Transcriptional regulation of BMP2 expression by the PTH-CREB signaling pathway in osteoblasts

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Zhang, Rongrong ^a   Edwards, James R ^b   Ko, Seon Yle ^c   Dong, Shanshan ^a   Liu, Hongbin ^a   Oyajobi, Babatunde O ^d   Papasian, Christopher ^e   Deng, Hong Wen ^a   Zhao, Ming ^a,f  

^a TULANE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c Dankook University   (South Korea)

^d University of Texas Health Science Center   (United States)

^e UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^f Tulane University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; PARATHYROID HORMONE; BMP2 PROTEIN, MOUSE; CREB1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BONE METABOLISM; BONE MORPHOGENETIC PROTEIN 2 GENE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE MUTATION; GENETIC REGULATION; HORMONE ACTION; MOLECULAR INTERACTION; MOUSE; NEWBORN; NONHUMAN; OSTEOBLAST; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; TRANSCRIPTION INITIATION; UPREGULATION;

RODENTIA;

ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION; MICE; MOLECULAR SEQUENCE DATA; OSTEOBLASTS; PARATHYROID HORMONE; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 79958249441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020780     Document Type: Article

References (55)

1. Iida-Klein A, Zhou H, Lu SS, Levine LR, Ducayen-Knowles M, et al. (2002) Anabolic action of parathyroid hormone is skeletal site specific at the tissue and cellular levels in mice. J Bone Miner Res 17: 808-816.
2. Yu S, Franceschi RT, Luo M, Fan J, Jiang D, et al. (2009) Critical role of activating transcription factor 4 in the anabolic actions of parathyroid hormone in bone. PLoS One 4: e7583.
3. Demiralp B, Chen HL, Koh AJ, Keller ET, McCauley LK, (2002) Anabolic actions of parathyroid hormone during bone growth are dependent on c-fos. Endocrinology 143: 4038-4047.
4. Zhou H, Iida-Klein A, Lu SS, Ducayen-Knowles M, Levine LR, et al. (2003) Anabolic action of parathyroid hormone on cortical and cancellous bone differs between axial and appendicular skeletal sites in mice. Bone 32: 513-520.
5. Mosekilde L, Tornvig L, Thomsen JS, Orhii PB, Banu MJ, et al. (2000) Parathyroid hormone and growth hormone have additive or synergetic effect when used as intervention treatment in ovariectomized rats with established osteopenia. Bone 26: 643-651.
6. Qi H, Li M, Wronski TJ, (1995) A comparison of the anabolic effects of parathyroid hormone at skeletal sites with moderate and severe osteopenia in aged ovariectomized rats. J Bone Miner Res 10: 948-955.
7. Neer RM, Arnaud CD, Zanchetta JR, Prince R, Gaich GA, et al. (2001) Hodsman AB, Eriksen EF, Ish-Shalom S, Genant HK, Wang O, Mitlak BH Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 344: 1434-1441.
8. Hodsman AB, Bauer DC, Dempster DW, Dian L, Hanley DA, et al. (2005) Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr Rev 26: 688-703.
9. Cosman F, (2006) Anabolic therapy for osteoporosis: parathyroid hormone. Curr Rheumatol Rep 8: 63-69.
10. Thomas T, (2006) Intermittent parathyroid hormone therapy to increase bone formation. Joint Bone Spine 73: 262-269.
11. Tintut Y, Patel J, Parhami F, Demer LL, (2000) Tumor necrosis factor-alpha promotes in vitro calcification of vascular cells via the cAMP pathway. Circulation 102: 2636-2642.
12. Schnoke M, Midura RJ, (2007) Pulsed electromagnetic fields rapidly modulate intracellular signaling events in osteoblastic cells: comparison to parathyroid hormone and insulin. J Orthop Res 25: 933-940.
13. Qin L, Partridge NC, (2005) Stimulation of amphiregulin expression in osteoblastic cells by parathyroid hormone requires the protein kinase A and cAMP response element-binding protein signaling pathway. J Cell Biochem 96: 632-640.
14. Tyson DR, Swarthout JT, Partridge NC, (1999) Increased osteoblastic c-fos expression by parathyroid hormone requires protein kinase A phosphorylation of the cyclic adenosine 3′,5′-monophosphate response element-binding protein at serine 133. Endocrinology 140: 1255-1261.
