European Journal of Cancer
Volume 46, Issue 2 , Pages 298-311 , January 2010

MicroRNAs: Predictors and modifiers of chemo- and radiotherapy in different tumour types

  • Richard Hummel

      Affiliations

    • Department of Surgery, Flinders Medical Centre, Flinders University, Flinders Drive, 5042 Bedford Park SA, Adelaide, Australia
  • ,
  • Damian J. Hussey

      Affiliations

    • Department of Surgery, Flinders Medical Centre, Flinders University, Flinders Drive, 5042 Bedford Park SA, Adelaide, Australia
  • ,
  • Joerg Haier

      Affiliations

    • Comprehensive Cancer Center Muenster, University Hospital Muenster, University of Muenster, Waldeyerstrasse 1, 48149 Muenster, Germany
    • Corresponding Author InformationCorresponding author: Tel.: +49 251 83 57630; fax: +49 251 83 57631.

Received 8 September 2009 ,Revised 20 October 2009 ,Accepted 29 October 2009.

References 

  1. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature. 2004;429(6990):457–463
  2. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;3(6):415–428
  3. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006;31(2):89–97[Epub 2006 January 5. Review]
  4. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer – a mechanism for early oncogenic pathway addiction?. Nat Rev Cancer. 2006;6(2):107–116[Review]
  5. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat Genet. 1999;21(2):163–167
  6. Chuang JC, Jones PA. Epigenetics and microRNAs. Pediatr Res. 2007;61(5 Pt 2):24R–29R[Review]
  7. Sigalotti L, Fratta E, Coral S, et al. Epigenetic drugs as pleiotropic agents in cancer treatment: biomolecular aspects and clinical applications. J Cell Physiol. 2007;212(2):330–344[Review]
  8. Mulero-Navarro S, Esteller M. Epigenetic biomarkers for human cancer: the time is now. Crit Rev Oncol Hematol. 2008;68(1):1–11[Epub 2008 Apr 21. Review]
  9. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. MiRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36:D154–D158
  10. Garzon R, Fabbri M, Cimmino A, Calin GA, Croce CM. MicroRNA expression and function in cancer. Trends Mol Med. 2006;12(12):580–587[Epub 2006 October 30. Review]
  11. Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol. 2007;302(1):1–12[Epub 2006 August 16. Review]
  12. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–297
  13. Ambros V. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing. Cell. 2003;113(6):673–676[Review. Erratum in: Cell 2003;114(2):269]
  14. Cowland JB, Hother C, Grønbaek K. MicroRNAs and cancer. APMIS. 2007;115(10):1090–1106
  15. 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
  16. Brennecke J, Stark A, Russell RB, Cohen SM. Principles of microRNA-target recognition. PLoS Biol. 2005;3:e85
  17. Lim LP, Lau NC, Garrett-Engele P, et al. Microarray analysis shows that some microRNAs downregulate large numbers of targetmRNAs. Nature. 2005;433:769–773
  18. 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. 2006;9(6):435–443
  19. Saito Y, Friedman JM, Chihara Y, et al. Epigenetic therapy upregulates the tumor suppressor microRNA-126 and its host gene EGFL7 in human cancer cells. Biochem Biophys Res Commun. 2009;379(3):726–731[Epub 2008 December 29]
  20. 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 USA. 2004;101(9):2999–3004[Epub 2004 February 18]
  21. Michael MZ, O’Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res. 2003;1(12):882–891
  22. Yanaihara N, Caplen N, Bowman E, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9(3):189–198
  23. Cho WC. OncomiRs: the discovery and progress of microRNAs in cancers. Mol Cancer. 2007;6:60
  24. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–838
  25. Kuehbacher A, Urbich C, Dimmeler S. Targeting microRNA expression to regulate angiogenesis. Trends Pharmacol Sci. 2008;29(1):12–15[Epub 2007 December 18]
  26. Calin GA, Ferracin M, Cimmino A, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793–1801[Erratum in: N Engl J Med 2006;355(5):533]
  27. Eder M, Scherr M. MicroRNA and lung cancer. N Engl J Med. 2005;352:2446–2448
  28. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435(7043):828–833
  29. Lu Z, Liu M, Stribinskis V, et al. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene. 2008;27(31):4373–4379[Epub 2008 March 31]
  30. Blower PE, Verducci JS, Lin S, et al. MicroRNA expression profiles for the NCI-60 cancer cell panel. Mol Cancer Ther. 2007;6(5):1483–1491[Epub 2007 May 4]
  31. Kovalchuk O, Filkowski J, Meservy J, et al. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther. 2008;7(7):2152–2159
  32. Boren T, Xiong Y, Hakam A, et al. MicroRNAs and their target messenger RNAs associated with ovarian cancer response to chemotherapy. Gynecol Oncol. 2009;113(2):249–255[Epub 2009 February 23]
  33. Xia L, Zhang D, Du R, et al. MiR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer. 2008;123(2):372–379
