Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes

Journal of Cell Biology

Volumn 162, Issue 1, 2003, Pages 139-148

  Terpstra, Leonieke ^a,f   Prud'Homme, Josée ^a   Arabian, Alice ^a   Takeda, Shu ^b   Karsenty, Gérard ^b   Dedhar, Shoukat ^c,d   St Arnaud, René ^a,e  

^a SHRINERS HOSPITAL FOR CHILDREN   (Canada)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c VANCOUVER GENERAL HOSPITAL   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Chondrocytes; Cre lox; Cyclin D1; Gene targeting; Integrin linked kinase

Indexed keywords

COLLAGEN TYPE 10; COLLAGEN TYPE 2; CYCLIN D1; INTEGRIN; INTEGRIN LINKED KINASE; PARATHYROID HORMONE RECEPTOR; PHOSPHOTRANSFERASE; RECOMBINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDRODYSPLASIA; CONTROLLED STUDY; DWARFISM; GENE INACTIVATION; GROWTH PLATE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

NON-PROGRAMMATIC;

ANIMALS; APOPTOSIS; CARTILAGE; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; CYCLIN D1; DISEASE MODELS, ANIMAL; DOWN-REGULATION; DWARFISM; EXOSTOSES, MULTIPLE HEREDITARY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH PLATE; INTEGRASES; INTEGRINS; MALE; MICE; MICE, KNOCKOUT; OSTEOGENESIS; PROTEIN-SERINE-THREONINE KINASES; TRANSGENES; VIRAL PROTEINS;

ANIMALIA; ERINACEIDAE; MUS MUSCULUS;

EID: 0038148536     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200302066     Document Type: Article

References (50)

