GLI1 interferes with the DNA mismatch repair system in pancreatic cancer through bhlhe41-mediated suppression of MLH1

Cancer Research

Volumn 73, Issue 24, 2013, Pages 7313-7323

  Inaguma, Shingo ^a   Riku, Miho ^a   Hashimoto, Mitsuyoshi ^a   Murakami, Hideki ^a   Saga, Shinsuke ^a   Ikeda, Hiroshi ^a   Kasai, Kenji ^a  

^a AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLNITROSOUREA; PROTEIN MLH1; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2;

ARTICLE; BHLHE41 GENE; BINDING SITE; CANCER CELL CULTURE; CONTROLLED STUDY; DEC2 GENE; GENE ACTIVATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC SCREENING; GLI1 GENE; GLI2 GENE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MISMATCH REPAIR; MLH1 GENE; NUCLEOTIDE SEQUENCE; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; SHARP1 GENE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DNA MISMATCH REPAIR; HUMANS; NUCLEAR PROTEINS; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84891276250     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2008     Document Type: Article

References (44)

1. Hile SE, Shabashev S, Eckert KA. Tumor-specific microsatellite instability: Do distinct mechanisms underlie the MSI-L and EMAST phenotypes Mutat Res 2013;743-4:67-77.
2. Shah SN, Hile SE, Eckert KA. Defective mismatch repair, microsatellite mutation bias, and variability in clinical cancer phenotypes. Cancer Res 2010;70:431-5.
3. Kastrinos F, Mukherjee B, Tayob N, Wang F, Sparr J, Raymond VM, et al. Risk of pancreatic cancer in families with Lynch syndrome. JAMA 2009;302:1790-5.
4. Win AK, Young JP, Lindor NM, Tucker KM, Ahnen DJ, Young GP, et al. Colorectal and other cancer risks for carriers and noncarriers from families with a DNA mismatch repair gene mutation: A prospective cohort study. J Clin Oncol 2012;30:958-64.
5. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010;11:220-8.
6. Wang L, Tsutsumi S, Kawaguchi T, Nagasaki K, Tatsuno K, Yamamoto S, et al. Whole-exome sequencing of human pancreatic cancers and characterization of genomic instability caused by MLH1 haploinsufficiency and complete deficiency. Genome Res 2012;22:208-19.
7. Barakat MT, Humke EW, Scott MP. Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. Trends Mol Med 2010;16:337-48.
8. Karamboulas C, Ailles L. Developmental signaling pathways in cancer stem cells of solid tumors. Biochim Biophys Acta 2013;1830:2481-95.
9. Harris LG, Pannell LK, Singh S, Samant RS, Shevde LA. Increased vascularity and spontaneous metastasis of breast cancer by hedgehog signaling mediated upregulation of cyr61. Oncogene 2012;31: 3370-80.
10. Inaguma S, Kasai K, Ikeda H. GLI1 facilitates the migration and invasion of pancreatic cancer cells through MUC5AC-mediated attenuation of E-cadherin. Oncogene 2011;30:714-23.
11. Nagai S, Nakamura M, Yanai K, Wada J, Akiyoshi T, Nakashima H, et al. Gli1 contributes to the invasiveness of pancreatic cancer through matrix metalloproteinase-9 activation. Cancer Sci 2008;99:1377-84.
12. Singh RR, Kunkalla K, Qu C, Schlette E, Neelapu SS, Samaniego F, et al. ABCG2 is a direct transcriptional target of hedgehog signaling and involved in stroma-induced drug tolerance in diffuse large B-cell lymphoma. Oncogene 2011;30:4874-86.
13. Li X, Deng W, Nail CD, Bailey SK, Kraus MH, Ruppert JM, et al. Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation. Oncogene 2006;25:609-21.
14. Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Po A, Sico MA, et al. Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itchdependent ubiquitination. Nat Cell Biol 2006;8:1415-23.
15. Leung C, Lingbeek M, Shakhova O, Liu J, Tanger E, Saremaslani P, et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004;428:337-41.
16. Po A, Ferretti E, Miele E, De Smaele E, Paganelli A, Canettieri G, et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J 2010;29:2646-58.
17. Stecca B, Ruiz i Altaba A. A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers. EMBO J 2009;28:663-76.
18. Wang X, Venugopal C, Manoranjan B, McFarlane N, O'Farrell E, Nolte S, et al. Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells. Oncogene 2012;31:187-99.
19. Zbinden M, Duquet A, Lorente-Trigos A, Ngwabyt SN, Borges I, Ruiz i Altaba A. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J 2010; 29:2659-74.
