Mechanisms of blister induction by autoantibodies

Experimental Dermatology

Volumn 14, Issue 12, 2005, Pages 861-875

  Sitaru, Cassian ^a   Zillikens, Detlef ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Adhesion molecule; Complement; Leucocytes; Signal transduction; Steric hindrance

Indexed keywords

AUTOANTIBODY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ACANTHOLYSIS; AMINO TERMINAL SEQUENCE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; BULLOUS SKIN DISEASE; CELL ADHESION; CELL CULTURE; COMPLEMENT ACTIVATION; DERMATITIS HERPETIFORMIS; EPIDERMOLYSIS BULLOSA ACQUISITA; HISTOPATHOLOGY; HUMAN; INNATE IMMUNITY; KERATINOCYTE; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PATHOGENESIS; PEMPHIGUS; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION;

AUTOANTIBODIES; AUTOANTIGENS; BLISTER; HUMANS; PEMPHIGUS; SKIN DISEASES, VESICULOBULLOUS;

EID: 28444460336     PISSN: 09066705     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2005.00367.x     Document Type: Review

References (161)

1. Witebsky E, Rose N R, Terplan K, Paine J R, Egan R W. Chronic thyroiditis and autoimmunization. J Am Med Assoc 1957: 164: 1439-1447.
2. Rose N R, Bona C. Defining criteria for autoimmune diseases (Witebsky's postulates revisited). Immunol Today 1993: 14: 426-430.
3. Manz R A, Hauser A E, Hiepe F, Radbruch A. Maintenance of serum antibody levels. Annu Rev Immunol 2005: 23: 367-386.
4. Wentworth P Jr, McDunn J E, Wentworth A D et al. Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation. Science 2002: 298: 2195-2199.
5. Wentworth A D, Jones L H, Wentworth P Jr, Janda K D, Lerner R A. Antibodies have the intrinsic capacity to destroy antigens. Proc Natl Acad Sci USA 2000: 97: 10930-10935.
6. Zhu X, Wentworth P Jr, Wentworth A D, Eschenmoser A, Lerner R A, Wilson I A. Probing the antibody-catalyzed water-oxidation pathway at atomic resolution. Proc Natl Acad Sci USA 2004: 101: 2247-2252.
7. Beutner E H, Jordon R E. Demonstration of skin antibodies in serum of pemphigus vulgaris patients by indirect immunofluorescence staining. Proc Soc Exp Biol Med 1964: 117: 505-510.
8. Beutner E H, Lever W F, Witebsky E. Autoantibodies in pemphigus vulgaris. Response to an intercellular substance of epidermis. JAMA 1965: 92: 682-688.
9. Beutner E H, Rhodes E L, Holborow E J. Autoimmunity in chronic bullous skin diseases. Immunofluorescent demonstration of three types of antibodies to skin in sera of patients with pemphigus, bullous pemphigoid and in other human sera. Clin Exp Immunol 1967: 2: 141-151.
10. Jordon R E, Beutner E H, Witebsky E, Blumental G, Hale W L, Lever W F. Basement zone antibodies in bullous pemphigoid. Jama 1967: 200: 751-756.
11. Chorzelski T P, Jablonska S, Beutner E H, Maciejowska E, Jarzabek-Chorzelska M. Herpes gestations with identical lesions in the newborn. Passive transfer of the disease? Arch Dermatol 1976: 112: 1129-1131.
12. Katz A, Minto J O, Toole J W, Medwidsky W. Immunopathologic study of herpes gestationis in mother and infant. Arch Dermatol 1977: 113: 1069-1072.
13. Moncada B, Kettelsen S, Hernandez-Moctezuma J L, Ramirez F. Neonatal pemphigus vulgaris: role of passively transferred pemphigus antibodies. Br J Dermatol 1982: 106: 465-467.
14. Wasserstrum N, Laros R K Jr. Transplacental transmission of pemphigus. JAMA 1983: 249: 1480-1482.
15. Hup J M, Bruinsma R A, Boersma E R. de Jong M C. Neonatal pemphigus vulgaris: transplacental transmission of antibodies. Pediatr Dermatol 1986: 3: 468-472.
16. Ruach M, Ohel G, Rahav D, Samueloff A. Pemphigus vulgaris and pregnancy. Obstet Gynecol Surv 1995: 50: 755-760.
17. Chowdhury M M, Natarajan S. Neonatal pemphigus vulgaris associated with mild oral pemphigus vulgaris in the mother during pregnancy. Br J Dermatol 1998: 139: 500-503.
18. Chen S H, Chopra K, Evans T Y, Raimer S S, Levy M L, Tyring S K. Herpes gestationis in a mother and child. J Am Acad Dermatol 1999: 40: 847-849.
