Prospects of miRNA-based therapy for pancreatic cancer

Current Drug Targets

Volumn 14, Issue 10, 2013, Pages 1101-1109

  Pai, Priya ^a   Rachagani, Satyanarayana ^a   Are, Chandrakanth ^a   Batra, Surinder K ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

MiRNA; Pancreatic cancer; Therapy

Indexed keywords

ANTAGOMIR; ANTI MIR OLIGONUCLEOTIDES; ANTINEOPLASTIC AGENT; CYCLIN D2; EXPORTIN 5; GEMCITABINE; LET 7; LIPOSOME; LOCKED NUCLEIC ACID; MICRO RNA 196A; MICRO RNA 216A; MICRO RNA 217; MICRORNA; MICRORNA 122; MICRORNA 155; MICRORNA 200; MICRORNA 20A; MICRORNA 21; MICRORNA 210; MICRORNA 221; MICRORNA 26A; MICRORNA 29; MICRORNA 34A; MICRORNA ANTAGONIST; MIRAVIRSEN; RNA INDUCED SILENCING COMPLEX; STAT3 PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; UVOMORULIN;

ADENO ASSOCIATED VIRUS; APOPTOSIS; BIOGENESIS; BREAST CANCER; CANCER THERAPY; CELL CYCLE ARREST; CELL PROLIFERATION; DISEASE COURSE; DRUG DELIVERY SYSTEM; ENDOSCOPIC ULTRASOUND GUIDED FINE NEEDLE BIOPSY; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEPATITIS C; HUMAN; LUNG CANCER; LUNG NON SMALL CELL CANCER; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; REVIEW; SPLENOMEGALY; SPONGE; SURVIVAL RATE; TUMOR DIFFERENTIATION;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; RNA-BINDING PROTEINS;

EID: 84881357000     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/13894501113149990181     Document Type: Review

