The Id3/E47 axis mediates cell-cycle control in human pancreatic ducts and adenocarcinoma

Molecular Cancer Research

Volumn 9, Issue 6, 2011, Pages 782-790

  Lee, Seung Hee ^a,e   Hao, Ergeng ^a,e   Kiselyuk, Alice ^b,c   Shapiro, James ^g   Shields, David J ^d,f   Lowy, Andrew ^d   Levine, Fred ^e   Itkin Ansari, Pamela ^a,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e BURNHAM INSTITUTE   (United States)

^f PFIZER INC   (United States)

^g UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GROWTH FACTOR; HEXACYCLINE; HEXACYCLINE E; HISTONE H3; INHIBITOR OF DIFFERENTIATION 3; KI 67 ANTIGEN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E47; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREATITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL CYCLE; GENE EXPRESSION REGULATION; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; MALE; MICE; MICE, INBRED C57BL; NEOPLASM PROTEINS; PANCREATIC DUCTS; PANCREATIC NEOPLASMS; PANCREATITIS; TRANSCRIPTION FACTOR 3;

ADENOVIRIDAE; MURINAE;

EID: 79959207440     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0535     Document Type: Article

References (48)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Li J, Wientjes MG, Au JL. Pancreatic cancer: pathobiology, treatment options, and drug delivery. AAPS J 2010;12:223-32.
3. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
4. Strosberg J, Gardner N, Kvols L. Survival and prognostic factor analysis in patients with metastatic pancreatic endocrine carcinomas. Pancreas 2009;38:255-8.
5. Stathis A, Moore MJ. Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 2010;7:163-72.
6. Koliopanos A, Avgerinos C, Paraskeva C, Touloumis Z, Kelgiorgi D, Dervenis C. Molecular aspects of carcinogenesis in pancreatic cancer. Hepatobiliary Pancreat Dis Int 2008;7:345-56.
7. Strimpakos A, Saif MW, Syrigos KN. Pancreatic cancer: from molecular pathogenesis to targeted therapy. Cancer Metastasis Rev 2008;27:495-522.
8. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 2000;113:3897-905.
9. Zebedee Z, Hara E. Id proteins in cell cycle control and cellular senescence. Oncogene 2001;20:8317-25. (Pubitemid 34121902)
10. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990;61:49-59.
11. Norton JD, Atherton GT. Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol 1998;18:2371-81.
12. Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM. Id proteins in cell growth and tumorigenesis. Cancer Cell 2003;3:525-30. (Pubitemid 36808647)
13. Perk J, Iavarone A, Benezra R. Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005;5:603-14. (Pubitemid 41081386)
14. Wilson JW, Deed RW, Inoue T, Balzi M, Becciolini A, Faraoni P, et al. Expression of Id helix-loop-helix proteins in colorectal adenocarcinoma correlates with p53 expression and mitotic index. Cancer Res 2001;61:8803-10. (Pubitemid 34013894)
15. Damdinsuren B, Nagano H, Kondo M, Yamamoto H, Hiraoka N, Yamamoto T, et al. Expression of Id proteins in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Int J Oncol 2005;26:319-27.
16. Kim D, Peng XC, Sun XH. Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Mol Cell Biol 1999;19:8240-53. (Pubitemid 30414018)
17. Morrow MA, Mayer EW, Perez CA, Adlam M, Siu G. Overexpression of the Helix-Loop-Helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 1999;36:491-503.
18. Wice BM, Gordon JI. Forced expression of Id-1 in the adult mouse small intestinal epithelium is associated with development of adenomas. J Biol Chem 1998;273:25310-9. (Pubitemid 28443297)
19. Lasorella A, Boldrini R, Dominici C, Donfrancesco A, Yokota Y, Inserra A, et al. Id2 is critical for cellular proliferation and is the oncogenic effector of N-myc in human neuroblastoma. Cancer Res 2002;62:301-6. (Pubitemid 34074019)
20. Sakaguchi Y, Inaba M, Kusafuka K, Okazaki K, Ikehara S. Establishment of animal models for three types of pancreatitis and analyses of regeneration mechanisms. Pancreas 2006;33:371-81. (Pubitemid 44690727)
21. Demeterco C, Hao E, Lee SH, Itkin-Ansari P, Levine F. Adult human beta-cell neogenesis? Diabetes Obes Metab 2009;11 Suppl 4:46-53.
22. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50. (Pubitemid 38050041)
23. Schwartz R, Engel I, Fallahi-Sichani M, Petrie HT, Murre C. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc Natl Acad Sci U S A 2006;103:9976-81. (Pubitemid 43993608)
24. Kiselyuk A, Farber-Katz S, Cohen T, Lee SH, Geron I, Azimi B, et al. Phenothiazine neuroleptics signal to the human insulin promoter as revealed by a novel high-throughput screen. J Biomol Screen 2010;15:663-70.