19. Rocha-Alvarez R, Friedman H, Campbell I T, Souza-Aguiar L, Martins-Castro R, Diaz L A. Pregnant women with endemic pemphigus foliaceus (Fogo Selvagem) give birth to disease-free babies. J Invest Dermatol 1992: 99: 78-82.
20. Wu H, Wang Z H, Yan A et al. Protection against pemphigus foliaceus by desmoglein 3 in neonates [see comments]. N Engl J Med 2000: 343: 31-35.
21. Veldman C, Stauber A, Wassmuth R, Uter W, Schuler G, Hertl M. Dichotomy of autoreactive Th1 and Th2 cell responses to desmoglein 3 in patients with pemphigus vulgaris (PV) and healthy carriers of PV-associated HLA class II alleles. J Immunol 2003: 170: 635-642.
22. Veldman C M, Gebhard K L, Uter W et al. T cell recognition of desmoglein 3 peptides in patients with pemphigus vulgaris and healthy individuals. J Immunol 2004: 172: 3883-3892.
23. Gebhard K L, Veldman C M, Wassmuth R, Schultz E, Schuler G, Hertl M. Ex vivo analysis of desmoglein 1-responsive T-helper (Th) 1 and Th2 cells in patients with pemphigus foliaceus and healthy individuals. Exp Dermatol 2005: 14: 586-592.
24. Schiltz J R, Michel B. Production of epidermal acantholysis in normal human skin in vitro by the IgG fraction from pemphigus serum. J Invest Dermatol 1976: 67: 254-260.
25. Schiltz J R, Michel B, Papay R. Pemphigus antibody interaction with human epidermal cells in culture. J Clin Invest 1978: 62: 778-788.
26. Hu C H, Michel B, Schiltz J R. Epidermal acantholysis induced in vitro by pemphigus autoantibody. An ultrastructural study. Am J Pathol 1978: 90: 345-361.
27. Schiltz J R, Michel B, Papay R. Appearance of 'pemphigus acantholysis factor' in human skin cultured with pemphigus antibody. J Invest Dermatol 1979: 73: 575-581.
28. Schiltz J R, Hu C H, Michel B. Corticosteroids, aurothioglucose and soybean trypsin inhibitor do not prevent pemphigus antibody-induced acantholysis in vitro. Br J Dermatol 1979: 101: 279-284.
29. Schiltz J R. Pemphigus acantholysis: a unique immunological injury. J Invest Dermatol 1980: 74: 359-362.
30. Anhalt G J, Labib R S, Voorhees J J, Beals T F, Diaz L A. Induction of pemphigus in neonatal mice by passive transfer of IgG from patients with the disease. N Engl J Med 1982: 306: 1189-1196.
31. Takahashi Y, Patel H P, Labib R S, Diaz L A, Anhalt G J. Experimentally induced pemphigus vulgaris in neonatal BALB/c mice: a time-course study of clinical, immunologic, ultrastructural, and cytochemical changes. J Invest Dermatol 1985: 84: 41-46.
32. Roscoe J T, Diaz L, Sampaio S A et al. Brazilian pemphigus foliaceus autoantibodies are pathogenic to BALB/c mice by passive transfer. J Invest Dermatol 1985: 85: 538-541.
33. Futamura S, Martins C, Rivitti E A, Labib R S, Diaz L A, Anhalt G J. Ultrastructural studies of acantholysis induced in vivo by passive transfer of IgG from endemic pemphigus foliaceus (Fogo Selvagem). J Invest Dermatol 1989: 93: 480-485.
34. Anhalt G J, Kim S C, Stanley J R et al. Paraneoplastic pemphigus. An autoimmune mucocutaneous disease associated with neoplasia. N Engl J Med 1990: 323: 1729-1735.
35. Jordon R E, Schroeter A L, Rogers R S D, Perry H O. Classical and alternate pathway activation of complement in pemphigus vulgaris lesions. J Invest Dermatol 1974: 63: 256-259.
36. Jordon R E. Complement activation in bullous skin diseases. J Invest Dermatol 1975: 65: 162-169.
37. Hashimoto T, Nishikawa T, Kurihara S, Hatano H. Complement-fixing pemphigus antibodies. Arch Dermatol 1978: 114: 1191-1192.
38. Hashimoto K, Shafran K M, Webber P S, Lazarus G S, Singer K H. Anti-cell surface pemphigus autoantibody stimulates plasminogen activator activity of human epidermal cells. A mechanism for the loss of epidermal cohesion and blister formation. J Exp Med 1983: 157: 259-272.
39. Hashimoto K, Wun T C, Baird J, Lazarus G S, Jensen P J. Characterization of keratinocyte plasminogen activator inhibitors and demonstration of the prevention of pemphigus IgG-induced acantholysis by a purified plasminogen activator inhibitor. J Invest Dermatol 1989: 92: 310-314.
