C-Myc-mediated repression of miR-15-16 in hypoxia is induced by increased HIF-2α and promotes tumor angiogenesis and metastasis by upregulating FGF2

Oncogene

Volumn 34, Issue 11, 2015, Pages 1393-1406

  Xue, G ^a   Yan, H L ^a   Zhang, Y ^a   Hao, L Q ^b   Zhu, X T ^a   Mei, Q ^a   Sun, S H ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; FIBROBLAST GROWTH FACTOR 2; MICRORNA; MIRN15 MICRORNA, HUMAN; MIRN16 MICRORNA, HUMAN; MYC PROTEIN; MYC PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CANCER TRANSPLANTATION; CELL HYPOXIA; CELL MOTION; COLORECTAL TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HT 29 CELL LINE; HUMAN; MALE; METASTASIS; MIDDLE AGED; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PROMOTER REGION; RNA INTERFERENCE; TUMOR CELL LINE; UPREGULATION; XENOGRAFT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; COLORECTAL NEOPLASMS; FEMALE; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; MALE; MICE; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MYC; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS; UP-REGULATION;

EID: 84897351790     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.82     Document Type: Article

References (41)

1. Finger EC, Giaccia AJ. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metast Rev 2010; 29: 285-293.
2. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI et al. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 2008; 456: 814-818.
3. 2 availability on human cancer. Nat Rev Cancer 2008; 8: 967-975.
4. Bristow RG, Hill RP. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 2008; 8: 180-192.
5. Horan AD, Koch CJ. The K(m) for radiosensitization of human tumor cells by oxygen is much greater than 3mmHg and is further increased by elevated levels of cysteine. Radiat Res 2001; 156: 388-398.
6. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metast Rev 2007; 26: 225-239.
7. Chaudary N, Hill RP. Hypoxia and metastasis. Clin Cancer Res 2007; 13: 1947-1949.
8. Ruan K, Song G, Ouyang G. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 2009; 107: 1053-1062.
9. Le QT, Denko NC, Giaccia AJ. Hypoxic gene expression and metastasis. Cancer Metast Rev 2004; 23: 293-310.
10. Chan DA, Giaccia AJ. Hypoxia, gene expression, and metastasis. Cancer Metast Rev 2007; 26: 333-339.
11. Voss MJ, Niggemann B, Zänker KS, Entschladen F. Tumour reactions to hypoxia. Curr Mol Med 2010; 10: 381-386.
12. Fong S, Itahana Y, Sumida T, Singh J, Coppe JP, Liu Y et al. Id-1as a molecular target in therapy for breast cancer cell invasion and metastasis. Proc Natl Acad Sci USA 2003; 100: 13543-13548.
13. Gupta GP, Perk J, Acharyya S, de Candia P, Mittal V, Todorova-Manova K et al. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc Natl Acad Sci USA 2007; 104: 19506-19511.
14. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10: 704-714.
15. Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S et al. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci USA 2009; 106: 1814-1819.
16. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234.
17. Kulshreshtha R, Davuluri RV, Calin GA, Ivan M. A microRNA component of the hypoxic response. Cell Death Differ, 2008; 15: 667-671.
18. Ivan M, Harris AL, Martelli F, Kulshreshtha R. Hypoxia response and microRNAs: no longer two separate worlds. J Cell Mol Med 2008; 12: 1426-1431.
19. Kaluz S, Kaluzová M, Liao SY, Lerman M, Stanbridge EJ. Transcriptional control of the tumor- and hypoxia-marker carbonic anhydrase 9: a one transcription factor (HIF-1) show? Biochim Biophys Acta 2009; 1795: 162-172.
20. Yan HL, Xue G, Mei Q, Wang YZ, Ding FX, Liu MF et al. Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis. EMBO J 2009; 28: 2719-2732.
21. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK et al. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 2009; 35: 856-867.
22. Aqeilan RI, Calin GA, Croce CM. miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 2010; 17: 215-220.
23. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102: 13944-13949.
24. Shoushtari AN, Szmulewitz RZ, Rinker-Schaeffer CW. Metastasis-suppressor genes in clinical practice: lost in translation? Nat Rev Clin Oncol 2011; 8: 333-342.
25. Hackl C, Man S, Francia G, Milsom C, Xu P, Kerbel RS. Metronomic oral topotecan prolongs survival and reduces liver metastasis in improved preclinical orthotopic and adjuvant therapy colon cancer models. Gut 2013; 62: 259-271.
26. Cao Y, Arbiser J, D'Amato RJ, D'Amore PA, Ingber DE, Kerbel R et al. Forty-year journey of angiogenesis translational research. Sci Transl Med 2011; 3: 114rv3.
27. Lerner M, Harada M, Lovén J, Castro J, Davis Z, Oscier D et al. DLEU2, frequently deleted in malignancy, functions as a critical host gene of the cell cycle inhibitory microRNAs miR-15a and miR-16-1. Exp Cell Res 2009; 315: 2941-292.
28. Marinescu VD, Kohane IS, Riva A. MAPPER: a search engine for the computational identification of putative transcription factor binding sites in multiple genomes. BMC Bioinform 2005; 6: 79.
29. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008; 40: 43-50.
30. Dang CV, Kim JW, Gao P, Yustein J. The interplay between MYC and HIF in cancer. Nat Rev Cancer 2008; 8: 51-56.
31. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102: 13944-13949.
32. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008; 14: 1271-1277.
33. Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev, 2007; 3: 30-38.
34. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT et al. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci USA 2010; 107: 6334-6339.
35. Khew-Goodall Y, Goodall GJ. Myc-modulated miR-9 makes more metastases. Nat Cell Biol 2010; 12: 209-211.
36. Buendia MA, Bourre L, Cairo S. Myc target miRs and liver cancer: small molecules to get Myc sick. Gastroenterology 2012; 142: 214-218.
37. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2011; 12: 9-22.
38. Gordan JD, Thompson CB, Simon MC. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007; 12: 108-113.
39. Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller KI et al. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007; 11: 407-420.
40. Banning A, Kipp A, Schmitmeier S, Löwinger M, Florian S, Krehl S et al. Glutathione peroxidase 2 inhibits cyclooxygenase-2-mediated migration and invasion of HT-29 adenocarcinoma cells but supports their growth as tumors in nude mice. Cancer Res 2008; 68: 9746-9753.
41. Fromowitz FB, Viola MV, Chao S, Oravez S, Mishriki Y, Finkel G et al. ras p21 expression in the progression of breast cancer. Hum Pathol 1987; 18: 1268-1275.