MicroRNA response to hypoxic stress in soft tissue sarcoma cells: MicroRNA mediated regulation of HIF3α

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Gits, Caroline M M ^a   van Kuijk, Patricia F ^a   de Rijck, Jonneke C W M ^a   Muskens, Nikky ^a   Jonkers, Moniek B E ^a   van IJcken, Wilfred F ^b   Mathijssen, Ron H J ^a   Verweij, Jaap ^a   Sleijfer, Stefan ^a   Wiemer, Erik A C ^a  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

HIF3 ; Hypoxia; MiR 210 3p; MiR 485 5p; MiRNA; Soft tissue sarcomas

Indexed keywords

CARBONATE DEHYDRATASE IX; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; MICRORNA; MICRORNA 185 3P; MICRORNA 210 3P; MICRORNA 216A 5P; MICRORNA 485 5P; MICRORNA 625 5P; UNCLASSIFIED DRUG; VASCULOTROPIN A; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HIF3A PROTEIN, HUMAN; MIRN210 MICRORNA, HUMAN; MIRN485 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CA9 GENE; CELL HYPOXIA; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HIF3ALPHA GENE; LUCIFERASE ASSAY; MICROARRAY ANALYSIS; PREDICTIVE VALUE; REAL TIME POLYMERASE CHAIN REACTION; SARCOMA CELL LINE; SOFT TISSUE SARCOMA; UPREGULATION; VEGFA GENE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; PATHOLOGY; PROGNOSIS; SARCOMA; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; PROGNOSIS; SARCOMA; SIGNAL TRANSDUCTION;

EID: 84902051563     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-429     Document Type: Article

References (61)

1. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2(1):38-47. 10.1038/nrc704, 11902584.
2. Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A 1993, 90(9):4304-4308. 10.1073/pnas.90.9.4304, 46495, 8387214.
3. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A 1997, 94(9):4273-4278. 10.1073/pnas.94.9.4273, 20712, 9113979.
4. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003, 23(24):9361-9374. 10.1128/MCB.23.24.9361-9374.2003, 309606, 14645546.
5. Heikkila M, Pasanen A, Kivirikko KI, Myllyharju J. Roles of the human hypoxia-inducible factor (HIF)-3alpha variants in the hypoxia response. Cell Mol Life Sci 2011, 68(23):3885-3901. 10.1007/s00018-011-0679-5, 21479871.
6. Maynard MA, Qi H, Chung J, Lee EH, Kondo Y, Hara S, Conaway RC, Conaway JW, Ohh M. Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 2003, 278(13):11032-11040. 10.1074/jbc.M208681200, 12538644.
7. Pasanen A, Heikkila M, Rautavuoma K, Hirsila M, Kivirikko KI, Myllyharju J. Hypoxia-inducible factor (HIF)-3alpha is subject to extensive alternative splicing in human tissues and cancer cells and is regulated by HIF-1 but not HIF-2. Int J Biochem Cell Biol 2010, 42(7):1189-1200. 10.1016/j.biocel.2010.04.008, 20416395.
8. Hara S, Hamada J, Kobayashi C, Kondo Y, Imura N. Expression and characterization of hypoxia-inducible factor (HIF)-3alpha in human kidney: suppression of HIF-mediated gene expression by HIF-3alpha. Biochem Biophys Res Commun 2001, 287(4):808-813. 10.1006/bbrc.2001.5659, 11573933.
9. Maynard MA, Evans AJ, Hosomi T, Hara S, Jewett MA, Ohh M. Human HIF-3alpha4 is a dominant-negative regulator of HIF-1 and is down-regulated in renal cell carcinoma. FASEB J 2005, 19(11):1396-1406. 10.1096/fj.05-3788com, 16126907.
10. Maynard MA, Evans AJ, Shi W, Kim WY, Liu FF, Ohh M. Dominant-negative HIF-3 alpha 4 suppresses VHL-null renal cell carcinoma progression. Cell Cycle 2007, 6(22):2810-2816. 10.4161/cc.6.22.4947, 17998805.
11. Tanaka T, Wiesener M, Bernhardt W, Eckardt KU, Warnecke C. The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 2009, 424(1):143-151. 10.1042/BJ20090120, 19694616.
12. Airley RE, Phillips RM, Evans AE, Double J, Burger AM, Feibig HH, West CM, Stratford IJ. Hypoxia-regulated glucose transporter glut-1 may influence chemosensitivity to some alkylating agents: results of EORTC (first translational award) study of the relevance of tumour hypoxia to the outcome of chemotherapy in human tumour-derived xenografts. Int J Oncol 2005, 26(6):1477-1484.
13. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996, 56(19):4509-4515.
14. Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Bean JM, Prosnitz LR, Dewhirst MW. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 1996, 56(5):941-943.
15. Nordsmark M, Hoyer M, Keller J, Nielsen OS, Jensen OM, Overgaard J. The relationship between tumor oxygenation and cell proliferation in human soft tissue sarcomas. Int J Radiat Oncol Biol Phys 1996, 35(4):701-708. 10.1016/0360-3016(96)00132-0, 8690636.
16. Wiemer EA. The role of microRNAs in cancer: no small matter. Eur J Cancer 2007, 43(10):1529-1544. 10.1016/j.ejca.2007.04.002, 17531469.
17. Chen CZ. MicroRNAs as oncogenes and tumor suppressors. N Engl J Med 2005, 353(17):1768-1771. 10.1056/NEJMp058190, 16251533.
18. Di Leva G, Croce CM. Roles of small RNAs in tumor formation. Trends Mol Med 2010, 16(6):257-267. 10.1016/j.molmed.2010.04.001, 2885513, 20493775.
19. Lujambio A, Lowe SW. The microcosmos of cancer. Nature 2012, 482(7385):347-355. 10.1038/nature10888, 3509753, 22337054.
20. Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol 2007, 302(1):1-12. 10.1016/j.ydbio.2006.08.028, 16989803.
21. Li X, Wu Z, Fu X, Han W. A microRNA component of the neoplastic microenvironment: microregulators with far-reaching impact. Biomed Res Int 2013, 2013:762183. 3591172, 23509776.
22. Wentz-Hunter KK, Potashkin JA. The role of miRNAs as key regulators in the neoplastic microenvironment. Mol Biol Int 2011, 2011:839872. 3200203, 22091413.
23. Crosby ME, Devlin CM, Glazer PM, Calin GA, Ivan M. Emerging roles of microRNAs in the molecular responses to hypoxia. Curr Pharm Des 2009, 15(33):3861-3866. 10.2174/138161209789649367, 19925433.
