Advertisement

The AAPS Journal

, Volume 12, Issue 3, pp 309–317 | Cite as

microRNA and Cancer

  • Mengfeng Li
  • Jun Li
  • Xiaofan Ding
  • Mian He
  • Shi-Yuan Cheng
Review Article Theme and Issue: siRNA and microRNA: From Target Validation to Therapy

Abstract

MicroRNAs (miRNAs), a class of small, regulatory, non-coding RNA molecules, display aberrant expression patterns and functional abnormalities in human diseases including cancers. This review summarizes the abnormally expressed miRNAs in various types of human cancers, possible mechanisms underlying such abnormalities, and miRNA-modulated molecular pathways critical for cancer development. Practical implications of miRNAs as biomarkers, novel drug targets and therapeutic tools for diagnosis, prognosis, and treatments of human cancers are also discussed.

Key words

biomarker cancer drug discovery drug target microRNA 

Notes

Grant supports

A Ministry of Science and Technology of China grant ([973]2005CB724605); a Natural Science Foundation of China grant (30872930); and a grant from the Science and Technology Department of the Zhuhai Municipality of Guangdong Province (PC20071076) to M.-F. Li; grants from the National Institutes of Health (CA102011, CA130966), American Cancer Society (RSG CSM-107144) and the Hillman Fellows Program for Innovative Cancer Research to S.-Y. Cheng.

