Tumor suppressor microRNAs, miR-100 and -125b, are regulated by 1,25-dihydroxyvitamin D in primary prostate cells and in patient tissue

Cancer Prevention Research

Volumn 6, Issue 5, 2013, Pages 483-494

  Giangreco, Angeline A ^a   Vaishnav, Avani ^a   Wagner, Dennis ^b   Finelli, Antonio ^c   Fleshner, Neil ^c   Van Der Kwast, Theodorus ^c   Vieth, Reinhold ^b   Nonn, Larisa ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; MICRORNA 100; MICRORNA 125B; POLO LIKE KINASE 1; TRANSCRIPTION FACTOR E2F3;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER TISSUE; CELL ASSAY; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; PRIORITY JOURNAL; PROSTATE CANCER; RECEPTOR UPREGULATION;

ADENOCARCINOMA; ADULT; AGED; APOPTOSIS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL CYCLE PROTEINS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CLINICAL TRIALS, PHASE II AS TOPIC; E2F3 TRANSCRIPTION FACTOR; FOLLOW-UP STUDIES; GENE EXPRESSION PROFILING; HUMANS; LASER CAPTURE MICRODISSECTION; MALE; MICRORNAS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROGNOSIS; PROSTATE; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CALCITRIOL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR MARKERS, BIOLOGICAL; VITAMIN D;

EID: 84877258964     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-12-0253     Document Type: Article

References (55)

