The Role of MicroRNAs in Molecular Pathology of Esophageal Cancer and Their Potential Usage in Clinical Oncology

Česká verzia

Authors: A. Kovaříková ¹; R. Héžová ^1,2; J. Srovnal ³; M. Rédová‑ lojová ^1,2; O. Slabý ^1,2
Authors place of work: CEITEC – Středoevropský technologický institut, MU, Brno ¹; Klinika komplexní onkologické péče, Masarykův onkologický ústav, Brno ²; Ústav molekulární a translační medicíny, LF UP v Olomouci ³
Published in the journal: Klin Onkol 2014; 27(2): 87-96
Category: Reviews

Summary

MicroRNAs are an abundant class of non‑coding RNAs (approx. 18– 25 nucleotides in length) that suppress translation through binding to their target mRNAs, eventually leading to mRNAs degradation. Sequences of these endogenous RNA molecules are highly conserved, even among unrelated species, indicating their involvement in basic biological processes, such as development, differentiation, proliferation or apoptosis. MiRNAs also participate on regulation of cancer stem cell functioning, immune system and malignant transformation. This review provides a comprehensive overview of miRNAs functions in esophageal cancer, their roles in key pathogenetic pathways and disease development, as well as their potential usage in clinical routine as biomarkers improving diagnosis, prognosis and prediction of therapeutic response. Through regulation of signaling pathways important in malignant transformation, miRNAs present also promising therapeutic targets.

Key words:
microRNAs – esophageal cancer – Barrett‘s esophagus – regulation of gene expression – diagnosis – prognosis

Zdroje

1. Klener P (ed.). Protinádorová chemoterapie. Praha: Galén 1996.

2. Klener P (ed.). Klinická onkologie. Praha: Galén 2002.

3. Kano M, Seki N, Kikkawa N et al. MiR‑ 145, miR‑ 133a and miR‑ 133b: tumor‑ suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer 2010; 127(12): 2804– 2014.

4. Adam Z, Krejčí M, Vorlíček J et al. Speciální onkologie. 3. vyd. Praha: Galén 2010.

5. Zemanova M, Petruzelka L, Pazdro A et al. Prospective non‑randomized study of preoperative concurrent platinum plus 5- fluorouracil‑based chemoradiotherapy with or without paclitaxel in esophageal cancer patients: long‑term follow‑up. Dis Esophagus 2010; 23(2): 160– 167.

6. Jemal A, Siegel R, Ward E et al. Cancer statistics, 2008. CA Cancer J Clin 2008; 58(2): 71– 96.

7. Lopes AB, Fagundes RB. Esophageal squamous cell carcinoma – precursor lesions and early diagnosis. World J Gastrointest Endosc 2012; 4(1): 9– 16.

8. Holmes RS and Vaughan TL. Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol 2007; 17(1): 2– 9.

9. Roth MJ, Liu SF, Dawsey SM et al. Cytologic detection of esophageal squamous cell carcinoma and precursor lesions using balloon and sponge samplers in asymptomatic adults in Linxian, China. Cancer 1997; 80(11): 2047– 2059.

10. Kolář Z (ed.). Molekulární patologie nádorů. Olomouc: Epava 2003.

11. Zhao Y, Srivastava D. A developmental view of microRNA function. Trends Biochem Sci 2007; 32(4): 189– 197.

12. Stark A, Brennecke J, Russell RB et al. Identification of Drosophila MicroRNA targets. PLoS Biol 2003; 1(3): E60.

13. Liu X, Fortin K, Mourelatos Z. MicroRNAs: biogenesis and molecular functions. Brain Pathol 2008; 18(1): 113– 121.

14. 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 2006; 103(7): 2257– 2261.

15. Klener P, Klener P jr (eds). Nová protinádorová léčiva a léčebné strategie v onkologii. Praha: Grada 2010.

16. 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(5): 1689– 1700.

17. Zhu L, Yan W, Rodriguez‑ Canales J et al. MicroRNA analysis of microdissected normal squamous esophageal epithelium and tumor cells. Am J Cancer Res 2011; 1(5): 574– 584.

18. Liu M, Wang Z, Yang S et al. TNF‑alpha is a novel target of miR‑ 19a. Int J Oncol 2011; 38(4): 1013– 1022.

19. 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(15): 2529– 2538.

