Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression

Journal of Clinical Investigation

Volumn 123, Issue 3, 2013, Pages 1068-1081

  Santidrian, Antonio F ^a   Matsuno Yagi, Akemi ^a   Ritland, Melissa ^a   Seo, Byoung B ^a,b   LeBoeuf, Sarah E ^a   Gay, Laurie J ^a   Yagi, Takao ^a   Felding Habermann, Brunhilde ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Daegu University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG METASTASIS; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; OXIDATION REDUCTION STATE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TUMOR XENOGRAFT;

ACRYLAMIDES; ANIMALS; AUTOPHAGY; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; DISEASE PROGRESSION; ELECTRON TRANSPORT COMPLEX I; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, SCID; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; NAD; NEOPLASM TRANSPLANTATION; NIACIN; NIACINAMIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PIPERIDINES; PROTEIN TRANSPORT; PROTEINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84874635096     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64264     Document Type: Article

References (63)

1. Dawood S, Broglio K, Buzdar AU, Hortobagyi GN, Giordano SH. Prognosis of women with metastatic breast cancer by HER2 status and trastuzumab treatment: an institutional-based review. J Clin Oncol. 2010;28(1):92-98.
2. Polyak K. Heterogeneity in breast cancer. J Clin Invest. 2011;121(10):3786-3788.
3. Warburg O. On respiratory impairment in cancer cells. Science. 1956;124(3215):269-270.
4. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009; 324(5930):1029-1033.
5. Schwartz JP, Passonneau JV, Johnson GS, Pastan I. The effect of growth conditions on NAD+ and NADH concentrations and the NAD+:NADH ratio in normal and transformed fibroblasts. J Biol Chem. 1974;249(13):4138-4143.
6. Brandon M, Baldi P, Wallace DC. Mitochondrial mutations in cancer. Oncogene. 2006; 25(34):4647-4662. (Pubitemid 44187615)
7. Ishikawa K, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science. 2008;320(5876):661-664. (Pubitemid 351928347)
8. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005;39:359-407. (Pubitemid 43011120)
9. Kulawiec M, Owens KM, Singh KK. Cancer cell mitochondria confer apoptosis resistance and promote metastasis. Cancer Biol Ther. 2009;8(14):1378-1385.
10. Ma Y, Bai RK, Trieu R, Wong LJ. Mitochondrial dysfunction in human breast cancer cells and their transmitochondrial cybrids. Biochim Biophys Acta. 2010;1797(1):29-37.
11. Shen L, et al. Evaluating mitochondrial DNA in patients with breast cancer and benign breast disease. J Cancer Res Clin. Oncol. 2011;137(4):669-675.
12. Carew JS, Huang P. Mitochondrial defects in cancer. Mol Cancer. 2002;1:9.
13. Parrella P, et al. Detection of mitochondrial DNA mutations in primary breast cancer and fine-needle aspirates. Cancer Res. 2001;61(20):7623-7626. (Pubitemid 32995057)
14. Mayr JA, et al. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res. 2008;14(8):2270-2275. (Pubitemid 351551057)
15. Chambers AF. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res. 2009; 69(13):5292-5293.
16. Fendt L, et al. Accumulation of mutations over the entire mitochondrial genome of breast cancer cells obtained by tissue microdissection. Breast Cancer Res Treat. 2011;128(2):327-336.
17. De VS, Van WR, Grivell LA, Marres CA. Primary structure and import pathway of the rotenoneinsensitive NADH-ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae. Eur J Biochem. 1992;203(3):587-592.
18. Seo BB, Kitajima-Ihara T, Chan EK, Scheffler IE, Matsuno-Yagi A, Yagi T. Molecular remedy of complex I defects: rotenone-insensitive internal NADHquinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc Natl Acad Sci U S A. 1998;95(16):9167-9171.
19. Seo BB, Wang J, Flotte TR, Yagi T, Matsuno-Yagi A. Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex I defects in human cells. J Biol Chem. 2000;275(48):37774-37778. (Pubitemid 32004893)
20. Marella M, Seo BB, Flotte TR, Matsuno-Yagi A, Yagi T. No immune responses by the expression of the yeast Ndi1 protein in rats. PLoS One. 2011; 6(10):e25910.
21. Barber-Singh J, Seo BB, Nakamaru-Ogiso E, Lau YS, Matsuno-Yagi A, Yagi T. Neuroprotective effect of long-term NDI1 gene expression in a chronic mouse model of Parkinson disorder. Rejuvenation Res. 2009;12(4):259-267.
22. Marella M, Seo BB, Thomas BB, Matsuno-Yagi A, Yagi T. Successful amelioration of mitochondrial optic neuropathy using the yeast NDI1 gene in a rat animal model. PLoS One. 2010;5(7):e11472.
23. Perry CN, Huang C, Liu W, Magee N, Carreira RS, Gottlieb RA. Xenotransplantation of mitochondrial electron transfer enzyme, Ndi1, in myocardial reperfusion injury. PLoS One. 2011;6(2):e16288.
24. Sanz A, et al. Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc Natl Acad Sci U S A. 2010;107(20):9105-9110.
25. Sharma LK, Fang H, Liu J, Vartak R, Deng J, Bai Y. Mitochondrial respiratory complex I dysfunction promotes tumorigenesis through ROS alteration and AKT activation. Hum Mol Genet. 2011; 20(23):4605-4616.
