The deleterious role of basophils in systemic lupus erythematosus

Current Opinion in Immunology

Volumn 25, Issue 6, 2013, Pages 704-711

  Pellefigues, Christophe ^a   Charles, Nicolas ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; IMMUNOGLOBULIN E; INTERLEUKIN 4;

ANTIBODY PRODUCTION; B LYMPHOCYTE; BASOPHIL; DISEASE MODEL; HUMAN; IMMUNE SYSTEM; IMMUNOREGULATION; LEUKOCYTE FUNCTION; LYMPHOID ORGAN; NONHUMAN; PATHOGENESIS; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TH2 CELL;

ANIMALS; BASOPHILS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; TH2 CELLS;

EID: 84889086650     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.10.003     Document Type: Review

References (78)

1. Rahman A., Isenberg D.A. Systemic lupus erythematosus. N Engl J Med 2008, 358:929-939.
2. Villegas-Zambrano N., Martinez-Taboada V.M., Bolivar A., San Martin M., Alvarez L., Marin M.J., Lopez-Hoyos M. Correlation between clinical activity and serological markers in a wide cohort of patients with systemic lupus erythematosus: an eight-year prospective study. Ann N Y Acad Sci 2009, 1173:60-66.
3. Daugas E. Treatment of proliferative glomerulonephritis of systemic lupus erythematosus. Recent development and current recommendations. Rev Med Interne 2008, 29:710-717.
4. Karasuyama H., Mukai K., Obata K., Tsujimura Y., Wada T. Nonredundant roles of basophils in immunity. Annu Rev Immunol 2011, 29:45-69.
5. Charles N., Watford W.T., Ramos H.L., Hellman L., Oettgen H.C., Gomez G., Ryan J.J., O'Shea J.J., Rivera J. Lyn kinase controls basophil GATA-3 transcription factor expression and induction of Th2 cell differentiation. Immunity 2009, 30:533-543.
6. Sokol C.L., Barton G.M., Farr A.G., Medzhitov R. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat Immunol 2008, 9:310-318.
7. Rodriguez Gomez M., Talke Y., Hofmann C., Ketelsen I., Hermann F., Reich B., Goebel N., Schmidbauer K., Dunger N., Bruhl H., et al. Basophils control T-cell responses and limit disease activity in experimental murine colitis. Mucosal Immunol 2013 (June 12), [Epub ahead of print]. 10.1038/mi.2013.38.
8. Kim S., Shen T., Min B. Basophils can directly present or cross-present antigen to CD8 lymphocytes and alter CD8T cell differentiation into IL-10-producing phenotypes. J Immunol 2009, 183:3033-3039.
9. Otsuka A., Nakajima S., Kubo M., Egawa G., Honda T., Kitoh A., Nomura T., Hanakawa S., Sagita Moniaga C., Kim B., et al. Basophils are required for the induction of Th2 immunity to haptens and peptide antigens. Nat Commun 2013, 4:1738.
10. Perrigoue J.G., Saenz S.A., Siracusa M.C., Allenspach E.J., Taylor B.C., Giacomin P.R., Nair M.G., Du Y., Zaph C., van Rooijen N., et al. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat Immunol 2009, 10:697-705.
11. Sokol C.L., Chu N.Q., Yu S., Nish S.A., Laufer T.M., Medzhitov R. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol 2009, 10:713-720.
12. Yoshimoto T., Yasuda K., Tanaka H., Nakahira M., Imai Y., Fujimori Y., Nakanishi K. Basophils contribute to T(H)2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol 2009, 10:706-712.
13. Hammad H., Plantinga M., Deswarte K., Pouliot P., Willart M.A., Kool M., Muskens F., Lambrecht B.N. Inflammatory dendritic cells - not basophils - are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med 2010, 207:2097-2111.