  34. Miller TE, Ghoshal K, Ramaswamy B, et al. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem. 2008;283(44):29897–29903[Epub 2008 August 15]
  35. Yang N, Kaur S, Volinia S, et al. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res. 2008;68(24):10307–10314
  36. Koturbash I, Boyko A, Rodriguez-Juarez R, et al. Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis. 2007;28(8):1831–1838[Epub 2007 March 7]
  37. Ilnytskyy Y, Koturbash I, Kovalchuk O. Radiation-induced bystander effects in vivo are epigenetically regulated in a tissue-specific manner. Environ Mol Mutagen. 2009;50(2):105–113
  38. Weidhaas JB, Babar I, Nallur SM, et al. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res. 2007;67(23):11111–11116
  39. Josson S, Sung SY, Lao K, Chung LW, Johnstone PA. Radiation modulation of microRNA in prostate cancer cell lines. Prostate. 2008;68(15):1599–1606
  40. Duale N, Lindeman B, Komada M, et al. Molecular portrait of cisplatin induced response in human testis cancer cell lines based on gene expression profiles. Mol Cancer. 2007;6:53
  41. Rossi L, Bonmassar E, Faraoni I. Modification of miR gene expression pattern in human colon cancer cells following exposure to 5-fluorouracil in vitro. Pharmacol Res. 2007;56(3):248–253[Epub 2007 July 10]
  42. Calin GA, Croce CM. MicroRNA signatures in human cancer. Nat Rev Cancer. 2006;6:857–866
  43. Volinia S, Calin GA, Liu CG, et al. A microRNAexpression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103:2257–2261
  44. 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. 2006;130(7):2113–2129
  45. Si ML, Zhu S, Wu H, et al. miR-21-mediated tumor growth. Oncogene. 2007;26(19):2799–2803[Epub 2006 October 30]
  46. Bandres E, Cubedo E, Agirre X, et al. Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer. 2006;5:29–38
  47. Meng F, Henson R, Wehbe-Janek H. Etal. The MicroRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangiocytes. J Biol Chem. 2007;282:8256–8264
  48. Salter KH, Acharya CR, Walters KS, et al. An integrated approach to the prediction of chemotherapeutic response in patients with breast cancer. PLoS ONE. 2008;3(4):e1908
  49. Sun M, Estrov Z, Ji Y, et al. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol Cancer Ther. 2008;7(3):464–473
  50. Zhao HY, Ooyama A, Yamamoto M, et al. Down regulation of c-Myc and induction of an angiogenesis inhibitor, thrombospondin-1, by 5-FU in human colon cancer KM12C cells. Cancer Lett. 2008;270(1):156–163[Epub 2008 June 25]
  51. Yang L, Belaguli N, Berger DH. MicroRNA and colorectal cancer. World J Surg. 2009;[Epub ahead of print]
  52. Svoboda M, Izakovicova Holla L, Sefr R, et al. Micro-RNAs miR125b and miR137 are frequently upregulated in response to capecitabine chemoradiotherapy of rectal cancer. Int J Oncol. 2008;33(3):541–547
  53. 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
  54. Blower PE, Chung JH, Verducci JS, et al. MicroRNAs modulate the chemosensitivity of tumor cells. Mol Cancer Ther. 2008;7(1):1–9[Epub 2008 January 9]
  55. Nasser MW, Datta J, Nuovo G, 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(48):33394–33405[Epub 2008 September 25]
  56. Bu Y, Lu C, Bian C, et al. Knockdown of Dicer in MCF-7 human breast carcinoma cells results in G1 arrest and increased sensitivity to cisplatin. Oncol Rep. 2009;21(1):13–17
  57. Fontana L, Fiori ME, Albini S, et al. Antagomir-17–5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS ONE. 2008;3(5):e2236
  58. Fujita Y, Kojima K, Hamada N, et al. Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochem Biophys Res Commun. 2008;377(1):114–119[Epub 2008 October 1]
  59. Michan S, Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem J. 2007;404:1–13
  60. Ji Q, Hao X, Meng Y, et al. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer. 2008;8:266
  61. Yang H, Kong W, He L, et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 2008;68(2):425–433[Erratum in: Cancer Res 2008;68(5):1609]
  62. Lo AK, To KF, Lo KW, et al. Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci USA. 2007;104(41):16164–16169[Epub 2007 October 2]
  63. Tsang WP, Kwok TT. Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis. 2008;13(10):1215–1222
  64. Su H, Yang JR, Xu T, et al. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 2009;69(3):1135–1142[Epub 2009 January 20]
  65. Tsuchiya Y, Nakajima M, Takagi S, Taniya T, Yokoi T. MicroRNA regulates the expression of human cytochrome P450 1B1. Cancer Res. 2006;66(18):9090–9098
  66. Shimada T, Hayes CL, Yamazaki H, et al. Activation of chemically diverse procarcinogens by human cytochrome P450 1B1. Cancer Res. 1996;56:2979–2984
  67. Spink D, Spink B, Cao J, et al. Induction of cytochrome P450 1B1 and catechol estrogen metabolism in ACHN human renal adenocarcinoma cells. J Steroid Biochem Mol Biol. 1997;62:223–232
