Potassium increases the antitumor effects of ascorbic acid in breast cancer cell lines in vitro
- Authors:
- Giovanni Vanni Frajese
- Monica Benvenuto
- Massimo Fantini
- Elena Ambrosin
- Pamela Sacchetti
- Laura Masuelli
- Maria Gabriella Giganti
- Andrea Modesti
- Roberto Bei
-
Affiliations: Department of Sports Science, Human and Health, University of Rome ‘Foro Italico’, Rome I‑00135, Italy, Department of Clinical Sciences and Translational Medicine, University of Rome ‘Tor Vergata’, Rome I‑00133, Italy, Department of Experimental Medicine, University of Rome ‘Sapienza’, Rome I‑00185, Italy - Published online on: April 27, 2016 https://doi.org/10.3892/ol.2016.4506
- Pages: 4224-4234
This article is mentioned in:
Abstract
Khaw KT, Bingham S, Welch A, Luben R, Wareham N, Oakes S and Day N: Relation between plasma ascorbic acid and mortality in men and women in EPIC-Norfolk prospective study: A prospective population study. European Prospective Investigation into Cancer and Nutrition. Lancet. 357:657–663. 2001. View Article : Google Scholar : PubMed/NCBI | |
Block G: Epidemiologic evidence regarding vitamin C and cancer. Am J Clin Nutr. 54(Suppl 6): 1310S–1314S. 1991.PubMed/NCBI | |
Cameron E and Pauling L: The orthomolecular treatment of cancer. I. The role of ascorbic acid in host resistance. Chem Biol Interact. 9:273–283. 1974. View Article : Google Scholar : PubMed/NCBI | |
Creagan ET, Moertel CG, O'Fallon JR, Schutt AJ, O'Connell MJ, Rubin J and Frytak S: Failure of high-dose vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer. A controlled trial. N Engl J Med. 301:687–690. 1979. View Article : Google Scholar : PubMed/NCBI | |
Ohno S, Ohno Y, Suzuki N, Soma G and Inoue M: High-dose vitamin C (ascorbic acid) therapy in the treatment of patients with advanced cancer. Anticancer Res. 29:809–815. 2009.PubMed/NCBI | |
Levine M, Conry-Cantilena C, Wang Y, Welch RW, Washko PW, Dhariwal KR, Park JB, Lazarev A, Graumlich JF, King J and Cantilena LR: Vitamin C pharmacokinetics in healthy volunteers: Evidence for a recommended dietary allowance. Proc Natl Acad Sci USA. 93:3704–3709. 1996. View Article : Google Scholar : PubMed/NCBI | |
Levine M, Wang Y, Padayatty SJ and Morrow J: A new recommended dietary allowance of vitamin C for healthy young women. Proc Natl Acad Sci USA. 98:9842–9846. 2001. View Article : Google Scholar : PubMed/NCBI | |
Padayatty SJ, Sun H, Wang Y, Riordan HD, Hewitt SM, Katz A, Wesley RA and Levine M: Vitamin C pharmacokinetics: Implications for oral and intravenous use. Ann Intern Med. 140:533–537. 2004. View Article : Google Scholar : PubMed/NCBI | |
Hoffer LJ, Levine M, Assouline S, Melnychuk D, Padayatty SJ, Rosadiuk K, Rousseau C, Robitaille L and Miller WH Jr: Phase I clinical trial of i.v. ascorbic acid in advanced malignancy. Ann Oncol. 19:1969–1974. 2008. View Article : Google Scholar : PubMed/NCBI | |
Parrow NL, Leshin JA and Levine M: Parenteral ascorbate as a cancer therapeutic: A reassessment based on pharmacokinetics. Antioxid Redox Signal. 19:2141–2156. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ma Y, Chapman J, Levine M, Polireddy K, Drisko J and Chen Q: High-dose parenteral ascorbate enhanced chemosensitivity of ovarian cancer and reduced toxicity of chemotherapy. Sci Transl Med. 6:222ra182014. View Article : Google Scholar : PubMed/NCBI | |
Cone CD Jr: Unified theory on the basic mechanism of normal mitotic control and oncogenesis. J Theor Biol. 30:151–181. 1971. View Article : Google Scholar : PubMed/NCBI | |
Hughes FM Jr and Cidlowski JA: Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Adv Enzyme Regul. 39:157–171. 1999. View Article : Google Scholar : PubMed/NCBI | |
