keywords

ALLERGEN; CD23 ANTIGEN; FC EPSILON RECEPTOR 1; FC RECEPTOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; OVALBUMIN; UNCLASSIFIED DRUG; ANTI-IGE; ANTIIDIOTYPIC ANTIBODY; IMMUNOGLOBULIN E RECEPTOR;

AIRWAY; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIZATION; THROMBOCYTE; ANIMAL; ASTHMA; BRONCHUS HYPERREACTIVITY; IMMUNOLOGY; LEUKOCYTE; LUNG; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALLERGENS; ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ASTHMA; BLOOD PLATELETS; BRONCHIAL HYPERREACTIVITY; CHEMOTAXIS; LEUKOCYTES; LUNG; MALE; MICE; OVALBUMIN; RECEPTORS, IGE;

EID: 40949141930     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200702-214OC     Document Type: Article

References (52)

1. Jeffery PK, Wardlaw AJ, Nelson FC, Collins JV, Kay AB. Bronchial biopsies in asthma: an ultrastructural, quantitative study and correlation with hyperreactivity. Am Rev Respir Dis 1989;140:1745-1753.
2. Gresele P, Dottorini M, Selli ML, Iannacci L, Canino S, Todisco T, Romano S, Crook P, Page CP, Nenci GG. Altered platelet function associated with the bronchial hyperresponsiveness accompanying nocturnal asthma. J Allergy Clin Immunol 1993;91:894-902.
3. Sullivan PJ, Jafar ZH, Harbinson PL, Restrick LJ, Costello JF, Page CP. Platelet dynamics following allergen challenge in allergic asthmatics. Respiration 2000;67:514-517.
4. Pitchford SC, Yano H, Lever R, Riffo-Vasquez Y, Ciferri S, Giannini S, Momi S, Spina D, O'Connor B, Gresele P, Page CP. Platelets are essential for leukocyte recruitment in allergic inflammation. J Allergy Clin Immunol 2003;112:109-118.
5. Coyle AJ, Page CP, Atkinson L, Flanagan R, Metzger WJ. The requirement for platelets in allergen-induced late asthmatic airway obstruction: eosinophil infiltration and heightened airway responsiveness in allergic rabbits. Am Rev Respir Dis 1990;142:587-593.
6. Lellouch-Tubiana A, Lefort J, Simon MT, Pfister A, Vargaftig BB. Eosinophil recruitment into guinea pig lungs after PAF-acether and allergen administration: modulation by prostacyclin, platelet depletion, and selective antagonists. Am Rev Respir Dis 1988;137:948-954.
7. Pinckard RN, Halonen M, Palmer JD, Butler C, Shaw JO, Henson PM. Intravascular aggregation and pulmonary sequestration of platelets during IgE-induced systemic anaphylaxis in the rabbit: abrogation of lethal anaphylactic shock by platelet depletion. J Immunol 1977;119:2185-2193.
8. Barrios RJ, Kheradmand F, Batts L, Corry DB. Asthma: pathology and pathophysiology. Arch Pathol Lab Med 2006;130:447-451.
9. Pitchford SC, Momi S, Giannini S, Casali L, Spina D, Page CP, Gresele P. Platelet P-selectin is required for pulmonary eosinophil and lymphocyte recruitment in a murine model of allergic inflammation. Blood 2005;105:2074-2081.
10. Schenk BI, Petersen FD, Flad HD, Brandt E. Platelet-derived chemokines CXC chemokine ligand (CXCL)7 connective tissue-activating peptide III, and CXCL4 differentially and cross-regulate neutrophil adhesion and transendothelial migration. J Immunol 2002;169:2602-2610.
11. Bengtsson T, Fryden A, Zalavary S, Whiss PA, Orselius K, Grenegard M. Platelets enhance neutrophil locomotion: evidence for a role of P-selectin. Scand J Clin Lab Invest 1999;59:439-449.
12. Pitchford SC, Riffo-Vasquez Y, Sousa A, Momi S, Gresele P, Spina D, Page CP. Platelets are necessary for airway wall remodelling in a murine model of chronic allergic inflammation. Blood 2004;103:639-647.
