Dual effects of the membrane-anchored MMP regulator RECK on chondrogenic differentiation of ATDC5 cells

Journal of Cell Science

Volumn 120, Issue 5, 2007, Pages 849-857

  Kondo, Shunya ^a,b   Shukunami, Chisa ^b   Morioka, Yoko ^a   Matsumoto, Naoya ^a   Takahashi, Rei ^a   Oh, Junseo ^a,f   Atsumi, Tadao ^c   Umezawa, Akihiro ^d   Kudo, Akira ^e   Kitayama, Hitoshi ^a   Hiraki, Yuji ^b   Noda, Makoto ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c Japan Science and Technology Agency   (Japan)

^d NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f Korea University College of Medicine   (South Korea)

Author keywords

Chondrogenesis; ECM remodeling; MMP; RECK; Tissue morphogenesis

Indexed keywords

COLLAGEN TYPE 2; MATRIX METALLOPROTEINASE; MESSENGER RNA; REVERSION INDUCING CYSTEINE RICH PROTEIN WITH KAZAL MOTIFS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL LINE; CHONDROGENESIS; CHROMOSOME CONDENSATION; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; EXTRACELLULAR MATRIX; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CARTILAGE; CELL DIFFERENTIATION; CELL LINE; CHONDROCYTES; COLLAGEN; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION PROFILING; GENE SILENCING; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; MATRIX METALLOPROTEINASES; MEMBRANE GLYCOPROTEINS; MICE; MUTATION;

MAMMALIA; MUS;

EID: 34047181098     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03388     Document Type: Article

References (52)