20. Eichberger T, Sander V, Schnidar H, Regl G, Kasper M, Schmid C, et al. Overlapping and distinct transcriptional regulator properties of the GLI1 and GLI2 oncogenes. Genomics 2006;87:616-32.
21. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S, Blaas L, et al. Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol Cell Biol 2006;26:6283-98.
22. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, et al. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 2002;277: 5548-55.
23. Fujimoto K, Shen M, Noshiro M, Matsubara K, Shingu S,Honda K, et al. Molecular cloning and characterization of DEC2, a new member of basic helix-loop-helix proteins. Biochem Biophys Res Commun 2001; 280:164-71.
24. Azmi S, Ozog A, Taneja R. Sharp-1/DEC2 inhibits skeletal muscle differentiation through repression of myogenic transcription factors. J Biol Chem 2004;279:52643-52.
25. Honma S, Kawamoto T, Takagi Y, Fujimoto K, Sato F, Noshiro M, et al. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 2002;419:841-4.
26. Noshiro M, Kawamoto T, Furukawa M, Fujimoto K, Yoshida Y, Sasabe E, et al. Rhythmic expression of DEC1 and DEC2 in peripheral tissues: DEC2 is a potent suppressor for hepatic cytochrome P450s opposing DBP. Genes Cells 2004;9:317-29.
27. Nakamura H, Tanimoto K, Hiyama K, Yunokawa M, Kawamoto T, Kato Y, et al. Human mismatch repair gene, MLH1, is transcriptionally repressed by the hypoxia-inducible transcription factors, DEC1 and DEC2. Oncogene 2008;27:4200-9.
28. Blasi MF, Ventura I, Aquilina G, Degan P, Bertario L, Bassi C, et al. A human cell-based assay to evaluate the effects of alterations in the MLH1 mismatch repair gene. Cancer Res 2006;66:9036-44.
29. Xie J, Guillemette S, Peng M, Gilbert C, Buermeyer A, Cantor SB. An MLH1 mutation links BACH1/FANCJ to colon cancer, signaling, and insight toward directed therapy. Cancer Prev Res 2010;3: 1409-16.
30. Kasai K, Inaguma S, Yoneyama A, Yoshikawa K, Ikeda H. SCL/TAL1 interrupting locus derepresses GLI1 from the negative control of suppressor-of-fused in pancreatic cancer cell. Cancer Res 2008;68: 7723-9.
31. Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 2012;30:460-5.
32. Rajurkar M, De Jesus-Monge WE, Driscoll DR, Appleman VA, Huang H, Cotton JL, et al. The activity of Gli transcription factors is essential for Kras-induced pancreatic tumorigenesis. Proc Natl Acad Sci U S A 2012;109:E1038-47.
33. Nolan-Stevaux O, Lau J, Truitt ML, Chu GC, Hebrok M, Fernandez- Zapico ME, et al. GLI1 is regulated through Smoothened-independent mechanisms in neoplastic pancreatic ducts and mediates PDAC cell survival and transformation. Genes Dev 2009;23: 24-36.
34. Mazumdar T, DeVecchio J, Shi T, Jones J, Agyeman A, Houghton JA. Hedgehog signaling drives cellular survival in human colon carcinoma cells. Cancer Res 2011;71:1092-102.
35. Gore SM, Kasper M, Williams T, Regl G, Aberger F, Cerio R, et al. Neuronal differentiation in basal cell carcinoma: Possible relationship to Hedgehog pathway activation J Pathol 2009;219:61-8.
36. Shi I, Hashemi Sadraei N, Duan ZH, Shi T. Aberrant signaling pathways in squamous cell lung carcinoma. Cancer Informat 2011;10:273-85.
37. Koyabu Y, Nakata K, Mizugishi K, Aruga J, Mikoshiba K. Physical and functional interactions between Zic and Gli proteins. J Biol Chem 2001;276:6889-92.
38. Laner-Plamberger S, Kaser A, Paulischta M, Hauser-Kronberger C, Eichberger T, Frischauf AM. Cooperation between GLI and JUN enhances transcription of JUN and selected GLI target genes. Oncogene 2009;28:1639-51.
39. Mizugishi K, Aruga J, Nakata K, Mikoshiba K. Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J Biol Chem 2001;276:2180-8.
40. Gerber AN, Wilson CW, Li YJ, Chuang PT. The hedgehog regulated oncogenes Gli1 and Gli2 block myoblast differentiation by inhibiting MyoD-mediated transcriptional activation. Oncogene 2007;26: 1122-36.
41. Li Y, Xie M, Song X, Gragen S, Sachdeva K, Wan Y, et al. DEC1 negatively regulates the expression of DEC2 through binding to the E-box in the proximal promoter. J Biol Chem 2003;278: 16899-907.
42. Dekker M, de Vries S, Aarts M, Dekker R, Brouwers C, Wiebenga O, et al. Transient suppression ofMLH1allows effective single-nucleotide substitution by single-stranded DNA oligonucleotides. Mutat Res 2011;715:52-60.
43. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 1991;51:3075-9.
44. Hong SM, Park JY, Hruban RH, Goggins M. Molecular signatures of pancreatic cancer. Arch Pathol Lab Med 2011;135:716-27.