Targeted Deletion of Capn4 in Cells of the Chondrocyte Lineage Impairs Chondrocyte Proliferation and Differentiation

REFERENCES

• Aikawa, T., G. V. Segre, and K. Lee. 2001. Fibroblast growth factor inhibits chondrocytic growth through induction of p21 and subsequent inactivation of cyclin E-Cdk2. J. Biol. Chem. 276:29347–29352.
   PubMed Web of Science ®Google Scholar
• Arthur, J. S., J. S. Elce, C. Hegadorn, K. Williams, and P. A. Greer. 2000. Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol. Cell. Biol. 20:4474–4481.
   PubMed Web of Science ®Google Scholar
• Beier, F., Z. Ali, D. Mok, A. C. Taylor, T. Leask, C. Albanese, R. G. Pestell, and P. LuValle. 2001. TGFbeta and PTHrP control chondrocyte proliferation by activating cyclin D1 expression. Mol. Biol. Cell 12:3852–3863.
   PubMed Web of Science ®Google Scholar
• Carragher, N. O., M. A. Westhoff, D. Riley, D. A. Potter, P. Dutt, J. S. Elce, P. A. Greer, and M. C. Frame. 2002. v-Src-induced modulation of the calpain-calpastatin proteolytic system regulates transformation. Mol. Cell. Biol. 22:257–269.
   PubMed Web of Science ®Google Scholar
• Carrano, A. C., E. Eytan, A. Hershko, and M. Pagano. 1999. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1:193–199.
   PubMed Web of Science ®Google Scholar
• Chen, Z., E. Knutson, A. Kurosky, and T. Albrecht. 2001. Degradation of p21cip1 in cells productively infected with human cytomegalovirus. J. Virol. 75:3613–3625.
   PubMed Web of Science ®Google Scholar
• Choi, Y. H., S. J. Lee, P. Nguyen, J. S. Jang, J. Lee, M. L. Wu, E. Takano, M. Maki, P. A. Henkart, and J. B. Trepel. 1997. Regulation of cyclin D1 by calpain protease. J. Biol. Chem. 272:28479–28484.
   PubMed Web of Science ®Google Scholar
• Cong, J., D. E. Goll, A. M. Peterson, and H. P. Kapprell. 1989. The role of autolysis in activity of the Ca2+-dependent proteinases (mu-calpain and m-calpain). J. Biol. Chem. 264:10096–10103.
   PubMed Web of Science ®Google Scholar
• Delmas, C., N. Aragou, S. Poussard, P. Cottin, J. M. Darbon, and S. Manenti. 2003. MAP kinase-dependent degradation of p27Kip1 by calpains in choroidal melanoma cells. Requirement of p27Kip1 nuclear export. J. Biol. Chem. 278:12443–12451.
   PubMed Web of Science ®Google Scholar
• Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:32377–32379.
   PubMed Web of Science ®Google Scholar
• Feldman, R. M., C. C. Correll, K. B. Kaplan, and R. J. Deshaies. 1997. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91:221–230.
   PubMed Web of Science ®Google Scholar
• Fero, M. L., M. Rivkin, M. Tasch, P. Porter, C. E. Carow, E. Firpo, K. Polyak, L. H. Tsai, V. Broudy, R. M. Perlmutter, K. Kaushansky, and J. M. Roberts. 1996. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85:733–744.
   PubMed Web of Science ®Google Scholar
• Goll, D. E., V. F. Thompson, H. Li, W. Wei, and J. Cong. 2003. The calpain system. Physiol. Rev. 83:731–801.
   PubMed Web of Science ®Google Scholar
• Gupta, S., T. Barrett, A. J. Whitmarsh, J. Cavanagh, H. K. Sluss, B. Derijard, and R. J. Davis. 1996. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15:2760–2770.
   PubMed Web of Science ®Google Scholar
• Gupta, S., D. Campbell, B. Derijard, and R. J. Davis. 1995. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267:389–393.
   PubMed Web of Science ®Google Scholar
• Gützkow, K. B., S. Naderi, and H. K. Blomhoff. 2002. Forskolin-mediated G1 arrest in acute lymphoblastic leukaemia cells: phosphorylated pRB sequesters E2Fs. J. Cell Sci. 115:1073–1082.
   PubMedGoogle Scholar
• Hocevar, B. A., T. L. Brown, and P. H. Howe. 1999. TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 18:1345–1356.
   PubMed Web of Science ®Google Scholar
• Iordanov, M., K. Bender, T. Ade, W. Schmid, C. Sachsenmaier, K. Engel, M. Gaestel, H. J. Rahmsdorf, and P. Herrlich. 1997. CREB is activated by UVC through a p38/HOG-1-dependent protein kinase. EMBO J. 16:1009–1022.
