Nitric oxide is a positive regulator of the Warburg effect in ovarian cancer cells

Cell Death and Disease

Volumn 5, Issue 6, 2014, Pages

  Caneba, C A ^a,b   Yang, L ^a,b   Baddour, J ^a,b   Curtis, R ^a,b   Win, J ^a,b   Hartig, S ^c   Marini, J ^c   Nagrath, D ^a,b  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; ARGININE; CITRULLINE; CYTOCHROME C OXIDASE; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTIC ACID; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BREAST CANCER; CELL METABOLISM; CELL PROLIFERATION; GENE EXPRESSION; GLYCOLYSIS; MITOCHONDRIAL RESPIRATION; OVARY CANCER; OXYGEN CONSUMPTION; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; CITRIC ACID CYCLE; FEMALE; HUMAN; METABOLISM; MITOCHONDRION; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CITRIC ACID CYCLE; FEMALE; GLUTATHIONE; GLYCOLYSIS; HUMANS; MITOCHONDRIA; NADP; NITRIC OXIDE; OVARIAN NEOPLASMS; REACTIVE OXYGEN SPECIES;

EID: 84903764168     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.264     Document Type: Article

References (61)

1. Cannistra SA. Cancer of the ovary. N Engl J Med 2004; 351: 2519-2529.
2. Bast Jr RC, Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer 2009; 9: 415-428.
3. Rieder J, Jahnke R, Schloesser M, Seibel M, Czechowski M, Marth C et al. Nitric oxidedependent apoptosis in ovarian carcinoma cell lines. Gynecol Oncol 2001; 82: 172-176.
4. Chowdhury R, Godoy LC, Thiantanawat A, Trudel LJ, Deen WM, Wogan GN. Nitric oxide produced endogenously is responsible for hypoxia-induced HIF-1alpha stabilization in colon carcinoma cells. Chem Res Toxicol 2012; 25: 2194-2202.
5. Raharijaona M, Le Pennec S, Poirier J, Mirebeau-Prunier D, Rouxel C, Jacques C et al. PGC-1-related coactivator modulates mitochondrial-nuclear crosstalk through endogenous nitric oxide in a cellular model of oncocytic thyroid tumours. PLoS One 2009; 4: e7964.
6. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M et al. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci USA 2004; 101: 16507-16512.
7. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M et al. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals (Proc Natl Acad Sci USA 2004:101:16507-16512). Erratum in Proc Natl Acad Sci USA 2005; 102: 5635.
8. Le Pennec S, Mirebeau-Prunier D, Boutet-Bouzamondo N, Jacques C, Guillotin D, Lauret E et al. Nitric oxide and calcium participate in the fine regulation of mitochondrial biogenesis in follicular thyroid carcinoma cells. J Biol Chem 2011; 286: 18229-18239.
9. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003; 299: 896-899.
10. Sanuphan A, Chunhacha P, Pongrakhananon V, Chanvorachote P. Long-term nitric oxide exposure enhances lung cancer cell migration. Biomed Res Int 2013; 2013: 186972.
11. Pervin S, Singh R, Hernandez E, Wu G, Chaudhuri G. Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res 2007; 67: 289-299.
12. Cronauer MV, Ince Y, Engers R, Rinnab L, Weidemann W, Suschek CV et al. Nitric oxide-mediated inhibition of androgen receptor activity: possible implications for prostate cancer progression. Oncogene 2007; 26: 1875-1884.
13. Leist M, Single B, Naumann H, Fava E, Simon B, Kuhnle S et al. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 1999; 249: 396-403.
14. Kisley LR, Barrett BS, Bauer AK, Dwyer-Nield LD, Barthel B, Meyer AM et al. Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res 2002; 62: 6850-6856.
15. Aguilar-Melero P, Ferrin G, Muntane J. Effects of nitric oxide synthase-3 overexpression on post-translational modifications and cell survival in HepG2 cells. J Proteomics 2012; 75: 740-755.
16. Simeone AM, Broemeling LD, Rosenblum J, Tari AM. HER2/neu reduces the apoptotic effects of N-(4-hydroxyphenyl)retinamide (4-HPR) in breast cancer cells by decreasing nitric oxide production. Oncogene 2003; 22: 6739-6747.
17. Hussain SP, Trivers GE, Hofseth LJ, He P, Shaikh I, Mechanic LE et al. Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res 2004; 64: 6849-6853.
