Docosahexaenoic Acid-mediated Inhibition of Heat Shock Protein 90-p23 Chaperone Complex and Downstream Client Proteins in Lung and Breast Cancer

References

• Demaison L, Sergiel JP, Moreau D, and Grynberg A: Influence of the phospholipid n-6/n-3 polyunsaturated fatty acid ratio on the mitochondrial oxidative metabolism before and after myocardial ischemia. Biochim Biophys Acta 1227, 53–59, 1994.
   PubMed Web of Science ®Google Scholar
• de Lima TM, Amarante-Mendes GP, and Curi R: Docosahexaenoic acid enhances the toxic effect of imatinib on Bcr-Abl expressing HL-60 cells. Toxicol In Vitro 21, 1678–1685, 2007.
   PubMed Web of Science ®Google Scholar
• Badawi AF, El-Sohemy A, Stephen LL, Ghoshal AK, and Archer MC: The effect of dietary n-3 and n-6 polyunsaturated fatty acids on the expression of cyclooxygenase 1 and 2 and levels of p21ras in rat mammary glands. Carcinogenesis 19, 905–910, 1998.
   PubMed Web of Science ®Google Scholar
• Bang HO and Dyerberg J HN: The composition of food consumed by Greenland Eskimos. Acta Med Scand 200, 69–73, 1976.
   PubMed Web of Science ®Google Scholar
• Cao X, Bloomston M, Zhang T, Frankel WL, Jia G, et al.: Synergistic antipancreatic tumor effect by simultaneously targeting hypoxic cancer cells with HSP90 inhibitor and glycolysis inhibitor. Clin Cancer Res 14, 1831–1839, 2008.
   PubMed Web of Science ®Google Scholar
• Bégin ME, Ells G, Das UN, and Horrobin DF: Differential killing of human carcinoma cells supplemented with n-3 and n-6 polyunsaturated fatty acids. J Natl Cancer Inst 77, 1053–1062, 1986.
   PubMed Web of Science ®Google Scholar
• Richter K, Moser S, Hagn F, Friedrich R, Hainzl O, et al.: Intrinsic inhibition of the Hsp90 ATPase activity. J Biol Chem 281, 11301–11311, 2006.
   PubMed Web of Science ®Google Scholar
• Ding W-Q and Lind SE: Phospholipid hydroperoxide glutathione peroxidase plays a role in protecting cancer cells from docosahexaenoic acid-induced cytotoxicity. Mol Cancer Ther 6, 1467–1474, 2007.
   PubMed Web of Science ®Google Scholar
• Chapkin RS, Wang N, Fan Y-Y, Lupton JR, and Prior IA: Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochim Biophys Acta 1778, 466–471, 2008.
   PubMed Web of Science ®Google Scholar
• Zagzag D, Lukyanov Y, Lan L, Ali MA, Esencay M, et al.: Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab Invest 86, 1221–1232, 2006.
   PubMed Web of Science ®Google Scholar
• Biondo PD, Brindley DN, Sawyer MB, and Field CJ: The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy. J Nutr Biochem 19, 787–796, 2008.
   PubMed Web of Science ®Google Scholar
• Menendez JA, Lupu R, and Colomer R: Exogenous supplementation with omega-3 polyunsaturated fatty acid docosahexaenoic acid (DHA; 22:6n-3) synergistically enhances taxane cytotoxicity and downregulates Her-2/neu (c-erbB-2) oncogene expression in human breast cancer cells. Eur J Cancer Prev 14, 263–270, 2005.
   PubMed Web of Science ®Google Scholar
• Cheng G, Zielonka J, Dranka BP, McAllister D, Mackinnon AC, et al.: Mitochondria-targeted drugs synergize with 2-deoxyglucose to trigger breast cancer cell death. Cancer Res 72, 2634–2644, 2012.
   PubMed Web of Science ®Google Scholar
• Menéndez J and Vázquez-Martín A: HER2 (erbB-2)-targeted effects of the omega-3 polyunsaturated fatty acid, alpha-linolenic acid (ALA; 18:3n-3), in breast cancer cells: the “fat features” of the “Mediterranean diet” as an “anti-HER2 cocktail”. Clin Transl Oncol 8, 812–820, 2006.
   PubMedGoogle Scholar
• Sreedhar AS, Soti C, and Csermely P: Inhibition of Hsp90: a new strategy for inhibiting protein kinases. Biochim Biophys Acta 1697, 233–242, 2004.
   PubMed Web of Science ®Google Scholar
• Mitri Z, Constantine T, and O'Regan R: The HER2 receptor in breast cancer: Pathophysiology, clinical use, and new advances in therapy. Chemother Res Pract 2012, 743193, 2012.