   PubMedGoogle Scholar
• Ishida, N., T. Hara, T. Kamura, M. Yoshida, K. Nakayama, and K. I. Nakayama. 2002. Phosphorylation of p27Kip1 on serine 10 is required for its binding to CRM1 and nuclear exports. J. Biol. Chem. 277:14355–14358.
   PubMed Web of Science ®Google Scholar
• Khan, Q. A., A. Dipple, and L. M. Anderson. 2002. Protease inhibitor-induced stabilization of p21(waf1/cip1) and cell-cycle arrest in chemical carcinogen-exposed mammary and lung cells. Mol. Carcinog. 33:1–8.
   PubMedGoogle Scholar
• Kiyokawa, H., R. D. Kineman, K. O. Manova-Todorova, V. C. Soares, E. S. Hoffman, M. Ono, D. Khanam, A. C. Hayday, L. A. Frohman, and A. Koff. 1996. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85:721–732.
   PubMed Web of Science ®Google Scholar
• Kobayashi, T., J. Lu, B. S. Cobb, S. J. Rodda, A. P. McMahon, E. Schipani, M. Merkenschlager, and H. M. Kronenberg. 2008. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc. Natl. Acad. Sci. U. S. A. 105:1949–1954.
   PubMed Web of Science ®Google Scholar
• Kronenberg, H. M. 2007. The role of the perichondrium in fetal bone development. Ann. N. Y. Acad. Sci. 1116:59–64.
   PubMedGoogle Scholar
• Le, X. F., F. X. Claret, A. Lammayot, L. Tian, D. Deshpande, R. LaPushin, A. M. Tari, and R. C. Bast, Jr. 2003. The role of cyclin-dependent kinase inhibitor p27Kip1 in anti-HER2 antibody-induced G1 cell cycle arrest and tumor growth inhibition. J. Biol. Chem. 278:23441–23450.
   PubMed Web of Science ®Google Scholar
• Lee, C., T. J. Gardella, A. B. Abou-Samra, S. R. Nussbaum, G. V. Segre, J. T. Potts, Jr., H. M. Kronenberg, and H. Juppner. 1994. Role of the extracellular regions of the parathyroid hormone (PTH)/PTH-related peptide receptor in hormone binding. Endocrinology 135:1488–1495.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Liu, Z., J. Xu, J. S. Colvin, and D. M. Ornitz. 2002. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev. 16:859–869.
   PubMed Web of Science ®Google Scholar
• Livingstone, C., G. Patel, and N. Jones. 1995. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14:1785–1797.
   PubMed Web of Science ®Google Scholar
• Long, F., U. I. Chung, S. Ohba, J. McMahon, H. M. Kronenberg, and A. P. McMahon. 2004. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 131:1309–1318.
   PubMed Web of Science ®Google Scholar
• MacLean, H. E., J. Guo, M. C. Knight, P. Zhang, D. Cobrinik, and H. M. Kronenberg. 2004. The cyclin-dependent kinase inhibitor p57(Kip2) mediates proliferative actions of PTHrP in chondrocytes. J. Clin. Invest. 113:1334–1343.
   PubMedGoogle Scholar
• Matsushime, H., M. E. Ewen, D. K. Strom, J. Y. Kato, S. K. Hanks, M. F. Roussel, and C. J. Sherr. 1992. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell 71:323–334.
   PubMed Web of Science ®Google Scholar
• Nakayama, K., N. Ishida, M. Shirane, A. Inomata, T. Inoue, N. Shishido, I. Horii, D. Y. Loh, and K. Nakayama. 1996. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85:707–720.
   PubMed Web of Science ®Google Scholar
• Ohbayashi, N., M. Shibayama, Y. Kurotaki, M. Imanishi, T. Fujimori, N. Itoh, and S. Takada. 2002. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev. 16:870–879.
   PubMedGoogle Scholar
• Ornitz, D. M., and P. J. Marie. 2002. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 16:1446–1465.
   PubMed Web of Science ®Google Scholar
• Parada, Y., L. Banerji, J. Glassford, N. C. Lea, M. Collado, C. Rivas, J. L. Lewis, M. Y. Gordon, N. S. Thomas, and E. W. Lam. 2001. BCR-ABL and interleukin 3 promote haematopoietic cell proliferation and survival through modulation of cyclin D2 and p27Kip1 expression. J. Biol. Chem. 276:23572–23580.
   PubMed Web of Science ®Google Scholar
• Patel, Y. M., and M. D. Lane. 2000. Mitotic clonal expansion during preadipocyte differentiation: calpain-mediated turnover of p27. J. Biol. Chem. 275:17653–17660.
