Insights into the epigenetic mechanisms controlling pancreatic carcinogenesis

Cancer Letters

Volumn 328, Issue 2, 2013, Pages 212-221

  McCleary Wheeler, Angela L ^a,c   Lomberk, Gwen A ^b,c   Weiss, Frank U ^d   Schneider, Günter ^e   Fabbri, Muller ^f   Poshusta, Tara L ^a   Dusetti, Nelson J ^g   Baumgart, Sandra ^h   Iovanna, Juan L ^g   Ellenrieder, Volker ^h   Urrutia, Raul ^b,c   Fernandez Zapico, Martin E ^a,b,c  

^a Division of Oncology Research   (United States)

^b MAYO CLINIC   (United States)

^c MAYO CLINIC CANCER CENTER   (United States)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f CHILDREN S HOSPITAL LOS ANGELES   (United States)

^g AIX MARSEILLE UNIVERSITY   (France)

^h PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Chromatin; DNA methylation; Epigenetics; MicroRNA; Pancreatic cancer

Indexed keywords

MICRORNA;

CANCER GROWTH; CANCER INVASION; CANCER MODEL; CARCINOGENESIS; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; INHERITANCE; NONHUMAN; ONCOGENE; PANCREAS ADENOCARCINOMA; PANCREAS CARCINOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SHORT SURVEY; SOMATIC MUTATION; UPREGULATION;

EID: 84870342265     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.10.005     Document Type: Review

References (91)

