Genetic identification and functional validation of FcγRIV as key molecule in autoantibody-induced tissue injury

Journal of Pathology

Volumn 228, Issue 1, 2012, Pages 8-19

  Kasperkiewicz, Michael ^a   Nimmerjahn, Falk ^b   Wende, Sabina ^a   Hirose, Misa ^a   Iwata, Hiroaki ^a   Jonkman, Marcel F ^c   Samavedam, Unni ^a   Gupta, Yask ^a   Möller, Steffen ^a   Rentz, Ellen ^d   Hellberg, Lars ^a   Kalies, Kathrin ^a   Yu, Xinhua ^e   Schmidt, Enno ^a   Häsler, Robert ^f   Laskay, Tamás ^a   Westermann, Jürgen ^a   Köhl, Jörg ^a,g   Zillikens, Detlef ^a   Ludwig, Ralf J ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d BIOTEST AG   (Germany)

^e RESEARCH CENTER BORSTEL   (Germany)

^f UNIVERSITY OF KIEL   (Germany)

^g UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

autoimmune disease; epidermolysis bullosa acquisita; Fc RIV; inflammation

Indexed keywords

AUTOANTIBODY; CD16 ANTIGEN; COLLAGEN ANTIBODY; COLLAGEN TYPE 7 ANTIBODY; FC RECEPTOR; FC RECEPTOR I; FC RECEPTOR IIB; FC RECEPTOR IV; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; BLISTER; CONTROLLED STUDY; EPIDERMOLYSIS BULLOSA ACQUISITA; EXPERIMENTAL MODEL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC IDENTIFICATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; INFLAMMATION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYSTEMS BIOLOGY; TISSUE INJURY; VALIDATION STUDY; WEIGHTED GENE CO EXPRESSION NETWORK ANALYSIS; WILD TYPE;

ANIMALS; ANTIBODIES, BLOCKING; AUTOANTIBODIES; AUTOIMMUNE DISEASES; COLLAGEN TYPE VII; DISEASE MODELS, ANIMAL; EPIDERMOLYSIS BULLOSA ACQUISITA; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN ISOTYPES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; ORGAN SPECIFICITY; RECEPTORS, IGG;

EID: 84864779338     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4023     Document Type: Article

References (55)

