Cell cycle and adhesion defects in mice carrying a targeted deletion of the integrin β4 cytoplasmic domain

EMBO Journal

Volumn 17, Issue 14, 1998, Pages 3940-3951

  Murgia, Chiara ^a,c   Blaikie, Pamela ^a   Kim, Nancy ^a   Dans, Michael ^a   Petrie, Howard T ^a,b   Giancotti, Filippo G ^a,b  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b Weill Cornell Medical Center   (United States)

^c ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Blistering skin disease; Cell cycle; Gene targeting; Integrin; Signaling

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; CYTOPLASM PROTEIN; INTEGRIN; KALININ; PROTEIN P27; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; ATRESIA; BASEMENT MEMBRANE; BLISTER; CELL ADHESION; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EMBRYO CELL; EPIDERMOLYSIS BULLOSA; GENE DELETION; GENE TARGETING; HOMOZYGOSITY; INTESTINE CELL; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STEM CELL; STOP CODON;

ANIMALS; ANTIGENS, CD; ANTIGENS, SURFACE; BASEMENT MEMBRANE; CELL ADHESION; CELL ADHESION MOLECULES; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYTOPLASM; CYTOSKELETON; DESMOSOMES; DUODENUM; EPIDERMOLYSIS BULLOSA, JUNCTIONAL; INTEGRIN ALPHA6BETA4; INTEGRIN BETA4; INTEGRINS; INTESTINAL MUCOSA; KERATINOCYTES; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; PYLORUS; SEQUENCE DELETION; SKIN; TUMOR SUPPRESSOR PROTEINS;

EID: 0032528060     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.14.3940     Document Type: Article

References (67)