1. Sandoval J., Esteller M. Cancer epigenomics: beyond genomics. Curr. Opin. Genet. Dev. 2012, 22:50-55.
2. Rodriguez-Paredes M., Esteller M. Cancer epigenetics reaches mainstream oncology. Nat. Med. 2011, 17:330-339.
3. Lomberk G., Mathison A.J., Grzenda A., Urrutia R. The sunset of somatic genetics and the dawn of epigenetics: a new frontier in pancreatic cancer research. Curr. Opin. Gastroenterol. 2008, 24:597-602.
4. Esteller M. Epigenetics in cancer. N. Engl. J. Med. 2008, 358:1148-1159.
5. Haig D. The (dual) origin of epigenetics. Cold Spring Harb. Symp. Quant. Biol. 2004, 69:67-70.
6. Gottschling D.E. Summary: epigenetics--from phenomenon to field. Cold Spring Harb. Symp. Quant. Biol. 2004, 69:507-519.
7. Waddington C.H., Pantelouris E.M. Transplantation of nuclei in newt's eggs. Nature 1953, 172:1050-1051.
8. Goldberg A.D., Allis C.D., Bernstein Epigenetics E. A landscape takes shape. Cell 2007, 128:635-638.
9. Avery O.T., MacLeod C.M., McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Inductions of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 1979, 149:297-326.
10. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Can. 2011, 11:726-734.
11. Hruban R.H., Goggins M., Parsons J., Kern S.E. Progression model for pancreatic cancer. Clin. Can. Res. 2000, 6:2969-2972.
12. Schutte M., Hruban R.H., Geradts J., Maynard R., Hilgers W., Rabindran S.K., Moskaluk C.A., Hahn S.A., Schwarte-Waldhoff I., Schmiegel W., Baylin S.B., Kern S.E., Herman J.G. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Can. Res. 1997, 57:3126-3130.
13. 2+/calcineurin signaling pathway. EMBO J. 2006, 25:3714-3724.
14. Koenig A., Linhart T., Schlengemann K., Reutlinger K., Wegele J., Adler G., Singh G., Hofmann L., Kunsch S., Buch T., Schafer E., Gress T.M., Fernandez-Zapico M.E., Ellenrieder V. NFAT-induced histone acetylation relay switch promotes c-Myc-dependent growth in pancreatic cancer cells. Gastroenterology 2010, 138:1189-1199. e1181-1182.
15. Grzenda A., Ordog T., Urrutia R. Polycomb and the emerging epigenetics of pancreatic cancer. J. Gastrointest. Can. 2011, 42:100-111.
16. Bird A. DNA methylation patterns and epigenetic memory. Genes & Dev. 2002, 16:6-21.
17. Bestor T.H. The DNA methyltransferases of mammals. Hum. Mol. Genet. 2000, 9:2395-2402.
18. Pradhan S., Bacolla A., Wells R.D., Roberts R.J. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J. Biol. Chem. 1999, 274:33002-33010.
19. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
20. Hata K., Okano M., Lei H., Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002, 129:1983-1993.
21. Suetake I., Shinozaki F., Miyagawa J., Takeshima H., Tajima S. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J. Biol. Chem. 2004, 279:27816-27823.
22. Wienholz B.L., Kareta M.S., Moarefi A.H., Gordon C.A., Ginno P.A., Chedin F. DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo. PLoS Genet. 2010, 6:e1001106.
23. Vairapandi M., Duker N.J. Enzymic removal of 5-methylcytosine from DNA by a human DNA-glycosylase. Nucl. Acids Res. 1993, 21:5323-5327.
24. Bhattacharya S.K., Ramchandani S., Cervoni N., Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999, 397:579-583.
25. Tahiliani M., Koh K.P., Shen Y.H., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., Rao A. Conversion of 5-Methylcytosine to 5- Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1. Science 2009, 324:930-935.
26. Valinluck V., Sowers L.C. Inflammation-mediated cytosine damage: a mechanistic link between inflammation and the epigenetic alterations in human cancers. Can. Res. 2007, 67:5583-5586.
27. Valinluck V., Sowers L.C. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Can. Res. 2007, 67:946-950.
28. Valinluck V., Tsai H.H., Rogstad D.K., Burdzy A., Bird A., Sowers L.C. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucl. Acids Res. 2004, 32:4100-4108.
29. Sato N., Fukushima N., Maitra A., Matsubayashi H., Yeo C.J., Cameron J.L., Hruban R.H., Goggins M. Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays. Can. Res. 2003, 63:3735-3742.
30. Sato N., Maitra A., Fukushima N., van Heek N.T., Matsubayashi H., Iacobuzio- Donahue C.A., Rosty C., Goggins M. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Can. Res. 2003, 63:4158-4166.
31. Sato N., Fukushima N., Hruban R.H., Goggins M. CpG island methylation profile of pancreatic intraepithelial neoplasia. Mod. Pathol. 2008, 21:238-244.