20. 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(9): 2545– 2551.

21. Li X, Lin R, Li J. Epigenetic silencing of microRNA‑ 375 regulates PDK1 expression in esophageal cancer. Dig Dis Sci 2011; 56(10): 2849– 2856.

22. Kong KL, Kwong DL, Chan TH et al. MicroRNA‑ 375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin‑like growth factor 1 receptor. Gut 2012; 61(1): 33– 42.

23. MacCallum DE, Hupp TR, Midgley CA et al. The p53 response to ionising radiation in adult and developing murine tissues. Oncogene 1996; 13(12): 2575– 2587.

24. Hu Y, Correa AM, Hoque A et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer 2011; 128(1): 132– 143.

25. Yuan Y, Zeng ZY, Liu XH et al. MicroRNA‑ 203 inhibits cell proliferation by repressing DeltaNp63 expression in human esophageal squamous cell carcinoma. BMC Cancer 2011; 11: 57.

26. 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(7): 1025– 1032.

27. Tsuchiya S, Fujiwara T, Sato F et al. MicroRNA‑ 210 regulates cancer cell proliferation through targeting fibroblast growth factor receptor‑like 1 (FGFRL1). J Biol Chem 2011; 286(1): 420– 428.

28. Zhang T, Zhao D, Wang Q et al. MicroRNA‑ 1322 regulates ECRG2 allele specifically and acts as a potential biomarker in patients with esophageal squamous cell carcinoma. Mol Carcinog 2013; 52(8): 581– 590.

29. Liu Q, Lv GD, Qin X et al. Role of microRNA let‑ 7 and effect to HMGA2 in esophageal squamous cell carcinoma. Mol Biol Rep 2012; 39(2): 1239– 1246. doi: 10.1007/ s11033‑011‑0854‑7.

30. 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. doi: 10.1186/ 1423‑0127‑18‑24.

31. 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(1): 182– 188. doi: 10.1038/ bjc.2011.509.

32. van Baal JW, Verbeek RE, Bus P et al. MicroRNA‑ 145 in Barrett‘s oesophagus: regulating BMP4 signalling via GATA6. Gut 2013; 62(5): 664– 675. doi: 10.1136/ gutjnl‑ 2011- 301061.

33. 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(5): 3253– 3260. doi: 10.1007/ s11033- 010- 0480- 9.

34. Ohashi S, Natsuizaka M, Naganuma S et al. A NOTCH3- mediated squamous cell differentiation program limits expansion of EMT‑ competent cells that express the ZEB transcription factors. Cancer Res 2011; 71(21): 6836– 6847. doi: 10.1158/ 0008- 5472.CAN‑ -11- 0846.

35. 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(8): 1036– 1044. doi: 10.3748/ wjg.v17.i8.1036.

36. Matsushima K, Isomoto H, Yamaguchi N et al. MiRNA‑ 205 modulates cellular invasion and migration via regulating zinc finger E‑ box binding homeobox 2 expression in esophageal squamous cell carcinoma cells. J Transl Med 2011; 9: 30. doi: 10.1186/ 1479- 5876- -9-30.

37. Yokobori T, Suzuki S, Tanaka N et al. MiR‑ 150 is associated with poor prognosis in esophageal squamous cell carcinoma via targeting the EMT inducer ZEB1. Cancer Sci 2013; 104(1): 48– 54. doi: 10.1111/ cas.12030.

38. 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(11): 7986– 7994. doi: 10.1074/ jbc.M109.062877.

39. 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(12): 10725– 10734. doi: 10.1074/ jbc.M110.165654.

40. Xu X, Chen Z, Zhao X et al. MicroRNA‑ 25 promotes cell migration and invasion in esophageal squamous cell carcinoma. Biochem Biophys Res Commun 2012; 421(4): 640– 645. doi: 10.1016/ j.bbrc.2012.03.048.

41. Zhang T, Wang Q, Zhao D et al. The oncogenetic role of microRNA‑ 31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond) 2011; 121(10): 437– 447. doi: 10.1042/ CS20110207.

42. Xi Y, Nakajima G, Gavin E et al. Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin‑fixed paraffin‑embedded samples. RNA 2007; 13(10): 1668– 1674.

