Kindlin-1 mutant zebrafish as an in vivo model system to study adhesion mechanisms in the epidermis

Journal of Investigative Dermatology

Volumn 133, Issue 9, 2013, Pages 2180-2190

  Postel, Ruben ^a   Margadant, Coert ^a   Fischer, Boris ^b   Kreft, Maaike ^a   Janssen, Hans ^a   Secades, Pablo ^a   Zambruno, Giovanna ^c   Sonnenberg, Arnoud ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF COLOGNE   (Germany)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; INTEGRIN LINKED KINASE; KINDLIN 1; KINDLIN 2; MESSENGER RNA; REGULATOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; VERY LATE ACTIVATION ANTIGEN 3;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CELL CONTACT; CRYSTAL STRUCTURE; EMBRYO; EPIDERMIS; EXTRACELLULAR MATRIX; IN VIVO STUDY; INTERNALIZATION; LOSS OF FUNCTION MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; POIKILODERMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SKIN FRAGILITY; STOP CODON; ZEBRA FISH;

EID: 84884412366     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2013.154     Document Type: Article

References (60)

1. Al-Kilani A, de Freitas O, Dufour S et al. (2011) Negative feedback from integrins to cadherins: A micromechanical study. Biophys J 101:336-44
2. Ashton GHS (2004) Kindler syndrome. Clin Exp Dermatol 29:116-21
3. Bandyopadhyay A, Rothschild G, Kim S et al. (2012) Uncovering functional differences between kindlin-1 and kindlin-2 in keratinocytes. J Cell Sci 125:2172-84
4. Brakebusch C, Grose R, Quondamatteo F et al. (2000) Skin and hair follicle integrity is crucially dependent on b1 integrin expression in keratinocytes. EMBO J 19:3990-03
5. Burute M, Thery M (2012) Spatial segregation between cell-cell and cell-matrix adhesions. Curr Opin Cell Biol 24:628-36
6. Carney TJ, Feitosa NM, Sonntag C et al. (2010) Genetic analysis of fin development in zebrafish identifies furin and hemicentin1 as potential novel fraser syndrome disease genes. PLoS Genet 6:e1000907
7. Chattopadhyay N, Wang Z, Ashman LK et al. (2003) alpha3beta1 integrin-CD151, acomponent of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. J Cell Biol 163:1351-62
8. Delwel GO, Kuikman I, van der Schors RC et al. (1997) Identification of the cleavage sites in the alpha6A integrin subunit: Structural requirements for cleavage and functional analysis of the uncleaved alpha6Abeta1 integrin. Biochem J 324:263-72
9. deHart GW, Healy KE, Jones JC (2003) The role of alpha3beta1 integrin in determining the supramolecular organization of laminin-5 in the extracellular matrix of keratinocytes. Exp Cell Res 283:67-79
10. de Rooij J, Kerstens A, Danuser G et al. (2005) Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J Cell Biol 171:153-64
11. DiPersio CM, Hodivala-Dilke KM, Jaenisch R et al. (1997) a3b1 integrin is required for normal development of the epidermal basement membrane. J Cell Biol 137:729-42
12. Dowling JJ, Gibbs E, Russell M et al. (2008a) Kindlin-2 is an essential component of intercalated discs and is required for vertebrate cardiac structure and function. Circ Res 102:423-31
13. Dowling JJ, Vreede AP, Kim S et al. (2008b) Kindlin-2 is required for myocyte elongation and is essential for myogenesis. BMC Cell Biol 9:36
14. Geiger B, Yamada KM (2011) Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol 3, piia005033
15. Gimond C, van Der Flier A, van Delft S et al. (1999) Induction of cell scattering by expression of beta1 integrins in beta1-deficient epithelial cells requires activation of members of the rho family of GTPases and downregulation of cadherin and catenin function. J Cell Biol 147:1325-40