32. Vincent A., Omura N., Hong S.M., Jaffe A., Eshleman J., Goggins M. Genome-wide analysis of promoter methylation associated with gene expression profile in pancreatic adenocarcinoma. Clin. Can. Res. 2011, 17:4341-4354.
33. Wang X., Feng Y., Pan L., Wang Y., Xu X., Lu J., Huang B. The proximal GC-rich region of p16(INK4a) gene promoter plays a role in its transcriptional regulation. Mol. Cell Biochem. 2007, 301:259-266.
34. Navarro A., Yin P., Monsivais D., Lin S.M., Du P., Wei J.J., Bulun S.E. Genome-wide DNA methylation indicates silencing of tumor suppressor genes in uterine leiomyoma. PLoS One 2012, 7:e33284.
35. Potapova A., Hasemeier B., Romermann D., Metzig K., Gohring G., Schlegelberger B., Langer F., Kreipe H., Lehmann U. Epigenetic inactivation of tumour suppressor gene KLF11 in myelodysplastic syndromes. Eur. J. Haematol. 2010, 84:298-303.
36. Fernandez-Zapico M.E., Gonzalez-Paz N.C., Weiss E., Savoy D.N., Molina J.R., Fonseca R., Smyrk T.C., Chari S.T., Urrutia R., Billadeau D.D. Ectopic expression of VAV1 reveals an unexpected role in pancreatic cancer tumorigenesis. Can. Cell 2005, 7:39-49.
37. Rosty C., Geradts J., Sato N., Wilentz R.E., Roberts H., Sohn T., Cameron J.L., Yeo C.J., Hruban R.H., Goggins M. p16 Inactivation in pancreatic intraepithelial neoplasias (PanINs) arising in patients with chronic pancreatitis. Am. J. Surg. Pathol. 2003, 27:1495-1501.
38. Luger K., Richmond T.J. The histone tails of the nucleosome. Curr. Opin. Genet. Dev. 1998, 8:140-146.
39. Kornberg R.D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 1999, 98:285-294.
40. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
41. Mersfelder E.L., Parthun M.R. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucl. Acids Res. 2006, 34:2653-2662.
42. Cosgrove M.S., Boeke J.D., Wolberger C. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 2004, 11:1037-1043.
43. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
44. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Ann. Rev. Biochem. 2005, 74:481-514.
45. Lehmann A., Denkert C., Budczies J., Buckendahl A.C., Darb-Esfahani S., Noske A., Muller B.M., Bahra M., Neuhaus P., Dietel M., Kristiansen G., Weichert W. High class I HDAC activity and expression are associated with RelA/p65 activation in pancreatic cancer in vitro and in vivo. BMC Can. 2009, 9:395.
46. Dal Molin M., Hong S.M., Hebbar S., Sharma R., Scrimieri F., de Wilde R.F., Mayo S.C., Goggins M., Wolfgang C.L., Schulick R.D., Lin M.T., Eshleman J.R., Hruban R.H., Maitra A., Matthaei H. Loss of expression of the SWI/SNF chromatin remodeling subunit BRG1/SMARCA4 is frequently observed in intraductal papillary mucinous neoplasms of the pancreas. Hum. Pathol. 2012, 43:585-591.
47. Gayther S.A., Batley S.J., Linger L., Bannister A, Thorpe K., Chin S.F., Daigo Y., Russell P., Wilson A., Sowter H.M., Delhanty J.D., Ponder B.A., Kouzarides T., Caldas C. Mutations truncating the EP300 acetylase in human cancers. Nat. Genet. 2000, 24:300-303.
48. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., Davies H., Jones D., Lin M.L., Teague J., Bignell G., Butler A., Cho J., Dalgliesh G.L., Galappaththige D., Greenman C., Hardy C., Jia M., Latimer C., Lau K.W., Marshall J., McLaren S., Menzies A., Mudie L., Stebbings L., Largaespada D.A., Wessels L.F., Richard S., Kahnoski R.J., Anema J., Tuveson D.A., Perez-Mancera P.A., Mustonen V., Fischer A., Adams D.J., Rust A., Chan-on W., Subimerb C., Dykema K., Furge K., Campbell P.J., Teh B.T., Stratton M.R., Futreal P.A. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469:539-542.
49. Shain A.H., Giacomini C.P., Matsukuma K., Karikari C.A., Bashyam M.D., Hidalgo M., Maitra A., Pollack J.R. Convergent structural alterations define SWItch/Sucrose NonFermentable (SWI/SNF) chromatin remodeler as a central tumor suppressive complex in pancreatic cancer. Proc. Natl. Acad. Sci. USA 2012, 109:E252-9.
50. Rosson G.B., Bartlett C., Reed W., Weissman B.E. BRG1 loss in MiaPaCa2 cells induces an altered cellular morphology and disruption in the organization of the actin cytoskeleton. J. Cell. Physiol. 2005, 205:286-294.
51. Yang X.J., Seto E., HATs, structure HDACs: from function and regulation to novel strategies for therapy and prevention. Oncogene 2007, 26:5310-5318.
