150th Anniversary series: Desmosomes and autoimmune disease, perspective of dynamic desmosome remodeling and its impairments in pemphigus

Cell Communication and Adhesion

Volumn 21, Issue 6, 2014, Pages 269-280

  Kitajima, Yasuo ^a  

^a GIFU UNIVERSITY   (Japan)

Author keywords

Desmoglein 3; EGFR; PKC; Src; Wound healing

Indexed keywords

AUTOANTIBODY; CALCIUM ION; CATENIN; DESMOCOLLIN; DESMOGLEIN; DESMOGLEIN 3; DESMOGLEIN 3 ANTIBODY; DESMOPLAKIN; DESMOSOMAL CADHERIN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN G; MEMBRANE ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38; PEMPHIGUS ANTIBODY; PLAKOGLOBIN; PLAKOPHILIN; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; KERATIN;

ACANTHOLYSIS; ANTIGEN BINDING; AUTOIMMUNE DISEASE; CELL ADHESION; CHEMICAL STRUCTURE; DERMATITIS HERPETIFORMIS; DESMOSOME; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENZYME ACTIVATION; HISTOPATHOLOGY; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPATHOGENESIS; INTERMEDIATE FILAMENT; INTERNALIZATION; KERATINOCYTE; NONHUMAN; PARANEOPLASTIC PEMPHIGUS; PEMPHIGUS; PEMPHIGUS FOLIACEUS; PEMPHIGUS HERPETIFORMIS; PEMPHIGUS VEGETANS; PEMPHIGUS VULGARIS; PHENOTYPIC VARIATION; REVIEW; SIGNAL TRANSDUCTION; STEREOSPECIFICITY; ULTRASTRUCTURE; WOUND HEALING; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PATHOLOGY;

ANIMALS; DESMOSOMES; HUMANS; KERATINS; MODELS, BIOLOGICAL; PEMPHIGUS; SIGNAL TRANSDUCTION;

EID: 84911867477     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.3109/15419061.2014.943397     Document Type: Review

References (95)

