The role of microRNAs in human cancer

Signal Transduction and Targeted Therapy

Volumn 1, Issue , 2016, Pages

  Peng, Yong ^a,b   Croce, Carlo M ^c  

^a SICHUAN UNIVERSITY   (China)

^b State Key Laboratory of Biotherapy Collaborative Innovation Center for Biotherapy   (China)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85059644548     PISSN: 20959907     EISSN: 20593635     Source Type: Journal    
DOI: 10.1038/sigtrans.2015.4     Document Type: Review

References (121)

1. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75: 843–854.
2. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000; 403: 901–906.
3. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853–858.
4. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001; 294: 858–862.
5. Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294: 862–864.
6. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99: 15524–15529.
7. 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.
8. Calin GA, Cimmino A, Fabbri M, Ferracin M, Wojcik SE, Shimizu M et al. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci USA 2008; 105: 5166–5171.
9. Klein U, Lia M, Crespo M, Siegel R, Shen Q, Mo T et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 2010; 17: 28–40.
10. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006; 13: 1097–1101.
11. Lee Y, Kim M, Han J, Yeom KH, Lee S et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051–4060.
12. Macfarlane LA, Murphy PR. MicroRNA: biogenesis, function and role in cancer. Curr Genomics 2010; 11: 537–561.
13. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215–233.
14. Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 2013; 153: 654–665.
15. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: micro-RNAs can up-regulate translation. Science 2007; 318: 1931–1934.
16. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 2012; 109: E2110–E2116.
17. He S, Chu J, Wu LC, Mao H, Peng Y, Alvarez-Breckenridge CA et al. MicroRNAs activate natural killer cells through Toll-like receptor signaling. Blood 2013; 121: 4663–4671.
18. Fukuda T, Yamagata K, Fujiyama S, Matsumoto T, Koshida I, Yoshimura K et al. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat Cell Biol 2007; 9: 604–611.
19. Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008; 454: 56–61.
20. Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of micro-RNAs. Nature 2009; 459: 1010–1014.
21. Alarcón CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF. N6-methyladenosine marks primary microRNAs for processing. Nature 2015; 519: 482–485.
22. Calin GA, Croce CM. MicroRNAs and chromosomal abnormalities in cancer cells. Oncogene 2006; 25: 6202–6210.
23. Tagawa H, Seto M. A microRNA cluster as a target of genomic amplification in malignant lymphoma. Leukemia 2005; 19: 2013–2016.
24. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628–9632.
25. Mavrakis KJ, Wolfe AL, Oricchio E, Palomero T, de Keersmaecker K, McJunkin K et al. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 2010; 12: 372–379.
26. Zhang L, Huang J, Yang N, Greshock J, Megraw MS, Giannakakis A et al. MicroRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci USA 2006; 103: 9136–9141.
27. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 2004; 101: 2999–3004.
28. O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435: 839–843.
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. Wang B, Hsu SH, Wang X, Kutay H, Bid HK, Yu J et al. Reciprocal regulation of microRNA-122 and c-Myc in hepatocellular cancer: role of E2F1 and transcription factor dimerization partner 2. Hepatology 2014; 59: 555–566.
31. Han H, Sun D, Li W, Shen H, Zhu Y, Li C et al. c-Myc-MicroRNA functional feedback loop affects hepatocarcinogenesis. Hepatology 2013; 57: 2378–2389.
32. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447: 1130–1134.
33. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17: 193–199.
34. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007; 26: 731–743.
35. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26: 745–752.
36. Yamakuchi M, Lowenstein CJ. MiR-34, SIRT1, and p53: The feedback loop. Cell Cycle 2009; 8: 712–715.