1. Alberts,B., Bray,D., Lewis,J., Raff,M., Roberts,K. and Watson,J.D. (1994) Extracellular matrix receptors on animal cells; the integrins. In Molecular Biology of the Cell. 3rd edn. Garland Publishing. Inc., New York and London, pp. 995-999.
2. Aberdam,D. et al. (1994) Herlitz's junctional epidermolysis bullosa is genetically linked to mutations in the nicein/kalinin (laminin-5) LAMC2 gene. Nature Genet., 6, 299-304.
3. Borradori,L. and Sonnenberg,A. (1996) Hemidesmosomes: roles in adhesion, signaling and human diseases. Curr. Opin. Cell Biol., 8, 647-656.
4. Borradori,L., Koch,P.J., Niessen,C.M., Erkeland,S. and van Leusden,M.R. (1997) The localization of bullous pemphigoid antigen 180 (BP180) in hemidesmosomes is mediated by its cytoplasmic domain and seems to be regulated by the β4 integrin subunit. J. Cell Biol., 136, 1333-1347.
5. Brieher,W.M., Yap,A.S. and Gumbiner,B.M. (1996) Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135, 487-496.
6. Burridge,K. and Chrzanowska-Wonidka,M. (1996) Focal adhesions, contractility, and signaling. Annu. Rev. Dev. Biol., 12, 463-519.
7. Calautti,E., Missero,C., Stein,P.L., Ezzel,R.M. and Dotto,G.P. (1995) Fyn tyrosine kinase is involved in keratinocyte differentiation control. Genes Dev., 9, 2279-2291.
8. Carter,W.G., Kaur,P., Gil,S.G., Gahr,P.J. and Wayner,E.A. (1990) Distinct functions for integrins α3β1 in focal adhesions and α6β4/bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Bioi., 111, 3141-3154.
9. Carter,W.G., Ryan,M.C. and Gahr,P.J. (1991) Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell. 65, 599-610.
10. Casaccia-Bonnefil,P., Tikoo,R., Kiyokawa,H., Friedrich,V., Jr, Chao,M.V. and Koff,A. (1997) Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev., 11, 2335-2346.
11. De Arcangelis,A., Neuville,P., Boukamel,R., Lefebvre,O., Kedinger,M. and Simon-Assmann,P. (1996) Inhibition of laminin alpha 1-chain expression leads to alteration of basement membrane assembly and cell differentiation. J. Cell Biol., 133, 417-430.
12. DiPersio,C.M., Hodivala-Dilke,K.M., Jaenisch,R., Kreidberg,J.A. and Hynes,R.O. (1997) α3β1 integrin is required for normal development of the epidermal basement membrane. J. Cell Biol., 137, 729-742.
13. Dowling,J., Yu,Q.-C. and Fuchs,E. (1996) β4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol., 134, 559-572.
14. Einheber,S., Milner,T.A., Giancotti,F.G. and Salzer,J.L. (1993) Axonal regulation of Schwann cell integrin expression suggests a role for α6β4 in myelination. J. Cell Biol., 123, 1223-1236.
15. Engvall,E., Davis,G.E., Dickerson,K., Ruoslahti,E., Varon,S. and Manthorpe,M. (1986) Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site. J. Cell Biol., 103, 2457-2465
16. Fang,F., Orend,G., Watanabe,N., Hunter,T. and Ruoslahti,E. (1996) Dependence of cyclin E-CDK 2 kinase activity on cell anchorage. Science, 271, 499-502.
17. Gandarillas,A. and Watt,F.M. (1997) c-Myc promotes differentiation of human epidermal stem cells. Genes Dev., 11, 2869-2882.
18. Georges-Labouesse,E., Messaddeq,N., Yehia,G., Cadalbert,L., Dierich,A. and Le Meur,M. (1996) Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nature Genet., 13, 370-373.
19. Giancotti,F.G. (1996) Signal transduction by the α6β4 integrin: charting the path between laminin binding and nuclear events. J. Cell Sci., 109, 1165-1172.
20. Giancotti,F.G. (1997) Integrin signaling: specificity and control of cell survival and cell cycle progression. Curr. Opin. Cell Biol., 9, 691-700.
21. Giancotti,F.G. and Mainiero,F. (1994) Integrin-mediated adhesion and signaling in tumorigenesis. Biochim. Biophys. Acta, 1198, 47-64.
22. Giancotti,F.G., Stepp,M.A., Suzuki,S., Engvall,E. and Ruoslahti,E. (1992) Proteolytic processing of endogenous and recombinant β4 integrin subunit. J. Cell Biol., 118, 951-959.
23. Gordon,J.I. and Hermiston,M.L. (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr. Opin. Cell Biol., 6, 795-803.
24. Green,H. (1977) Terminal differentiation of cultured human epidermal cells. Cell, 11, 405-416.