1. Al-Amoudi A, Diez DC, Betts MJ, Frangakis AS (2007). The molecular architecture of cadherins in native epidermal desmosomes. Nature. 450: 832-837.
2. Amagai M (1999). Autoimmunity against desmosomal cadherins in pemphigus. J Dermatol Sci. 20: 92-102.
3. Amagai M, Karpati S, Prussick R, Klaus-Kovtun V, Stanley JR (1992). Autoantibodies against the amino-terminal cadherinlike binding domain of pemphigus vulgaris antigen are pathogenic. J Clin Invest. 90: 919-926.
4. Amagai M, Matsuyoshi N, Wang MH, Andl C, Stanley JR (2000). Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nature Med. 6: 1275-1277.
5. Amagai M, Stanley JR (2011). Desmoglein as a target in skin disease and beyond. J Invest Dermatol. 132: 776-784.
6. Anhalt GJ, Kim SC, Stanley JR, Korman NJ, Jabs DA, Kory M, Izumi H, Ratrie H III, Mutasim D, Ariss-Abdo L, Labib RS (1990). Paraneoplastic pemphigus. An autoimmune mucocutaneous disease associated with neoplasia. N Engl J Med. 323: 1729-1735.
7. Aoyama Y, Kitajima Y (1999). Pemphigus vulgaris-IgG causes a rapid depletion of desmoglein 3 (Dsg3) from the Triton X-100 soluble pools, leading to the formation of Dsg3-depleted desmosomes in a human squamous carcinoma cell line, DJM-1 cells. J Invest Dermatol. 112: 67-671.
8. Aoyama Y, Nagai M, Kitajima Y (2010). Binding of pemphigus vulgaris IgG to antigens in desmosome core domains excludes immune complexes rather than directly splitting desmosomes. Br J Dermatol. 162: 1049-1055.
9. Aoyama Y, Owada MK, Kitajima Y (1999). A pathogenic autoantibody, pemphigus vulgaris-IgG, induces phosphorylation of desmoglein 3, and its dissociation from plakoglobin in cultured keratinocytes. Eur J Immunol. 29: 2233-2240.
10. Aoyama Y, Yamamoto Y, Yamaguchi F, Kitajima Y (2009). Low to high Ca 2-switch causes phosphorylation and association of desmocollin 3 with plakoglobin and desmoglein 3 in cultured keratinocytes. Exp Dermatol. 18: 404-408.
11. Bazzi H, Getz A, Mahoney MG, Ishida-Yamamoto A, Langbein L, Wahl JK III, Christiano AM (2006). Desmoglein 4 is expressed in highly differentiated keratinocytes and trichocytes in human epidermis and hair follicle. Differentiation. 74: 129-140.
12. Bektas M, Jolly PS, Berkowitz P, Amagai M, Rubenstein DS (2013). A pathophysiologic role for epidermal growth factor receptor in pemphigus acantholysis. J Biol Chem. 288: 9447-9456.
13. Berkowitz P, Hu P, Warren S, Liu Z, Diaz LA, Rubenstein DS (2006). p38MAPK inhibition prevents disease in pemphigus vulgaris mice. Proc Natl Acad Sci USA. 103: 12855-12860.
14. Brennan D, Hu Y, Medhat W, Dowling A, Mahoney MG (2010). Superfi cial dsg2 expression limits epidermal blister formation mediated by pemphigus foliaceus antibodies and exfoliative toxins. Dermatol Res Pract. 2010: 10, Article ID 410278.
15. Calkins CC, Setzer SV, Jennings JM, Summers S, Tsunoda K, Amagai M, Kowalczyk AP (2006). Desmoglein endocytosis and desmosome disassembly are coordinated responses to pemphigus autoantibodies. J Biol Chem. 281: 7623-7634.
16. Chernyavsky AI, Arredondo J, Kitajima Y, Sato-Nagai M, Grando SA (2007). Desmoglein versus non-desmoglein signaling in pemphigus acantholysis: characterization of novel signaling pathways downstream of pemphigus vulgaris antigens. J Biol Chem. 282: 13804-13812.
17. Chitaev NA, Troyanovsky SM (1997). Direct Ca 2-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. J Cell Biol. 138: 193-201.
18. Cirillo N (2014). 150th anniversary series: Desmosomes in physiology and disease. Cell Commun Adhes. 21: 85-88.
19. Cirillo N, Al-Jandan BA (2013). Desmosomal adhesion and pemphigus vulgaris: the fi rst half of the story. Cell Commun Adhes. 20: 1-10.
20. Cirillo N, Alshwaimi E, McCullough M, Prime SS (2014). Pemphigus vulgaris autoimmune globulin induces Srcdependent tyrosine-phosphorylation of plakophilin 3 and its detachment from desmoglein 3. Autoimmunity. 47: 134-140.