References

  1. 1.
    Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009;10:704–14.PubMedGoogle Scholar
  2. 2.
    Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009;60:167–79.PubMedGoogle Scholar
  3. 3.
    Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.PubMedGoogle Scholar
  4. 4.
    Esquela-Kerscherand A, Slack FJ. Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer. 2006;6:259–69.Google Scholar
  5. 5.
    Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature. 2008;455:58–63.PubMedGoogle Scholar
  6. 6.
    Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. Short RNAs repress translation after initiation in mammalian cells. Mol Cell. 2006;21:533–42.PubMedGoogle Scholar
  7. 7.
    Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol. 2005;7:719–23.PubMedGoogle Scholar
  8. 8.
    Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A. 2008;105:1608–13.PubMedGoogle Scholar
  9. 9.
    Li LC, Okino ST, Zhao H, Pookot D, Place RF, Urakami S et al. Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci U S A. 2006;103:17337–42.PubMedGoogle Scholar
  10. 10.
    Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005;120:15–20.PubMedGoogle Scholar
  11. 11.
    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 U S A. 2002;99:15524–9.PubMedGoogle Scholar
  12. 12.
    Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 2004;64:3753–6.PubMedGoogle Scholar
  13. 13.
    Aguda BD, Kim Y, Piper-Hunter MG, Friedman A, Marsh CB. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci U S A. 2008;105:19678–83.PubMedGoogle Scholar
  14. 14.
    Iorio MV, Casalini P, Tagliabue E, Menard S, Croce CM. MicroRNA profiling as a tool to understand prognosis, therapy response and resistance in breast cancer. Eur J Cancer. 2008;44:2753–9.PubMedGoogle Scholar
  15. 15.
    Kondo N, Toyama T, Sugiura H, Fujii Y, Yamashita H. miR-206 expression is down-regulated in estrogen receptor alpha-positive human breast cancer. Cancer Res. 2008;68:5004–8.PubMedGoogle Scholar
  16. 16.
    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.PubMedGoogle Scholar
  17. 17.
    Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J, Benz CC. Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene. 2008;28:5643–7.Google Scholar
  18. 18.
    Scott GK, Goga A, Bhaumik D, Berger CE, Sullivan CS, Benz CC. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem. 2007;282:1479–86.PubMedGoogle Scholar
  19. 19.
    Hossain A, Kuo MT, Saunders GF. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol. 2006;26:8191–201.PubMedGoogle Scholar
  20. 20.
    Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szasz AM, Wang ZC et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell. 2009;137:1032–46.PubMedGoogle Scholar
  21. 21.
    Lehmann U, Hasemeier B, Christgen M, Muller M, Romermann D, Langer F et al. Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J Pathol. 2008;214:17–24.PubMedGoogle Scholar
  22. 22.
    Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ. Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem. 2009;284:5731–41.PubMedGoogle Scholar
  23. 23.
    Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007;131:1109–23.PubMedGoogle Scholar
  24. 24.
    Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL et al. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem. 2008;283:29897–903.PubMedGoogle Scholar
  25. 25.
    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;14:1340–8.PubMedGoogle Scholar
  26. 26.
    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;28:6773–84.PubMedGoogle Scholar
  27. 27.
    Mertens-Talcott SU, Chintharlapalli S, Li X, Safe S. The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells. Cancer Res. 2007;67:11001–11.PubMedGoogle Scholar
  28. 28.
    Pandeyand DP, Picard D. miR-22 inhibits estrogen signaling by directly targeting the estrogen receptor alpha mRNA. Mol Cell Biol. 2009;29:3783–90.Google Scholar
  29. 29.
    Zhu S, Si ML, Wu H, Mo YY. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem. 2007;282:14328–36.PubMedGoogle Scholar
  30. 30.
    Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.PubMedGoogle Scholar
  31. 31.
    Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 2008;10:202–10.PubMedGoogle Scholar
  32. 32.
    Fulci V, Chiaretti S, Goldoni M, Azzalin G, Carucci N, Tavolaro S et al. Quantitative technologies establish a novel microRNA profile of chronic lymphocytic leukemia. Blood. 2007;109:4944–51.PubMedGoogle Scholar
  33. 33.