25. Guo,L., Degenstein,L., Dowling,J., Yu,Q.-C., Wollmann,R., Perman,B. and Fuchs,E. (1995) Gene targetting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell, 81, 233-243.
26. Hall,P.A. and Watt,F.M. (1989) Stem cells: the generation and maintenance of cellular diversity. Development, 106, 619-633.
27. Hemler,M.E. (1990) VLA proteins in the integrin family. Annu. Rev. Immunol., 8, 365-400.
28. Hieda,Y., Nishizawa,Y., Uematsu,J. and Owaribe,K. (1992) Identification of a new hemidesmosomal protein, HD1: a major high molecular mass component of isolated hemidesmosomes. J. Cell. Biol., 116, 1497-1506.
29. Hogervorst,F., Kuikman,I., von dem Borne,A.E.G. Kr. and Sonnenberg,A. (1990) Cloning and sequence analysis of β4 cDNA: an integrin subunit that contains a unique 118 kd cytoplasmic domain. EMBO J., 9, 745-770.
30. Hynes,R.O. (1987) Integrins: a family of cell surface receptors. Cell, 48, 549-554.
31. Jones,P.H. and Watt,F.M. (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell, 73, 713-724.
32. Jones,P.H., Harper,S. and Watt,F.M. (1995) Stem cell patterning and fate in human epidermis. Cell, 80, 83-93.
33. Kajiji,S., Tamura,R.N. and Quaranta,V. (1989) A novel integrin (αEβ4) from human epithelial cells suggests a fourth family of integrin adhesion receptors. EMBO J., 8, 673-680.
34. Kenne1,S.J., Foote,J.J., Falcioni,R., Sonnenberg,A., Stringer,C.D., Crouse,C. and Hemler,M.E. (1989) Analysis of the tumor-associated antigen TSP-180. Identity with alpha 6-beta-4 in the integrin superfamily. J. Biol. Chem., 264, 15515-15521.
35. Kennel,S.J., Godfrey,V. Chang,L.Y., Lankford,T.K., Foote,L.J. and Makkinje,A. (1992) The β4 subunit of the integrin family is displayed on a restricted subset of endothelium in mice. J. Cell Biol., 101, 145-150.
36. Kimmel,K.A. and Carey,T.E. (1986) Altered expression in squarnuos carcinoma cells of an orientation restricted epithelial antigen detected by monoclonal antibody A9. Cancer Res., 46, 3614-2623.
37. Klein,S., Giancotti,F.G., Presta,M., Albelda,S.M., Buck,C.A. and Rifkin,D.B. (1993) Basic fibroblast growth factor modulates integrin expression in microvascular endothelial cells. Mol. Biol. Cell, 4, 973-982.
38. Mainiero,F., Pepe,A., Wary,K.K., Spinardi,L., Mohammadi,M., Schlessinger,J. and Giancotti,F.G. (1995) Signal transduction by the α6β4 integrin; distinct β4 subunit sites mediate recruitment of Shc/ Grb2 and association with the cytoskeleton of hemidesmosomes. EMBO J., 14, 4470-4481.
39. Mainiero,F., Murgia,C., Wary,K.K., Curatola,A.M., Pepe,A., Blumemberg,M., Westwick,J.K., Der,C.J. and Giancotti,F.G. (1997) The coupling of α6β4 integrin to Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J., 16, 2365-2375.
40. Niessen,C.M., Hulsman,E.H.M., Rots,E.S., Sanchez-Aparicio,P. and Sonnenberg,A. (1997) Integrin α6β4 forms a complex with the cytosleletal protein HD1 and induces its redistribution in transfected COS-7 cells. Mol. Biol. Cell, 8, 555-566.
41. Orian-Rousseau,V., Aberdam,D., Fontao,L., Chevalier,L., Meneguzzi,G., Kedinger,M. and Simon-Assmann,P. (1995) Developmental expression of laminin-5 and HD1 in the intestine; epithelial to mesenchymal shift for the laminin γ2 chain subunit deposition. Dev. Dynam., 206, 12-23.
42. Pulkkinen,L., Christiano,A.M. Airenne,T., Haakana,H., Tryggvason,K. and Uitto,J. (1994) Mutations in the γ2 chain gene (LAMC2) of kalinin/laminin 5 in the junctional forms of epidermolysis bullosa. Nature Genet., 6, 293-298.
43. Reznieczek,G.A., de Pereda,J.M., Reipert,S. and Wiche,G. (1998) Linking integrin α6β4-based cell adhesion to the intermediate filament cytoskeleton: direct interaction between the β4 subunit and plectin at multiple molecular sites. J. Cell Biol. 141, 209-225.
44. Rousselle,P., Lunstrum,G.P., Keene,D.R. and Burgeson,R.E. (1991) Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol., 114, 567-576.
45. Ruoslahti,E. and Pierschbacher,D. (1987) New perspectives in cell adhesion: RGD and integrins. Science, 238, 491-497.