   PubMedGoogle Scholar
• Corps AN, Pozzan T, Hesketh TR, and Metacalfe JC: cis-Unsaturated fatty acids inhibit cap formation on lymphocytes by depleting cellular ATP. J Biol Chem 255, 10566–10568, 1980.
   PubMed Web of Science ®Google Scholar
• Banerji U: Heat shock protein 90 as a drug target: some like it hot. Clin Cancer Res 15, 9–14, 2009.
   PubMed Web of Science ®Google Scholar
• Schley PD, Brindley DN, and Field CJ: (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. J Nutr 137, 548–553, 2007.
   PubMed Web of Science ®Google Scholar
• Whitesell L and Cook P: Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells. Mol Endocrinol 10, 705–712, 1996.
   PubMed Web of Science ®Google Scholar
• Subik K, Lee J, and Baxter L: The expression patterns of ER, PR, HER2, CK5/6, EGFR, Ki-67 and AR by immunohistochemical analysis in breast cancer cell lines. Breast cancer basic Clin Res 4, 35–41, 2010.
   PubMedGoogle Scholar
• Jenski LJ, Sturdevant LK, Ehringer WD, and Stillwell W: Omega 3 fatty acids increase spontaneous release of cytosolic components from tumor cells. Lipids 26, 353–358, 1991.
   PubMed Web of Science ®Google Scholar
• Stanley WC, Khairallah RJ, and Dabkowski ER: Update on lipids and mitochondrial function: impact of dietary n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 15, 122–126, 2012.
   PubMed Web of Science ®Google Scholar
• Madsen L, Frøyland L, Dyrøy E, Helland K, and Berge RK: Docosahexaenoic and eicosapentaenoic acids are differently metabolized in rat liver during mitochondria and peroxisome proliferation. J Lipid Res 39, 583–593, 1998.
   PubMed Web of Science ®Google Scholar
• Whitesell L, Mimnaugh EG, De Costa B, Myers CE, and Neckers LM: Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci U S A 91, 8324–8328, 1994.
   PubMed Web of Science ®Google Scholar
• Burstein HJ: The distinctive nature of HER2-positive breast cancers. N Engl J Med 353, 1652–1654, 2005.
   PubMed Web of Science ®Google Scholar
• Dunn JE: Cancer epidemiology in populations of the United States—with emphasis on Hawaii and California—and Japan. Cancer Res 35, 3240–3245, 1975.
   PubMed Web of Science ®Google Scholar
• Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, et al.: C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43–54, 2001.
   PubMed Web of Science ®Google Scholar
• Falchook GS, Wheler JJ, Naing A, Jackson EF, Janku F, et al.: Targeting hypoxia-inducible factor-1α (HIF-1α) in combination with antiangiogenic therapy: a phase I trial of bortezomib plus bevacizumab. Oncotarget 5, 10280–10292, 2014.
   PubMed Web of Science ®Google Scholar
• Grenert JP, Johnson BD, and Toft DO: The Importance of ATP Binding and Hydrolysis by Hsp90 in Formation and Function of Protein Heterocomplexes. J Biol Chem 274, 17525–17533, 1999.
   PubMed Web of Science ®Google Scholar
• Srinivasan S and Dunn JF: Stabilization of hypoxia-inducible factor-1α in buffer containing cobalt chloride for Western blot analysis. Anal Biochem 416, 120–122, 2011.
   PubMed Web of Science ®Google Scholar
• Pelicano H, Martin DS, Xu R-H, and Huang P: Glycolysis inhibition for anticancer treatment. Oncogene 25, 4633–4646, 2006.
   PubMed Web of Science ®Google Scholar
• Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3, 721–732, 2003.
   PubMed Web of Science ®Google Scholar
• Tan M and Yu D: Molecular mechanisms of erbB2-mediated breast cancer chemoresistance. Adv Exp Med Biol 608, 119–129, 2007.
   PubMed Web of Science ®Google Scholar
• Narayanan BA, Narayanan NK, and Reddy BS: Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells. Int J Oncol 19, 1255–1262, 2001.
   PubMed Web of Science ®Google Scholar
• de Kok JB, Roelofs RW, Giesendorf BA, Pennings JL, Waas ET, et al.: Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes. Lab Invest 85, 154–159, 2005.
   PubMed Web of Science ®Google Scholar
• Neckers L: Heat shock protein 90: the cancer chaperone. J Biosci 32, 517–530, 2007.
   PubMed Web of Science ®Google Scholar
• Peng X, Guo X, Borkan SC, Bharti A, Kuramochi Y, et al.: Heat shock protein 90 stabilization of ErbB2 expression is disrupted by ATP depletion in myocytes. J Biol Chem 280, 13148–13152, 2005.
   PubMed Web of Science ®Google Scholar
• Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, et al.: Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239–250, 1997.
