Differential downregulation of E-Cadherin and desmoglein by epidermal growth factor

Dermatology Research and Practice

Volumn 2012, Issue , 2012, Pages

  Chavez, Miquella G ^a   Buhr, Christian A ^b   Petrie, Whitney K ^c   Wandinger Ness, Angela ^d   Kusewitt, Donna F ^e   Hudson, Laurie G ^b,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESMOGLEIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MATRIX METALLOPROTEINASE INHIBITOR; RAB11 PROTEIN; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL ADHESION; CONTROLLED STUDY; DOWN REGULATION; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MALE; MOUSE; NONHUMAN; WOUND;

EID: 84866249558     PISSN: None     EISSN: 16876113     Source Type: Journal    
DOI: 10.1155/2012/309587     Document Type: Article

References (87)

1. Arnoux V., Come C., Kusewitt D., Hudson L., Savagner P., Savagner P., Cutaneous wound reepithelializaton: a partial and reversible EMT. Rise and Fall of Epithelial Phenotype: Concepts of Epithelial-Mesenchymal Transition 2005 Berlin, Germany Springer 111 134
2. Thiery J. P., Acloque H., Huang R. Y. J., Nieto M. A., Epithelial-mesenchymal transitions in development and disease. Cell 2009 139 5 871 890 2-s2.0-70450198396 10.1016/j.cell.2009.11.007
3. Nakamura M., Tokura Y., Epithelial-mesenchymal transition in the skin. Journal of Dermatological Science 2011 61 1 7 13 2-s2.0-78650678823 10.1016/j.jdermsci.2010.11.015
4. Kalluri R., Weinberg R. A., The basics of epithelial-mesenchymal transition. Journal of Clinical Investigation 2009 119 6 1420 1428 2-s2.0-67650999875 10.1172/JCI39104
5. Kuwahara M., Hatoko M., Tada H., Tanaka A., E-cadherin expression in wound healing of mouse skin. Journal of Cutaneous Pathology 2001 28 4 191 199 2-s2.0-0035077311 10.1034/j.1600-0560.2001.028004191.x
6. Danjo Y., Gipson I. K., Actin purse string filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement. Journal of Cell Science 1998 111, part 22 3323 3332 2-s2.0-0031797018
7. Krawczyk W. S., Wilgram G. F., Hemidesmosome and desmosome morphogenesis during epidermal wound healing. Journal of Ultrastructure Research 1973 45 1-2 93 101 2-s2.0-0015815368
8. Sciubba J. J., Waterhouse J. P., Meyer J., A fine structural comparison of the healing of incisional wounds of mucosa and skin. Journal of Oral Pathology 1978 7 4 214 227 2-s2.0-0018150422
9. Mariner D. J., Davis M. A., Reynolds A. B., EGFR signaling to p120-catenin through phosphorylation at Y228. Journal of Cell Science 2004 117 8 1339 1350 2-s2.0-2342420097 10.1242/jcs.01001
10. Lorch J. H., Klessner J., Park J. K., Getsios S., Wu Y. L., Stack M. S., Green K. J., Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens intercellular adhesion in squamous cell carcinoma cells. Journal of Biological Chemistry 2004 279 35 37191 37200 2-s2.0-4344680669 10.1074/jbc.M405123200
11. Brown M. V., Burnett P. E., Denning M. F., Reynolds A. B., PDGF receptor activation induces p120-catenin phosphorylation at serine 879 via a PKC α -dependent pathway. Experimental Cell Research 2009 315 1 39 49 2-s2.0-56949098275 10.1016/j.yexcr.2008.09.025
12. Gaudry C. A., Palka H. L., Dusek R. L., Huen A. C., Khandekar M. J., Hudson L. G., Green K. J., Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. Journal of Biological Chemistry 2001 276 27 24871 24880 2-s2.0-0035816721 10.1074/jbc.M102731200
13. Jiang R., Shi Z., Johnson J. J., Liu Y., Stack M. S., stackm@missouri.edu Kallikrein-5 promotes cleavage of desmoglein-1 and loss of cell-cell cohesion in oral squamous cell carcinoma. Journal of Biological Chemistry 2011 286 11 9127 9135 10.1074/jbc.M110.191361
