MicroRNA dysregulation in esophageal neoplasia: The biological rationale for novel therapeutic options

Current Pharmaceutical Design

Volumn 19, Issue 7, 2013, Pages 1236-1241

  Fassan, Matteo ^a   Baffa, Raffaele ^b   Kiss, András ^c   Zaninotto, Giovanni ^a   Rugge, Massimo ^a,d  

^a UNIVERSITY OF PADOVA   (Italy)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

Author keywords

Biomarkers; Esophageal cancer; MiRNAs; Preneoplastic lesions

Indexed keywords

ANTINEOPLASTIC AGENT; BONE MORPHOGENETIC PROTEIN 6; CISPLATIN; DOUBLE STRANDED DNA; FLUOROURACIL; K RAS PROTEIN; LOCKED NUCLEIC ACID; MICRORNA; MICRORNA 10B; MICRORNA 143; MICRORNA 21; MIRAVIRSEN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR GATA 6;

APOPTOSIS; ARTICLE; BARRETT ADENOCARCINOMA; BARRETT ESOPHAGUS; CANCER ADJUVANT THERAPY; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER MORTALITY; CANCER PATIENT; CANCER PROGNOSIS; CARCINOGENESIS; DISEASE SEVERITY; DRUG TARGETING; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; ESOPHAGUS MUCOSA; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; HISTOPATHOLOGY; HUMAN; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TISSUE SECTION; TREATMENT RESPONSE; TUMOR SUPPRESSOR GENE;

EID: 84876715427     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319070007     Document Type: Article

References (88)

