Retinoid signaling regulates CTGF expression in hypertrophic chondrocytes with differential involvement of MAP kinases

Journal of Bone and Mineral Research

Volumn 20, Issue 5, 2005, Pages 867-877

  Shimo, Tsuyoshi ^a,b   Koyama, Eiki ^a   Sugito, Hiroki ^a   Wu, Changshan ^a   Shimo, Satoko ^a   Pacifici, Maurizio ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

BMPs; Chondrocyte maturation; Connective tissue growth factor; Mitogen activated protein kinases; Retinoid signaling; Skeletogenesis

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COLLAGEN TYPE 10; CONNECTIVE TISSUE GROWTH FACTOR; HORMONE ANTAGONIST; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; RETINOIC ACID; RETINOIC ACID RECEPTOR GAMMA; RETINOID; RO 41 5253; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL CULTURE; CELL FUNCTION; CELL MATURATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; ENCHONDRAL OSSIFICATION; ENZYME INHIBITION; GENE EXPRESSION; GROWTH PLATE; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, NORTHERN; CHICK EMBRYO; CHONDROCYTES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HYPERTROPHY; IMMEDIATE-EARLY PROTEINS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PROTEIN BINDING; RETINOIDS; SIGNAL TRANSDUCTION; TIME FACTORS; TRETINOIN;

EID: 17644402750     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/JBMR.041235     Document Type: Article

References (40)