14. Sullivan B.M., Liang H.E., Bando J.K., Wu D., Cheng L.E., McKerrow J.K., Allen C.D., Locksley R.M. Genetic analysis of basophil function in vivo. Nat Immunol 2011, 12:527-535.
15. Charles N., Hardwick D., Daugas E., Illei G.G., Rivera J. Basophils the T helper 2 environment can promote the development of lupus nephritis. Nat Med 2010, 16:701-707.
16. Denzel A., Maus U.A., Rodriguez Gomez M., Moll C., Niedermeier M., Winter C., Maus R., Hollingshead S., Briles D.E., Kunz-Schughart L.A., et al. Basophils enhance immunological memory responses. Nat Immunol 2008, 9:733-742.
17. Rodriguez Gomez M., Talke Y., Goebel N., Hermann F., Reich B., Mack M. Basophils support the survival of plasma cells in mice. J Immunol 2010, 185:7180-7185.
18. Tang H., Cao W., Kasturi S.P., Ravindran R., Nakaya H.I., Kundu K., Murthy N., Kepler T.B., Malissen B., Pulendran B. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat Immunol 2010, 11:608-617.
19. Egawa M., Mukai K., Yoshikawa S., Iki M., Mukaida N., Kawano Y., Minegishi Y., Karasuyama H. Inflammatory monocytes recruited to allergic skin acquire an anti-inflammatory M2 phenotype via basophil-derived interleukin-4. Immunity 2013, 38:570-580.
20. Anthony R.M., Kobayashi T., Wermeling F., Ravetch J.V. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 2011, 475:110-113.
21. 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 T cells and mast cells. Immunity 2005, 23:191-202.
22. Wada T., Ishiwata K., Koseki H., Ishikura T., Ugajin T., Ohnuma N., Obata K., Ishikawa R., Yoshikawa S., Mukai K., et al. Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks. J Clin Invest 2010, 120:2867-2875.
23. Chen K., Xu W., Wilson M., He B., Miller N.W., Bengten E., Edholm E.S., Santini P.A., Rath P., Chiu A., et al. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat Immunol 2009, 10:889-898.
24. Liu Z., Davidson A. Taming lupus - a new understanding of pathogenesis is leading to clinical advances. Nat Med 2012, 18:871-882.
25. Scheinecker C., Bonelli M., Smolen J.S. Pathogenetic aspects of systemic lupus erythematosus with an emphasis on regulatory T cells. J Autoimmun 2010, 35:269-275.
26. Shimizu S., Sugiyama N., Masutani K., Sadanaga A., Miyazaki Y., Inoue Y., Akahoshi M., Katafuchi R., Hirakata H., Harada M., et al. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J Immunol 2005, 175:7185-7192.
27. Peng S.L., Szabo S.J., Glimcher L.H. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc Natl Acad Sci U S A 2002, 99:5545-5550.
28. Alunno A., Bartoloni E., Bistoni O., Nocentini G., Ronchetti S., Caterbi S., Valentini V., Riccardi C., Gerli R. Balance between regulatory T and Th17 cells in systemic lupus erythematosus: the old and the new. Clin Dev Immunol 2012, 2012:823085.
29. Hsu H.C., Yang P., Wang J., Wu Q., Myers R., Chen J., Yi J., Guentert T., Tousson A., Stanus A.L., et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 2008, 9:166-175.
30. Simpson N., Gatenby P.A., Wilson A., Malik S., Fulcher D.A., Tangye S.G., Manku H., Vyse T.J., Roncador G., Huttley G.A., et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum 2010, 62:234-244.
31. Linterman M.A., Rigby R.J., Wong R.K., Yu D., Brink R., Cannons J.L., Schwartzberg P.L., Cook M.C., Walters G.D., Vinuesa C.G. Follicular helper T cells are required for systemic autoimmunity. J Exp Med 2009, 206:561-576.
32. Blanco P., Palucka A.K., Gill M., Pascual V., Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 2001, 294:1540-1543.