1. 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.
2. 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.
3. 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: 1793-801.
4. Visone R, Petrocca F, Croce CM. Micro-RNAs in gastrointestinal and liver disease. Gastroenterology 2008; 135: 1866-9.
5. Fassan M, Croce CM, Rugge M. miRNAs in precancerous lesions of the gastrointestinal tract. World J Gastroenterol 2011; 17: 5231-9.
6. Fassan M, Sachsenmeir K, Rugge M, Baffa R. Role of miRNA in distinguishing primary brain tumors from secondary tumors metastatic to the brain. Front Biosci (Schol Ed) 2011; 3: 970-9.
7. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 2010; 9: 775-89.
8. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10: 704-14.
9. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-33.
10. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350-5.
11. Farazi TA, Spitzer JI, Morozov P, Tuschl T. miRNAs in human cancer. J Pathol 2011; 223: 102-15.
12. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011; 12: 861-74.
13. Lopez-Serra P, Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 2012; 31: 1609-22.
14. 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: 2999-3004.
15. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-61.
16. Volinia S, Galasso M, Costinean S, et al. Reprogramming of miRNA networks in cancer and leukemia. Genome Res 2010; 20: 589-99.
17. Nair VS, Maeda LS, Ioannidis JP. Clinical outcome prediction by microRNAs in human cancer: a systematic review. J Natl Cancer Inst 2012; 104: 528-40.
18. Hoefig KP, Thorns C, Roehle A, et al. Unlocking pathology archives for microRNA-profiling. Anticancer Res 2008; 28: 119-23.
19. Wheeler G, Valoczi A, Havelda Z, Dalmay T. In situ detection of animal and plant microRNAs. DNA Cell Biol 2007; 26: 251-5.
20. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 2011; 11: 849-64.
21. Sandhu S, Garzon R. Potential applications of microRNAs in cancer diagnosis, prognosis, and treatment. Semin Oncol 2011; 38: 781-7.
22. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012; 148: 1172-87.
23. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med 2003; 349: 2241-52.
24. Thallinger CM, Raderer M, Hejna M. Esophageal cancer: a critical evaluation of systemic second-line therapy. J Clin Oncol 2011; 29: 4709-14.
25. van Hagen P, Hulshof MC, van Lanschot JJ, et al. CROSS Group. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 2012; 366: 2074-84.
26. Hummel R, Watson DI, Smith C, et al. Mir-148a improves response to chemotherapy in sensitive and resistant oesophageal adenocarcinoma and squamous cell carcinoma cells. J Gastrointest Surg 2011; 15: 429-38.
27. Imanaka Y, Tsuchiya S, Sato F, Shimada Y, Shimizu K, Tsujimoto G. MicroRNA-141 confers resistance to cisplatin-induced apoptosis by targeting YAP1 in human esophageal squamous cell carcinoma. J Hum Genet 2011; 56: 270-6.
28. Hong L, Han Y, Zhang H, et al. The prognostic and chemotherapeutic value of miR-296 in esophageal squamous cell carcinoma. Ann Surg 2010; 251: 1056-63.
29. Zhang H, Li M, Han Y, et al. Down-regulation of miR-27a might reverse multidrug resistance of esophageal squamous cell carcinoma. Dig Dis Sci 2010; 55: 2545-51.
30. Hamano R, Miyata H, Yamasaki M, et al. Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res 2011; 17: 3029-38.
31. Obad S, dos Santos CO, Petri A, et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet 2011; 43: 371-8.
32. Stenvang J, Lindow M, Kauppinen S. Targeting of microRNAs for therapeutics. Biochem Soc Trans 2008; 36: 1197-200.
33. Elmén J, Lindow M, Schütz S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008; 452: 896-9.
34. Landford 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.
35. Zaninotto G, Minnei F, Guirroli E, et al. The Veneto Region's Barrett's Oesophagus Registry: aims, methods, preliminary results. Dig Liver Dis 2007; 39: 18-25.
36. Varghese S, Lao-Sirieix P, Fitzgerald RC. Identification and clinical implementation of biomarkers for Barrett's esophagus. Gastroenterology 2012; 142: 435-441.
