The flavonoid luteolin inhibits Fcγ-dependent respiratory burst in granulocytes, but not skin blistering in a new model of pemphigoid in adult mice

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Oswald, Eva ^a,b   Sesarman, Alina ^a   Franzke, Claus Werner ^a   Wölfle, Ute ^a   Bruckner Tuderman, Leena ^a,b   Jakob, Thilo ^a   Martin, Stefan F ^a   Sitaru, Cassian ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; COLLAGEN XVII; COMPLEMENT COMPONENT C3; FC RECEPTOR; IMMUNOGLOBULIN G; LUTEOLIN; UNCLASSIFIED DRUG; COLLAGEN TYPE 17; GELATINASE B; NONFIBRILLAR COLLAGEN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BLISTER; BULLOUS PEMPHIGOID; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MODEL; DOSE RESPONSE; EX VIVO STUDY; FEMALE; GRANULOCYTE; IMMUNOREACTIVITY; IN VIVO STUDY; INFLAMMATORY CELL; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PASSIVE IMMUNIZATION; RESPIRATORY BURST; AFFINITY CHROMATOGRAPHY; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOLOGY; METABOLISM; NEUTROPHIL; RABBIT;

ANIMALIA; MUS; ORYCTOLAGUS CUNICULUS;

ANIMALS; AUTOANTIGENS; BLISTER; CHROMATOGRAPHY, AFFINITY; COMPLEMENT C3; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GRANULOCYTES; IMMUNOBLOTTING; IMMUNOGLOBULIN G; LUTEOLIN; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUTROPHILS; NON-FIBRILLAR COLLAGENS; PEMPHIGOID, BULLOUS; RABBITS; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST;

EID: 84856661232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031066     Document Type: Article

References (51)