1. Gabriel SE, Michaud K,. Epidemiological studies in incidence, prevalence, mortality, and comorbidity of the rheumatic diseases. Arthritis Res Ther 2009; 11: 229.
2. Kasperkiewicz M, Schmidt E,. Current treatment of autoimmune blistering diseases. Curr Drug Discov Technol 2009; 6: 270-280.
3. Bauer JW, Bilgic H, Baechler EC,. Gene-expression profiling in rheumatic disease: tools and therapeutic potential. Nat Rev Rheumatol 2009; 5: 257-265.
4. Zhao W, Langfelder P, Fuller T, et al., Weighted gene coexpression network analysis: state of the art. J Biopharm Stat 2010; 20: 281-300.
5. Sitaru C,. Experimental models of epidermolysis bullosa acquisita. Exp Dermatol 2007; 16: 520-523.
6. Bieber K, Sun S, Ishii N, et al., Animal models for autoimmune bullous dermatoses. Exp Dermatol 2010; 19: 2-11.
7. Woodley DT, Briggaman RA, O'Keefe EJ, et al., Identification of the skin basement-membrane autoantigen in epidermolysis bullosa acquisita. N Engl J Med 1984; 310: 1007-1013.
8. Woodley DT, Burgeson RE, Lunstrum G, et al., Epidermolysis bullosa acquisita antigen is the globular carboxyl terminus of type VII procollagen. J Clin Invest 1988; 81: 683-687.
9. Sitaru C, Kromminga A, Hashimoto T, et al., Autoantibodies to type VII collagen mediate Fcγ-dependent granulocyte activation and induce dermal-epidermal separation in cryosections of human skin. Am J Pathol 2002; 161: 301-311.
10. Recke A, Sitaru C, Vidarsson G, et al., Pathogenicity of IgG subclass autoantibodies to type VII collagen: induction of dermal-epidermal separation. J Autoimmun 2010; 34: 435-444.
11. Sitaru C, Mihai S, Otto C, et al., Induction of dermal-epidermal separation in mice by passive transfer of antibodies to type VII collagen. J Clin Invest 2005; 115: 870-878.
12. Woodley DT, Chang C, Saadat P, et al., Evidence that anti-type VII collagen antibodies are pathogenic and responsible for the clinical, histological, and immunological features of epidermolysis bullosa acquisita. J Invest Dermatol 2005; 124: 958-964.
13. Woodley DT, Ram R, Doostan A, et al., Induction of epidermolysis bullosa acquisita in mice by passive transfer of autoantibodies from patients. J Invest Dermatol 2006; 126: 1323-1330.
14. Chen M, Doostan A, Bandyopadhyay P, et al., The cartilage matrix protein subdomain of type VII collagen is pathogenic for epidermolysis bullosa acquisita. Am J Pathol 2007; 170: 2009-2018.
15. Sitaru C, Chiriac MT, Mihai S, et al., Induction of complement-fixing autoantibodies against type VII collagen results in subepidermal blistering in mice. J Immunol 2006; 177: 3461-3468.
16. Kasperkiewicz M, Müller R, Manz R, et al., Heat shock protein 90 inhibition in autoimmunity to type VII collagen: evidence that non-malignant plasma cells are not therapeutic targets. Blood 2011; 117: 6135-6142.
17. Ludwig RJ, Zillikens D,. Pathogenesis of epidermolysis bullosa acquisita. Dermatol Clin 2011; 29: 493-501.
18. Sitaru C, Zillikens D,. Mechanisms of blister induction by autoantibodies. Exp Dermatol 2005; 14: 861-875.
19. Nimmerjahn F, Bruhns P, Horiuchi K, et al., FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 2005; 23: 41-51.
20. Mah N, Thelin A, Lu T, et al., A comparison of oligonucleotide and cDNA-based microarray systems. Physiol Genomics 2004; 16: 361-370.
21. Li C, Wong WH,. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 2001; 98: 31-36.
22. Witten D, Tibshirani R,. A Comparison of Fold-change and the t-Statistic for Microarray Data Analysis. Stanford University: Stanford, USA, 2007.
23. Langfelder P, Horvath S,. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008; 9: 559.
24. Chiriac MT, Roesler J, Sindrilaru A, et al., NADPH oxidase is required for neutrophil-dependent autoantibody-induced tissue damage. J Pathol 2007; 212: 56-65.
25. Lambeth JD, Kawahara T, Diebold B,. Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 2007; 43: 319-331.
26. Shimanovich I, Mihai S, Oostingh GJ, et al., Granulocyte-derived elastase and gelatinase B are required for dermal-epidermal separation induced by autoantibodies from patients with epidermolysis bullosa acquisita and bullous pemphigoid. J Pathol 2004; 204: 519-527.
27. Mauch C, Krieg T, Bauer EA,. Role of the extracellular matrix in the degradation of connective tissue. Arch Dermatol Res 1994; 287: 107-114.
28. Kähäri VM, Saarialho-Kere U,. Matrix metalloproteinases in skin. Exp Dermatol 1997; 6: 199-213.
29. Sesarman A, Mihai S, Chiriac MT, et al., Binding of avian Igγ to type VII collagen does not activate complement and leucocytes and fails to induce subepidermal blistering in mice. Br J Dermatol 2008; 158: 463-471.