14. Simpson C. L., Kojima S. I., Cooper-Whitehair V., Getsios S., Green K. J., Plakoglobin rescues adhesive defects induced by ectodomain truncation of the desmosomal cadherin desmoglein 1: implications for exfoliative toxin-mediated skin blistering. American Journal of Pathology 2010 177 6 2921 2937 2-s2.0-78649515383 10.2353/ajpath.2010.100397
15. Cirillo N., Campisi G., Gombos F., Perillo L., Femiano F., Lanza A., Cleavage of desmoglein 3 can explain its depletion from keratinocytes in pemphigus vulgaris. Experimental Dermatology 2008 17 10 858 863 2-s2.0-51949092571 10.1111/j.1600-0625.2008.00719.x
16. Dahl K. D. C., Symowicz J., Ning Y., Gutierrez E., Fishman D. A., Adley B. P., Stack M. S., Hudson L. G., Matrix metalloproteinase 9 is a mediator of epidermal growth factor-dependent E-cadherin loss in ovarian carcinoma cells. Cancer Research 2008 68 12 4606 4613 2-s2.0-49649098028 10.1158/0008-5472.CAN- 07-5046
17. Ryniers F., Stove C., Goethals M., Brackenier L., Noë V., Bracke M., Vandekerckhove J., Mareel M., Bruyneel E., Plasmin produces an E-cadherin fragment that stimulates cancer cell invasion. Biological Chemistry 2002 383 1 159 165 2-s2.0-0036005969 10.1515/BC.2002.016
18. Noë V., Fingleton B., Jacobs K., Crawford H. C., Vermeulen S., Steelant W., Bruyneel E., Matrisian L. M., Mareel M., Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. Journal of Cell Science 2001 114, part 1 111 118 2-s2.0-0035147313
19. Bryant D. M., Kerr M. C., Hammond L. A., Joseph S. R., Mostov K. E., Teasdale R. D., Stow J. L., EGF induces macropinocytosis and SNX1-modulated recycling of E-cadherin. Journal of Cell Science 2007 120, part 10 1818 1828 2-s2.0-34250628372 10.1242/jcs.000653
20. Calkins C. C., Setzer S. V., Jennings J. M., Summers S., Tsunoda K., Amagai M., Kowalczyk A. P., Desmoglein endocytosis and desmosome disassembly are coordinated responses to pemphigus autoantibodies. Journal of Biological Chemistry 2006 281 11 7623 7634 2-s2.0-33645227215 10.1074/jbc.M512447200
21. Cirillo N., Gombos F., Lanza A., Changes in desmoglein 1 expression and subcellular localization in cultured keratinocytes subjected to anti-desmoglein 1 pemphigus autoimmunity. Journal of Cellular Physiology 2007 210 2 411 416 2-s2.0-33845656934 10.1002/jcp.20856
22. Delva E., Jennings J. M., Calkins C. C., Kottke M. D., Faundez V., Kowalczyk A. P., Pemphigus vulgaris IgG-induced desmoglein-3 endocytosis and desmosomal disassembly are mediated by a clathrin- and dynamin-independent mechanism. Journal of Biological Chemistry 2008 283 26 18303 18313 2-s2.0-49649095012 10.1074/jbc.M710046200
23. Jennings J. M., Tucker D. K., Kottke M. D., Saito M., Delva E., Hanakawa Y., Amagai M., Kowalczyk A. P., akowalc@emory.edu Desmosome disassembly in response to pemphigus vulgaris IgG occurs in distinct phases and can be reversed by expression of exogenous Dsg3. Journal of Investigative Dermatology 2011 131 3 706 718 10.1038/jid.2010.389
24. Miyashita Y., Ozawa M., Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. Journal of Biological Chemistry 2007 282 15 11540 11548 2-s2.0-34249663775 10.1074/jbc.M608351200
25. Palacios F., Tushir J. S., Fujita Y., D'Souza-Schorey C., Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Molecular and Cellular Biology 2005 25 1 389 402 2-s2.0-11144296871 10.1128/MCB.25.1.389-402.2005
26. Xiao K., Garner J., Buckley K. M., Vincent P. A., Chiasson C. M., Dejana E., Faundez V., Kowalczyk A. P., p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Molecular Biology of the Cell 2005 16 11 5141 5151 2-s2.0-27644506192 10.1091/mbc.E05-05-0440
