Overexpression of Lon contributes to survival and aggressive phenotype of cancer cells through mitochondrial complex I-mediated generation of reactive oxygen species

Cell Death and Disease

Volumn 4, Issue 6, 2013, Pages

  Cheng, C W ^a   Kuo, C Y ^a   Fan, C C ^b,c   Fang, W C ^a   Jiang, S S ^a   Lo, Y K ^a   Wang, T Y ^b   Kao, M C ^d   Lee, A Y L ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

^c YUANPEI UNIVERSITY   (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

cell survival; lon protease; mitochondria; reactive oxygen species (ROS); tumorigenesis

Indexed keywords

CASPASE 3; ENDOPEPTIDASE LA; MITOGEN ACTIVATED PROTEIN KINASE; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER SURVIVAL; CARCINOGENESIS; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; LUNG NON SMALL CELL CANCER; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

EID: 84879678155     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.204     Document Type: Article

References (56)

1. Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria in cancer cells: what is so special about them? Trends Cell Biol 2008; 18: 165-173.
2. Ralph SJ, Rodriguez-Enriquez S, Neuzil J, Saavedra E, Moreno-Sanchez R. The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation-why mitochondria are targets for cancer therapy. Mol Aspects Med 2010; 31: 145-170.
3. Galluzzi L, Morselli E, Kepp O, Vitale I, Rigoni A, Vacchelli E et al. Mitochondrial gateways to cancer. Mol Aspects Med 2010; 31: 1-20.
4. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998; 281: 1309-1312.
5. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
6. Stowe DF, Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 2009; 11: 1373-1414.
7. Pan JS, Hong MZ, Ren JL. Reactive oxygen species: a double-edged sword in oncogenesis. World J Gastroenterol 2009; 15: 1702-1707.
8. Schumacker PT. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 2006; 10: 175-176.
9. Lee HC, Wei YH. Mitochondrial DNA instability and metabolic shift in human cancers. Int J Mol Sci 2009; 10: 674-701.
10. Hamanaka RB, Chandel NS. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 2010; 35: 505-513.
11. Wu WS. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev 2006; 25: 695-705.
12. Runchel C, Matsuzawa A, Ichijo H. Mitogen-activated protein kinases in mammalian oxidative stress responses. Antioxid Redox Signal 2011; 15: 205-218.
13. Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 2004; 23: 2838-2849.
14. Hong J, Zhou J, Fu J, He T, Qin J, Wang L et al. Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness. Cancer Res 2011; 71: 3980-3990.
15. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549.
16. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, Lopez M et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 2010; 107: 8788-8793.
17. Lee AY, Hsu CH, Wu SH. Functional domains of Brevibacillus thermoruber lon protease for oligomerization and DNA binding: role of N-terminal and sensor and substrate discrimination domains. J Biol Chem 2004; 279: 34903-34912.
18. Venkatesh S, Lee J, Singh K, Lee I, Suzuki CK. Multitasking in the mitochondrion by the ATP-dependent Lon protease. Biochim Biophys Acta 2012; 1823: 56-66.
19. Bota DA, Davies KJ. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 2002; 4: 674-680.
20. Matsushima Y, Goto Y, Kaguni LS. Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). Proc Natl Acad Sci USA 2010; 107: 18410-18415.
21. Hori O, Ichinoda F, Tamatani T, Yamaguchi A, Sato N, Ozawa K et al. Transmission of cell stress from endoplasmic reticulum to mitochondria: enhanced expression of Lon protease. J Cell Biol 2002; 157: 1151-1160.
22. Bota DA, Ngo JK, Davies KJ. Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic Biol Med 2005; 38: 665-677.
23. Wang HM, Cheng KC, Lin CJ, Hsu SW, Fang WC, Hsu TF et al. Obtusilactone A and (-)-sesamin induce apoptosis in human lung cancer cells by inhibiting mitochondrial Lon protease and activating DNA damage checkpoints. Cancer Sci 2010; 101: 2612-2620.
24. Ngo JK, Davies KJ. Mitochondrial Lon protease is a human stress protein. Free Radic Biol Med 2009; 46: 1042-1048.
25. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007; 129: 111-122.
26. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004; 6: 1-6.
27. Su LJ, Chang CW, Wu YC, Chen KC, Lin CJ, Liang SC et al. Selection of DDX5 as a novel internal control for Q-RT-PCR from microarray data using a block bootstrap re-sampling scheme. BMC Genomics 2007; 8: 140.
