Role of Rho GTPases in desmosomal adhesion and pemphigus pathogenesis

Annals of Anatomy

Volumn 193, Issue 3, 2011, Pages 177-180

  Spindler, Volker ^a   Waschke, Jens ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Desmoglein; Desmosome; Pemphigus; Rho GTPase

Indexed keywords

AUTOANTIBODY; DESMOGLEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANTIBODY PRODUCTION; ANTIGEN BINDING; BLISTER; CELL ADHESION; CELL JUNCTION; DESMOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; EPIDERMIS; HISTOPATHOLOGY; HUMAN; MUCOSA; NONHUMAN; PATHOGENESIS; PEMPHIGUS; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; DESMOSOMES; HUMANS; MODELS, IMMUNOLOGICAL; PEMPHIGUS; RHO GTP-BINDING PROTEINS; SKIN;

EID: 79955785245     PISSN: 09409602     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aanat.2011.02.003     Document Type: Review

References (43)

1. Amagai M., Ahmed A.R., Kitajima Y., Bystryn J.C., 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. 2006, 15:815-831.
2. Aoyama Y., Owada M.K., Kitajima Y. A pathogenic autoantibody, pemphigus vulgaris-IgG, induces phosphorylation of desmoglein 3, and its dissociation from plakoglobin in cultured keratinocytes. Eur. J. Immunol. 1999, 29:2233-2240.
3. Bass-Zubek A.E., Hobbs R.P., Amargo E.V., Garcia N.J., Hsieh S.N., Chen X., Wahl J.K., Denning M.F., Green K.J. Plakophilin 2: a critical scaffold for PKCα that regulates intercellular junction assembly. J. Cell Biol. 2008, 181:605-613.
4. Bédane C., Prost C., Thomine E., Intrator L., Joly P., Caux F., Blecker M., Bernard P., Leboutet M., Tron F., Lauret P., Bonnetblanc J., Dubertret L. Binding of autoantibodies is not restricted to desmosomes in pemphigus vulgaris. Arch. Dermatol. Res. 1996, 288:343-352.
5. Berkowitz P., Hu P., Liu Z., Diaz L.A., Enghild J.J., Chua M.P., Rubenstein D.S. Desmosome signaling. Inhibition of p38MAPK prevents pemphigus vulgaris IgG-induced cytoskeleton reorganization. J. Biol. Chem. 2005, 280:23778-23784.
6. Berkowitz P., Hu P., Warren S., Liu Z., Diaz L.A., Rubenstein D.S. p38MAPK inhibition prevents disease in pemphigus vulgaris mice. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12855-12860.
7. Braga V.M., Machesky L.M., Hall A., Hotchin N.A. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 1997, 137:1421-1431.
8. Caldelari R., de Bruin A., Baumann D., Suter M.M., Bierkamp C., Balmer V., Muller E. A central role for the armadillo protein plakoglobin in the autoimmune disease pemphigus vulgaris. J. Cell Biol. 2001, 153:823-834.
9. Delva E., Tucker D.K., Kowalczyk A.P. The desmosome. Cold Spring Harb. Perspect. Biol. 2009, 1.
10. Dovas A., Choi Y., Yoneda A., Multhaupt H.A.B., Kwon S.-H., Kang D., Oh E.-S., Couchman J.R. Serine 34 Phosphorylation of Rho guanine dissociation inhibitor (RhoGDIα links signaling from conventional protein kinase C to RhoGTPase in cell adhesion. J. Biol. Chem. 2010, 285:23296-23308.
11. Gliem M., Heupel W.-M., Spindler V., Harms G.S., Waschke J. Actin reorganization contributes to loss of cell adhesion in pemphigus vulgaris. Am. J. Physiol. Cell Physiol. 2010, 299:C606-C613.
12. Godsel L.M., Dubash A.D., Bass-Zubek A.E., Amargo E.V., Klessner J.L., Hobbs R.P., Chen X., Green K.J. Plakophilin 2 couples actomyosin remodeling to desmosomal plaque assembly via RhoA. Mol. Biol. Cell 2010, 21:2844-2859.
13. Godsel L.M., Hsieh S.N., Amargo E.V., Bass A.E., Pascoe-McGillicuddy L.T., Huen A.C., Thorne M.E., Gaudry C.A., Park J.K., Myung K., Goldman R.D., Chew T.-L., Green K.J. Desmoplakin assembly dynamics in four dimensions. J. Cell Biol. 2005, 171:1045-1059.
14. Green K.J., Getsios S., Troyanovsky S., Godsel L.M. Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb. Perspect. Biol. 2010, 2. a000125.
15. Hall A., Nobes C.D. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos. Trans. R Soc. Lond. B: Biol. Sci. 2000, 355:965-970.
16. Heupel W.-M., Müller 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. 2009, 284:8589-8595.
17. Heupel W.M., Zillikens D., Drenckhahn D., Waschke J. Pemphigus vulgaris IgG directly inhibit desmoglein 3-mediated transinteraction. J. Immunol. 2008, 181:1825-1834.
18. Holinstat M., Mehta D., Kozasa T., Minshall R.D., Malik A.B. Protein kinase α-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J. Biol. Chem. 2003, 278:28793-28798.