27. Wallis S., Lloyd S., Wise I., Ireland G., Fleming T. P., Garrod D., The α isoform of protein kinase C is involved in signaling the response of desmosomes to wounding in cultured epithelial cells. Molecular Biology of the Cell 2000 11 3 1077 1092 2-s2.0-0034020357
28. Stoscheck C. M., Nanney L. B., King L. E. Jr., Quantitative determining of EGF-R during epidermal wound healing. Journal of Investigative Dermatology 1992 99 5 645 649 2-s2.0-0026447907
29. Wenczak B. A., Lynch J. B., Nanney L. B., Epidermal growth factor receptor distribution in burn wounds. Implications for growth factor-mediated repair. Journal of Clinical Investigation 1992 90 6 2392 2401 2-s2.0-0027050983
30. Repertinger S. K., Campagnaro E., Fuhrman J., El-Abaseri T., Yuspa S. H., Hansen L. A., EGFR enhances early healing after cutaneous incisional wounding. Journal of Investigative Dermatology 2004 123 5 982 989 2-s2.0-6344270007 10.1111/j.0022-202X.2004.23478.x
31. Barrientos S., Stojadinovic O., Golinko M. S., Brem H., Tomic-Canic M., Growth factors and cytokines in wound healing. Wound Repair and Regeneration 2008 16 5 585 601 2-s2.0-51349167276 10.1111/j.1524-475X.2008.00410.x
32. Hardwicke J., Schmaljohann D., Boyce D., Thomas D., Epidermal growth factor therapy and wound healingpast, present and future perspectives. Surgeon 2008 6 3 172 177 2-s2.0-45249103749
33. Shirley S. H., Hudson L. G., He J., Kusewitt D. F., The skinny on slug. Molecular Carcinogenesis 2010 49 10 851 861 2-s2.0-77958149240 10.1002/mc.20674
34. Kusewitt D. F., Choi C., Newkirk K. M., Leroy P., Li Y., Chavez M. G., Hudson L. G., Slug/Snai2 is a downstream mediator of epidermal growth factor receptor-stimulated reepithelialization. Journal of Investigative Dermatology 2009 129 2 491 495 2-s2.0-58549116088 10.1038/jid.2008.222
35. McCawley L. J., Li S., Wattenberg E. V., Hudson L. G., Sustained activation of the mitogen-activated protein kinase pathway: a mechanism underlying receptor tyrosine kinase specificity for matrix metalloproteinase-9 induction and cell migration. Journal of Biological Chemistry 1999 274 7 4347 4353 2-s2.0-0033548181 10.1074/jbc.274.7.4347
36. McCawley L. J., O'Brien P., Hudson L. G., Overexpression of the epidermal growth factor receptor contributes to enhanced ligand-mediated motility in keratinocyte cell lines. Endocrinology 1997 138 1 121 127 2-s2.0-0031022707 10.1210/en.138.1.121
37. Hudson L. G., Newkirk K. M., Chandler H. L., Choi C., Fossey S. L., Parent A. E., Kusewitt D. F., Cutaneous wound reepithelialization is compromised in mice lacking functional Slug (Snai2). Journal of Dermatological Science 2009 56 1 19 26 2-s2.0-69049106307 10.1016/j.jdermsci.2009.06.009
38. Clark R. A. F., The Molecular and Cellular Biology of Wound Repair 1988 New York, NY, USA Plenum Press
39. Moll I., Houdek P., Schäfer S., Nuber U., Moll R., Diversity of desmosomal proteins in regenerating epidermis: immunohistochemical study using a human skin organ culture model. Archives of Dermatological Research 1999 291 7-8 437 446 2-s2.0-0032841919 10.1007/s004030050435
40. Nanney L. B., Paulsen S., Davidson M. K., Cardwell N. L., Whitsitt J. S., Davidson J. M., Boosting epidermal growth factor receptor expression by gene gun transfection stimulates epidermal growth in vivo. Wound Repair and Regeneration 2000 8 2 117 127 2-s2.0-0034051546 10.1046/j.1524-475X.2000.00117.x
41. Hudson L. G., McCawley L. J., Contributions of the epidermal growth factor receptor to keratinocyte motility. Microscopy Research and Technique 1998 43 5 444 455 2-s2.0-0032387827 10.1002/(SICI)1097-0029(19981201)43:5444::AID- JEMT10>3.0.CO;2-C
