Laminin-5-deficient human keratinocytes: Defective adhesion results in a saltatory and inefficient mode of migration

Experimental Cell Research

Volumn 313, Issue 8, 2007, Pages 1575-1587

  Hartwig, Benedikt ^a,b   Borm, Bodo ^a,c   Schneider, Holm ^d   Arin, Meral J ^b   Kirfel, Gregor ^a   Herzog, Volker ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cell adhesion; Cell migration; Junctional epidermolysis bullosa; Keratinocytes; Laminin 5 deficiency; Saltatory migration

Indexed keywords

ALPHA5 INTEGRIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; KALININ;

ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; EPIDERMIS; EPIDERMOLYSIS BULLOSA; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MICROSCOPY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SKIN BIOPSY; WOUND HEALING;

EID: 34247152600     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.02.003     Document Type: Article

References (70)

1. Stossel T.P. On the crawling of animal cells. Science 21 (1993) 1086-1094
2. Sheetz M.P. Cell migration by graded attachment to substrates and contraction. Semin. Cell Biol. 5 (1994) 149-155
3. Lauffenburger D.A., and Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 84 (1996) 359-369
4. Mitchison T.J., and Cramer L.P. Actin-based cell motility and cell locomotion. Cell 84 (1996) 371-379
5. Buck C.A., and Horwitz A.F. Cell surface receptors for extracellular matrix molecules. Annu. Rev. Cell Biol. 3 (1987) 179-205
6. Ruoshlati E., and Pierschbacher M.D. New perspectives in cell adhesion: RGD and integrins. Science 238 (1987) 491-497
7. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69 (1992) 11-25
8. Sonnenberg A. Integrins and their ligands. Curr. Top. Microbiol. Immunol. 184 (1993) 7-35
9. Damsky C.H., and Ilic D. Integrin signaling: it's where the action is. Curr. Opin. Cell Biol. 14 (2002) 594-602
10. Gil S.G., Brown T.A., Ryan M.C., and Carter W.G. Junctional epidermolysis bullosis: defects in expression of epiligrin/nicein/kalinin and integrin beta 4 that inhibit hemidesmosome formation. J. Invest. Dermatol. 103 (1994) 31S-38S
11. Nguyen B.P., Ren X.D., Schwartz M.A., and Carter W.G. Ligation of integrin alpha 3beta 1 by laminin 5 at the wound edge activates Rho-dependent adhesion of leading keratinocytes on collagen. J. Biol. Chem. 276 (2001) 43860-43870
12. Timpl R. Macromolecular organization of basement membranes. Curr. Opin. Cell Biol. 8 (1996) 618-624
13. Burgeson R.E., Chiquet M., Deutzmann R., Ekblom P., Engel J., Kleinman H., Martin G.R., Meneguzzi G., Paulsson M., and Sanes J. A new nomenclature for the laminins. Matrix Biol. 14 (1994) 209-211
14. Koch M., Olson P.F., Albus A., Jin W., Hunter D.D., Brunken W.J., Burgeson R.E., and Champliaud M.F. Characterization and expression of the laminin gamma3 chain: a novel, non-basement membrane-associated, laminin chain. J. Cell Biol. 145 (1999) 605-618
15. Galliano M.F., Aberdam D., Aguzzi A., Ortonne J.P., and Meneguzzi G. Cloning and complete primary structure of the mouse laminin alpha 3 chain. Distinct expression pattern of the laminin alpha 3A and alpha 3B chain isoforms. J. Biol. Chem. 270 (1995) 21820-21826
16. Pegoraro E., Fanin M., Trevisan C.P., Angelini C., and Hoffman E.P. A novel laminin alpha2 isoform in severe laminin alpha2 deficient congenital muscular dystrophy. Neurology 55 (2000) 1128-1134