13. Luster AD, Alon R, von Adrian UH. Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol 2005;6:1182-1190.
14. Muller WA. New mechanism and pathways for monocyte recruitment. J Exp Med 2001;194:F47-F51.
15. Feng D, Nagy JA, Pyne K, Dvorak HF, Dvorak AM. Platelets exit venules by a transcellular pathway at sites of F-Met peptide-induced acute inflammation in guinea pigs. Int Arch Allergy Immunol 1998;116:188-195.
16. Hasegawa S, Pawankar R, Suzuki K, Nakahata T, Furukawa S, Okumura K, Ra C. Functional expression of the high affinity receptor for IgE (FcepsilonRI) in human platelets and its intracellular expression in human megakaryocytes. Blood 1999;93:2543-2551.
17. Joseph M, Gounni AS, Kusnierz JP, Vorng H, Sarfati M, Kinet JP, Tonnel AB, Capron A, Capron M. Expression and functions of the high-affinity IgE receptor on human platelets and megakaryocyte precursors. Eur J Immunol 1997;27:2212-2218.
18. Matsuda H, Ushio H, Geba GP, Askenase PW. Human platelets can initiate T cell-dependent contact sensitivity through local serotonin release mediated by IgE antibodies. J Immunol 1997;158:2891-2897.
19. Cines DB, Van Der KH, Levinson AI. In vitro binding of an IgE protein to human platelets. J Immunol 1986;136:3433-3440.
20. Cardot E, Pestel J, Callebaut I, Lassalle P, Tsicopoulos A, Gras-Masse H, Capron A, Joseph M. Specific activation of platelets from patients allergic to Dermatophagoides pteronyssinus by specific peptides derived from the allergen Der p I. Int Arch Allergy Immunol 1992;98:127-134.
21. Ishizuka T, Okajima F, Ishiwara M, Iizuka K, Ichimonji I, Kawata T, Tsukagoshi H, Dobashi K, Nakazawa T, Mori M. Sensitized mast cells migrate toward the antigen: a response regulated by p38 mitogenactivated protein kinase and Rho-associated coiled-coil-forming protein kinase. J Immunol 2001;167:2298-2304.
22. Svensson L, Rudin A, Wenneras C. Allergen extracts directly mobilize and activate human eosinophils. Eur J Immunol 2004;34:1744-1751.
23. Orida N, Feldman JD, Katz DH, Liu FT. IgE mediated chemotaxis of rat basophilic leukaemia cells towards specific antigen. J Exp Med 1983;157:2166-2171.
24. Pitchford S, Momi S, Casali L, Gresele P. Platelets migrate in response to allergen in vivo and in vitro: role of IgE [abstract]. Pathophysiol Haemost Thromb 2003;33:24.
25. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcRγ chain deletion results in pleiotropic effector cell defects. Cell 1994;76:519-529.
26. Valone FH, Austen KF, Goetzl EJ. Modulation of the random migration of human platelets. J Clin Invest 1974;54:1100-1106.
27. Zigmond SH, Hirsh JG. Leukocyte locomotion and chemotaxis: new methods for evaluation, and demonstration of a cell-derived chemotactic factor. J Exp Med 1973;137:387-410.
28. Vicente-Manzaranes M, Montoya MC, Mellado M, Frade JM, del Pozo MA, Nieto M, de Landazuri MO, Martinez AC, Sanchez-Madrid F. The chemokine SDF-1 alpha triggers a chemotactic response and induces cell polarization in human B lymphocytes. Eur J Immunol 1998;28:2197-2207.
29. Joseph M, Capron A, Ameisen JC, Capron M, Vorng H, Pancre V, Kusnierz JP, Auriault C. The receptor for IgE on blood platelets. Eur J Immunol 1986;16:306-312.
30. εR2) of eosinophils, platelets, and macrophages. J Exp Med 1986;164:72-89.
31. Borkowski TA, Jouvin MH, Lin SY, Kinet P. Minimal requirements for IgE-mediated regulation of surface FcεRI. J Immunol 2001;167:1290-1296.
32. Novak N, Tepel C, Koch S, Brix K, Bieber T, Kraft S. Evidence for a differential expression of the FcεRIγ chain in dendritic cells of atopic and nonatopic donors. J Clin Invest 2003;111:1047-1056.