    Dijkstra MK, van Lom K, Tielemans D, Elstrodt F, Langerak AW, van 't Veer MB et al. 17p13/TP53 deletion in B-CLL patients is associated with microRNA-34a downregulation. Leukemia. 2009;23:625–7.PubMedGoogle Scholar
  34. 34.
    Stamatopoulos B, Meuleman N, Haibe-Kains B, Saussoy P, Van Den Neste E, Michaux L et al. microRNA-29c and microRNA-223 down-regulation has in vivo significance in chronic lymphocytic leukemia and improves disease risk stratification. Blood. 2009;113:5237–45.PubMedGoogle Scholar
  35. 35.
    Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V et al. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 2006;66:11590–3.PubMedGoogle Scholar
  36. 36.
    Akao Y, Nakagawa Y, Kitade Y, Kinoshita T, Naoe T. Downregulation of microRNAs-143 and -145 in B-cell malignancies. Cancer Sci. 2007;98:1914–20.PubMedGoogle Scholar
  37. 37.
    Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103:2257–61.PubMedGoogle Scholar
  38. 38.
    Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, Hasan L et al. miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res. 2009;69:5553–9.PubMedGoogle Scholar
  39. 39.
    Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104:15805–10.PubMedGoogle Scholar
  40. 40.
    Nasser MW, Datta J, Nuovo G, Kutay H, Motiwala T, Majumder S et al. Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J Biol Chem. 2008;283:33394–405.PubMedGoogle Scholar
  41. 41.
    Kluiver J, Poppema S, de Jong D, Blokzijl T, Harms G, Jacobs S et al. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol. 2005;207:243–9.PubMedGoogle Scholar
  42. 42.
    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;435:828–33.PubMedGoogle Scholar
  43. 43.
    Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafre 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;282:23716–24.PubMedGoogle Scholar
  44. 44.
    Noonan EJ, Place RF, Pookot D, Basak S, Whitson JM, Hirata H et al. miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene. 2009;28:1714–24.PubMedGoogle Scholar
  45. 45.
    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;14:1271–7.PubMedGoogle Scholar
  46. 46.
    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;9:435–43.PubMedGoogle Scholar
  47. 47.
    Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science. 2008;322:1695–9.PubMedGoogle Scholar
  48. 48.
    Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65:6029–33.PubMedGoogle Scholar
  49. 49.
    Gilliesand JK, Lorimer IA. Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle. 2007;6:2005–9.Google Scholar
  50. 50.
    Wang Y, Lee AT, Ma JZ, Wang J, Ren J, Yang Y et al. Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J Biol Chem. 2008;283:13205–15.PubMedGoogle Scholar
  51. 51.
    Zhang X, Liu S, Hu T, Liu S, He Y, Sun S. Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology. 2009;50:490–9.PubMedGoogle Scholar
  52. 52.
    Connolly E, Melegari M, Landgraf P, Tchaikovskaya T, Tennant BC, Slagle BL et al. Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. Am J Pathol. 2008;173:856–64.PubMedGoogle Scholar
  53. 53.
    Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y et al. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 2009;69:1135–42.PubMedGoogle Scholar
  54. 54.
    Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S et al. Methylation mediated silencing of microRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res. 2008;68:5049–58.PubMedGoogle Scholar
  55. 55.
    Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, Liu CG et al. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 2007;67:6092–9.PubMedGoogle Scholar
  56. 56.
    Grady WM, Parkin RK, Mitchell PS, Lee JH, Kim YH, Tsuchiya KD et al. Epigenetic silencing of the intronic microRNA hsa-miR-342 and its host gene EVL in colorectal cancer. Oncogene. 2008;27:3880–8.PubMedGoogle Scholar
  57. 57.
    Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A. 2007;104:15472–7.PubMedGoogle Scholar
  58. 58.
    Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 2008;68:4123–32.PubMedGoogle Scholar
  59. 59.
    Slaby O, Svoboda M, Fabian P, Smerdova T, Knoflickova D, Bednarikova M et al. Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology. 2007;72:397–402.PubMedGoogle Scholar
  60. 60.
    Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2008;27:2128–36.PubMedGoogle Scholar
  61. 61.
    Liu T, Tang H, Lang Y, Liu M, Li X. MicroRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett. 2009;273:233–42.PubMedGoogle Scholar
