Repetitive immunization breaks tolerance to type XVII collagen and leads to bullous pemphigoid in mice

Journal of Immunology

Volumn 187, Issue 3, 2011, Pages 1176-1183

  Hirose, Misa ^a   Recke, Andreas ^a   Beckmann, Tina ^a   Shimizu, Atsushi ^b   Ishiko, Akira ^c   Bieber, Katja ^a   Westermann, Jürgen ^a   Zillikens, Detlef ^a   Schmidt, Enno ^a   Ludwig, Ralf J ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TOHO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; COLLAGEN TYPE 17; IMMUNOGLOBULIN E; MEMBRANE PROTEIN; PROTEIN BP180; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BLISTER; BULLOUS PEMPHIGOID; CELL INFILTRATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE MODEL; EOSINOPHIL; FEMALE; IMMUNIZATION; IMMUNOCOMPETENCE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALS; AUTOANTIGENS; BINDING SITES, ANTIBODY; CHEMOTAXIS, LEUKOCYTE; COMPLEMENT ACTIVATION; DISEASE MODELS, ANIMAL; EOSINOPHILS; EPIDERMIS; FEMALE; IMMUNE TOLERANCE; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; NEUTROPHILS; NON-FIBRILLAR COLLAGENS; PEMPHIGOID, BULLOUS; VACCINES, SUBUNIT; VACCINES, SYNTHETIC; VACCINES, VIROSOME;

EID: 80051612982     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100596     Document Type: Article

References (42)

