High mitochondrial DNA copy number and bioenergetic function are associated with tumor invasion of esophageal squamous cell carcinoma cell lines

International Journal of Molecular Sciences

Volumn 13, Issue 9, 2012, Pages 11228-11246

  Lin, Chen Sung ^a,b   Lee, Hui Ting ^a,c   Lee, Shu Yu ^a,b   Shen, Yao An ^a   Wang, Liang Shun ^d   Chen, Yann Jang ^a   Wei, Yau Huei ^a,e  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e MACKAY MEDICAL COLLEGE   (Taiwan)

Author keywords

Bioenergetic function; Epithelial mesenchymal transition (EMT); Esophageal squamous cell carcinoma (ESCC); Invasion; Mitochondrial DNA (mtDNA)

Indexed keywords

ADENOSINE TRIPHOSPHATE; LACTATE DEHYDROGENASE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; SUCCINATE DEHYDROGENASE; UVOMORULIN; CADHERIN; DNA BINDING PROTEIN; MITOCHONDRIAL PROTEIN; TRANSCRIPTION FACTOR; VIMENTIN;

ARTICLE; BIOENERGY; BIOGENESIS; CANCER INVASION; CARCINOMA CELL; CELL MIGRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE SILENCING; GLYCOLYSIS; HUMAN; HUMAN CELL; NONHUMAN; OXYGEN CONSUMPTION; PHENOTYPE; PROTEIN CONTENT; PROTEIN EXPRESSION; BIOSYNTHESIS; DISEASE COURSE; ENERGY METABOLISM; ESOPHAGUS TUMOR; GENETICS; METABOLISM; MITOCHONDRION; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; TUMOR INVASION;

ADENOSINE TRIPHOSPHATE; CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DISEASE PROGRESSION; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; ENERGY METABOLISM; EPITHELIAL-MESENCHYMAL TRANSITION; ESOPHAGEAL NEOPLASMS; GENE DOSAGE; GENE KNOCKDOWN TECHNIQUES; HUMANS; L-LACTATE DEHYDROGENASE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEOPLASM INVASIVENESS; OXYGEN CONSUMPTION; TRANSCRIPTION FACTORS; VIMENTIN;

EID: 84866939677     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms130911228     Document Type: Article

References (48)

