Epigenetic impacts of ascorbate on human metastatic melanoma cells

Frontiers in Oncology

Volumn 4 AUG, Issue , 2014, Pages

  Venturelli, Sascha ^a   Sinnberg, Tobias W ^b   Berger, Alexander ^a   Noor, Seema ^b   Levesque, Mitch ^c   Böcker, Alexander ^d   Niessner, Heike ^b   Lauer, Ulrich M ^a   Bitzer, Michael ^a   Garbe, Claus ^b   Busch, Christian ^b  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d EVOTEC AG   (Germany)

Author keywords

Ascorbate; Cancer; DNMT; Epigenetics; HDAC; Melanoma; MicroRNA; Vitamin c

Indexed keywords

ASCORBIC ACID; DNA METHYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE DEACETYLASE INHIBITOR 2; HISTONE DEACETYLASE INHIBITOR 4; HISTONE DEACETYLASE INHIBITOR 7; HISTONE DEACETYLASE INHIBITOR 8; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE; COMPUTER MODEL; CONTROLLED STUDY; ENZYME INHIBITION; EPIGENETICS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; MELANOMA CELL; NASOPHARYNX CARCINOMA; PROTEIN INTERACTION; UPREGULATION;

EID: 84906279217     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00227     Document Type: Article

References (47)