References (105)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62: 10-29.
2. Matsuno S, Egawa S, Fukuyama S, et al. Pancreatic Cancer Registry in Japan: 20 years of experience. Pancreas 2004; 28: 219-30.
3. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-97.
4. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123: 631-40.
5. Carthew RW. Gene regulation by microRNAs. Curr Opin Genet Dev 2006; 16: 203-8.
6. Pasquinelli AE, Reinhart BJ, Slack F, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000; 408: 86-89.
7. Chen JF, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006; 38: 228-33.
8. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005; 436: 214-20.
9. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303: 83-6.
10. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834-838.
11. Gao Y, Schug J, McKenna LB, et al. Tissue-specific regulation of mouse microRNA genes in endoderm-derived tissues. Nucleic Acids Res 2011; 39: 454-63.
12. Bloomston M, Frankel WL, Petrocca F, et al. MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 2007; 297: 1901-8.
13. Calin GA, Dumitru CD, Shimizu M, 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: 15524-9.
14. Calin GA, Liu CG, Sevignani C, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci USA 2004; 101: 11755-60.
15. Jiang J, Lee EJ, Gusev Y, Schmittgen TD. Real-time expression profiling of microRNA precursors in human cancer cell lines. Nucleic Acids Res 2005; 33: 5394-403.
16. Lee EJ, Gusev Y, Jiang J, et al. Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 2007; 120: 1046-54.
17. Metzler M, Wilda M, Busch K, Viehmann S, Borkhardt A. High expression of precursor microRNA-155/BIC RNA in children with Burkitt lymphoma. Genes Chromosomes Cancer 2004; 39: 167-9.
18. 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: 882-91.
19. Takamizawa J, Konishi H, Yanagisawa K, 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.
20. Caldas C, Brenton JD. Sizing up miRNAs as cancer genes. Nat Med 2005; 11: 712-4.
21. Croce CM, Calin GA. miRNAs, cancer, and stem cell division. Cell 2005; 122: 6-7.
22. Esquela-Kerscher A and Slack FJ. Oncomirs -microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-69.
23. McManus MT. MicroRNAs and cancer. Semin Cancer Biol 2003; 13: 253-8.
24. Meltzer PS. Cancer genomics: small RNAs with big impacts. Nature 2005; 435: 745-6.
25. Olson P, Lu J, Zhang H, et al. MicroRNA dynamics in the stages of tumorigenesis correlate with hallmark capabilities of cancer. Genes Dev 2009; 23: 2152-65.
26. Chang TC, Wentzel EA, Kent OA, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26: 745-52.
27. 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 2005; 102: 13944-9.
28. Johnson SM, Grosshans H, Shingara J, et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120: 635-47.
29. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-34.
30. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003; 17: 3011-6.
31. Singh SK, Pal BM, Girschick HJ, Bhadra U. MicroRNAs--micro in size but macro in function. FEBS J 2008; 275: 4929-44.
32. 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: 10513-8.
33. Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M. microRNAs in cancer management. Lancet Oncol 2012; 13: e249-e258.
34. Rothe F, Ignatiadis M, Chaboteaux C, et al. Global microRNA expression profiling identifies MiR-210 associated with tumor proliferation, invasion and poor clinical outcome in breast cancer. PLoS One 2011; 6: e20980.
35. Weber JA, Baxter DH, Zhang S, et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010; 56: 1733-41.
36. Wang K, Zhang S, Marzolf B, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 2009; 106: 4402-7.
37. Valadi H, Ekstrom 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: 654-9.
38. Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108: 5003-8.
39. Pigati L, Yaddanapudi SC, Iyengar R, et al. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One 2010; 20;5: e13515.
40. Montgomery RL and van RE. Therapeutic advances in MicroRNA targeting. J Cardiovasc Pharmacol 2011; 57: 1-7.
41. Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012; 3: 1-3.
42. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438: 685-9.
43. Thum T, Gross C, Fiedler J, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008; 456: 980-4.
44. Care A, Catalucci D, Felicetti F, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007; 13: 613-618.
45. Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012; 3: 1-3.
46. Lanford RE, Hildebrandt-Eriksen ES, Petri A, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327: 198-201.
47. Gumireddy K, Young DD, Xiong X, et al. Small-molecule inhibitors of microrna miR-21 function. Angew Chem Int Ed Engl 2008; 47: 7482-4.
48. Young DD, Connelly CM, Grohmann C, Deiters A. Small molecule modifiers of microRNA miR-122 function for the treatment of hepatitis C virus infection and hepatocellular carcinoma. J Am Chem Soc 2010; 132: 7976-81.
49. Bose D, Jayaraj GG, Kumar S, Maiti S. A Molecular-Beacon-Based Screen for Small Molecule Inhibitors of miRNA Maturation. ACS Chem Biol 2013; 8(5): 930-8.
50. Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA 2010; 16: 2043-50.
51. Bader AG, Brown D, Stoudemire J, Lammers P. Developing therapeutic microRNAs for cancer. Gene Ther 2011; 18: 1121-6.
52. Wang V, Wu W. MicroRNA-based therapeutics for cancer. BioDrugs 2009; 23: 15-23.
53. Trang P, Wiggins JF, Daige CL, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther 2011; 19: 1116-22.
54. Li L, Xie X, Luo J, et al. Targeted expression of miR-34a using the T-VISA system suppresses breast cancer cell growth and invasion. Mol Ther 2012; 20: 2326-34.
55. Kota J, Chivukula RR, O'Donnell KA, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137: 1005-17.
56. Janssen HL, Reesink HW, Lawitz EJ, et al. Treatment of HCV Infection by Targeting MicroRNA. N Engl J Med 2013; 368(18): 1685-94.
57. Bader AG. miR-34 -a microRNA replacement therapy is headed to the clinic. Front Genet 2012; 3: 120.
58. Petrocca F, Lieberman J. Micromanipulating cancer: microRNAbased therapeutics? RNA Biol 2009; 6: 335-40.
59. Long XB, Sun GB, Hu S, et al. Let-7a microRNA functions as a potential tumor suppressor in human laryngeal cancer. Oncol Rep 2009; 22: 1189-95.
60. Esquela-Kerscher A, Trang P, Wiggins JF, et al. The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle 2008; 7: 759-64.