21. Cirillo N, Lanza A, Prime SS (2010). Induction of hyperadhesion attenuates autoimmune-induced keratinocyte cell-cell detachment and processing of adhesion molecules via mechanisms that involve PKC. Exp Cell Res. 316: 580-592.
22. Delva E, Jennings JM, Calkins CC, Kottke MD, Faundez V, Kowalczyk AP (2008). Pemphigus vulgaris IgG-induced desmoglein-3 endocytosis and desmosomal disassembly are mediated by a clathrin-and dynamin-independent mechanism. J Biol Chem. 283: 18303-18313.
23. Demlehner MP, Schfer S, Grund C, Franke WW (1995). Continual assembly of half-desmosomal structures in the absence of cell contacts and their frustrated endocytosis: a coordinated Sisyphus cycle. J Cell Biol. 131: 745-760.
24. Esaki C, Seishima M, Yamada T, Osada K, Kitajima Y (1995). 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. 105: 329-333.
25. Futei Y, Amagai M, Sekiguchi M, Nishifuji K, Fujii Y, Nishikawa T (2000). Use of domain-swapped molecules for conformational epitope mapping of desmoglein 3 in pemphigus vulgaris. J Invest Dermatol. 115: 829-834
26. Garrod DR, Berika MY, Bardsley WF, Holmes D, Tabernero L (2005). Hyper-adhesion in desmosomes: its regulation in wound healing and possible relationship to cadherin crystal structure. J Cell Sci. 118: 5743-5754.
27. Garrod D, Kimura TE (2008). Hyper-adhesion: a new concept in cell-cell adhesion. Biochem Soc Trans. 36: 195-201.
28. Galichet A, Borradori L, Mller EJ (2014). A new light on an old disease: adhesion signaling in pemphigus vulgaris. J Invest Dermatol. 134: 8-10.
29. Gaudry CA, Palka HL, Dusek RL, Huen AC, Khandekar MJ, Hudson LG, Green KJ (2001). Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. J Biol Chem. 276: 24871-24880.
30. Gil MP, Modol T, Espaa A, Lpez-Zabalza MJ (2012). Inhibition of FAK prevents blister formation in the neonatal mouse model of pemphigus vulgaris. Exp Dermatol. 21: 254-259.
31. Gosavi P, Kundu ST, Khapare N, Sehgal L, Karkhanis MS, Dalal NS (2011). E-cadherin and plakoglobin recruit plakophilin3 to the cell border to initiate desmosome assembly. Cell Mol Life Sci. 68: 1439-1454.
32. Grando AG (2012). Pemphigus autoimmunity: Hypotheses and realities. Autoimmunity. 45: 7-35.
33. Hacker-Foegen MK, Janson M, Amagai M, Fairley JA, Lin MS (2003). Pathogenicity and epitope characteristics of antidesmoglein-1 from pemphigus foliaceus patients expressing only IgG1 autoantibodies. J Invest Dermatol. 121: 1373-1378.
34. Harmon RM, Green KJ (2013). Structural and functional diversity of desmosomes. Cell Commun Adhes. 20: 171-187.
35. He W, Cowin P, Stokes DL (2003). Untangling desmosomal knots with electron tomography. Science. 302: 109-113.
36. Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa SH (1980). Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell. 19: 245-254.
37. Hennings H, Holbrook KA (1983). Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture: an ultrastructural study. Exp Cell Res. 143: 127-142.
38. Heupel WM, Zillikens D, Drenckhahn D, Waschke J. (2008). Pemphigus vulgaris IgG directly inhibit desmoglein 3-mediated transinteraction (homophilic trans-interaction): single molecule atomic measurement. J Immunol. 181: 1825-1834.
39. Hisamatsu Y, Amagai M, Garrod DR, Kanzaki T, Hashimoto T (2004). The detection of IgG and IgA autoantibodies to desmocollins 1-3 by enzyme-linked immunosorbent assays using baculovirus-expressed proteins, in atypical pemphigus but not in typical pemphigus. Br J Dermatol. 151: 73-83.
40. Hobbs RP, Amargo EV, Somasundaram A, Simpson CL, Prakriya M, Denning MF, Green KJ (2011). The calcium ATPase SERCA2 regulates desmoplakin dynamics and intercellular adhesive strength through modulation of PKCa signaling. FASEB J. 25: 990-1001.