  62. 62.
    Zhang Z, Li Z, Gao C, Chen P, Chen J, Liu W et al. miR-21 plays a pivotal role in gastric cancer pathogenesis and progression. Lab Invest. 2008;88:1358–66.PubMedGoogle Scholar
  63. 63.
    Takagi T, Iio A, Nakagawa Y, Naoe T, Tanigawa N, Akao Y. Decreased expression of microRNA-143 and -145 in human gastric cancers. Oncology. 2009;77:12–21.PubMedGoogle Scholar
  64. 64.
    Hu X, Macdonald DM, Huettner PC, Feng Z, El Naqa IM, Schwarz JK et al. A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol. 2009;114:457–64.PubMedGoogle Scholar
  65. 65.
    Yang H, Kong W, He L, Zhao JJ, O'Donnell JD, Wang J et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008;68:425–33.PubMedGoogle Scholar
  66. 66.
    Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res. 2007;67:8433–8.PubMedGoogle Scholar
  67. 67.
    Yan D, Zhou X, Chen X, Hu DN, Dong XD, Wang J et al. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest Ophthalmol Vis Sci. 2009;50:1559–65.PubMedGoogle Scholar
  68. 68.
    Mullerand DW, Bosserhoff AK. Integrin beta 3 expression is regulated by let-7a miRNA in malignant melanoma. Oncogene. 2008;27:6698–706.Google Scholar
  69. 69.
    Felicetti F, Errico MC, Bottero L, Segnalini P, Stoppacciaro A, Biffoni M et al. The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Res. 2008;68:2745–54.PubMedGoogle Scholar
  70. 70.
    Chang SS, Jiang WW, Smith I, Poeta LM, Begum S, Glazer C et al. MicroRNA alterations in head and neck squamous cell carcinoma. Int J Cancer. 2008;123:2791–7.PubMedGoogle Scholar
  71. 71.
    Liu X, Jiang L, Wang A, Yu J, Shi F, Zhou X. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett. 2009;286:217–22.PubMedGoogle Scholar
  72. 72.
    Childs G, Fazzari M, Kung G, Kawachi N, Brandwein-Gensler M, McLemore M et al. Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am J Pathol. 2009;174:736–45.PubMedGoogle Scholar
  73. 73.
    O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435:839–43.PubMedGoogle Scholar
  74. 74.
    Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R et al. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 2008;582:1564–8.PubMedGoogle Scholar
  75. 75.
    Braun CJ, Zhang X, Savelyeva I, Wolff S, Moll UM, Schepeler T et al. p53-Responsive micrornas 192 and 215 are capable of inducing cell cycle arrest. Cancer Res. 2008;68:10094–104.PubMedGoogle Scholar
  76. 76.
    Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 2008;6:14.PubMedGoogle Scholar
  77. 77.
    Yu Z, Wang C, Wang M, Li Z, Casimiro MC, Liu M et al. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol. 2008;182:509–17.PubMedGoogle Scholar
  78. 78.
    Leone G, DeGregori J, Sears R, Jakoi L, Nevins JR. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature. 1997;387:422–6.PubMedGoogle Scholar
  79. 79.
    Egle A, Harris AW, Bouillet P, Cory S. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc Natl Acad Sci U S A. 2004;101:6164–9.PubMedGoogle Scholar
  80. 80.
    Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S et al. p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A. 2009;106:3207–12.PubMedGoogle Scholar
  81. 81.
    Kong YW, Cannell IG, de Moor CH, Hill K, Garside PG, Hamilton TL et al. The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc Natl Acad Sci U S A. 2008;105:8866–71.PubMedGoogle Scholar
  82. 82.
    Kan T, Sato F, Ito T, Matsumura N, David S, Cheng Y et al. The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology. 2009;136:1689–700.PubMedGoogle Scholar
  83. 83.
    Park SY, Lee JH, Ha M, Nam JW, Kim VN. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol. 2009;16:23–9.PubMedGoogle Scholar
  84. 84.
    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;26:731–43.PubMedGoogle Scholar
  85. 85.
    Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A. 2008;105:13421–6.PubMedGoogle Scholar
  86. 86.
    Choy EY, Siu KL, Kok KH, Lung RW, Tsang CM, To KF et al. An Epstein–Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med. 2008;205:2551–60.PubMedGoogle Scholar
  87. 87.
    Jin WB, Wu FL, Kong D, Guo AG. HBV-encoded microRNA candidate and its target. Comput Biol Chem. 2007;31:124–6.PubMedGoogle Scholar
  88. 88.
    Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–71.PubMedGoogle Scholar
  89. 89.
    Chenand Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood. 2008;111:1217–26.Google Scholar
  90. 90.
    Wurdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J et al. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell. 2008;14:382–93.PubMedGoogle Scholar