1. Nousari, H. C., and G. J. Anhalt. 1999. Pemphigus and bullous pemphigoid. Lancet 354: 667-672. (Pubitemid 29391440)
2. Di Zenzo, G., G. Marazza, and L. Borradori. 2007. Bullous pemphigoid: physiopathology, clinical features and management. Adv. Dermatol. 23: 257-288.
3. Ujiie, H., A. Shibaki, W. Nishie, and H. Shimizu. 2010. What's new in bullous pemphigoid. J. Dermatol. 37: 194-204.
4. Stanley, J. R., P. Hawley-Nelson, S. H. Yuspa, E. M. Shevach, and S. I. Katz. 1981. Characterization of bullous pemphigoid antigen: a unique basement membrane protein of stratified squamous epithelia. Cell 24: 897-903. (Pubitemid 11071328)
5. Stanley, J. R., T. Tanaka, S. Mueller, V. Klaus-Kovtun, and D. Roop. 1988. Isolation of complementary DNA for bullous pemphigoid antigen by use of patients' autoantibodies. J. Clin. Invest. 82: 1864-1870. (Pubitemid 19054931)
6. Labib, R. S., G. J. Anhalt, H. P. Patel, D. F. Mutasim, and L. A. Diaz. 1986. Molecular heterogeneity of the bullous pemphigoid antigens as detected by immunoblotting. J. Immunol. 136: 1231-1235. (Pubitemid 16156221)
7. Diaz, L. A., H. Ratrie, III, W. S. Saunders, S. Futamura, H. L. Squiquera, G. J. Anhalt, and G. J. Giudice. 1990. Isolation of a human epidermal cDNA corresponding to the 180-kD autoantigen recognized by bullous pemphigoid and herpes gestationis sera. Immunolocalization of this protein to the hemidesmosome. J. Clin. Invest. 86: 1088-1094. (Pubitemid 20370412)
8. Zillikens, D. 1999. Acquired skin disease of hemidesmosomes. J. Dermatol. Sci. 20: 134-154. (Pubitemid 29251589)
9. Zillikens, D., P. A. Rose, S. D. Balding, Z. Liu, M. Olague-Marchan, L. A. Diaz, and G. J. Giudice. 1997. Tight clustering of extracellular BP180 epitopes recognized by bullous pemphigoid autoantibodies. J. Invest. Dermatol. 109: 573-579. (Pubitemid 27433604)
10. Schmidt, E., K. Obe, E. B. Bröcker, and D. Zillikens. 2000. Serum levels of autoantibodies to BP180 correlate with disease activity in patients with bullous pemphigoid. Arch. Dermatol. 136: 174-178. (Pubitemid 30090755)
11. Sitaru, C., E. Schmidt, S. Petermann, L. S. Munteanu, E. B. Bröcker, and D. Zillikens. 2002. Autoantibodies to bullous pemphigoid antigen 180 induce dermal-epidermal separation in cryosections of human skin. J. Invest. Dermatol. 118: 664-671. (Pubitemid 34309987)
12. Liu, Z., L. A. Diaz, J. L. Troy, A. F. Taylor, D. J. Emery, J. A. Fairley, and G. J. Giudice. 1993. A passive transfer model of the organ-specific autoimmune disease, bullous pemphigoid, using antibodies generated against the hemidesmosomal antigen, BP180. J. Clin. Invest. 92: 2480-2488. (Pubitemid 23333558)
13. Yamamoto, K., N. Inoue, R. Masuda, A. Fujimori, T. Saito, S. Imajoh-Ohmi, H. Shinkai, and H. Sakiyama. 2002. Cloning of hamster type XVII collagen cDNA, and pathogenesis of anti-type XVII collagen antibody and complement in hamster bullous pemphigoid. J. Invest. Dermatol. 118: 485-492. (Pubitemid 34227166)
14. Nishie, W., D. Sawamura, M. Goto, K. Ito, A. Shibaki, J. R. McMillan, K. Sakai, H. Nakamura, E. Olasz, K. B. Yancey, et al. 2007. Humanization of autoantigen. Nat. Med. 13: 378-383. (Pubitemid 46376680)
15. Olasz, E. B., J. Roh, C. L. Yee, K. Arita, M. Akiyama, H. Shimizu, J. C. Vogel, and K. B. Yancey. 2007. Human bullous pemphigoid antigen 2 transgenic skin elicits specific IgG in wild-type mice. J. Invest. Dermatol. 127: 2807-2817. (Pubitemid 350134825)
16. Zone, J. J., T. Taylor, C. Hull, L. Schmidt, and L. Meyer. 2007. IgE basement membrane zone antibodies induce eosinophil infiltration and histological blisters in engrafted human skin on SCID mice. J. Invest. Dermatol. 127: 1167-1174. (Pubitemid 46625148)
17. Fairley, J. A., C. T. Burnett, C. L. Fu, D. L. Larson, M. G. Fleming, and G. J. Giudice. 2007. A pathogenic role for IgE in autoimmunity: bullous pemphigoid IgE reproduces the early phase of lesion development in human skin grafted to nu/nu mice. J. Invest. Dermatol. 127: 2605-2611. (Pubitemid 47585071)
18. Liu, Z., W. Sui, M. Zhao, Z. Li, N. Li, R. Thresher, G. J. Giudice, J. A. Fairley, C. Sitaru, D. Zillikens, et al. 2008. Subepidermal blistering induced by human autoantibodies to BP180 requires innate immune players in a humanized bullous pemphigoid mouse model. J. Autoimmun. 31: 331-338.
19. Nishie, W., D. Sawamura, K. Natsuga, S. Shinkuma, M. Goto, A. Shibaki, H. Ujiie, E. Olasz, K. B. Yancey, and H. Shimizu. 2009. A novel humanized neonatal autoimmune blistering skin disease model induced by maternally transferred antibodies. J. Immunol. 183: 4088-4093.
20. Ujiie, H., A. Shibaki, W. Nishie, D. Sawamura, G. Wang, Y. Tateishi, Q. Li, R. Moriuchi, H. Qiao, H. Nakamura, et al. 2010. A novel active mouse model for bullous pemphigoid targeting humanized pathogenic antigen. J. Immunol. 184: 2166-2174.
21. Sitaru, C., S. Mihai, C. Otto, M. T. Chiriac, I. Hausser, B. Dotterweich, H. Saito, C. Rose, A. Ishiko, and D. Zillikens. 2005. Induction of dermal-epidermal separation in mice by passive transfer of antibodies specific to type VII collagen. J. Clin. Invest. 115: 870-878. (Pubitemid 40489391)