40. Anhalt G J, Till G O, Diaz L A, Labib R S, Patel H P, Eaglstein N F. Defining the role of complement in experimental pemphigus vulgaris in mice. J Immunol 1986: 137: 2835-2840.
41. Rock B, Labib R S, Diaz L A. Monovalent Fab immunoglobulin fragments from endemic pemphigus foliaceus autoantibodies reproduce the human disease in neonatal Balb/c mice. J Clin Invest 1990: 85: 296-299.
42. Mascaro J M Jr, Espana A, Liu Z et al. Mechanisms of acantholysis in pemphigus vulgaris: role of IgG valence. Clin Immunol Immunopathol 1997: 85: 90-96.
43. Payne A S, Ishii K, Kacir S et al. Genetic and functional characterization of human pemphigus vulgaris monoclonal autoantibodies isolated by phage display. J Clin Invest 2005: 115: 888-899.
44. Rock B, Martins C R, Theofilopoulos A N et al. The pathogenic effect of IgG4 autoantibodies in endemic pemphigus foliaceus (fogo selvagem). N Engl J Med 1989: 320: 1463-1469.
45. Hacker-Foegen M K, Janson M, Amagai M, Fairley J A, Lin M S. Pathogenicity and epitope characteristics of anti-desmoglein-1 from pemphigus foliaceus patients expressing only IgG1 autoantibodies. J Invest Dermatol 2003: 121: 1373-1378.
46. Eyre R W, Stanley J R. Human autoantibodies against a desmosomal protein complex with a calcium-sensitive epitope are characteristic of pemphigus foliaceus patients. J Exp Med 1987: 165: 1719-1724.
47. Eyre R W, Stanley J R. Identification of pemphigus vulgaris antigen extracted from normal human epidermis and comparison with pemphigus foliaceus antigen. J Clin Invest 1988: 81: 807-812.
48. Amagai M, Klaus-Kovtun V, Stanley J R. Autoantibodies against a novel epithelial cadherin in pemphigus vulgaris, a disease of cell adhesion. Cell 1991: 67: 869-877.
49. Kljuic A, Bazzi H, Sundberg J P et al. Desmoglein 4 in hair follicle differentiation and epidermal adhesion: evidence from inherited hypotrichosis and acquired pemphigus vulgaris. Cell 2003: 113: 249-260.
50. Nguyen V T, Ndoye A, Grando S A. Pemphigus vulgaris antibody identifies pemphaxin. A novel keratinocyte annexin-like molecule binding acetylcholine. J Biol Chem 2000: 275: 29466-29476.
51. Nguyen V T, Ndoye A, Grando S A. Novel human alpha9 acetylcholine receptor regulating keratinocyte adhesion is targeted by pemphigus vulgaris autoimmunity. Am J Pathol 2000: 157: 1377-1391.
52. Amagai M, Karpati S, Prussick R, Klaus-Kovtun V, Stanley J R. Autoantibodies against the amino-terminal cadherin-like binding domain of pemphigus vulgaris antigen are pathogenic. J Clin Invest 1992: 90: 919-926.
53. Bhol K, Natarajan K, Nagarwalla N, Mohimen A, Aoki V, Ahmed A R. Correlation of peptide specificity and IgG subclass with pathogenic and nonpathogenic autoantibodies in pemphigus vulgaris: a model for autoimmunity. Proc Natl Acad Sci USA 1995: 92: 5239-5243.
54. Amagai M, Hashimoto T, Shimizu N, Nishikawa T. Absorption of pathogenic autoantibodies by the extracellular domain of pemphigus vulgaris antigen (Dsg3) produced by baculovirus. J Clin Invest 1994: 94: 59-67.
55. Amagai M, Hashimoto T, Green K J, Shimizu N, Nishikawa T. Antigen-specific immunoadsorption of pathogenic autoantibodies in pemphigus foliaceus. J Invest Dermatol 1995: 104: 895-901.
56. Amagai M, Nishikawa T, Nousari H C, Anhalt G J, Hashimoto T. Antibodies against desmoglein 3 (pemphigus vulgaris antigen) are present in sera from patients with paraneoplastic pemphigus and cause acantholysis in vivo in neonatal mice. J Clin Invest 1998: 102: 775-782.
57. Nguyen V T, Ndoye A, Shultz L D, Pittelkow M R, Grando S A. Antibodies against keratinocyte antigens other than desmogleins 1 and 3 can induce pemphigus vulgaris-like lesions. J Clin Invest 2000: 106: 1467-1479.
58. Grando S A, Pittelkow M R, Shultz L D, Dmochowski M, Nguyen V T. Pemphigus: an unfolding story. J Invest Dermatol 2001: 117: 990-995.
59. Nagasaka T, Nishifuji K, Ota T, Whittock N V, Amagai M. Defining the pathogenic involvement of desmoglein 4 in pemphigus and staphylococcal scalded skin syndrome. J Clin Invest 2004: 114: 1484-1492.
