Regulation of RUNX2 transcription factor-DNA interactions and cell proliferation by vitamin D3 (cholecalciferol) prohormone activity

Journal of Bone and Mineral Research

Volumn 27, Issue 4, 2012, Pages 913-925

  Underwood, Karen F ^a   D'Souza, David R ^a,c   Mochin Peters, Maria ^a   Pierce, Adam D ^a   Kommineni, Sravya ^a   Choe, Moran ^a   Bennett, Jessica ^a   Gnatt, Averell ^a   Habtemariam, Bahru ^a,b   MacKerell, Alexander D ^b   Passaniti, Antonino ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^c Greenebaum Cancer Center/BRB 9 045 ^*  (United States)

Author keywords

cell proliferation; computational methods; DNA binding; RUNX2 transcription factor; Vitamin D3

Indexed keywords

ALENDRONIC ACID; COLECALCIFEROL; NOCODAZOLE; OSTEOCALCIN; TERAMEPROCOL; TRANSCRIPTION FACTOR RUNX2; VASCULOTROPIN; VITAMIN D RECEPTOR;

ARTICLE; BINDING SITE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL LINE; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CRYSTAL STRUCTURE; DNA BINDING; DRUG STRUCTURE; ENDOTHELIUM CELL; HORMONE ACTION; OSSIFICATION; OSTEOPOROSIS; OSTEOSARCOMA CELL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 84858734844     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1504     Document Type: Article

References (56)