1. Mihai S, Sitaru C, (2007) Immunopathology and molecular diagnosis of autoimmune bullous diseases. J Cell Mol Med 11: 462-81.
2. Sitaru C, (2009) Bullous pemphigoid: a prototypical antibody-mediated organ-specific autoimmune disease. J Invest Dermatol 129: 822-4.
3. Stanley JR, Hawley-Nelson P, Yuspa SH, Shevach EM, Katz SI, (1981) Characterization of bullous pemphigoid antigen: a unique basement membrane protein of stratified squamous epithelia. Cell 24: 897-903.
4. Stanley JR, Tanaka T, Mueller S, Klaus-Kovtun V, Roop D, (1988) Isolation of complementary DNA for bullous pemphigoid antigen by use of patients' autoantibodies. J Clin Invest 82: 1864-70.
5. Diaz LA, Ratrie H, Saunders WS, Futamura S, Squiquera HL, et al. (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: 1088-94.
6. Giudice GJ, Emery DJ, Diaz LA, (1992) Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 99: 243-50.
7. Giudice GJ, Emery DJ, Zelickson BD, Anhalt GJ, Liu Z, et al. (1993) Bullous pemphigoid and herpes gestationis autoantibodies recognize a common non-collagenous site on the BP180 ectodomain. J Immunol 151: 5742-50.
8. Büdinger L, Borradori L, Yee C, Eming R, Ferencik S, et al. (1998) Identification and characterization of autoreactive T cell responses to bullous pemphigoid antigen 2 in patients and healthy controls. J Clin Invest 102: 2082-9.
9. Lin MS, Gharia MA, Swartz SJ, Diaz LA, Giudice GJ, (1999) Identification and characterization of epitopes recognized by T lymphocytes and autoantibodies from patients with herpes gestationis. J Immunol 162: 4991-7.
10. Egan CA, Taylor TB, Meyer LJ, Petersen MJ, Zone JJ, (1999) Bullous pemphigoid sera that contain antibodies to BPAg2 also contain antibodies to LABD97 that recognize epitopes distal to the NC16A domain. J Invest Dermatol 112: 148-52.
11. Perriard J, Jaunin F, Favre B, Büdinger L, Hertl M, et al. (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: 141-7.
12. Haase C, Büdinger L, Borradori L, Yee C, Merk HF, et al. (1998) Detection of IgG autoantibodies in the sera of patients with bullous and gestational pemphigoid: ELISA studies utilizing a baculovirus-encoded form of bullous pemphigoid antigen 2. J Invest Dermatol 110: 282-6.
13. Schmidt E, Obe K, Bröcker EB, Zillikens D, (2000) Serum levels of autoantibodies to BP180 correlate with disease activity in patients with bullous pemphigoid. Arch Dermatol 136: 174-8.
14. Iwata Y, Komura K, Kodera M, Usuda T, Yokoyama Y, et al. (2008) Correlation of IgE autoantibody to BP180 with a severe form of bullous pemphigoid. Arch Dermatol 144: 41-8.
15. Di Zenzo G, Thoma-Uszynski S, Fontao L, Calabresi V, Hofmann SC, et al. (2008) Multicenter prospective study of the humoral autoimmune response in bullous pemphigoid. Clin Immunol 128: 415-26.
16. Sitaru C, Schmidt E, Petermann S, Munteanu LS, Bröcker E, et al. (2002) Autoantibodies to bullous pemphigoid antigen 180 induce dermal-epidermal separation in cryosections of human skin. J Invest Dermatol 118: 664-71.
17. Herrero-Gonzalez JE, Brauns O, Egner R, Rönspeck W, Mascaro JM, et al. (2006) Immunoadsorption against two distinct epitopes on human type XVII collagen abolishes dermal-epidermal separation induced in vitro by autoantibodies from pemphigoid gestationis patients. Eur J Immunol 36: 1039-48.
18. Liu Z, Diaz LA, Troy JL, Taylor AF, Emery DJ, et al. (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: 2480-8.
19. Yamamoto K, Inoue N, Masuda R, Fujimori A, Saito T, et al. (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: 485-92.
20. Nishie W, Sawamura D, Goto M, Ito K, Shibaki A, et al. (2007) Humanization of autoantigen. Nat Med 13: 378-83.
21. Liu Z, Sui W, Zhao M, Li Z, Li N, et al. (2009) Subepidermal blistering induced by human autoantibodies to BP180 requires innate immune players in a humanized bullous pemphigoid mouse model. J Autoimmun 31: 331-8.
22. Nishie W, Sawamura D, Natsuga K, Shinkuma S, Goto M, et al. (2009) A novel humanized neonatal autoimmune blistering skin disease model induced by maternally transferred antibodies. J Immunol 183: 4088-93.
23. Ujiie H, Shibaki A, Nishie W, Sawamura D, Wang G, et al. (2010) A novel active mouse model for bullous pemphigoid targeting humanized pathogenic antigen. J Immunol 184: 2166-74.
24. Hall RP3, Murray JC, McCord MM, Rico MJ, Streilein RD, (1993) Rabbits immunized with a peptide encoded for by the 230-kD bullous pemphigoid antigen cDNA develop an enhanced inflammatory response to UVB irradiation: a potential animal model for bullous pemphigoid. J Invest Dermatol 101: 9-14.
25. Kiss M, Husz S, Jánossy T, Marczinovits I, Molnár J, et al. (2005) Experimental bullous pemphigoid generated in mice with an antigenic epitope of the human hemidesmosomal protein BP230. J Autoimmun 24: 1-10.
