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MicroRNAs: Biogenesis, Roles for Carcinogenesis and as Potential Biomarkers for Cancer Diagnosis and Prognosis

  • Kavitha, Nowroji (Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia) ;
  • Vijayarathna, Soundararajan (Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia) ;
  • Jothy, Subramanion Lachumy (Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia) ;
  • Oon, Chern Ein (Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia) ;
  • Chen, Yeng (Dental Research & Training Unit, and Oral Cancer Research and Coordinating Centre (OCRCC), Faculty of Dentistry, University of Malaya) ;
  • Kanwar, Jagat Rakesh (Nanomedicine-Laboratory of Immunology and Molecular Biomedical Research (NLIMBR), School of Medicine (SoM), Molecular and Medical Research (MMR) Strategic Research Centre, Faculty of Health, Deakin University) ;
  • Sasidharan, Sreenivasan (Institute for Research in Molecular Medicine (INFORMM), Universiti Sains Malaysia)
  • Published : 2014.10.11

Abstract

MicroRNAs (miRNAs) are short non-coding RNAs of 20-24 nucleotides that play important roles in carcinogenesis. Accordingly, miRNAs control numerous cancer-relevant biological events such as cell proliferation, cell cycle control, metabolism and apoptosis. In this review, we summarize the current knowledge and concepts concerning the biogenesis of miRNAs, miRNA roles in cancer and their potential as biomarkers for cancer diagnosis and prognosis including the regulation of key cancer-related pathways, such as cell cycle control and miRNA dysregulation. Moreover, microRNA molecules are already receiving the attention of world researchers as therapeutic targets and agents. Therefore, in-depth knowledge of microRNAs has the potential not only to identify their roles in cancer, but also to exploit them as potential biomarkers for cancer diagnosis and identify therapeutic targets for new drug discovery.

Keywords

References

  1. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-33. https://doi.org/10.1016/j.cell.2009.01.002
  2. Baumhoer D, Zillmer S, Unger K, et al (2012). MicroRNA profiling with correlation to gene expression revealed the oncogenic miR-17-92 cluster to be up-regulated in osteosarcoma. Cancer Genet, 205, 212-19. https://doi.org/10.1016/j.cancergen.2012.03.001
  3. Beitzinger M, Meister G (2010). MicroRNAs: from decay to decoy. Cell, 140, 612-14. https://doi.org/10.1016/j.cell.2010.02.020
  4. Berezikov E, Guryev V, Van De Belt J, et al (2005). Phylogenetic shadowing and computational identification of human microRNA genes. Cell, 120, 21-4. https://doi.org/10.1016/j.cell.2004.12.031
  5. Bhayani MK, Calin GA, Lai SY (2012). Functional relevance of miRNA* sequences in human disease. Mutat Res-Fund Mol M, 731, 14-9. https://doi.org/10.1016/j.mrfmmm.2011.10.014
  6. Bueno MJ, Malumbres M (2011). MicroRNAs and the cell cycle. Biochim Biophys Acta, 1812, 592-601. https://doi.org/10.1016/j.bbadis.2011.02.002
  7. Calin GA, Cimmino A, Fabbri M, et al (2008). MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci USA, 105, 5166-71. https://doi.org/10.1073/pnas.0800121105
  8. Calin GA, Croce CM (2006). MicroRNA signatures in human cancers. Nat Rev Cancer, 6, 857-66. https://doi.org/10.1038/nrc1997
  9. Carthew RW, Sontheimer EJ (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136, 642-55. https://doi.org/10.1016/j.cell.2009.01.035
  10. Chang CJ, Chao CH, Xia W, et al (2011). p53 regulates epithelialmesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol, 13, 317-23. https://doi.org/10.1038/ncb2173
  11. Corsini LR, Bronte G, Terrasi M, et al (2012). The role of microRNAs in cancer: diagnostic and prognostic biomarkers and targets of therapies. Expert Opin Ther Tar, 16, 103-9. https://doi.org/10.1517/14728222.2011.645805
  12. Cortez MA, Welsh JW, Calin GA (2012). Circulating microRNAs as noninvasive biomarkers in breast cancer. Rec Res Cancer Res, 195, 151-61. https://doi.org/10.1007/978-3-642-28160-0_13
  13. Croce CM (2013). Ultraconserved regions encoding ncRNAs. US Patent App. 2013, 13/910,410.
  14. Croce CM, Liu CG, Calin GA, Sevignani C (2010). Diagnosis and treatment of cancers with microRNA located in or near cancer associated chromosomal features. Patents, US20100234241 A1.