1. Campbell FC, Xu H, El-Tanani M, Crowe P, Bingham V,. The yin and yang of vitamin D receptor (VDR) signaling in neoplastic progression: operational networks and tissue-specific growth control. Biochem Pharmacol. 2010; 79 (1): 1-9.
2. Adams JS, Hewison M,. Unexpected actions of vitamin D: new perspectives on the regulation of innate and adaptive immunity. Nat Clin Pract Endocrinol Metab. 2008; 4 (2): 80-90. (Pubitemid 351156900)
3. Christakos S, Ajibade DV, Dhawan P, Fechner AJ, Mady LJ,. Vitamin D: metabolism. Endocrinol Metab Clin North Am. 2010; 39 (2): 243-53, table of contents.
4. Chen TC, Persons KS, Lu Z, Mathieu JS, Holick MF,. An evaluation of the biologic activity and vitamin D receptor binding affinity of the photoisomers of vitamin D3 and previtamin D3. J Nutr Biochem. 2000; 11 (5): 267-72. (Pubitemid 30392412)
5. Narvaez CJ, Zinser G, Welsh J,. Functions of 1alpha,25-dihydroxyvitamin D(3) in mammary gland: from normal development to breast cancer. Steroids. 2001; 66 (3-5): 301-8. (Pubitemid 32140908)
6. Knight JA, Lesosky M, Barnett H, Raboud JM, Vieth R,. Vitamin D and reduced risk of breast cancer: a population-based case-control study. Cancer Epidemiol Biomarkers Prev. 2007; 16 (3): 422-9. (Pubitemid 46548644)
7. Hiatt RA, Krieger N, Lobaugh B, Drezner MK, Vogelman JH, Orentreich N,. Prediagnostic serum vitamin D and breast cancer. J Natl Cancer Inst. 1998; 90 (6): 461-3. (Pubitemid 28160638)
8. Jacobs ET, Martinez ME, Jurutka PW,. Vitamin d: marker or mechanism of action?. Cancer Epidemiol Biomarkers Prev. 2011; 20 (4): 585-90.
9. Stein GS, Lian JB, van Wijnen AJ, Stein JL, Montecino M, Javed A, Zaidi SK, Young DW, Choi JY, Pockwinse SM,. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene. 2004; 23 (24): 4315-29. (Pubitemid 38758597)
10. Sun L, Vitolo M, Qiao M, Anglin I, Passaniti A,. Regulation of TGFß1-mediated growth inhibition and apoptosis by RUNX2 isoforms. Oncogene. 2004; 3 (27): 4722-34. (Pubitemid 38859460)
11. Ducy P, Karsenty G,. Two distinct osteoblast-specific cis-acting elements control expression of a mouse osteocalcin gene. Mol Cell Biol. 1995; 15 (4): 1858-69.
12. Zelzer E, Glotzer DJ, Hartmann C, Thomas D, Fukai N, Soker S, Olsen BR,. Tissue specific regulation of VEGF expression during bone development requires Cbfa1/Runx2. Mech Dev. 2001; 106 (1-2): 97-106. (Pubitemid 32701077)
13. Sun L, Vitolo M, Passaniti A,. Runt-related gene 2 in endothelial cells: inducible expression and specific regulation of cell migration and invasion. Cancer Res. 2001; 61 (13): 4994-5001. (Pubitemid 32681526)
14. Anglin I, Passaniti A,. Runx protein signaling in human cancers. Cancer Treat Res. 2004; 119: 189-215.
15. Deeb KK, Trump DL, Johnson CS,. Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat Rev Cancer. 2007; 7 (9): 684-700. (Pubitemid 47327412)
16. Pratap J, Lian JB, Javed A, Barnes GL, van Wijnen AJ, Stein JL, Stein GS,. Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev. 2006; 25 (4): 589-600. (Pubitemid 46071865)
17. Bae SC, Lee YH,. Phosphorylation, acetylation and ubiquitination: the molecular basis of RUNX regulation. Gene. 2006; 366 (1): 58-66. (Pubitemid 43199594)
18. Vitolo MI, Anglin IE, Mahoney WM Jr, Renoud KJ, Gartenhaus RB, Bachman KE, Passaniti A,. The RUNX2 transcription factor cooperates with the YES-associated protein, YAP65, to promote cell transformation. Cancer Biol Ther. 2007; 6 (6): 856-63. (Pubitemid 351574974)
19. Qiao M, Shapiro P, Fosbrink M, Rus H, Kumar R, Passaniti A,. Cell cycle-dependent phosphorylation of the RUNX2 transcription factor by cdc2 regulates endothelial cell proliferation. J Biol Chem. 2006; 281 (11): 7118-28. (Pubitemid 43847476)
20. Rajgopal A, Young DW, Mujeeb KA, Stein JL, Lian JB, van Wijnen AJ, Stein GS,. Mitotic control of RUNX2 phosphorylation by both CDK1/cyclin B kinase and PP1/PP2A phosphatase in osteoblastic cells. J Cell Biochem. 2007; 100 (6): 1509-17. (Pubitemid 46515582)