26. Feliciani C, Caldarola G, Kneisel A, Podstawa E, Pfütze M, et al. (2009) IgG autoantibody reactivity against bullous pemphigoid (BP) 180 and BP230 in elderly patients with pruritic dermatoses. Br J Dermatol 161: 306-12.
27. Naito K, Morioka S, Ikeda S, Ogawa H, (1984) Experimental bullous pemphigoid in guinea pigs: the role of pemphigoid antibodies, complement, and migrating cells. J Invest Dermatol 82: 227-30.
28. Anhalt GJ, Diaz LA, (1987) Animal models for bullous pemphigoid. Clin Dermatol 5: 117-25.
29. Neale TJ, Wilson CB, (1982) Glomerular antigens in glomerulonephritis. Springer Semin Immunopathol 5: 221-49.
30. Seelinger G, Merfort I, Schempp CM, (2008) Anti-oxidant, anti-inflammatory and anti-allergic activities of luteolin. Planta Med 74: 1667-1677.
31. Sesarman A, Oswald E, Chiriac MT, Csorba K, Vuta V, et al. (2012) Interaction of human IgG autoantibodies with murine innate immunity factors: implications for disease models using the passive transfer of IgG in mice. submitted.
32. Chiriac MT, Licarete E, Rados AM, Sas AG, Lupan I, et al. (2012) A novel model of adult bullous pemphigoid in wild-type mice. submitted.
33. Sitaru C, Mihai S, Otto C, Chiriac MT, Hausser I, et al. (2005) Induction of dermal-epidermal separation in mice by passive transfer of antibodies specific to type VII collagen. J Clin Invest 115: 870-8.
34. Nagai H, Takizawa T, Nishiyori T, Koda A, (1982) Experimental glomerulonephritis in mice as a model for immunopharmacological studies. Jpn J Pharmacol 32: 1117-24.
35. Mihai S, Chiriac M, Herrero-Gonzales J, Goodall M, Jefferis R, et al. (2007) IgG4 autoantibodies induce dermal-epidermal separation. J Cell Mol Med 11: 1117-28.
36. Katz SI, Hertz KC, Yaoita H, (1976) Herpes gestationis. Immunopathology and characterization of the HG factor. J Clin Invest 57: 1434-41.
37. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, et al. (2006) Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol 7: 284-92.
38. Liu Z, Giudice GJ, Zhou X, Swartz SJ, Troy JL, Fairley JA, Till GO, Diaz LA, (1997) A major role for neutrophils in experimental bullous pemphigoid. J Clin Invest 100: 1256-1263.
39. Iwata Y, Komura K, Kodera M, Usuda T, Yokoyama Y, Hara T, Muroi E, Ogawa F, Takenaka M, Sato S, (2008) Correlation of ige autoantibody to bp180 with a severe form of bullous pemphigoid. Arch Dermatol 144: 41-48.
40. Sitaru C, (2009) Bullous pemphigoid: a prototypical antibody-mediated organ-specific autoimmune disease. J Invest Dermatol 129: 822-824.
41. Csorba K, Sesarman A, Oswald E, Feldrihan V, Fritsch A, et al. (2010) Cross-reactivity of autoantibodies from patients with epidermolysis bullosa acquisita with murine collagen VII. Cell Mol Life Sci 67: 1343-51.
42. Sesarman A, Sitaru AG, Olaru F, Zillikens D, Sitaru C, (2008) Neonatal Fc receptor deficiency protects from tissue injury in experimental epidermolysis bullosa acquisita. J Mol Med 86: 951-9.
43. Sesarman A, Mihai S, Chiriac MT, Olaru F, Sitaru AG, et al. (2008) Binding of avian IgY to type VII collagen does not activate complement and leucocytes and fails to induce subepidermal blistering in mice. Br J Dermatol 158: 463-71.
44. Chen C, Peng W, Tsai K, Hsu S, (2007) Luteolin suppresses inflammation-associated gene expression by blocking NF-kappaB and AP-1 activation pathway in mouse alveolar macrophages. Life Sci 81: 1602-14.
45. Woelfle U, Simon-Haarhaus B, Merfort I, Schempp CM, (2010) Reseda luteola l. extract displays antiproliferative and pro-apoptotic activities that are related to its major flavonoids. Phytother Res 24: 1033-1036.
46. Sitaru C, Kromminga A, Hashimoto T, Bröcker EB, Zillikens D, (2002) Autoantibodies to type VII collagen mediate Fcgamma-dependent neutrophil activation and induce dermal-epidermal separation in cryosections of human skin. Am J Pathol 161: 301-11.
47. Shimanovich I, Mihai S, Oostingh GJ, Ilenchuk TT, Bröcker E, et al. (2004) 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 204: 519-27.
48. Liu Z, Zhou X, Shapiro SD, Shipley JM, Twining SS, et al. (2000) The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 102: 647-55.
49. Shimanovich I, Mihai S, Oostingh GJ, Ilenchuk TT, Bröcker E, et al. (2004) 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 204: 519-527.
50. Sitaru AG, Sesarman A, Mihai S, Chiriac MT, Zillikens D, et al. (2010) T cells are required for the production of blister-inducing autoantibodies in experimental epidermolysis bullosa acquisita. J Immunol 184: 1596-1603.
51. Sitaru C, Chiriac MT, Mihai S, Büning J, Gebert A, et al. (2006) Induction of complement-fixing autoantibodies against type VII collagen results in subepidermal blistering in mice. J Immunol 177: 3461-8.