Hypoxia-induced reactive oxygen species cause chromosomal abnormalities in endothelial cells in the tumor microenvironment

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Kondoh, Miyako ^a   Ohga, Noritaka ^a   Akiyama, Kosuke ^a   Hida, Yasuhiro ^b   Maishi, Nako ^a   Towfik, Alam Mohammad ^a   Inoue, Nobuo ^a   Shindoh, Masanobu ^a   Hida, Kyoko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANOXIA; CELL CYCLE; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 17; ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; KARYOTYPE; MICE; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84894044753     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080349     Document Type: Article

References (48)

1. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285: 1182-1186. doi:10.1056/NEJM197111182852108. PubMed: 4938153.
2. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 3: 177-182. doi:10.1038/nm0297-177. PubMed: 9018236.
3. Enholm B, Paavonen K, Ristimäki A, Kumar V, Gunji Yet al (1997) Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14:2475-2483 (Pubitemid 27268166)
4. Liu Y, Cox SR, Morita T, Kourembanas S (1995) Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ Res 77: 638-463. doi:10.1161/01.RES.77.3.638. PubMed: 7641334.
5. Brahimi-Horn MC, Pouysségur J (2009) HIF at a glance. J Cell Sci 122: 1055-1057. doi:10.1242/jcs.035022. PubMed: 19339544.
6. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613. PubMed: 8756616. (Pubitemid 26272112)
7. Blouw B, Song H, Tihan T, Bosze J, Ferrara N et al. (2003) The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 4: 133-146. doi:10.1016/S1535-6108(03)00194-6. PubMed: 12957288. (Pubitemid 37040829)
8. Bos R, Zhong H, Hanrahan CF, Mommers EC, Semenza GL et al. (2001) Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 93: 309-314. doi: 10.1093/jnci/93.4.309. PubMed: 11181778 (Pubitemid 32219818)
9. Giatromanolaki A, Koukourakis MI, Sivridis E, Turley H, Talks K et al. (2001) Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 85: 881-890. doi:10.1054/bjoc.2001.2018. PubMed: 11556841 (Pubitemid 33010557)
10. Kimura H, Braun RD, Ong ET, Hsu R, Secomb TW et al. (1996) Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma. Cancer Res 56: 5522-5528. PubMed: 8968110 (Pubitemid 27011389)
11. Muraki C, Ohga N, Hida Y, Nishihara H, Kato Y et al. (2012) Cyclooxygenase-2 inhibition causes antiangiogenic effects on tumor endothelial and vascular progenitor cells. Int J Cancer 130: 59-70. doi:10.1002/ijc.25976. PubMed: 21384343.
12. Bussolati B, Assenzio B, Deregibus MC, Camussi G (2006) The proangiogenic phenotype of human tumor-derived endothelial cells depends on thrombospondin-1 downregulation via phosphatidylinositol 3-kinase/Akt pathway. J Mol Med (Berl) 84: 852-863. doi:10.1007/s00109-006-0075-z. (Pubitemid 44477419)
13. Kurosu T, Ohga N, Hida Y, Maishi N, Akiyama K et al. (2011) HuR keeps an angiogenic switch on by stabilising mRNA of VEGF and COX-2 in tumour endothelium. Br J Cancer 104: 819-829. doi:10.1038/bjc.2011.20. PubMed: 21285980.
14. Yamamoto K, Ohga N, Hida Y, Maishi N, Kawamoto T et al. (2012) Biglycan is a specific marker and an autocrine angiogenic factor of tumour endothelial cells. Br J Cancer 106: 1214-1223. doi:10.1038/bjc.2012.59. PubMed: 22374465.
15. Ohga N, Ishikawa S, Maishi N, Akiyama K, Hida Y et al. (2012) Heterogeneity of tumor endothelial cells: comparison between tumor endothelial cells isolated from high- and low-metastatic tumors. Am J Pathol 180: 1294-1307. doi:10.1016/j.ajpath.2011.11.035. PubMed: 22245217.