Wang Z: Roles of K+ channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch. 448:274–286. 2004. View Article : Google Scholar : PubMed/NCBI | |
DeCoursey TE, Chandy KG, Gupta S and Cahalan MD: Voltage-gated K+ channels in human T lymphocytes: A role in mitogenesis? Nature. 307:465–468. 1984. View Article : Google Scholar : PubMed/NCBI | |
Pardo LA: Voltage-gated potassium channels in cell proliferation. Physiology (Bethesda). 19:285–292. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wonderlin WF and Strobl JS: Potassium channels, proliferation and G1 progression. J Membr Biol. 154:91–107. 1996. View Article : Google Scholar : PubMed/NCBI | |
Boros LG, Lee PW, Brandes JL, Cascante M, Muscarella P, Schirmer WJ, Melvin WS and Ellison EC: Nonoxidative pentose phosphate pathways and their direct role in ribose synthesis in tumors: Is cancer a disease of cellular glucose metabolism? Med Hypotheses. 50:55–59. 1998. View Article : Google Scholar : PubMed/NCBI | |
Smith NK, Stabler SB, Cameron IL and Medina D: X-Ray microanalysis of electrolyte content of normal, preneoplastic, and neoplastic mouse mammary tissue. Cancer Res. 41:3877–3880. 1981.PubMed/NCBI | |
Arrebola F, Fernández-Segura E, Campos A, Crespo PV, Skepper JN and Warley A: Changes in intracellular electrolyte concentrations during apoptosis induced by UV irradiation of human myeloblastic cells. Am J Physiol Cell Physiol. 290:C638–C649. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mobasheri A, Fox R, Evans I, Cullingham F, Martín-Vasallo P and Foster CS: Epithelial Na, K-ATPase expression is down-regulated in canine prostate cancer; a possible consequence of metabolic transformation in the process of prostate malignancy. Cancer Cell Int. 3:82003. View Article : Google Scholar : PubMed/NCBI | |
Chen JQ, Contreras RG, Wang R, Fernandez SV, Shoshani L, Russo IH, Cereijido M and Russo J: Sodium/potassium ATPase (Na+, K+-ATPase) and ouabain/related cardiac glycosides: A new paradigm for development of anti-breast cancer drugs? Breast Cancer Res Treat. 96:1–15. 2006. View Article : Google Scholar : PubMed/NCBI | |
Parkinson GN, Lee MP and Neidle S: Crystal structure of parallel quadruplexes from human telomeric DNA. Nature. 417:876–880. 2002. View Article : Google Scholar : PubMed/NCBI | |
Salvati E, Rizzo A, Iachettini S, Zizza P, Cingolani C, D'Angelo C, Porru M, Mondello C, Aiello A, Farsetti A, et al: A basal level of DNA damage and telomere deprotection increases the sensitivity of cancer cells to G-quadruplex interactive compounds. Nucleic Acids Res. 43:1759–1769. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dai J, Carver M and Yang D: Polymorphism of human telomeric quadruplex structures. Biochimie. 90:1172–1183. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kelland LR: Overcoming the immortality of tumour cells by telomere and telomerase based cancer therapeutics - current status and future prospects. Eur J Cancer. 41:971–979. 2005. View Article : Google Scholar : PubMed/NCBI | |
Paoli G: The Bio-magnetic nature of cancer and the role of potassium ascorbate and ribose against cellar degeneration. J Nucl Energy. 7:114–119. 2003. | |
Croci S, Pedrazzi G, Passeri G, Delsignore R and Ortalli I: Red cell Hb oxidation of healthy subjects compared to breast cancer patients. Anticancer Res. 22:2903–2906. 2002.PubMed/NCBI | |
Croci S, Pedrazzi G, Passeri G, Piccolo P and Ortalli I: Acetylphenylhydrazine induced haemoglobin oxidation in erythrocytes studied by Mössbauer spectroscopy. Biochim Biophys Acta. 1568:99–104. 2001. View Article : Google Scholar : PubMed/NCBI | |
Croci S, Bruni L, Bussolati S, Castaldo M and Dondi M: Potassium bicarbonate and D-ribose effects on A72 canine and HTB-126 human cancer cell line proliferation in vitro. Cancer Cell Int. 11:302011. View Article : Google Scholar : PubMed/NCBI | |