17. Beck K., Dixon T.W., Engel J., and Parry D.A. Ionic interactions in the coiled-coil domain of laminin determine the specificity of chain assembly. J. Mol. Biol. 23 1 (1993) 311-323
18. Marinkovich M.P., Lunstrum G.P., and Burgeson R.E. The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J. Biol. Chem. 267 (1992) 17900-17906
19. Carter W.G., Ryan M.C., and Gahr P.J. Epiligrin, a new cell adhesion ligand for integrin alpha 3 beta 1 in epithelial basement membranes. Cell 65 (1991) 599-610
20. Rousselle P., Lunstrum G.P., Keene D.R., and Burgeson R.E. Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol. 114 (1991) 567-576
21. Vailly J., Szepetowski P., Mattei M.G., Pedeutour F., Burgeson R., Ortonne J.P., and Meneguzzi G. The genes for nicein/kalinin 125-and 100-kDa subunits, candidates for junctional epidermolysis bullosa, map to chromosomes 1q32 and 1q25-q31. Genomics 21 (1994) 286-288
22. Aumailley M., Bruckner-Tuderman L., Carter W.G., Deutzmann R., Edgar D., Ekblom P., Engel J., Engvall E., Hohenester E., Jones J.C., Kleinman H.K., Marinkovich M.P., Martin G.R., Mayer U., Meneguzzi G., Miner J.H., Miyazaki K., Patarroyo M., Paulsson M., Quaranta V., Sanes J.R., Sasaki T., Sekiguchi K., Sorokin L.M., Talts J.L., Tryggvason K., Uitto J., Virtanen I., Von der Mark K., Wewer U.M., Yamada Y., and Yurchenco P.D. A simplified laminin nomenclature. Matrix Biol. 24 (2005) 326-332
23. Green K.J., and Jones J.C. Desmosomes and hemidesmosomes: structure and function of molecular components. FASEB J. 10 (1996) 871-881
24. Burgeson R.E., and Christiano A.M. The dermal-epidermal junction. Curr. Opin. Cell Biol. 9 (1997) 651-658
25. Fuchs E., Dowling J., Segre J., Lo S.H., and Yu Q.C. Integrators of epidermal growth and differentiation: distinct functions for beta 1 and beta 4 integrins. Curr. Opin. Genet Dev. 7 (1997) 672-682
26. Borradori L., and Sonnenberg A. Structure and function of hemidesmosomes: more than simple adhesion complexes. J. Invest. Dermatol. 112 (1999) 411-418
27. Lampe P.D., Nguyen B.P., Gil S., Usui M., Olerud J., Takada Y., and Carter W.G. Cellular interaction of integrin alpha3beta1 with laminin 5 promotes gap junctional communication. J. Cell Biol. 143 (1998) 1735-1747
28. Goldfinger L.E., Hopkinson S.B., deHart G.W., Collawn S., Couchman J.R., and Jones J.C. The alpha3 laminin subunit, alpha6beta4 and alpha3beta1 integrin coordinately regulate wound healing in cultured epithelial cells and in the skin. J. Cell Sci. 112 (1999) 2615-26129
29. Nguyen B.P., Gil S.G., and Carter W.G. Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J. Biol. Chem. 275 (2000) 31896-31907
30. Santoro M.M., Gaudino G., and Marchisio P.C. The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev. Cell 5 (2003) 257-271
31. Ryan M.C., Lee K., Miyashita Y., and Carter W.G. Targeted disruption of the LAMA3 gene in mice reveals abnormalities in survival and late stage differentiation of epithelial cells. J. Cell Biol. 145 (1999) 1309-1323
32. Xia Y., Gil S.G., and Carter W.G. Anchorage mediated by integrin alpha6beta4 to laminin-5 (epiligrin) regulates tyrosine phosphorylation of a membrane-associated 80-kD protein. J. Cell Biol. 132 (1996) 727-740
33. Hintermann E., Bilban M., Sharabi A., and Quaranta V. Inhibitory role of alpha 6 beta 4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on alpha 3 beta 1 integrin. J. Cell Biol. 153 (2001) 465-478
34. Zhang K., and Kramer R.H. Laminin 5 deposition promotes keratinocyte motility. Exp. Cell Res. 227 (1996) 309-322