  68. Henderson IC, Canellos GP. Cancer of the breast: the past decade (first of two parts). N Engl J Med. 1980;302:17–30
  69. Ingelman-Sundberg M, Sim SC, Gomez A, Rodriguez-Antona C. Influence of cytochrome P450 polymorphisms on drug therapies: pharmacogenetic, pharmacoepigenetic and clinical aspects. Pharmacol Ther. 2007;116(3):496–526[Epub 2007 October 9. Review]
  70. Herr I, Ucur E, Herzer K, et al. Glucocorticoid cotreatment induces apoptosis resistance toward cancer therapy in carcinomas. Cancer Res. 2003;63(12):3112–3120
  71. Rainer J, Ploner C, Jesacher S, et al. Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia. 2009;[Epub ahead of print]
  72. Vreugdenhil E, Verissimo CS, Mariman R, et al. MicroRNAs miR-18 and miR-124a Downregulate the Glucocorticoid Receptor: Implications for Glucocorticoid Responsiveness in the Brain. Endocrinology. 2009;150(5):2220–2228[Epub 2009 January 8]
  73. 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. 2008;283(45):31079–31086[Epub 2008 September 12]
  74. 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(13):5004–5008
  75. Merritt WM, Lin YG, Han LY, et al. Dicer, Drosha, and outcomes in patients with ovarian cancer. N Engl J Med. 2008;359(25):2641–2650
  76. Nakajima G, Hayashi K, Xi Y, et al. Non-coding MicroRNAs hsa-let-7g and hsa-miR-181b are Associated with Chemoresponse to S-1 in Colon Cancer. Cancer Genom Proteom. 2006;3(5):317–324
  77. Schetter AJ, Leung SY, Sohn JJ, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008;299(4):425–436
  78. Sorrentino A, Liu CG, Addario A, et al. Role of microRNAs in drug-resistant ovarian cancer cells. Gynecol Oncol. 2008;111(3):478–486[Epub 2008 September 26]
  79. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med. 2009;15(1):31–33[Epub 2009 January 4]
  80. Weiss GJ, Bemis LT, Nakajima E, et al. EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. Ann Oncol. 2008;19(6):1053–1059[Epub 2008 February 27]
  81. Gal H, Makovitzki A, Amariglio N, et al. A rapid assay for drug sensitivity of glioblastoma stem cells. Biochem Biophys Res Commun. 2007;358:908–913
  82. Gal H, Pandi G, Kanner AA, et al. MIR-451 and Imatinib mesylate inhibit tumor growth of glioblastoma stem cells. Biochem Biophys Res Commun. 2008;376(1):86–90[Epub 2008 August 31]
  83. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654–659[Epub 2007 May 7]
  84. Hunter MP, Ismail N, Zhang X, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008;3(11):e3694;[Epub 2008 November 11]
  85. Chim SS, Shing TK, Hung EC, et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem. 2008;54(3):482–490[Epub 2008 January 24]
  86. Gilad S, Meiri E, Yogev Y, et al. Serum microRNAs are promising novel biomarkers. PLoS One. 2008;3(9):e3148
  87. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105(30):10513–10518[Epub 2008 July 28]
  88. Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470–1476[Epub 2008 November 16]
  89. Rosell R, Wei J, Taron M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin Lung Cancer. 2009;10(1):8–9[No abstract available]
  90. Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteom. 2009;6(3):267–283
  91. Chen X, Ba Y, Ma L, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18(10):997–1006
  92. Resnick KE, Alder H, Hagan JP, et al. The detection of differentially expressed microRNAs from the serum of ovarian cancer patients using a novel real-time PCR platform. Gynecol Oncol. 2009;112(1):55–59[Epub 2008 October 26]
  93. Zhu W, Qin W, Atasoy U, Sauter ER. Circulating microRNAs in breast cancer and healthy subjects. BMC Res Notes. 2009;2:89
  94. Lawrie CH, Gal S, Dunlop HM, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol. 2008;141(5):672–675[Epub 2008 March 3]
  95. Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009;10(1):42–46
  96. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110(1):13–21
  97. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Kerin MJ. MicroRNAs as novel biomarkers for breast cancer. J Oncol. 2009;2009:950201;[Epub 2009 July 20]
  98. Chin LJ, Slack FJ. A truth serum for cancer – microRNAs have major potential as cancer biomarkers. Cell Res. 2008;18(10):983–984
  99. Grimm D. Small silencing RNAs: state-of-the-art. Adv Drug Deliv Rev. 2009;61(9):672–703[Epub 2009 May 7. Review]
  100. Wang K, Zhang S, Marzolf B, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA. 2009;106(11):4402–4407[Epub 2009 February 25]
  101. Shih KK, Levine DA. Exosomal microRNAs step into the biomarker arena. Gynecol Oncol. 2008;110(1):1–2
  102. Michael A, Bajracharya SD, Yuen PS, et al. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2009;[Epub ahead of print]

PII: S0959-8049(09)00814-4

doi: 10.1016/j.ejca.2009.10.027

European Journal of Cancer
Volume 46, Issue 2 , Pages 298-311 , January 2010