   PubMed Web of Science ®Google Scholar
• Stebbins CL, Stice JP, Hart CM, Mbai FN, and Knowlton AA: Effects of dietary decosahexaenoic acid (DHA) on eNOS in human coronary artery endothelial cells. J Cardiovasc Pharmacol Ther 13, 261–268, 2008.
   PubMed Web of Science ®Google Scholar
• Korb V, Tep K, Escriou V, Richard C, Scherman D, et al.: Current data on ATP-containing liposomes and potential prospects to enhance cellular energy status for hepatic applications. Crit Rev Ther Drug Carrier Syst 25, 305–345, 2008.
   PubMed Web of Science ®Google Scholar
• Chiu LC-M, Wong EY-L, and Ooi VEC: Docosahexaenoic acid from a cultured microalga inhibits cell growth and induces apoptosis by upregulating Bax/Bcl-2 ratio in human breast carcinoma MCF-7 cells. Ann N Y Acad Sci 1030, 361–368, 2004.
   PubMed Web of Science ®Google Scholar
• Watkins SM, Carter LC, and German JB: Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production. J Lipid Res 39, 1583–1588, 1998.
   PubMed Web of Science ®Google Scholar
• Rogers KR, Kikawa KD, Mouradian M, Hernandez K, McKinnon KM, et al.: Docosahexaenoic acid alters epidermal growth factor receptor-related signaling by disrupting its lipid raft association. Carcinogenesis 31, 1523–1530, 2010.
   PubMed Web of Science ®Google Scholar
• Gschwind A, Fischer OOM, and Ullrich A: The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 4, 1–10, 2004.
   Web of Science ®Google Scholar
• Hiltunen JK, Filppula SA, Koivuranta KT, Siivari K, Qin YM, et al.: Peroxisomal beta-oxidation and polyunsaturated fatty acids. Ann N Y Acad Sci 804, 116–128, 1996.
   PubMed Web of Science ®Google Scholar
• Clem B, Telang S, Clem A, Yalcin A, Meier J, et al.: Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Ther 7, 110–120, 2008.
   PubMed Web of Science ®Google Scholar
• Koppenol WH, Bounds PL, and Dang CV: Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 11, 325–337, 2011.
   PubMed Web of Science ®Google Scholar
• Pepe S and McLennan PL: (n-3) Long chain PUFA dose-dependently increase oxygen utilization efficiency and inhibit arrhythmias after saturated fat feeding in rats. J Nutr 137, 2377–2383, 2007.
   PubMed Web of Science ®Google Scholar
• Bégin ME, Ells G, and Horrobin DF: Polyunsaturated fatty acid-induced cytotoxicity against tumor cells and its relationship to lipid peroxidation. J Natl Cancer Inst 80, 188–194, 1988.
   PubMed Web of Science ®Google Scholar
• Hynes NE, Gschwind A, Fischer O, Ullrich A, Slamon D, et al.: ErbB2: From an EGFR relative to a central target for cancer therapy. Cancer Res 76, 3659–3662, 2016.
   PubMed Web of Science ®Google Scholar
• Madsen L, Rustan AC, Vaagenes H, Berge K, Dyrøy E, et al.: Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 34, 951–963, 1999.
   PubMed Web of Science ®Google Scholar
• Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408, 2001.
   PubMed Web of Science ®Google Scholar
• Mouradian M, Kikawa KD, Dranka BP, Komas SM, Kalyanaraman B, et al.: Docosahexaenoic acid attenuates breast cancer cell metabolism and the Warburg phenotype by targeting bioenergetic function. Mol Carcinog 54, 810–820, 2015.
   PubMed Web of Science ®Google Scholar
• Mouradian M, Kikawa KD, Johnson ED, Beck KL, and Pardini RS: Key roles for GRB2-associated-binding protein 1, phosphatidylinositol-3-kinase, cyclooxygenase 2, prostaglandin E2 and transforming growth factor alpha in linoleic acid-induced upregulation of lung and breast cancer cell growth. Prostaglandins Leukot Essent Fatty Acids 90, 105–115, 2014.
   PubMed Web of Science ®Google Scholar
• Klausner RD, Bhalla DK, Dragsten P, Hoover RL, and Karnovsky MJ: Model for capping derived from inhibition of surface receptor capping by free fatty acids. Proc Natl Acad Sci U S A 77, 437–441, 1980.
   PubMed Web of Science ®Google Scholar
• Hsu P and Sabatini D: Cancer cell metabolism: Warburg and beyond. Cell 134, 703–707, 2008.
   PubMed Web of Science ®Google Scholar
• Pardini RS, Wilson D, Schiff S, and Bajo SA, Pierce R: Nutritional intervention with omega-3 Fatty acids in a case of malignant fibrous histiocytoma of the lungs. 2005.