1. Chen Q, Espey MG, Krishna MC, Mitchell JB, Corpe CP, Buettner GR, Shacter E, Levine M. Pharmacologic ascorbic acid concentrations selectively kill cancer cells: action as a pro-drug to deliver hydrogen peroxide to tissues. Proc Natl Acad Sci USA (2005) 102:13604-9.
2. Chen Q, Espey MG, Sun AY, Pooput C, Kirk KL, Krishna MC, Khosh DB, Drisko J, Levine M. Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice. Proc Natl Acad Sci USA (2008) 105:11105-9. doi: 10.1073/pnas.0804226105.
3. Du J, Martin SM, Levine M, Wagner BA, Buettner GR, Wang SH, Taghiyev AF, Du C, Knudson CM, Cullen JJ. Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin Cancer Res (2010) 16:509-20. doi: 10.1158/1078-0432.CCR- 09-1713.
4. Chen Q, Espey MG, Sun AY, Lee JH, Krishna MC, Shacter E, Choyke PL, Pooput C, Kirk KL, Buettner GR, Levine M. Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc Natl Acad Sci USA (2007) 104:8749-54.
5. Sinnberg T, Noor S, Venturelli S, Berger A, Schuler P, Garbe C, Busch C. The ROS induced cytotoxicity of ascorbate is attenuated by hypoxia and HIF-1alpha in the NCI60 cancer cell lines. J Cell Mol Med (2014) 18:530-41. doi: 10.1111/jcmm.12207.
6. Kuiper C, Dachs GU, Currie MJ, Vissers MC. Intracellular ascorbate enhances hypoxia-inducible factor (HIF)-hydroxylase activity and preferentially suppresses the HIF-1 transcriptional response. Free Radic Biol Med (2014) 69:308-17. doi: 10.1016/j.freeradbiomed.2014.01.033.
7. Kuiper C, Dachs GU, Munn D, Currie MJ, Robinson BA, Pearson JF, Vissers MC. Increased Tumor Ascorbate is Associated with Extended Disease-Free Survival and Decreased Hypoxia-Inducible Factor-1 Activation in Human Colorectal Cancer. Front Oncol (2014) 4:10. doi: 10.3389/fonc.2014.00010.
8. Kuiper C, Molenaar IG, Dachs GU, Currie MJ, Sykes PH, Vissers MC. Low ascorbate levels are associated with increased hypoxia-inducible factor-1 activity and an aggressive tumor phenotype in endometrial cancer. Cancer Res (2010) 70:5749-58. doi: 10.1158/0008-5472.CAN-10-0263.
9. Bram S, Froussard P, Guichard M, Jasmin C, Augery Y, Sinoussi-Barre F, Wray W. Vitamin C preferential toxicity for malignant melanoma cells. Nature (1980) 284:629-31.
10. Meadows GG1, Pierson HF, Abdallah RM. Ascorbate in the treatment of experimental transplanted melanoma. Am J Clin Nutr (1991) 54:1284S-1291S.
11. Kang JS, Cho D, Kim YI, Hahm E, Yang Y, Kim D, Hur D, Park H, Bang S, Hwang YI, Lee WJ. L-ascorbic acid (vitamin C) induces the apoptosis of B16 murine melanoma cells via a caspase-8-independent pathway. Cancer Immunol Immunother (2003) 52:693-8.
12. Cha J, Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A, Rath M. Ascorbate depletion increases growth and metastasis of melanoma cells in vitamin C deficient mice. Exp Oncol (2011) 33:226-30.
13. Cha J, Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A, Rath M. Ascorbate supplementation inhibits growth and metastasis of B16FO melanoma and 4T1 breast cancer cells in vitamin C-deficient mice. Int J Oncol (2013) 42:55-64. doi: 10.3892/ijo.2012.1712.
14. Schleich T, Rodemeister S, Venturelli S, et al. Decreased plasma ascorbate levels in stage IV melanoma patients. Metab Nutr Oncol (2013) DOI http://dx.doi.org/10.1055/s-0033-1348256.
15. Verrax J, Calderon PB. Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects. Free Radic Biol Med (2009) 47:32-40. doi: 10.1016/j.freeradbiomed.2009.02.016.
16. Stephenson CM, Levin RD, Spector T, Lis CG. Phase I clinical trial to evaluate the safety, tolerability, and pharmacokinetics of high-dose intravenous ascorbic acid in patients with advanced cancer. Cancer Chemother Pharmacol (2013) 72:139-46. doi: 10.1007/s00280-013-2179-9.
17. Hoffer LJ, Levine M, Assouline S, Melnychuk D, Padayatty SJ, Rosadiuk K, Rousseau C, Robitaille L, Miller WH Jr. Phase I clinical trial of i.v. ascorbic acid in advanced malignancy. Ann Oncol (2008) 19:1969-74. doi: 10.1093/annonc/mdn377.
18. Welsh JL, Wagner BA, van't Erve TJ, Zehr PS, Berg DJ, Halfdanarson TR, Yee NS, Bodeker KL, Du J, Roberts LJ 2nd, Drisko J, Levine M, Buettner GR, Cullen JJ. Pharmacological ascorbate with gemcitabine for the control of metastatic and node positive pancreatic cancer (PACMAN): results from a phase I clinical trial. Cancer Chemother Pharmacol (2013) 71:765-75. doi: 10.1007/s00280-013-2070-8.
19. Riordan HD, Casciari JJ, González MJ, Riordan NH, Miranda-Massari JR, Taylor P, Jackson JA. A pilot clinical study of continuous intravenous ascorbate in terminal cancer patients. P R Health Sci J (2005) 24:269-76.
20. Ma Y, Chapman J, Levine M, Polireddy K, Drisko J, Chen Q. High-dose parenteral ascorbate enhanced chemosensitivity of ovarian cancer and reduced toxicity of chemotherapy. Sci Transl Med (2014) 6:222ra18. doi: 10.1126/scitranslmed.3007154.
21. Clarke JD, Hsu A, Yu Z, Dashwood RH, Ho E. Differential effects of sulforaphane on histone deacetylases, cell cycle arrest and apoptosis in normal prostate cells versus hyperplastic and cancerous prostate cells. Mol Nutr Food Res (2011) 55:999-1009. doi: 10.1002/mnfr.201000547.
22. Berger A, Venturelli S, Kallnischkies M, Böcker A, Busch C, Weiland T, Noor S, Leischner C, Weiss TS, Lauer UM, BischoffSC, Bitzer M. Kaempferol, a new nutrition-derived pan-inhibitor of human histone deacetylases. J Nutr Biochem (2013) 24:977-85. doi: 10.1016/j.jnutbio.2012.07.001.