  15. Croce CM: Causes and consequences of microRNA dysregulation in cancer (2009). Nat Rev Genetics, 10, 704-14. https://doi.org/10.1038/nrg2634
  16. Deng G, Sui G (2013). Noncoding RNA in oncogenesis: a new era of identifying key players. Int J Mol Sci, 14, 18319-49. https://doi.org/10.3390/ijms140918319
  17. Duan W, Gao L, Wu X, et al (2010). MicroRNA-34a is an important component of PRIMA-1-induced apoptotic network in human lung cancer cells. Int J Cancer, 127, 313-20.
  18. Fabbri M, Garzon R, Cimmino A, et al (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA, 104, 15805-10. https://doi.org/10.1073/pnas.0707628104
  19. Farazi TA, Hoell JI, Morozov P, Tuschl T (2013). MicroRNAs in human cancer. Adv Exp Med Biol, 774, 1-20. https://doi.org/10.1007/978-94-007-5590-1_1
  20. Farooqi AA, Qureshi MZ, Coskunpinar E, et al (2014). miR-421, miR-155 and miR-650: Emerging trends of regulation of cancer and apoptosis. Asian Pac J Cancer Prev, 15, 1909-12. https://doi.org/10.7314/APJCP.2014.15.5.1909
  21. Fink SP, Kishore Guda D(2013) Application of next-generation sequencing in RNA biomarker discovery in cancer research, In next generation sequencing in cancer research, Wu, Wei, Choudhry, Hani (Eds.), Springer, 1, 383.
  22. Fornari F, Gramantieri L, Ferracin M, et al (2008). MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene, 27, 5651-61. https://doi.org/10.1038/onc.2008.178
  23. Frankel LB, Christoffersen NR, Jacobsen A, et al (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Bio Chem, 283, 1026-33. https://doi.org/10.1074/jbc.M707224200
  24. Garzon R, Heaphy CE, Havelange V, et al (2009). MicroRNA 29b functions in acute myeloid leukemia. Blood, 114, 5331-41. https://doi.org/10.1182/blood-2009-03-211938
  25. Garzon R, Marcucci G, Croce CM (2010). Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discovery, 9, 775-89. https://doi.org/10.1038/nrd3179
  26. Ghildiyal M, Zamore PD (2009). Small silencing RNAs: an expanding universe. Nat Rev Genet, 10, 94-108. https://doi.org/10.1038/nrg2504
  27. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005). Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell, 123, 631-40. https://doi.org/10.1016/j.cell.2005.10.022
  28. Griffiths-Jones S, Saini HK, Van Dongen S, Enright AJ (2008). miRBase: tools for microRNA genomics. Nucleic Acids Res, 36, 154-8. https://doi.org/10.1093/nar/gkn221
  29. Han J, Pedersen JS, Kwon SC, et al (2009). Posttranscriptional crossregulation between Drosha and DGCR8. Cell, 136, 75-84. https://doi.org/10.1016/j.cell.2008.10.053
  30. Hanke M, Hoefig K, Merz H, et al (2010). A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. In: Urologic Oncology: Seminars and Original Investigations, 11, 655-61.
  31. He L, He X, Lowe SW, Hannon GJ (2007). microRNAs join the p53 network-another piece in the tumour-suppression puzzle. Nat Rev Cancer, 7, 819-22. https://doi.org/10.1038/nrc2232
  32. Heneghan HM, Miller N, Kerin MJ (2010). MiRNAs as biomarkers and therapeutic targets in cancer. Curr Opin Pharmacol, 10, 543-50. https://doi.org/10.1016/j.coph.2010.05.010
  33. Hu Z, Chen X, Zhao Y, et al (2010). Serum MicroRNA signatures identified in a genome-wide serum MicroRNA expression profiling predict survival of non-small-cell lung cancer. J Clin Oncol, 28, 1721-6. https://doi.org/10.1200/JCO.2009.24.9342
  34. Iliopoulos D, Lindahl-Allen M, Polytarchou C, et al (2010). Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell, 39, 761-72. https://doi.org/10.1016/j.molcel.2010.08.013
  35. Inui M, Martello G, Piccolo S (2010). MicroRNA control of signal transduction. Nat Rev Mol Cell Biol, 11, 252-63. https://doi.org/10.1038/nrn2804
  36. Iorio MV, Casalini P, Piovan C, Braccioli L, Tagliabue E (2012). Current and future developments in cancer therapy research: mirnas as new promising targets or tools. In Biotargets of Cancer in Current Clinical Practice, Bologna, M. (Ed.), Springer. XVI, 563.
