1,25-Dihydroxyvitamin D3 suppresses telomerase expression and human cancer growth through microRNA-498

Journal of Biological Chemistry

Volumn 287, Issue 49, 2012, Pages 41297-41309

  Kasiappan, Ravi ^a   Shen, Zheng ^a   Tse, Anfernee K W ^a   Jinwal, Umesh ^a   Tang, Jinfu ^a   Lungchukiet, Panida ^a   Sun, Yuefeng ^a   Kruk, Patricia ^a   Nicosia, Santo V ^a,b   Zhang, Xiaohong ^a,b   Bai, Wenlong ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ,25-DIHYDROXYVITAMIN D3; ANTI-TUMOR ACTIVITIES; CANCER CELLS; CATALYTIC SUBUNITS; CELL DIVISIONS; CELL LINES; COACTIVATORS; DNA REPLICATIONS; DOMINANT MECHANISM; EMBRYONIC STEMS; HUMAN CANCER; HUMAN TELOMERASE; MICROARRAY ANALYSIS; MICRORNAS; MOUSE TUMORS; MRNA EXPRESSION; NEW MECHANISMS; NON-CODING RNAS; OVARIAN CANCER CELLS; OVARIAN CANCERS; OVARIAN TUMOR; PROLIFERATING CELLS; PROMOTER ACTIVITIES; QUANTITATIVE POLYMERASE CHAIN REACTION; REGULATORY REGIONS; RESPONSE ELEMENTS; SMALL RNA; TELOMERASE; TELOMERASE ACTIVITY; TELOMERASE EXPRESSION; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERES; UNTRANSLATED REGIONS; VITAMIN D RECEPTOR; VITAMIN-D;

CELL CULTURE; CELL PROLIFERATION; CELLS; GENE ENCODING; POLYMERASE CHAIN REACTION; VITAMINS;

RNA;

CALCITRIOL; MICRORNA; MICRORNA 498; SEOCALCITOL; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN TISSUE; MICRORNA 498 GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA GENE; TELOMERASE REVERSE TRANSCRIPTASE GENE; VITAMIN D RESPONSIVE ELEMENT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CALCITRIOL; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME; HUMANS; MICE; MICE, NUDE; MICRORNAS; MUTAGENESIS; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, UNTRANSLATED; TELOMERASE;

EID: 84870328638     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.407189     Document Type: Article

References (57)