16. Greciano PG, Moyano JV, Buschmann MM et al. (2012) Laminin-511 partners with laminin-332 to mediate directional migration of Madin-Darby canine kidney epithelial cells. Mol Biol Cell 23:121-36
17. Harburger DS, Bouaouina M, Calderwood DA (2009) Kindlin-1 and-2 directly bind the C-Terminal region of b integrin cytoplasmic tails and exert integrin-specific activation effects. J Biol Chem 284:11485-97
18. Has C, Ludwig RJ, Herz C et al. (2008) C-Terminally truncated kindlin-1 leads to abnormal adhesion and migration of keratinocytes. Br J Dermatol 159:1192-6
19. Has C, Spartà G, Kiritsi D et al. (2012) Integrin a3 mutations with kidney, lung, and skin disease. N Engl J Med 366:1508-14
20. Has C, Wessagowit V, Pascucci M et al. (2006) Molecular basis of Kindler syndrome in Italy: Novel and recurrent Alu/Alu recombination, splice site, nonsense, and frameshift mutations in the KIND1 gene. J Invest Dermatol 126:1776-83
21. He Y, Esser P, Heinemann A et al. (2011) Kindlin-1 and-2 have overlapping functions in epithelial cells; implications for phenotype modification. Am J Pathol 178:975-82
22. Herz C, Aumailley M, Schulte C et al. (2006) Kindlin-1 is a phosphoprotein involved in regulation of polarity, proliferation, and motility of epidermal keratinocytes. J Biol Chem 281:36082-90
23. Hodivala-Dilke KM, DiPersio CM, Kreidberg JA et al. (1998) Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol 142:1357-69
24. Jobard F, Bouadjar B, Caux F et al. (2003) Identification of mutations in a new gene encoding a FERM family protein with a pleckstrin homology domain in Kindler syndrome. Hum Mol Genet 12:925-35
25. Kern JS, Herz C, Han E et al. (2007) Chronic colitis due to an epithelial barrier defect: The role of kindlin-1 isoforms. J Pathol 213:462-70
26. Kim JP, Zhang K, Kramer RH et al. (1992) Integrin receptors and RGD sequences in human keratinocyte migration: Unique anti-migratory function of a3b1 epiligrin receptor. J Invest Dermatol 98:764-70
27. Knoll R, Postel R, Wang J et al. (2007) Laminin-Alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116:515-25
28. Lai-Cheong JE, Ussar S, Arita K et al. (2008) Colocalization of Kindlin-1, Kindlin-2, and Migfilin at keratinocyte focal adhesion and relevance to the pathophysiology of Kindler Syndrome. J Invest Dermatol 128: 2156-65
29. Larjava H, Plow EF, Wu C (2008) Kindlins: Essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep 9:1203-8
30. Lissitzky JC, Luis J, Munzer JS et al. (2000) Endoproteolytic processing of integrin pro-Alpha subunits involves the redundant function of furin and proprotein convertase (PC) 5A, but not paired basic amino acid converting enzyme (PACE) 4, PC5B or PC7. Biochem J 346:133-8
31. Lorenz K, Grashoff C, Torka R et al. (2007) Integrin-linked kinase is required for epidermal and hair follicle morphogenesis. J Cell Biol 177:501-13
32. Mackinnon AC, Qadota H, Norman KR et al. (2002) C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 12:787-97
33. Margadant C, Charafeddine RA, Sonnenberg A (2010) Unique and redundant functions of integrins in the epidermis. FASEB J 24:4133-52
34. Margadant C, Frijns E, Wilhelmsen K et al. (2008) Regulation of hemidesmosome disassembly by growth factor receptors. Curr Opin Cell Biol 20:589-96
35. Margadant C, Kreft M, de Groot DJ et al. (2012) Distinct roles of talin and kindlin in regulating integrin a5b1 function and trafficking. Curr Biol 22:1554-63
36. Margadant C, Raymond K, Kreft M et al. (2009) Integrin a3b1 inhibits directional migration and wound re-epithelialization in the skin. J Cell Sci 122:278-88
37. Martinez-Rico C, Pincet F, Thiery JP et al. (2010) Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J Cell Sci 123:712-22
38. Meves A, Stremmel C, Gottschalk K et al. (2009) The kindlin protein family: New members to the club of focal adhesion proteins. Trends Cell Biol 19:504-13
