Actin reorganization contributes to loss of cell adhesion in pemphigus vulgaris

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 3, 2010, Pages

  Gliem, Martin ^a   Heupel, Wolfgang Moritz ^a   Spindler, Volker ^a   Harms, Gregory S ^b   Waschke, Jens ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cytoskeleton; Cytotoxic necrotizing factor 1; Desmoglein; Rho GTPase

Indexed keywords

ACTIN; CYTOCHALASIN D; CYTOTOXIC NECROTIZING FACTOR 1; IMMUNOGLOBULIN G; JASPAMIDE; LATRUNCULIN B; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; AUTOANTIBODY; BACTERIAL TOXIN; DEPSIPEPTIDE; DESMOGLEIN 3; DSG3 PROTEIN, HUMAN; ESCHERICHIA COLI PROTEIN; FUSED HETEROCYCLIC RINGS; THIAZOLIDINE DERIVATIVE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CONTROLLED STUDY; DEPOLYMERIZATION; HUMAN; HUMAN CELL; KERATINOCYTE; PATHOGENESIS; PEMPHIGUS VULGARIS; PRIORITY JOURNAL; CELL LINE; DRUG EFFECTS; ENZYME ACTIVATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMMUNOLOGY; METABOLISM; PATHOLOGY; PEMPHIGUS; PHYSIOLOGY; TIME; ULTRASTRUCTURE;

ACTINS; AUTOANTIBODIES; BACTERIAL TOXINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL ADHESION; CELL LINE; CYTOCHALASIN D; DEPSIPEPTIDES; DESMOGLEIN 3; ENZYME ACTIVATION; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMANS; IMMUNOGLOBULIN G; KERATINOCYTES; PEMPHIGUS; RHO GTP-BINDING PROTEINS; THIAZOLIDINES; TIME FACTORS;

EID: 77956591114     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00075.2010     Document Type: Article

References (43)