1. Li, J.Y.; Liu, B.Q.; Li, G.Y.; Chen, Z.J.; Sun, X.I.; Rong, S.D. Atlas of cancer mortality in the People's Republic of China. An aid for cancer control and research. Int. J. Epidemiol. 1981, 10, 127-133.
2. Li, J.Y. Cancer mapping as an epidemiologic research resource in China. Recent Results Cancer Res. 1989, 114, 115-136.
3. Law, S.; Wong, J. Esophageal cancer surgery: Lessons from 1200 resections. Hawaii Med. J. 2004, 63, 203-205.
4. Wu, I.C.; Lu, C.Y.; Kuo, F.C.; Tsai, S.M.; Lee, K.W.; Kuo, W.R.; Cheng, Y.J.; Kao, E.L.; Yang, M.S.; Ko, Y.C. Interaction between cigarette, alcohol and betel nut use on esophageal cancer risk in Taiwan. Eur. J. Clin. Invest. 2006, 36, 236-241.
5. Lin, C.S.; Chang, S.C.; Wei, Y.H.; Chou, T.Y.; Wu, Y.C.; Lin, H.C.; Wang, L.S.; Hsu, W.H. Prognostic variables in thoracic esophageal squamous cell carcinoma. Ann. Thorac. Surg. 2009, 87, 1056-1065.
6. Lin, C.S.; Chang, S.C.; Wang, L.S.; Chou, T.Y.; Hsu, W.H.; Wu, Y.C.; Wei, Y.H. The role of mitochondrial DNA alterations in esophageal squamous cell carcinomas. J. Thorac. Cardiovascular Surg. 2010, 139, 189-197.
7. Lee, H.C.; Wei, Y.H. Mitochondrial role in life and death of the cell. J. Biomed. Sci. 2000, 7, 2-15.
8. Lodish, H.; Berk, A.; Matsudaira, P.; Kaiser, C.A.; Krieger, M.; Scott, M.P.; Zipursky, S.L.; Darnell, J. Molecular Cell Biology; WH Freeman: New York, NY, USA, 2004; pp 301-347.
9. Warburg, O. On respiratory impairment in cancer cells. Science 1956, 124, 269-270.
10. Warburg, O. On the origin of cancer cells. Science 1956, 123, 309-314.
11. Warburg, O. Origin of cancer cells. Oncologia 1956, 9, 75-83.
12. Kim, J.W.; Dang, C.V. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 2006, 66, 8927-8930.
13. Chan, D.C. Mitochondria: Dynamic organelles in disease, aging, and development. Cell 2006, 125, 1241-1252.
14. Lee, H.C.; Wei, Y.H. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int. J. Biochem. Cell Biol. 2005, 37, 822-834.
15. Andrews, R.M.; Kubacka, I.; Chinnery, P.F.; Lightowlers, R.N.; Turnbull, D.M.; Howell, N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 1999, 23, 147.
16. Lecrenier, N.; Foury, F. New features of mitochondrial DNA replication system in yeast and man. Gene 2000, 246, 37-48.
17. Moraes, C.T. What regulates mitochondrial DNA copy number in animal cells? Trends Genet. 2001, 17, 199-205.
18. Asin-Cayuela, J.; Gustafsson, C.M. Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci. 2007, 32, 111-117.
19. Ekstrand, M.I.; Falkenberg, M.; Rantanen, A.; Park, C.B.; Gaspari, M.; Hultenby, K.; Rustin, P.; Gustafsson, C.M.; Larsson, N.G. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 2004, 13, 935-944.
20. Lee, H.C.; Yin, P.H.; Lin, J.C.; Wu, C.C.; Chen, C.Y.; Wu, C.W.; Chi, C.W.; Tam, T.N.; Wei, Y.H. Mitochondrial genome instability and mtDNA depletion in human cancers. Ann. N. Y. Acad. Sci. 2005, 1042, 109-122.
21. Wu, C.W.; Yin, P.H.; Hung, W.Y.; Li, A.F.; Li, S.H.; Chi, C.W.; Wei, Y.H.; Lee, H.C. Mitochondrial DNA mutations and mitochondrial DNA depletion in gastric cancer. Genes Chromosom. Cancer 2005, 44, 19-28.
22. Tseng, L.M.; Yin, P.H.; Chi, C.W.; Hsu, C.Y.; Wu, C.W.; Lee, L.M.; Wei, Y.H.; Lee, H.C. Mitochondrial DNA mutations and mitochondrial DNA depletion in breast cancer. Genes Chromosom. Cancer 2006, 45, 629-638.
23. Kim, M.M.; Clinger, J.D.; Masayesva, B.G.; Ha, P.K.; Zahurak, M.L.; Westra, W.H.; Califano, J.A. Mitochondrial DNA quantity increases with histopathologic grade in premalignant and malignant head and neck lesions. Clin. Cancer Res. 2004, 10, 8512-8515.
24. Hu, C.P.; Hsieh, H.G.; Chien, K.Y.; Wang, P.Y.; Wang, C.I.; Chen, C.Y.; Lo, S.J.; Wuu, K.D.; Chang, C.M. Biologic properties of three newly established human esophageal carcinoma cell lines. J. Natl. Cancer Inst. 1984, 72, 577-583.
25. Nishihira, T.; Hashimoto, Y.; Katayama, M.; Mori, S.; Kuroki, T. Molecular and cellular features of esophageal cancer cells. J. Cancer Res. Clin. Oncol. 1993, 119, 441-449.
26. Heddi, A.; Lestienne, P.; Wallace, D.C.; Stepien, G. Mitochondrial DNA expression in mitochondrial myopathies and coordinated expression of nuclear genes involved in ATP production. J. Biol. Chem. 1993, 268, 12156-12163.