28. Landi MT, Dracheva T, Rotunno M, Figueroa JD, Liu H, Dasgupta A et al. Gene expression signature of cigarette smoking and its role in lung adenocarcinoma development and survival. PLoS One 2008; 3: e1651.
29. Fulda S, Gorman AM, Hori O, Samali A. Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010 214074.
30. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW et al. Hypoxiamediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996; 379: 88-91.
31. Zhou X, Ferraris JD, Burg MB. Mitochondrial reactive oxygen species contribute to high NaCl-induced activation of the transcription factor TonEBP/OREBP. Am J Physiol Renal Physiol 2006; 290: F1169-F1176.
32. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Ann Rev Biochem 2006; 75: 69-92.
33. Bayot A, Basse N, Lee I, Gareil M, Pirotte B, Bulteau AL et al. Towards the control of intracellular protein turnover: mitochondrial Lon protease inhibitors versus proteasome inhibitors. Biochimie 2008; 90: 260-269.
34. Bayot A, Gareil M, Rogowska-Wrzesinska A, Roepstorff P, Friguet B, Bulteau AL. Identification of novel oxidized protein substrates and physiological partners of the mitochondrial ATP-dependent Lon-like protease Pim1. J Biol Chem 2010; 285: 11445-11457.
35. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 2003; 3: 11-22.
36. Pani G, Galeotti T, Chiarugi P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev 2010; 29: 351-378.
37. Cannito S, Novo E, Compagnone A, Valfre di Bonzo L, Busletta C, Zamara E et al. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 2008; 29: 2267-2278.
38. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S et al. Epithelialmesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010; 101: 293-299.
39. Varambally S, Yu J, Laxman B, Rhodes DR, Mehra R, Tomlins SA et al. Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 2005; 8: 393-406.
40. Ruan K, Song G, Ouyang G. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 2009; 107: 1053-1062.
41. Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 2006; 31: 164-172.
42. Jego G, Hazoume A, Seigneuric R, Garrido C. Targeting heat shock proteins in cancer. Cancer Lett 2010; 332: 275-285.
43. Korde AS, Yadav VR, Zheng YM, Wang YX. Primary role of mitochondrial Rieske ironsulfur protein in hypoxic ROS production in pulmonary artery myocytes. Free Radic Biol Med 2011; 50: 945-952.
44. Guillon B, Bulteau AL, Wattenhofer-Donze M, Schmucker S, Friguet B, Puccio H et al. Frataxin deficiency causes upregulation of mitochondrial Lon and ClpP proteases and severe loss of mitochondrial Fe-S proteins. Febs J 2009; 276: 1036-1047.
45. Major T, von Janowsky B, Ruppert T, Mogk A, Voos W. Proteomic analysis of mitochondrial protein turnover: identification of novel substrate proteins of the matrix protease pim1. Mol Cell Biol 2006; 26: 762-776.
46. Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BB. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 2012; 16: 1295-1322.
47. Wada T, Stepniak E, Hui L, Leibbrandt A, Katada T, Nishina H et al. Antagonistic control of cell fates by JNK and p38-MAPK signaling. Cell Death Differ 2008; 15: 89-93.
48. Kim MS, Lee EJ, Kim HR, Moon A. p38 kinase is a key signaling molecule for H-Rasinduced cell motility and invasive phenotype in human breast epithelial cells. Cancer Res 2003; 63: 5454-5461.
49. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006; 160: 1-40.
50. Tapia PC. Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: "Mitohormesis" for health and vitality. Med Hypotheses 2006; 66: 832-843.
51. Ristow M, Zarse K. How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 2010; 45: 410-418.
52. Chang SE, Foster S, Betts D, Marnock WE. DOK, a cell line established from human dysplastic oral mucosa, shows a partially transformed non-malignant phenotype. Int J Cancer 1992; 52: 896-902.
53. Lu YC, Chen YJ, Wang HM, Tsai CY, Chen WH, Huang YC et al. Oncogenic function and early detection potential of miRNA-10b in oral cancer as identified by microRNA profiling. Cancer Prev Res 2012; 5: 665-674.
54. Masutomi K, Yu EY, Khurts S, Ben-Porath I, Currier JL, Metz GB et al. Telomerase maintains telomere structure in normal human cells. Cell 2003; 114: 241-253.
55. Granot Z, Kobiler O, Melamed-Book N, Eimerl S, Bahat A, Lu B et al. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol Endocrinol 2007; 21: 2164-2177.
56. Liu E, Lee AY, Chiba T, Olson E, Sun P, Wu X. The ATR-mediated S phase checkpoint prevents rereplication in mammalian cells when licensing control is disrupted. J Cell Biol 2007; 179: 643-657.