1. Attwell, S., C. Roskelley, and S. Dedhar. 2000. The integrin-linked kinase (ILK) suppresses anoikis. Oncogene. 19:3811-3815.
2. Beier, F., R.J. Lee, A.C. Taylor, R.G. Pestell, and P. LuValle. 1999. Identification of the cyclin D1 gene as a target of activating transcription factor 2 in chondrocytes. Proc. Natl. Acad. Sci. USA. 96:1433-1438.
3. Bitgood, M.J., and A.P. McMahon. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:126-138.
4. Cruet-Hennequart, S., S. Maubant, J. Luis, P. Gauduchon, C. Staedel, and S. Dedhar. 2003. Alpha-V integrins regulate cell proliferation through integrin-linked kinase (ILK) in ovarian cancer cells. Oncogene. 22:1688-1702.
5. D'Amico, M., J. Hulit, D.F. Amanatullah, B.T. Zafonte, C. Albanese, B. Bouzahzah, M. Fu, L.H. Augenlicht, L.A. Donehower, K.I. Takemaru, et al. 2000. The integrin-linked kinase regulates the cyclin D1 gene through glycogen synthase kinase 3beta and CREB-dependent pathways. J. Biol. Chem. 275:32649-32657.
6. Delcommenne, M., C. Tan, V. Gray, L. Rue, J. Woodgett, and S. Dedhar. 1998. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA. 95:11211-11216.
7. Di-Poi, N., N.S. Tan, L. Michalik, W. Wahli, and B. Desvergne. 2002. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol. Cell. 10:721-733.
8. Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:32377-32379.
9. Friedrich, E.B., S. Sinha, L. Li, S. Dedhar, T. Force, A. Rosenzweig, and R.E. Gerszten. 2002. Role of integrin-linked kinase in leukocyte recruitment. J. Biol. Chem. 277:16371-16375.
10. Grashoff, C., A. Aszodi, T. Sakai, E.B. Hunziker, and R. Fassler. 2003. Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO. Rep. 4:432-438.
11. Hannigan, G.E., C. Leung-Hagesteijn, L. Fitz-Gibbon, M.G. Coppolino, G. Radeva, J. Filmus, J.C. Bell, and S. Dedhar. 1996. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature. 379:91-96.
12. He, B., R.A. Deckelbaum, D. Miao, M.L. Lipman, M. Pollak, D. Goltzman, and A.C. Karaplis. 2001. Tissue-specific targeting of the pthrp gene: the generation of mice with floxed alleles. Endocrinology. 142:2070-2077.
13. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 497 pp.
14. Hynes, R. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
15. Inoshita, S., Y. Terada, O. Nakashima, M. Kuwahara, S. Sasaki, F. Marumo. 1999. Regulation of the G1/S transition phase in mesangial cells by E2F1. Kidney Int. 56:1238-1241.
16. Kaartinen, V., and A. Nagy. 2001. Removal of the floxed neo gene from a conditional knockout allele by the adenoviral Cre recombinase in vivo. Genesis. 31:126-129.
17. Karsenty, G., and E.F. Wagner. 2002. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell. 2:389-406.
18. Laird, P.W., A. Zijderveld, K. Linders, M.A. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19:4293.
19. Lanske, B., A.C. Karaplis, K. Lee, A. Luz, A. Vortkamp, A. Pirro, M. Karperien, L.H. Defize, C. Ho, R.C. Mulligan, et al. 1996. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science. 273:663-666.
20. Lee, K., B. Lanske, A.C. Karaplis, J.D. Deeds, H. Kohno, R.A. Nissenson, H.M. Kronenberg, and G.V. Segre. 1996. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology. 137:5109-5118.
21. Lefebvre, V., S. Garofalo, G. Zhou, M. Metsaranta, E. Vuorio, and B. De Crombrugghe. 1994. Characterization of primary cultures of chondrocytes from type II collagen/beta-galactosidase transgenic mice. Matrix Biol. 14:329-335.
22. Linsenmayer, T.F., Q.A. Chen, E. Gibney, M.K. Gordon, J.K. Marchant, R. Mayne, and T.M. Schmid. 1991. Collagen types IX and X in the developing chick tibiotarsus: analyses of mRNAs and proteins. Development. 111:191-196.
23. Loeser, R.F., S. Sadiev, L. Tan, and M.B. Goldring. 2000. Integrin expression by primary and immortalized human chondrocytes: evidence of a differential cole for alpha1beta1 and alpha2beta1 integrins in mediating chondrocyte adhesion to types II and VI collagen. Osteoarthritis Cartilage. 8:96-105.
24. Long, F., E. Schipani, H. Asahara, H. Kronenberg, and M. Montminy. 2001a. The CREB family of activators is required for endochondral bone development. Development. 128:541-550.
25. Long, F., X.M. Zhang, S. Karp, Y. Yang, and A.P. McMahon. 2001b. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development. 128:5099-5108.
26. Mackinnon, A.C., H. Qadota, K.R. Norman, D.G. Moerman, and B.D. Williams. 2002. C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr. Biol. 12:787-797.