60. Juhasz I, Lazarus G S, Murphy G F, Shih I M, Herlyn M. Development of pemphigus vulgaris-like lesions in severe combined immunodeficiency disease mice reconstituted with lymphocytes from patients. J Clin Invest 1993: 92: 2401-2407.
61. Radisch T, Riechers R, Hertl M. The humanized SCID mouse model to study HLA class II-linked autoimmunity to desmoglein 3 in pemphigus vulgaris. Br J Dermatol 2002: 146: 189-193.
62. Fan J L, Memar O, McCormick D J, Prabhakar B S. BALB/c mice produce blister-causing antibodies upon immunization with a recombinant human desmoglein 3. J Immunol 1999: 163: 6228-6235.
63. Kaithamana S, Fan J L, Memar O, Uitto J, Seetharamaiah G S, Prabhakar B S. Relevance of differential immunogenicity of human and mouse recombinant desmoglein-3 for the induction of acantholytic autoantibodies in mice. Clin Exp Immunol 2003: 132: 16-23.
64. Amagai M, Tsunoda K, Suzuki H, Nishifuji K, Koyasu S, Nishikawa T. Use of autoantigen-knockout mice in developing an active autoimmune disease model for pemphigus. J Clin Invest 2000: 105: 625-631.
65. Ohyama M, Amagai M, Tsunoda K et al. Immunologic and histopathologic characterization of an active disease mouse model for pemphigus vulgaris. J Invest Dermatol 2002: 118: 199-204.
66. Tsunoda K, Ota T, Suzuki H et al. Pathogenic autoantibody production requires loss of tolerance against desmoglein 3 in both T and B cells in experimental pemphigus vulgaris. Eur J Immunol 2002: 32: 627-633.
67. Liu Z, Li N, Diaz L A. Immunopathological mechanisms of acantholysis in pemphigus vulgaris: an explanation by ultrastructural observations. J Invest Dermatol 2004: 122: XIII-XIV.
68. Schaefer B M, Jaeger C J, Kramer M D. Plasminogen activator system in pemphigus vulgaris. Br J Dermatol 1996: 135: 726-732.
69. Feliciani C, Toto P, Wang B, Sauder D N, Amerio P, Tulli A. Urokinase plasminogen activator mRNA is induced by IL-1alpha and TNF-alpha in in vitro acantholysis. Exp Dermatol 2003: 12: 466-471.
70. Anhalt G J, Patel H P, Labib R S, Diaz L A, Proud D. Dexamethasone inhibits plasminogen activator activity in experimental pemphigus in vivo but does not block acantholysis. J Immunol 1986: 136: 113-117.
71. Schuh T, Besch R, Braungart E et al. Protease inhibitors prevent plasminogen-mediated, but not pemphigus, vulgaris-induced, acantholysis in human epidermis. Biol Chem 2003: 384: 311-315.
72. Mahoney M G, Wang Z H, Stanley J R. Pemphigus vulgaris and pemphigus foliaceus antibodies are pathogenic in plasminogen activator knockout mice. J Invest Dermatol 1999: 113: 22-25.
73. Patel H P, Diaz L A, Anhalt G J, Labib R S, Takahashi Y. Demonstration of pemphigus antibodies on the cell surface of murine epidermal cell monolayers and their internalization. J Invest Dermatol 1984: 83: 409-415.
74. Karpati S, Amagai M, Prussick R, Cehrs K, Stanley J R. Pemphigus vulgaris antigen, a desmoglein type of cadherin, is localized within keratinocyte desmosomes. J Cell Biol 1993: 122: 409-415.
75. Kitajima Y, Inoue S, Yaoita H. Effects of pemphigus antibody on the regeneration of cell-cell contact in keratinocyte cultures grown in low to normal Ca++ concentration. J Invest Dermatol 1987: 89: 167-171.
76. Esaki C, Seishima M, Yamada T, Osada K, Kitajima Y. Pharmacologic evidence for involvement of phospholipase C in pemphigus IgG-induced inositol 1,4,5-trisphosphate generation, intracellular calcium increase, and plasminogen activator secretion in DJM-1 cells, a squamous cell carcinoma line. J Invest Dermatol 1995: 105: 329-333.
77. Osada K, Seishima M, Kitajima Y. Pemphigus IgG activates and translocates protein kinase C from the cytosol to the particulate/cytoskeleton fractions in human keratinocytes. J Invest Dermatol 1997: 108: 482-487.
78. Kitajima Y, Aoyama Y, Seishima M. Transmembrane signaling for adhesive regulation of desmosomes and hemidesmosomes, and for cell-cell detachment induced by pemphigus IgG in cultured keratinocytes: involvement of protein kinase C. J Investig Dermatol Symp Proc 1999: 4: 137-144.