52. Vo N., Goodman R.H. CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 2001, 276:13505-13508.
53. Lomberk G., Wallrath L., Urrutia R. The heterochromatin protein 1 family. Genome. Biol. 2006, 7:228.
54. Schneider G., Kramer O.H., Schmid R.M., Saur D. Acetylation as a transcriptional control mechanism-HDACs and HATs in pancreatic ductal adenocarcinoma. J. Gastrointest. Can. 2011, 42:85-92.
55. Baumgart S., Glesel E., Singh G., Chen N.M., Reutlinger K., Zhang J., Billadeau D.D., Fernandez-Zapico M.E., Gress T.M., Singh S.K., Ellenrieder V. Restricted heterochromatin formation links NFATc2 repressor activity with growth promotion in pancreatic cancer. Gastroenterology 2012, 142:388-398.
56. Lo Re A.E., Fernandez-Barrena M.G., Almada L.L., Mills L., Elsawa S.F., Lund G., Ropolo A., Molejon M.I., Vaccaro M.I., Fernandez-Zapico M.E. A Novel AKT1-GLI3-VMP1 pathway mediates KRAS-induced autophagy in cancer cells. J. Biol. Chem. 2012, 287:25325-25334.
57. Mathison A., Liebl A., Bharucha J., Mukhopadhyay D., Lomberk G., Shah V., Urrutia R. Pancreatic stellate cell models for transcriptional studies of desmoplasia-associated genes. Pancreatology 2010, 10:505-516.
58. Fernandez-Zapico M.E., Mladek A., Ellenrieder V., Folch-Puy E., Miller L., Urrutia R. An mSin3A interaction domain links the transcriptional activity of KLF11 with its role in growth regulation. EMBO J. 2003, 22:4748-4758.
59. Ouaissi M., Sielezneff I., Silvestre R., Sastre B., Bernard J.P., Lafontaine J.S., Payan M.J., Dahan L., Pirro N., Seitz J.F., Mas E., Lombardo D., Ouaissi A. High histone deacetylase 7 (HDAC7) expression is significantly associated with adenocarcinomas of the pancreas. Ann. Surg. Oncol. 2008, 15:2318-2328.
60. Fritsche P., Seidler B., Schuler S., Schnieke A., Gottlicher M., Schmid R.M., Saur D., Schneider G. HDAC2 mediates therapeutic resistance of pancreatic cancer cells via the BH3- only protein NOXA. Gut 2009, 58:1399-1409.
61. Ouaissi M., Cabral S., Tavares J., da Silva A.C., Mathieu Daude F., Mas E., Bernard J., Sastre B., Lombardo D., Ouaissi A. Histone deacetylase (HDAC) encoding gene expression in pancreatic cancer cell lines and cell sensitivity to HDAC inhibitors. Can. Biol. Ther. 2008, 7:523-531.
62. Schneider G., Kramer O.H., Fritsche P., Schuler S., Schmid R.M., Saur D. Targeting histone deacetylases in pancreatic ductal adenocarcinoma. J. Cell. Mol. Med. 2010, 14:1255-1263.
63. Marshall G.M., Gherardi S., Xu N., Neiron Z., Trahair T., Scarlett C.J., Chang D.K., Liu P.Y., Jankowski K., Iraci N., Haber M., Norris M.D., Keating J., Sekyere E., Jonquieres G., Stossi F., Katzenellenbogen B.S., Biankin A.V., Perini G., Liu T. Transcriptional upregulation of histone deacetylase 2 promotes Myc-induced oncogenic effects. Oncogene 2010, 29:5957-5968.
64. Aghdassi A., Sendler M., Guenther A., Mayerle J., Behn C.O., Heidecke C.D., Friess H., Buchler M., Evert M., Lerch M.M., Weiss F.U. Recruitment of histone deacetylases HDAC1 and HDAC2 by the transcriptional repressor ZEB1 downregulates E-cadherin expression in pancreatic cancer. Gut 2012, 61:439-448.
65. von Burstin J., Eser S., Paul M.C., Seidler B., Brandl M., Messer M., von Werder A., Schmidt A., Mages J., Pagel P., Schnieke A., Schmid R.M., Schneider G., Saur D. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology 2009, 137:361-371. e361-365.
66. Grzenda A.L., Lomberk G., Urrutia R. Different EZH2 isoforms are expressed in pancreatic cells: Evidence for a polycomb-mediated subcode within the context of the histone code. Pancreas 2007, 35:404.
67. Cao R., Wang L.J., Wang H.B., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 2002, 298:1039-1043.
68. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., Morey L., Van Eynde A., Bernard D., Vanderwinden J.M., Bollen M., Esteller M., Di Croce L., de Launoit Y., Fuks F. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006, 439:871-874.
69. Kotake Y., Cao R., Viatour P., Sage J., Zhang Y., Xiong Y. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007, 21:49-54.
70. Wei Y., Xia W., Zhang Z., Liu J., Wang H., Adsay N.V., Albarracin C., Yu D., Abbruzzese J.L., Mills G.B., Bast R.C., Hortobagyi G.N., Hung M.C. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol. Carcinog. 2008, 47:701-706.