  37. Iorio MV, Croce CM (2012). MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med, 4, 143-59. https://doi.org/10.1002/emmm.201100209
  38. Iorio MV, Croce CM (2012). microRNA involvement in human cancer. Carcinogenesis, 33, 1126-33. https://doi.org/10.1093/carcin/bgs140
  39. Iorio MV, Ferracin M, Liu CG, et al (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Res, 65, 7065-70. https://doi.org/10.1158/0008-5472.CAN-05-1783
  40. Jansson MD, Lund AH (2012). MicroRNA and cancer. Mol Oncol, 6, 590-610. https://doi.org/10.1016/j.molonc.2012.09.006
  41. Josephine WD, Cui M, Shibata R, Cheng L, Zhang DY (2013). Diagnostic methodology and technology. In Molecular Genetic Pathology, Cheng, Liang, Zhang, David Y., Eble, John N. (Eds.), Springer, 2nd ed., XXI, 1136 p.
  42. Karreth FA, Tay Y, Perna D, et al (2011). In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAFinduced mouse model of melanoma. Cell, 147, 382-95. https://doi.org/10.1016/j.cell.2011.09.032
  43. Khan N, Cheng J, Pezacki JP, Berezovski MV (2011). Quantitative analysis of microRNA in blood serum with protein-facilitated affinity capillary electrophoresis. Anal Chem, 83, 6196-01. https://doi.org/10.1021/ac2016213
  44. Kim VN, Han J, Siomi MC (2009). Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol, 10, 126-39. https://doi.org/10.1038/nrm2632
  45. Kobayashi E, Hornicek FJ, Duan Z (2012). MicroRNA involvement in osteosarcoma. Clin Sarcoma Res, 12, 359-739.
  46. Kong YW, Ferland-Mccollough D, Jackson TJ, Bushell M (2012). microRNAs in cancer management. The Lancet Oncol, 13, 249-258. https://doi.org/10.1016/S1470-2045(12)70073-6
  47. Krell J, Frampton AE, Colombo T, et al (2013). The p53 miRNA interactome and its potential role in the cancer clinic. Epigenomics, 5, 417-28. https://doi.org/10.2217/epi.13.41
  48. Krol J, Loedige I, Filipowicz W (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet, 11, 597-610.
  49. Kumar MS, Pester RE, Chen CY, et al (2009). Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev, 23, 2700-4. https://doi.org/10.1101/gad.1848209
  50. Lawrie CH (2008). MicroRNA expression in lymphoid malignancies: new hope for diagnosis and therapy? J Cell Mol Med, 12, 1432-44. https://doi.org/10.1111/j.1582-4934.2008.00399.x
  51. Lee RC, Feinbaum, RL, d Ambros V (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843-54. https://doi.org/10.1016/0092-8674(93)90529-Y
  52. Lhakhang TW, Chaudhry M (2012). Current approaches to micro-RNA analysis and target gene prediction. J App Gene, 53, 149-58. https://doi.org/10.1007/s13353-011-0060-2
  53. Lim LP, Lau NC, Garrett-Engele P, et al (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 433, 769-73. https://doi.org/10.1038/nature03315
  54. Lin C, Huang F, Zhang Y, Tuokan T, Kuerban G. (2014). Roles of MiR-101 and its target gene cox-2 in early diagnosis of cervical cancer in Uygur women. Asian Pac J Cancer Prev, 15, 45-8. https://doi.org/10.7314/APJCP.2014.15.1.45
  55. Link A, Balaguer F, Shen Y, et al (2010). MicroRNAs as novel biomarkers for colon cancer screening. Cancer Epidem Biomar Prev, 19, 1766-74. https://doi.org/10.1158/1055-9965.EPI-10-0027
  56. Liu R, Zhang C, Hu Z, et al (2011). A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur J Cancer, 47, 784-91. https://doi.org/10.1016/j.ejca.2010.10.025