24. Kulshreshtha R, Davuluri RV, Calin GA, Ivan M. A microRNA component of the hypoxic response. Cell Death Differ 2008, 15(4):667-671. 10.1038/sj.cdd.4402310, 18219318.
25. Kulshreshtha R, Ferracin M, Negrini M, Calin GA, Davuluri RV, Ivan M. Regulation of microRNA expression: the hypoxic component. Cell Cycle 2007, 6(12):1426-1431.
26. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M. A microRNA signature of hypoxia. Mol Cell Biol 2007, 27(5):1859-1867. 10.1128/MCB.01395-06, 1820461, 17194750.
27. Cha ST, Chen PS, Johansson G, Chu CY, Wang MY, Jeng YM, Yu SL, Chen JS, Chang KJ, Jee SH, Tan C, Lin MT, Kuo ML. MicroRNA-519c suppresses hypoxia-inducible factor-1alpha expression and tumor angiogenesis. Cancer Res 2010, 70(7):2675-2685. 10.1158/0008-5472.CAN-09-2448, 20233879.
28. Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, Ramakrishnan S. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J Clin Invest 2010, 120(11):4141-4154. 10.1172/JCI42980, 2964978, 20972335.
29. Kelly TJ, Souza AL, Clish CB, Puigserver P. A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like. Mol Cell Biol 2011, 31(13):2696-2706. 10.1128/MCB.01242-10, 3133367, 21555452.
30. Taguchi A, Yanagisawa K, Tanaka M, Cao K, Matsuyama Y, Goto H, Takahashi T. Identification of hypoxia-inducible factor-1 alpha as a novel target for miR-17-92 microRNA cluster. Cancer Res 2008, 68(14):5540-5545. 10.1158/0008-5472.CAN-07-6460, 18632605.
31. Xu Q, Liu LZ, Qian X, Chen Q, Jiang Y, Li D, Lai L, Jiang BH. MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res 2012, 40(2):761-774. 10.1093/nar/gkr730, 3258133, 21917858.
32. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, Huso D, Lowenstein CJ. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci U S A 2010, 107(14):6334-6339. 10.1073/pnas.0911082107, 2851979, 20308559.
33. Pothof J, Verkaik NS, van IJcken W, Wiemer EA, TA VT, van der Horst GT, Jaspers NG, van Gent DC, Hoeijmakers JH, Persengiev SP. MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response. EMBO J 2009, 28(14):2090-2099. 10.1038/emboj.2009.156, 2718280, 19536137.
34. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108. 10.1038/nprot.2008.73, 18546601.
35. Beasley NJ, Wykoff CC, Watson PH, Leek R, Turley H, Gatter K, Pastorek J, Cox GJ, Ratcliffe P, Harris AL. Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Res 2001, 61(13):5262-5267.
36. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000, 60(24):7075-7083.
37. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003, 9(6):677-684. 10.1038/nm0603-677, 12778166.
38. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120(1):15-20. 10.1016/j.cell.2004.12.035, 15652477.
39. Greither T, Wurl P, Grochola L, Bond G, Bache M, Kappler M, Lautenschlager C, Holzhausen HJ, Wach S, Eckert AW, et al. Expression of microRNA 210 associates with poor survival and age of tumor onset of soft-tissue sarcoma patients. Int J Cancer 2012, 130(5):1230-1235. 10.1002/ijc.26109, 21455991.
40. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 2009, 69(3):1221-1229. 10.1158/0008-5472.CAN-08-2516, 2997438, 19141645.
41. Guimbellot JS, Erickson SW, Mehta T, Wen H, Page GP, Sorscher EJ, Hong JS. Correlation of microRNA levels during hypoxia with predicted target mRNAs through genome-wide microarray analysis. BMC Med Genomics 2009, 2:15. 10.1186/1755-8794-2-15, 2667434, 19320992.
42. Hebert C, Norris K, Scheper MA, Nikitakis N, Sauk JJ. High mobility group A2 is a target for miRNA-98 in head and neck squamous cell carcinoma. Mol Cancer 2007, 6:5. 10.1186/1476-4598-6-5, 1783857, 17222355.
43. Xu X, Jia R, Zhou Y, Song X, Wang J, Qian G, Ge S, Fan X. Microarray-based analysis: identification of hypoxia-regulated microRNAs in retinoblastoma cells. Int J Oncol 2011, 38(5):1385-1393.
44. Shen G, Li X, Jia YF, Piazza GA, Xi Y. Hypoxia-regulated microRNAs in human cancer. Acta Pharmacol Sin 2013, 34(3):336-341. 10.1038/aps.2012.195, 3587916, 23377548.