1. Amagai M, Ahmed AR, Kitajima Y, Bystryn JC, Milner Y, Gniadecki R, Hertl M, Pincelli C, Kurzen H, Fridkis-Hareli M, Aoyama Y, Frusic-Zlotkin M, Muller E, David M, Mimouni D, Vind-Kezunovic D, Michel B, Mahoney M, Grando S. Are desmoglein autoantibodies essential for the immunopathogenesis of pemphigus vulgaris, or just "witnesses of disease"? Exp Dermatol 15: 815-831, 2006.
2. Baumgartner W, Schutz GJ, Wiegand J, Golenhofen N, Drenckhahn D. Cadherin function probed by laser tweezer and single molecule fluorescence in vascular endothelial cells. J Cell Sci 116: 1001-1011, 2003.
3. Berkowitz P, Hu P, Liu Z, Diaz LA, Enghild JJ, Chua MP, Rubenstein Desmosome signaling DS. Inhibition of p38MAPK prevents pemphigus vulgaris IgG-induced cytoskeleton reorganization. J Biol Chem 280: 23778-23784, 2005.
4. Berkowitz P, Hu P, Warren S, Liu Z, Diaz LA, Rubenstein DS. p38MAPK inhibition prevents disease in pemphigus vulgaris mice. Proc Natl Acad Sci USA 103: 12855-12860, 2006.
5. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871, 1994.
6. Bystryn JC, Grando SA. A novel explanation for acantholysis in pemphigus vulgaris: the basal cell shrinkage hypothesis. J Am Acad Dermatol 54: 513-516, 2006.
7. Caldelari R, de Bruin A, Baumann D, Suter MM, Bierkamp C, Balmer V, Muller E. A central role for the armadillo protein plakoglobin in the autoimmune disease pemphigus vulgaris. J Cell Biol 153: 823-834, 2001. (Pubitemid 34286113)
8. Calkins CC, Setzer SV, Jennings JM, Summers S, Tsunoda K, Amagai M, Kowalczyk AP. Desmoglein endocytosis and desmosome disassembly are coordinated responses to pemphigus autoantibodies. J Biol Chem 281: 7623-7634, 2006.
9. Campbell JJ, Knight MM. An improved confocal FRAP technique for the measurement of long-term actin dynamics in individual stress fibers. Microvasc Res Tech 70: 1034-1040, 2007.
10. Casella JF, Flanagan MD, Lin S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293: 302-305, 1981.
11. Chernyavsky AI, Arredondo J, Kitajima Y, Sato-Nagai M, Grando SA. Desmoglein versus non-desmoglein signaling in pemphigus acantholysis: characterization of novel signaling pathways downstream of pemphigus vulgaris antigens. J Biol Chem 282: 13804-13812, 2007. (Pubitemid 47100562)
12. Cirillo N, Lanza A, Prime SS. Induction of hyper-adhesion attenuates autoimmune-induced keratinocyte cell-cell detachment and processing of adhesion molecules via mechanisms that involve PKC. Exp Cell Res 316: 580-592.
13. Coue M, Brenner SL, Spector I, Korn ED. Inhibition of actin polymerization by latrunculin A. FEBS Lett 213: 316-318, 1987.
14. de Bruin A, Caldelari R, Williamson L, Suter MM, Hunziker T, Wyder M, Muller EJ. Plakoglobin-dependent disruption of the desmosomal plaque in pemphigus vulgaris. Exp Dermatol 16: 468-475, 2007.
15. Edidin M, Kuo SC, Sheetz MP. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science 254: 1379-1382, 1991.
16. Frusic-Zlotkin M, Raichenberg D, Wang X, David M, Michel B, Milner Y. Apoptotic mechanism in pemphigus autoimmunoglobulins-induced acantholysis-possible involvement of the EGF receptor. Autoimmunity 39: 563-575, 2006. (Pubitemid 44768925)
17. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701, 2008.
18. Heupel WM, Engerer P, Schmidt E, Waschke J. Pemphigus vulgaris IgG cause loss of desmoglein-mediated adhesion and keratinocyte dissociation independent of epidermal growth factor receptor. Am J Pathol 174:475-485, 2009.
19. Heupel WM, Muller T, Efthymiadis A, Schmidt E, Drenckhahn D, Waschke J. Peptides targeting the desmoglein 3 adhesive interface prevent autoantibody-induced acantholysis in pemphigus. J Biol Chem 284: 8589-8595, 2009.
20. Heupel WM, Zillikens D, Drenckhahn D, Waschke J. Pemphigus vulgaris IgG directly inhibit desmoglein 3-mediated transinteraction. J Immunol 181: 1825-1834, 2008.
21. Jolly PS, Berkowitz P, Bektas M, Lee HE, Chua M, Diaz LA, Rubenstein DS. p38MAPK signaling and desmoglein-3 internalization are linked events in pemphigus acantholysis. J Biol Chem 285: 8936-8941.