  57. Lopez-Serra P, Esteller M (2011). DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene, 31, 1609-22.
  58. Lujambio A, Calin GA, Villanueva A, et al (2008). A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA, 105, 13556-61. https://doi.org/10.1073/pnas.0803055105
  59. Lujambio A, Lowe SW (2012). The microcosmos of cancer. Nature, 482, 347-55. https://doi.org/10.1038/nature10888
  60. Malumbres M, Barbacid M (2001). Milestones in cell division: to cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer, 1, 222-31. https://doi.org/10.1038/35106065
  61. Martinez NJ, Gregory RI (2013). Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA, 19, 605-12. https://doi.org/10.1261/rna.036434.112
  62. Mcbride O, Merry D, Givol D (1986). The gene for human p53 cellular tumor antigen is located on chromosome 17 short arm (17p13). Proc Natl Acad Sci U.S.A, 83, 130-4. https://doi.org/10.1073/pnas.83.1.130
  63. Melo SA, Esteller M (2011). A precursor microRNA in a cancer cell nucleus: get me out of here! Cell Cycle, 10, 922-5. https://doi.org/10.4161/cc.10.6.15119
  64. Melo SA, Esteller M (2011). Dysregulation of microRNAs in cancer: playing with fire. FEBS Letters, 585, 2087-99. https://doi.org/10.1016/j.febslet.2010.08.009
  65. Melo SA, Moutinho C, Ropero S, et al (2010). A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer cell, 18, 303-15. https://doi.org/10.1016/j.ccr.2010.09.007
  66. Melo SA, Ropero S, Moutinho C, et al (2009). A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genetics, 41, 365-70. https://doi.org/10.1038/ng.317
  67. Meng F, Henson R, Wehbe-Janek H, et al (2007). MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology, 133, 647-58. https://doi.org/10.1053/j.gastro.2007.05.022
  68. Mitchell PS, Tewari M (2010). Circulating microRNAs in cancer. In Kikuchi Y. and Rykova EY. (Eds.), Nucleic acids and molecular biology series: extracellular nucleic acids, Springer, 129-46.
  69. Mollaie HR, Monavari SH, Arabzadeh SA, et al (2013). RNAi and miRNA in viral infections and cancers. Asian Pac J Cancer Prev, 14, 7045-56. https://doi.org/10.7314/APJCP.2013.14.12.7045
  70. Nana-Sinkam SP, Croce CM (2011). MicroRNAs as therapeutic targets in cancer. Transl Res, 157, 216-25. https://doi.org/10.1016/j.trsl.2011.01.013
  71. Nishida N, Mimori K, Mori M, Calin GA (2013). EGFR gets in the way of microRNA biogenesis. Cell Research, 23, 1157-8. https://doi.org/10.1038/cr.2013.87
  72. Ofir M, Hacohen D, Ginsberg D (2011). MiR-15 and miR-16 are direct transcriptional targets of E2F1 that limit E2F-induced proliferation by targeting cyclin E. Mol Cancer Res, 9, 440-7. https://doi.org/10.1158/1541-7786.MCR-10-0344
  73. Orang AV, Safaralizadeh R, Hosseinpour Feizi MA (2014). Insights into the diverse roles of miR-205 in human cancers. Asian Pac J Cancer Prev, 15, 577-583. https://doi.org/10.7314/APJCP.2014.15.2.577
  74. Parasramka MA, Ho E, Williams DE, Dashwood RH (2012). MicroRNAs, diet, and cancer: new mechanistic insights on the epigenetic actions of phytochemicals. Mol Carcinogen, 51, 213-30. https://doi.org/10.1002/mc.20822
  75. Petrocca F, Visone R, Onelli MR, et al (2008). E2F1-regulated microRNAs impair TGF$\beta$-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell, 13, 272-86. https://doi.org/10.1016/j.ccr.2008.02.013
  76. Ramshankar V, Krishnamurthy A (2013). Lung cancer detection by screening - presenting circulating miRNAs as a promising next generation biomarker breakthrough. Asian Pac J Cancer Prev, 14, 2167-72. https://doi.org/10.7314/APJCP.2013.14.4.2167
  77. Reinhart BJ, Slack FJ, Basson M, et al (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901-6. https://doi.org/10.1038/35002607
  78. Ruby JG, Jan CH, Bartel DP (2007). Intronic microRNA precursors that bypass Drosha processing. Nature, 448, 83-6. https://doi.org/10.1038/nature05983
  79. Saito Y, Liang G, Egger G, et al (2006). Specific activation of microRNA-127 with downregulation of the proto-oncogene by chromatin-modifying drugs in human cancer cells. Cancer Cell, 9, 435-43. https://doi.org/10.1016/j.ccr.2006.04.020