37. Fiocca R, Mastracci L, Milione M, Parente P, Savarino V. Gruppo Italiano Patologi Apparato Digerente (GIPAD); Società Italiana di Anatomia Patologica e Citopatologia Diagnostica/International Academy of Pathology, Italian division (SIAPEC/IAP). Microscopic esophagitis and Barrett's esophagus: the histology report. Dig Liver Dis 2011;43 Suppl 4: S319-30.
38. Fassan M, Mastracci L, Grillo F, et al. Early HER2 dysregulation in gastric and oesophageal carcinogenesis. Histopathology 2012; In Press.
39. Segat D, Cassaro M, Dazzo E, et al. Pericentriolar material analyses in normal esophageal mucosa, Barrett's metaplasia and adenocarcinoma. Histol Histopathol 2010; 25: 551-60.
40. Rugge M, Fassan M, Zaninotto G, et al. Aurora kinase A in Barrett's carcinogenesis. Hum Pathol 2010; 41: 1380-6.
41. Kan T, Meltzer SJ. MicroRNAs in Barrett's esophagus and esophageal adenocarcinoma. Curr Opin Pharmacol 2009; 9: 727-32.
42. Smith CM, Watson DI, Michael MZ, Hussey DJ. MicroRNAs, development of Barrett's esophagus, and progression to esophageal adenocarcinoma. World J Gastroenterol 2010; 16: 531-7.
43. Feber A, Xi L, Luketich JD, et al. MicroRNA expression profiles of esophageal cancer. J Thorac Cardiovasc Surg 2008; 135: 255-60; discussion 260.
44. Hino K, Tsuchiya K, Fukao T, et al. Inducible expression of microRNA-194 is regulated by HNF-1alpha during intestinal epithelial cell differentiation. RNA 2008; 14: 1433-4
45. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, et al. miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ 2008; 15: 1187-95.
46. Yi R, Poy MN, Stoffel M, Fuchs E. A skin microRNA promotes differentiation by repressing 'stemness'. Nature 2008; 452: 225-9.
47. Mathé EA, Nguyen GH, Bowman ED, et al. MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res 2009; 15: 6192-200.
48. Yang H, Gu J, Wang KK, et al. MicroRNA expression signatures in Barrett's esophagus and esophageal adenocarcinoma. Clin Cancer Res 2009; 15: 5744-52.
49. Wijnhoven BP, Hussey DJ, Watson DI, Tsykin A, Smith CM, Michael MZ. South Australian Oesophageal Research Group. MicroRNA profiling of Barrett's oesophagus and oesophageal adenocarcinoma. Br J Surg 2010; 97: 853-61.
50. Fassan M, Volinia S, Palatini J, et al. MicroRNA expression profiling in human Barrett's carcinogenesis. Int J Cancer 2011; 129: 1661-70.
51. Bansal A, Lee IH, Hong X, et al. Feasibility of mcroRNAs as biomarkers for Barrett's Esophagus progression: a pilot crosssectional, phase 2 biomarker study. Am J Gastroenterol 2011; 106: 1055-63.
52. Fassan M, Pizzi M, Battaglia G, et al. Programmed cell death 4 (PDCD4) expression during multistep Barrett's carcinogenesis. J Clin Pathol 2010; 63: 692-6.
53. Kimura S, Naganuma S, Susuki D, et al. Expression of microRNAs in squamous cell carcinoma of human head and neck and the esophagus: miR-205 and miR-21 are specific markers for HNSCC and ESCC. Oncol Rep 2010; 23: 1625-33.
54. Maru DM, Singh RR, Hannah C, et al. MicroRNA-196a is a potential marker of progression during Barrett's metaplasia-dysplasiainvasive adenocarcinoma sequence in esophagus. Am J Pathol 2009; 174: 1940-8.
55. Luzna P, Gregar J, Uberall I, Radova L, Prochazka V, Ehrmann J Jr. Changes of microRNAs-192, 196a and 203 correlate with Bar rett's esophagus diagnosis and its progression compared to normal healthy individuals. Diagn Pathol 2011; 6: 114.
56. Haiart S, Watson DI, Leong MP, Astill D, Bright T, Hussey DJ. MicroRNA-196a & microRNA-101 expression in Barrett's oesophagus in patients with medically and surgically treated gastrooesophageal reflux. BMC Res Notes 2011; 4: 41.
57. Kan T, Sato F, Ito T, 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.
58. Smith CM, Watson DI, Leong MP, et al. miR-200 family expression is downregulated upon neoplastic progression of Barrett's esophagus. World J Gastroenterol 2011; 17: 1036-44.
59. Odze RD, Lauwers GY. Histopathology of Barrett's esophagus after ablation and endoscopic mucosal resection therapy. Endoscopy 2008; 40: 1008-15.
60. Dijckmeester WA, Wijnhoven BP, Watson DI, et al. MicroRNA-143 and-205 expression in neosquamous esophageal epithelium following Argon plasma ablation of Barrett's esophagus. J Gastrointest Surg 2009; 13: 846-53.
61. Akao Y, Nakagawa Y, Naoe T. MicroRNA-143 and-145 in colon cancer. DNA Cell Biol 2007; 26: 311-20.