22. Kitajima Y, Aoyama Y, Seishima M. Transmembrane signaling for adhesive regulation of desmosomes and hemidesmosomes, and for cellcell datachment induced by pemphigus IgG in cultured keratinocytes: involvement of protein kinase C. J Investig Dermatol Symp Proc 4: 137-144, 1999.
23. Kottke MD, Delva E, Kowalczyk AP. The desmosome: cell science lessons from human diseases. J Cell Sci 119: 797-806, 2006.
24. Lanza A, Cirillo N, Rossiello R, Rienzo M, Cutillo L, Casamassimi A, de Nigris F, Schiano C, Rossiello L, Femiano F, Gombos F, Napoli C. Evidence of key role of Cdk2 overexpression in pemphigus vulgaris. J Biol Chem 283: 8736-8745, 2008.
25. Lewis JE, Wahl JK 3rd, Sass KM, Jensen PJ, Johnson KR, Wheelock MJ. Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J Cell Biol 136: 919-934, 1997.
26. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285: 895-898, 1999.
27. Mao X, Choi EJ, Payne AS. Disruption of desmosome assembly by monovalent human pemphigus vulgaris monoclonal antibodies. J Invest Dermatol 129: 908-918, 2009.
28. Marchenko S, Chernyavsky AI, Arredondo J, Gindi V, Grando SA. Antimitochondrial autoantibodies in pemphigus vulgaris: a missing link in disease pathophysiology. J Biol Chem 285: 3695-3704.
29. Nguyen VT, Ndoye A, Grando SA. Pemphigus vulgaris antibody identifies pemphaxin. A novel keratinocyte annexin-like molecule binding acetylcholine. J Biol Chem 275: 29466-29476, 2000. (Pubitemid 32043822)
30. Panasenko OO, Kim MV, Marston SB, Gusev NB. Interaction of the small heat shock protein with molecular mass 25 kDa (hsp25) with actin. Eur J Biochem 270: 892-901, 2003.
31. Perez-Moreno M, Jamora C, Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112: 535-548, 2003.
32. Sako Y, Nagafuchi A, Tsukita S, Takeichi M, Kusumi A. Cytoplasmic regulation of the movement of E-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: corralling and tethering by the membrane skeleton. J Cell Biol 140: 1227-1240, 1998.
33. Schmidt E, Gutberlet J, Siegmund D, Berg D, Wajant H, Waschke J. Apoptosis is not required for acantholysis in pemphigus vulgaris. Am J Physiol Cell Physiol 296: C162-C172, 2009.
34. Spindler V, Drenckhahn D, Zillikens D, Waschke J. Pemphigus IgG causes skin splitting in the presence of both desmoglein 1 and desmoglein 3. Am J Pathol 171: 906-916, 2007. (Pubitemid 47440989)
35. Spindler V, Heupel WM, Efthymiadis A, Schmidt E, Eming R, Rankl C, Hinterdorfer P, Müller T, Drenckhahn D, Waschke J. Desmocollin 3-mediated binding is crucial for keratinocyte cohesion and is impaired in pemphigus. J Biol Chem 284: 30556-30564, 2009.
36. Stanley JR, Amagai M. Pemphigus, bullous impetigo, and the staphylococcal scalded-skin syndrome. N Engl J Med 355: 1800-1810, 2006.
37. Vasioukhin V, Bauer C, Yin M, Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100: 209-219, 2000.
38. Vu TN, Lee TX, Ndoye A, Shultz LD, Pittelkow MR, Dahl MV, Lynch PJ, Grando SA. The pathophysiological significance of nondesmoglein targets of pemphigus autoimmunity. Development of antibodies against keratinocyte cholinergic receptors in patients with pemphigus vulgaris and pemphigus foliaceus. Arch Dermatol 134: 971-980, 1998.
39. Waschke J. The desmosome and pemphigus. Histochem Cell Biol 130: 21-54, 2008.
40. Waschke J, Spindler V, Bruggeman P, Zillikens D, Schmidt G, Drenckhahn D. Inhibition of Rho A activity causes pemphigus skin blistering. J Cell Biol 175: 721-727, 2006. (Pubitemid 44878505)
41. Williamson L, Raess NA, Caldelari R, Zakher A, de Bruin A, Posthaus H, Bolli R, Hunziker T, Suter MM, Muller EJ. Pemphigus vulgaris identifies plakoglobin as key suppressor of c-Myc in the skin. EMBO J 25: 3298-3309, 2006.
42. Windoffer R, Kolsch A, Woll S, Leube RE. Focal adhesions are hotspots for keratin filament precursor formation. J Cell Biol 173: 341-348, 2006.
43. Yoon KH, Yoon M, Moir RD, Khuon S, Flitney FW, Goldman RD. Insights into the dynamic properties of keratin intermediate filaments in living epithelial cells. J Cell Biol 153: 503-516, 2001.