42. Bhora F. Y., Dunkin B. J., Batzri S., Aly H. M., Bass B. L., Sidawy A. N., Harmon J. W., Effect of growth factors on cell proliferation and epithelialization in human skin. Journal of Surgical Research 1995 59 2 236 244 2-s2.0-0029089228 10.1006/jsre.1995.1160
43. Hudson L. G., Toscano W. A. Jr., Greenlee W. F., 2,3,7,8- Tetrachlorodibenzo-p-dioxin (TCDD) modulates epidermal growth factor (EGF) binding to basal cells from a human keratinocyte cell line1. Toxicology and Applied Pharmacology 1986 82 3 481 492 2-s2.0-0022644237
44. Pittelkow M. R., Cook P. W., Shipley G. D., Derynck R., Coffey R. J., Autonomous growth of human keratinocytes requires epidermal growth factor receptor occupancy. Cell Growth & Differentiation 1993 4 6 513 521 2-s2.0-0027613333
45. Shibamoto S., Hayakawa M., Takeuchi K., Hori T., Oku N., Miyazawa K., Kitamura N., Takeichi M., Ito F., Tyrosine phosphorylation of β -catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhesion and Communication 1994 1 4 295 305
46. Hazan R. B., Norton L., The epidermal growth factor receptor modulates the interaction of E- cadherin with the actin cytoskeleton. Journal of Biological Chemistry 1998 273 15 9078 9084 2-s2.0-0032502669 10.1074/jbc.273.15.9078
47. Moon H. S., Choi E. A., Park H. Y., Choi J. Y., Chung H. W., Kim J. I., Park W. I., Expression and tyrosine phosphorylation of E-cadherin, β-and γ -catenin, and epidermal growth factor receptor in cervical cancer cells. Gynecologic Oncology 2001 81 3 355 359 10.1006/gyno.2001.6163
48. Bolós V., Peinado H., Pérez-Moreno M. A., Fraga M. F., Esteller M., Cano A., The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. Journal of Cell Science 2003 116, part 3 499 511 2-s2.0-0037326569 10.1242/jcs.00224
49. Guaita S., Puig I., Francí C., Garrido M., Domínguez D., Batlle E., Sancho E., Dedhar S., De Herreros A. G., Baulida J., Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. Journal of Biological Chemistry 2002 277 42 39209 39216 2-s2.0-0037131409 10.1074/jbc.M206400200
50. Bryant D. M., Wylie F. G., Stow J. L., Regulation of endocytosis, nuclear translocation, and signaling of fibroblast growth factor receptor 1 by E-cadherin. Molecular Biology of the Cell 2005 16 1 14 23 2-s2.0-11144274556 10.1091/mbc.E04-09-0845
51. Kamei T., Matozaki T., Sakisaka T., Kodama A., Yokoyama S., Peng Y. F., Nakano K., Takaishi K., Takai Y., Coendocytosis of cadherin and c-Met coupled to disruption of cell-cell adhesion in MDCK cellsregulation by Rho, Rac and Rab small G proteins. Oncogene 1999 18 48 6776 6784 2-s2.0-0033581834
52. Palacios F., Schweitzer J. K., Boshans R. L., D'Souza-Schorey C., ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nature Cell Biology 2002 4 12 929 936 2-s2.0-0036902709 10.1038/ncb881
53. Ning Y., Buranda T., Hudson L. G., Activated epidermal growth factor receptor induces integrin α 2 internalization via caveolae/raft-dependent endocytic pathway. Journal of Biological Chemistry 2007 282 9 6380 6387 2-s2.0-34250348787 10.1074/jbc.M610915200
54. Lu Z., Ghosh S., Wang Z., Hunter T., Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β -catenin, and enhanced tumor cell invasion. Cancer Cell 2003 4 6 499 515 2-s2.0-0345736990 10.1016/S1535-6108(03)00304-0
55. Huang F., Khvorova A., Marshall W., Sorkin A., Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. Journal of Biological Chemistry 2004 279 16 16657 16661 2-s2.0-1942469322 10.1074/jbc.C400046200
56. Sigismund S., Argenzio E., Tosoni D., Cavallaro E., Polo S., di Fiore P. P., Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Developmental Cell 2008 15 2 209 219 2-s2.0-48549088895 10.1016/j.devcel.2008.06.012
