Aberrant microRNA-155 expression is an early event in the multistep progression of pancreatic adenocarcinoma

Pancreatology

Volumn 10, Issue 1, 2010, Pages 66-73

  Ryu, Ji Kon ^a,c   Hong, Seung Mo ^a   Karikari, Collins A ^a   Hruban, Ralph H ^a   Goggins, Michael G ^a   Maitra, Anirban ^a,b  

^a Sol Goldman Pancreatic Cancer Research Center   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Seoul National University College of Medicine   (South Korea)

Author keywords

MicroRNA; MiR 155; MiR 21; Pancreatic intraepithelial neoplasia; PanIN

Indexed keywords

LOCKED NUCLEIC ACID; MICRORNA;

ARTICLE; CONTROLLED STUDY; GENE; GENE OVEREXPRESSION; GENETIC REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; MIR 155 GENE; MIR 21 GENE; MIR 221 GENE; PANCREAS ADENOCARCINOMA; PANCREAS TUMOR; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE MICROARRAY;

EID: 77949564293     PISSN: 14243903     EISSN: 14243911     Source Type: Journal    
DOI: 10.1159/000231984     Document Type: Article

References (55)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al: Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96.
2. Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, et al: Resected adenocarcinoma of the pancreas - 616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000; 4: 567-579.
3. Pisters PW, Wolff RA, Crane CH, Evans DB: Combined-modality treatment for operable pancreatic adenocarcinoma. Oncology (Williston Park) 2005; 19: 393-404, 409-410, 412-416.
4. Goggins M: Identifying molecular markers for the early detection of pancreatic neoplasia. Semin Oncol 2007; 34: 303-310.
5. Hruban RH, Maitra A, Kern SE, Goggins M: Precursors to pancreatic cancer. Gastroenterol Clin North Am 2007; 36: 831-849, vi.
6. Hruban RH, Takaori K, Klimstra DS, Adsay NV, Albores-Saavedra J, Biankin AV, et al: An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol 2004; 28: 977-987.
7. Hruban RH, Adsay NV, Albores-Saavedra J, Compton C, Garrett ES, Goodman SN, et al: Pancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol 2001; 25: 579-586.
8. Feldmann G, Beaty R, Hruban RH, Maitra A: Molecular genetics of pancreatic intraepithelial neoplasia. J Hepatobiliary Pancreat Surg 2007; 14: 224-232.
9. Van Heek NT, Meeker AK, Kern SE, Yeo CJ, Lillemoe KD, Cameron JL, et al: Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am J Pathol 2002; 161: 1541-1547.
10. Moskaluk CA, Hruban RH, Kern SE: p16 and K-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Res 1997; 57: 2140-2143.
11. Goggins M, Hruban RH, Kern SE: BRCA2 is inactivated late in the development of pancreatic intraepithelial neoplasia: evidence and implications. Am J Pathol 2000; 156: 1767-1771.
12. Maitra A, Adsay NV, Argani P, Iacobuzio- Donahue C, De Marzo A, Cameron JL, et al: Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol 2003; 16: 902-912.
13. Feldmann G, Maitra A: Molecular genetics of pancreatic ductal adenocarcinomas and recent implications for translational efforts. J Mol Diagn 2008; 10: 111-122.
14. Chang TC, Mendell JT: The Roles of micro- RNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet 2007; 8: 215-239.
15. He L, Hannon GJ: MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5: 522-531.
16. Zhang B, Pan X, Cobb GP, Anderson TA: microRNAs as oncogenes and tumor suppressors. Dev Biol 2007; 302: 1-12.
17. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, 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: 15524-15529.
18. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, et al: A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628-9632.
19. Rinaldi A, Poretti G, Kwee I, Zucca E, Catapano CV, Tibiletti MG, et al: Concomitant MYC and microRNA cluster miR-17-92 (C13orf25) amplification in human mantle cell lymphoma. Leuk Lymphoma 2007; 48: 410-412.
20. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, 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: 435-443.
21. Brueckner B, Stresemann C, Kuner R, Mund C, Musch T, Meister M, et al: The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res 2007; 67: 1419-1423.
22. Han L, Witmer PD, Casey E, Valle D, Sukumar S: DNA methylation regulates Micro- RNA expression. Cancer Biol Ther 2007; 6: 1284-1288.
23. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT: c-Myc-regulated micro- RNAs modulate E2F1 expression. Nature 2005; 435: 839-843.
24. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, et al: Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008; 40: 43-50.
25. Lu Z, Liu M, Stribinskis V, Klinge CM, Ramos KS, Colburn NH, et al: MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 2008; 27: 4373-4379.
26. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH: Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 2008; 283: 1026-1033.