Masuelli L, Marzocchella L, Quaranta A, Palumbo C, Pompa G, Izzi V, Canini A, Modesti A, Galvano F and Bei R: Apigenin induces apoptosis and impairs head and neck carcinomas EGFR/ErbB2 signaling. Front Biosci (Landmark Ed). 16:1060–1068. 2011. View Article : Google Scholar : PubMed/NCBI | |
Masuelli L, Marzocchella L, Focaccetti C, Tresoldi I, Palumbo C, Izzi V, Benvenuto M, Fantini M, Lista F, Tarantino U, et al: Resveratrol and diallyl disulfide enhance curcumin-induced sarcoma cell apoptosis. Front Biosci (Landmark Ed). 17:498–508. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bei R, Masuelli L, Moriconi E, Visco V, Moretti A, Kraus MH and Muraro R: Immune responses to all ErbB family receptors detectable in serum of cancer patients. Oncogene. 18:1267–1275. 1999. View Article : Google Scholar : PubMed/NCBI | |
Bei R, Budillon A, Masuelli L, Cereda V, Vitolo D, Di Gennaro E, Ripavecchia V, Palumbo C, Ionna F, Losito S, et al: Frequent overexpression of multiple ErbB receptors by head and neck squamous cell carcinoma contrasts with rare antibody immunity in patients. J Pathol. 204:317–325. 2004. View Article : Google Scholar : PubMed/NCBI | |
Faggioni G, Pomponi A, De Santis R, Masuelli L, Ciammaruconi A, Monaco F, Di Gennaro A, Marzocchella L, Sambri V, Lelli R, et al: West Nile alternative open reading frame (N-NS4B/WARF4) is produced in infected West Nile Virus (WNV) cells and induces humoral response in WNV infected individuals. Virol J. 9:2832012. View Article : Google Scholar : PubMed/NCBI | |
Masuelli L, Budillon A, Marzocchella L, Mrozek MA, Vitolo D, Di Gennaro E, Losito S, Sale P, Longo F, Ionna F, et al: Caveolin-1 overexpression is associated with simultaneous abnormal expression of the E-cadherin/α-β catenins complex and multiple ErbB receptors and with lymph nodes metastasis in head and neck squamous cell carcinomas. J Cell Physiol. 227:3344–3353. 2012. View Article : Google Scholar : PubMed/NCBI | |
Masuelli L, Bei R, Sacchetti P, Scappaticci I, Francalanci P, Albonici L, Coletti A, Palumbo C, Minieri M, Fiaccavento R, et al: Beta-catenin accumulates in intercalated disks of hypertrophic cardiomyopathic hearts. Cardiovasc Res. 60:376–387. 2003. View Article : Google Scholar : PubMed/NCBI | |
Masuelli L, Pompa G, Fabrizi M, Quaranta A, Vozza I, Piccoli L, Antonelli A, Marzocchella L, Di Carlo S, Perrotti V, et al: Patients with peri-implantitis, unlike those with a healthy periimplant microenvironment, display antibodies to more than one heat shock protein (HSP 27, HSP 65 and HSP 90) linear epitope. Eur J Inflamm. 9:257–267. 2011. | |
Ingrosso G, Fantini M, Nardi A, Benvenuto M, Sacchetti P, Masuelli L, Ponti E, Frajese GV, Lista F, Schillaci O, et al: Local radiotherapy increases the level of autoantibodies to ribosomal P0 protein but not to heat shock proteins, extracellular matrix molecules and EGFR/ErbB2 receptors in prostate cancer patients. Oncol Rep. 29:1167–1174. 2013.PubMed/NCBI | |
Palumbo C, Albonici L, Bei R, Bocci C, Scarpa S, Di Nardo P and Modesti A: HMBA induces cell death and potentiates doxorubicin toxicity in malignant mesothelioma cells. Cancer Chemother Pharmacol. 54:398–406. 2004. View Article : Google Scholar : PubMed/NCBI | |
Toyota H, Yanase N, Yoshimoto T, Moriyama M, Sudo T and Mizuguchi J: Calpain-induced Bax-cleavage product is a more potent inducer of apoptotic cell death than wild-type Bax. Cancer Lett. 189:221–230. 2003. View Article : Google Scholar : PubMed/NCBI | |
Du J, Cullen JJ and Buettner GR: Ascorbic acid: Chemistry, biology and the treatment of cancer. Biochim Biophys Acta. 1826:443–457. 2012.PubMed/NCBI | |