27. Inoue, S.; Yokota, M.; Nakada, K.; Miyoshi, H.; Hayashi, J. Pathogenic mitochondrial DNA-induced respiration defects in hematopoietic cells result in anemia by suppressing erythroid differentiation. FEBS Lett. 2007, 581, 1910-1916.
28. Gladden, L.B. Lactate metabolism: A new paradigm for the third millennium. J. Physiol. 2004, 558, 5-30.
29. Goldman, R.D.; Kaplan, N.O.; Hall, T.C. Lactic dehydrogenase in human neoplastic tissues. Cancer Res. 1964, 24, 389-399.
30. Giatromanolaki, A.; Sivridis, E.; Gatter, K.C.; Turley, H.; Harris, A.L.; Koukourakis, M.I. Lactate dehydrogenase 5 (LDH-5) expression in endometrial cancer relates to the activated VEGF/VEGFR2(KDR) pathway and prognosis. Gynecol. Oncol. 2006, 103, 912-918.
31. Koukourakis, M.I.; Giatromanolaki, A.; Sivridis, E.; Gatter, K.C.; Harris, A.L. Lactate dehydrogenase 5 expression in operable colorectal cancer: Strong association with survival and activated vascular endothelial growth factor pathway-A report of the tumour angiogenesis research group. J. Clin. Oncol. 2006, 24, 4301-4308.
32. Koukourakis, M.I.; Giatromanolaki, A.; Sivridis, E.; Gatter, K.C.; Harris, A.L. Pyruvate dehydrogenase and pyruvate dehydrogenase kinase expression in non small cell lung cancer and tumor-associated stroma. Neoplasia N. Y. 2005, 7, 1-6.
33. Yilmaz, M.; Christofori, G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009, 28, 15-33.
34. Gogvadze, V.; Orrenius, S.; Zhivotovsky, B. Mitochondria in cancer cells: What is so special about them? Trends Cell Biol. 2008, 18, 165-173.
35. Gogvadze, V.; Zhivotovsky, B.; Orrenius, S. The Warburg effect and mitochondrial stability in cancer cells. Mol. Asp. Med. 2010, 31, 60-74.
36. Pedersen, P.L. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J. Bioenerget. Biomembr. 2007, 39, 211-222.
37. Gogvadze, V.; Zhivotovsky, B. Alteration of mitochondrial function and cell sensitization to death. J. Bioenerget. Biomembr. 2007, 39, 23-30.
38. DeBerardinis, R.J.; Cheng, T. Q's next: The diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 2010, 29, 313-324.
39. Liu, C.S.; Kuo, C.L.; Cheng, W.L.; Huang, C.S.; Lee, C.F.; Wei, Y.H. Alteration of the copy number of mitochondrial DNA in leukocytes of patients with hyperlipidemia. Ann. N. Y. Acad. Sci. 2005, 1042, 70-75.
40. Chomczynski, P.; Mackey, K. Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. BioTechniques 1995, 19, 942-945.
41. Chen, C.T.; Shih, Y.R.; Kuo, T.K.; Lee, O.K.; Wei, Y.H. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 2008, 26, 960-968.
42. Lin, C.S.; Wang, L.S.; Tsai, C.M.; Wei, Y.H. Low copy number and low oxidative damage of mitochondrial DNA are associated with tumor progression in lung cancer tissues after neoadjuvant chemotherapy. Interact. Cardio.Vasc. Thorac. Surg. 2008, 7, 954-958.
43. Ma, Y.S.; Wu, S.B.; Lee, W.Y.; Cheng, J.S.; Wei, Y.H. Response to the increase of oxidative stress and mutation of mitochondrial DNA in aging. Biochim. Biophys. Acta 2009, 1790, 1021-1029.
44. Bai, R.K.; Perng, C.L.; Hsu, C.H.; Wong, L.J. Quantitative PCR analysis of mitochondrial DNA content in patients with mitochondrial disease. Ann. N. Y. Acad. Sci. 2004, 1011, 304-309.
45. Chang, C.C.; Yang, S.H.; Chien, C.C.; Chen, S.H.; Pan, S.; Lee, C.L.; Lin, C.M.; Sun, H.L.; Huang, C.C.; Wu, Y.Y. et al. Clinical meaning of age-related expression of fecal cytokeratin 19 in colorectal malignancy. BMC Cancer 2009, 9, 376.
46. Jeng, J.Y.; Yeh, T.S.; Lee, J.W.; Lin, S.H.; Fong, T.H.; Hsieh, R.H. Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 2008, 103, 347-357.
47. Senger, D.R.; Perruzzi, C.A.; Streit, M.; Koteliansky, V.E.; de Fougerolles, A.R.; Detmar, M. The alpha(1)beta(1) and alpha(2)beta(1) integrins provide critical support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor angiogenesis. Am. J. Pathol. 2002, 160, 195-204.
48. Larson, E.M.; Doughman, D.J.; Gregerson, D.S.; Obritsch, W.F. A new, simple, nonradioactive, nontoxic in vitro assay to monitor corneal endothelial cell viability. Invest. Ophthalmol. Vis. Sci. 1997, 38, 1929-1933.