43. Taylor DD, Gercel‑ Taylor C. MicroRNA signatures of tumor‑ derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110(1): 13– 21. doi: 10.1016/ j.ygyno.2008.04.033.

44. 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. doi: 10.1111/ j.1365- 2141.2008.07077.x.

45. Zen K, Zhang CY. Circulating microRNAs: a novel class of biomarkers to diagnose and monitor human cancers. Med Res Rev 2010; 32(2): 326– 348. doi: 10.1002/ med.20215.

46. Han C, Chen Z, Yang M et al. Human SCAMP5, a novel secretory carrier membrane protein, facilitates calcium‑ triggered cytokine secretion by interaction with SNARE machinery. J Immunol 2009; 182(5): 2986– 2996. doi: 10.4049/ jimmunol.0802002.

47. Lodes MJ, Caraballo M, Suciu D et al. Detection of cancer with serum miRNAs on an oligonucleotide microarray. PloS One 2009; 4(7): e6229. doi: 10.1371/ journal.pone.0006229.

48. Komatsu S, Ichikawa D, Takeshita H et al. Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer 2011; 105(1): 104– 111. doi: 10.1038/ bjc.2011.198.

49. Wu C, Li M, Hu C et al. Clinical significance of serum mir‑ 223, mir‑ 25 and mir‑ 375 in patients with esophageal squamous cell carcinoma. Mol Biol Rep 2014; 41(3): 1257– 1266. doi: 10.1007/ s11033- 013- 2970- z.

50. Liu R, Liao J, Yang M et al. Circulating miR‑ 155 expression in plasma: a potential biomarker for early diagnosis of esophageal cancer in humans. J Toxicol Environ Health A 2012; 75(18): 1154– 1162. doi: 10.1080/ 15287394.2012.699856.

51. 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(12): 1871– 1879. doi: 10.1373/ clinchem.2010.147553.

52. Guo Y, Chen Z, Zhang L et al. Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res 2008; 68(1): 26– 33. doi: 10.1158/ 0008- 5472.CAN‑ 06- 4418.

53. Maru DM, Singh RR, Hannah C et al. MicroRNA‑ 196a is a potential marker of progression during Barrett‘s metaplasia‑ dysplasia‑ invasive adenocarcinoma sequence in esophagus. Am J Pathol 2009; 174(5): 1940– 1948. doi: 10.2353/ ajpath.2009.080718.

54. Drakaki A, Iliopoulos D. MicroRNA gene networks in oncogenesis. Curr Genomics 2009; 10(1): 35– 41. doi: 10.2174/ 138920209787581299.

55. Yang H, Gu J, Wang KK et al. MicroRNA expression signatures in Barrett‘s esophagus and esophageal adenocarcinoma. Clin Cancer Res 2009; 15(18): 5744– 5752. doi: 10.1158/ 1078- 0432.CCR‑ 09- 0385.

56. 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(6): 1056– 1063. doi: 10.1097/ SLA.0b013e3181dd4ea9.

57. 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(2): 102– 109. doi: 10.1007/ s00795- 009- 0443- 1.

58. Feber A, Xi L, Pennathur A et al. MicroRNA prognostic signature for nodal metastases and survival in esophageal adenocarcinoma. Ann Thorac Surg 2011; 91(5): 1523– 1530. doi: 10.1016/ j.athoracsur.2011.01.056.

59. Wang T, Zang WQ, Li M et al. Effect of miR‑ 451 on the biological behavior of the esophageal carcinoma cell line EC9706. Dig Dis Sci 2013; 58(3): 706– 714. doi: 10.1007/ s10620- 012- 2395- x.

60. Ito T, Sato F, Kan T et al. Polo‑like kinase 1 regulates cell proliferation and is targeted by miR‑ 593* in esophageal cancer. Int J Cancer 2011; 129(9): 2134– 2146. doi: 10.1002/ ijc.25874.

61. 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(19): 6192– 6200. doi: 10.1158/ 1078- 0432.CCR‑ 09- 1467.

62. Wijnhoven BP, Hussey DJ, Watson DI et al. MicroRNA profiling of Barrett‘s oesophagus and oesophageal adenocarcinoma. Br J Surg 2010; 97(6): 853– 861. doi: 10.1002/ bjs.7000.