Chen Q, Espey MG, Krishna MC, Mitchell JB, Corpe CP, Buettner GR, Shacter E and 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. 102:13604–13609. 2005. View Article : Google Scholar : PubMed/NCBI | |
Du J, Martin SM, Levine M, Wagner BA, Buettner GR, Wang SH, Taghiyev AF, Du C, Knudson CM and Cullen JJ: Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin Cancer Res. 16:509–520. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chen P, Yu J, Chalmers B, Drisko J, Yang J, Li B and Chen Q: Pharmacological ascorbate induces cytotoxicity in prostate cancer cells through ATP depletion and induction of autophagy. Anticancer Drugs. 23:437–444. 2012. View Article : Google Scholar : PubMed/NCBI | |
Martinovich GG, Golubeva EN, Martinovich IV and Cherenkevich SN: Redox regulation of calcium signaling in cancer cells by ascorbic acid involving the mitochondrial electron transport chain. J Biophys. 2012:9216532012. View Article : Google Scholar : PubMed/NCBI | |
Han SS, Kim K, Hahm ER, Lee SJ, Surh YJ, Park HK, Kim WS, Jung CW, Lee MH, Park K, et al: L-ascorbic acid represses constitutive activation of NF-kappaB and COX-2 expression in human acute myeloid leukemia, HL-60. J Cell Biochem. 93:257–270. 2004. View Article : Google Scholar : PubMed/NCBI | |
Park S, Ahn ES, Lee S, Jung M, Park JH, Yi SY and Yeom CH: Proteomic analysis reveals upregulation of RKIP in S-180 implanted BALB/C mouse after treatment with ascorbic acid. J Cell Biochem. 106:1136–1145. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ranzato E, Biffo S and Burlando B: Selective ascorbate toxicity in malignant mesothelioma: A redox Trojan mechanism. Am J Respir Cell Mol Biol. 44:108–117. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chen Q, Espey MG, Sun AY, Lee JH, Krishna MC, Shacter E, Choyke PL, Pooput C, Kirk KL, Buettner GR and Levine M: Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc Natl Acad Sci USA. 104:8749–8754. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cha J, Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A and Rath M: Ascorbate supplementation inhibits growth and metastasis of B16FO melanoma and 4T1 breast cancer cells in vitamin C-deficient mice. Int J Oncol. 42:55–64. 2013.PubMed/NCBI | |
Kim JE, Cho HS, Yang HS, Jung DJ, Hong SW, Hung CF, Lee WJ and Kim D: Depletion of ascorbic acid impairs NK cell activity against ovarian cancer in a mouse model. Immunobiology. 217:873–881. 2012. View Article : Google Scholar : PubMed/NCBI | |
Riordan HD, Riordan NH, Jackson JA, Casciari JJ, Hunninghake R, González MJ, Mora EM, Miranda-Massari JR, Rosario N and Rivera A: Intravenous vitamin C as a chemotherapy agent: A report on clinical cases. P R Health Sci J. 23:115–118. 2004.PubMed/NCBI | |
Shimpo K, Nagatsu T, Yamada K, Sato T, Niimi H, Shamoto M, Takeuchi T, Umezawa H and Fujita K: Ascorbic acid and adriamycin toxicity. Am J Clin Nutr. 54(Suppl 6): 1298S–1301S. 1991.PubMed/NCBI | |
Vollbracht C, Schneider B, Leendert V, Weiss G, Auerbach L and Beuth J: Intravenous vitamin C administration improves quality of life in breast cancer patients during chemo-/radiotherapy and aftercare: Results of a retrospective, multicentre, epidemiological cohort study in Germany. In Vivo. 25:983–990. 2011.PubMed/NCBI | |
L'Allemain G, Paris S and Pouysségur J: Growth factor action and intracellular pH regulation in fibroblasts. Evidence for a major role of the Na+/H+ antiport. J Biol Chem. 259:5809–5815. 1984.PubMed/NCBI | |
Gerson DF, Kiefer H and Eufe W: Intracellular pH of mitogen-stimulated lymphocytes. Science. 216:1009–1010. 1982. View Article : Google Scholar : PubMed/NCBI | |
Bruni L, Babarinde AA, Ortalli I and Croci S: K-D:rib dampens Hs 578T cancer cell chemoinvasion and proliferation. Cancer Cell Int. 14:772014. View Article : Google Scholar : PubMed/NCBI | |