79. Berkowitz P, Hu P, Liu Z et al. Desmosome signaling. Inhibition of p38MAPK prevents pemphigus vulgaris IgG-induced cytoskeleton reorganization. J Biol Chem 2005: 280: 23778-23784.
80. Sanchez-Carpintero I, Espana A, Pelacho B et al. In vivo blockade of pemphigus vulgaris acantholysis by inhibition of intracellular signal transduction cascades. Br J Dermatol 2004: 151: 565-570.
81. Muller E, Caldelari R, De Bruin A et al. Pathogenesis in pemphigus vulgaris: a central role for the armadillo protein plakoglobin. J Invest Dermatol 2000: 115: 332.
82. Caldelari R, de Bruin A, Baumann D et al. A central role for the armadillo protein plakoglobin in the autoimmune disease pemphigus vulgaris. J Cell Biol 2001: 153: 823-834.
83. Wang X, Bregegere F, Frusic-Zlotkin M, Feinmesser M, Michel B, Milner Y. Possible apoptotic mechanism in epidermal cell acantholysis induced by pemphigus vulgaris autoimmunoglobulins. Apoptosis 2004: 9: 131-143.
84. Sekiguchi M, Futei Y, Fujii Y, Iwasaki T, Nishikawa T, Amagai M. Dominant autoimmune epitopes recognized by pemphigus antibodies map to the n-terminal adhesive region of desmogleins. J Immunol 2001: 167: 5439-5448.
85. Tsunoda K, Ota T, Aoki M et al. Induction of pemphigus phenotype by a mouse monoclonal antibody against the amino-terminal adhesive interface of desmoglein 3. J Immunol 2003: 170: 2170-2178.
86. Shimizu A, Ishiko A, Ota T, Tsunoda K, Amagai M, Nishikawa T. IgG binds to desmoglein 3 in desmosomes and causes a desmosomal split without keratin retraction in a pemphigus mouse model. J Invest Dermatol 2004: 122: 1145-1153.
87. Hashimoto T. Immunopathology of IgA pemphigus. Clin Dermatol 2001: 19: 683-689.
88. Hashimoto T, Kiyokawa C, Mori O et al. Human desmocollin 1 (Dsc1) is an autoantigen for the subcorneal pustular dermatosis type of IgA pemphigus. J Invest Dermatol 1997: 109: 127-131.
89. Hashimoto T, Komai A, Futei Y, Nishikawa T, Amagai M. Detection of IgA autoantibodies to desmogleins by an enzyme-linked immunosorbent assay: the presence of new minor subtypes of IgA pemphigus. Arch Dermatol 2001: 137: 735-738.
90. Prost C, Intrator L, Wechsler J et al. IgA autoantibodies bind to pemphigus vulgaris antigen in a case of intraepidermal neutrophilic IgA dermatosis. J Am Acad Dermatol 1991: 25: 846-848.
91. Wang J, Kwon J, Ding X, Fairley J A, Woodley D T, Chan L S. Nonsecretory IgA1 autoantibodies targeting desmosomal component desmoglein 3 in intraepidermal neutrophilic IgA dermatosis. Am J Pathol 1997: 150:1901-1907.
92. Karpati S, Amagai M, Liu W L, Dmochowski M, Hashimoto T, Horvath A. Identification of desmoglein 1 as autoantigen in a patient with intraepidermal neutrophilic IgA dermatosis type of IgA pemphigus. Exp Dermatol 2000: 9: 224-228.
93. Supapannachart N, Mutasim D F. The distribution of IgA pemphigus antigen in human skin and the role of IgA anti-cell surface antibodies in the induction of intraepidermal acantholysis. Arch Dermatol 1993: 129: 605-608.
94. Domloge-Hultsch N, Gammon W R, Briggaman R A, Gil S G, Carter W G, Yancey K B. Epiligrin, the major human keratinocyte integrin ligand, is a target in both an acquired autoimmune and an inherited subepidermal blistering skin disease. J Clin Invest 1992: 90: 1628-1633.
95. Lazarova Z, Sitaru C, Zillikens D, Yancey K B. Comparative analysis of methods for detection of anti-laminin 5 autoantibodies in patients with anti-epiligrin cicatricial pemphigoid. J Am Acad Dermatol 2004: 51: 886-892.
96. Lazarova Z, Yee C, Darling T, Briggaman R A, Yancey K B. Passive transfer of anti-laminin 5 antibodies induces subepidermal blisters in neonatal mice. J Clin Invest 1996: 98: 1509-1518.
97. Lazarova Z, Hsu R, Briggaman R A, Yancey K B. Fab fragments directed against laminin 5 induce subepidermal blisters in neonatal mice. Clin Immunol 2000: 95: 26-32.
98. Hsu R, Lazarova Z, Yee C, Yancey K B. Noncomplement fixing, IgG4 autoantibodies predominate in patients with anti-epiligrin cicatricial pemphigoid. J Invest Dermatol 1997: 109: 557-561.