   Google Scholar
• Maloney A and Workman P: HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin Biol Ther 2, 3–24, 2002.
   PubMed Web of Science ®Google Scholar
• Calder PC: n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83, 1505S–1519S, 2006.
   PubMed Web of Science ®Google Scholar
• Kato T, Hancock RL, Mohammadpour H, McGregor B, Manalo P, et al.: Influence of omega-3 fatty acids on the growth of human colon carcinoma in nude mice. Cancer Lett 187, 169–177, 2002.
   PubMed Web of Science ®Google Scholar
• Wick AN, Drury DR, Nakada HI, and Wolfe JB: Localization of the primary metabolic block produced by 2-deoxyglucose. J Biol Chem 224, 963–969, 1957.
   PubMed Web of Science ®Google Scholar
• Kikawa KD, Noah T, Ahwah SM, and Pardini RS: Docosahexaenoic Acid (DHA) Induces P53-dependent growth inhibition in transformed colon and lung cell lines expressing wildtype P53. J Cancer Sci Ther 3, 1–4, 2010.
   Google Scholar
• Neckers L and Ivy SP: Heat shock protein 90. Curr Opin Oncol 15, 419–424, 2003.
   PubMed Web of Science ®Google Scholar
• Stillwell W, Ehringer W, and Jenski LJ: Docosahexaenoic acid increases permeability of lipid vesicles and tumor cells. Lipids 28, 103–108, 1993.
   PubMed Web of Science ®Google Scholar
• Lee EJ, Yun U-J, Koo KH, Sung JY, Shim J, et al.: Down-regulation of lipid raft-associated onco-proteins via cholesterol-dependent lipid raft internalization in docosahexaenoic acid-induced apoptosis. Biochim Biophys Acta 1841, 190–203, 2014.
   PubMed Web of Science ®Google Scholar
• Wiech H, Buchner J, Zimmermann R, and Jakob U: Hsp90 chaperones protein folding in vitro. Nature 358, 169–170, 1992.
   PubMed Web of Science ®Google Scholar
• Calviello G, Di Nicuolo F, Gragnoli S, Piccioni E, Serini S, et al.: n-3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1alpha induction pathway. Carcinogenesis 25, 2303–2310, 2004.
   PubMed Web of Science ®Google Scholar
• Kato T, Kolenic N, and Pardini RS: Docosahexaenoic acid (DHA), a primary tumor suppressive omega-3 fatty acid, inhibits growth of colorectal cancer independent of p53 mutational status. Nutr Cancer 58, 178–187, 2007.
   PubMed Web of Science ®Google Scholar
• Savino M, Garrubba M, Parrella P, Baorda F, Copetti M, et al.: Development of real-time quantitative reverse transcription-PCR for Her2 detection in peripheral blood from patients with breast cancer. Clin Chim Acta 384, 52–56, 2007.
   PubMed Web of Science ®Google Scholar
• Scatena R, Bottoni P, Pontoglio A, Mastrototaro L, and Giardina B: Glycolytic enzyme inhibitors in cancer treatment. Expert Opin Investig Drugs 17, 1533–1545, 2008.
   PubMed Web of Science ®Google Scholar
• Stravopodis DJ, Margaritis LH, and Voustinas GE: Drug-mediated targeted disruption of multiple protein activities through functional inhibition of the Hsp90 chaperone complex. Curr Med Chem 14, 3122–3138, 2007.
   PubMed Web of Science ®Google Scholar
• Pepe S and McLennan P: Modulation of myocardial oxygen requirements by dietary lipids in the isolated erythrocyte perfused working rat heart. J Mol Cell Cardiol 24, 1992, 1992.
   Google Scholar
• Lianos GD, Alexiou GA, Mangano A, Mangano A, Rausei S, et al.: The role of heat shock proteins in cancer. Cancer Lett 360, 114–118, 2015.
   PubMed Web of Science ®Google Scholar
• Singh JC, Jhaveri K, and Esteva FJ: HER2-positive advanced breast cancer: optimizing patient outcomes and opportunities for drug development. Br J Cancer 111, 1888–1898, 2014.
   PubMed Web of Science ®Google Scholar
• Kikawa KD, Herrick JS, Tateo RE, Mouradian M, Tay JS, et al.: Induced oxidative stress and cell death in the A549 lung adenocarcinoma cell line by ionizing radiation is enhanced by supplementation with docosahexaenoic acid. Nutr Cancer 62, 1017–1024, 2010.
   PubMed Web of Science ®Google Scholar
• Pardini RS: Nutritional intervention with omega-3 fatty acids enhances tumor response to anti-neoplastic agents. Chem Biol Interact 162, 89–105, 2006.
   PubMed Web of Science ®Google Scholar