MicroRNAs in cancer: Small molecules with a huge impact

Journal of Clinical Oncology

Volumn 27, Issue 34, 2009, Pages 5848-5856

  Iorio, Marilena V ^a   Croce, Carlo M ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 106B-25; MICRORNA 10B; MICRORNA 122A; MICRORNA 125B; MICRORNA 15; MICRORNA 155; MICRORNA 15A; MICRORNA 16-1; MICRORNA 17-92; MICRORNA 181; MICRORNA 19A; MICRORNA 19B; MICRORNA 200; MICRORNA 205; MICRORNA 21; MICRORNA 221; MICRORNA 29; MICRORNA 34A; MICRORNA 373; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANGIOGENESIS; BREAST CANCER; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER INVASION; CANCER THERAPY; CARCINOGENESIS; CHRONIC LYMPHATIC LEUKEMIA; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; HUMAN; LIVER CELL CARCINOMA; LUNG CANCER; LYMPHOMA; METASTASIS; MULTIPLE MYELOMA; ONCOGENE; PRIORITY JOURNAL; PROGNOSIS; REVIEW; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; ANIMAL; DRUG ANTAGONISM; GENETIC EPIGENESIS; GENETICS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 73349125465     PISSN: 0732183X     EISSN: None     Source Type: Journal    
DOI: 10.1200/JCO.2009.24.0317     Document Type: Review

References (105)