27. Nagy, A., J. Rossant, R. Nagy, W. Abramow-Newerly, and J.C. Roder. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 90:8424-8428.
28. Novak, A., S.C. Hsu, C. Leung-Hagesteijn, G. Radeva, J. Papkoff, R. Montesano, C. Roskelley, R. Grosschedl, and S. Dedhar. 1998. Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways. Proc. Natl. Acad. Sci. USA. 95:4374-4379.
29. Ovchinnikov, D.A., J.M. Deng, G. Ogunrinu, and R.R. Behringer. 2000. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis. 26:145-146.
30. Persad, S., S. Attwell, V. Gray, M. Delcommenne, A. Troussard, J. Sanghera, and S. Dedhar. 2000. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoptosis of PTEN-mutant prostate cancer cells. Proc. Natl. Acad. Sci. USA. 97:3207-3212.
31. Persad, S., S. Attwell, V. Gray, N. Mawji, J.T. Deng, D. Leung, J. Yan, J. Sanghera, M.P. Walsh, and S. Dedhar. 2001a. Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343. J. Biol. Chem. 276:27462-27469.
32. Persad, S., A.A. Troussard, T.R. McPhee, D.J. Mulholland, and S. Dedhar. 2001b. Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J. Cell Biol. 153:1161-1174.
33. Poole, A.R. 1991. The growth plate: cellular physiology, cartilage assembly and mineralization. In Cartilage: Molecular Aspects. B.K. Hall and S.A. Newman, editors. CRC Press, Boca Raton, FL. 179-211.
34. Radeva, G., T. Petrocelli, E. Behrend, C. Leung-Hagesteijn, J. Filmus, J. Slingerland, and S. Dedhar. 1997. Overexpression of the integrin-linked kinase promotes anchorage-independent cell cycle progression. J. Biol. Chem. 272:13937-13944.
35. Sauer, B., and N. Henderson. 1990. Targeted insertion of exogenous DNA into the eukaryotic genome by the Cre recombinase. New Biol. 2:441-449.
36. Schipani, E., H.E. Ryan, S. Didrickson, T. Kobayashi, M. Knight, and R.S. Johnson. 2001. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 15:2865-2876.
37. Schmidt, M., S. de Mattos Fernandez, A. van der Horst, R. Klompmaker, G.J. Kops, E.W. Lam, B.M. Burgering, and R.H. Medema. 2002. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol. Cell. Biol. 22:7842-7852.
38. Seger, D., R. Seger, and S. Shaltiel. 2001. The CK2 phosphorylation of vitronectin. Promotion of cell adhesion via the alpha(v)beta 3-phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 276:16998-17006.
39. Shum, L., and G. Nuckolls. 2002. The life cycle of chondrocytes in the developing skeleton. Arthritis Res. 4:94-106.
40. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70-71.
41. St-Jacques, B., M. Hammerschmidt, and A.P. McMahon. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13:2072-2086.
42. Takeda, S., J.P. Bonnamy, M.J. Owen, P. Ducy, and G. Karsenty. 2001. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 15:467-481.
43. Troussard, A.A., C. Tan, T.N. Yoganathan, and S. Dedhar. 1999. Cell-extracellular matrix interactions stimulate the AP-1 transcription factor in an integrin-linked kinase- and glycogen synthase kinase 3-dependent manner. Mol. Cell. Biol. 19:7420-7427.
44. Troussard, A.A., N.M. Mawji, C. Ong, A. Mui, R. St-Arnaud, and S. Dedhar. 2003. Conditional knock-out of integrin-linked kinase (ILK) demonstrates an essential role in PKB/Akt activation. J. Biol. Chem. 278:22374-22378.
45. Watanabe, G., A. Howe, R.J. Lee, C. Albanese, I.W. Shu, A.N. Karnezis, L. Zon, J. Kyriakis, K. Rundell, and R.G. Pestell. 1996. Induction of cyclin D1 by simian virus 40 small tumor antigen. Proc. Natl. Acad Sci. USA. 93:12861-12866.
46. Wilkinson, D. 1992. Whole mount in situ hybridization to vertebrate embryos. In In Situ Hybridization: A Practical Approach. D. Wilkinson, editor. IRL Press, Oxford, UK. 75-83.
47. Wu, C., and S. Dedhar. 2001. Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J. Cell Biol. 155:505-510.
48. Wu, C., S.Y. Keightley, C. Leung-Hagesteijn, G. Radeva, M. Coppolino, S. Goicoechea, J.A. McDonald, and S. Dedhar. 1998. Integrin-linked protein kinase regulates fibronectin matrix assembly, E- cadherin expression, and tumorigenicity. J. Biol. Chem. 273:528-536.
49. Zervas, C.G., S.L. Gregory, and N.H. Brown. 2001. Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J. Cell Biol. 152:1007-1018.
50. Zhou, G., V. Lefebvre, Z. Zhang, H. Eberspaecher, and B. de Crombrugghe. 1998. Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. J. Biol. Chem. 273:14989-14997.