Calcium-dependent conformation of desmoglein 1 is required for its cleavage by exfoliative toxin

Journal of Investigative Dermatology

Volumn 121, Issue 2, 2003, Pages 383-389

  Hanakawa, Yasushi ^a   Selwood, Trevor ^a   Woo, Denise ^a   Lin, Chenyan ^a   Schechter, Norman M ^a   Stanley, John R ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cadherins; Impetigo; Serine protease; Staphylococcus

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; DESMOGLEIN 1; EPITOPE; EXFOLIATIN; TRYPTOPHAN;

AMINO ACID SEQUENCE; ARTICLE; CALCIUM DEPLETION; CIRCULAR DICHROISM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUOROMETRY; HUMAN; HYDROLYSIS; IMMUNOFLUORESCENCE; IMPETIGO BULLOSA; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; STAPHYLOCOCCUS AUREUS; STRATUM CORNEUM; TEMPERATURE DEPENDENCE;

EID: 0042122431     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2003.12362.x     Document Type: Article

References (43)

1. Amagai M, Hashimoto T, Green KJ, Shimizu N, Nishikawa T: Antigen-specific immuoabsorption of pathogenic autoantibodies in pemphigus foliaceus. J Invest Dermatol 104:895-901, 1995a
2. Amagai M, Ishii K, Hashimoto T, Gamou S, Shimizu N, Nishikawa T: Conformational epitopes of pemphigus antigens (Dsg1 and Dsg3) are calcium dependent and glycosylation independent. J Invest Dermatol 105:243-247, 1995b
3. Amagai M, Matsuyoshi N, Wang ZH, Andl C, Stanley JR: Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nature Med 6:1275-1277, 2000
4. Amagai M, Yamaguchi T, Hanakawa Y, Nishifuji K, Sugai M, Stanley JR: Staphylococcal exfoliative toxin B specifically cleaves desmoglein 1. J Invest Dermatol 118:845-850, 2002
5. Angst BD, Marcozzi C, Magee AI: The cadherin superfamily. Diversity in form and function. J Cell Sci 114:629-641, 2001
6. Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L: C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296:1308-1313, 2002
7. Cavarelli J, Prevost G, Bourguet W, et al: The structure of Staphylococcus aureus epidermolytic toxin A, an atypic serine protease, at 1.7A resolution. Structure 5:813-824, 1997
8. Chidgey M, Brakebusch C, Gustafsson E, et al: Mice lacking desmocollin 1 show epidermal fragility accompanied by barrier defects and abnormal differentiation. J Cell Biol 155:821-832, 2001
9. Chitaev NA, Troyanovsky SM: Direct Ca2+-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. J Cell Biol 138:193-201, 1997
10. Eyre RW, Stanley JR: Human autoantibodies against a desmosomal protein complex with a calcium-sensitive epitope are characteristic of pemphigus foliaceus patients. J Exp Med 165:1719-1724, 1987
11. Garrod D, Chidgey M, North A: Desmosomes: Differentiation, development, dynamics and disease. Curr Opin Cell Biol 8:670-678, 1996
12. Green KJ, Gaudry CA: Are desmosomes more than tethers for intermediate filaments? Nature Rev Mol Cell Biol 1:208-216, 2000
13. Hanakawa Y, Schechter N, Lin C, et al: Molecular mechanisms of blister formation in bullous impetigo and staphylococcal scalded skin syndrome. J Clin Invest 110:53-60, 2002
14. Hashimoto T, Kiyokawa C, Mori O, et al: Human desmocollin 1 (Dsc1) is an autoantigen for the subcorneal pustular dermatosis type of IgA pemphigus. I Invest Dermatol 109:127-131, 1997
15. Ishii K, Amagai M, Hall RP, Hashimoto T, et al: Characterization of autoantibodies in pemphigus using antigen-specific enzyme-linked immunosorbent assays with baculovirus-expressed recombinant desmogleins. J Immunol 159:2010-2017, 1997
16. Kemler R, Ozawa M, Ringwald M: Calcium-dependent cell adhesion molecules. Curr Opin Cell Biol 1:892-897, 1989
17. Koch PJ, Mahoney MG, Ishikawa H, et al: Targeted disruption of the pemphigus vulgaris antigen (desmoglein 3) gene in mice causes loss of keratinocyte cell adhesion with a phenotype similar to pemphigus vulgaris. J Cell Biol 137:1091-1102, 1997a
18. Koch AW, Pokutta S, Lustig A, Engel J: Calcium binding and homoassociation of E-cadherin domains. Biochemistry 36:7697-7705, 1997b
19. Kondo I, Sakurai S, Sarai Y: New type of exfoliatin obtained from staphylococcal strains, belonging to phage groups other than group II, isolated from patients with impetigo and Ritter's disease. Infect Immun 10:851-861, 1974