37. Xiao J, Lin H, Luo X, Luo X, Wang Z. miR-605 joins p53 network to form a p53: miR-605:Mdm2 positive feedback loop in response to stress. EMBO J 2011; 30: 524–532.
38. Zhang Y, Liao JM, Zeng SX, Lu H. p53 downregulates Down syndrome-associated DYRK1A through miR-1246. EMBO Rep 2011; 12: 811–817.
39. 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.
40. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451: 1125–1129.
41. Wong QW, Lung RW, Law PT, Lai PB, Chan KY, To KF et al. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology 2008; 135: 257–269.
42. Eyholzer M, Schmid S, Schardt JA, Haefliger S, Mueller BU, Pabst T. Complexity of miR-223 regulation by CEBPA in human AML. Leuk Res 2010; 34: 672–676.
43. Stamatopoulos B, Meuleman N, Haibe-Kains B, Saussoy P, Van Den Neste E et al. microRNA-29c and microRNA-223 down-regulation has in vivo significance in chronic lymphocytic leukemia and improves disease risk stratification. Blood 2009; 113: 5237–5245.
44. Fukao T, Fukuda Y, Kiga K, Sharif J, Hino K, Enomoto Y et al. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 2007; 129: 617–631.
45. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, Nervi C et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005; 123: 819–831.
46. Han L, Witmer PD, Casey E, Valle D, Sukumar S. DNA methylation regulates MicroRNA expression. Cancer Biol Ther 2007; 6: 1284–1288.
47. Saito Y, Jones PA. Epigenetic activation of tumor suppressor microRNAs in human cancer cells. Cell Cycle 2006; 5: 2220–2222.
48. Fazi F, Racanicchi S, Zardo G, Starnes LM, Mancini M, Travaglini L et al. Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 2007; 12: 457–466.
49. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006; 9: 435–443.
50. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 2008; 105: 13556–13561.
51. Lehmann U, Hasemeier B, Christgen M, Müller M, Römermann D, Länger F et al. Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J Pathol 2008; 214: 17–24.
52. Lujambio A, Esteller M. CpG island hypermethylation of tumor suppressor microRNAs in human cancer. Cell Cycle 2007; 6: 1455–1459.
53. Donzelli S, Mori F, Bellissimo T, Sacconi A, Casini B, Frixa T et al. Epigenetic silencing of miR-145-5p contributes to brain metastasis. Oncotarget 2015; 6: 35183–35201.
54. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 2006; 20: 2202–2207.
55. Walz AL, Ooms A, Gadd S, Gerhard DS, Smith MA, Guidry Auvil JM et al. Recurrent DGCR8, DROSHA, and SIX homeodomain mutations in favorable histology Wilms tumors. Cancer Cell 2015; 27: 286–297.
56. Iliou MS, da Silva-Diz V, Carmona FJ, Ramalho-Carvalho J, Heyn H, Villanueva A et al. Impaired DICER1 function promotes stemness and metastasis in colon cancer. Oncogene 2014; 33: 4003–4015.
57. Merritt WM, Lin YG, Han LY, Kamat AA, Spannuth WA, Schmandt R et al. Dicer, Drosha, and outcomes in patients with ovarian cancer. N Engl J Med 2008; 359: 2641–2650.
58. Pampalakis G, Diamandis EP, Katsaros D, Sotiropoulou G. Down-regulation of dicer expression in ovarian cancer tissues. Clin Biochem 2010; 43: 324–327.
59. Faggad A, Budczies J, Tchernitsa O, Darb-Esfahani S, Sehouli J, Müller BM et al. Prognostic significance of Dicer expression in ovarian cancer-link to global microRNA changes and oestrogen receptor expression. J Pathol 2010; 220: 382–391.
60. Karube Y, Tanaka H, Osada H, Tomida S, Tatematsu Y, Yanagisawa K et al. Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 2005; 96: 111–115.
61. Dome JS, Coppes MJ. Recent advances in Wilms tumor genetics. Curr Opin Pediatr 2002; 14: 5–11.
62. Zhang J, Fan XS, Wang CX, Liu B, Li Q, Zhou XJ. Up-regulation of Ago2 expression in gastric carcinoma. Med Oncol 2013; 30: 628.
63. Völler D, Reinders J, Meister G, Bosserhoff AK. Strong reduction of AGO2 expression in melanoma and cellular consequences. Br J Cancer 2013; 109: 3116–3124.
64. Melo SA, Moutinho C, Ropero S, Calin GA, Rossi S, Spizzo R et al. A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer Cell 2010; 18: 303–315.
65. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646–674.