33. Mathian A., Weinberg A., Gallegos M., Banchereau J., Koutouzov S. IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black×New Zealand White) F1 but not in BALB/c mice. J Immunol 2005, 174:2499-2506.
34. Obermoser G., Pascual V. The interferon-alpha signature of systemic lupus erythematosus. Lupus 2010, 19:1012-1019.
35. Garcia-Romo G.S., Caielli S., Vega B., Connolly J., Allantaz F., Xu Z., Punaro M., Baisch J., Guiducci C., Coffman R.L., et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011, 3:73ra20.
36. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., Meller S., Chamilos G., Sebasigari R., Riccieri V., et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011, 3:73ra19.
37. Atta A.M., Sousa C.P., Carvalho E.M., Sousa-Atta M.L. Immunoglobulin E and systemic lupus erythematosus. Braz J Med Biol Res 2004, 37:1497-1501.
38. Xu Y., Harder K.W., Huntington N.D., Hibbs M.L., Tarlinton D.M. Lyn tyrosine kinase: accentuating the positive and the negative. Immunity 2005, 22:9-18.
39. Hibbs M.L., Tarlinton D.M., Armes J., Grail D., Hodgson G., Maglitto R., Stacker S.A., Dunn A.R. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995, 83:301-311.
40. Nishizumi H., Taniuchi I., Yamanashi Y., Kitamura D., Ilic D., Mori S., Watanabe T., Yamamoto T. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 1995, 3:549-560.
41. Odom S., Gomez G., Kovarova M., Furumoto Y., Ryan J.J., Wright H.V., Gonzalez-Espinosa C., Hibbs M.L., Harder K.W., Rivera J. Negative regulation of immunoglobulin E-dependent allergic responses by Lyn kinase. J Exp Med 2004, 199:1491-1502.
42. Ohnmacht C., Schwartz C., Panzer M., Schiedewitz I., Naumann R., Voehringer D. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 2010, 33:364-374.
43. Camussi G., Tetta C., Benveniste J. Detection of basophil sensitization by IgE antibodies to nuclear antigens in connective tissue diseases. Int Arch Allergy Appl Immunol 1982, 69:358-362.
44. Cassard L., Jonsson F., Arnaud S., Daeron M. Fcgamma receptors inhibit mouse and human basophil activation. J Immunol 2012, 189:2995-3006.
45. Iikura M., Yamaguchi M., Fujisawa T., Miyamasu M., Takaishi T., Morita Y., Iwase T., Moro I., Yamamoto K., Hirai K. Secretory IgA induces degranulation of IL-3-primed basophils. J Immunol 1998, 161:1510-1515.
46. Charles N., Rivera J. Basophils and autoreactive IgE in the pathogenesis of systemic lupus erythematosus. Curr Allergy Asthma Rep 2011, 11:378-387.
47. Marichal T., Ohata K., Bedoret D., Mesnil C., Sabatel C., Kobiyama K., Lekeux P., Coban C., Akira S., Ishii K.J., et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 2011, 17:996-1002.
48. Komiya A., Nagase H., Okugawa S., Ota Y., Suzukawa M., Kawakami A., Sekiya T., Matsushima K., Ohta K., Hirai K., et al. Expression and function of toll-like receptors in human basophils. Int Arch Allergy Immunol 2006, 140(Suppl. 1):23-27.
49. Scheibner K.A., Lutz M.A., Boodoo S., Fenton M.J., Powell J.D., Horton M.R. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol 2006, 177:1272-1281.
50. Wakahara K., Baba N., Van V.Q., Begin P., Rubio M., Ferraro P., Panzini B., Wassef R., Lahaie R., Caussignac Y., et al. Human basophils interact with memory T cells to augment Th17 responses. Blood 2012, 120:4761-4771.
51. Wong C.K., Cao J., Yin Y.B., Lam C.W. Interleukin-17A activation on bronchial epithelium and basophils: a novel inflammatory mechanism. Eur Respir J 2010, 35:883-893.
