Transmembrane collagen XVII modulates integrin dependent keratinocyte migration via PI3K/Rac1 signaling

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Löffek, Stefanie ^a   Hurskainen, Tiina ^b   Jackow, Joanna ^a   Sigloch, Florian Christoph ^c   Schilling, Oliver ^c   Tasanen, Kaisa ^b   Bruckner Tuderman, Leena ^a,c   Franzke, Claus Werner ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF OULU   (Finland)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA4 INTEGRIN; COLLAGEN TYPE 17; FOCAL ADHESION KINASE; INTEGRIN; LAMININ; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIZATION; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; KERATINOCYTE; LAMELLIPODIUM; MOUSE; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; WOUND;

ANIMALS; ANTIGENS, CD29; AUTOANTIGENS; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL ADHESION MOLECULES; CELL MOVEMENT; FOCAL ADHESION KINASE 1; INTEGRIN BETA4; KERATINOCYTES; MICE; MICE, KNOCKOUT; NEOPLASM INVASIVENESS; NEUROPEPTIDES; NON-FIBRILLAR COLLAGENS; PHOSPHATIDYLINOSITOL 3-KINASES; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; WOUND HEALING;

EID: 84895545504     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087263     Document Type: Article

References (38)

1. Bruckner-Tuderman L, Has C (2012) Molecular heterogeneity of blistering disorders: the paradigm of epidermolysis bullosa. J Invest Dermatol 132, E2-5.
2. Tsuruta D, Hashimoto T, Hamill KJ, Jones JC (2011) Hemidesmosomes and focal contact proteins: functions and cross-talk in keratinocytes, bullous diseases and wound healing. J Dermatol Sci 62, 1-7.
3. Nievers MG, Schaapveld RQ, Sonnenberg A (1999) Biology and function of hemidesmosomes. Matrix Biol 18, 5-17. (Pubitemid 29213823)
4. Carragher NO, Frame MC (2004) Focal adhesion and actin dynamics: a place where kinases and proteases meet to promote invasion. Trends Cell Biol 14, 241-9. (Pubitemid 38591328)
5. Schober M, Raghavan S, Nikolova M, Polak L, Pasolli HA, et al. (2007) Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol 176, 667-80. (Pubitemid 46333981)
6. Tasanen K, Tunggal L, Chometon G, Bruckner-Tuderman L, Aumailley M (2004) Keratinocytes from patients lacking collagen XVII display a migratory phenotype. Am J Pathol 164, 2027-38. (Pubitemid 38669351)
7. Franzke C-W, Has C, Schulte C, Huilaja L, Tasanen K, et al. (2006) C-terminal truncation impairs glycosylation of transmembrane collagen XVII and leads to intracellular accumulation. J Biol Chem 281, 30260-8. (Pubitemid 44537033)
8. Leivo T, Kiistala U, Vesterinen M, Owaribe K, Burgeson RE, et al. (2000) Reepithelialization rate and protein expression in the suction-induced wound model: comparison between intact blisters, open wounds and calcipotriol- pretreated open wounds. The British journal of dermatology 142, 991-1002. (Pubitemid 30304614)
9. Dabelsteen E, Gron B, Mandel U, Mackenzie I (1998) Altered expression of epithelial cell surface glycoconjugates and intermediate filaments at the margins of mucosal wounds. J Invest Dermatol 111, 592-7. (Pubitemid 28452318)
10. Parikka M, Nissinen L, Kainulainen T, Bruckner-Tuderman L, Salo T, et al. (2006) Collagen XVII promotes integrin-mediated squamous cell carcinoma transmigration - a novel role for alphaIIb integrin and tirofiban. Exp Cell Res 312, 1431-8.
11. Stelkovics E, Korom I, Marczinovits I, Molnar J, Rasky K, et al. (2008) Collagen XVII/BP180 protein expression in squamous cell carcinoma of the skin detected with novel monoclonal antibodies in archived tissues using tissue microarrays and digital microscopy. Applied immunohistochemistry & molecular morphology: AIMM/official publication of the Society for Applied Immunohistochemistry 16, 433-41.
12. Hurskainen T, Moilanen J, Sormunen R, Franzke C-W, Soininen R, et al. (2012) Transmembrane collagen XVII is a novel component of the glomerular filtration barrier. Cell Tissue Res 348, 579-88.
13. Franzke C-W, Bruckner-Tuderman L, Blobel CP (2009) Shedding of collagen XVII/BP180 in skin depends on both ADAM10 and ADAM9. J Biol Chem 284, 23386-96.
14. König A, Lauharanta J, Bruckner-Tuderman L (1992) Keratinocytes and fibroblasts from a patient with mutilating dystrophic epidermolysis bullosa synthesize drastically reduced amounts of collagen VII: lack of effect of transforming growth factor-beta. J Invest Dermatol 99, 808-12. (Pubitemid 23002046)
15. Franzke C-W, Tasanen K, Schacke H, Zhou Z, Tryggvason K, et al. (2002) Transmembrane collagen XVII, an epithelial adhesion protein, is shed from the cell surface by ADAMs. EMBO J 21, 5026-35.
