Attenuation of constitutive DNA damage signaling by 1,25- dihydroxyvitamin D3

Aging

Volumn 4, Issue 4, 2012, Pages 270-278

  Dorota Halicka, H ^a   Zhao, Hong ^a   Li, Jiangwei ^a   Traganos, Frank ^a   Studzinski, George P ^b   Darzynkiewicz, Zbigniew ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Aging; Apoptosis; ATM activation; Calcitriol; Cancer prevention; Cell cycle; DNA repair; Histone H2AX phosphorylation; mTOR; Oxidative DNA damage; Replication stress

Indexed keywords

EID: 84863228908     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100450     Document Type: Article

References (70)

1. Garland CF, Garland FC, Gorham ED, Lipkin M, Newmark H, Mohr SB, Holick MF. The role of vitamin D in cancer prevention. Am J Publ Health 2006; 96:252-261.
2. Gocek E, Studzinski GP. Vitamin D and differentiation in cancer. Crit Rev Clin Lab Sci 2009;46:190-209.
3. Krishnan AV, Trump DL, Johnson CS, Feldman D. The role of vitamin D in cancer prevention and treatment. Endocrinol Metab Clin N Am 2010; 39:401-418.
4. Fleet JC, Desmet M, Johnson R, Li Y. Vitamin D and cancer: a review of molecular mechanisms. Biochem J 2012; 221:61-76.
5. Zinser GM, Suckow M, Welsh J. Vitamin D receptor (VDR) ablation alters carcinogen-induced tumorigenesis in mammary gland, epidermis and lymphoid tissues. J Steroid Biochem Mol Biol. 2005;97:153-164.
6. Trump DL, Deeb KK, Johnson CS. Vitamin D: considerations in the continued development as an agent for cancer prevention and therapy. Cancer J 2010;16:1-9.
7. Giardina C, Madigan JP, Godman Tierney CA, Brenner BM, Rosenberg DW. Vitamin D resistance and colon cancer prevention. Carcinogenesis 2012; Jan 5 (Epub).
8. Weisman Y. Non-classic unexpected functions of vitamin D. Pediatr Endocrin Rev 2010;8:103-107.
9. Studzinski GP, Wang X, Ji Y, Wang Q, Zhang Y, Kutner A, Harrison JS. The rationale for deltanoids in therapy for myeloid leukemia: role of KSR-MAPK-C/EBP pathway. J Steroid Biochem Mol Biol 2005;97:47-55.
10. Ting HJ, Yasmin-Karim S, Yan S-J, Hsu JW, Lin T-H, Zeng W, Messing J, Sheu T-J, Bao B-Y, Li W, Messing E, Lee Y-F. A positive feedback signaling loop between ATM and the vitamin D receptor is critical for cancer chemoprevention by vitamin D. Cancer Res. 2012;72:958-968.
11. De Haes P, Garmyn M, Verstuyf A, De Clercq P, Vandewalle M, Degreef H, et al. 1,25-Dihydroxyvitamin D3 and analogues protect primary human keratinocytes against UVB-induced DNA damage. J Photochem Photobiol B. 2005;78:141-148.
12. Wong G, Gupta R, Dixon KM, Deo SS, Choong SM, Halliday GM, et al. 1,25-Dihydroxyvitamin D and three low-calcemic analogs decrease UV-induced DNA damage via the rapid response pathway. J Steroid Biochem Mol Biol. 2004;89-90:567-570.
13. Chatterjee M. Vitamin D and genomic stability. Mutat Res 2001;475:69-87.
14. Hanada K, Sawamura D, Nakano H, Hashimoto I. Possible role of 1,25-dihydroxyvitamin D3-induced metallothionein in photoprotection against UVB injury in mouse skin and cultured rat keratinocytes. J Dermatol Sci. 1995;9:203-208.
15. De Haes P, Garmyn M, Degreef H, Vantieghem K, Bouillon R, Segaert S. 1,25-Dihydroxyvitamin D3 inhibits ultraviolet Binduced apoptosis, Jun kinase activation, and interleukin-6 production in primary human keratinocytes. J Cell Biochem 2003;89:663-673.
16. Banakar MC, Paramasivan SK, Chattopadhyay MB, Datta S, Chakraborty P, Chatterjee M, et al. 1alpha, 25-dihydroxyvitamin D3 prevents DNA damage and restores antioxidant enzymes in rat hepatocarcinogenesis induced by diethylnitrosamine and promoted by phenobarbital. World J Gastroenterol 2004;0:1268-1275.