18. Garcia-Navas R, Munder M, Mollinedo F. Depletion of L-arginine induces autophagy as a cytoprotective response to endoplasmic reticulum stress in human T lymphocytes. Autophagy 2012; 8: 28.
19. Luiking YC, Ten Have GA, Wolfe RR, Deutz NE. Arginine de novo and nitric oxide production in disease states. Am J Physiol Endocrinol Metab 2012; 303: E1177-E1189.
20. Haines RJ, Pendleton LC, Eichler DC. Argininosuccinate synthase: at the center of arginine metabolism. Int J Biochem Mol Biol 2011; 2: 8-23.
21. Walters RG, Coin LJ, Ruokonen A, de Smith AJ, El-Sayed Moustafa JS, Jacquemont JS et al. Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity. PLoS One 2013; 8: e58048.
22. Yang TS, Lu SN, Chao Y, Sheen IS, Lin CC, Wang TE et al. A randomised phase II study of pegylated arginine deiminase (ADI-PEG 20) in Asian advanced hepatocellular carcinoma patients. Br J Cancer 2010; 103: 954-960.
23. Nicholson LJ, Smith PR, Hiller L, Szlosarek PW, Kimberley C, Sehouli J et al. Epigenetic silencing of argininosuccinate synthetase confers resistance to platinum-induced cell death but collateral sensitivity to arginine auxotrophy in ovarian cancer. Int J Cancer 2009; 125: 1454-1463.
24. Szlosarek PW, Grimshaw MJ, Wilbanks GD, Hagemann T, Wilson JL, Burke F et al. Aberrant regulation of argininosuccinate synthetase by TNF-alpha in human epithelial ovarian cancer. Int J Cancer 2007; 121: 6-11.
25. Nagrath D, Soto-Gutierrez A. Reply to: 'Is the pathway of energy metabolism modified in advanced cirrhosis?'. J Hepatol 2014; S0168-8278: 00303-1.
26. Nishikawa T, Bellance N, Damm A, Bing H, Zhu Z, Handa K et al. A switch in the source of ATP production and a loss in capacity to perform glycolysis are hallmarks of hepatocyte failure in advance liver disease. J Hepatol 2014; 60: 1203-1211.
27. Glasauer A, Sena LA, Diebold LP, Mazar AP, Chandel NS. Targeting SOD1 reduces experimental non-small-cell lung cancer. J Clin Invest 2014; 124: 117-128.
28. Mullen AR, Wheaton WW, Jin ES, Chen PH, Sullivan LB, Cheng T et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2012; 481: 385-388.
29. Metallo CM, Vander Heiden MG. Understanding metabolic regulation and its influence on cell physiology. Mol Cell 2013; 49: 388-398.
30. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, Hiller K et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2012; 481: 380-384.
31. Le A, Rajeshkumar NV, Maitra A, Dang CV. Conceptual framework for cutting the pancreatic cancer fuel supply. Clin Cancer Res 2012; 18: 4285-4290.
32. Lu C, Thompson CB. Metabolic regulation of epigenetics. Cell Metab 2012; 16: 9-17.
33. Nagrath D, Caneba C, Karedath T, Bellance N. Metabolomics for mitochondrial and cancer studies. Biochim Biophys Acta 2011; 1807: 650-663.
34. Wang F, Zhang R, Xia T, Hsu E, Cai Y, Gu Z et al. Inhibitory effects of nitric oxide on invasion of human cancer cells. Cancer Lett 2007; 257: 274-282.
35. De Vitto H, Mendonca BS, Elseth KM, Vesper BJ, Portari EA, Gallo CV et al. Part II. Mitochondrial mutational status of high nitric oxide adapted cell line BT-20 (BT-20-HNO) as it relates to human primary breast tumors. Tumour Biol 2013; 34: 337-347.
36. De Vitto H, Mendonca BS, Elseth KM, Onul A, Xue J, Vesper BJ et al. Part III. Molecular changes induced by high nitric oxide adaptation in human breast cancer cell line BT-20 (BT-20-HNO): a switch from aerobic to anaerobic metabolism. Tumour Biol 2013; 34: 403-413.
37. Sen S, Kawahara B, Chaudhuri G. Mitochondrial-associated nitric oxide synthase activity inhibits cytochrome c oxidase: implications for breast cancer. Free Radic Biol Med 2013; 57: 210-220.
38. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 1994; 345: 50-54.
39. Clementi E, Brown GC, Foxwell N, Moncada S. On the mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc Natl Acad Sci USA 1999; 96: 1559-1562.
40. Almeida A, Almeida J, Bolanos JP, Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA 2001; 98: 15294-15299.