57. Khan E. M., Heidinger J. M., Levy M., Lisanti M. P., Ravid T., Goldkorn T., Epidermal growth factor receptor exposed to oxidative stress undergoes Src- and caveolin-1-dependent perinuclear trafficking. Journal of Biological Chemistry 2006 281 20 14486 14493 2-s2.0-33646141025 10.1074/jbc.M509332200
58. Manders E. M. M., Verbeek F. J., Aten J. A., Measurement of co-localization of objects in dual-colour confocal images. Journal of Microscopy 1993 169 3 375 382 2-s2.0-0027418205
59. Lewis J. E., Wahl J. K., Sass K. M., Jensen P. J., Johnson K. R., Wheelock M. J., Cross-talk between adherens junctions and desmosomes depends on plakoglobin. Journal of Cell Biology 1997 136 4 919 934 2-s2.0-0031029677 10.1083/jcb.136.4.919
60. Garrod D., Chidgey M., Desmosome structure, composition and function. Biochimica et Biophysica Acta 2008 1778 3 572 587 2-s2.0-39849097562 10.1016/j.bbamem.2007.07.014
61. Maretzky T., Reiss K., Ludwig A., Buchholz J., Scholz F., Proksch E., de Strooper B., Hartmann D., Saftig P., ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and β -catenin translocation. Proceedings of the National Academy of Sciences of the United States of America 2005 102 26 9182 9187 2-s2.0-21544467772 10.1073/pnas. 0500918102
62. Najy A. J., Day K. C., Day M. L., The ectodomain shedding of E-cadherin by ADAM15 supports ErbB receptor activation. Journal of Biological Chemistry 2008 283 26 18393 18401 2-s2.0-49649103585 10.1074/jbc.M801329200
63. Johnson S. K., Ramani V. C., Hennings L., Haun R. S., Kallikrein 7 enhances pancreatic cancer cell invasion by shedding E-cadherin. Cancer 2007 109 9 1811 1820 2-s2.0-34247597726 10.1002/cncr.22606
64. Marambaud P., Shioi J., Serban G., Georgakopoulos A., Sarner S., Nagy V., Baki L., Wen P., Efthimiopoulos S., Shao Z., Wisniewski T., Robakis N. K., A presenilin-1/ γ -secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO Journal 2002 21 8 1948 1956 2-s2.0-18344380083 10.1093/emboj/21.8.1948
65. Ferber E. C., Kajita M., Wadlow A., Tobiansky L., Niessen C., Ariga H., Daniel J., Fujita Y., A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. Journal of Biological Chemistry 2008 283 19 12691 12700 2-s2.0-45149113604 10.1074/jbc.M708887200
66. Wilkins-Port C. E., Ye Q., Mazurkiewicz J. E., Higgins P. J., TGF- β 1 + EGF-initiated invasive potential in transformed human keratinocytes is coupled to a plasmin/mmp-10/mmp-1-dependent collagen remodeling axis: role for PAI-1. Cancer Research 2009 69 9 4081 4091 2-s2.0-65949087684 10.1158/0008-5472.CAN-09-0043
67. Dahl K. D. C., Zeineldin R., Hudson L. G., PEA3 is necessary for optimal epidermal growth factor receptor-stimulated matrix metalloproteinase expression and invasion of ovarian tumor cells. Molecular Cancer Research 2007 5 5 413 421 2-s2.0-34250180482 10.1158/1541-7786.MCR-07-0019
68. 2+ and matrix metalloproteinase-9 in primary keratinocyte migration. Wound Repair and Regeneration 2007 15 6 907 915 2-s2.0-36249014208 10.1111/j.1524-475X.2007.00315.x
69. Charvat S., Chignol M. C., Souchier C., le Griel C., Schmitt D., Serres M., Cell migration and MMP-9 secretion are increased by epidermal growth factor in HaCaT-ras transfected cells. Experimental Dermatology 1998 7 4 184 190 2-s2.0-0031657969
70. Park S., Jung H. H., Park Y. H., Ahn J. S., Im Y. H., imyh00@skku.edu ERK/MAPK pathways play critical roles in EGFR ligands-induced MMP1 expression. Biochemical and Biophysical Research Communications 2011 407 4 680 686 10.1016/j.bbrc.2011.03.075
71. Hudson L. G., Moss N. M., Stack M. S., EGF-receptor regulation of matrix metalloproteinases in epithelial ovarian carcinoma. Future Oncology 2009 5 3 323 338 2-s2.0-66949178329 10.2217/fon.09.10