99. Lazarova Z, Hsu R, Yee C, Yancey K B. Human antilaminin 5 autoantibodies induce subepidermal blisters in an experimental human skin graft model. J Invest Dermatol 2000: 114: 178-184.
100. Shimanovich I, Mihai S, Oostingh G J 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.
101. Murakami H, Nishioka S, Setterfield J et al. Analysis of antigens targeted by circulating IgG and IgA autoantibodies in 50 patients with cicatricial pemphigoid. J Dermatol Sci 1998: 17: 39-44.
102. Schmidt E, Skrobek C, Kromminga A et al. Cicatricial pemphigoid: IgA and IgG autoantibodies target epitopes on both intra- and extracellular domains of bullous pemphigoid antigen 180. Br J Dermatol 2001: 145: 778-783.
103. Setterfield J, Shirlaw P J, Kerr-Muir M et al. Mucous membrane pemphigoid: a dual circulating antibody response with IgG and IgA signifies a more severe and persistent disease. Br J Dermatol 1998: 138: 602-610.
104. Tyagi S, Bhol K, Natarajan K, Livir-Rallatos C, Foster C S, Ahmed A R. Ocular cicatricial pemphigoid antigen: partial sequence and biochemical characterization. Proc Natl Acad Sci USA 1996: 93: 14714-14719.
105. Bhol K C, Dans M J, Simmons R K, Foster C S, Giancotti F G, Ahmed A R. The autoantibodies to alpha 6 beta 4 integrin of patients affected by ocular cicatricial pemphigoid recognize predominantly epitopes within the large cytoplasmic domain of human beta 4. J Immunol 2000: 165: 2824-2829.
106. Bhol K C, Goss L, Kumari S, Colon J E, Ahmed A R. Autoantibodies to alpha 6 integrin in patients with oral pemphigoid. J Dent Res 2001: 80: 1711-1715.
107. Kumari S, Bhol K C, Simmons R K et al. Identification of ocular cicatricial pemphigoid antibody binding site(s) in human beta4 integrin. Invest Ophthalmol Vis Sci 2001: 42: 379-385.
108. Chan R Y, Bhol K, Tesavibul N et al. The role of antibody to human beta4 integrin in conjunctival basement membrane separation: possible in vitro model for ocular cicatricial pemphigoid. Invest Ophthalmol Vis Sci 1999: 40: 2283-2290.
109. Colon J E, Bhol K C, Razzaque M S, Ahmed A R. In vitro organ culture model for mucous membrane pemphigoid. Clin Immunol 2001: 98: 229-234.
110. Sams W M Jr, Gleich G J. Failure to transfer bullous pemphigoid with serum from patients. Proc Soc Exp Biol Med 1971: 136: 1027-1031.
111. Anhalt G J, Bahn C F, Labib R S, Voorhees J J, Sugar A, Diaz L A. Pathogenic effects of bullous pemphigoid autoantibodies on rabbit corneal epithelium. J Clin Invest 1981: 68: 1097-1101.
112. Gammon W R, Merritt C C, Lewis D M, Sams W M Jr, Wheeler C E Jr, Carlo J. Leukocyte chemotaxis to the dermal-epidermal junction of human skin mediated by pemphigoid antibody and complement: mechanism of cell attachment in the in vitro leukocyte attachment method. J Invest Dermatol 1981: 76: 514-522.
113. Gammon W R, Merritt C C, Lewis D M, Sams W M, Carlo J R, Wheeler C E. An in vitro model of immune complex-mediated basement membrane zone separation caused by pemphigoid antibodies, leukocytes, and complement. J Invest Dermatol 1982: 78: 285-290.
114. Naito K, Morioka S, Ogawa H. The pathogenic mechanisms of blister formation in bullous pemphigoid. J Invest Dermatol 1982: 79: 303-306.
115. Pehamberger H, Gschnait F, Konrad K, Holubar K. Bullous pemphigoid, herpes gestationis and linear dermatitis herpetiformis: circulating anti-basement membrane zone antibodies; in vitro studies. J Invest Dermatol 1980: 74: 105-108.
116. Naito K, Morioka S, Ikeda S, Ogawa H. Experimental bullous pemphigoid in guinea pigs: the role of pemphigoid antibodies, complement, and migrating cells. J Invest Dermatol 1984: 82: 227-230.
117. Gammon W R, Briggaman R A. Absence of specific histologic changes in guinea pig skin treated with bullous pemphigoid antibodies. J Invest Dermatol 1988: 90: 495-500.
118. Anhalt G J, Diaz L A. Animal models for bullous pemphigoid. Clin Dermatol 1987: 5: 117-125.
119. Mitsuhashi Y, Takahashi M, Kiuchi H, Mikami H, Hashimoto I, Katabira Y. Induction of pemphigoid lesions in neonatal mice. J Dermatol 1986: 13: 259-265.