63. Huang SD, Yuan Y, Zhuang CW et al. MicroRNA‑ 98 and microRNA‑ 214 post transcriptionally regulate enhancer of zeste homolog 2 and inhibit migration and invasion in human esophageal squamous cell carcinoma. Mol Cancer 2012; 11: 51. doi: 10.1186/ 1476- 4598- 11- 51.

64. Revilla‑ Nuin B, Parrilla P, Lozano JJ et al. Predictive value of microRNAs in the progression of Barrett esophagus to adenocarcinoma in a long‑term follow‑up study. Ann Surg 2013; 257(5): 886– 893. doi: 10.1097/ SLA.0b013e31826ddba6.

65. Bansal A, Lee IH, Hong X et al. Feasibility of microRNAs as biomarkers for Barrett‘s esophagus progression: a pilot cross‑ sectional, phase 2 biomarker study. Am J Gastroenterol 2011; 106(6): 1055– 1063. doi: 10.1038/ ajg.2011.37.

66. Luthra R, Singh RR, Luthra MG et al. MicroRNA‑ 196a targets annexin A1: a microRNA‑ mediated mechanism of annexin A1 downregulation in cancers. Oncogene 2008; 27(52): 6667– 6678. doi: 10.1038/ onc.2008.256.

67. Hummel R, Hussey DJ, Michael MZ et al. MiRNAs and their association with locoregional staging and survival following surgery for esophageal carcinoma. Ann Surg Oncol 2011; 18(1): 253– 260. doi: 10.1245/ s10434- 010- 1213-y.

68. Fassan M, Volinia S, Palatini J et al. MicroRNA expression profiling in human Barrett‘s carcinogenesis. Int J Cancer 2011; 129(7): 1661– 1670. doi: 10.1002/ ijc.25823.

69. 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(3): e33987. doi: 10.1371/ journal.pone.0033987.

70. 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(7): 523– 530. doi: 10.1111/ j.1442- 2050.2011.01177.x.

71. Mori Y, Ishiguro H, Kuwabara Y et al. MicroRNA‑ 21 induces cell proliferation and invasion in esophageal squamous cell carcinoma. Mol Med Report 2009; 2(2): 235– 239. doi: 10.3892/ mmr_00000089.

72. 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(6): 1915– 1922. doi: 10.1158/ 1078- 0432.CCR‑ 08- 2545.

73. Lin DC, Zhang Y, Pan QJ et al. PLK1 Is transcriptionally activated by NF‑ kappaB during cell detachment and enhances anoikis resistance through inhibiting beta‑catenin degradation in esophageal squamous cell carcinoma. Clin Cancer Res 2011; 17(13): 4285– 4295. doi: 10.1158/ 1078- 0432.CCR‑ 10-3236.

74. 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(9): 3029– 3038. doi: 10.1158/ 1078- 0432.CCR‑ 10- 2532.

75. Sugito N, Ishiguro H, Kuwabara Y et al. RNASEN regulates cell proliferation and affects survival in esophageal cancer patients. Clin Cancer Res 2006; 12(24): 7322– 7328.

76. Slabý O, Svoboda M et al (eds). MikroRNA v onkologii. 1. vyd. Praha: Galén 2012.

77. Zhou Y, Hong L. Prediction value of mir‑ 483 and mir‑ 214 in prognosis and multidrug resistance of esophageal squamous cell carcinoma. Genet Test Mol Biomarkers 2013; 17(6): 470– 474. doi: 10.1089/ gtmb.2012.0518.

78. Odenthal M, Bollschweiler E, Grimminger PP et al. Microrna profiling in locally advanced esophageal cancer indicates a high potential of mir‑ 192 in prediction of multimodality therapy response. Int J Cancer 2013; 133(10): 2454– 2463. doi: 10.1002/ ijc.28253.

79. Krützfeldt J, Rajewsky N, Braich R et al. Silencing of microRNAs in vivo with ‚antagomirs‘. Nature 2005; 438(7068): 685– 689.

80. Imanaka Y, Tsuchiya S, Sato F et al. MicroRNA‑ 141 confers resistance to cisplatin‑induced apoptosis by targeting YAP1 in human esophageal squamous cell carcinoma. J Hum Genet 2011; 56(4): 270– 276. doi: 10.1038/ jhg.2011.1.