21. Shen R, Wang X, Drissi H, Liu F, O'Keefe RJ, Chen D,. Cyclin D1-cdk4 induce runx2 ubiquitination and degradation. J Biol Chem. 2006; 281 (24): 16347-53.
22. Qiao M, Shapiro P, Kumar R, Passaniti A,. Insulin-like growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a PI3K/ERK-dependent and Akt-independent signaling pathway. J Biol Chem. 2004; 279: 42709-18. (Pubitemid 39372157)
23. Fujita T, Azuma Y, Fukuyama R, Hattori Y, Yoshida C, Koida M, Ogita K, Komori T,. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J Cell Biol. 2004; 166 (1): 85-95. (Pubitemid 38931919)
24. D'Souza DR, Salib MM, Bennett J, Mochin-Peters M, Asrani K, Goldblum SE, Renoud KJ, Shapiro P, Passaniti A,. Hyperglycemia regulates RUNX2 activation and cellular wound healing through the aldose reductase polyol pathway. J Biol Chem. 2009; 284 (27): 17947-55.
25. Pierce AD, Anglin IE, Vitolo MI, Mochin MT, Underwood KF, Goldblum SE, Kommineni S, Passaniti A,. Glucose-activated RUNX2 phosphorylation promotes endothelial cell proliferation and an angiogenic phenotype. J Cell Biochem. 2011; [Epub ahead of print].
26. Renard P, Ernest I, Houbion A, Art M, Le Calvez H, Raes M, Remacle J,. Development of a sensitive multi-well colorimetric assay for active NFkappaB. Nucleic Acids Res. 2001; 29 (4): E21.
27. Laflamme C, Curt S, Rouabhia M,. Epidermal growth factor and bone morphogenetic proteins upregulate osteoblast proliferation and osteoblastic markers and inhibit bone nodule formation. Arch Oral Biol. 2010; 55 (9): 689-701.
28. Hicks S, Assefa H, Sindelar R,. Computer-aided design of enzyme inhibitors: recent studies. Curr Opin Drug Disc Dev. 1998; 1: 223-34.
29. Connolly ML,. Solvent-accessible surfaces of proteins and nucleic acids. Science. 1983; 221 (4612): 709-13.
30. Nicklaus MC, Neamati N, Hong H, Mazumder A, Sunder S, Chen J, Milne GW, Pommier Y,. HIV-1 integrase pharmacophore: discovery of inhibitors through three-dimensional database searching. J Med Chem. 1997; 40 (6): 920-9. (Pubitemid 27131621)
31. Read JT, Cheng H, Hendy SC, Nelson CC, Rennie PS,. Receptor-DNA interactions: EMSA and footprinting. Methods Mol Biol. 2009; 505: 97-122.
32. Kundu M, Javed A, Jeon JP, Horner A, Shum L, Eckhaus M, Muenke M, Lian JB, Yang Y, Nuckolls GH, Stein GS, Liu PP,. Cbfbeta interacts with Runx2 and has a critical role in bone development. Nat Genet. 2002; 32 (4): 639-44. (Pubitemid 35435177)
33. Warren AJ, Bravo J, Williams RL, Rabbitts TH,. Structural basis for the heterodimeric interaction between the acute leukaemia-associated transcription factors AML1 and CBFbeta. EMBO J. 2000; 19 (12): 3004-15. (Pubitemid 30386771)
34. Akamatsu Y, Ohno T, Hirota K, Kagoshima H, Yodoi J, Shigesada K,. Redox regulation of the DNA binding activity in transcription factor PEBP2. The roles of two conserved cysteine residues. J Biol Chem. 1997; 272 (23): 14497-500. (Pubitemid 27251706)
35. Bravo J, Li Z, Speck NA, Warren AJ,. The leukemia-associated AML1 (Runx1)-CBFbeta complex functions as a DNA-induced molecular clamp. Nat Struct Biol. 2001; 8 (4): 371-8. (Pubitemid 32275025)
36. Ferrin TE, Huang CC, Jarvis LE, Langridge R,. The MIDAS display system. J Mol Graphics. 1988; 6: 13-27.
37. Tahirov TH, Inoue-Bungo T, Morii H, Fujikawa A, Sasaki M, Kimura K, Shiina M, Sato K, Kumasaka T, Yamamoto M, Ishii S, Ogata K,. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. Cell. 2001; 104 (5): 755-67. (Pubitemid 32241025)
38. Tang YY, Shi J, Zhang L, Davis A, Bravo J, Warren AJ, Speck NA, Bushweller JH,. Energetic and functional contribution of residues in the core binding factor beta (CBFbeta) subunit to heterodimerization with CBFalpha. J Biol Chem. 2000; 275 (50): 39579-88. (Pubitemid 32058984)