   PubMedGoogle Scholar
• Raingeaud, J., S. Gupta, J. S. Rogers, M. Dickens, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270:7420–7426.
   PubMed Web of Science ®Google Scholar
• Rodda, S. J., and A. P. McMahon. 2006. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133:3231–3244.
   PubMed Web of Science ®Google Scholar
• Rodier, G., A. Montagnoli, L. Di Marcotullio, P. Coulombe, G. F. Draetta, M. Pagano, and S. Meloche. 2001. p27 cytoplasmic localization is regulated by phosphorylation on Ser10 and is not a prerequisite for its proteolysis. EMBO J. 20:6672–6682.
   PubMed Web of Science ®Google Scholar
• Schipani, E., K. Kruse, and H. Juppner. 1995. A constitutively active mutant PTH-PTHrP receptor in Jansen-type metaphyseal chondrodysplasia. Science 268:98–100.
   PubMed Web of Science ®Google Scholar
• Shimada, M., P. A. Greer, A. P. McMahon, M. L. Bouxsein, and E. Schipani. 2008. In vivo targeted deletion of calpain small subunit, capn4, in cells of the osteoblast lineage impairs cell proliferation, differentiation, and bone formation. J. Biol. Chem. 283:21002–21010.
   PubMedGoogle Scholar
• Shimada, M., M. J. Mahon, P. A. Greer, and G. V. Segre. 2005. The receptor for parathyroid hormone and parathyroid hormone-related peptide is hydrolyzed and its signaling properties are altered by directly binding the calpain small subunit. Endocrinology 146:2336–2344.
   PubMedGoogle Scholar
• Shimizu, K., T. Hamamoto, T. Hamakubo, W. J. Lee, K. Suzuki, Y. Nakagawa, T. Murachi, and T. Yamamuro. 1991. Immunohistochemical and biochemical demonstration of calcium-dependent cysteine proteinase (calpain) in calcifying cartilage of rats. J. Orthop. Res. 9:26–36.
   PubMed Web of Science ®Google Scholar
• Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209–219.
   PubMed Web of Science ®Google Scholar
• Sutterlüty, H., E. Chatelain, A. Marti, C. Wirbelauer, M. Senften, U. Muller, and W. Krek. 1999. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat. Cell Biol. 1:207–214.
   PubMed Web of Science ®Google Scholar
• Tan, Y., N. Dourdin, C. Wu, T. De Veyra, J. S. Elce, and P. A. Greer. 2006. Conditional disruption of ubiquitous calpains in the mouse. Genesis 44:297–303.
   PubMedGoogle Scholar
• Tan, Y., J. Rouse, A. Zhang, S. Cariati, P. Cohen, and M. J. Comb. 1996. FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J. 15:4629–4642.
   PubMed Web of Science ®Google Scholar
• Tsvetkov, L. M., K. H. Yeh, S. J. Lee, H. Sun, and H. Zhang. 1999. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr. Biol. 9:661–664.
   PubMed Web of Science ®Google Scholar
• Urano, T., H. Yashiroda, M. Muraoka, K. Tanaka, T. Hosoi, S. Inoue, Y. Ouchi, and H. Toyoshima. 1999. p57(Kip2) is degraded through the proteasome in osteoblasts stimulated to proliferation by transforming growth factor beta1. J. Biol. Chem. 274:12197–12200.
   PubMed Web of Science ®Google Scholar
• Wang, X. D., J. L. Rosales, A. Magliocco, R. Gnanakumar, and K. Y. Lee. 2003. Cyclin E in breast tumors is cleaved into its low molecular weight forms by calpain. Oncogene 22:769–774.
   PubMed Web of Science ®Google Scholar
• Yamada, Y., T. Miyashita, P. Savagner, W. Horton, K. S. Brown, J. Abramczuk, H. X. Xie, K. Kohno, M. Bolander, and L. Bruggeman. 1990. Regulation of the collagen II gene in vitro and in transgenic mice. Ann. N. Y. Acad. Sci. 580:81–87.
   PubMedGoogle Scholar
• Yasuda, T., K. Shimizu, Y. Nakagawa, S. Yamamoto, H. Niibayashi, and T. Yamamuro. 1995. m-Calpain in rat growth plate chondrocyte cultures: its involvement in the matrix mineralization process. Dev. Biol. 170:159–168.
   PubMed Web of Science ®Google Scholar
• Zimmerman, U. J., L. Boring, J. H. Pak, N. Mukerjee, and K. K. Wang. 2000. The calpain small subunit gene is essential: its inactivation results in embryonic lethality. IUBMB Life 50:63–68.
   PubMedGoogle Scholar