41. Maletic SD, Dragicevic LM, Zikic RV, Stajn AS, Kostic MM. Effects of nitric oxide donor, isosorbide dinitrate, on energy metabolism of rat reticulocytes. Physiol Res 1999; 48: 417-427.
42. Li J, Hu X, Selvakumar P, Russell 3rd RR, Cushman SW, Holman GD et al. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol Endocrinol Metab 2004; 287: E834-E841.
43. Semenza GL. Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol 2000; 59: 47-53.
44. Caneba CA, Bellance N, Yang L, Pabst L, Nagrath D. Pyruvate uptake is increased in highly invasive ovarian cancer cells under anoikis conditions for anaplerosis, mitochondrial function, and migration. Am J Physiol Endocrinol Metab 2012; 303: E1036-E1052.
45. Yang L, Moss T, Mangala LS, Marini J, Zhao H, Wahlig S et al. Metabolic shifts toward glutamine regulate tumor growth, invasion and bioenergetics in ovarian cancer. Mol Syst Biol 2014; 10: 728.
46. Chung JS, Park S, Park SH, Park ER, Cha PH, Kim BY et al. Overexpression of Romo1 promotes production of reactive oxygen species and invasiveness of hepatic tumor cells. Gastroenterology 2012; 143: 1084-1094 e1087.
47. Hung WY, Huang KH, Wu CW, Chi CW, Kao HL, Li AF et al. Mitochondrial dysfunction promotes cell migration via reactive oxygen species-enhanced beta5-integrin expression in human gastric cancer SC-M1 cells. Biochim Biophys Acta 2012; 1820: 1102-1110.
48. Goh J, Enns L, Fatemie S, Hopkins H, Morton J, Pettan-Brewer C et al. Mitochondrial targeted catalase suppresses invasive breast cancer in mice. BMC Cancer 2011; 11: 191.
49. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res 2008; 68: 1777-1785.
50. Du Q, Zhang X, Liu Q, Bartels CE, Geller DA. Nitric oxide production upregulates Wnt/betacatenin signaling by inhibiting Dickkopf-1. Cancer Res 2013; 73: 6526-6537.
51. Bellows CF, Jaffe BM. Glutamine is essential for nitric oxide synthesis by murine macrophages. J Surg Res 1999; 86: 213-219.
52. Ni Y, Schwaneberg U, Sun ZH. Arginine deiminase, a potential anti-tumor drug. Cancer Lett 2008; 261: 1-11.
53. Kelly MP, Jungbluth AA,Wu BW, Bomalaski J, Old LJ, Ritter G. Arginine deiminase PEG20 inhibits growth of small cell lung cancers lacking expression of argininosuccinate synthetase. Br J Cancer 2012; 106: 324-332.
54. Kim RH, Coates JM, Bowles TL, McNerney GP, Sutcliffe J, Jung JU et al. Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis. Cancer Res 2009; 69: 700-708.
55. Feun LG, Marini A, Walker G, Elgart G, Moffat F, Rodgers SE et al. Negative argininosuccinate synthetase expression in melanoma tumours may predict clinical benefit from arginine-depleting therapy with pegylated arginine deiminase. Br J Cancer 2012; 106: 1481-1485.
56. Antunes F, Boveris A, Cadenas E. On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide. Proc Natl Acad Sci USA 2004; 101: 16774-16779.
57. Sen S, Kawahara B, Fry NL, Farias-Eisner R, Zhang D, Mascharak PK et al. A lightactivated NO donor attenuates anchorage independent growth of cancer cells: important role of a cross talk between NO and other reactive oxygen species. Arch Biochem Biophys 2013; 540: 33-40.
58. Maciag AE, Holland RJ, Robert Cheng YS, Rodriguez LG, Saavedra JE, Anderson LM et al. Nitric oxide-releasing prodrug triggers cancer cell death through deregulation of cellular redox balance. Redox Biol 2013; 1: 115-124.
59. Nakamura J, Asakura S, Hester SD, de Murcia G, Caldecott KW, Swenberg JA. Quantitation of intracellular NAD(P)H can monitor an imbalance of DNA single strand break repair in base excision repair deficient cells in real time. Nucleic Acids Res 2003; 31: e104.
60. Long AR, O'Brien CC, Malhotra K, Schwall CT, Albert AD, Watts A et al. A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol 2013; 13: 25.
61. Bonome T, Levine DA, Shih J, Randonovich M, Pise-Masison CA, Bogomolniy F et al. A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer Res 2008; 68: 5478-5486.