39. Montanez E, Ussar S, Schifferer M et al. (2008) Kindlin2 controls bidirectional signaling of integrins. Genes Dev 22:1325-30
40. Nagae M, Re S, Mihara E et al. (2012) Crystal structure of a5b1 integrin ectodomain: Atomic details of the fibronectin receptor. J Cell Biol 197:131-40
41. Nakrieko KA, Welch I, Dupuis H et al. (2008) Impaired hair follicle morphogenesis and polarized keratinocyte movement upon conditional inactivation of integrin-linked kinase in the epidermis. Mol Biol Cell 19:1462-73
42. Natsuga K, Shinkuma S, Nishie W et al. (2010) Animal models of epidermolysis bullosa. Dermatol Clin 28:137-42
43. O'Toole EA, Marinkovich MP, Hoeffler WK et al. (1997) Laminin-5 inhibits human keratinocyte migration. Exp Cell Res 233:330-9
44. Postel R, Vakeel P, Topczewski J et al. (2008) Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin-ECM adhesion complex. Dev Biol 318:92-101
45. Raghavan S, Bauer C, Mundschau G et al. (2000) Conditional ablation of b1 integrin in skin: Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J Cell Biol 150:1149-60
46. Sachs N, Secades P, van Hulst L et al. (2012) Loss of integrin a3 prevents skin tumor formation by promoting epidermal turnover and depletion of slowcycling cells. Proc Natl Acad Sci USA 109:21468-73
47. Sadler E, Klausegger A, Muss W et al. (2006) Novel KIND1 gene mutation in Kindler syndrome patients with severe gastro-intestinal tract involvement. Arch Dermatol 142:1619-24
48. Shigeta M, Sanzen N, Osawa M et al. (2003) CD151 regulates epithelial cellcell adhesion through PKC-And Cdc42-dependent actin cytoskeletal reorganization. J Cell Biol 163:165-76
49. Siegel DH, Ashton GH, Penagos HG et al. (2003) Loss of kindlin-1, a human homolog of the Caenorhabditis elegans actin-extracellular matrix linker protein UNC-112, causes kindler syndrome. Am J Hum Genet 73:174-87
50. Sonawane M, Carpio Y, Geisler R et al. (2005) Zebrafish penner/lethal giant larvae 2 functions in hemidesmosome formation, maintenance of cellular morphology and growth regulation in the developing basal epidermis. Development 132:3255-65
51. Sonawane M, Martin-Maischein H, Schwarz H et al. (2009) Lgl2 and E-cadherin act antagonistically to regulate hemidesmosome formation during epidermal development in zebrafish. Development 136:1231-40
52. Thisse C, Thisse B, Schilling TF et al. (1993) Structure of the zebrafish snail1 gene and its expression in wild-Type, spadetail and no tail mutant embryos. Development 119:1203-15
53. Ussar S, Moser M, Widmaier M et al. (2008) Loss of Kindlin-1 causes skin atrophy and lethal neonatal intestinal epithelial dysfunction. PLoS Genet 4:e1000289
54. Ussar S,Wang H-V, Linder S et al. (2006) The kindlins: Subcellular localization and expression during murine development. Exp Cell Res 312:3142-51
55. Wang Z, Symons JM, Goldstein SL et al. (1999) Alpha3beta1 integrin regulates epithelial cytoskeletal organization. J Cell Sci 112:2925-35
56. Webb AE, Sanderford J, Frank D et al. (2007) Laminin alpha5 is essential for the formation of the zebrafish fins. Dev Biol 311:369-82
57. Weber GF, Bjerke MA, DeSimone DW (2011) Integrins and cadherins join forces to form adhesive networks. J Cell Sci 124:1183-93
58. White SJ, McLean WH (2005) Kindler surprise: Mutations in a novel actinassociated protein cause Kindler syndrome. J Dermatol Sci 38:169-75
59. Wienholds E, van Eeden F, Kosters M et al. (2003) Efficient target-selected mutagenesis in zebrafish. Genome Res 13:2700-7
60. Zhang F, Tom CC, Kugler MC et al. (2003) Distinct ligand binding sites in integrin alpha3beta1 regulate matrix adhesion and cell-cell contact. J Cell Biol 163:177-88