30. Nimmerjahn F, Ravetch JV,. Fcγ receptors as regulators of immune responses. Nat Rev Immunol 2008; 8: 34-47.
31. Sesarman A, Sitaru AG, Olaru F, et al., Neonatal Fc receptor deficiency protects from tissue injury in experimental epidermolysis bullosa acquisita. J Mol Med 2008; 86: 951-959.
32. Baerenwaldt A, Biburger M, Nimmerjahn F,. Mechanisms of action of intravenous immunoglobulins. Expert Rev Clin Immunol 2010; 6: 425-434.
33. Ishii N, Hashimoto T, Zillikens D, et al., High-dose intravenous immunoglobulin (IVIG) therapy in autoimmune skin blistering diseases. Clin Rev Allergy Immunol 2010; 38: 186-195.
34. Yuasa T, Kubo S, Yoshino T, et al., Deletion of Fcγ receptor IIB renders H-2b mice susceptible to collagen-induced arthritis. J Exp Med 1999; 189: 187-194.
35. Blank MC, Stefanescu RN, Masuda E, et al., Decreased transcription of the human FCGR2B gene mediated by the -343 G/C promoter polymorphism and association with systemic lupus erythematosus. Hum Genet 2005; 117: 220-227.
36. Nakamura A, Yuasa T, Ujike A, et al., Fcγ receptor IIB-deficient mice develop Goodpasture's syndrome upon immunization with type IV collagen: a novel murine model for autoimmune glomerular basement membrane disease. J Exp Med 2000; 191: 899-906.
37. Watanabe N, Akikusa B, Park SY, et al., Mast cells induce autoantibody-mediated vasculitis syndrome through tumor necrosis factor production upon triggering Fcγ receptors. Blood 1999; 94: 3855-3863.
38. Baudino L, Nimmerjahn F, Azeredo da Silveira S, et al., Differential contribution of three activating IgG Fc receptors (FcγRI, FcγRIII, and FcγRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. J Immunol 2008; 180: 1948-1953.
39. Giorgini A, Brown HJ, Lock HR, et al., FcγRIII and FcγRIV are indispensable for acute glomerular inflammation induced by switch variant monoclonal antibodies. J Immunol 2008; 181: 8745-8752.
40. Zhao M, Trimbeger ME, Li N, et al., Role of FcRs in animal model of autoimmune bullous pemphigoid. J Immunol 2006; 177: 3398-3405.
41. Nimmerjahn F, Lux A, Albert H, et al., FcγRIV deletion reveals its central role for IgG2a and IgG2b activity in vivo. Proc Natl Acad Sci USA 2010; 107: 19396-19401.
42. Hammers CM, Bieber K, Kalies K, et al., Complement-fixing anti-type VII collagen antibodies are induced in Th1-polarized lymph nodes of epidermolysis bullosa acquisita-susceptible mice. J Immunol 2011; 187: 5043-5050.
43. Pamuk ON, Tsokos GC,. Spleen tyrosine kinase inhibition in the treatment of autoimmune, allergic and autoinflammatory diseases. Arthritis Res Ther 2010; 12: 222.
44. Gupta R, Woodley DT, Chen M,. Epidermolysis bullosa acquisita. Clin Dermatol 2012; 30: 60-69.
45. Chen M, Marinkovich MP, Veis A, et al., Interactions of the amino-terminal noncollagenous (NC1) domain of type VII collagen with extracellular matrix components. A potential role in epidermal-dermal adherence in human skin. J Biol Chem 1997; 272: 14516-14522.
46. Lapiere JC, Chen JD, Iwasaki T, et al., Type VII collagen specifically binds fibronectin via a unique subdomain within the collagenous triple helix. J Invest Dermatol 1994; 103: 637-641.
47. Chen M, Keene DR, Costa FK, et al., The carboxyl terminus of type VII collagen mediates antiparallel dimer formation and constitutes a new antigenic epitope for epidermolysis bullosa acquisita autoantibodies. J Biol Chem 2001; 276: 21649-21655.
48. Zhang B, Horvath S,. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 2005; 4:Article 17.
49. Langfelder P, Zhang B, Horvath S,. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 2008; 24: 719-720.
50. Langfelder P, Horvath S,. Eigengene networks for studying the relationships between co-expression modules. BMC Syst Biol 2007; 1: 54.
51. * Gene Ontology Consortium. The Gene Ontology in 2010: extensions and refinements. Nucleic Acids Res 2010; 38:(database issue): D331-335.
52. Dennis G Jr, Sherman BT, Hosack DA, et al., DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003; 4: P3.
53. von Mering C, Jensen LJ, Kuhn M, et al., STRING 7-recent developments in the integration and prediction of protein interactions. Nucleic Acids Res 2007; 35:(database issue): D358-362.
54. Tan YD, Fornage M, Xu H,. Ranking analysis of F-statistics for microarray data. BMC Bioinformatics 2008; 9: 142.
55. Kalies K, Blessenohl M, Nietsch J, et al., T cell zones of lymphoid organs constitutively express Th1 cytokine mRNA: specific changes during the early phase of an immune response. J Immunol 2006; 176: 741-749.