19. Huen A.C., Park J.K., Godsel L.M., Chen X., Bannon L.J., Amargo E.V., Hudson T.Y., Mongiu A.K., Leigh I.M., Kelsell D.P., Gumbiner B.M., Green K.J. Intermediate filament-membrane attachments function synergistically with actin-dependent contacts to regulate intercellular adhesive strength. J. Cell Biol. 2002, 159:1005-1017.
20. Jackson B., Peyrollier K., Pedersen E., Basse A., Karlsson R., Wang Z., Lefever T., Ochsenbein A., Schmidt G., Aktories K., Stanley A., Quondamatteo F., Ladwein M., Rottner K., van Hengel J., Brakebusch C. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol. Biol. Cell 2011, (mbc.E09-10-0859).
21. Kalantari-Dehaghi M., Molina D.M., Farhadieh M., John Morrow W., Liang X., Felgner P.L., Grando S.A. New targets of pemphigus vulgaris antibodies identified by protein array technology. Exp. Dermatol. 2011, 20:154-156.
22. Mahoney M.G., Wang Z., Rothenberger K., Koch P.J., Amagai M., Stanley J.R. Explanations for the clinical and microscopic localization of lesions in pemphigus foliaceus and vulgaris. J. Clin. Invest. 1999, 103:461-468.
23. Mao X., Choi E.J., Payne A.S. Disruption of desmosome assembly by monovalent human pemphigus vulgaris monoclonal antibodies. J. Invest. Dermatol. 2008, 129(4):908-918.
24. Marchenko S., Chernyavsky A.I., Arredondo J., Gindi V., Grando S.A. Antimitochondrial autoantibodies in pemphigus vulgaris. J. Biol. Chem. 2010, 285:3695-3704.
25. Marcozzi C., Burdett I.D., Buxton R.S., Magee A.I. J. Cell Sci. 1998, 111:495-509.
26. Meng W., Takeichi M. Adherens junction: molecular architecture and regulation. Cold Spring Harb. Perspect. Biol. 2009, 1.
27. Menon M.B., Schwermann J., Singh A.K., Franz-Wachtel M., Pabst O., Seidler U., Omary M.B., Kotlyarov A., Gaestel M. p38 MAP kinase and MAPKAP kinases MK2/3 cooperatively phosphorylate epithelial keratins. J. Biol. Chem. 2010, 285:33242-33251.
28. Nie Z., Merritt A., Rouhi-Parkouhi M., Tabernero L., Garrod D. Membrane-impermeable cross-linking provides evidence for homophilic, isoform-specific binding of desmosomal cadherins in epithelial cells. J. Biol. Chem. 2011, 286:2143-2154.
29. 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.
30. Perez-Moreno M., Fuchs E. Catenins: keeping cells from getting their signals crossed. Dev. Cell 2006, 11:601-612.
31. Sato M., Aoyama Y., Kitajima Y. Assembly pathway of desmoglein 3 to desmosomes and its perturbation by pemphigus vulgaris-IgG in cultured keratinocytes, as revealed by time-lapsed labeling immunoelectron microscopy. Lab. Invest. 2000, 80:1583-1592.
32. 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. 2007, 171:906-916.
33. Spindler V., Heupel W.-M., 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. 2009, 284:30556-30564.
34. Spindler V., Vielmuth F., Schmidt E., Rubenstein D.S., Waschke J. Protective endogenous cyclic adenosine 5'-monophosphate signaling triggered by pemphigus autoantibodies. J. Immunol. 2010, 185:6831-6838.
35. Stanley J.R., Amagai M. Pemphigus, bullous impetigo, and the staphylococcal scalded-skin syndrome. N. Engl. J. Med. 2006, 355:1800-1810.
36. Syed S.E., Trinnaman B., Martin S., Major S., Hutchinson J., Magee A.I. Molecular interactions between desmosomal cadherins. Biochem. J. 2002, 362:317-327.
37. Thomason H.A., Scothern A., McHarg S., Garrod D.R. Desmosomes: adhesive strength and signalling in health and disease. Biochem. J. 2010, 429:419-433.
38. Vasioukhin V., Bowers E., Bauer C., Degenstein L., Fuchs E. Desmoplakin is essential in epidermal sheet formation. Nat. Cell Biol. 2001, 3:1076-1085.
39. Waschke J. The desmosome and pemphigus. Histochem. Cell Biol. 2008, 130:21-54.
40. Waschke J., Bruggeman P., Baumgartner W., Zillikens D., Drenckhahn D. Pemphigus foliaceus IgG causes dissociation of desmoglein 1-containing junctions without blocking desmoglein 1 transinteraction. J. Clin. Invest. 2005, 115:3157-3165.
41. Waschke J., Spindler V., Bruggeman P., Zillikens D., Schmidt G., Drenckhahn D. Inhibition of Rho A activity causes pemphigus skin blistering. J. Cell Biol. 2006, 175:721-727.
42. Woll S., Windoffer R., Leube R.E. p38 MAPK-dependent shaping of the keratin cytoskeleton in cultured cells. J. Cell Biol. 2007, 177:795-807.
43. Yamagami J., Payne A.S., Kacir S., Ishii K., Siegel D.L., Stanley J.R. Homologous regions of autoantibody heavy chain complementarity-determining region 3 (H-CDR3) in patients with pemphigus cause pathogenicity. J. Clin. Invest. 2010, 120:4111-4117.