22. Ludwig, R. J., A. Recke, K. Bieber, S. Müller, Ade. C. Marques, D. Banczyk, M. Hirose, M. Kasperkiewicz, N. Ishii, E. Schmidt, et al. 2011. Generation of antibodies of distinct subclasses and specificity is linked to H2s in an active mouse model of epidermolysis bullosa acquisita. J. Invest. Dermatol. 131: 167-176.
23. Denzler, K. L., S. C. Farmer, J. R. Crosby, M. Borchers, G. Cieslewicz, K. A. Larson, S. Cormier-Regard, N. A. Lee, and J. J. Lee. 2000. Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J. Immunol. 165: 5509-5517.
24. Sitaru, C., M. T. Chiriac, S. Mihai, J. Büning, A. Gebert, A. Ishiko, and D. Zillikens. 2006. Induction of complement-fixing autoantibodies against type VII collagen results in subepidermal blistering in mice. J. Immunol. 177: 3461-3468. (Pubitemid 44277867)
25. Kasperkiewicz, M., M. Hirose, A. Recke, E. Schmidt, D. Zillikens, and R. J. Ludwig. 2010. Clearance rates of circulating and tissue-bound autoantibodies to type VII collagen in experimental epidermolysis bullosa acquisita. Br. J. Dermatol. 162: 1064-1070.
26. Ishiko, A., and H. Shimizu. 2001. Electron microscopy in diagnosis of autoimmune bullous disorders. Clin. Dermatol. 19: 631-637. (Pubitemid 32927180)
27. Ishiko, A., H. Shimizu, A. Kikuchi, T. Ebihara, T. Hashimoto, and T. Nishikawa. 1993. Human autoantibodies against the 230-kD bullous pemphigoid antigen (BPAG1) bind only to the intracellular domain of the hemidesmosome, whereas those against the 180-kD bullous pemphigoid antigen (BPAG2) bind along the plasma membrane of the hemidesmosome in normal human and swine skin. J. Clin. Invest. 91: 1608-1615. (Pubitemid 23127364)
28. Dvorak, A. M., M. C. Mihm, Jr., J. E. Osage, T. H. Kwan, K. F. Austen, and B. U. Wintroub. 1982. Bullous pemphigoid, an ultrastructural study of the inflammatory response: eosinophil, basophil and mast cell granule changes in multiple biopsies from one patient. J. Invest. Dermatol. 78: 91-101. (Pubitemid 12165736)
29. Chan, L. S., C. J. Vanderlugt, T. Hashimoto, T. Nishikawa, J. J. Zone, M. M. Black, F. Wojnarowska, S. R. Stevens, M. Chen, J. A. Fairley, et al. 1998. Epitope spreading: lessons from autoimmune skin diseases. J. Invest. Dermatol. 110: 103-109. (Pubitemid 28105841)
30. Perriard, J., F. Jaunin, B. Favre, L. Büdinger, M. Hertl, J. H. Saurat, and L. Borradori. 1999. IgG autoantibodies from bullous pemphigoid (BP) patients bind antigenic sites on both the extracellular and the intracellular domains of the BP antigen 180. J. Invest. Dermatol. 112: 141-147. (Pubitemid 29061967)
31. Yamada, H., T. Hashimoto, and T. Nishikawa. 1989. IgG subclasses of intercellular and basement membrane zone antibodies: the relationship to the capability of complement fixation. J. Invest. Dermatol. 92: 585-587. (Pubitemid 19122113)
32. Arbesman, C. E., J. I. Wypych, R. E. Reisman, and E. H. Beutner. 1974. IgE levels in sera of patients with pemphigus or bullous pemphigoid. Arch. Dermatol. 110: 378-381.
33. Watanabe, N., S. Kojima, and Z. Ovary. 1976. Suppression of IgE antibody production in SJL mice. I. Nonspecific suppressor T cells. J. Exp. Med. 143: 833-845.
34. Yoshimoto, T., A. Bendelac, J. Hu-Li, and W. E. Paul. 1995. Defective IgE production by SJL mice is linked to the absence of CD4+, NK1.1+ T cells that promptly produce interleukin 4. Proc. Natl. Acad. Sci. USA 92: 11931-11934. (Pubitemid 26014224)
35. Provost, T. T., and T. B. Tomasi Jr. 1974. Immunopathology of bullous pemphigoid. Basement membrane deposition of IgE, alternate pathway components and fibrin. Clin. Exp. Immunol. 18: 193-200.
36. Parodi, A., and A. Rebora. 1992. Serum IgE antibodies bind to the epidermal side of the basement membrane zone splits in bullous pemphigoid. Br. J. Dermatol. 126: 526-527.
37. Okazaki, A., S. Miyagawa, Y. Yamashina, W. Kitamura, and T. Shirai. 2000. Polymorphisms of HLA-DR and -DQ genes in Japanese patients with bullous pemphigoid. J. Dermatol. 27: 149-156. (Pubitemid 30202170)
38. Weisenseel, P., S. Martin, K. Partscht, G. Messer, and J. C. Prinz. 2007. Relevance of the low-affinity type of the Fcgamma-receptor IIIa-polymorphism in bullous pemphigoid. Arch. Dermatol. Res. 299: 163-164. (Pubitemid 46835384)
39. Guilabert, A., F. Lozano, P. Iranzo, M. Julià, B. Suárez-Casasús, N. Moreno, J. Herrero-Gonzalez, and J. M. Mascaró Jr. 2010. The role of Fc gamma receptors polymorphisms in bullous pemphigoid. J. Am. Acad. Dermatol. 63: 161-163.
40. Petkova, S. B., R. Yuan, S. W. Tsaih, W. Schott, D. C. Roopenian, and B. Paigen. 2008. Genetic influence on immune phenotype revealed strain-specific variations in peripheral blood lineages. Physiol. Genomics 34: 304-314. (Pubitemid 352758845)
41. Palaszynski, K. M., K. K. Loo, J. F. Ashouri, H. B. Liu, and R. R. Voskuhl. 2004. Androgens are protective in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. J. Neuroimmunol. 146: 144-152. (Pubitemid 38032966)
42. Du, C., M. W. Khalil, and S. Sriram. 2001. Administration of dehydroepiandrosterone suppresses experimental allergic encephalomyelitis in SJL/J mice. J. Immunol. 167: 7094-7101. (Pubitemid 33144206)