52. Spiegl N., Didichenko S., McCaffery P., Langen H., Dahinden C.A. Human basophils activated by mast cell-derived IL-3 express retinaldehyde dehydrogenase-II and produce the immunoregulatory mediator retinoic acid. Blood 2008, 112:3762-3771.
53. Bauer J.W., Baechler E.C., Petri M., Batliwalla F.M., Crawford D., Ortmann W.A., Espe K.J., Li W., Patel D.D., Gregersen P.K., et al. Elevated serum levels of interferon-regulated chemokines are biomarkers for active human systemic lupus erythematosus. PLoS Med 2006, 3:e491.
54. Gaga M., Ong Y.E., Benyahia F., Aizen M., Barkans J., Kay A.B. Skin reactivity and local cell recruitment in human atopic and nonatopic subjects by CCL2/MCP-1 and CCL3/MIP-1alpha. Allergy 2008, 63:703-711.
55. Heinemann A., Hartnell A., Stubbs V.E., Murakami K., Soler D., LaRosa G., Askenase P.W., Williams T.J., Sabroe I. Basophil responses to chemokines are regulated by both sequential and cooperative receptor signaling. J Immunol 2000, 165:7224-7233.
56. Iikura M., Ebisawa M., Yamaguchi M., Tachimoto H., Ohta K., Yamamoto K., Hirai K. Transendothelial migration of human basophils. J Immunol 2004, 173:5189-5195.
57. Iikura M., Miyamasu M., Yamaguchi M., Kawasaki H., Matsushima K., Kitaura M., Morita Y., Yoshie O., Yamamoto K., Hirai K. Chemokine receptors in human basophils: inducible expression of functional CXCR4. J Leukoc Biol 2001, 70:113-120.
58. Ochensberger B., Tassera L., Bifrare D., Rihs S., Dahinden C.A. Regulation of cytokine expression and leukotriene formation in human basophils by growth factors, chemokines and chemotactic agonists. Eur J Immunol 1999, 29:11-22.
59. Lit L.C., Wong C.K., Tam L.S., Li E.K., Lam C.W. Raised plasma concentration and ex vivo production of inflammatory chemokines in patients with systemic lupus erythematosus. Ann Rheum Dis 2006, 65:209-215.
60. Vila L.M., Molina M.J., Mayor A.M., Cruz J.J., Rios-Olivares E., Rios Z. Association of serum MIP-1alpha, MIP-1beta, and RANTES with clinical manifestations, disease activity, and damage accrual in systemic lupus erythematosus. Clin Rheumatol 2007, 26:718-722.
61. Gilet J., Chang Y., Chenivesse C., Legendre B., Vorng H., Duez C., Wallaert B., Porte H., Senechal S., Tsicopoulos A. Role of CCL17 in the generation of cutaneous inflammatory reactions in Hu-PBMC-SCID mice grafted with human skin. J Invest Dermatol 2009, 129:879-890.
62. Lim L.H., Burdick M.M., Hudson S.A., Mustafa F.B., Konstantopoulos K., Bochner B.S. Stimulation of human endothelium with IL-3 induces selective basophil accumulation in vitro. J Immunol 2006, 176:5346-5353.
63. Geiser T., Dewald B., Ehrengruber M.U., Clark-Lewis I., Baggiolini M. The interleukin-8-related chemotactic cytokines GRO alpha, GRO beta, and GRO gamma activate human neutrophil and basophil leukocytes. J Biol Chem 1993, 268:15419-15424.
64. Wang A., Fairhurst A.M., Tus K., Subramanian S., Liu Y., Lin F., Igarashi P., Zhou X.J., Batteux F., Wong D., et al. CXCR4/CXCL12 hyperexpression plays a pivotal role in the pathogenesis of lupus. J Immunol 2009, 182:4448-4458.
65. Kroeger K.M., Sullivan B.M., Locksley R.M. I.L-18 IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38alpha-dependent pathway. J Leukoc Biol 2009, 86:769-778.