66. Trimarchi JM, Lees JA. Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 2002; 3: 11–20.
67. Coller HA, Forman JJ, Legesse-Miller A. ‘Myc’ed messages’: Myc induces transcription of E2F1 while inhibiting its translation via a microRNA polycistron. PLoS Genet 2007; 3: e146.
68. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V et al. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 2007; 282: 2135–2143.
69. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007; 282: 2130–2134.
70. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435: 828–833.
71. Hatfield SD, Shcherbata HR, Fischer KA, Nakahara K, Carthew RW et al. Stem cell division is regulated by the microRNA pathway. Nature 2005; 435: 974–978.
72. Gillies JK, Lorimer IA. Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle 2007; 6: 2005–2009.
73. Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafrè SA et al. miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 2007; 282: 23716–23724.
74. le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A et al. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 2007; 26: 3699–3708.
75. Visone R, Russo L, Pallante P, De Martino I, Ferraro A, Leone V et al. MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocr Relat Cancer 2007; 14: 791–798.
76. Lal A, Kim HH, Abdelmohsen K, Kuwano Y, Pullmann Jr R, Srikantan S et al. p16 (INK4a) translation suppressed by miR-24. PLoS One 2008; 3: e1864.
77. Dolezalova D, Mraz M, Barta T, Plevova K, Vinarsky V, Holubcova Z et al. MicroRNAs regulate p21(Waf1/Cip1) protein expression and the DNA damage response in human embryonic stem cells. Stem Cells 2012; 30: 1362–1372.
78. Yi C, Wang Q, Wang L, Huang Y, Li L, Liu L et al. MiR-663, a microRNA targeting p21WAF1/CIP1, promotes the proliferation and tumorigenesis of nasophar-yngeal carcinoma. Oncogene 2012; 31: 4421–4433.
79. Du B, Wang Z, Zhang X, Feng S, Wang G, He J et al. MicroRNA-545 suppresses cell proliferation by targeting cyclin D1 and CDK4 in lung cancer cells. PLoS One 2014; 9: e88022.
80. Peng Y, Dai Y, Hitchcock C, Yang X, Kassis ES, Liu L et al. Insulin growth factor signaling is regulated by microRNA-486, an underexpressed microRNA in lung cancer. Proc Natl Acad Sci USA 2013; 110: 15043–15048.
81. Lima RT, Busacca S, Almeida GM, Gaudino G, Fennell DA, Vasconcelos MH. MicroRNA regulation of core apoptosis pathways in cancer. Eur J Cancer 2011; 47: 163–174.
82. Li C, Hashimi SM, Good DA, Cao S, Duan W, Plummer PN et al. Apoptosis and microRNA aberrations in cancer. Clin Exp Pharmacol Physiol 2012; 39: 739–746.
83. Pichiorri F, Suh SS, Rocci A, De Luca L, Taccioli C, Santhanam R et al. Down-regulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 2010; 18: 367–381.
84. Fornari F, Gramantieri L, Giovannini C, Veronese A, Ferracin M, Sabbioni S et al. MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2009; 69: 5761–5767.
85. Burns DM, D’Ambrogio A, Nottrott S, Richter JD. CPEB and two poly(A) poly-merases control miR-122 stability and p53 mRNA translation. Nature 2011; 473: 105–108.
86. 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.
87. Sacconi A, Biagioni F, Canu V, Mori F, Di Benedetto A, Lorenzon L et al. miR-204 targets Bcl-2 expression and enhances responsiveness of gastric cancer. Cell Death Dis 2012; 3: e423.
88. Zhang H, Li Y, Huang Q, Ren X, Hu H, Sheng H et al. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ 2011; 18: 1702–1710.
89. Nie J, Liu L, Zheng W, Chen L, Wu X, Xu Y et al. microRNA-365, down-regulated in colon cancer, inhibits cell cycle progression and promotes apoptosis of colon cancer cells by probably targeting Cyclin D1 and Bcl-2. Carcinogenesis 2012; 33: 220–225.
90. Denoyelle C, Lambert B, Meryet-Figuière M, Vigneron N, Brotin E, Lecerf C et al. miR-491-5p-induced apoptosis in ovarian carcinoma depends on the direct inhibition of both BCL-XL and EGFR leading to BIM activation. Cell Death Dis 2014; 5: e1445.
91. Zhang CZ, Zhang JX, Zhang AL, Shi ZD, Han L, Jia ZF et al. MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol Cancer 2010; 9: 229.
92. Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, van Rooij E et al. Modulation of K-Ras-dependent lung tumorigenesis by MicroRNA-21. Cancer Cell 2010; 18: 282–293.