16. Hida K, Hida Y, Amin DN, Flint AF, Panigrahy D et al. (2004) Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res 64: 8249-8255. doi:10.1158/0008-5472.CAN-04-1567. PubMed: 15548691. (Pubitemid 39491762)
17. Akino T, Hida K, Hida Y, Tsuchiya K, Freedman D et al. (2009) Cytogenetic abnormalities of tumor-associated endothelial cells in human malignant tumors. Am J Pathol 175: 2657-2667. doi:10.2353/ajpath.2009.090202. PubMed: 19875502.
18. Huang LE, Bindra RS, Glazer PM, Harris AL (2007) Hypoxia-induced genetic instability - a calculated mechanism underlying tumor progression. J Mol Med (Berl) 85: 139-148. doi:10.1007/s00109-006-0133-6. PubMed: 17180667. (Pubitemid 46188219)
19. Brown JM (1979) Evidence for acutely hypoxic cells in mouse tumours, and a possible mechanism of reoxygenation. Br J Radiol 52: 650-656. doi:10.1259/0007-1285-52-620-650. PubMed: 486895
20. Negoro S, Kunisada K, Fujio Y, Funamoto M, Darville MI et al. (2001) Activation of signal transducer and activator of transcription 3 protects cardiomyocytes from hypoxia/reoxygenation-induced oxidative stress through the upregulation of manganese superoxide dismutase. Circulation 104: 979-981. doi:10.1161/hc3401.095947. PubMed: 11524388. (Pubitemid 32803871)
21. Guyton KZ, Kensler TW (1993) Oxidative mechanisms in carcinogenesis. Br Med Bull 49: 523-544. PubMed: 8221020 (Pubitemid 23243827)
22. Klaunig JE, Xu Y, Isenberg JS, Bachowski S, Kolaja KL et al. (1998) The role of oxidative stress in chemical carcinogenesis. Environ Health Perspect 106 Suppl 1: 289-295. doi:10.1289/ehp.98106s1289. PubMed: 9539021 (Pubitemid 28196053)
23. Corn PG, El-Deiry WS (2007) Microarray analysis of p53-dependent gene expression in response to hypoxia and DNA damage. Cancer Biol Ther 6: 1858-1866. doi:10.1158/1535-7163.MCT-07-0068. PubMed: 18087215. (Pubitemid 351590397)
24. Moeller BJ, Cao Y, Li CY, Dewhirst MW (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5: 429-441. doi:10.1016/S1535- 6108(04)00115-1. PubMed: 15144951 (Pubitemid 38610245)
25. Kozlowski JM, Hart IR, Fidler IJ, Hanna N (1984) A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J Natl Cancer Inst 72: 913-7 (Pubitemid 14131734)
26. Maishi N, Ohga N, Hida Y, Akiyama K, Kitayama K et al. (2012): CXCR7: a novel tumor endothelial marker in renal cell carcinoma. Pathol Int 62: 309-317
27. Osawa T, Ohga N, Hida Y, Kitayama K, Akiyama K et al. (2012) Prostacyclin receptor in tumor endothelial cells promotes angiogenesis in an autocrine manner. Cancer Sci 103: 1038-1044. doi:10.1111/j.1349-7006.2012.02261.x. PubMed: 22380928.
28. Matsuda K, Ohga N, Hida Y, Muraki C, Tsuchiya K et al. (2010) Isolated tumor endothelial cells maintain specific character during long-term culture. Biochem Biophys Res Commun 394: 947-954. doi:10.1016/j.bbrc.2010.03.089. PubMed: 20302845.
29. Ohga N, Hida K, Hida Y, Muraki C, Tsuchiya K et al. (2009) Inhibitory effects of epigallocatechin-3 gallate, a polyphenol in green tea, on tumor-associated endothelial cells and endothelial progenitor cells. Cancer Sci 100: 1963-1970. doi:10.1111/j.1349-7006.2009.01255.x. PubMed: 19650861.
30. Kawamoto T, Ohga N, Akiyama K, Hirata N, Kitahara S et al. (2012) Tumor-derived microvesicles induce proangiogenic phenotype in endothelial cells via endocytosis. PLOS ONE 7: e34045. doi:10.1371/journal.pone.0034045. PubMed: 22479517.