15. Swarthout JT, D'Alonzo RC, Selvamurugan N, Partridge NC, (2002) Parathyroid hormone-dependent signaling pathways regulating genes in bone cells. Gene 282: 1-17.
16. Swarthout JT, Tyson DR Jr, Jefcoat SC, Partridge NC, (2002) Induction of transcriptional activity of the cyclic adenosine monophosphate response element binding protein by parathyroid hormone and epidermal growth factor in osteoblastic cells. J Bone Miner Res 17: 1401-1407.
17. Inoue D, Kido S, Matsumoto T, (2004) Transcriptional induction of FosB/DeltaFosB gene by mechanical stress in osteoblasts. J Biol Chem 279: 49795-49803.
18. Ogasawara A, Arakawa T, Kaneda T, Takuma T, Sato T, et al. (2001) Fluid shear stress-induced cyclooxygenase-2 expression is mediated by C/EBP beta, cAMP-response element-binding protein, and AP-1 in osteoblastic MC3T3-E1 cells. J Biol Chem 276: 7048-7054.
19. Takai H, Nakayama Y, Kim DS, Arai M, Araki S, et al. (2007) Androgen receptor stimulates bone sialoprotein (BSP) gene transcription via cAMP response element and activator protein 1/glucocorticoid response elements. J Cell Biochem 102: 240-251.
20. Matsuo N, Tanaka S, Gordon MK, Koch M, Yoshioka H, et al. (2005) CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts. J Biol Chem 281: 5445-5452.
21. Detry C, Lamour V, Castronovo V, Bellahcène A, (2008) CREB-1 and AP-1 transcription factors JunD and Fra-2 regulate bone sialoprotein gene expression in human breast cancer cells. Bone 42: 422-431.
22. Huang WC, Xie Z, Konaka H, Sodek J, Zhau HE, et al. (2005) Human osteocalcin and bone sialoprotein mediating osteomimicry of prostate cancer cells: role of cAMP-dependent protein kinase A signaling pathway. Cancer Res 65: 2303-2313.
23. Zhao L, Li G, Zhou GQ, (2009) SOX9 directly binds CREB as a novel synergism with the PKA pathway in BMP-2-induced osteochondrogenic differentiation. J Bone Miner Res 24: 826-836.
24. Pekkinen M, Ahlström ME, Riehle U, Huttunen MM, Lamberg-Allardt CJ, (2008) Effects of phosphodiesterase 7 inhibition by RNA interference on the gene expression and differentiation of human mesenchymal stem cell-derived osteoblasts. Bone 43: 84-91.
25. Ghayor C, Ehrbar M, San Miguel B, Grätz KW, Weber FE, (2009) cAMP enhances BMP2-signaling through PKA and MKP1-dependent mechanisms. Biochem Biophys Res Commun 381: 247-252.
26. Nakao Y, Koike T, Ohta Y, Manaka T, Imai Y, et al. (2009) Parathyroid hormone enhances bone morphogenetic protein activity by increasing intracellular 3′, 5′-cyclic adenosine monophosphate accumulation in osteoblastic MC3T3-E1 cells. Bone 44: 872-877.
27. Kinoshita T, Kobayashi S, Ebara S, Yoshimura Y, Horiuchi H, et al. (2000) Phosphodiesterase inhibitors, pentoxifylline and rolipram, increase bone mass mainly by promoting bone formation in normal mice. Bone 27: 811-817.
28. Horiuchi H, Saito N, Kinoshita T, Wakabayashi S, Tsutsumimoto T, et al. (2001) Enhancement of bone morphogenetic protein-2-induced new bone formation in mice by the phosphodiesterase inhibitor pentoxifylline. Bone 28: 290-294.
29. Horiuchi H, Saito N, Kinoshita T, Wakabayashi S, Yotsumoto N, et al. (2002) Effect of phosphodiesterase inhibitor-4, rolipram, on new bone formations by recombinant human bone morphogenetic protein-2. Bone 30: 589-593.
30. Chandhoke TK, Huang YF, Liu F, Gronowicz GA, Adams DJ, et al. (2008) Osteopenia in transgenic mice with osteoblast-targeted expression of the inducible cAMP early repressor. Bone 43: 101-109.
31. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, et al. (1988) Novel regulators of bone formation: molecular clones and activities. Science 242: 1528-1534.
32. Rosen V, Nove J, Song JJ, Thies RS, Cox K, et al. (1994) Responsiveness of clonal limb bud cell lines to bone morphogenetic protein 2 reveals a sequential relationship between cartilage and bone cell phenotypes. J Bone Miner Res 9: 1759-1768.
33. Zhao M, Harris SE, Horn D, Geng Z, Nishimura R, et al. (2002) Bone morphogenetic protein receptor signaling is necessary for normal murine postnatal bone formation. J Cell Biol 157: 1049-1060.