72. Izumi G., Sakisaka T., Baba T., Tanaka S., Morimoto K., Takai Y., Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. Journal of Cell Biology 2004 166 2 237 248 2-s2.0-3342986329 10.1083/jcb.200401078
73. Ivanov A. I., Nusrat A., Parkos C. A., Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Molecular Biology of the Cell 2004 15 1 176 188 2-s2.0-0347360336 10.1091/mbc.E03-05-0319
74. Le T. L., Yap A. S., Stow J. L., Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. Journal of Cell Biology 1999 146 1 219 232 2-s2.0-0001331879 10.1083/jcb.146.1.219
75. Paterson A. D., Parton R. G., Ferguson C., Stow J. L., Yap A. S., Characterization of E-cadherin endocytosis in isolated MCF-7 and Chinese hamster ovary cells. The initial fate of unbound E-cadherin. Journal of Biological Chemistry 2003 278 23 21050 21057 2-s2.0-0038418651 10.1074/jbc.M300082200
76. Akhtar N., Hotchin N. A., Rac1 regulates adherens junctions through endocytosis of E-cadherin. Molecular Biology of the Cell 2001 12 4 847 862 2-s2.0-0035158750
77. Bryant D. M., Stow J. L., The ins and outs of E-cadherin trafficking. Trends in Cell Biology 2004 14 8 427 434 2-s2.0-4143146438 10.1016/j.tcb.2004. 07.007
78. D'Souza-Schorey C., Disassembling adherens junctions: breaking up is hard to do. Trends in Cell Biology 2005 15 1 19 26 2-s2.0-11844276068 10.1016/j.tcb.2004.11.002
79. Klessner J. L., Desai B. V., Amargo E. V., Getsios S., Green K. J., EGFR and ADAMs cooperate to regulate shedding and endocytic trafficking of the desmosomal cadherin desmoglein 2. Molecular Biology of the Cell 2009 20 1 328 337 2-s2.0-63049110385 10.1091/mbc.E08-04-0356
80. Santiago-Josefat B., Esselens C., Bech-Serra J. J., Arribas J., Post-transcriptional up-regulation of ADAM17 upon epidermal growth factor receptor activation and in breast tumors. Journal of Biological Chemistry 2007 282 11 8325 8331 2-s2.0-34247236142 10.1074/jbc.M608826200
81. Bech-Serra J. J., Santiago-Josefat B., Esselens C., Saftig P., Baselga J., Arribas J., Canals F., Proteomic identification of desmoglein 2 and activated leukocyte cell adhesion molecule as substrates of ADAM17 and ADAM10 by difference gel electrophoresis. Molecular and Cellular Biology 2006 26 13 5086 5095 2-s2.0-33745477470 10.1128/MCB.02380-05
82. Heupel W. M., Engerer P., Schmidt E., Waschke J., Pemphigus vulgaris IgG cause loss of desmoglein-mediated adhesion and keratinocyte dissociation independent of epidermal growth factor receptor. American Journal of Pathology 2009 174 2 475 485 2-s2.0-59649096544 10.2353/ajpath.2009.080392
83. Chernyavsky A. I., Arredondo J., Kitajima Y., Sato-Nagai M., Grando S. A., Desmoglein versus non-desmoglein signaling in pemphigus acantholysis: characterization of novel signaling pathways downstream of pemphigus vulgaris antigens. Journal of Biological Chemistry 2007 282 18 13804 13812 2-s2.0-34250354415 10.1074/jbc.M611365200
84. Frušić-Zlotkin M., Raichenberg D., Wang X., David M., Michel B., Milner Y., Apoptotic mechanism in pemphigus autoimmunoglobulins- induced acantholysispossible involvement of the EGF receptor. Autoimmunity 2006 39 7 563 575 2-s2.0-33751085125 10.1080/08916930600971836
85. Acloque H., Adams M. S., Fishwick K., Bronner-Fraser M., Nieto M. A., Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. Journal of Clinical Investigation 2009 119 6 1438 1449 2-s2.0-67650996280 10.1172/JCI38019
86. Shaye D. D., Casanova J., Llimargas M., Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nature Cell Biology 2008 10 8 964 970 2-s2.0-48649098952 10.1038/ncb1756
87. Revenu C., Gilmour D., EMT 2.0: shaping epithelia through collective migration. Current Opinion in Genetics and Development 2009 19 4 338 342 2-s2.0-68949155116 10.1016/j.gde.2009.04.007