CREB Cooperates with BMP-Stimulated Smad Signaling to Enhance Transcription of the Smad6 Promoter

Journal of Cellular Physiology

Volumn 198, Issue 3, 2004, Pages 428-440

  Ionescu, Andreia M ^a   Drissi, Hicham ^a   Schwarz, Edward M ^a   Kato, Mitsuyasu ^b   Puzas, J Edward ^a   McCance, Dennis J ^a   Rosier, Randy N ^a   Zuscik, Michael J ^a   O'Keefe, Regis J ^a,c  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 10; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DNA BINDING PROTEIN; HEDGEHOG PROTEIN, VERTEBRATE; PARATHYROID HORMONE RELATED PROTEIN; PROTEIN KINASE A KINASE; PROTEIN SERINE THREONINE KINASE; SMAD PROTEIN; SMAD6 PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL; ANIMAL CELL; ARTICLE; BASE PAIRING; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL SPECIFICITY; COLX GENE; COMPARATIVE STUDY; DNA RESPONSIVE ELEMENT; DRUG EFFECT; ELECTROPHORETIC MOBILITY; EMBRYO; GEL MOBILITY SHIFT ASSAY; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH PLATE; INHIBITION KINETICS; LHH GENE; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMAD6 GENE; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE X; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEDGEHOG PROTEINS; MOLECULAR SEQUENCE DATA; PARATHYROID HORMONE-RELATED PROTEIN; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMAD6 PROTEIN; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

VERTEBRATA;

EID: 1242339699     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10421     Document Type: Article

References (51)

1. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C. 1998. A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18:967-977.
2. Bai S, Shi X, Yang X, Cao X. 2000. Smad6 as a transcriptional corepressor. J Biol Chem 275:8267-8270.
3. Benbrook DM, Jones NC. 1994. Different binding specificities and tranactivation of variant CRE's by CREB complexes. Nucleic Acids Res 22:1463-1469.
4. Buckwalter JA, Mower D, Ungar R, Schaeffer J, Ginsberg B. 1986. Morphometric analysis of chondrocyte hypertrophy. J Bone Joint Surg [Am] 68:243-255.
5. Cancedda R, Descalzi Cancedda F, Castagnola P. 1995. Chondrocyte differentiation. Int Rev Cytol 159:265-358.
6. Castagnola P, Moro G, Descalzi-Cancedda F, Cancedda R. 1986. Type X collagen synthesis during in vitro development of chick embryo tibial chondrocytes. J Cell Biol 102:2310-2317.
7. Chen X, Rubock MJ, Whitman M. 1996. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature 383:691-696.
8. Clemens JW, Lala DS, Parker KL, Richards JS. 1994. Steroidogenic factor-1 binding and transcriptional activity of the cholesterol side-chain cleavage promoter in rat granulosa cells. Endocrinology 134:1499-1508.
9. Derynck R, Zhang Y, Feng XH. 1998. Smads: Transcriptional activators of TGF-beta responses. Cell 95:737-740.
10. Eresh S, Riese J, Jackson DB, Bohmann D, Bienz M. 1997. A CREB-binding site as a target for decapentaplegic signalling during Drosophila endoderm induction. EMBO J 16:2014-2022.
11. Erlebacher A, Filvaroff EH, Gitelman SE, Derynck R. 1995. Toward a molecular understanding of skeletal development. Cell 80:371-378.
12. Fitzpatrick SL, Richards JS. 1993. Cis-acting elements of the rat aromatase promoter required for cyclic 3′-, 5′-monophosphate induction in ovarian granulosa cells and constitutive expression in R2C Leydig cells. Mol Endocrinol 7:341-354.
13. Gibson GJ, Kohler WJ, Schaffler MB. 1995. Chondrocyte apoptosis in endochondral ossification of chick sterna. Dev Dyn 203:468-476.
14. Gonzalez GA, Montminy MR. 1989. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
15. Gonzalez GA, Yamamoto KK, Fischer WH, Karr D, Menzel P, Biggs WD, Vale WW, Montminy MR. 1989. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 337:749-752.
16. Gupta IR, Piscione TD, Grisaru S, Phan T, Macias-Silva M, Zhou X, Whiteside C, Wrana JL, Rosenblum ND. 1999. Protein kinase A is a negative regulator of renal branching morphogenesis and modulates inhibitory and stimulatory bone morphogenetic proteins. J Biol Chem 274:26305-26314.
17. Hanafusa H, Ninomiya-Tsuji J, Masuyama N, Nishita M, Fujisawa J, Shibuya H, Matsumoto K, Nishida E. 1999. Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-beta-induced gene expression. J Biol Chem 274:27161-27167.
18. Harada S, Sampath TK, Aubin JE, Rodan GA. 1997. Osteogenic protein-1 up-regulation of the collagen X promoter activity is mediated by a MEF-2-like sequence and requires an adjacent AP-1 sequence. Mol Endocrinol 11:1832-1845.
19. Hata A, Lagna G, Massague J, Hemmati-Brivanlou A. 1998. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12:186-197.
20. Hatori M, Klatte KJ, Teixeira CC, Shapiro IM. 1995. End labeling studies of fragmented DNA in the avian growth plate: Evidence of apoptosis in terminally differentiated chondrocytes. J Bone Miner Res 10:1960-1968.
21. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA, Jr., Wrana JL, Falb D. 1997. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 89:1165-1173.
22. Hughes SH, Greenhouse JJ, Petropoulos CJ, Sutrave P. 1987. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J Virol 61:3004-3012.
23. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. 1997. Smad6 inhibits signalling by the TGF-beta superfamily. Nature 389:622-626.
24. Ionescu AM, Schwarz EM, Vinson C, Puzas JE, Rosier R, Reynolds PR, O'Keefe RJ. 2001. PTHrP modulates chondrocyte differentiation through AP-1 and CREB signaling. J Biol Chem 276:11639-11647.
25. Ishida W, Hamamoto T, Kusanagi K, Yagi K, Kawabata M, Takehara K, Sampath TK, Kato M, Miyazono K. 2000. Smad6 is a Smad1/5-induced smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. J Biol Chem 275:6075-6079.
26. Juppner H, Abou-Samra AB, Freeman M, Kong XF, Richards J, Kolakowski LFJ, Hock J, Potts JTJ, Kronenberg HN, Segre GV. 1991. A G protein-linked receptor for parathyroid hormone and parathyroid hormone-related peptide. Science 254:1024-1026.
27. Karaplis AC, Luz A, Glowacki J, Bronson RT, Tybulewicz VL, Kronenberg HM, Mulligan RC. 1994. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev 8:277-289.
28. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A. 1997. Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388:304-308.
29. Kretzschmar M, Doody J, Massague J. 1997. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389:618-622.
30. Kusanagi K, Inoue H, Ishidou Y, Mishima HK, Kawabata M, Miyazono K. 2000. Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol Biol Cell 11:555-565.
31. Labbe E, Silvestri C, Hoodless PA, Wrana JL, Attisano L. 1998. Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol Cell 2:109-120.
32. Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LHK, Ho C, Mulligan RC, Abou-Samra AB, Juppner H, Segre GV, Kronenberg HM. 1996. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth [see comments]. Science 273:663-666.
33. Leboy PS, Vaias L, Uschmann B, Golub E, Adams SL, Pacifici M. 1989. Ascorbic acid induces alkaline phosphatase, type X collagen, and calcium deposition in cultured chick chondrocytes. J Biol Chem 264:17281-17286.
34. Lebrun JJ, Takabe K, Chen Y, Vale W. 1999. Roles of pathway-specific and inhibitory Smads in activin receptor signaling. Mol Endocrinol 13:15-23.
35. Lee YS, Chuong CM. 1997. Activation of protein kinase A is a pivotal step involved in both BMP-2- and cyclic AMP-induced chondrogenesis. J Cell Physiol 170:153-165.
36. Lee K, Lanske B, Karaplis AC, Deeds JD, Kohno H, Nissenson RA, Kronenberg HM, Segre GV. 1996. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 137:5109-5118.
37. Linsenmayer TF, Chen QA, Gibney E, Gordon MK, Marchant JK, Mayne R, Schmid TM. 1991. Collagen types IX and X in the developing chick tibiotarsus: Analyses of mRNAs and proteins. Development 111:191-196.
38. Mundlos S, Olsen BR. 1997a. Heritable diseases of the skeleton. Part I: Molecular insights into skeletal development-transcription factors and signaling pathways. FASEB J 11:125-132.
39. Mundlos S, Olsen BR. 1997b. Heritable diseases of the skeleton. Part II: Molecular insights into skeletal development-matrix components and their homeostasis. FASEB J 11:227-233.
40. Pathi S, Rutenberg JB, Johnson RL, Vortkamp A. 1999. Interaction of Ihh an BMP/noggin signaling during cartilage differentiation. Dev Biol 209:239-253.
41. Sano Y, Harada J, Tashiro S, Gotoh-Mandeville R, Maekawa T, Ishii S. 1999. ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-beta signaling. J Biol Chem 274:8949-8957.
42. Swarthout JT, Doggett TA, Lemker JL, Partridge NC. 2001. Stimulation of extracellular signal-regulated kinases and proliferation in rat osteoblastic cells by parathyroid hormone is protein kinase C-dependent. J Biol Chem 276:7586-7592.
43. Szuts D, Eresh S, Bienz M. 1998. Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction. Genes Dev 12:2022-2035.
44. Towler DA, Rodan GA. 1995. Identification of a rat osteocalcin promoter 3′-, 5′-cyclic adenosine monophosphate response region containing two PuGGTCA steroid hormone receptor binding motifs. Endocrinology 136:1089-1096.
45. Volk SW, Luvalle P, Leask T, Leboy PS. 1998. A BMP responsive transcriptional region in the chicken type X collagen gene. J Bone Miner Res 13:1521-1529.
46. Wilson TE, Mouw AR, Weaver CA, Milbrandt J, Parker KL. 1993. The orphan nuclear receptor NGFI-B regulates expression of the gene encoding steroid 21-hydroxylase. Mol Cell Biol 13:861-868.
47. Xu X, Yin Z, Hudson JB, Ferguson EL, Frasch M. 1998. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev 12:2354-2370.
48. Yakymovych I, Ten Dijke P, Heldin CH, Souchelnytskyi S. 2001. Regulation of Smad signaling by protein kinase C. FASEB J 15:553-555.
49. Zhang Y, Feng XH, Derynck R. 1998. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 394:909-913.
50. Zhang D, Ferguson C, O'Keefe RJ, Puzas JE, Rosier RN, Reynolds PR. 2002. A role for the BMP antagonist chordin in endochondral ossification. J Bone Min Res 17(2):293-300.
51. Zhou S, Zawel L, Lengauer C, Kinzler KW, Vogelstein B. 1998. Characterization of human FAST-1, a TGF beta and activin signal transducer. Mol Cell 2:121-127.