41. Hu P, O'Keefe EJ, Rubenstein DS (2001). Tyrosine phosphorylation of human keratinocyte-catenin and plakoglobin reversibly regulates their binding to E-cadherin and-catenin. J Invest Dermatol. 117: 1059-1067.
42. Ishii K, Amaga M, Komai A, Ebihara T, Chorzelski TP, Jablonska S, Ohya K, Nishikawa T, Hashimoto T (1999). Desmoglein 1 and desmoglein 3 are the target autoantigens in herpetiform pemphigus. Arch Dermatol. 135: 943-947.
43. Ishii K, Harada R, Matsuo I, Shirakata Y, Hashimoto K, Amagai M (2005). In vitro keratinocyte dissociation assay for evaluation of the pathogenicity of anti-desmoglein 3 IgG autoantibodies in pemphigus vulgaris. J Invest Dermatol. 124: 939-946.
44. Jennings JM, Tucker DK, Kottke MD, Saito M, Delva E, Hanakawa Y, Amagai M, Kowalczyk AP (2011). Desmosome disassembly in response to pemphigus vulgaris IgG occurs in distinct phases and can be reversed by expression of exogenous Dsg3. J Invest Dermatol. 131: 706-718.
45. Jolly PS, Berkowitz P, Bektas M, Lee HE, Chua M, Diaz LA, Rubenstein DS (2010). p38MAPK signaling and desmoglein-3 internalization are linked events in pemphigus acantholysis. J Biol Chem. 285: 8936-8941.
46. Kasperkiewicz M, Kowalewski C, Jab ł o L ska S (2014). Pemphigus herpetiformis: From fi rst description until now. J Am Acad Dermatol. 70: 780-787. doi:10.S0190-9622(13)01301-7.
47. Kimura TE, Merritt AJ, Garrod DR (2007). Calcium-independent desmosomes of keratinocytes are hyper-adhesive. J Invest Dermatol. 127: 775-781.
48. Kitajima Y (2013). New insights into desmosome regulation and pemphigus blistering as a desmosome-remodeling disease. Kaohsiung J Med Sci. 29: 1-13.
49. Kitajima Y, Aoyama Y (2007). Perspective of pemphigus from bedside and laboratory-bench. Clin Rev Allergy Immunol. 33: 57-66.
50. 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 (2008). Evidence of key role of Cdk2 overexpression in pemphigus vulgaris. J Biol Chem. 283: 8736-8745.
51. Lewis JE, Wahl JK III, Sass KM, Jensen PJ, Johnson KR, Wheelock MJ (1997). Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J Cell Biol. 136: 919-934.
52. Mahoney MZ, Wang Z, Rothenberger K, Koch PJ, Amagai M, Stanley JR (1999). Explanations for the clinical and microscopic localization of lesions in pemphigus foliaceus and vulgaris. J Clin Invest. 103: 461-468.
53. Mao X, Choi EJ, Payne AS (2009). Disruption of desmosome assembly by monovalent human pemphigus vulgaris monoclonal antibodies. J Invest Dermatol. 129: 908-918.
54. Mao X, Li H, Sano Y, Gaestel M, Mo Park J, Payne AS (2014). MAPKAP Kinase 2 (MK2)-Dependent and-Independent Models of Blister Formation in Pemphigus Vulgaris. J Invest Dermatol. 134: 68-76.
55. Michels C, Buchta T, Bloch W, Krieg T, Niessen CM (2009). Classical cadherins regulate desmosome formation. J Invest Dermatol. 129: 2072-2075.
56. Miravet S, Piedra J, Castao J, Raurell I, Franc C, Duach M, Garca de Herreros A (2003). Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates beta-catenin-mediated transcription. Mol Cell Biol. 23: 7391-7402.
57. Muller R, Svoboda V, Wenzel E, Gebert S, Hunzelmann N, Muller HH, Hertl M (2006). IgG reactivity against nonconformational NH-terminal epitopes of the desmoglein 3 ectodomain relates to clinical activity and phenotype of pemphigus vulgaris. Exp Dermatol. 15: 606-614.
58. Nagao S, Kitajima Y, Nagata K, Inoue S, Yaoita H, Nozawa Y (1989). Correlation between cell-cell contact formation and activation of protein kinase C in a human squamous cell carcinoma cell line. J Invest Dermatol. 1989. 92: 175-178.
59. Nekrasova O, Green KJ (2013). Desmosome assembly and dynamics. Trends Cell Biol. 23: 537-546.
60. Nie Z, Merritt A, Rouhi-Parkouhi M, Tabernero L, Garrod D (2011). Membrane-impermeable cross-linking provides evidence for homophilic, isoform-specifi c binding of desmosomal cadherins in epithelial cells. J Biol Chem. 2286: 2143-2154.