27. Ma L, Teruya-Feldstein J, Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449: 682-688.
28. Korpal M, Lee ES, Hu G, Kang Y: The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283: 14910-14914.
29. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al: The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
30. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-2261.
31. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, Hagan JP, et al: MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 2007; 297: 1901-1908.
32. Szafranska AE, Davison TS, John J, Cannon T, Sipos B, Maghnouj A, et al: MicroRNA expression alterations are linked to tumorigenesis and non-neoplastic processes in pancreatic ductal adenocarcinoma. Oncogene 2007; 26: 4442-4452.
33. Lee EJ, Gusev Y, Jiang J, Nuovo GJ, Lerner MR, Frankel WL, et al: Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 2007; 120: 1046-1054. (Pubitemid 46214304)
34. Zhang Y, Li M, Wang H, Fisher WE, Lin PH, Yao Q, et al: Profiling of 95 microRNAs in pancreatic cancer cell lines and surgical specimens by real-time PCR analysis. World J Surg 2009; 33: 698-709.
35. 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: 2171-2176.
36. Habbe N, Koorstra JB, Mendell JT, Offerhaus GJ, Ryu JK, Feldmann G, et al: MicroRNA miR-155 is a biomarker of early pancreatic neoplasia. Cancer Biol Ther 2009; 8: 1-7.
37. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, et al: Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 40: 43-50.
38. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
39. Hustinx SR, Leoni LM, Yeo CJ, Brown PN, Goggins M, Kern SE, et al: Concordant loss of MTAP and p16/CDKN2A expression in pancreatic intraepithelial neoplasia: evidence of homozygous deletion in a noninvasive precursor lesion. Mod Pathol 2005; 18: 959-963. (Pubitemid 41059957)
40. Lee KM, Cao D, Itami A, Pour PM, Hruban RH, Maitra A, et al: Class III beta-tubulin, a marker of resistance to paclitaxel, is overexpressed in pancreatic ductal adenocarcinoma and intraepithelial neoplasia. Histopathology 2007; 51: 539-546. (Pubitemid 47437824)
41. Cao D, Zhang Q, Wu LS, Salaria SN, Winter JW, Hruban RH, et al: Prognostic significance of maspin in pancreatic ductal adenocarcinoma: tissue microarray analysis of 223 surgically resected cases. Mod Pathol 2007; 20: 570-578. (Pubitemid 46631999)
42. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, al: MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008; 299: 425-436. (Pubitemid 351185951)
43. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, et al: Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA 2005; 102: 3627-3632. (Pubitemid 40354662)
44. Kluiver J, Poppema S, De Jong D, Blokzijl T, Harms G, Jacobs S, et al: BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol 2005; 207: 243-249. (Pubitemid 41404155)
45. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005; 65: 7065-7070. (Pubitemid 41161233)
46. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, et al: Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189-198. (Pubitemid 43357945)
47. Wang X, Tang S, Le SY, Lu R, Rader JS, Meyers C, et al: Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS ONE 2008; 3:e2557.
48. Chen HC, Chen GH, Chen YH, Liao WL, Liu CY, Chang KP, et al: MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. Br J Cancer Mar 24 2009; 100(6):1002-1011.
49. Jung M, Mollenkopf HJ, Grimm C, Wagner I, Albrecht M, Waller T, et al: MicroRNA profiling of clear cell renal cell cancer identifies a robust signature to define renal malignancy. J Cell Mol Med 2009, in press.
50. Gironella M, Seux M, Xie MJ, Cano C, Tomasini R, Gommeaux J, et al: Tumor protein 53- induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development. Proc Natl Acad Sci USA 2007; 104: 16170-16175.
51. Kong W, Yang H, He L, Zhao JJ, Coppola D, Dalton WS, et al: MicroRNA-155 is regulated by the transforming growth factor beta/ Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 2008; 28: 6773-6784.
52. Seux M, Iovanna J, Dagorn JC, Dusetti NJ: MicroRNAs in pancreatic ductal adenocarcinoma: new diagnostic and therapeutic clues. Pancreatology 2009; 9: 66-72.
53. Canto MI, Goggins M, Yeo CJ, Griffin C, Axilbund JE, Brune K, et al: Screening for pancreatic neoplasia in high-risk individuals: an EUS-based approach. Clin Gastroenterol Hepatol 2004; 2: 606-621.
54. Canto MI, Goggins M, Hruban RH, Petersen GM, Giardiello FM, Yeo C, et al: Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study. Clin Gastroenterol Hepatol 2006; 4: 766-781.
55. Brune K, Abe T, Canto M, O'Malley L, Klein AP, Maitra A, et al: Multifocal neoplastic precursor lesions associated with lobular atrophy of the pancreas in patients having a strong family history of pancreatic cancer. Am J Surg Pathol 2006; 30: 1067-1076.