120. Zillikens D, Schmidt E, Reimer S et al. Antibodies to desmogleins 1 and 3, but not to BP180, induce blisters in human skin grafted onto SCID mice. J Pathol 2001: 193: 117-124.
121. Stanley J R, Hawley-Nelson P, Yuspa S H, Shevach E M, Katz S I. Characterization of bullous pemphigoid antigen: a unique basement membrane protein of stratified squamous epithelia. Cell 1981: 24: 897-903.
122. Diaz L A, Ratrie H D, Saunders W S et al. 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 1990: 86: 1088-1094.
123. Labib R S, Anhalt G J, Patel H P, Mutasim D F, Diaz L A. Molecular heterogeneity of the bullous pemphigoid antigens as detected by immunoblotting. J Immunol 1986: 136: 1231-1235.
124. Giudice G J, Emery D J, Diaz L A. Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 1992: 99: 243-250.
125. Sitaru C, Schmidt E, Petermann S, Munteanu S L, Bröcker E B, Zillikens D. Autoantibodies to bullous pemphigoid antigen 180 induce dermal-epidermal separation in cryosections of human skin. J Invest Dermatol 2002: 118: 664-671.
126. Herrero-González J E, Brauns O, Egner R et al. Immunoadsorption against two distinct epitopes on human type XVII collagen abolishes dermal-epidermal separation induced by autoantibodies from pemphigoid gestationis patients. J Invest Dermatol 2005: 125: A13.
127. Liu Z, Diaz L A, Troy J L et al. A passive transfer model of the organ-specific autoinumme disease, bullous pemphigoid, using antibodies generated against the hemidesmosomal antigen, BP180. J Clin Invest 1993: 92: 2480-2488.
128. Liu Z, Diaz L A, Swartz S J, Troy J L, Fairley J A, Giudice G J. Molecular mapping of a pathogenically relevant BP180 epitope associated with experimentally induced murine bullous pemphigoid. J Immunol 1995: 155: 5449-5454.
129. Chen R, Ning G, Zhao M L et al. Mast cells play a key role in nentrophil recruitment in experimental bullous pemphigoid. J Clin Invest 2001: 108: 1151-1158.
130. Chen R, Fairley J A, Zhao M L et al. Macrophages, but not T and B lymphocytes, are critical for subepidermal blister formation in experimental bullous pemphigoid: macrophage-mediated neutrophil activation depends on mast cell activation. J Immunol 2002: 169: 3987-3992.
131. Liu Z, Giudice G J, Zhou X et al. A major role for neutrophils in experimental bullous pemphigoid. J Clin Invest 1997: 100: 1256-1263.
132. Liu Z, Shipley J M, Vu T H et al. Gelatinase B-deficient mice are resistant to experimental bullous pemphigoid. J Exp Med 1998: 188: 475-482.
133. Liu Z, Shapiro S D, Zhou X et al. A critical role for neutrophil elastase in experimental bullous pemphigoid. J Clin Invest 2000: 105: 113-123.
134. Liu Z, Zhou X, Shapiro S D et al. The serpin alpha 1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 2000: 102: 647-655.
135. Yamamoto K, Inoue N, Masuda R et al. Cloning of hamster type XVII collagen cDNA, and pathogenesis of anti-type XVII collagen antibody and complement in hamster bullous pemphigoid. J Invest Dermatol 2002: 118: 485-492.
136. Xu L, Robinson N D, Miller S D, Chan L S. Characterization of BALB/c mice B lymphocyte autoimmune response to skin basement membrane component type XVII collagen, the target antigen of the autoimmune skin disease bullous pemphigoid. Immunol Lett 2000: 77: 105-111.
137. Hall R P D, Murray J C, McCord M M, Rico M J, Streilein R D. Rabbits immunized with a peptide encoded for by the 230-kD bullous pemphigoid antigen cDNA develop an enhanced inflammatory response to U-VB irradiation: a potential animal model for bullous pemphigoid. J Invest Dermatol 1993: 101: 9-14.
138. Kiss M, Husz S, Janossy T et al. Experimental bullous pemphigoid generated in mice with an antigenic epitope of the human hemidesmosomal protein BP230. J Autoimmun 2005: 24: 1-10.
139. Woodley D T, Briggaman R A, O'Keefe E J, Inman A O, Queen L L, Gammon W R. Identification of the skin basement-membrane autoantigen in epidermolysis bullosa acquisita. N Engl J Med 1984: 310: 1007-1013.
140. Sitaru C, Kromminga A, Hashimoto T, Bröcker E B, Zillikens D. Autoantibodies to type VII collagen mediate Fcgamma-dependent granulocyte activation and induce dermal-epidermal separation in cryosections of human skin. Am J Pathol 2002: 161: 301-311.