20. Koulu L, Kusumi A, Steinberg MS, Klaus Kovtun V, Stanley JR: Human autoantibodies against a desmosomal core protein in pemphigus foliaceus. J Exp Med 160:1509-1518, 1984
21. Kowalczyk AP, Anderson JE, Borgwardt JE, Hashimoto T, Stanley JR, Green KJ: Pemphigus sera recognize conformationally sensitive epitopes in the amino-terminal region of desmoglein-1 (Dsg1). J Invest Dermatol 105:147-152, 1995
22. Ladhani S, Joannou CL, Lochrie DP, Evans RW, Poston SM: Clinical, microbial, and biochemical aspects of the exfoliative toxins causing staphylococcal scalded-skin syndrome. Clin Microbiol Rev 12:224-242, 1999
23. Mahoney MG, Wang Z, Rothenberger K, Koch PJ, Amagai M, Stanley JR: Explanation for the clinical and microscopic localization of lesions in pemphigus foliaceus and vulgaris. J Clin Invest 103:461-468, 1999
24. Marcozzi C, Burdett ID, Buxton RS, Magee AI: Coexpression of both types of desmosomal cadherin and plakoglobin confers strong intercellular adhesion. J Cell Sci 111:495-509, 1998
25. Melish ME, Glasgow LA: The staphylococcal scalded-skin syndrome. Development of an experimental model. N Engl J Med 282:1114-1119, 1970
26. Melish ME, Glasgow LA: Staphylococcal scalded skin syndrome: The expanded clinical syndrome. J Pediatrics 78:938-967, 1971
27. Melish ME, Glasgow LA, Turner MD: The staphylococcal scalded-skin syndrome. Isolation and partial characterization of the exfoliative toxin. J Infect Dis 125:129-140, 1972
28. Nagar B, Overduin M, Ikura M, Rini JM: Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380:360-364, 1996
29. Ozawa M, Engel J, Kemler R: Single amino acid substitutions in one Ca2+ binding site of uvomorulin abolish the adhesive function. Cell 63:1033-1038, 1990
30. Papageorgiou AC, Plano LR, Collins CM, Acharya KR: Structural similarities and differences in Staphylococcus aureus exfoliative toxins A and B as revealed by their crystal structures. Protein Sci 9:610-618, 2000
31. Pertz O, Bozic D, Koch AW, Fauser C, Brancaccio A, Engel J: A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J 18:1738-1747, 1999
32. Pokutta S, Herrenknecht K, Kemler R, Engel J: Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur J Biochem 223:1019-1026, 1994
33. Ringwald M, Schuh R, Vestweber D, et al: The structure of cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca2+-dependent cell adhesion. EMBO J 6:3647-3653, 1987
34. Shapiro L, Fannon AM, Kwong PD, et al: Structural basis of cell-cell adhesion by cadherins. Nature 374:327-337, 1995
35. Stanley JR, Koulu L, Klaus Kovtun V, Steinberg MS: A monoclonal antibody to the desmosomal glycoprotein desmoglein I binds the same polypeptide as human autoantibodies in pemphigus foliaceus. J Immunol 136:1227-1230, 1986
36. Steinberg MS, McNutt PM: Cadherins and their connections: Adhesion junctions have broader functions. Curr Opin Cell Biol 11:554-560, 1999
37. Syed SE, Trinnaman B, Martin S, Major S, Hutchinson J, Magee AI: Molecular interactions between desmosomal cadherins. Biochem J 362:317-327, 2002
38. Tamura K, Shan WS, Hendrickson WA, Colman DR, Shapiro L: Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20:1153-1163, 1998
39. Vath GM, Earhart CA, Rago JV, Kim MH, Bohach GA, Schlievert PM, Ohlendorf DH: The structure of the superantigen exfoliative toxin A suggests a novel regulation as a serine protease. Biochemistry 36:1559-1566, 1997
40. Vath GM, Earhart CA, Monie DD, Iandolo JJ, Schlievert PM, Ohlendorf DH: The crystal structure of exfoliative toxin B: A superantigen with enzymatic activity. Biochemistry 38:10239-10246, 1999
41. Wallis S, Lloyd S, Wise I, Ireland G, Fleming TP, Garrod D: The alpha isoform of protein kinase C is involved in signaling the response of desmosomes to wounding in cultured epithelial cells. Mol Biol Cell 11:1077-1092, 2000
42. Yamaguchi T, Nishifuji K, Sasaki M, et al: Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect Immun 70:5835-5845, 2002
43. Yasuda H, Kobayashi H, Hashimoto T, Itoh K, Yamane M, Nakamura J: Subcorneal pustular dermatosis type of IgA pemphigus: Demonstration of autoantibodies to desmocollin-1 and clinical review. Br J Dermatol 143:144-148, 2000