61. Torrisani J, Bournet B, du Rieu MC, et al. let-7 MicroRNA transfer in pancreatic cancer-derived cells inhibits in vitro cell proliferation but fails to alter tumor progression. Hum Gene Ther 2009; 20: 831-44.
62. 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.
63. Schetter AJ, Leung SY, Sohn JJ, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008; 299: 425-36.
64. 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 2008; 27: 2128-36.
65. 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.
66. Meng F, Henson R, Wehbe-Janek H, et al. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007; 133: 647-58.
67. Garchow BG, Bartulos EO, Leung YT, et al. Silencing of microRNA-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol Med 2011; 3: 605-15.
68. Wu CW, Ng SS, Dong YJ, et al. Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut 2012; 61: 739-45.
69. Gao W, Lu X, Liu L, et al. MiRNA-21: a biomarker predictive for platinum-based adjuvant chemotherapy response in patients with non-small cell lung cancer. Cancer Biol Ther 2012; 13: 330-40.
70. Liu R, Chen X, Du Y, et al. Serum microRNA expression profile as a biomarker in the diagnosis and prognosis of pancreatic cancer. Clin Chem 2012; 58: 610-8.
71. Seike M, Goto A, Okano T, et al. MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proc Natl Acad Sci USA 2009; 106: 12085-90.
72. Ji J, Shi J, Budhu A, et al. MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 2009; 361: 1437-47.
73. Lu J, He ML, Wang L, et al. MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res 2011; 71: 225-33.
74. Sander S, Bullinger L, Wirth T. Repressing the repressor: a new mode of MYC action in lymphomagenesis. Cell Cycle 2009; 8: 556-9.
75. Liu XX, Li XJ, Zhang B, et al. MicroRNA-26b is underexpressed in human breast cancer and induces cell apoptosis by targeting SLC7A11. FEBS Lett 2011; 585: 1363-7.
76. Mavrakis KJ, Van Der Meulen J, Wolfe AL, et al. A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL). Nat Genet 2011; 43: 673-8.
77. Huse JT, Brennan C, Hambardzumyan D, et al. The PTENregulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 2009; 23: 1327-37.
78. Zhao JJ, Lin J, Lwin T, et al. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 2010; 115: 2630-9.
79. Santanam U, Zanesi N, Efanov A, et al. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci USA 2010; 107: 12210-5.
80. Han YC, Park CY, Bhagat G, et al. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 2010; 207: 475-489.
81. 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 USA 2007; 104: 15805-10.
82. Rokhlin OW, Scheinker VS, Taghiyev AF, et al. MicroRNA-34 mediates AR-dependent p53-induced apoptosis in prostate cancer. Cancer Biol Ther 2008; 7: 1288-96.
83. Dillhoff M, Liu J, Frankel W, Croce C, Bloomston M. MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival. J Gastrointest Surg 2008; 12: 2171-6.
84. Ali S, Almhanna K, Chen W, Philip PA, Sarkar FH. Differentially expressed miRNAs in the plasma may provide a molecular signature for aggressive pancreatic cancer. Am J Transl Res 2010; 3: 28-47.
85. Schultz NA, Andersen KK, Roslind A, et al. Prognostic microRNAs in cancer tissue from patients operated for pancreatic cancer--five microRNAs in a prognostic index. World J Surg 2012; 36: 2699-707.
86. Matthaei H, Wylie D, Lloyd MB, et al. miRNA biomarkers in cyst fluid augment the diagnosis and management of pancreatic cysts. Clin Cancer Res 2012; 18: 4713-24.
87. Habbe N, Koorstra JB, Mendell JT, et al. MicroRNA miR-155 is a biomarker of early pancreatic neoplasia. Cancer Biol Ther 2009; 8: 340-6.
88. Kawaguchi T, Komatsu S, Ichikawa D, et al. Clinical impact of circulating miR-221 in plasma of patients with pancreatic cancer. Br J Cancer 2013; 108: 361-9.
89. Wang J, Chen J, Chang P, et al. MicroRNAs in plasma of pancreatic ductal adenocarcinoma patients as novel blood-based biomarkers of disease. Cancer Prev Res (Phila) 2009; 2: 807-13.
90. Park JK, Lee EJ, Esau C, Schmittgen TD. Antisense inhibition of microRNA-21 or -221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 2009; 38: e190-9.
91. Moriyama T, Ohuchida K, Mizumoto K, et al. MicroRNA-21 modulates biological functions of pancreatic cancer cells including their proliferation, invasion, and chemoresistance. Mol Cancer Ther 2009; 8: 1067-74.
92. Hwang JH, Voortman J, Giovannetti E, et al. Identification of microRNA-21 as a biomarker for chemoresistance and clinical outcome following adjuvant therapy in resectable pancreatic cancer. PLoS One 2010; 5: e10630.
93. Cai B, An Y, Lv N, et al. miRNA-181b increases the sensitivity of pancreatic ductal adenocarcinoma cells to gemcitabine in vitro and in nude mice by targeting BCL-2. Oncol Rep 2013; 29: 1769-76.
94. Li A, Omura N, Hong SM, et al. Pancreatic cancers epigenetically silence SIP1 and hypomethylate and overexpress miR-200a/200b in association with elevated circulating miR-200a and miR-200b levels. Cancer Res 2010; 70: 5226-37.
95. Yan H, Wu J, Liu W, et al. MicroRNA-20a overexpression inhibited proliferation and metastasis of pancreatic carcinoma cells. Hum Gene Ther 2010; 21: 1723-34.
96. Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003; 4: 437-50.
97. Yu S, Lu Z, Liu C, et al. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res 2010; 70: 6015-25.
98. Weiss FU, Marques IJ, Woltering JM, et al. Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology 2009; 137: 2136-45.
99. Mees ST, Mardin WA, Sielker S, et al. Involvement of CD40 targeting miR-224 and miR-486 on the progression of pancreatic ductal adenocarcinomas. Ann Surg Oncol 2009; 16: 2339-50.
100. Ji Q, Hao X, Zhang M, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009; 4: e6816.
101. Li Y, Vandenboom TG, Wang Z, et al. miR-146a suppresses invasion of pancreatic cancer cells. Cancer Res 2010; 70: 1486-95.
102. Chen C, Zhang Y, Zhang L, Weakley SM, Yao Q. MicroRNA-196: critical roles and clinical applications in development and cancer. J Cell Mol Med 2011; 15: 14-23.
103. Zhao WG, Yu SN, Lu ZH, et al. The miR-217 microRNA functions as a potential tumor suppressor in pancreatic ductal adenocarcinoma by targeting KRAS. Carcinogenesis 2010; 31: 1726-33.
104. Hou B, Jian Z, Chen S, et al. [Expression of miR-216a in pancreatic cancer and its clinical significance]. Nan Fang Yi Ke Da Xue Xue Bao 2012; 32: 1628-31.
105. Park JY, Helm J, Coppola D, et al. MicroRNAs in pancreatic ductal adenocarcinoma. World J Gastroenterol 2011; 17: 817-27.