Loss of mitochondrial DNA enhances angiogenic and invasive potential of hepatoma cells

Oncology Reports

Volumn 23, Issue 3, 2010, Pages 779-786

  Cheon, Hwanju ^a,b   Moon, Hyo Eun ^b   Lee, Myung Shik ^b   Kim, Soung Soo ^a  

^a Yonsei University   (South Korea)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

Angiogenesis; Hypoxia inducible factor 2 ; mtDNA; Vascular endothelial growth factor

Indexed keywords

ETHIDIUM BROMIDE; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MATRIX METALLOPROTEINASE; MESSENGER RNA; MITOCHONDRIAL DNA; UROKINASE; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CANCER INVASION; CELL HYPOXIA; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE MUTATION; HEPATOMA CELL; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DNA, MITOCHONDRIAL; EXTRACELLULAR MATRIX PROTEINS; GENE DELETION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; MUTATION; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77349088713     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or-00000698     Document Type: Article

References (36)

1. Warburg O: On the origin of cancer cells. Science 123: 309-314, 1956.
2. Brandon M, Baldi P and Wallace DC: Mitochondrial mutations in cancer. Oncogene 25: 4647-4662, 2006.
3. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, Nakada K, Honma Y and Hayashi J: ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320: 661-664, 2008.
4. Ohta S: Contribution of somatic mutations in the mitochondrial genome to the development of cancer and tolerance against anticancer drugs. Oncogene 25: 4768-4776, 2006.
5. Petros JA, Baumann AK, Ruiz-Pesini E, Amin MB, Sun CQ, Hall J, Lim S, Issa MM, Flanders WD, Hosseini SH, Marshall FF and Wallace DC: mtDNA mutations increase tumorigenicity in prostate cancer. Proc Natl Acad Sci USA 102: 719-724, 2005.
6. Shidara Y, Yamagata K, Kanamori T, Nakano K, Kwong JQ, Manfredi G, Oda H and Ohta S: Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65: 1655-1663, 2005.
7. Moon HE, Cheon H, Chun KH, Lee SK, Kim YS, Jung BK, Park JA, Kim SH, Jeong JW and Lee MS: Metastasis-associated protein 1 enhances angiogenesis by stabilization of HIF-1alpha. Oncol Rep 16: 929-935, 2006.
8. Moon HE, Cheon H and Lee MS: Metastasis-associated protein 1 inhibits p53-induced apoptosis. Oncol Rep 18: 1311-1314, 2007.
9. Park SY, Chang I, Kim JY, Kang SW, Park SH, Singh K and Lee MS: Resistance of mitochondrial DNA-depleted cells against cell death: role of mitochondrial superoxide dismutase. J Biol Chem 279: 7512-7520, 2004.
10. Shweiki D, Itin A, Soffer D and Keshet E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843-845, 1992.
11. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD and Semenza GL: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613, 1996.
12. Chambers AF, Groom AC and MacDonald IC: Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2: 563-572, 2002.
13. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, Iyer N, LaRusch J, Pak B, Taghavi P and Semenza GL: Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 63: 1138-1143, 2003.
14. Petrella BL, Lohi J and Brinckerhoff CE: Identification of membrane type-1 matrix metalloproteinase as a target of hypoxia-inducible factor-2 alpha in von Hippel-Lindau renal cell carcinoma. Oncogene 24: 1043-1052, 2005.
15. King MP and Attardi G: Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246: 500-503, 1989.
16. Butow RA and Avadhani NG: Mitochondrial signaling: the retrograde response. Mol Cell 14: 1-15, 2004.
17. Ryan MT and Hoogenraad NJ: Mitochondrial-nuclear communications. Annu Rev Biochem 76: 701-722, 2007.
18. Kallio PJ, Wilson WJ, O'Brien S, Makino Y and Poellinger L: Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem 274: 6519-6525, 1999.
19. Hagen T, Taylor CT, Lam F and Moncada S: Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302: 1975-1978, 2003.
20. Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47, 2002.
21. Turcotte S, Desrosiers RR and Beliveau R: HIF-1alpha mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J Cell Sci 116: 2247-2260, 2003.
22. Blouin CC, Page EL, Soucy GM and Richard DE: Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 103: 1124-1130, 2004.
23. Maranchie JK and Zhan Y: Nox4 is critical for hypoxia-inducible factor 2-alpha transcriptional activity in von Hippel-Lindau-deficient renal cell carcinoma. Cancer Res 65: 9190-9193, 2005.
24. Shimba S, Wada T, Hara S and Tezuka M: EPAS1 promotes adipose differentiation in 3T3-L1 cells. J Biol Chem 279: 40946-40953, 2004.
25. Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT and Hoogenraad NJ: A mitochondrial specific stress response in mammalian cells. EMBO J 21: 4411-4419, 2002.
26. Koshikawa N, Iyozumi A, Gassmann M and Takenaga K: Constitutive upregulation of hypoxia-inducible factor-1alpha mRNA occurring in highly metastatic lung carcinoma cells leads to vascular endothelial growth factor overexpression upon hypoxic exposure. Oncogene 22: 6717-6724, 2003.
27. Aguirre Ghiso JA, Alonso DF, Farias EF, Gomez DE and de Kier Joffe EB: Deregulation of the signaling pathways controlling urokinase production. Its relationship with the invasive phenotype. Eur J Biochem 263: 295-304, 1999.
28. Deryugina EI and Quigley JP: Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 25: 9-34, 2006.
29. Duffy MJ: Urokinase-type plasminogen activator: a potent marker of metastatic potential in human cancers. Biochem Soc Trans 30: 207-210, 2002.
30. Egeblad M and Werb Z: New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174, 2002.
31. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z and Hanahan D: Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2: 737-744, 2000.
32. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson AH, Drummond AH, Galloway WA, Gilbert R, Gordon JL, et al: Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature 370: 555-557, 1994.
33. Suzuki M, Raab G, Moses MA, Fernandez CA and Klagsbrun M: Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site. J Biol Chem 272: 31730-31737, 1997.
34. Amuthan G, Biswas G, Ananadatheerthavarada HK, Vijayasarathy C, Shephard HM and Avadhani NG: Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 21: 7839-7849, 2002.
35. Amuthan G, Biswas G, Zhang SY, Klein-Szanto A, Vijayasarathy C and Avadhani NG: Mitochondria-to-nucleus stress signaling induces phenotypic changes, tumor progression and cell invasion. EMBO J 20: 1910-1920, 2001.
36. van Waveren C, Sun Y, Cheung HS and Moraes CT: Oxidative phosphorylation dysfunction modulates expression of extracellular matrix - remodeling genes and invasion. Carcinogenesis 27: 409-418, 2006.