1. Blackburn, E. H. (2001) Switching and signaling at the telomere. Cell 106, 661-673
2. Harrington, L., McPhail, T., Mar, V., Zhou, W., Oulton, R., Bass, M. B., Arruda, I., and Robinson, M. O. (1997) A mammalian telomerase-associated protein. Science 275, 973-977 (Pubitemid 27087712)
3. Blasco, M. A., Funk, W., Villeponteau, B., and Greider, C. W. (1995) Functional characterization and developmental regulation of mouse telomerase RNA. Science 269, 1267-1270
4. Cohen, S. B., Graham, M. E., Lovrecz, G. O., Bache, N., Robinson, P. J., and Reddel, R. R. (2007) Protein composition of catalytically active human telomerase from immortal cells. Science 315, 1850-1853 (Pubitemid 46580145)
5. Venteicher, A. S., Abreu, E. B., Meng, Z., McCann, K. E., Terns, R. M., Veenstra, T. D., Terns, M. P., and Artandi, S. E. (2009) A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 323, 644-648
6. Wang, S., and Zhu, J. (2003) Evidence for a relief of repression mechanism for activation of the human telomerase reverse transcriptase promoter. J. Biol. Chem. 278, 18842-18850 (Pubitemid 36799266)
7. Smith, L. L., Coller, H. A., and Roberts, J. M. (2003) Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat. Cell Biol. 5, 474-479 (Pubitemid 36592272)
8. Liu, K., Hodes, R. J., and Weng, N. (2001) Cutting edge. Telomerase activation in human T lymphocytes does not require increase in telomerase reverse transcriptase (hTERT) protein but is associated with hTERT phosphorylation and nuclear translocation. J. Immunol. 166, 4826-4830 (Pubitemid 32280689)
9. Bartel, D. P. (2009) MicroRNAs. Target recognition and regulatory functions. Cell 136, 215-233
10. Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060 (Pubitemid 39472426)
11. Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L., and Bradley, A. (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902-1910 (Pubitemid 39386503)
12. Maniataki, E., and Mourelatos, Z. (2005) A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev. 19, 2979-2990 (Pubitemid 41798114)
13. He, L., and Hannon, G. J. (2004) MicroRNAs. Small RNAs with a big role in gene regulation. Nat. Rev. Genet 5, 522-531 (Pubitemid 38868508)
14. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (Pubitemid 40094598)
15. Kumar, M. S., Lu, J., Mercer, K. L., Golub, T. R., and Jacks, T. (2007) Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673-677 (Pubitemid 46676103)
16. Valastyan, S., Reinhardt, F., Benaich, N., Calogrias, D., Szász, A. M., Wang, Z. C., Brock, J. E., Richardson, A. L., and Weinberg, R. A. (2009) A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032-1046
17. Dusso, A. S., Brown, A. J., and Slatopolsky, E. (2005) Vitamin D. (2012) Am. J. Physiol. Renal Physiol. 289, F8-F28
18. Nagpal, S., Na, S., and Rathnachalam, R. (2005) Noncalcemic actions of vitamin D receptor ligands. Endocr. Rev. 26, 662-687 (Pubitemid 41127276)
19. Holick, M. F. (2007) Vitamin D deficiency. N. Engl. J. Med. 357, 266-281
20. Garland, C. F., Garland, F. C., Gorham, E. D., Lipkin, M., Newmark, H., Mohr, S. B., and Holick, M. F. (2006) The role of vitamin D in cancer prevention. Am. J. Public Health 96, 252-261 (Pubitemid 43167123)
21. Evans, R. M. (1988) The steroid and thyroid hormone receptor superfamily. Science 240, 889-895
22. Tsai, M. J., and O'Malley, B. W. (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63, 451-486
23. Zou, A., Elgort, M. G., and Allegretto, E. A. (1997) Retinoid X receptor (RXR) ligands activate the human 25-hydroxyvitamin D3-24-hydroxylase promoter via RXR heterodimer binding to two vitamin D-responsive elements and elicit additive effects with 1,25-dihydroxyvitamin D3. J. Biol. Chem. 272, 19027-19034 (Pubitemid 27318259)
24. 2/M arrest by 1,25-dihydroxyvitamin D3 in ovarian cancer cells mediated through the induction of GADD45 via an exonic enhancer. J. Biol. Chem. 278, 48030-48040
25. Li, P., Li, C., Zhao, X., Zhang, X., Nicosia, S. V., and Bai, W. (2004) p27(Kip1) stabilization and G(1) arrest by 1,25-dihydroxyvitamin D(3) in ovarian cancer cells mediated through down-regulation of cyclin E/cyclin-dependent kinase 2 and Skp1-Cullin-F-box protein/Skp2 ubiquitin ligase. J. Biol. Chem. 279, 25260-25267 (Pubitemid 38756778)
26. Jiang, F., Bao, J., Li, P., Nicosia, S. V., and Bai, W. (2004) Induction of ovarian cancer cell apoptosis by 1,25-dihydroxyvitamin D3 through the down-regulation of telomerase. J. Biol. Chem. 279, 53213-53221 (Pubitemid 40051824)
27. Chen, C., Ridzon, D. A., Broomer, A. J., Zhou, Z., Lee, D. H., Nguyen, J. T., Barbisin, M., Xu, N. L., Mahuvakar, V. R., Andersen, M. R., Lao, K. Q., Livak, K. J., and Guegler, K. J. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179
28. Baker, A. R., McDonnell, D. P., Hughes, M., Crisp, T. M., Mangelsdorf, D. J., Haussler, M. R., Pike, J. W., Shine, J., and O'Malley, B. W. (1988) Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc. Natl. Acad. Sci. U.S.A. 85, 3294-3298
29. Ebert, M. S., Neilson, J. R., and Sharp, P. A. (2007) MicroRNA sponges. Competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721-726 (Pubitemid 47338166)
30. Valastyan, S., and Weinberg, R. A. (2009) Assaying microRNA loss-of-function phenotypes in mammalian cells. Emerging tools and their potential therapeutic utility. RNA Biol. 6, 541-545