71. Ougolkov A.V., Bilim V.N., Billadeau D.D. Regulation of pancreatic tumor cell proliferation and chemoresistance by the histone methyltransferase enhancer of zeste homologue 2. Clin. Can. Res. 2008, 14:6790-6796.
72. Lomberk G., Mathison A.J., Grzenda A., Seo S., DeMars C.J., Rizvi S., Bonilla-Velez J., Calvo E., Fernandez-Zapico M.E., Iovanna J., Buttar N.S., Urrutia R. Sequence-specific recruitment of heterochromatin protein 1 via interaction with Kruppel-like factor 11, a human transcription factor involved in tumor suppression and metabolic diseases. J. Biol. Chem. 2012, 287:13026-13039.
73. Yamada N., Nishida Y., Tsutsumida H., Hamada T., Goto M., Higashi M., Nomoto M., Yonezawa S. MUC1 expression is regulated by DNA methylation and histone H3 lysine 9 modification in cancer cells. Can. Res. 2008, 68:2708-2716.
74. Hollingsworth M.A., Strawhecker J.M., Caffrey T.C., Mack D.R. Expression of Muc1, Muc2, Muc3 and Muc4 Mucin Messenger-Rnas in human pancreatic and intestinal tumor-cell lines. Int. J. Can. 1994, 57:198-203.
75. Masaki Y., Oka M., Ogura Y., Ueno T., Nishihara K., Tangoku A., Takahashi M., Yamamoto M., Irimura T. Sialylated MUC1 mucin expression in normal pancreas, benign pancreatic lesions, and pancreatic ductal adenocarcinoma. Hepatogastroenterology 1999, 46:2240-2245.
76. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
77. Schier A.F., Giraldez A.J. MicroRNA function and mechanism: insights from zebra fish. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:195-203.
78. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van Dongen S., Inoue K., Enright A.J., Schier A.F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79.
79. Vasuden Switching from repression to activation: microRNAs can up-regulate translation. Science 2007, 318:1931-1934.
80. Bloomston M., Frankel W.L., Petrocca F., Volinia S., Alder H., Hagan J.P., Liu C.G., Bhatt D., Taccioli C., Croce C.M. MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 2007, 297:1901-1908.
81. Szafranska A.E., Davison T.S., John J., Cannon T., Sipos B., Maghnouj A., Labourier E., Hahn S.A. MicroRNA expression alterations are linked to tumorigenesis and non-neoplastic processes in pancreatic ductal adenocarcinoma. Oncogene 2007, 26:4442-4452.
82. Lee E.J., Gusev Y., Jiang J., Nuovo G.J., Lerner M.R., Frankel W.L., Morgan D.L., Postier R.G., Brackett D.J., Schmittgen T.D. Expression profiling identifies microRNA signature in pancreatic cancer. Int. J. Can. 2007, 120:1046-1054.
83. Habbe N., Koorstra J.B., Mendell J.T., Offerhaus G.J., Ryu J.K., Feldmann G., Mullendore M.E., Goggins M.G., Hong S.M., Maitra A. MicroRNA miR-155 is a biomarker of early pancreatic neoplasia. Can. Biol. Ther. 2009, 8:340-346.
84. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., zur Hausen A., Brunton V.G., Morton J., Sansom O., Schuler J., Stemmler M.P., Herzberger C., Hopt U., Keck T., Brabletz S., Brabletz T. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell. Biol. 2009, 11:1487-1495.
85. Brabletz S., Bajdak K., Meidhof S., Burk U., Niedermann G., Firat E., Wellner U., Dimmler A., Faller G., Schubert J., Brabletz T. The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J. 2011, 30:770-782.
86. Burk U., Schubert J., Wellner U., Schmalhofer O., Vincan E., Spaderna S., Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008, 9:582-589.
87. Nalls D., Tang S.N., Rodova M., Srivastava R.K., Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One 2011, 6:e24099.
88. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., Ferlito M., Lowenstein C.J., Arking D.E., Beer M.A., Maitra A., Mendell J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26:745-752.
89. Gironella M., Seux M., Xie M.J., Cano C., Tomasini R., Gommeaux J., Garcia S., Nowak J., Yeung M.L., Jeang K.T., Chaix A., Fazli L., Motoo Y., Wang Q., Rocchi P., Russo A., Gleave M., Dagorn J.C., Iovanna J.L., Carrier A., Pebusque M.J., Dusetti N.J. 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.
90. Weiss F.U., Marques I.J., Woltering J.M., Vlecken D.H., Aghdassi A., Partecke L.I., Heidecke C.D., Lerch M.M., Bagowski C.P. Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology 2009, 137:2136-2145.
91. Yu J., Li A., Hong S.M., Hruban R.H., Goggins M. MicroRNA alterations of pancreatic intraepithelial neoplasias. Clin. Can. Res. 2012, 18:981-992.