1. Apte, S. S., Seldin, M. E, Hayashi, M. and Olsen, B. R. (1992). Cloning of the human and mouse type X collagen genes and mapping of the mouse type X collagen gene to chromosome 10. Eur. J. Biochem. 206, 217-224.
2. Apte, S. S., Fukai, N., Beier, D. R. and Olsen, B. R. (1997). The matrix metalloproteinase-14 (MMP-14) gene is structurally distinct from other MMP genes and is co-expressed with the TIMP-2 gene during mouse embryogenesis. J. Biol. Chem. 272, 25511-25517.
3. Atsumi, T., Miwa, Y., Kimata, K. and Ikawa, Y. (1990). A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Differ. Dev. 30, 109-116.
4. Behonick, D. J. and Werb, Z. (2003). A bit of give and take: the relationship between the extracellular matrix and the developing chondrocyte. Mech. Dev. 120, 1327-1336.
5. Braissant, O., Foufelle, F., Scotto, C., Dauca, M. and Wahli, W. (1996). Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 137, 354-366.
6. Buckwalter, J. A. (2002). Articular cartilage injuries. Clin. Orthop. Relat. Res. 402, 21-37.
7. Cancedda, R., Descalzi Cancedda, E. and Castagnola, P. (1995). Chondrocyte differentiation. Int. Rev. Cytol. 159, 265-358.
8. Chin, J. R. and Werb, Z. (1997). Matrix metalloproteinases regulate morphogenesis, migration and remodeling of epithelium, tongue skeletal muscle and cartilage in the mandibular arch. Development 124, 1519-1530.
9. Echizenya, M., Kondo, S., Takahashi, R., Oh, J., Kawashima, S., Kitayama, H., Takahashi, C. and Noda, M. (2005). The membrane-anchored MMP-regulator RECK is a target of myogenic regulatory factors. Oncogene 24, 5850-5857.
10. Egeblad, M. and Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174.
11. Fujii, M., Takeda, K., Imamura, T., Aoki, H., Sampath, T. K., Enomoto, S., Kawabata, M., Kato, M., Ichijo, H. and Miyazono, K. (1999). Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 10, 3801-3813.
12. Fujita, T., Azuma, Y., Fukuyama, R., Hattori, Y., Yoshida, C., Koida, M., Ogita, K. and Komori, T. (2004). Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J. Cell Biol. 166, 85-95.
13. Furumoto, K, Arii, S., Mori, A., Furuyama, H., Gorrin Rivas, M. J., Nakao, T., Isobe, N., Murata, T., Takahashi, C., Noda, M. et al. (2001). RECK gene expression in hepatocellular carcinoma: correlation with invasion-related clinicopathological factors and its clinical significance. Reverse-inducing cysteine-rich protein with Kazal motifs. Hepatology 33, 189-195.
14. Hall, B. K. and Miyake, T. (2000). All for one and one for all: condensations and the initiation of skeletal development. BioEssays 22, 138-147.
15. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S. A., Mankani, M., Robey, P. G., Poole, A. R., Pidoux, I. et al. (1999). MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
16. Imabayashi, H., Mori, T., Gojo, S., Kiyono, T., Sugiyama, T., Irie, R., Isogai, T., Hata, J., Toyama, Y. and Umezawa, A. (2003). Redifferentiation of dedifferentiated chondrocytes and chondrogenesis of human bone marrow stromal cells via chondrosphere formation with expression profiling by large-scale cDNA analysis. Exp. Cell Res. 288, 35-50.
17. Itoh, T., Ikeda, T., Gomi, H., Nakao, S., Suzuki, T. and Itohara, S. (1997). Unaltered secretion of beta-amyloid precursor protein in gelatinase A (matrix metalloproteinase 2)-deficient mice. J. Biol. Chem. 272, 22389-22392.
18. Jackson, C., Nguyen, M., Arkell, J. and Sambrook, P. (2001). Selective matrix metalloproteinase (MMP) inhibition in rheumatoid arthritis-targetting gelatinase A activation. Inflamm. Res. 50, 183-186.
19. James, C. G., Appleton, C. T., Ulici, V., Underhill, T. M. and Beier, F. (2005). Microarray analyses of gene expression during chondrocyte differentiation identifies novel regulators of hypertrophy. Mol. Biol. Cell 16, 5316-5333.
20. Kimura, T., Mattei, M. G., Stevens, J. W., Goldring, M. B., Ninomiya, Y. and Olsen, B. R. (1989). Molecular cloning of rat and human type IX collagen cDNA and localization of the alpha 1(IX) gene on the human chromosome 6. Eur. J. Biochem. 179, 71-78.
21. Knudson, C. B. and Toole, B. P. (1985). Changes in the pericellular matrix during differentiation of limb bud mesoderm. Dev. Biol. 112, 308-318.
22. Kohyama, J., Abe, H., Shimazaki, T., Koizumi, A., Nakashima, K., Gojo, S., Taga, T., Okano, H., Hata, J. and Umezawa, A. (2001). Brain from bone: efficient "meta-differentiation" of marrow stroma-derived mature osteoblasts to neurons with Noggin or a demethylating agent. Differentiation 68, 235-244.
23. Lambert, E., Dassé, E., Haye, B. and Petitfrère, E. (2004). TIMPs as multifacial proteins. Crit. Rev. Oncol. Hematol. 49, 187-198.
24. Martel-Pelletier, J., Welsch, D. J. and Pelletier, J. P. (2001). Metalloproteases and inhibitors in arthritic diseases. Best Pract. Res. Clin. Rheumatol. 15, 805-829.
25. Masui, T., Doi R., Koshiba, T., Fujimoto, K., Tsuji, S., Nakajima, S., Koizumi, M., Toyoda, E., Talachan, S., Ito, D. et al. (2003). RECK expression in pancreatic cancer: its correlation with lower invasiveness and better prognosis. Clin. Cancer Res. 9, 1779-1784.
26. Mizoguchi, I., Nakamura, M., Takahashi, I,, Kagayama, M. and Mitani, H. (1990). An immunohistochemical study of localization of type I and type II collagens in mandibular condylar cartilage compared with tibial growth plate. Histochemistry 93, 593-599.