66. Mok M.Y., Huang F.P., Ip W.K., Lo Y., Wong F.Y., Chan E.Y., Lam K.F., Xu D. Serum levels of IL-33 and soluble ST2 and their association with disease activity in systemic lupus erythematosus. Rheumatology (Oxford) 2010, 49:520-527.
67. Yang Z., Liang Y., Xi W., Li C., Zhong R. Association of increased serum IL-33 levels with clinical and laboratory characteristics of systemic lupus erythematosus in Chinese population. Clin Exp Med 2011, 11:75-80.
68. Pecaric-Petkovic T., Didichenko S.A., Kaempfer S., Spiegl N., Dahinden C.A. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 2009, 113:1526-1534.
69. Suzukawa M., Iikura M., Koketsu R., Nagase H., Tamura C., Komiya A., Nakae S., Matsushima K., Ohta K., Yamamoto K., et al. An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J Immunol 2008, 181:5981-5989.
70. Garcia-Gonzalez A., Gonzalez-Lopez L., Valera-Gonzalez I.C., Cardona-Munoz E.G., Salazar-Paramo M., Gonzalez-Ortiz M., Martinez-Abundis E., Gamez-Nava J.I. Serum leptin levels in women with systemic lupus erythematosus. Rheumatol Int 2002, 22:138-141.
71. Suzukawa M., Nagase H., Ogahara I., Han K., Tashimo H., Shibui A., Koketsu R., Nakae S., Yamaguchi M., Ohta K. Leptin enhances survival and induces migration, degranulation, and cytokine synthesis of human basophils. J Immunol 2011, 186:5254-5260.
72. Moneib H.A., Salem S.A., Aly D.G., Khedr H.T., Wafaey H.A., Hassan H.E. Assessment of serum vascular endothelial growth factor and nail fold capillaroscopy changes in systemic lupus erythematosus with and without cutaneous manifestations. J Dermatol 2012, 39:52-57.
73. de Paulis A., Prevete N., Fiorentino I., Rossi F.W., Staibano S., Montuori N., Ragno P., Longobardi A., Liccardo B., Genovese A., et al. Expression and functions of the vascular endothelial growth factors and their receptors in human basophils. J Immunol 2006, 177:7322-7331.
74. Somparn P., Hirankarn N., Leelahavanichkul A., Khovidhunkit W., Thongboonkerd V., Avihingsanon Y. Urinary proteomics revealed prostaglandin H(2)D-isomerase, not Zn-alpha2-glycoprotein, as a biomarker for active lupus nephritis. J Proteomics 2012, 75:3240-3247.
75. Monneret G., Boumiza R., Gravel S., Cossette C., Bienvenu J., Rokach J., Powell W.S. Effects of prostaglandin D(2) and 5-lipoxygenase products on the expression of CD203c and CD11b by basophils. J Pharmacol Exp Ther 2005, 312:627-634.
76. Yoshimura-Uchiyama C., Iikura M., Yamaguchi M., Nagase H., Ishii A., Matsushima K., Yamamoto K., Shichijo M., Bacon K.B., Hirai K. Differential modulation of human basophil functions through prostaglandin D2 receptors DP and chemoattractant receptor-homologous molecule expressed on Th2 cells/DP2. Clin Exp Allergy 2004, 34:1283-1290.
77. Fattal I., Shental N., Mevorach D., Anaya J.M., Livneh A., Langevitz P., Zandman-Goddard G., Pauzner R., Lerner M., Blank M., et al. An antibody profile of systemic lupus erythematosus detected by antigen microarray. Immunology 2010, 130:337-343.
78. Bieneman A.P., Chichester K.L., Chen Y.H., Schroeder J.T. Toll-like receptor 2 ligands activate human basophils for both IgE-dependent and IgE-independent secretion. J Allergy Clin Immunol 2005, 115:295-301.