34. Ionescu AM, Drissi H, Schwarz EM, Kato M, Puzas JE, et al. (2004) CREB Cooperates with BMP-stimulated Smad signaling to enhance transcription of the Smad6 promoter. J Cell Physiol 198: 428-440.
35. Zhao M, Edwards RJ, Ko SY, Parlato S, Harris SE, et al. (2009) CREB induces BMP2 transcription in osteoblasts and CREB knockout reduces bone mass in mice. Bone 44 (suppl 1): S27.
36. Liu H, Zhang RR, Dong SS, Edwards J, Ko SY, et al. (2010) Contributions of PTH-mediator CREB to postnatal bone mass in human and mouse through regulation of osteoblast function. ASBMR 2010 Annual Meeting at Toronto, Canada, Oral presentation, #1221.
37. Impey S, McCorkle SR, Cha-Molstad H, Dwyer JM, Yochum GS, et al. (2004) Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119: 1041-1054.
38. Zhao M, Qiao M, Oyajobi BO, Mundy GR, Chen D, (2003) E3 Ubiquitin ligase Smurf1 mediates Cbfa1 degradation and plays a specific role in osteoblast differentiation. J Biol Chem 278: 27939-27944.
39. Zhao M, Qiao M, Harris SE, Chen D, Oyajobi BO, et al. (2006) The zinc finger transcription factor Gli2 mediates bone morphogenetic protein 2 expression in osteoblasts in response to hedgehog signaling. Mol Cell Biol 26: 6197-6208.
40. Zhao M, Ko SY, Liu JH, Chen D, Wang BL, et al. (2009) Inhibition of microtubule assembly in osteoblasts stimulates BMP-2 expression and bone formation through the transcription factor Gli2. Mol Cell Biol 29: 1291-1305.
41. Persengiev SP, Green MR, (2003) The role of ATF/CREB family members in cell growth, survival and apoptosis. Apoptosis 8: 225-218.
42. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, et al. (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell 117: 387-398.
43. Han CY, Wang Y, Yu L, Powers D, Xiong X, et al. (2009) Small Molecules with potent osteogenic-inducing activity in osteoblast cells. Bioorg Med Chem Lett 19: 1442-1445.
44. Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, et al. (2008) Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135: 825-837.
45. Blois JT, Mataraza JM, Mecklenbraüker J, Tarakhovsky A, Chiles TC, (2004) B cell receptor-induced cAMP-response element-binding protein activation in B lymphocytes requires novel protein kinase Cdelta. J Biol Chem 279: 30123-30132.
46. Solomou EE, Juang YT, Tsokos DC, (2001) Protein kinase C-theta participates in the activation of cyclic AMP-responsive element-binding protein and its subsequent binding to the -180 site of the IL-2 promoter in normal human T lymphocytes. J Immunol 166: 5665-5674.
47. Garrett IR, Chen D, Gutierrez G, Zhao M, Escobedo A, et al. (2003) Selective inhibitors of the osteoblast proteasome stimulate bone formation in vivo and in vitro. J Clin Invest 111: 1771-1782.
48. Zhao M, Qiao M, Chen D, Harris SE, Oyajobi OB, et al. (2005) β-catenin is a powerful enhancer of BMP-2 gene expression in osteoblasts in vitro and in vivo. Bone 36 (Suppl 2): S142.
49. Su JL, Yang CY, Zhao M, Kuo ML, Yen ML, (2007) Forkhead proteins are critical for bone morphogenetic protein-2 regulation and anti-tumor activity of resveratrol. J Biol Chem 282: 19385-19398.
50. Groppe J, Greenwald J, Wiater E, Rodriguez-Leon J, Economides AN, et al. (2002) Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420: 636-642.
51. Groppe J, Greenwald J, Wiater E, Rodriguez-Leon J, Economides AN, et al. (2003) Structural basis of BMP signaling inhibition by Noggin, a novel twelve-membered cystine knot protein. J Bone Joint Surg Am 85: 52-58.
52. 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.
53. Cardinaux JR, Notis JC, Zhang Q, Vo N, Craig JC, et al. (2000) Recruitment of CREB binding protein is sufficient for CREB-mediated gene activation. Mol Cell Biol 20: 1546-1552.
54. Ghosh-Choudhury N, Windle JJ, Koop BA, Harris MA, Guerrero DL, et al. (1996) Immortalized murine osteoblasts derived from BMP 2-T-antigen expressing transgenic mice. Endocrinology 137: 331-339.
55. Mantamadiotis T, Lemberger T, Bleckmann SC, Kern H, Kretz O, et al. (2000) Disruption of CREB function in brain leads to neurodegeneration. Nat Genet 31: 47-54.