61. Nguyen B, Dusek RL, Beaudry VG, Marinkovich MP, Attardi LD (2009). Loss of the desmosomal protein perp enhances the phenotypic effects of pemphigus vulgaris autoantibodies. J Invest Dermatol. 129: 1710-1718.
62. North AJ, Bardsley WG, Hyam J, Bornslaeger EA, Cordingley HC, Trinnaman B, Hatzfeld M, Green KJ, Magee AI, Garrod DR (1999). Molecular map of the desmosomal plaque. J Cell Sci. 112: 4325-4336.
63. Oktarina DA, van der Wier G, Diercks GF, Jonkman MF, Pas HH (2011). IgG-induced clustering of desmogleins 1 and 3 in skin of patients with pemphigus fi ts with the desmoglein nonassembly depletion hypothesis. Br J Dermatol. 165: 552-562.
64. Osada K, Seishima M, Kitajima Y (1997). Pemphigus IgG activates and translocates protein kinase C from the cytosol to the particulate/cytoskeleton fractions in human keratinocytes. J Invest Dermatol. 108: 482-487.
65. O'Toole EA, Mak LL, Guitart J, Woodley DT, Hashimoto T, Amagai M, Chan LS (2000). Induction of keratinocyte IL-8 expression and secretion by IgG autoantibodies as a novel mechanism of epidermal neutrophil recruitment in a pemphigus variant. Clin Exp Immunol. 119: 217-224.
66. Pelacho B, Natal C, Espaa A, Snchez-Carpintero I, Iraburu MJ, Lez-Zabalza MJ (2004). Pemphigus vulgaris autoantibodies induce apoptosis in HaCaT keratinocytes. FEBS Lett. 566: 6-10.
67. Pretel M, Espa A, Marquina M, Pelacho B, Lez-Picazo JM, Lez-Zabalza MJ (2009). An imbalance in Akt/mTOR is involved in the apoptotic and acantholytic processes in a mouse model of pemphigus vulgaris. Exp Dermatol. 18: 771-780.
68. Puviani M, Marconi A, Cozzani E, Pincelli C (2003). Fas ligand in pemphigus sera induces keratinocyte apoptosis through the activation of caspase-8. J Invest Dermatol. 120: 164-167.
69. Sato M, Aoyama Y, Kitajima Y (2000). 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. 80: 1583-1592.
70. Schulze K, Galichet A, Sayar BS, Scothern A, Howald D, Zymann H, Siffert M, Zenhusern D, Bolli R, Koch PJ, Garrod D, Suter MM, Mller EJ (2012). An adult passive transfer mouse model to study desmoglein 3 signaling in pemphigus vulgaris. J Invest Dermatol. 132: 346-355.
71. Seishima M, Iwasaki-Bessho Y, Itoh Y, Nozawa Y, Amagai M, Kitajima Y (1999). Phosphatidylcholine-specifi c phospholipase C, but not phospholipase D, is involved in pemphigus IgG-induced signal transduction. Arch Dermatol Res. 291: 606-613.
72. Seishima M, Satoh S, Nojiri M, Osada K, Kitajima Y (1997). Pemphigus IgG induces expression of urokinase plasminogen activator receptor on the cell surface of cultured keratinocytes. J Invest Dermatol. 109: 650-655.
73. Sharpe GR, Gillespie JI, Greenwell JR (1989). An increase in intracellular free calcium is an early event during differentiation of cultured human keratinocytes. FEBS. 254: 25-28.
74. Sheu HM, Kitajama Y, Yaoita H (1989). Involvement of protein kinase C in translocation of desmoplakins from cytosol to plasma membrane during desmosome formation in human squamous cell carcinoma cells grown in low and normal calcium concentration. Exp Cell Res. 185: 176-190.
75. Shirakata Y, Amagai M, Hanakawa Y, Nishikawa T, Hashimoto K (1998). Lack of mucosal involvement in pemphigus foliaceus may be due to low expression of desmoglein 1. J Invest Dermatol. 110: 76-78.
76. Shirakata Y, Kimura R, Nanba D, Iwamoto R, Tokumaru S, Morimoto C, Yokota K, Nakamura M, Sayama K, Mekada E, Higashiyama S, Hashimoto K (2005). Heparin-binding EGFlike growth factor accelerates keratinocyte migration and skin wound healing. J Cell Sci. 118: 2363-2370.
77. Shu E, Yamamoto Y, Aoyama Y, Kitajima Y (2007). Intraperitoneal injection of pemphigus vulgaris-IgG into mouse depletes epidermal keratinocytes of desmoglein 3 associated with generation of acantholysis. Arch Dermatol Res. 299: 165-167.
78. Spindler V, Endlich A, Hartlieb E, Vielmuth F, Schmidt E, Waschke J (2011). The extent of desmoglein 3 depletion in pemphigus vulgaris is dependent on Ca(2)-induced differentiation: a role in suprabasal epidermal skin splitting. Am J Pathol. 179: 1905-1916.