23. Venturelli S, Berger A, Böcker A, Busch C, Weiland T, Noor S, Leischner C, Schleicher S, Mayer M, Weiss TS, BischoffSC, Lauer UM, Bitzer M. Resveratrol as a Pan-HDAC Inhibitor Alters the Acetylation Status of Histone Proteins in Human- Derived Hepatoblastoma Cells. PLoS One (2013) 8: e73097. doi: 10.1371/journal.pone.0073097.
24. Ellis L, Atadja PW, Johnstone RW. Epigenetics in cancer: targeting chromatin modifications. Mol Cancer Ther (2009) 8:1409-20. doi: 10.1158/1535-7163.MCT-08-0860.
25. Chuang JC, Jones PA. Epigenetics and microRNAs. Pediatr Res (2007) 61:24R-29R.
26. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K. MicroRNAs and epigenetics. FEBS J (2011) 278:1598-609. doi: 10.1111/j.1742-4658.2011.08089.x.
27. Lovat F, Valeri N, Croce CM. MicroRNAs in the pathogenesis of cancer. Semin Oncol (2011) 38:724-33. doi: 10.1053/j.seminoncol.2011.08.006.
28. Antonov AV, Knight RA, Melino G, Barlev NA, Tsvetkov PO. MIRUMIR: an online tool to test microRNAs as biomarkers to predict survival in cancer using multiple clinical data sets. Cell Death Differ (2013) 20:367. doi: 10.1038/cdd.2012.137.
29. Carey TE, Takahashi T, Resnick LA, Oettgen HF, Old LJ. Cell surface antigens of human malignant melanoma: mixed hemadsorption assays for humoral immunity to cultured autologous melanoma cells. Proc Natl Acad Sci U S A (1976) 73:3278-82.
30. Lockshin A, Giovanella BC, De Ipolyi PD, Williams LJ Jr, Mendoza JT, Yim SO, Stehlin JS Jr. Exceptional lethality for nude mice of cells derived from a primary human melanoma. Cancer Res (1985) 45:345-50.
31. Labute P. 2009. Protonate3D: assignment of ionization states and hydrogen coordinates to macromolecular structures. Proteins 75:187-205. doi: 10.1002/prot.22234.
32. Reischauer, S. 2009. Lgl2 executes its function as a tumor suppressor by regulating ErbB signaling in the zebrafish epidermis. PLoS Genet (2009) 5:e1000720. doi: 10.1371/journal.pgen.1000720.
33. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, Cho JW, Park YM, Jung G. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology (2008) 135:2128-40. doi: 10.1053/j.gastro.2008.07.027.
34. Eigentler TK1, Figl A, Krex D, Mohr P, Mauch C, Rass K, Bostroem A, Heese O, Koelbl O, Garbe C, Schadendorf D; Dermatologic Cooperative Oncology Group and the National Interdisciplinary Working Group on Melanoma. Number of metastases, serum lactate dehydrogenase level, and type of treatment are prognostic factors in patients with brain metastases of malignant melanoma. Cancer (2011) 117:1697-703. doi: 10.1002/cncr.25631.
35. Garbe C, Peris K, Hauschild A, Saiag P, Middleton M, Spatz A, Grob JJ, Malvehy J, Newton-Bishop J, Stratigos A, Pehamberger H, Eggermont AM; European Dermatology Forum; European Association of Dermato-Oncology; European Organization of Research and Treatment of Cancer. Diagnosis and treatment of melanoma. European consensus-based interdisciplinary guideline--Update 2012. Eur J Cancer (2012) 48:2375-90. doi: 10.1016/j.ejca.2012.06.013.
36. Garbe C, Abusaif S, Eigentler TK. Vemurafenib. Recent Results Cancer Res (2014) 201:215-25. doi: 10.1007/978-3-642-54490-3_13.
37. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: Prolongation of survival times in terminal human cancer. Proc Natl Acad Sci U S A (1976) 73:3685-9.
38. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: reevaluation of prolongation of survival times in terminal human cancer. Proc Natl Acad Sci U S A (1978) 75:4538-42.
39. Mikirova N, Casciari J, Riordan N, Hunninghake R. Clinical experience with intravenous administration of ascorbic acid: achievable levels in blood for different states of inflammation and disease in cancer patients. J Transl Med (2013) 11:191.
40. Meeran SM1, Ahmed A, Tollefsbol TO. Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics (2010) 1:101-16.
41. Venturelli S1, Berger A, Weiland T, Zimmermann M, Häcker S, Peter C, Wesselborg S, Königsrainer A, Weiss TS, Gregor M, Fulda S, Lauer UM, Bitzer M. Dual antitumour effect of 5-azacytidine by inducing a breakdown of resistance-mediating factors and epigenetic modulation. Gut (2011) 60:156-65. doi: 10.1136/gut.2010.208041.
42. Weiland T, Berger A, Essmann F, Lauer UM, Bitzer M, Venturelli S. Kinetic tracking of therapy-induced senescence using the real-time cell analyzer single plate system. Assay Drug Dev Technol (2012) 10:289-95. doi: 10.1089/adt.2011.0402.
43. Venturelli S, Berger A, Weiland T, Essmann F, Waibel M, Nuebling T, Häcker S, Schenk M, Schulze-OsthoffK, Salih HR, Fulda S, Sipos B, Johnstone RW, Lauer UM, Bitzer M. Differential induction of apoptosis and senescence by the DNA methyltransferase inhibitors 5-azacytidine and 5-aza-2'-deoxycytidine in solid tumor cells. Mol Cancer Ther (2013) 12:2226-36. doi: 10.1158/1535-7163.MCT-13-0137.
44. Padayatty SJ, Sun AY, Chen Q, Espey MG, Drisko J, Levine M. Vitamin C: intravenous use by complementary and alternative medicine practitioners and adverse effects. PLoS One (2010) 5:e11414. doi: 10.1371/journal.pone.0011414.
45. Busch C, Krochmann J, Drews U. The chick embryo as an experimental system for melanoma cell invasion. PLoS One (2013) 8:e53970. doi: 10.1371/journal.pone.0053970.
46. Schriek G, Oppitz M, Busch C, Just L, Drews U. Human SK-Mel 28 melanoma cells resume neural crest cell migration after transplantation into the chick embryo. Melanoma Res (2005) 15:225-34.
47. Busch C, Drews U, Garbe C, Eisele SR, Oppitz M. Neural crest cell migration of mouse B16-F1 melanoma cells transplanted into the chick embryo is inhibited by the BMP-antagonist noggin. Int J Oncol (2007) 31:1367-78.