46. Ruzzi,L., Gagnoux-Palacios,L., Pinolaq,M., Belli,S., Meneguzzi,G., D'Alessio,M.D. and Zambruno,G.A. (1997) Homozygous mutation in the integrin α6 gene in junctional epidermolysis bullosa with pyloric atresia. J. Clin. Invest., 99, 2826-2831.
47. Schlütter,C., Duchrow,M., Wohlenberg,C., Becker,M.H.G., Key,G. Flad,H.-D. and Gerdes,J. (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining protein. J. Cell Biol., 123, 513-522.
48. Shaw,L.M., Rabinovitz,I., Wang,H., Toker,A. and Mercurio,A.M. (1997) Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion. Cell, 91, 949-960.
49. Shimizu,H., Hashimoto,T. and Eady,R.A. (1991) Human monoclonal anti basement membrane zone antibodies derived from virally transformed lymphocytes of a patient with bullous pemphigoid recognize epitopes associated with hemidesmosomes. Br. J. Dermatol., 124, 217-220.
50. Simon-Assmann,P., Duclos,B., Orian-Rousseau,V., Arnold,C., Mathelin,C., Engvall,E. and Kedinger, M. (1994) Differential expression of laminin isoforms and α6-β4 integrin subunits in the developing human and mouse intestine. Dev. Dynam., 201, 71-85.
51. Sonnenberg,A., Linders,C.J.T., Daams,J.H. and Kennel,S.J. (1990) The α6βl (VLA-6) and α6β4 protein complexes: tissue distribution and biochemical properties. J. Cell Sci., 96, 207-217.
52. Spinardi,L., Ren,Y.-L., Sanders,R. and Giancotti,F.G. (1993) The β4 subunit cytoplasmic domain mediates the interaction of α6β4 integrin with the cytoskeleton of hemidesmosomes. Mol. Biol. Cell, 4, 871-884.
53. Spinardi,L., Einheber,S., Cullen.,T., Milner,T.A. and Giancotti,F.G. (1995) A recombinant tail-less integrin β4 subunit disrupts hemidesmosomes, but does not suppress α6β4-mediated cell adhesion to laminins. J. Cell Biol. 129, 473-487.
54. Stepp,M.A., Spurr-Michaud,S., Tisdale,A., Elwell,J. and Gipson,I.K. (1990) Alpha 6 beta 4 integrin heterodimer is a component of hemidesmosomes. Proc. Natl Acad. Sci. USA, 87, 8970-8974.
55. Stoward,P.J. and Everson Pearse,A.G. (1991) Histochemistry. Churchill Livingston, Edinburgh, UK, Vol. 3, pp. 637-638.
56. Suzuki,S. and Naitoh,Y. (1990) Amino acid sequence of a novel integrin β4 subunit and primary expression of the mRNA in epithelial cells. EMBO J., 9, 757-763.
57. Swiatek,P.J. and Gridley,T. (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger protein Krox20. Genes Dev., 7, 2071-2084.
58. Timpl,R. and Brown,J.C. (1996) Supramolecular assembly of basement membranes. BioEssays, 18, 123-132.
59. Tybulewicz,V.L., Crawford,C.E., Jackson,P.K., Bronson,R.T. and Mulligan,R.C. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell, 65, 1153-1563.
60. Vailly,J. et al. (1994) The 100-kDa chain of nicein/kalinin is a laminin B2 chain variant. Eur. J. Biochem. 219, 209-218.
61. Van der Neut,R., Krimpenfort,P., Calafat,J., Niessen,C.M. and Sonnenberg,A. (1996) Epithelial detachment due to absence of hemidesmosomes in integrin β4 null mice. Nature Genet., 13,366-369.
62. Vidal,F., Aberdam,D., Miquel,C., Christiano,A.M., Pulkkinen,L., Uitto,J., Ortonne,J.P. and Meneguzzi, G. (1995) Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nature Genet., 10, 229-234.
63. Yurchenco,P.D. and O'Rear,J.J. (1994) Basal lamina assembly. Curr. Opin. Cell Biol., 6, 674-681.
64. Wadsworth,S., Halvorson,M.J. and Coligan,J.E. (1992) Developmentally regulated expression of the β4 integrin on immature mouse thymocytes. J. Immunol., 149, 421-428.
65. Wary,K.K., Mainiero,F., Isakoff,S.J., Marcantonio,E.E. and Giancotti,F.G. (1996) The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell, 87, 733-743.
66. Wolf,G.T., Carey,T.E., Schmaltz,S.P., McClatchey,K.D., Poore,J., Glaser,L., Hayashida,D.J.S. and Hsu,S. (1990) Altered antigen expression predicts outcome in squamous cell carcinomas of the head and neck. J. Natl Cancer Inst., 82, 1566-1572.
67. Zhu,X., Ohtsubo,M., Bohmer,R., Roberts,J.M. and Assoian,R.K. (1996) Adhesion dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein. J. Cell Biol., 133, 391-403.