1. Lee RC, Feinbaum RL, Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843-854, 1993
2. Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116:281-297, 2004
3. Calin GA, Dumitru CD, Shimizu M, et al: Frequent deletions and down-regulation of microRNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 99:15524-15529, 2002
4. Calin GA, Sevignani C, Dumitru CD, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A 101:2999-3004, 2004
5. Pekarsky Y, Santanam U, Cimmino A, et al: Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res 66:11590-11593, 2006
6. Calin GA, Ferracin M, Cimmino A, et al: A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353:1793-1801, 2005
7. Cimmino A, Calin GA, Fabbri M, et al: MiR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 102:13944-13949, 2005
8. Mott JL, Kobayashi S, Bronk SF, et al: Mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26:6133-6140, 2007
9. Metzler M, Wilda M, Busch K, et al: High expression of precursor microRNA-155/BIC RNA in children with Burkitt lymphoma. Genes Chromosomes Cancer 39:167-169, 2004
10. Kluiver J, Poppema S, de JD, et al: BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol 207:243-249, 2005
11. Costinean S, Zanesi N, Pekarsky Y, et al: Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci U S A 103:7024-7029, 2006
12. He L, Thomson JM, Hemann MT, et al: A microRNA polycistron as a potential human oncogene. Nature 435:828-833, 2005
13. Xiao C, Srinivasan L, Calado DP, et al: Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9:405-414, 2008
14. O'Donnell KA, Wentzel EA, Zeller KI, et al: C-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839-843, 2005
15. Petrocca F, Visone R, Onelli MR, et al: E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13:272-286, 2008
16. Löffler D, Brocke-Heidrich K, Pfeifer G, et al: Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110:1330-1333, 2007
17. Pichiorri F, Suh SS, Ladetto M, et al: MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc Natl Acad Sci U S A 105:12885-12890, 2008
18. Iorio MV, Ferracin M, Liu CG, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65:7065-7070, 2005
19. Yan LX, Huang XF, Shao Q, et al: MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14:2348-2360, 2008
20. Qian B, Katsaros D, Lu L, et al: High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and high TGF-beta1. Breast Cancer Res Treat 117:131-140, 2009
21. Scott GK, Goga A, Bhaumik D, et al: Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 282:1479-1486, 2007
22. Iorio MV, Casalini P, Piovan C, et al: MicroRNA-205 regulates HER3 in human breast cancer. Cancer Res 69:2195-2200, 2009
23. Wu H, Zhu S, Mo YY: Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19:439-448, 2009
24. Ma L, Teruya-Feldstein J, Weinberg RA:. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:682-688, 2007
25. Huang Q, Gumireddy K, Schrier M, et al: The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10:202-210, 2008
26. Gregory PA, Bracken CP, Bert AG, et al: MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 7:3112-3118, 2008
27. Park SM, Gaur AB, Lengyel E, et al: The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22:894-907, 2008
28. Yanaihara N, Caplen N, Bowman E, et al: Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9:189-198, 2006
29. Johnson SM, Grosshans H, Shingara J, et al: RAS is regulated by the let-7 microRNA family. Cell 120:635-647, 2005
30. Mayr C, Hemann MT, Bartel DP: Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315:1576-1579, 2007
31. Sampson VB, Rong NH, Han J, et al: MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 67:9762-9770, 2007
32. Yu SL, Chen HY, Chang GC, et al: MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell 13:48-57, 2008
33. Gramantieri L, Ferracin M, Fornari F, et al: Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res 67:6092-6099, 2007
34. Fornari F, Gramantieri L, Ferracin M, et al: MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 27:5651-5661, 2008
35. He L, He X, Lim LP, et al: A microRNA component of the p53 tumour suppressor network. Nature 447:1130-1134, 2007
36. Raveche ES, Salerno E, Scaglione BJ, et al: Abnormal microRNA-16 locus with synteny to human 13q14 linked to CLL in NZB mice. Blood 109:5079-5086, 2007
37. Calin GA, Cimmino A, Fabbri M, et al: MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci U S A 105:5166-5171, 2008
38. Garzon R, Volinia S, Liu CG, et al: MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 111:3183-3189, 2008
39. Le Beau MM, Albain KS, Larson RA, et al: Clinical and cytogenetic correlations in 63 patients with therapy-related myelodysplastic syndromes and acute nonlymphocytic leukemia: Further evidence for characteristic abnormalities of chromosomes no. 5 and 7. J Clin Oncol 4:325-345, 1986
40. Fabbri M, Garzon R, Cimmino A, 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 104:15805-15810, 2007
41. Wang H, Garzon R, Sun H, et al: NF-kappaBYY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 14:369-381, 2008
42. Garzon R, Liu S, Fabbri M, et al: MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene re-expression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 113:6411-6418, 2009
43. Tam W, Hughes SH, Hayward WS, et al: Avian bic, a gene isolated from a common retroviral site in avian leukosis virus-induced lymphomas that encodes a noncoding RNA, cooperates with c-myc in lymphomagenesis and erythroleukemogenesis. J Virol 76:4275-4286, 2002
44. Thai TH, Calado DP, Casola S, et al: Regulation of the germinal center response by microRNA-155. Science 316:604-608, 2007
45. Rodriguez A, Vigorito E, Clare S, et al: Requirement of bic/microRNA-155 for normal immune function. Science 316:608-611, 2007
46. Tili E, Michaille JJ, Cimino A, et al: Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 179:5082-5089, 2007
47. Ronchetti D, Lionetti M, Mosca L, et al: An integrative genomic approach reveals coordinated expression of intronic miR-335, miR-342, and miR-561 with deregulated host genes in multiple myeloma. BMC Med Genomics 1:37, 2008
48. Chan JA, Krichevsky AM, Kosik KS: MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029-6033, 2005
49. Ciafrè SA, Galardi S, Mangiola A, et al: Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334:1351-1358, 2005
50. Iorio MV, Visone R, Di LG, et al: MicroRNA signatures in human ovarian cancer. Cancer Res 67:8699-8707, 2007
51. Markou A, Tsaroucha EG, Kaklamanis L, et al: Prognostic value of mature microRNA-21 and microRNA-205 overexpression in non-small cell lung cancer by quantitative real-time RT-PCR. Clin Chem 54:1696-1704, 2008