62. van Baal JW, Verbeek RE, Bus P, et al. microRNA-145 in Barrett's oesophagus: regulating BMP4 signalling via GATA6. Gut 2012; In Press.
63. Hu Y, Correa AM, Hoque A, et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer 2011; 128: 132-43.
64. Ye Y, Wang KK, Gu J, et al. Genetic variations in microRNArelated genes are novel susceptibility loci for esophageal cancer risk. Cancer Prev Res (Phila) 2008; 1: 460-9.
65. Stoner G D, Gupta A. Etiology and chemoprevention of esophageal squamous cell carcinoma. Carcinogenesis 2001; 22: 1737-46.
66. Toh Y, Oki E, Ohgaki K, et al. Alcohol drinking, cigarette smoking, and the development of squamous cell carcinoma of the esophagus: molecular mechanisms of carcinogenesis. Int J Clin Oncol 2010; 15: 135-44.
67. Matsushima K, Isomoto H, Kohno S, Nakao K. MicroRNAs and esophageal squamous cell carcinoma. Digestion 2010; 82: 138-44.
68. Zhang C, Wang C, Chen X, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem 2010; 56: 1871-9.
69. Komatsu S, Ichikawa D, Takeshita H, et al. Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer 2011; 105: 104-11.
70. Guo Y, Chen Z, Zhang L, et al. Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res 2008; 68: 26-33.
71. Ogawa R, Ishiguro H, Kuwabara Y, et al. Expression profiling of micro-RNAs in human esophageal squamous cell carcinoma using RT-PCR. Med Mol Morphol 2009; 42: 102-9.
72. Lin RJ, Xiao DW, Liao LD, et al. MiR-142-3p as a potential prognostic biomarker for esophageal squamous cell carcinoma. J Surg Oncol 2012; 105: 175-82.
73. Chen ZL, Zhao XH, Wang JW, et al. microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin. J Biol Chem 2011; 286: 10725-34.
74. Hiyoshi Y, Kamohara H, Karashima R, et al. MicroRNA-21 regulates the proliferation and invasion in esophageal squamous cell carcinoma. Clin Cancer Res 2009; 15: 1915-22.
75. Fassan M, Realdon S, Pizzi M, et al. Programmed cell death 4 nuclear loss and miR-21 or activated Akt overexpression in esophageal squamous cell carcinogenesis. Dis Esophagus 2012; 25: 263-8.
76. Ma WJ, Lv GD, Tuersun A, et al. Role of microRNA-21 and effect on PTEN in Kazakh's esophageal squamous cell carcinoma. Mol Biol Rep 2011; 38: 3253-60.
77. Kurashige J, Kamohara H, Watanabe M, et al. Serum microRNA-21 is a novel biomarker in patients with esophageal squamous cell carcinoma. J Surg Oncol 2012; In Press
78. Wu BL, Xu LY, Du ZP, et al. MiRNA profile in esophageal squamous cell carcinoma: downregulation of miR-143 and miR-145. World J Gastroenterol 2011; 17: 79-88.
79. Liu R, Liao J, Yang M, et al. The cluster of miR-143 and miR-145 affects the risk for esophageal squamous cell carcinoma through co-regulating fascin homolog 1. PLoS One 2012; 7: e33987.
80. Akagi I, Miyashita M, Ishibashi O, et al. Relationship between altered expression levels of MIR21, MIR143, MIR145, and MIR205 and clinicopathologic features of esophageal squamous cell carcinoma. Dis Esophagus 2011; 24: 523-30.
81. Yuan Y, Zeng ZY, Liu XH, et al. MicroRNA-203 inhibits cell proliferation by repressing _Np63 expression in human esophageal squamous cell carcinoma. BMC Cancer 2011; 11: 57.
82. Li X, Lin R, Li J. Epigenetic silencing of microRNA-375 regulates PDK1 expression in esophageal cancer. Dig Dis Sci 2011; 56: 2849-56.
83. Chen X, Hu H, Guan X, et al. CpG island methylation status of miRNAs in esophageal squamous cell carcinoma. Int J Cancer 2012; 130: 1607-13.
84. Lee KH, Goan YG, Hsiao M, et al. MicroRNA-373 (miR-373) post-transcriptionally regulates large tumor suppressor, homolog 2 (LATS2) and stimulates proliferation in human esophageal cancer. Exp Cell Res 2009; 315: 2529-38.
85. Tian Y, Luo A, Cai Y, et al. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem 2010; 285: 7986-94.
86. Ding DP, Chen ZL, Zhao XH, et al. miR-29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression. Carcinogenesis 2011; 32: 1025-32.
87. Li S, Li Z, Guo F, et al. miR-223 regulates migration and invasion by targeting Artemin in human esophageal carcinoma. J Biomed Sci 2011; 18: 24.
88. Kurashige J, Watanabe M, Iwatsuki M, et al. Overexpression of microRNA-223 regulates the ubiquitin ligase FBXW7 in oesophageal squamous cell carcinoma. Br J Cancer 2012; 106: 182-8.