16. Frijns E, Sachs N, Kreft M, Wilhelmsen K, Sonnenberg A (2011) EGF-induced MAPK signaling inhibits hemidesmosome formation through phosphorylation of the integrin {beta}4. J Biol Chem 285, 37650-62.
17. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76, 4350-4. (Pubitemid 9256559)
18. Schumann H, Hammami-Hauasli N, Pulkkinen L, Mauviel A, Kuster W, et al. (1997) Three novel homozygous point mutations and a new polymorphism in the COL17A1 gene: relation to biological and clinical phenotypes of junctional epidermolysis bullosa. Am J Hum Genet 60, 1344-53. (Pubitemid 27258066)
19. Nishie W, Sawamura D, Goto M, Ito K, Shibaki A, et al. (2007) Humanization of autoantigen. Nat Med 13, 378-83. (Pubitemid 46376680)
20. Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM (2010) Mechanical integration of actin and adhesion dynamics in cell migration. Annual review of cell and developmental biology 26, 315-33.
21. Golubovskaya VM, Nyberg C, Zheng M, Kweh F, Magis A, et al. (2008) A small molecule inhibitor, 1,2,4,5-benzenetetraamine tetrahydrochloride, targeting the y397 site of focal adhesion kinase decreases tumor growth. Journal of medicinal chemistry 51, 7405-16.
22. Fukata M, Nakagawa M, Kaibuchi K (2003) Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 15, 590-7. (Pubitemid 37176968)
23. Petrie RJ, Doyle AD, Yamada KM (2009) Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10, 538-49.
24. Shaw LM, Rabinovitz I, Wang HH, Toker A, Mercurio AM (1997) Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell 91, 949-60. (Pubitemid 28027828)
25. Shaw LM (2001) Identification of insulin receptor substrate 1 (IRS-1) and IRS-2 as signaling intermediates in the alpha6beta4 integrin-dependent activation of phosphoinositide 3-OH kinase and promotion of invasion. Mol Cell Biol 21, 5082-93.
26. Gambaletta D, Marchetti A, Benedetti L, Mercurio AM, Sacchi A, et al. (2000) Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J Biol Chem 275, 10604-10. (Pubitemid 30202127)
27. Mercurio AM, Rabinovitz I, Shaw LM (2001) The alpha 6 beta 4 integrin and epithelial cell migration. Curr Opin Cell Biol 13, 541-5. (Pubitemid 32817011)
28. Germain EC, Santos TM, Rabinovitz I (2009) Phosphorylation of a novel site on the {beta}4 integrin at the trailing edge of migrating cells promotes hemidesmosome disassembly. Mol Biol Cell 20, 56-67.
29. Mainiero F, Murgia C, Wary KK, Curatola AM, Pepe A, et al. (1997) The coupling of alpha6beta4 integrin to Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J 16, 2365-75. (Pubitemid 27260377)
30. Mariotti A, Kedeshian PA, Dans M, Curatola AM, Gagnoux-Palacios L, et al. (2001) EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J Cell Biol 155, 447-58.
31. Margadant C, Charafeddine RA, Sonnenberg A (2010) Unique and redundant functions of integrins in the epidermis. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 24, 4133-52.
32. Rabinovitz I, Toker A, Mercurio AM (1999) Protein kinase C-dependent mobilization of the alpha6beta4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J Cell Biol 146, 1147-60.
33. Qiao H, Shibaki A, Long HA, Wang G, Li Q, et al. (2009) Collagen XVII participates in keratinocyte adhesion to collagen IV, and in p38MAPK-dependent migration and cell signaling. J Invest Dermatol 129, 2288-95.
34. Hamill KJ, Hopkinson SB, Jonkman MF, Jones JC (2011) Type XVII collagen regulates lamellipod stability, cell motility, and signaling to Rac1 by targeting bullous pemphigoid antigen 1e to alpha6beta4 integrin. J Biol Chem 286, 26768-80.
35. Sehgal BU, DeBiase PJ, Matzno S, Chew TL, Claiborne JN, et al. (2006) Integrin beta4 regulates migratory behavior of keratinocytes by determining laminin-332 organization. J Biol Chem 281, 35487-98. (Pubitemid 46036585)
36. Beaulieu JF (1997) Extracellular matrix components and integrins in relationship to human intestinal epithelial cell differentiation. Prog Histochem Cytochem 31, 1-78.
37. Kashyap T, Germain E, Roche M, Lyle S, Rabinovitz I (2011) Role of beta4 integrin phosphorylation in human invasive squamous cell carcinoma: regulation of hemidesmosome stability modulates cell migration. Laboratory investigation; a journal of technical methods and pathology 91, 1414-26.
38. Kligys KR, Wu Y, Hopkinson SB, Kaur S, Platanias LC, et al. (2012) alpha6beta4 integrin: a master regulator of the expression of integrins in human keratinocytes. J Biol Chem.