52. Volinia S, Calin GA, Liu CG, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103:2257-2261, 2006
53. Schetter AJ, Leung SY, Sohn JJ, et al: MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 299:425-436, 2008
54. Roldo C, Missiaglia E, Hagan JP, et al: MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24:4677-4684, 2006
55. Bloomston M, Frankel WL, Petrocca F, et al: MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 297:1901-1908, 2007
56. Blenkiron C, Goldstein LD, Thorne NP, et al: MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 8:R214, 2007
57. Miller TE, Ghoshal K, Ramaswamy B, et al: MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 283:29897-29903, 2008
58. Zhao JJ, Lin J, Yang H, et al: MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem 283:31079-31086, 2008
59. Di Leva G, Gasparini P, Piovan C: A regulatory "miRcircuitry" involving miR-221&222 and ERα determines ERα status of breast cancer cells. J Natl Cancer Inst (in press)
60. Yu F, Yao H, Zhu P, et al: Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131:1109-1123, 2007
61. Kumar MS, Erkeland SJ, Pester RE, et al: Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A 105:3903-3908, 2008
62. Lebanony D, Benjamin H, Gilad S, et al: Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol 27:2030-2037, 2009
63. Murakami Y, Yasuda T, Saigo K, et al: Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25:2537-2545, 2006
64. Li W, Xie L, He X, et al: Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int J Cancer 123:1616-1622, 2008
65. Visone R, Pallante P, Vecchione A, et al: Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene 26:7590-7595, 2007
66. le Sage C, Nagel R, Egan DA, et al: Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26:3699-3708, 2007
67. Galardi S, Mercatelli N, Giorda E, et al: MiR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 282:23716-23724, 2007
68. Felicetti F, Errico MC, Bottero L, et al: The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Res 68:2745-2754, 2008
69. Zhang L, Huang J, Yang N, et al: MicroRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci U S A 103:9136-9141, 2006
70. Li N, Fu H, Tie Y, et al: MiR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 275:44-53, 2009
71. Gandellini P, Folini M, Longoni N, et al: MiR-205 Exerts tumor-suppressive functions in human prostate through down-regulation of protein kinase Cepsilon. Cancer Res 69:2287-2295, 2009
72. Asangani IA, Rasheed SA, Nikolova DA, et al: MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27:2128-2136, 2008
73. Zhu S, Wu H, Wu F, et al: MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18:350-359, 2008
74. Tavazoie SF, Alarcon C, Oskarsson T, et al: Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451:147-152, 2008
75. Rosenfeld N, Aharonov R, Meiri E, et al: MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26:462-469, 2008
76. Poliseno L, Tuccoli A, Mariani L, et al: MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108:3068-3071, 2006
77. Hua Z, Lv Q, Ye W, et al: MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 1:e116, 2006
78. Mertens-Talcott SU, Chintharlapalli S, Li X, et al: 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 67:11001-11011, 2007
79. Fish JE, Santoro MM, Morton SU, et al: MiR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15:272-284, 2008
80. Pulkkinen K, Malm T, Turunen M, et al: Hypoxia induces miR-210 in vitro and in vivo ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210. FEBS Lett 582:2397-2401, 2008
81. Dews M, Homayouni A, Yu D, et al: Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38:1060-1065, 2006
82. Kuehbacher A, Urbich C, Zeiher AM, et al: Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 101:59-68, 2007
83. Hu Z, Chen J, Tian T, et al: Genetic variants of miRNA sequences and non-small cell lung cancer survival. J Clin Invest 118:2600-2608, 2008
84. Thomson JM, Newman M, Parker JS, et al: Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 20:2202-2207, 2006
85. Nakamura T, Canaani E, Croce CM: Oncogenic All1 fusion proteins target Drosha-mediated microRNA processing. Proc Natl Acad Sci U S A 104:10980-10985, 2007
86. Karube Y, Tanaka H, Osada H, et al: Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 96:111-115, 2005
87. Merritt WM, Lin YG, Han LY, et al: Dicer, Drosha, and outcomes in patients with ovarian cancer. N Engl J Med 359:2641-2650, 2008
88. Weber B, Stresemann C, Brueckner B, et al: Methylation of human microRNA genes in normal and neoplastic cells. Cell Cycle 6:1001-1005, 2007
89. Saito Y, Liang G, Egger G, et al: Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9:435-443, 2006
90. Lehmann U, Hasemeier B, Christgen M, et al: Epigenetic inactivation of microRNA gene hsamir-9-1 in human breast cancer. J Pathol 214:17-24, 2008
91. Toyota M, Suzuki H, Sasaki 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 68:4123-4132, 2008
92. Brueckner B, Stresemann C, Kuner R, et al: The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res 67:1419-1423, 2007
93. Lujambio A, Ropero S, Ballestar E, et al: Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 67:1424-1429, 2007
94. Scott GK, Mattie MD, Berger CE, et al: Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res 66:1277-1281, 2006
95. Benetti R, Gonzalo S, Jaco I, et al: A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 15:268-279, 2008
96. Sinkkonen L, Hugenschmidt T, Berninger P, et al: MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat Struct Mol Biol 15:259-267, 2008
97. Chen JF, Mandel EM, Thomson JM, et al: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228-233, 2006
98. Si ML, Zhu S, Wu H, et al: MiR-21-mediated tumor growth. Oncogene 26:2799-2803, 2007
99. Meng F, Henson R, Lang M, et al: Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130:2113-2129, 2006
100. Weidhaas JB, Babar I, Nallur SM, et al: MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res 67:11111-11116, 2007
101. Weiler J, Hunziker J, Hall J: Anti-miRNA oligonucleotides (AMOs): Ammunition to target miRNAs implicated in human disease? Gene Ther 13:496-502, 2006
102. ∅rom UA, Kauppinen S, Lund AH: LNAmodified oligonucleotides mediate specific inhibition of microRNA function. Gene 372:137-141, 2006
103. Krützfeldt J, Rajewsky N, Braich R, et al: Silencing of microRNAs in vivo with 'antagomirs.' Nature 438:685-689, 2005
104. Ebert MS, Neilson JR, Sharp PA: MicroRNA sponges: Competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721-726, 2007
105. Dykxhoorn DM, Palliser D, Lieberman J: The silent treatment: SiRNAs as small molecule drugs. Gene Ther 13:541-552, 2006