35. Shang M., Koshikawa N., Schenk S., and Quaranta V. The LG3 module of laminin-5 harbors a binding site for integrin alpha3beta1 that promotes cell adhesion, spreading, and migration. J. Biol. Chem. 276 (2001) 33045-33053
36. O ́Toole E.A., Marinkovich M.P., Heffler W.K., Furthmayr H., and Woodley D.T. Laminin-5 inhibits human keratinocyte migration. Exp. Cell Res. 233 (1997) 330-339
37. Frank D.E., and Carter W.G. Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J. Cell Sci. 117 (2004) 1351-1363
38. Ryan M.C., Christiano A.M., Engvall E., Wewer U.M., Miner J.H., Sanes J.R., and Burgeson R.E. The functions of laminins: lessons from in vivo studies. Matrix Biol. 15 (1996) 369-381
39. Clark R.A.F. Wound repair. Overview and general consideration. In: Clark R.A.F. (Ed). The Molecular and Cellular Biology of Wound Repair (1995), Plenum Press, New York 3-50
40. Jonkman M.F. Hereditary skin diseases of hemodesmosomes. J. Dermatol. Sci. 20 (1999) 103-121
41. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., and Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106 (1988) 761-771
42. Muhle C., Jiang Q.J., Charlesworth A., Bruckner-Tuderman L., Meneguzzi G., and Schneider H. Novel and recurrent mutations in the laminin-5 genes causing lethal junctional epidermolysis bullosa: molecular basis and clinical course of Herlitz disease. Hum. Genet. 116 (2005) 33-42
43. Hinz B., Alt W., Johnen C., Herzog V., and Kaiser H.W. Quantifying lamella dynamics of cultured cells by SACED, a new computer-assisted motion analysis. Exp. Cell Res. 251 (1999) 234-243
44. Bear J.E., Svitkina T.M., Krause M., Schafer D.A., Loureiro J.J., Strasser G.A., Maly I.V., Chaga O.Y., Cooper J.A., Borisy G.G., and Gertler F.B. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109 (2002) 509-521
45. Curtis A.S. The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J. Cell Biol. 20 (1964) 199-215
46. Nakano A., Chao S.C., Pulkkinen L., Murrell D., Bruckner-Tuderman L., Pfendner E., and Uitto J. Laminin-5 mutations in junctional epidermolysis bullosa: molecular basis of Herlitz vs. non-Herlitz phenotypes. Hum. Genet. 110 (2002) 41-51
47. Borm B., Requardt R.P., Herzog V., and Kirfel G. Membrane ruffles in cell migration: indicators of inefficient lamellipodia adhesion and compartments of actin filament reorganization. Exp. Cell Res. 302 (2005) 83-95
48. Kirfel G., Rigort A., Borm B., Schulte C., and Herzog V. Structural and compositional analysis of the keratinocyte migration track. Cell Motil. Cytoskelet. 55 (2003) 1-13
49. Kirfel G., Borm B., Rigort A., and Herzog V. The secretory beta-amyloid precursor protein is a motogen for human epidermal keratinocytes. Eur. J. Cell Biol. 81 (2002) 664-676
50. Watt F.M., and Hertle M.D. Keratinocyte integrins. In: Leigh I.M., Lane B., and Watt F.M. (Eds). The Keratinocyte Handbook (1994), Cambridge University Press 153-164
51. Wu C., Bauer J.S., Juliano R.L., and McDonald J.A. The alpha 5 beta 1 integrin fibronectin receptor, but not the alpha 5 cytoplasmic domain, functions in an early and essential step in fibronectin matrix assembly. J. Biol. Chem. 268 (1993) 21883-21888
52. Zhang Z., Morla A.O., Vuori K., Bauer J.S., Juliano R.L., and Ruoslahti E. The alpha v beta 1 integrin functions as a fibronectin receptor but does not support fibronectin matrix assembly and cell migration on fibronectin. J. Cell Biol. 122 (1993) 235-242