45. Nallamshetty S, Chan SY, Loscalzo J. Hypoxia: a master regulator of microRNA biogenesis and activity. Free Radic Biol Med 2013, 64:20-30. 3762925, 23712003.
46. Bruning U, Cerone L, Neufeld Z, Fitzpatrick SF, Cheong A, Scholz CC, Simpson DA, Leonard MO, Tambuwala MM, Cummins EP, Taylor CT. MicroRNA-155 promotes resolution of hypoxia-inducible factor 1alpha activity during prolonged hypoxia. Mol Cell Biol 2011, 31(19):4087-4096. 10.1128/MCB.01276-10, 3187364, 21807897.
47. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 2009, 35(6):856-867. 10.1016/j.molcel.2009.09.006, 2782615, 19782034.
48. Chen KF, Lai YY, Sun HS, Tsai SJ. Transcriptional repression of human cad gene by hypoxia inducible factor-1alpha. Nucleic Acids Res 2005, 33(16):5190-5198. 10.1093/nar/gki839, 1214551, 16155188.
49. Haque I, Banerjee S, Mehta S, De A, Majumder M, Mayo MS, Kambhampati S, Campbell DR, Banerjee SK. Cysteine-rich 61-connective tissue growth factor-nephroblastoma-overexpressed 5 (CCN5)/Wnt-1-induced signaling protein-2 (WISP-2) regulates microRNA-10b via hypoxia-inducible factor-1alpha-TWIST signaling networks in human breast cancer cells. J Biol Chem 2011, 286(50):43475-43485. 10.1074/jbc.M111.284158, 3234824, 22020939.
50. Polytarchou C, Iliopoulos D, Hatziapostolou M, Kottakis F, Maroulakou I, Struhl K, Tsichlis PN. Akt2 regulates all Akt isoforms and promotes resistance to hypoxia through induction of miR-21 upon oxygen deprivation. Cancer Res 2011, 71(13):4720-4731. 10.1158/0008-5472.CAN-11-0365, 3129420, 21555366.
51. Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, Du Y, Wang Y, Chang WC, Chen CH, Hsu JL, Wu Y, Lam YC, James BP, Liu X, Liu CG, Patel DJ, Hung MC. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013, 497(7449):383-387. 10.1038/nature12080, 3717558, 23636329.
52. Donker RB, Mouillet JF, Nelson DM, Sadovsky Y. The expression of Argonaute2 and related microRNA biogenesis proteins in normal and hypoxic trophoblasts. Mol Hum Reprod 2007, 13(4):273-279. 10.1093/molehr/gam006, 17327266.
53. Augstein A, Poitz DM, Braun-Dullaeus RC, Strasser RH, Schmeisser A. Cell-specific and hypoxia-dependent regulation of human HIF-3alpha: inhibition of the expression of HIF target genes in vascular cells. Cell Mol Life Sci 2011, 68(15):2627-2642. 10.1007/s00018-010-0575-4, 21069422.
54. Makino Y, Uenishi R, Okamoto K, Isoe T, Hosono O, Tanaka H, Kanopka A, Poellinger L, Haneda M, Morimoto C. Transcriptional up-regulation of inhibitory PAS domain protein gene expression by hypoxia-inducible factor 1 (HIF-1): a negative feedback regulatory circuit in HIF-1-mediated signaling in hypoxic cells. J Biol Chem 2007, 282(19):14073-14082. 10.1074/jbc.M700732200, 17355974.
55. Chan YC, Banerjee J, Choi SY, Sen CK. miR-210: the master hypoxamir. Microcirculation 2012, 19(3):215-223. 10.1111/j.1549-8719.2011.00154.x, 3399423, 22171547.
56. Devlin C, Greco S, Martelli F, Ivan M. miR-210: more than a silent player in hypoxia. IUBMB Life 2011, 63(2):94-100.
57. Ivan M, Harris AL, Martelli F, Kulshreshtha R. Hypoxia response and microRNAs: no longer two separate worlds. J Cell Mol Med 2008, 12(5A):1426-1431. 10.1111/j.1582-4934.2008.00398.x, 18624759.
58. Costa FF, Bischof JM, Vanin EF, Lulla RR, Wang M, Sredni ST, Rajaram V, Bonaldo Mde F, Wang D, Goldman S, Tomita T, Soares MB. Identification of microRNAs as potential prognostic markers in ependymoma. PLoS One 2011, 6(10):e25114. 10.1371/journal.pone.0025114, 3203863, 22053178.
59. Cohen JE, Lee PR, Chen S, Li W, Fields RD. MicroRNA regulation of homeostatic synaptic plasticity. Proc Natl Acad Sci U S A 2011, 108(28):11650-11655. 10.1073/pnas.1017576108, 3136313, 21697510.
60. Faghihi MA, Zhang M, Huang J, Modarresi F, Van der Brug MP, Nalls MA, Cookson MR, St-Laurent G, Wahlestedt C. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol 2010, 11(5):R56. 10.1186/gb-2010-11-5-r56, 2898074, 20507594.
61. Kim TH, Kim YK, Kwon Y, Heo JH, Kang H, Kim G, An HJ. Deregulation of miR-519a, 153, and 485-5p and its clinicopathological relevance in ovarian epithelial tumours. Histopathology 2010, 57(5):734-743. 10.1111/j.1365-2559.2010.03686.x, 21083603.