39. Chi Y, Hong Y, Zong H, Wang Y, Zou W, Yang J, Kong X, Yun X, Gu J,. CDK11p58 represses vitamin D receptor-mediated transcriptional activation through promoting its ubiquitin-proteasome degradation. Biochem Biophys Res Commun. 2009; 386 (3): 493-8.
40. Barsony J, McKoy W,. Molybdate increases intracellular 3′,5′-guanosine cyclic monophosphate and stabilizes vitamin D receptor association with tubulin-containing filaments. J Biol Chem. 1992; 267 (34): 24457-65.
41. Hellman LM, Fried MG,. Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat Protoc. 2007; 2 (8): 1849-61. (Pubitemid 47308124)
42. Bhattacharya N, Sarno A, Idler IS, Fuhrer M, Zenz T, Dohner H, Stilgenbauer S, Mertens D,. High-throughput detection of nuclear factor-kappaB activity using a sensitive oligo-based chemiluminescent enzyme-linked immunosorbent assay. Int J Cancer. 2010; 127 (2): 404-11.
43. Hartzell DD, Trinklein ND, Mendez J, Murphy N, Aldred SF, Wood K, Urh M,. A functional analysis of the CREB signaling pathway using HaloCHIP-chip and high throughput reporter assays. BMC Genomics. 2009; 10: 497.
44. Vuori KA, Ahlskog JK, Sistonen L, Nikinmaa M,. TransLISA, a novel quantitative, nonradioactive assay for transcription factor DNA-binding analyses. FEBS J. 2009; 276 (24): 7366-74.
45. Hancock CN, Macias A, Lee EK, Yu SY, Mackerell AD Jr, Shapiro P,. Identification of novel extracellular signal-regulated kinase docking domain inhibitors. J Med Chem. 2005; 48 (14): 4586-95. (Pubitemid 40993419)
46. Costa JL, Eijk PP, van de Wiel MA, ten Berge D, Schmitt F, Narvaez CJ, Welsh J, Ylstra B,. Anti-proliferative action of vitamin D in MCF7 is still active after siRNA-VDR knock-down. BMC Genomics. 2009; 10: 499.
47. Stein GS, Lian JB, van Wijnen AJ, Stein JL, Javed A, Montecino M, Zaidi SK, Young D, Choi JY, Gutierrez S, Pockwinse S,. Nuclear microenvironments support assembly and organization of the transcriptional regulatory machinery for cell proliferation and differentiation. J Cell Biochem. 2004; 91 (2): 287-302.
48. Tokar EJ, Webber MM,. Cholecalciferol (vitamin D3) inhibits growth and invasion by up-regulating nuclear receptors and 25-hydroxylase (CYP27A1) in human prostate cancer cells. Clin Exp Metastasis. 2005; 22 (3): 275-84. (Pubitemid 41298009)
49. Lou YR, Laaksi I, Syvala H, Blauer M, Tammela TL, Ylikomi T, Tuohimaa P,. 25-Hydroxyvitamin D3 is an active hormone in human primary prostatic stromal cells. FASEB J. 2004; 18 (2): 332-4.
50. Kemmis CM, Salvador SM, Smith KM, Welsh J,. Human mammary epithelial cells express CYP27B1 and are growth inhibited by 25-hydroxyvitamin D-3, the major circulating form of vitamin D-3. J Nutr. 2006; 136 (4): 887-92.
51. Baran DT, Sorensen AM, Shalhoub V, Owen T, Stein G, Lian J,. The rapid nongenomic actions of 1 alpha,25-dihydroxyvitamin D3 modulate the hormone-induced increments in osteocalcin gene transcription in osteoblast-like cells. J Cell Biochem. 1992; 50 (2): 124-9.
52. Pommier Y, Cherfils J,. Interfacial inhibition of macromolecular interactions: nature's paradigm for drug discovery. Trends Pharmacol Sci. 2005; 26 (3): 138-45. (Pubitemid 40313593)
53. Pommier Y,. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem Rev. 2009; 109 (7): 2894-902.
54. Namba K, Abe M, Saito S, Satake M, Ohmoto T, Watanabe T, Sato Y,. Indispensable role of the transcription factor PEBP2/CBF in angiogenic activity of a murine endothelial cell MSS31. Oncogene. 2000; 19 (1): 106-14. (Pubitemid 30066356)
55. Barnes GL, Hebert KE, Kamal M, Javed A, Einhorn TA, Lian JB, Stein GS, Gerstenfeld LC,. Fidelity of Runx2 activity in breast cancer cells is required for the generation of metastases-associated osteolytic disease. Cancer Res. 2004; 64 (13): 4506-13. (Pubitemid 38856922)
56. Humphrey W, Dalke A, Schulten K,. VMD: visual molecular dynamics. J Mol Graph. 1996; 14 (1): 33-8. (Pubitemid 26152973)