1. Thacher TD, Clarke BL. Vitamin D insufficiency. Mayo Clin Proc 2011; 86:50-60.
2. Ginde AA, Liu MC, Camargo CA Jr. Demographic differences and trends of vitamin D insufficiency in the US population, 1988-2004. Arch Intern Med 2009; 169:626-32.
3. Schwartz GG. Vitamin D and the epidemiology of prostate cancer. Semin Dial 2005; 18:276-89. (Pubitemid 41159577)
4. Crawford ED. Understanding the epidemiology, natural history, and key pathways involved in prostate cancer. Urology 2009; 73:S4-10.
5. Marshall DT, Savage SJ, Garrett-Mayer E, Keane TE, Hollis BW, Horst RL, et al. Vitamin D3 supplementation at 4000 international units per day for one year results in a decrease of positive cores at repeat biopsy in subjects with low-risk prostate cancer under active surveillance. J Clin Endocrinol Metab 2012; 97:2315-24.
6. Getzenberg RH, Light BW, Lapco PE, Konety BR, Nangia AK, Acierno JS, et al. Vitamin D inhibition of prostate adenocarcinoma growth and metastasis in the Dunning rat prostate model system. Urology 1997; 50:999-1006. (Pubitemid 28021128)
7. Simboli-Campbell M, Narvaez CJ, Tenniswood M, Welsh J. 1,25Dihydroxyvitamin D3 induces morphological and biochemical markers of apoptosis in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol 1996; 58:367-76. (Pubitemid 26348970)
8. Moreno J, Krishnan AV, Feldman D. Molecular mechanisms mediating the anti-proliferative effects of vitamin D in prostate cancer. J Steroid Biochem Mol Biol 2005; 97:31-6. (Pubitemid 41546211)
9. Guyton KZ, Kensler TW, Posner GH. Vitamin D and vitamin D analogs as cancer chemopreventive agents. Nutr Rev 2003; 61: 227-38. (Pubitemid 37259932)
10. Zanatta L, Zamoner A, Zanatta AP, Bouraima-Lelong H, Delalande C, Bois C, et al. Nongenomic and genomic effects of 1alpha,25(OH)(2) vitamin D(3) in rat testis. Life Sci 2011; 89:515-23.
11. Hendrickson WK, Flavin R, Kasperzyk JL, Fiorentino M, Fang F, Lis R, et al. Vitamin D receptor protein expression in tumor tissue and prostate cancer progression. J Clin Oncol 2011; 29:2378-85.
12. Shui IM, Mucci LA, Kraft P, Tamimi RM, Lindstrom S, Penney KL, et al. Vitamin D-related genetic variation, plasma vitamin D, and risk of lethal prostate cancer: a prospective nested case-control study. J Natl Cancer Inst 2012; 104:690-9.
13. Garland CF, Garland FC. Do sunlight and vitamin D reduce the likelihood of colon cancer? Int J Epidemiol 2006; 35:217-20.
14. Beer TM, Javle MM, Ryan CW, Garzotto M, Lam GN, Wong A, et al. Phase I study of weekly DN-101, a new formulation of calcitriol, in patients with cancer. Cancer Chemother Pharmacol 2007; 59:581-7. (Pubitemid 46295122)
15. Gandini S, Boniol M, Haukka J, Byrnes G, Cox B, Sneyd MJ, et al. Metaanalysis of observational studies of serum 25-hydroxyvitamin D levels and colorectal, breast and prostate cancer and colorectal adenoma. Int J Cancer 2011; 128:1414-24.
16. Li H, Stampfer MJ, Hollis JB, Mucci LA, Gaziano JM, Hunter D, et al. A prospective study of plasma vitamin D metabolites, vitamin D receptor polymorphisms, and prostate cancer. PLoS Med 2007; 4:e103.
17. Ahonen MH, Tenkanen L, Teppo L, Hakama M, Tuohimaa P. Prostate cancer risk and prediagnostic serum 25-hydroxyvitamin D levels (Finland). Cancer Causes Control 2000; 11:847-52.
18. Krill D, De Flavia P, Dhir R, Luo J, Becich MJ, Lehman E, et al. Expression patterns of vitamin D receptor in human prostate. J Cell Biochem 2001; 82:566-72. (Pubitemid 32720672)
19. Barreto AM, Schwartz GG, Woodruff R, Cramer SD. 25-Hydroxyvitamin D3, the prohormone of 1,25-dihydroxyvitamin D3, inhibits the proliferation of primary prostatic epithelial cells. Cancer Epidemiol Biomarkers Prev 2000; 9:265-70. (Pubitemid 30165438)
20. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75:843-54. (Pubitemid 24014542)
21. Mirnezami AH, Pickard K, Zhang L, Primrose JN, Packham G. Micro RNAs: key players in carcinogenesis and novel therapeutic targets. Eur J Surg Oncol 2009; 35:339-47.
22. Ozen M, Creighton CJ, Ozdemir M, Ittmann M. Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 2008; 27:1788-93. (Pubitemid 351380263)
23. Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, Visakorpi T. Micro RNA expression profiling in prostate cancer. Cancer Res 2007; 67:6130-5. (Pubitemid 47037493)
24. Schaefer A, Jung M, Mollenkopf HJ, Wagner I, Stephan C, Jentzmik F, et al. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer 2010; 126:1166-76.
25. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006; 103:2257-61. (Pubitemid 43271657)
26. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. Micro RNA expression profiles classify human cancers. Nature 2005; 435:834-8. (Pubitemid 40839735)
27. Wang WL, Chatterjee N, Chittur SV, Welsh J, Tenniswood MP. Effects of 1alpha,25 dihydroxyvitamin D3 and testosterone on miRNA and mRNA expression in LNCaP cells. Mol Cancer 2011; 10:58.
28. Nonn L, Peng L, Feldman D, Peehl DM. Inhibition of p38 by vitamin D reduces interleukin-6 production in normal prostate cells via mitogenactivated protein kinase phosphatase 5: implications for prostate cancer prevention by vitamin D. Cancer Res 2006; 66:4516-24.
29. Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 1997; 18:1215-23. (Pubitemid 28132513)
30. Nonn L, Vaishnav A, Gallagher L, Gann PH. mRNA and micro-RNA expression analysis in laser-capture microdissected prostate biopsies: valuable tool for risk assessment and prevention trials. Exp Mol Pathol 2010; 88:45-51.
31. Wagner D, Dias AG, Schnabl K, Van der Kwast T, Vieth R. Determination of 1,25-dihydroxyvitamin D concentrations in human colon tissues and matched serumsamples. Anticancer Res 2012; 32:259-63.
32. Wagner D, Trudel D, Van der Kwast T, Nonn L, Giangreco A, Li D, et al. Randomized clinical trial of vitamin D3 doses on prostatic vitamin D metabolite levels and Ki67 labeling in prostate cancer patients. J Clin Endocrinol Metab. 2013 Mar 5. [Epub ahead of print].
33. Hwang HW, Wentzel EA, Mendell JT. Cell-cell contact globally activates microRNA biogenesis. Proc Natl Acad Sci U S A 2009; 106: 7016-21.
34. Sun D, Lee YS, Malhotra A, Kim HK, Matecic M, Evans C, et al. miR-99 family of Micro RNAs suppresses the expression of prostate-specific antigen and prostate cancer cell proliferation. Cancer Res 2011; 71: 1313-24.
35. Zhang Y, Yan LX, Wu QN, Du ZM, Chen J, Liao DZ, et al. miR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res 2011; 71:3552-62.
36. Henson BJ, Bhattacharjee S, O'Dee DM, Feingold E, Gollin SM. Decreased expression of miR-125b and miR-100 in oral cancer cells contributes to malignancy. Genes Chromosomes Cancer 2009; 48: 569-82.
37. Feng B, Wang R, Chen LB. MiR-100 resensitizes docetaxel-resistant human lung adenocarcinoma cells (SPC-A1) to docetaxel by targeting Plk1. Cancer Lett 2011; 317:184-91.
38. Huang L, Luo J, Cai Q, Pan Q, Zeng H, Guo Z, et al. MicroRNA-125b suppresses the development of bladder cancer by targeting E2F3. Int J Cancer 2011; 128:1758-69.
39. Zhang J, Chalmers MJ, Stayrook KR, Burris LL, Wang Y, Busby SA, et al. DNA binding alters coactivator interaction surfaces of the intact VDR-RXR complex. Nat Struct Mol Biol 2011; 18:556-63.
40. Freedman VH, Shin SI. Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 1974; 3:355-9.
41. Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, et al. Ancient animal microRNAs and the evolution of tissue identity. Nature 2010; 463:1084-8.
42. Gocek E, Wang X, Liu X, Liu CG, Studzinski GP. Micro RNA-32 upregulation by 1,25-dihydroxyvitamin D3 in human myeloid leukemia cells leads to Bim targeting and inhibition of AraC-induced apoptosis. Cancer Res 2011; 71:6230-9.
43. Wang X, Gocek E, Liu CG, Studzinski GP. Micro RNAs181 regulate the expression of p27Kip1 in human myeloid leukemia cells induced to differentiate by 1,25-dihydroxyvitamin D3. Cell Cycle 2009; 8: 736-41.
44. Peng X, Vaishnav A, Murillo G, Alimirah F, Torres KE, Mehta RG. Protection against cellular stress by 25-hydroxyvitamin D3 in breast epithelial cells. J Cell Biochem 2010; 110:1324-33.
45. Alvarez-Diaz S, Valle N, Ferrer-Mayorga G, Lombardia L, Herrera M, Domiguez O, et al. Micro RNA-22 is induced by vitamin D and contributes to its antiproliferative, antimigratory and gene regulatory effects in colon cancer cells. Hum Mol Genet 2012; 21:2157-65.
46. Zheng YS, Zhang H, Zhang XJ, Feng DD, Luo XQ, Zeng CW, et al. MiR100 regulates cell differentiation and survival by targeting RBSP3, a phosphatase-like tumor suppressor in acute myeloid leukemia. Oncogene 2011; 31:80-92.
47. Petrelli A, Perra A, Schernhuber K, Cargnelutti M, Salvi A, Migliore C, et al. Sequential analysis of multistage hepatocarcinogenesis reveals that miR-100 and PLK1 dysregulation is an early event maintained along tumor progression. Oncogene 2012; 31:4517-26.
48. Alpini G, Glaser SS, Zhang JP, Francis H, Han Y, Gong J, et al. Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J Hepatol 2011; 55:1339-45.
49. Shi XB, Xue L, Ma AH, Tepper CG, Kung HJ, White RW. miR125b promotes growth of prostate cancer xenograft tumor through targeting pro-apoptotic genes. Prostate 2011; 71: 538-49.
50. Leite KR, Sousa-Canavez JM, Reis ST, Tomiyama AH, Camara-Lopes LH, Sanudo A, et al. Change in expression of miR-let7c, miR-100, and miR-218 from high grade localized prostate cancer to metastasis. Urol Oncol 2011; 29:265-9.
51. Foster CS, Falconer A, Dodson AR, Norman AR, Dennis N, Fletcher A, et al. Transcription factor E2F3 overexpressed in prostate cancer independently predicts clinical outcome. Oncogene 2004; 23:5871-9. (Pubitemid 39093531)
52. Weichert W, Schmidt M, Gekeler V, Denkert C, Stephan C, Jung K, et al. Polo-like kinase 1 is overexpressed in prostate cancer and linked to higher tumor grades. Prostate 2004; 60:240-5. (Pubitemid 38971835)
53. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003; 22:5323-35. (Pubitemid 37279943)
54. Nair VS, Maeda LS, Ioannidis JP. Clinical outcome prediction by microRNAs in human cancer: a systematic review. J Natl Cancer Inst 2004; 104:528-40.
55. Dong Q, Meng P, Wang T, Qin W, Wang F, Yuan J, et al. Micro RNA let7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2. PLoS ONE 2010; 5:e10147.