25. Matsumura ME, Li F, Berthoux L, Wei B, Lobe DR, Jeon C, et al. Vascular injury induces posttranscriptional regulation of the Id3 gene: cloning of a novel Id3 isoform expressed during vascular lesion formation in rat and human atherosclerosis. Arterioscler Thromb Vasc Biol 2001;21:752-8. (Pubitemid 32448764)
26. Lowenfels AB, Maisonneuve P. Epidemiology and risk factors for pancreatic cancer. Best Pract Res Clin Gastroenterol 2006;20:197-209.
27. Lemoine NR. Molecular advances in pancreatic cancer. Digestion 1997;58:550-6. (Pubitemid 27515719)
28. Fong S, Debs RJ, Desprez PY. Id genes and proteins as promising targets in cancer therapy. Trends Mol Med 2004;10:387-92. (Pubitemid 39061140)
29. Tsuchiya T, Okaji Y, Tsuno NH, Sakurai D, Tsuchiya N, Kawai K, et al. Targeting Id1 and Id3 inhibits peritoneal metastasis of gastric cancer. Cancer Sci 2005;96:784-90. (Pubitemid 43019829)
30. Lee KT, Lee YW, Lee JK, Choi SH, Rhee JC, Paik SS, et al. Over-expression of Id-1 is significantly associated with tumour angiogenesis in human pancreas cancers. Br J Cancer 2004;90:1198-203. (Pubitemid 38496813)
31. Iacobuzio-Donahue CA, Ashfaq R, Maitra A, Adsay NV, Shen-Ong GL, Berg K, et al. Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res 2003;63:8614-22. (Pubitemid 38064035)
32. Kleeff J, Ishiwata T, Friess H, Buchler MW, Israel MA, Korc M. The helix-loop-helix protein Id2 is overexpressed in human pancreatic cancer. Cancer Res 1998;58:3769-72. (Pubitemid 28405627)
33. Grutzmann R, Boriss H, Ammerpohl O, Luttges J, Kalthoff H, Schackert HK, et al. Meta-analysis of microarray data on pancreatic cancer defines a set of commonly dysregulated genes. Oncogene 2005;24:5079-88. (Pubitemid 41129085)
34. Gradwohl G, Dierich A, LeMeur M, Guillemot F. neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 2000;97:1607-11. (Pubitemid 30118489)
35. Itkin-Ansari P, Marcora E, Geron I, Tyrberg B, Demeterco C, Hao E, et al. NeuroD1 in the endocrine pancreas: localization and dual function as an activator and repressor. Dev Dyn 2005;233:946-53. (Pubitemid 40853470)
36. Hao E, Tyrberg B, Itkin-Ansari P, Lakey JR, Geron I, Monosov EZ, et al. Beta-cell differentiation from nonendocrine epithelial cells of the adult human pancreas. Nat Med 2006;12:310-6. (Pubitemid 43355079)
37. Maruyama H, Kleeff J, Wildi S, Friess H, Buchler MW, Israel MA, et al. Id-1 and Id-2 are overexpressed in pancreatic cancer and in dysplastic lesions in chronic pancreatitis. Am J Pathol 1999;155:815-22. (Pubitemid 29426827)
38. Aguirre AJ, Bardeesy N, Sinha M, Lopez L, Tuveson DA, Horner J, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003;17:3112-26. (Pubitemid 38040774)
39. Schutte M, Hruban RH, Geradts J, Maynard R, HilgersW, Rabindran SK, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res 1997;57:3126-30. (Pubitemid 27351723)
40. Hustinx SR, Cao D, Maitra A, Sato N, Martin ST, Sudhir D, et al. Differentially expressed genes in pancreatic ductal adenocarcinomas identified through serial analysis of gene expression. Cancer Biol Ther 2004;3:1254-61. (Pubitemid 41350962)
41. Bain G, Cravatt CB, Loomans C, Alberola-Ila J, Hedrick SM, Murre C. Regulation of the helix-loop- helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat Immunol 2001;2:165-71. (Pubitemid 33707937)
42. Cao D, Ashfaq R, Goggins MG, Hruban RH, Kern SE, Iacobuzio-Donahue CA. Differential expression of multiple genes in association with MADH4/DPC4/SMAD4 inactivation in pancreatic cancer. Int J Clin Exp Pathol 2008;1:510-7.
43. Dufresne M, Clerc P, Dieng M, Edir A, Couvelard A, Delisle MB, et al. Id3 modulates cellular localization of bHLH Ptf1-p48 protein. Int J Cancer 2010 Sep 9. [Epub ahead of print].
44. Lim RW, Wu JM. Molecular mechanisms regulating expression and function of transcription regulator inhibitor of differentiation 3. Acta Pharmacol Sin 2005;26:1409-20. (Pubitemid 41789528)
45. Shuno Y, Tsuno NH, Okaji Y, Tsuchiya T, Sakurai D, Nishikawa T, et al. Id1/Id3 knockdown inhibits metastatic potential of pancreatic cancer. J Surg Res 2010;161:76-82.
46. Kamalian L, Forootan SS, Bao ZZ, Zhang Y, Gosney JR, Foster CS, et al. Inhibition of tumourigenicity of small cell lung cancer cells by suppressing Id3 expression. Int J Oncol 2010;37:595-603.
47. Arnold JM, Mok SC, Purdie D, Chenevix-Trench G. Decreased expression of the Id3 gene at 1p36.1 in ovarian adenocarcinomas. Br J Cancer 2001;84:352-9. (Pubitemid 32154428)
48. Higashikawa K, Yoneda S, Tobiume K, Saitoh M, Taki M, Mitani Y, et al. DeltaNp63alpha-dependent expression of Id-3 distinctively suppresses the invasiveness of human squamous cell carcinoma. Int J Cancer 2009;124:2837-44.