Lacroix M, Toillon RA and Leclercq G: p53 and breast cancer, an update. Endocr Relat Cancer. 13:293–325. 2006. View Article : Google Scholar : PubMed/NCBI | |
Subik K, Lee JF, Baxter L, Strzepek T, Costello D, Crowley P, Xing L, Hung MC, Bonfiglio T, Hicks DG and Tang P: The expression patterns of ER, PR, HER2, CK5/6, EGFR, Ki-67 and AR by immunohistochemical analysis in breast cancer cell lines. Breast Cancer (Auckl). 4:35–41. 2010.PubMed/NCBI | |
Sun D, Lopez-Guajardo CC, Quada J, Hurley LH and Von Hoff DD: Regulation of catalytic activity and processivity of human telomerase. Biochemistry. 38:4037–4044. 1999. View Article : Google Scholar : PubMed/NCBI | |
Harley CB, Futcher AB and Greider CW: Telomeres shorten during ageing of human fibroblasts. Nature. 345:458–460. 1990. View Article : Google Scholar : PubMed/NCBI | |
Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL and Shay JW: Specific association of human telomerase activity with immortal cells and cancer. Science. 266:2011–2015. 1994. View Article : Google Scholar : PubMed/NCBI | |
Zahler AM, Williamson JR, Cech TR and Prescott DM: Inhibition of telomerase by G-quartet DNA structures. Nature. 350:718–720. 1991. View Article : Google Scholar : PubMed/NCBI | |
Hurley LH: DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer. 2:188–200. 2002. View Article : Google Scholar : PubMed/NCBI | |
Neidle S and Parkinson G: Telomere maintenance as a target for anticancer drug discovery. Nat Rev Drug Discov. 1:383–393. 2002. View Article : Google Scholar : PubMed/NCBI | |
Hurley LH, Wheelhouse RT, Sun D, Kerwin SM, Salazar M, Fedoroff OY, Han FX, Han H, Izbicka E and Von Hoff DD: G-quadruplexes as targets for drug design. Pharmacol Ther. 85:141–158. 2000. View Article : Google Scholar : PubMed/NCBI | |
Redon S, Bombard S, Elizondo-Riojas MA and Chottard JC: Platinum cross-linking of adenines and guanines on the quadruplex structures of the AG3(T2AG3)3 and (T2AG3)4 human telomere sequences in Na+ and K+ solutions. Nucleic Acids Res. 31:1605–1613. 2003. View Article : Google Scholar : PubMed/NCBI | |
Phan AT and Patel DJ: Two-repeat human telomeric d(TAGGGTTAGGGT) sequence forms interconverting parallel and antiparallel G-quadruplexes in solution: Distinct topologies, thermodynamic properties, and folding/unfolding kinetics. J Am Chem Soc. 125:15021–15027. 2003. View Article : Google Scholar : PubMed/NCBI | |
Li J, Correia JJ, Wang L, Trent JO and Chaires JB: Not so crystal clear: The structure of the human telomere G-quadruplex in solution differs from that present in a crystal. Nucleic Acids Res. 33:4649–4659. 2005. View Article : Google Scholar : PubMed/NCBI | |
Włodarczyk A, Grzybowski P, Patkowski A and Dobek A: Effect of ions on the polymorphism, effective charge, and stability of human telomeric DNA. Photon correlation spectroscopy and circular dichroism studies. J Phys Chem B. 109:3594–3605. 2005. View Article : Google Scholar : PubMed/NCBI | |
Ambrus A, Chen D, Dai J, Bialis T, Jones RA and Yang D: Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res. 34:2723–2735. 2006. View Article : Google Scholar : PubMed/NCBI | |
Dai J, Carver M, Punchihewa C, Jones RA and Yang D: Structure of the Hybrid-2 type intramolecular human telomeric G-quadruplex in K+ solution: Insights into structure polymorphism of the human telomeric sequence. Nucleic Acids Res. 35:4927–4940. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hadi SM, Ullah MF, Shamim U, Bhatt SH and Azmi AS: Catalytic therapy of cancer by ascorbic acid involves redox cycling of exogenous/endogenous copper ions and generation of reactive oxygen species. Chemotherapy. 56:280–284. 2010. View Article : Google Scholar : PubMed/NCBI |