17. Krishnan AV, Shinghal R, Raghavachari N, Brooks JD, Peehl DM, Feldman D. Analysis of vitamin D-regulated gene expression in LNCaP human prostate cancer cells using cDNA microarrays. Prostate. 2004;59:243-251.
18. Wu-Wong JR, Nakane M, Ma J, Ruan X, Kroeger PE. Effects of Vitamin D analogs on gene expression profiling in human coronary artery smooth muscle cells. Atherosclerosis. 2006;186:20-28.
19. Haussler MR, Haussler CA, Whitfield GK, Hsieh JC, Thompson PD, Barthel TK, Bartik L,. Egan JB, Wu Y, Kubicek JL, Lowmiller CL, Moffet EW, Forster RE, Jurutka PW. The nuclear vitamin D receptor controls the expression of genes encoding factors which feed the "Fountain of Youth" to mediate healthful aging. J. Steroid Biochem. Mol Biol 2010;121:88-97.
20. Barzilai A, Yamamoto K. DNA damage responses to oxidative stress. DNA repair (Amst) 2004;3:1109-1115.
21. Vilenchik MM, Knudson AG. Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 2003;100:12871-12876.
22. Floyd RA, West M, Henssley K. Oxidative biochemical markers; clues to understanding aging in long-lived species. Exp Gerontol 2001;36:619-640.
23. Marnett LJ, Riggins JN, West JD. Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest 2003;111:583-593.
24. Valko M, Rhodes C-J, Moncol J, Izakovic M. Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006;160,1-40.
25. Kallay E, Pietschmann P, Toyokuni S, Bajna E, Hahn P, Mazzucco K, Bieglmayer C, Kato S, Cross HS. Characterization of a vitamin D receptor knockout mouse as a model of colorectal hyperproliferation and DNA damage. Carcinogenesis 2001;22:1429-1435.
26. Fedirko V, Bostick RM, Long Q, Flanders WD, McCullough ML, Sidelnikov E, Daniel CR, Rutherford RE, Shaukat A. Effects of supplemental vitamin D and calcium on oxidative DNA damage marker in normal colorectal mucosa: a randomized clinical trial. Cancer Epidemiol. Biomarkers Prev. 2010;19:280-291.
27. Schutze N, Fritzche J, Ebert-Dumig R, Schneider D, Kohrle J, Andreesen R, Kreutz M, Jakob F. The selenoprotein thioredoxin reductase is expressed in peripheral blood monocytes and THP1 human myeloid leukemia cells - regulation by 1,25- dihydroxyvitamin D3 and selenite. Biofactors 1999;10:329-338.
28. Peehl DM, Shinghal R, Nonn L, Seto E, Krishnan AV, Brooks JD, Feldman D. Molecular activity of 1,25-dihydroxyvitamin D3 in primary cultures of human prostatic epithelial cells revealed by cDNA microarray analysis. J. Steroid Biochem Mol. Biol 2004;92:131-141.
29. Swami S, Raghavachari N, Muller UR, Bao YP, Feldman D. Vitamin D growth inhibition of breast cancer cells: gene expression patterns assessed by cDNA microarray. Breast Cancer Res Treat 2003;80:49-62.
30. Palmer HG, Sanchez-Carbayo M, Ordonez-Moran P, Larriba MJ, Cordon-Cardo C, Munoz A. Genetic signatures of differentiation induced by 1α,25-dihydroxyvitamin D3 in human colon cancer cells. Cancer Res 2003;63:7799-7806.
31. Lambert JR, Kelly JA, Shim M, Huffer WE, Nordeen SK, Baek S J, Eling TE, Lucia, MS. Prostate derived factor in human prostate cancer cells: gene induction by vitamin D via a p53-dependent mechanism and inhibition of prostate cancer cell growth. J Cell Physiol 2006; 208:566-574.
32. Huang X, Tanaka T, Kurose A, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation on Ser-139 in cells untreated by genotoxic agents is cell-cycle phase specific and attenuated by scavenging reactive oxygen species. Int J Oncol 2006;29:495-501.
33. Tanaka T, Halicka HD, Huang X, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 2006;5:1940-1945.