33. Taube C, Dakhama A, Rha YH, Takeda K, Joetham A, Park JW, Balhorn A, Takai T, Poch KR, Nick JA, et al. Transient neutrophil infiltration after allergen challenge is dependent on specific antibodies and Fc gamma III receptors. J Immunol 2003;170:4301-4309.
34. Mehlhop PD, Van De Run M, Goldberg AB. Allergen induced bronchial hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc Natl Acad Sci USA 1997;94:1344-1349.
35. Hamelmann E, Tadeda K, Oshiba A, Gelfand EW. Role of IgE in the development of allergic inflammation and airway hyperresponsiveness: a murine model. Am J Respir Cell Mol Biol 1999;21:480-489.
36. Kung TT, Stelts D, Zurcher JA. Mast cells modulate allergic pulmonary eosinophilia in mice. Am J Respir Cell Mol Biol 1995;12:404-409.
37. Coyle AJ, Wagner K, Bertrand C, Tsuyuki S, Bews J, Heusseries C. Central role of immunoglobulin (Ig)E in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production: inhibition by a non-anaphylactic anti-IgE antibody. J Exp Med 1996;183:1303-1310.
38. Nakajima H, Iwamoto I, Tomoe S. CD4+ T-lymphocytes and interleukin-5 mediate antigen-induced eosinophil infiltration into the mouse trachea. Am Rev Respir Dis 1992;146:374-377.
39. Joseph M, Auriault C, Capron A, Vorng H, Viens P. A new function for platelets: IgE-dependent killing of schistosomes. Nature 1983;303:810-812.
40. Klouche M, Klinger MH, Kuhnel W, Wilhelm D. Endocytosis, storage, and release of IgE by human platelets: differences in patients with type I allergy and nonatopic subjects. J Allergy Clin Immunol 1997;100:235-241.
41. Bruhns P, Fremont S, Daeron M. Regulation of allergy by Fc receptors. Curr Opin Immunol 2006;17:662-669.
42. Clancy R. Cellular immunity to autologous platelets and serum-blocking factors in idiopathic thrombocytopenic purpura. Lancet 1972;7740:6-9.
43. Czapiga M, Gao JL, Kirk A, Lekstrom-Himes J. Human platelets exhibit chemotaxis using functional N-formyl peptide receptors. Exp Hematol 2005;33:73-84.
44. Kravis TC, Henson PM. Accumulation of platelets at sites of antigen-antibody-mediated injury: a possible role for IgE antibody and mast cells. J Immunol 1977;118:1569-1573.
45. Ciferri S, Emiliani C, Guglielmini G, Orlacchio A, Nenci GG, Gresele P. Platelets release their lysosomal content in vivo in humans upon activation. Thromb Haemost 2000;83:157-164.
46. Falcinelli E, Gugliemini G, Torti M, Gresele P. Intraplatelet signaling mechanisms of the priming effect of matrix metalloproteinase-2 on platelet aggregation. J Thromb Haemost 2005;3:2526-2535.
47. Corry DB, Rishi K, Kanellis J, Kiss A, Song LZ, Xu J, Feng L, Werb Z, Kheradmand F. Decrease allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency. Nat Immunol 2002;3:347-353.
48. Massberg S, Brand S, Gruner S, Page E, Muller I, Muller T, Bergme Richter M, Lorenz I, Konrad B, Nieswandt B, et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med 2002;196:887-896.
49. Zarbock A, Singbarti K, Ley K. Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest 2006;116:3211-3219.
50. Chignard M, Wal F, Lefort J, Vargaftig BB. Inhibition by sulphinpyrazone of the platelet dependent bronchoconstriction due to platelet-activating factor (PAF-acether) in the guinea pig. Eur J Pharmacol 1982;78:71-79.
51. Tomioka S, Bates JHT, Irvin CG. Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations. J Appl Physiol 2002;93:263-270.
52. Spina D, Page CP. Asthma, a time for a rethink? Trends Pharmacol Sci 2002;23:311-315.