31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609. (Pubitemid 34164012)
32. Ohyashiki K, Ohyashiki JH, Sandberg AA, Minowada J, Kinniburgh AJ (1987) Loss of a Hu-ets-1 allele in human leukemia cell lines ML-1, -2, and -3 with a chromosome change at 11q24. Cancer Res 47: 3842-3846. PubMed: 3109734. (Pubitemid 17105736)
33. Akiyama K, Ohga N, Hida Y, Kawamoto T, Sadamoto Y et al. (2012) Tumor endothelial cells acquire drug resistance by MDR1 up-regulation via VEGF signaling in tumor microenvironment. Am J Pathol 180: 1283-1293. doi:10.1016/j.ajpath.2011.11.029. PubMed: 22245726.
34. Hida K, Hida Y, Shindoh M (2008) Understanding tumor endothelial cell abnormalities to develop ideal anti-angiogenic therapies. Cancer Sci 99: 459-466. doi:10.1111/j.1349-7006.2007.00704.x. PubMed: 18167133. (Pubitemid 351228561)
35. Hida K, Kawamoto T, Ohga N, Akiyama K, Hida Y et al. (2011) Altered angiogenesis in the tumor microenvironment. Pathol Int 61: 630-637. doi:10.1111/j.1440-1827.2011.02726.x. PubMed: 22029673.
36. Taylor SM, Nevis KR, Park HL, Rogers GC, Rogers SL et al. (2010) Angiogenic factor signaling regulates centrosome duplication in endothelial cells of developing blood vessels. Blood 116: 3108-3117. doi:10.1182/blood-2010- 01-266197. PubMed: 20664058.
37. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432: 316-323. doi:10.1038/nature03097. PubMed: 15549093. (Pubitemid 39551659)
38. Vafa O, Wade M, Kern S, Beeche M, Pandita TK et al. (2002) c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9: 1031-1044. doi:10.1016/S1097-2765(02)00520-8. PubMed: 12049739. (Pubitemid 34626672)
39. Lee M, Choy WC, Abid MR (2011) Direct sensing of endothelial oxidants by vascular endothelial growth factor receptor-2 and c-Src. PLOS ONE 6: e28454. doi:10.1371/journal.pone.0028454. PubMed: 22145046.
40. Abid MR, Kachra Z, Spokes KC, Aird WC (2000) NADPH oxidase activity is required for endothelial cell proliferation and migration. FEBS Lett 486: 252-256. doi:10.1016/S0014-5793(00)02305-X. PubMed: 11119713
41. Kuroki M, Voest EE, Amano S, Beerepoot LV, Takashima S et al. (1996) Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J Clin Invest 98: 1667-1675. doi:10.1172/JCI118962. PubMed: 8833917 (Pubitemid 26327878)
42. Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S et al. (2002) Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem 277: 3101-3108. doi:10.1074/jbc.M107711200. PubMed: 11719508. (Pubitemid 34953170)
43. El-Remessy AB, Al-Shabrawey M, Platt DH, Bartoli M, Behzadian MA et al. (2007) Peroxynitrite mediates VEGF's angiogenic signal and function via a nitration-independent mechanism in endothelial cells. FASEB J 21: 2528-2539. doi:10.1096/fj.06-7854com. PubMed: 17384142. (Pubitemid 47230682)
44. Hida K, Akiyama K, Ohga N, Maishi N, Hida Y (2013) Tumor endothelial cells acquire drug resistance in a tumor microenvironment. J Biochem (in press).
45. McDonald DM, Foss AJ (2000) Endothelial cells of tumor vessels: abnormal but not absent. Cancer Metastasis Rev 19: 109-120. doi:10.1023/A:1026529222845. PubMed: 11191049 (Pubitemid 32004700)
46. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK et al. (2002) Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160: 985-1000. doi:10.1016/S0002-9440(10)64920-6. PubMed: 11891196. (Pubitemid 34224587)
47. Lluis JM, Buricchi F, Chiarugi P, Morales A, Fernandez-Checa JC (2007) Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-{kappa}B via c-SRC and oxidant-dependent cell death. Cancer Res 67: 7368-7377. doi:10.1158/0008-5472.CAN-07-0515. PubMed: 17671207. (Pubitemid 47206567)
48. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG et al. (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15: 232-239. doi:10.1016/j.ccr.2009.01.021. PubMed: 19249681.