141. Shigemoto T, Nashiro K, Tsuchida T, Seki Y, Tamaki K. Administration of IgG fraction of epidermolysis bullosa acquisita (EBA) serum into mice. J Dermatol 1988: 15: 123-127.
142. Borradori L, Caldwell J B, Briggaman R A et al. Passive transfer of autoantibodies from a patient with mutilating epidermolysis bullosa acquisita induces specific alterations in the skin of neonatal mice. Arch Dermatol 1995: 131: 590-595.
143. Sitaru C, Mihai S, Otto C et al. Induction of dermal-epidermal separation in adult mice by passive transfer of antibodies to type VII collagen. J Clin Invest 2005: 115: 870-878.
144. Woodley D T, Chang C, Saadat P, Ram R, Liu Z, Chen M. 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.
145. Guide S V, Marinkovich M P. Linear IgA bullous dermatosis. Clin Dermatol 2001: 19: 719-727.
146. Chorzelski T P, Jablonska S, Beutner S F, Furey N L. Linear IgA bullous dermatosis in immunopathology of the skin. In: Beutner E, Chorzelski T P, Bean S, eds. New York: John Wiley and Sons, 1979: 315-323.
147. Marinkovich M P, Taylor T B, Keene D R, Burgeson R E, Zone J J. LAD-1, the linear IgA bullous dermatosis autoantigen, is a novel 120-kDa anchoring filament protein synthesized by epidermal cells. J Invest Dermatol 1996: 106: 734-738.
148. Pas H H, Kloosterhuis G J, Heeres K, van der Meer J B, Jonkman M F. Bullous pemphigoid and linear IgA dermatosis sera recognize a similar 120-kDa keratinocyte collagenous glycoprotein with antigenic cross-reactivity to BP180. J Invest Dermatol 1997: 108: 423-429.
149. Hirako Y, Usukura J, Uematsu J, Hashimoto T, Kitajima Y, Owaribe K. Cleavage of BP180, a 180-kDa bullous pemphigoid antigen, yields a 120-kDa collagenous extracellular polypeptide. J Biol Chem 1998: 273: 9711-9717.
150. Schäcke H, Schumann H, Hammami-Hauasli N, Raghunath M, Bruckner-Tuderman L. Two forms of collagen XVII in keratinocytes: a full-length transmembrane protein and a soluble ectodomain. J Biol Chem 1998: 273: 25937-25943.
151. Zone J J, Taylor T B, Meyer L J, Petersen M J. The 97 kDa linear IgA bullous disease antigen is identical to a portion of the extracellular domain of the 180 kDa bullous pemphigoid antigen, BPAg2. J Invest Dermatol 1998: 110: 207-210.
152. Hirako Y, Nishizawa Y, Sitaru C et al. The 97-kDa (LABD97) and 120-kDa (LAD-1) fragments of bullous pemphigoid antigen 180/type XVII collagen have different N-termini. J Invest Dermatol 2003: 121: 1554-1556.
153. Hendrix J D, Mangum K L, Zone J J, Gammon W R. Cutaneous IgA deposits in bullous diseases function as ligands to mediate adherence of activated neutrophils. J Invest Dermatol 1990: 94: 667-672.
154. Monteiro R C, Van De Winkel J G. IgA Fc receptors. Annu Rev Immunol 2003: 21: 177-204.
155. Zone J J, Egan C A, Taylor T B, Meyer L J. IgA autoimmune disorders: development of a passive transfer mouse model. J Investig Dermatol Symp Proc 2004: 9: 47-51.
156. Chorzelski T P, Sulej J, Tchorzewska H, Jablonska S, Beutner E H, Kumar V. IgA class endomysium antibodies in dermatitis herpetiformis and coeliac disease. Ann N Y Acad Sci 1983: 420: 325-334.
157. Reunala T, Chorzelski T P, Viander M et al. IgA anti-endomysial antibodies in dermatitis herpetiformis: correlation with jejunal morphology, gluten-free diet and anti-gliadin antibodies. Br J Dermatol 1987: 117: 185-191.
158. Dieterich W, Laag E, Bruckner-Tuderman L et al. Antibodies to tissue transglutaminase as serologic markers in patients with dermatitis herpetiformis. J Invest Dermatol 1999: 113: 133-136.
159. Rose C, Dieterich W, Bröcker E B, Schuppan D, Zillikens D. Circulating autoantibodies to tissue transglutaminase differentiate patients with dermatitis herpetiformis from those with linear IgA disease. J Am Acad Dermatol 1999: 41: 957-961.
160. Sardy M, Karpati S, Merkl B, Paulsson M, Smyth N. Epidermal transglutaminase (TGase 3) is the autoantigen of dermatitis herpetiformis. J Exp Med 2002: 195: 747-757.
161. Marietta E, Black K, Camilleri M et al. A new model for dermatitis herpetiformis that uses HLA-DQ8 transgenic NOD mice. J Clin Invest 2004: 114: 1090-1097.