34. Zhao H, Tanaka T, Halicka HD, Traganos F, Zarebski M, Dobrucki J, Darzynkiewicz Z. Cytometric assessment of DNA damage by exogenous and endogenous oxidants reports the aging-related processes. Cytometry A 2007;71A:905-914.
35. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-5868.
36. Bartkova J, Bakkenist CJ, Rajpert-De Meyts E, Skakkebaek NE, Sehested M, Lukas J, Kastan MB, Bartek J. ATM activation in normal human tissues and testicular cancer. Cell Cycle 2005;4:838-845.
37. Tanaka T, Kajstura M, Halicka HD, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation and ATM activation are strongly amplified during mitogenic stimulation of lymphocytes. Cell Prolif 2007;40:1-13.
38. Zhao H, Tanaka T, Mitlitski V, Heeter J, Balazs EA, Darzynkiewicz Z. Protective effect of hyaluronate on oxidative DNA damage in WI-38 and A549 cells. Int J Oncol 2008;32:1159-1169.
39. Halicka HD, Zhao H, Li J, Traganos F, Zhang S, Lee M, Darzynkiewicz Z. Genome protective effect of metformin as revealed by reduced level of constitutive DNA damage signaling. Aging (Albany) 2011;3:1028-1038.
40. Zhao H, Dobrucki J, Rybak P, Traganos F, Halicka H.D. Darzynkiewicz Z. Induction of DNA damage signaling by oxidative stress in relation to DNA replication as detected using the "click chemistry" approach. Cytometry A 2011;79A:897-902.
41. Rigby WF, Noelle RJ, Krause K, Fanger MW. The effect of 1,25-dihydroxyvitamin D3 on human T lymphocyte activation and proliferation: a cell cycle analysis. J Immunol 1985;135:2279-2286.
42. Kowitz A, Greiner M, Thieroff-Ekerdt R. Inhibitory effect of 1alpha, 25-dihydroxyvitamin D3 on allogeneic lymphocyte stimulation and Langerhans cell maturation. Arch Dermatol Res 1998;290:540-546.
43. Mahon BD, Wittke A, Weaver V, Cantorna MT. The targets of vitamin D depend on the differentiation and activation status of CD4 positive T cells. J Cell Biochem 2003;89:922-932.
44. Pospelova TV, Demidenko ZN, Bukreeva EI, Gudkov VA, Blagosklonny MV. Cell Pseudo-DNA damage response in senescent cells. Cell Cycle 2009;8:4112-4118.
45. Burhans WC, Weinberger M. DNA replication stress, genome instability and aging. Nucleic Acids Res 2007;33:7545-7556.
46. Bartkova J, Hamerlik P, Stockhausen MT, Ehrman J, Hlobikova A, Laursen H, Kalita O, Kolar Z, Paulsen HS, Broholm H, Lukas J, Bartek J. Replication stress and oxidative damage contributes to aberrant constitutive activation of DNA damage signaling in human gliomas. Oncogene 2010;29:5095-5102.
47. Blagosklonny MV. Revisiting the antagonistic pleiotropy theory of aging: TOR-driven program and quasi-program. Cell Cycle. 2010;9:3151-3156.
48. O'Kelly J, Uskokovic M, Lemp N, Vadgama J, Koeffler HP. Novel Gemini-vitamin D3 analog inhibits tumor cell growth and modulates the Akt/mTOR signaling pathway. J. Steroid Biochem Mol Biol 2006;100:107-116.
49. Lisse TS, Liu M, Beckers J, Chen H, Adams JS, Hewison M. Gene targeting by vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling. FASEB J 2011;25:937-947.
50. Lisse TS, Hewison M. Vitamin D. A new player in mTOR signaling. Cell Cycle 2011;10:1888-1889.
51. Marcinkowska E, Kutner A. Side-chain modified vitamin D analogs require activation of both PI 3-K and erk1,2 signal transduction pathways to induce differentiation of human promyelocytic leukemia cells. Acta Biochim Pol 2002;49:393-406.
52. Zhang Y, Zhang J, Studzinski GP. AKT pathway is activated by 1, 25-dihydroxyvitamin D3 and participates in its anti-apoptotic effect and cell cycle control in differentiating HL60 cells. Cell Cycle 2006;5:447-451.