  80. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011). A ceRNA hypothesis: the rosetta stone of a hidden RNA language? Cell, 146, 353-8. https://doi.org/10.1016/j.cell.2011.07.014
  81. Sanchez-Diaz PC, Hsiao TH, Chang JC, et al (2013). Deregulated microRNAs in pediatric cancer stem cells target pathways involved in cell proliferation, cell cycle and development. PloS One, 8, 61622. https://doi.org/10.1371/journal.pone.0061622
  82. Shen J, Xia W, Khotskaya YB, et al (2013). EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature, 497, 383-7. https://doi.org/10.1038/nature12080
  83. Stenvang J, Silahtaroglu AN, Lindow M, Elmen J, Kauppinen S (2008). The utility of LNA in microRNA-based cancer diagnostics and therapeutics. Semin Cancer Biol, 18, 89-102. https://doi.org/10.1016/j.semcancer.2008.01.004
  84. Streichert T, Otto B, Lehmann U (2011). MicroRNA profiling using fluorescence-labeled beads: data acquisition and processing. Methods Mol Biol, 676, 253-68. https://doi.org/10.1007/978-1-60761-863-8_18
  85. Streichert T, Otto B, Lehmann U (2012). microRNA expression profiling in archival tissue specimens: methods and data processing. Mol Biotechnol, 50, 159-69. https://doi.org/10.1007/s12033-011-9427-1
  86. Su X, Chakravarti D, Cho MS, et al (2010). TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature, 467, 986-90. https://doi.org/10.1038/nature09459
  87. Su X, Xing J, Wang Z, et al (2013). microRNAs and ceRNAs:RNA networks in pathogenesis of cancer. Chin J Cancer Res, 25, 235-9.
  88. Suzuki HI, Yamagata K, Sugimoto K, et al (2009). Modulation of microRNA processing by p53. Nature, 460, 529-33. https://doi.org/10.1038/nature08199
  89. Taby R, Issa JPJ (2010). Cancer epigenetics. CA Cancer J Clin, 60, 376-92. https://doi.org/10.3322/caac.20085
  90. Toyota M, Suzuki H, Sasaki Y, et al (2008). Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res, 68, 4123-32. https://doi.org/10.1158/0008-5472.CAN-08-0325
  91. Van Kouwenhove M, Kedde M, Agami R (2011). MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer, 11, 644-56. https://doi.org/10.1038/nrc3107
  92. Varambally S, Cao Q, Mani RS, et al (2008). Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science, 322, 1695-9. https://doi.org/10.1126/science.1165395
  93. Vasudevan S, Tong Y, Steitz JA (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931-4. https://doi.org/10.1126/science.1149460
  94. Volinia S, Calin GA, Liu CG, et al (2006). A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA, 103, 2257-61. https://doi.org/10.1073/pnas.0510565103
  95. Volinia S, Galasso M, Sana ME, et al (2012). Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc Natl Acad Sci USA, 109, 3024-9. https://doi.org/10.1073/pnas.1200010109
  96. Wan SM, Lv F, Guan T (2012). Identification of genes and microRNAs involved in ovarian carcinogenesis. Asian Pac J Cancer Prev, 13, 3997-4000. https://doi.org/10.7314/APJCP.2012.13.8.3997
  97. Wong KY, Yu L, Chim CS (2011). DNA methylation of tumor suppressor miRNA genes: a lesson from the miR-34 family. Epigenomics, 3, 83-92. https://doi.org/10.2217/epi.10.74
  98. Wynendaele J, Bohnke A, Leucci E, et al (2010). An illegitimate microRNA target site within the 3'UTR of MDM4 affects ovarian cancer progression and chemosensitivity. Cancer Res, 70, 9641-9. https://doi.org/10.1158/0008-5472.CAN-10-0527
  99. Xu L, Dai WQ, Xu XF, et al (2012). Effects of multiple-target anti-microRNA antisense oligodeoxyribonucleotides on proliferation and migration ofgastric cancer cells. Asian Pac J Cancer Prev, 13, 3203-7. https://doi.org/10.7314/APJCP.2012.13.7.3203
  100. Zenz T, Mohr J, Eldering E, et al (2009). miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood, 113, 3801-8. https://doi.org/10.1182/blood-2008-08-172254
  101. Zhao SF, Zhang X, Zhang XJ, et al (2014). Induction of MicroRNA-9 mediates cytotoxicity of curcumin against SKOV3 ovarian cancer cells. Asian Pac J Cancer Prev, 15, 3363-8. https://doi.org/10.7314/APJCP.2014.15.8.3363

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