93. Wang P, Zhuang L, Zhang J, Fan J, Luo J, Chen H et al. The serum miR-21 level serves as a predictor for the chemosensitivity of advanced pancreatic cancer, and miR-21 expression confers chemoresistance by targeting FasL. Mol Oncol 2013; 7: 334–345.
94. Shaffiey F, Cross E, Sathyanarayana P. Mir-590 is a novel STAT5 regulated oncogenic miRNA and targets FasL in acute myeloid leukemia. Blood 2013; 122: 3811–3811.
95. Razumilava N, Bronk SF, Smoot RL, Fingas CD, Werneburg NW, Roberts LR et al. miR-25 targets TNF-related apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology 2012; 55: 465–475.
96. Kalluri R, Weinberg RA. The basics of epithelial mesenchymal transition. J Clin Invest 2009; 119: 1420–1428.
97. Kong W, Yang H, He L, Zhao JJ, Coppola D, Dalton WS et al. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 2008; 28: 6773–6784.
98. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593–601.
99. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008; 68: 7846–7854.
100. Hurteau GJ, Carlson JA, Spivack SD, Brock GJ. Over-expression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res 2007; 67: 7972–7976.
101. Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283: 14910–14914.
102. Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y, Li CW et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 2011; 13: 317–323.
103. Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med 2011; 208: 875–883.
104. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449: 682–688.
105. Ding X, Park SI, McCauley LK, Wang CY. Signaling between transforming growth factor β (TGF-β) and transcription factor SNAI2 represses expression of microRNA miR-203 to promote epithelial-mesenchymal transition and tumor metastasis. J Biol Chem 2013; 88: 10241–10253.
106. Zhang Z, Zhang B, Li W, Fu L, Fu L, Zhu Z et al. Epigenetic silencing of miR-203 upregulates SNAI2 and contributes to the invasiveness of malignant breast cancer cells. Genes Cancer 2011; 2: 782–791.
107. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010; 12: 247–256.
108. Almeida MI, Reis RM, Calin GA. MYC-microRNA-9-metastasis connection in breast cancer. Cell Res 2010; 20: 602–603.
109. Meng X, Wu J, Pan C, Wang H, Ying X, Zhou Y et al. Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD. Gastroenterology 2013; 145: 426–436.
110. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000; 6: 389–595.
111. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer 2002; 2: 795–803.
112. Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H et al. hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 2008; 14: 1340–1348.
113. Fasanaro P, D’Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G et al. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 2008; 283: 15878–15883.
114. Lou YL, Guo F, Liu FL, Gao FL, Zhang PQ, Niu X et al. MiR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem 2012; 370: 45–51.
115. Liu F, Lou YL, Wu J, Ruan QF, Xie A, Guo F et al. Upregulation of MicroRNA-210 regulates renal angiogenesis mediated by activation of VEGF signaling pathway under ischemia/perfusion injury in vivo and in vitro. Kidney Blood Press Res 2012; 35: 182–191.
116. Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D et al. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J Clin Invest 2010; 120: 4141–4154.
117. Liu LZ, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y et al. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1alpha expression. PLoS One 2011; 6: e19139.
118. Lei Z, Li B, Yang Z, Fang H, Zhang GM, Feng ZH et al. Regulation of HIF-1alpha and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration. PLoS One 2009; 4: e7629.
119. Cha ST, Chen PS, Johansson G, Chu CY, Wang MY, Jeng YM et al. MicroRNA-519c suppresses hypoxia-inducible factor-1alpha expression and tumor angiogenesis. Cancer Res 2010; 70: 2675–2685.
120. 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.
121. Umezu T, Tadokoro H, Azuma K, Yoshizawa S, Ohyashiki K, Ohyashiki JH. Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood 2014; 124: 3748–3757.