26. Pagniez-Mammeri H, Loublier S, Legrand A, Bénit P, Rustin P, Slama A. Mitochondrial complex I deficiency of nuclear origin I. Structural genes. Mol Genet Metab. 2012;105(2):163-172.
27. Mathew R, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell. 2009; 137(6):1062-1075.
28. Mathew R, White E. Autophagy in tumorigenesis and energy metabolism: friend by day, foe by night. Curr Opin Genet Dev. 2011;21(1):113-119.
29. Kenific CM, Thorburn A, Debnath J. Autophagy and metastasis: another double-edged sword. Curr Opin Cell Biol. 2010;22(2):241-245.
30. Klionsky DJ, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4(2):151-175. (Pubitemid 351231180)
31. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000; 290(5497):1717-1721. (Pubitemid 32004796)
32. Koch-Nolte F, Fischer S, Haag F, Ziegler M. Compartmentation of NAD+-dependent signalling. FEBS Lett. 2011;585(11):1651-1656.
33. Xu P, Sauve AA. Vitamin B3, the nicotinamide adenine dinucleotides and aging. Mech Ageing Dev. 2010;131(4):287-298.
34. Hasmann M, Schemainda I. FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res. 2003;63(21):7436-7442. (Pubitemid 37413486)
35. Brinkley BR, Beall PT, Wible LJ, Mace ML, Turner DS, Cailleau RM. Variations in cell form and cytoskeleton in human breast carcinoma cells in vitro. Cancer Res. 1980;40(9):3118-3129. (Pubitemid 10043512)
36. Chalkiadaki A, Guarente L. Sirtuins mediate mammalian metabolic responses to nutrient availability. Nat Rev Endocrinol. 2012;8(5):287-296.
37. Jang SY, Kang HT, Hwang ES. Nicotinamideinduced mitophagy: event mediated by high NAD+/NADH ratio and SIRT1 protein activation. J Biol Chem. 2012;287(23):19304-19314.
38. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992; 12(3):954-961.
39. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001; 193(6):727-740.
40. Yokota M, et al. Generation of trans-mitochondrial mito-mice by the introduction of a pathogenic G13997A mtDNA from highly metastatic lung carcinoma cells. FEBS Lett. 2010;584(18):3943-3948.
41. Dasgupta S, et al. Mitochondrial DNA mutations in respiratory complex-I in never-smoker lung cancer patients contribute to lung cancer progression and associated with EGFR gene mutation. J Cell Physiol. 2012;227(6):2451-2460.
42. Zimmermann FA, et al. Respiratory chain complex I is a mitochondrial tumor suppressor of oncocytic tumors. Front Biosci (Elite Ed). 2011;3:315-325.
43. Baracca A, Chiaradonna F, Sgarbi G, Solaini G, Alberghina L, Lenaz G. Mitochondrial Complex I decrease is responsible for bioenergetic dysfunction in K-ras transformed cells. Biochim Biophys Acta. 2010;1797(2):314-323.
44. Hu Y, et al. K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res. 2012;22(2):399-412.
45. Tu YF, Kaipparettu BA, Ma Y, Wong LJ. Mitochondria of highly metastatic breast cancer cell line MDA-MB-231 exhibits increased autophagic properties. Biochim Biophys Acta. 2011; 1807(9):1125-1132.
46. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol. 2011;12(1):21-35.
47. Wang B, Hasan MK, Alvarado E, Yuan H, Wu H, Chen WY. NAMPT overexpression in prostate cancer and its contribution to tumor cell survival and stress response. Oncogene. 2011;30(8):907-921.
48. Bajrami I, et al. Synthetic lethality of PARP and NAMPT inhibition in triple-negative breast cancer cells. EMBO Mol Med. 2012;4(10):1087-1096.
49. Schumacker PT. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell. 2006;10(3):175-176. (Pubitemid 44311072)
50. Kirkland JB. Niacin requirements for genomic stability. Mutat Res. 2012;733(1-2):14-20.
51. Pelicano H, et al. Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J Cell Biol. 2006;175(6):913-923. (Pubitemid 44969197)
52. Ghosh HS, McBurney M, Robbins PD. SIRT1 negatively regulates the mammalian target of rapamycin. PLoS One. 2010;5(2):e9199.
53. Pillai VB, et al. Exogenous NAD blocks cardiac hypertrophic response via activation of the SIRT3-LKB1-AMP-activated kinase pathway. J Biol Chem. 2010;285(5):3133-3144.
54. Lan F, Cacicedo JM, Ruderman N, Ido Y. SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem. 2008;283(41):27628- 27635.
55. Kume S, et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest. 2010;120(4):1043-1055.
56. Lee IH, et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A. 2008;105(9):3374-3379.
57. Donmez G, Guarente L. Aging and disease: connections to sirtuins. Aging Cell. 2010;9(2):285-290.
58. Zhang Q, Wang SY, Nottke AC, Rocheleau JV, Piston DW, Goodman RH. Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc Natl Acad Sci U S A. 2006;103(24):9029-9033. (Pubitemid 43902527)
59. Deng Y, et al. Redox-dependent Brca1 transcriptional regulation by an NADH-sensor CtBP1. Oncogene. 2010;29(50):6603-6608.
60. Di LJ, Fernandez AG, De SA, Longo DL, Gardner K. Transcriptional regulation of BRCA1 expression by a metabolic switch. Nat Struct Mol Biol. 2010; 17(12):1406-1413.
61. Merlo LM, Pepper JW, Reid BJ, Maley CC. Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006;6(12):924-935. (Pubitemid 44862677)
62. Chen EI, et al. Adaptation of energy metabolism in breast cancer brain metastases. Cancer Res. 2007; 67(4):1472-1486. (Pubitemid 46383371)
63. Trounce IA, Kim YL, Jun AS, Wallace DC. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 1996; 264:484-509.