79. Spindler V, Heupel WM, Efthymiadis A, Schmidt E, Eming R, Rankl C, Hinterdorfer P, Mller T, Drenckhahn D, Waschke J. (2009). Desmocollin 3-mediated binding is crucial for keratinocyte cohesion and is impaired in pemphigus. J Biol Chem. 284: 30556-30564.
80. Spindler V, Rtzer V, Dehner C, Kempf B, Gliem M, Radeva M, Hartlieb E, Harms GS, Schmidt E, Waschke J (2013). Peptidemediated desmoglein 3 crosslinking prevents pemphigus vulgaris autoantibody-induced skin blistering. J Clin Invest. 123: 800-811.
81. Spindler V, Waschke J (2014). Desmosomal cadherins and signaling: lessons from autoimmune disease. Cell Commun Adhes. 21: 77-84.
82. Stanley JR (1993). Cell adhesion molecules as targets of autoantibodies in pemphigus and pemphigoid, bullous diseases due to defective epidermal cell adhesion. Adv Immunol. 53: 291-325.
83. Thomason HA, Cooper NH, Ansell DM, Chiu M, Merrit AJ, Hardman MJ, Garrod DR (2012). Direct evidence that PKCpositively regulates wound re-epithelialization: correlation with changes in desmosomal adhesiveness. J. Pathol. 227: 346-356.
84. Tsunoda K, Ota T, Aoki M, Yamada T, Nagai T, Nakagawa T, Koyasu S, Nishikawa T, Amagai M (2003). Induction of pemphigus phenotype by a mouse monoclonal antibody against the amino-terminal adhesive interface of desmoglein 3. J Immunol. 170: 2170-2178.
85. Tu CL, Chang W, Bikle DD (2001). The extracellular calcium sensing receptor is required for calcium-induced differentiation in human keratinocytes. J Biol Chem. 276: 41079-41085.
86. Wallis S, Lloyd S, Wise I, Ireland G, Fleming TP, Garrod D (2000). 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.
87. Wang X, Brggre F, Frusi-Zlotkin M, Feinmesser M, Michel B, Milner Y (2004). Possible apoptotic mechanism in epidermal cell acantholysis induced by pemphigus vulgaris autoimmunoglobulins. Apoptosis. 9: 131-143.
88. Waschke J, Bruggeman P, Baumgartner W, Zillikens D, Drenckhahn D (2005). Direct Pemphigus foliaceus IgG causes dissociation of desmoglein 1-containing junctions without blocking desmoglein 1 transinteraction. J Clin Invest. 115: 3157-3165.
89. Waschke J, Spindler V, Bruggeman P, Zillikens D, Schmidt G, Drenckhahn D (2006). Inhibition of Rho A activity causes pemphigus skin blistering. J Cell Biol. 175: 721-727.
90. Williamson L, Raess NA, Caldelari R, Zakher A, de Bruin A, Posthaus H, Bolli R, Hunziker T, Suter MM, Muller EJ (2006). Pemphigus vulgaris identifi es plakoglobin as key suppressor of c-Myc in the skin. EMBO J. 25: 3298-3309.
91. Xie Z, Bikle DD (2007). The recruitment of phosphatidylinositol 3-kinase to the E-cadherin-catenin complex at the plasma membrane is required for calcium-induced phospholipase C-gamma1 activation and human keratinocyte differentiation. J Biol Chem. 282: 8695-8703.
92. Yamagami J, Payne AS, Kacir S, Ishii K, Siegel DL, Stanley JR (2010). Homologous regions of autoantibody heavy chain complementarity-determining region 3 (H-CDR3) in patients with pemphigus cause pathogenicity. J Clin Invest. 120: 4111-4117.
93. Yamamoto Y, Aoyama Y, Shu E, Tsunoda K, Amagai M, Kitajima Y (2007). Anti-desmoglein 3 (Dsg3) monoclonal antibodies deplete desmosomes of Dsg3 and differ in their Dsg3-depleting activities related to pathogenicity. J Biol Chem. 282: 17866-17876.
94. Yamada T, Aoyama Y, Owada MK, Kawakatsu H, Kitajima Y (2000). Scraped-wounding causes activation and association of C-Src tyrosine kinase with microtubules in cultured keratinocytes. Cell Struct Funct. 25: 351-359.
95. Yin T, Getsios S, Caldelari R, Godsel LM, Kowalczyk AP, Muller EJ Green KJ (2005). Mechanisms of plakoglobin-dependent adhesion: desmosome-specifi c functions in assembly and regulation by epidermal growth factor receptor. J Biol Chem. 280: 40355-40363.