31. Li, P., Lee, H., Guo, S., Unterman, T. G., Jenster, G., and Bai, W. (2003) AKT-independent protection of prostate cancer cells from apoptosis mediated through complex formation between the androgen receptor and FKHR. Mol. Cell. Biol. 23, 104-118 (Pubitemid 36008505)
32. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival. Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
33. Zhang, X., Jiang, F., Li, P., Li, C., Ma, Q., Nicosia, S. V., and Bai, W. (2005) Growth suppression of ovarian cancer xenografts in nude mice by vitamin D analogue EB1089. Clin. Cancer Res. 11, 323-328 (Pubitemid 40075811)
34. Toell, A., Polly, P., and Carlberg, C. (2000) All natural DR3-type vitamin D response elements show a similar functionality in vitro. Biochem. J. 352, 301-309 (Pubitemid 32011424)
35. Noda, M., Vogel, R. L., Craig, A. M., Prahl, J., DeLuca, H. F., and Denhardt, D. T. (1990) Identification of a DNA sequence responsible for binding of the 1,25-dihydroxyvitamin D3 receptor and 1,25-dihydroxyvitamin D3 enhancement of mouse secreted phosphoprotein 1 (SPP-1 or osteopontin) gene expression. Proc. Natl. Acad. Sci. U.S.A. 87, 9995-9999 (Pubitemid 120016571)
36. Morrison, N. A., Shine, J., Fragonas, J. C., Verkest, V., McMenemy, M. L., and Eisman, J. A. (1989) 1,25-Dihydroxyvitamin D-responsive element and glucocorticoid repression in the osteocalcin gene. Science 246, 1158-1161 (Pubitemid 20012774)
37. Vella, M. C., Choi, E. Y., Lin, S. Y., Reinert, K., and Slack, F. J. (2004) The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3′-UTR. Genes Dev. 18, 132-137 (Pubitemid 38141781)
38. Wu, L., and Belasco, J. G. (2008) Let me count the ways. Mechanisms of gene regulation by miRNAs and siRNAs. Mol. Cell 29, 1-7
39. Nilsen, T. W. (2007) Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet. 23, 243-249
40. Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840
41. Carthew, R. W., and Sontheimer, E. J. (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136, 642-655
42. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., and Thun, M. J. (2009) Cancer statistics, 2009. CA Cancer J. Clin. 59, 225-249
43. Zhang, X., Nicosia, S. V., and Bai, W. (2006) Vitamin D receptor is a novel drug target for ovarian cancer treatment. Curr. Cancer Drug Targets 6, 229-244 (Pubitemid 43764742)
44. 1-S checkpoint in ovarian cancer cells. Mol. Cell. Endocrinol. 338, 58-67
45. Yamamoto, H., Shevde, N. K., Warrier, A., Plum, L. A., DeLuca, H. F., and Pike, J. W. (2003) 2-Methylene-19-nor-(20S)-1,25-dihydroxyvitamin D3 potently stimulates gene-specific DNA binding of the vitamin D receptor in osteoblasts. J. Biol. Chem. 278, 31756-31765 (Pubitemid 37048356)
46. Ventura, A., and Jacks, T. (2009) MicroRNAs and cancer. Short RNAs go a long way. Cell 136, 586-591
47. Hammond, S. M. (2007) MicroRNAs as tumor suppressors. Nat. Genet. 39, 582-583
48. Deng, S., Calin, G. A., Croce, C. M., Coukos, G., and Zhang, L. (2008) Mechanisms of microRNA deregulation in human cancer. Cell Cycle 7, 2643-2646
49. Schepeler, T., Reinert, J. T., Ostenfeld, M. S., Christensen, L. L., Silahtaroglu, A. N., Dyrskjøt, L., Wiuf, C., Sørensen, F. J., Kruhøffer, M., Laurberg, S., Kauppinen, S., Ørntoft, T. F., and Andersen, C. L. (2008) Diagnostic and prognostic microRNAs in stage II colon cancer. Cancer Res. 68, 6416-6424
50. Porkka, K. P., Pfeiffer, M. J., Waltering, K. K., Vessella, R. L., Tammela, T. L., and Visakorpi, T. (2007) MicroRNA expression profiling in prostate cancer. Cancer Res. 67, 6130-6135 (Pubitemid 47037493)
51. Bicher, A., Ault, K., Kimmelman, A., Gershenson, D., Reed, E., and Liang, B. (1997) Loss of heterozygosity in human ovarian cancer on chromosome 19q. Gynecol. Oncol. 66, 36-40 (Pubitemid 27329305)
52. Amfo, K., Neyns, B., Teugels, E., Lissens, W., Bourgain, C., De Sutter, P., Vandamme, B., Vamos, E., and De Grève, J. (1995) Frequent deletion of chromosome 19 and a rare rearrangement of 19p13.3 involving the insulin receptor gene in human ovarian cancer. Oncogene 11, 351-358
53. Bièche, I., Noguès, C., Paradis, V., Olivi, M., Bedossa, P., Lidereau, R., and Vidaud, M. (2000) Quantitation of hTERT gene expression in sporadic breast tumors with a real-time reverse transcription-polymerase chain reaction assay. Clin. Cancer Res. 6, 452-459 (Pubitemid 30111463)
54. Sun, P. M., Wei, L. H., Luo, M. Y., Liu, G., Wang, J. L., Mustea, A., Könsgen, D., Lichtenegger, W., and Sehouli, J. (2007) The telomerase activity and expression of hTERT gene can serve as indicators in the anti-cancer treatment of human ovarian cancer. Eur. J. Obstet. Gynecol. Reprod. Biol. 130, 249-257 (Pubitemid 46099062)
55. Cancer Genome Atlas Research Network (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615
56. Xie, C. Q., Jeong, Y., Fu, M., Bookout, A. L., Garcia-Barrio, M. T., Sun, T., Kim, B. H., Xie, Y., Root, S., Zhang, J., Xu, R. H., Chen, Y. E., and Mangelsdorf, D. J. (2009) Expression profiling of nuclear receptors in human and mouse embryonic stem cells. Mol. Endocrinol. 23, 724-733
57. Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., Barzilai, A., Einat, P., Einav, U., Meiri, E., Sharon, E., Spector, Y., and Bentwich, Z. (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37, 766-770 (Pubitemid 41754896)