  91. 91.
    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;68:7846–54.PubMedGoogle Scholar
  92. 92.
    Hu Z, Chen J, Tian T, Zhou X, Gu H, Xu L et al. Genetic variants of miRNA sequences and non-small cell lung cancer survival. J Clin Invest. 2008;118:2600–8.PubMedGoogle Scholar
  93. 93.
    Jazdzewski K, Murray EL, Franssila K, Jarzab B, Schoenberg DR, de la Chapelle A. Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma. Proc Natl Acad Sci U S A. 2008;105:7269–74.PubMedGoogle Scholar
  94. 94.
    Jazdzewski K, Liyanarachchi S, Swierniak M, Pachucki J, Ringel MD, Jarzab B et al. Polymorphic mature microRNAs from passenger strand of pre-miR-146a contribute to thyroid cancer. Proc Natl Acad Sci U S A. 2009;106:1502–5.PubMedGoogle Scholar
  95. 95.
    Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353:1793–801.PubMedGoogle Scholar
  96. 96.
    Diederichsand S, Haber DA. Sequence variations of microRNAs in human cancer: alterations in predicted secondary structure do not affect processing. Cancer Res. 2006;66:6097–104.Google Scholar
  97. 97.
    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 U S A. 2004;101:2999–3004.PubMedGoogle Scholar
  98. 98.
    Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD et al. Global variation in copy number in the human genome. Nature. 2006;444:444–54.PubMedGoogle Scholar
  99. 99.
    Ouillette P, Erba H, Kujawski L, Kaminski M, Shedden K, Malek SN. Integrated genomic profiling of chronic lymphocytic leukemia identifies subtypes of deletion 13q14. Cancer Res. 2008;68:1012–21.PubMedGoogle Scholar
  100. 100.
    Xi Y, Shalgi R, Fodstad O, Pilpel Y, Ju J. Differentially regulated micro-RNAs and actively translated messenger RNA transcripts by tumor suppressor p53 in colon cancer. Clin Cancer Res. 2006;12:2014–24.PubMedGoogle Scholar
  101. 101.
    Melo SA, Ropero S, Moutinho C, Aaltonen LA, Yamamoto H, Calin GA et al. A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genet. 2009;41:365–70.PubMedGoogle Scholar
  102. 102.
    Chiosea S, Jelezcova E, Chandran U, Acquafondata M, McHale T, Sobol RW et al. Up-regulation of dicer, a component of the microRNA machinery, in prostate adenocarcinoma. Am J Pathol. 2006;169:1812–20.PubMedGoogle Scholar
  103. 103.
    Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9:189–98.PubMedGoogle Scholar
  104. 104.
    Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL et al. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. Rna. 2008;14:2348–60.PubMedGoogle Scholar
  105. 105.
    Lebanony D, Benjamin H, Gilad S, Ezagouri M, Dov A, Ashkenazi K et al. Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol. 2009;27:2030–7.PubMedGoogle Scholar
  106. 106.
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105:10513–8.PubMedGoogle Scholar
  107. 107.
    Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10:42–6.PubMedGoogle Scholar
  108. 108.
    Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M et al. Silencing of microRNAs in vivo with ‘antagomirs’. Nature. 2005;438:685–9.PubMedGoogle Scholar
  109. 109.
    Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods. 2007;4:721–6.PubMedGoogle Scholar
  110. 110.
    Mercatelli N, Coppola V, Bonci D, Miele F, Costantini A, Guadagnoli M et al. The inhibition of the highly expressed miR-221 and miR-222 impairs the growth of prostate carcinoma xenografts in mice. PLoS One. 2008;3:e4029.PubMedGoogle Scholar
  111. 111.
    Stenvang J, Silahtaroglu AN, Lindow M, Elmen J, Kauppinen S. The utility of LNA in microRNA-based cancer diagnostics and therapeutics. Semin Cancer Biol. 2008;18:89–102.PubMedGoogle Scholar
  112. 112.
    Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S et al. LNA-mediated microRNA silencing in non-human primates. Nature. 2008;452:896–9.PubMedGoogle Scholar

Copyright information

© American Association of Pharmaceutical Scientists 2010

Authors and Affiliations

  • Mengfeng Li
    • 1
    • 2
  • Jun Li
    • 1
    • 3
  • Xiaofan Ding
    • 1
    • 3
  • Mian He
    • 1
    • 2
  • Shi-Yuan Cheng
    • 4
  1. 1.Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of EducationGuangzhouChina
  2. 2.Department of Microbiology, Zhongshan School of MedicineSun Yat-sen UniversityGuangzhouChina
  3. 3.Department of Biochemistry, Zhongshan School of MedicineSun Yat-sen UniversityGuangzhouChina
  4. 4.Cancer Institute and Departments of Pathology and MedicineUniversity of PittsburghPittsburghUSA

Personalised recommendations