1. Chambon P 1996 A decade of molecular biology of retinoic acid receptors. FASEB J 10:940-954.
2. Wilson JG, Roth CB, Warkany J 1953 An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 92:189-217.
3. Wolbach SB, Hegsted DM 1953 Hypervitaminosis A in young ducks. The epiphyseal cartilage. Arch Pathol 55:47-54.
4. Dolle P, Ruberte E, Kastner P, Petkovich M, Stoner CM, Gudas LJ, Chambon P 1989 Differential expression of genes encoding [α, β and γ] retinoic acid receptors and CRABP in the developing limbs of the mouse. Nature 342:702-705.
5. Lohnes D, Mark M, Mendelsohn C, Dolle P, Dierich A, Gorry P, Gansmuller A, Chambon P 1994 Function of the retinoic acid receptors (RARs) during development. I. Craniofacial and skeletal abnormalities in RAR double mutants. Development 120:2723-2748.
6. Iwamoto M, Shapiro IM, Yagami K, Boskey AL, Leboy PS, Adams SL, Pacifici M 1993 Retinoic acid induces rapid mineralization and expression of mineralization-related genes in chondrocytes. Exp Cell Res 207:413-420.
7. Koyama E, Golden EB, Kirsch T, Adams SL, Chandraratna RAS, Michaille J-J, Pacifici M 1999 Retinoid signaling is required for chondrocyte maturation and endochondral bone formation during limb skeletogenesis. Dev Biol 208:375-391.
8. Jimenez MJG, Balbin M, Alvarez J, Komori T, Bianco P, Holmbeck K, Birkedal-hansen H, Lopez JM, Lopez-Otin C 2001 A regulatory cascade involving retinoic acid, Cbfa1, and matrix metalloproteases is coupled to the development of a process of perichondrial invasion and osteogenic differentiation during bone formation. J Cell Biol 155:1333-1344.
9. Bradham DM, Igarashi A, Potter RL, Grotendorst GR 1991 Connective tissue growth factor: A cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J Cell Biol 114:1285-1294.
10. Lau LF, Lam SC 1999 The CCN family of angiogenic regulators: The integrin connection. Exp Cell Res 248:44-57.
11. Nakanishi T, Kimura Y, Tamura T, Ichikawa H, Yamaai Y, Sugimoto T, Takigawa M 1997 Cloning ofa mRNA preferentially expressed in chondrocytes by differential display-PCR from a human chondrocytic cell line that is identical with connective tissue growth factor (CTGF). Biochem Biophys Res Commun 234:206-210.
12. Nakanishi T, Nishida T, Shimo T, Kobayashi K, Kubo T, Tamatani T, Tezuka K, Takigawa M 2000 Effects of CTGF/ Hcs24, a product of a hypertrophic chondrocyte-specific gene, on the proliferation and differentiation of chondrocytes in culture. Endocrinology 141:264-273.
13. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, Daluiski A, Lyons KM 2003 Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130:2779-2791.
14. Johnson GL, Lapadat R 2002 Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298:1911-1912.
15. Yoon YM, Oh CD, Kim DY, Lee YS, Park JW, Huh TL, Kang SS, Chun JS 2000 Epidermal growth factor negatively regulates chondrogenesis of mesenchymal cells by modulating the protein kinase C-alpha, Erk-1, and p38 MAPK signaling pathways. J Biol Chem 275:12353-12359.
16. Murakami S, Kan M, McKeehan WL, de Crombrugghe B 2000 Dp-regulation of the chondrogenic factor Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 97:1113-1118.
17. Hirota Y, Tsukazaki T, Yonekura A, Miyazaki Y, Osaki M, Shindo H, Yamashita S 2000 Activation of specific MEK-ERK cascade is necessary for TGF beta signaling and crosstalk with PKA and PKC pathways in cultured rat articular chondrocytes. Osteoarthritis Cartilage 8:241-247.
18. Yosimichi G, Nakanishi T, Nishida T, Hattori T, Takano-Yamamoto T, Takigawa M 2001 CTGF-Hcs24 induces chondrocyte differentiation through a p38 mitogen-activated protein kinase (p38MAPK), and proliferation through a p44/42 MAPK/extracellular-signal regulated kinase (ERK). Eur J Biochem 268:6058-6065.
19. Alsayed Y, Uddin S, Mahmud N, Lekmine F, Kalvakolanu DV, Minucci S, Bokoch G, Platanias LC 2001 Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to all-trans-retinoic acid. J Biol Chem 276:4012-4019.
20. Crowe DL, Kim R, Chandraratna RAS 2003 retinoic acid differentially regulates cancer cell proliferation via dose-dependent modulation of the mitogen-activated protein kinase pathway. Mol Cancer Res 1:532-540.
21. Mukudai Y, Kubota S, Takigawa M 2003 Conserved repressive regulation of connective tissue growth factor/hypertrophic chondrocyte-specific gene 24 (ctgf/hcs24) enabled by different elements and factors among vertebrate species. Biol Chem 384:1-9.
22. D'Angelo M, Pacifici M 1997 Articular chondrocytes produce factors that inhibit maturation of sternal chondrocytes in serum-free agarose cultures: A TGFb independent process. J Bone Miner Res 12:1368-1377.
23. Shimo T, Wu C, Billings PC, Piddington R, Rosenbloom J, Pacifici M, Koyama E 2002 Expression, gene regulation, and roles of Fisp12/CTGF in developing tooth germs. Dev Dyn 224:267-278.
24. Apfel C, Bauer F, Crettaz M, Forni L, Kamber M, Kaufmann F, LeMotte P, Pirson W, Klaus M 1992 A retinoic acid receptor [α] antagonist selectively counteracts retinoic acid effects. Proc Natl Acad Sci USA 89:7129-7133.
25. von Schroeder HP, Heersche JNM 1998 Retinoic acid responsiveness of cells and tissues in developing fetal limbs evaluated in a RAREhsplacZ transgenic mouse model. J Orthop Res 16:355-364.
26. Young PR, McLaughlin MM, Kumar S, Kassis S, Doyle ML, McNulty D, Gallagher TF, Fisher S, McDonnell PC, Carr SA, Huddleston MJ, Seibel G, Porter TG, Livi GP, Adams JL, Lee JC 1997 Pyridinyl imidazole inhibitors pf p38 mitogen-activated protein kinase bind in the ATP site. J Biol Chem 272:12116-12121.
27. Zhen X, Wei L, Wu Q, Zhang Y, Chen Q 2001 Mitogen-activated protein kinase p38 mediates regulation of chondrocyte differentiation by parathyroid hormone. J Biol Chem 276:4879-4885.
28. Leboy PS, Sullivan TA, Nooreyazdan M, Venezian RA 1997 Rapid chondrocyte mturation by serum-free culture with BMP-2 and ascorbic acid. J Cell Biochem 66:394-403.
29. Grimsrud CD, Romano PR, D'Souza M, Puzas JE, Reynolds PR, Rosier RN, O'Keefe RJ 1999 BMP-6 is an autocrine stimulator of chondrocyte differentiation. J Bone Miner Res 14:475-482.
30. Adams SL, Pallante KM, Niu Z, Cohen AJ, Lu J, Leboy PS 2003 Stimulation of type-X collagen gene transcription by retinoids occurs in part through the BMP signaling pathway. J Bone Joint Surg Am 85:29-33.
31. Iwamoto M, Kitagaki J, Tamamura Y, Gentili C, Koyama E, Enomoto H, Komori T, Pacifici M, Enomoto-Iwamoto M 2003 Runx2 expression and action in chondrocytes are regulated by retinoid signaling and parathyroid hormone-related peptide (PTHrP). Osteoarthritis Cartilage 11:6-15.
32. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao Y-H, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T 1997 Targeted disruption of Cbfa1 results in complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
33. Shalom-Barak T, Quach J, Lotz M 1998 Interleuikin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-kB. J Biol Chem 273:27467-27473.
34. 2 production by epidermal growth factor via mitogen-activated protein kinase in articular chondrocytes. J Biol Chem 278:9691-9697.
35. Iyama KI, Ninomiya Y, Olsen BR, Linsenmayer TF, Trelstad RL, Hayashi M 1991 Spatiotemporal pattern of type X collagen gene expression and collagen deposition in embryonic chick vertebrae undergoing endochondral ossification. Anat Rec 229:462-472.
36. Oh CD, Chang SH, Yoon YM, Lee SJ, Lee YS, Kang SS, Chun JS 2000 Opposing tole of mitogen-activated protein kinase subtypes, Erk-1/2 and p38, in the regulation of chondrogenesis of mesenchymes. J Biol Chem 275:5613-5619.
37. Hoffman LM, Weston AD, Underbill TM 2003 Molecular mechanisms regulating chondroblast differentiation. J Bone Joint Surg Am 85:124-132.
38. Legendre F, Dudhia J, Pujol J-P, Bogdanowicz P 2003 JAK/ STAT but not ERK1/ERK2 pathway mdiates interleukin (IL)-6/Soluble IL-6R down-regulation of type II collagen, aggrecan core, and link protein transcription in articular chondrocytes. J Biol Chem 278:2903-2912.
39. 2 via ATP in articular chondrocytes. J Biol Chem 278:13680-13687.
40. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, Karsenty G, Franceschi RT 2000 MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem 275:4453-4459.