53. Yang J, Ikezoe T, Nishioka C, Ni L, Koeffler HP, Yokoyama, A. Inhibition of mTORC1 by RAD001 (everolimus) potentiates the effects of 1,25-dihydroxyvitamin D(3) to induce growth arrest and differentiation of AML cells in vitro and in vivo. Exp Hematol 2010;38:666-676.
54. Klotz B, Mentrup B, Regensburger M, Zeck S, Schneidereit J, Schupp N, Linded C, Merz C, Ebert R, Jakob F. 1,25- dihydroxyvitamin D3 treatment delays cellular aging in human mesenchymal stem cells while maintaining their multipotent capacity. PLoS One 2012;7:e29959 Epub Jan 5.
55. Haussler MR, Haussler CA, Whitfield GK, Hsieh JC, Thompson PD, Barthel TK, Bartik L, Egan JB, Wu Y, Kubicek JL, Lowmiller CL, Moffet EW, Forster RE, Jurutka PW. The nuclear vitamin D receptor controls the expression of genes encoding factors which feed the "Fountain of Youth" to mediate healthful Aging. J Steroid Biochem Mol Biol 2010;121:88-97.
56. Touhimm P. Vitamin D and aging. J Steroid Biochem Mol Biol 2009;114:78-84.
57. Lanske B, Razzaque MS. Vitamin D and aging: old concepts and new insights. J Nutr Biochem 2007;18:771-777.
58. Forster RE, Jurutka PW, Hsieh JC, Haussler CA, Lowmiller CL, Kaneko I, Haussler MR, Kerr WH. Vitamin D receptor controls expression of the anti-aging klotho gene in mouse and human renal cells. Biochem Biophys Res Commun 2011;414:557-562.
59. Blagosklonny MV. Aging: ROS or TOR. Cell Cycle 2008;7:3344-3354.
60. Ting H-J, Yasmin-Karim S, Yan S-J, Hsu J-W, Lin T-H, Seng W, Messing J, Sheu T-J, Bao B-Y, Li WX, Messing E, Lee Y-F. A positive feedback signaling loop between ATM and vitamin D receptor is critical for cancer chemoprevention by vitamin D. Cancer Res 2012;72:958-968.
61. Colston K, Colston M J, Feldman D. 1,25-dihydroxyvitamin D3 and malignant melanoma: the presence of receptors and inhibition of cell growth in culture. Endocrinology 1981;108;1083-1086.
62. Lointier P, Wargovich M J, Saez S, Levin B, Wildrick DM, Boman BM. The role of vitamin D3 in the proliferation of a human colon cancer cell line in vitro. Anticancer Res 1987;7:817-821.
63. Gross M, Kost SB, Ennis B, Stumpf W, Kumar R. Effect of 1,25-dihydroxyvitamin D3 on mouse mammary tumor (GR) cells: evidence for receptors, cellular uptake, inhibition of growth and alteration in morphology at physiologic concentrations of hormone. J Bone Miner Res 1986;1:457-467.
64. Skowronski RJ, Peehl DM, Feldman D. Vitamin D and prostate cancer: 1,25 dihydroxyvitamin D3 receptors and actions in human prostate cancer cell lines. Endocrinology 1993;132:1952-1960.
65. Wang X, Patel R, Studzinski GP. hKSR-2, a vitamin Dregulated gene, inhibits apoptosis in arabinocytosine-treated HL60 leukemia cells. Mol Cancer Ther 2008;7:2798-2806.
66. Gocek E, Wang X, Liu X, Liu CG, Studzinski GP. MicroRNA-32 upregulation by 1,25-dihydroxyvitamin D3 in human myeloid leukemia cells leads to Bim targeting and inhibition of AraCinduced apoptosis. Cancer Res 2011;71:6230-6239.
67. Oka K, Tanaka T, Enoki T, Yoshimura K, Ohshima M, Kubo M, Murakami T, Gondou T, Minami Y, Takemoto Y, Harada E, Tsushimi T, Li T-S, Traganos F, Darzynkiewicz Z, Hamano K. DNA damage signaling is activated during cancer progression in human colorectal carcinoma. Cancer Biol Ther 2010;9:246-252.
68. Studzinski GP, Wang X, Danilenko M. DNA damage response: A barrier or a path to tumor progression? Cancer Biol Ther 2010;9:253-255.
69. Rothe G, Klouche M. Phagocyte functions. Meth Cell Biol 2004;75:679-708.
70. Darzynkiewicz Z. Bedner E. Gorczyca W, Melamed MR. Laser scanning cytometry. A new instrumentation with many applications. Exp Cell Res 1999;249:1-12.