53. Gu J., Sumida Y., Sanzen N., and Sekiguchi K. Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130(Cas)-CrkII-DOCK180 pathway. J. Biol. Chem. 276 (2001) 27090-27097
54. Kainulainen T., Hakkinen L., Hamidi S., Larjava K., Kallioinen M., Peltonen J., Salo T., Larjava H., and Oikarinen A. Laminin 5 expression is independent of the injury and the microenvironment during reepithelialization of wounds. J. Histochem. Cytochem. 46 (1998) 353-360
55. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Self-polarization and directional motility of cytoplasm. Curr. Biol. 9 (1999) 11-20
56. Kirfel G., and Herzog V. Migration of epidermal keratinocytes: mechanisms, regulation, and biological significance. Protoplasma 223 (2004) 67-78
57. Chernyavsky A.I., Arredondo J., Karlsson E., Wessler I., and Grando S.A. The Ras/Raf-1/MEK1/ERK signaling pathway coupled to integrin expression mediates cholinergic regulation of keratinocyte directional migration. J. Biol. Chem. 280 (2005) 39220-39228
58. Pullar C.E., Baier B.S., Kariya Y., Russell A.J., Horst B.A., Marinkovich M.P., and Isseroff R.R. beta 4 integrin and EGF coordinately regulate electric field-mediated directional migration via Rac1. Mol. Biol. Cell 17 (2006) 4925-4935
59. Martin P. Wound healing-Aiming for perfect skin regeneration. Science 276 (1997) 75-81
60. Patel G.K., Wilson C.H., Harding K.G., Finlay A.Y., and Bowden P.E. Numerous keratinocyte subtypes involved in wound re-epithelialization. J. Invest. Dermatol. 126 (2006) 497-502
61. Wakelin S.H., Bhogal B., Black M.M., Allen J., Wojnarowska F., Hashimoto T., Farr P.M., and Swain A.F. Epidermolysis bullosa acquisita associated with epidermal-binding circulating antibodies. Br. J. Dermatol. 136 (1997) 604-609
62. Kirtschig G., Marinkovich M.P., Burgeson R.E., and Yancey K.B. Anti-basement membrane autoantibodies in patients with anti-epiligrin cicatricial pemphigoid bind the alpha subunit of laminin 5. J. Invest. Dermatol. 105 (1995) 543-548
63. Jonkman M.F., Schuur J., Dijk F., Heeres K., de Jong M.C., van der Meer J.B., Yancey K.B., and Pas H.H. Inflammatory variant of epidermolysis bullosa acquisita with IgG autoantibodies against type VII collagen and laminin alpha3. Arch. Dermatol. 136 (2000) 227-231
64. Seo S.H., Kye Y.C., Kim S.N., and Kim S.C. Antiepiligrin cicatricial pemphigoid with autoantibodies to the beta subunit of laminin 5 and associated with severe laryngeal involvement necessitating tracheostomy. Dermatology 202 (2001) 63-66
65. Dainichi T., Takeshita H., Moroi Y., Urabe K., Yoshida M., Hisamatsu Y., Komai A., Duan H., Koga T., Hashimoto T., and Furue M. Cicatricial pemphigoid with autoantibodies against the laminin-5 gamma 2 subunit. Eur. J. Dermatol. 15 (2005) 189-193
66. Lazarova Z., Hsu R., Briggaman R.A., and Yancey K.B. Fab fragments directed against laminin-5 induce subepidermal blisters in neonatal mice. Clin. Immunol. 95 (2000) 26-32
67. Singer A.J., and Clark R.A. Cutaneous wound healing. N. Engl. J. Med. 341 (1999) 738-746
68. Wang J.F., Olson M.E., Reno C.R., Kulyk W., Wright J.B., and Hart D.A. Molecular and cell biology of skin wound healing in a pig model. Connect. Tissue Res. 41 (2000) 195-211
69. Werner S., and Grose R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83 (2003) 835-870
70. Schneider H., Muehle C., and Pacho F. Biological function of laminin-5 and pathogenic impact of its deficiency. Eur. J. Cell Biol. (2006) (PMID: 17000025)