27. Mori, T., Kiyono, T., Imabayashi, H., Takeda, Y., Tsuchiya, K., Miyoshi, S., Makino, H., Matsumoto, K., Saito, H., Ogawa, S. et al. (2005). Combination of hTERT and bmi-1, E6, or E7 induces prolongation of the life span of bone marrow stromal cells from an elderly donor without affecting their neurogenic potential. Mol. Cell. Biol. 25, 5183-5195.
28. Newman, B., Gigout, L. I., Sudre, L., Grant, M. E. and Wallis, G. A. (2001). Coordinated expression of matrix G1a protein is required during endochondral ossification for chondrocyte survival. J. Cell Biol. 154, 659-666.
29. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
30. Noda, M., Oh, J., Takahashi, R., Kondo, S., Kitayama, H. and Takahashi C. (2003). RECK: a novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling. Cancer Metastasis Rev. 22, 167-175.
31. Oh, J., Takahashi, R., Kondo, S., Mizoguchi, A., Adachi, E., Sasahara, R. M., Nishimura, S., Imamura, Y., Kitayama, H., Alexander, D. B. et al. (2001). The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107, 789-800.
32. Oh, J., Takahashi, R., Adachi, E., Kondo, S., Kuratomi, S., Noma, A., Alexander, D. B., Motoda, H., Okada, A., Seiki, M. et al. (2004). Mutations in two matrix metalloproteinase genes, MMP-2 and MT1-MMP, are synthetic lethal in mice. Oncogene 23, 5041-508.
33. Reponen, P., Sahlberg, C., Huhtala, P., Hurskainen, T., Thesleff, I. and Tryggvason, K. (1992). Molecular cloning of murine 72-kDa type IV collagenase and its expression during mouse development. J. Biol. Chem. 267, 7856-7862.
34. Reponen, P., Sahlberg, C., Munaut, C., Thesleff, I. and Tryggvason, K. (1994). High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development. J. Cell Biol. 124, 1091-1102.
35. Sandberg, M. and Vuorio, E. (1987). Localization of types I, II, and III collagen mRNAs in developing human skeletal tissues by in situ hybridization. J. Cell Biol. 104, 1077-1084.
36. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
37. Scheijen, B., Bronk, M., van der Meer, T. and Bernards, R. (2003). Constitutive E2F1 overexpression delays endochondral bone formation by inhibiting chondrocyte differentiation. Mol. Cell. Biol. 23, 3656-3668.
38. Shen, M., Yoshida, E., Yan, W., Kawamoto, T., Suardita, K., Koyano, Y., Fujimoto, K., Noshiro, M. and Kato, Y. (2002). Basic helix-loop-helix protein DEC1 promotes chondrocyte differentiation at the early and terminal stages. J. Biol. Chem. 277, 50112-50120.
39. Shukunami, C., Shigeno, C., Atsumi, T., Ishizeki, K., Suzuki, F. and Hiraki, Y. (1996). Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J. Cell Biol. 133, 457-468.
40. Shukunami, C., Ishizeki, K., Atsumi, T., Ohta, Y., Suzuki, F. and Hiraki, Y. (1997). Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J. Bone Miner. Res. 12, 1174-1188.
41. Shukunami, C., Ohta, Y., Sakuda, M. and Hiraki, Y. (1998). Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp. Cell Res. 241, 1-11.
42. Span, P. N., Sweep, C. G., Manders, P., Beex, L. V., Leppert, D. and Lindberg, R. L. (2003). Matrix metalloproteinase inhibitor reversion-inducing cysteine-rich protein with Kazal motifs: a prognostic marker for good clinical outcome in human breast carcinoma. Cancer 97, 2710-2715.
43. Takahashi, C, Sheng, Z., Horan, T. P., Kitayama, H., Maki, M., Hitomi, K., Kitaura, Y., Takai, S., Sasabara, R. M., Horimoto, A. et al. (1998). Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc. Natl. Acad Sci. USA 95, 13221-13226.
44. Takenaka, K., Ishikawa, S., Kawano, Y., Yanagihara, K., Miyahara, R., Otake, Y., Morioka, Y., Takahashi, C., Noda, M., Wada, H. et al. (2004). Expression of a novel matrix metalloproteinase regulator, RECK, and its clinical significance in resected non-small cell lung cancer. Eur. J. Cancer 40, 1617-1623.
45. Takeshita, S., Kaji, K. and Kudo, A. (2000). Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J. Bone Miner. Res. 15, 1477-1488.
46. Takeuchi, T., Hisanaga, M., Nagao, M., Ikeda, N., Fujii, H., Koyama, R, Mukogawa, T., Matsumoto, H., Kondo, S., Takahashi, C. et al. (2004). The membrane-anchored matrix metalloproteinase (MMP) regulator RECK in combination with MMP-9 serves as an informative prognostic indicator for colorectal cancer. Clin. Cancer Res. 10, 5572-5579.
47. Tanaka, H., Hojo, K., Yoshida, H., Yoshioka, T. and Sugita, K. (1993). Molecular cloning and expression of the mouse 105-kDa gelatinase cDNA. Biochem. Biophys. Res. Commun. 190, 732-740.
48. van Lent, P. L., Span, P. N., Sloetjes, A. W., Radstake, T. R., van Lieshout, A. W., Heuvel, J. J., Sweep, C. G. and van den Berg, W. B. (2005). Expression and localisation of the new metalloproteinase inhibitor RECK (reversion inducing cysteine-rich protein with Kazal motifs) in inflamed synovial membranes of patients with rheumatoid arthritis. Ann. Rheum. Dis. 64, 368-374.
49. Vu, T. H. and Werb, Z. (2000). Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14, 2123-2133.
50. Vu. T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M. and Werb, Z. (1998). MMP-9/ gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422.
51. Woods, A., Wang, G. and Beier, F. (2005). RhoA/ROCK signaling regulates Sox9 expression and actin organization during choadrogenesis. J. Biol. Chem. 280, 11626-11634.
52. Zhou, Z., Apte, S. S., Soininen, R., Cao, R., Baaklini, G. Y., Rauser, R. W., Wang, J., Cao, Y. and Tryggvason, K. (2000). Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 97, 4052-4057.