Inactivation of promoter 1B of APC causes partial gene silencing: Evidence for a significant role of the promoter in regulation and causative of familial adenomatous polyposis

Oncogene

Volumn 30, Issue 50, 2011, Pages 4977-4989

  Rohlin, A ^a   Engwall, Y ^a   Fritzell, K ^b   Goransson K ^b   Bergsten, A ^a   Einbeigi, Z ^a   Nilbert, M ^c,d   Karlsson, P ^a   Bjork J ^b   Nordling, M ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

APC; familial adenomatous ployposis; mutation; promoter; Q PCR

Indexed keywords

ADENOMATOUS POLYP; ADENOMATOUS POLYPOSIS GENE; ADULT; AGED; ALLELE; ARTICLE; CARCINOGENESIS; COLON MUCOSA; COLON POLYPOSIS; CONTROLLED STUDY; DISEASE REGISTRY; EXAMINATION; FAMILIAL ADENOMATOUS POLYPOSIS; FAMILIAL DISEASE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROMOTER REGION; RECTUM ADENOMA; RECTUM MUCOSA; SWEDEN;

ADENOMA; ADENOMATOUS POLYPOSIS COLI; ADENOMATOUS POLYPOSIS COLI PROTEIN; ADULT; AGED; ALLELES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GERM-LINE MUTATION; HUMANS; INTESTINAL MUCOSA; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; REGISTRIES; SWEDEN;

EID: 83555174494     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.201     Document Type: Article

References (46)

1. Amos-Landgraf JM, Kwong LN, Kendziorski CM, Reichelderfer M, Torrealba J, Weichert J et al. (2007). A target-selected Apc-mutant rat kindred enhances the modeling of familial human colon cancer. Proc Natl Acad Sci USA 104: 4036-4041. (Pubitemid 47181574)
2. Andreutti-Zaugg C, Couturier A, Chappuis P, Hutter P. (1999). Detection of protein truncating mutations in exons 1-14 of the APC gene using an in vivo fusion protein assay. Mutations in brief no. 214. Online. Hum Mutat 13: 170-171.
3. Bisgaard ML, Fenger K, Bulow S, Niebuhr E, Mohr J. (1994). Familial adenomatous polyposis (FAP): frequency, penetrance, and mutation rate. Hum Mutat 3: 121-125. (Pubitemid 24077228)
4. Blaker H, Scholten M, Sutter C, Otto HF, Penzel R. (2003). Somatic mutations in familial adenomatous polyps. Nuclear translocation of beta-catenin requires more than biallelic APC inactivation. Am J Clin Pathol 120: 418-423. (Pubitemid 37295114)
5. Castellsague E, Gonzalez S, Guino E, Stevens KN, Borras E, Raymond VM et al. (2010a). Allele-specific expression of APC in adenomatous polyposis families. Gastroenterology 139: 439-447, 447 e431.
6. Castellsague E, Gonzalez S, Guino E, Stevens KN, Borras E, Raymond VM et al. (2010b). Allele-specific expression of APC in adenomatous polyposis families. Gastroenterology 139: 439-447, 447.e1.
7. Charames GS, Ramyar L, Mitri A, Berk T, Cheng H, Jung J et al. (2008). A large novel deletion in the APC promoter region causes gene silencing and leads to classical familial adenomatous polyposis in a Manitoba Mennonite kindred. Hum Genet 124: 535-541.
8. Cowie S, Drmanac S, Swanson D, Delgrosso K, Huang S, du Sart D et al. (2004). Identification of APC gene mutations in colorectal cancer using universal microarray-based combinatorial sequencing-by-hybridization. Hum Mutat 24: 261-271. (Pubitemid 39095602)
9. De Rosa M, Morelli G, Cesaro E, Duraturo F, Turano M, Rossi GB et al. (2007). Alternative splicing and nonsense-mediated mRNA decay in the regulation of a new adenomatous polyposis coli transcript. Gene 395: 8-14. (Pubitemid 46670630)
10. Dobbie Z, Spycher M, Mary JL, Haner M, Guldenschuh I, Hurliman R et al. (1996). Correlation between the development of extracolonic manifestations in FAP patients and mutations beyond codon 1403 in the APC gene. J Med Genet 33: 274-280. (Pubitemid 26102452)
11. Esteller M, Sparks A, Toyota M, Sanchez-Cespedes M, Capella G, Peinado MA et al. (2000). Analysis of adenomatous polyposis coli promoter hypermethylation in human cancer. Cancer Res 60: 4366-4371. (Pubitemid 32103613)
12. Fiering S, Bender MA, Groudine M. (1999). Analysis of mammalian cis-regulatory DNA elements by homologous recombination. Methods Enzymol 306: 42-66. (Pubitemid 29356824)
13. Fodde R, van der Luijt R, Wijnen J, Tops C, van der Klift H, van Leeuwen-Cornelisse I et al. (1992). Eight novel inactivating germ line mutations at the APC gene identified by denaturing gradient gel electrophoresis. Genomics 13: 1162-1168.
14. Gayther SA, Wells D, SenGupta SB, Chapman P, Neale K, Tsioupra K et al. (1994). Regionally clustered APC mutations are associated with a severe phenotype and occur at a high frequency in new mutation cases of adenomatous polyposis coli. Hum Mol Genet 3: 53-56. (Pubitemid 24038142)
15. Gismondi V, Bafico A, Biticchi R, Pedemonte S, Molina F, Heouaine A et al. (1997). Characterization of 19 novel and six recurring APC mutations in Italian adenomatous polyposis patients, using two different mutation detection techniques. Hum Mutat 9: 370-373. (Pubitemid 27157660)
16. Hamada F, Bienz M. (2004). The APC tumor suppressor binds to C-terminal binding protein to divert nuclear beta-catenin from TCF. Dev Cell 7: 677-685. (Pubitemid 39462688)
17. Hiltunen MO, Alhonen L, Koistinaho J, Myohanen S, Paakkonen M, Marin S et al. (1997). Hypermethylation of the APC (adenomatous polyposis coli) gene promoter region in human colorectal carcinoma. Int J Cancer 70: 644-648. (Pubitemid 27158441)
18. Horii A, Nakatsuru S, Ichii S, Nagase H, Nakamura Y. (1993). Multiple forms of the APC gene transcripts and their tissue-specific expression. Hum Mol Genet 2: 283-287. (Pubitemid 23129089)
19. Hosoya K, Yamashita S, Ando T, Nakajima T, Itoh F, Ushijima T. (2009). Adenomatous polyposis coli 1A is likely to be methylated as a passenger in human gastric carcinogenesis. Cancer Lett 285: 182-189.
20. Joensuu EI, Abdel-Rahman WM, Ollikainen M, Ruosaari S, Knuutila S, Peltomaki P. (2008). Epigenetic signatures of familial cancer are characteristic of tumor type and family category. Cancer Res 68: 4597-4605.
21. Johannesson T, Holmqvist D, Martinsson T, Wahlstrom J. (1991). An improved technique for chromosome preparations from human lymphocytes. Hereditas 115: 295-297.
22. Judson H, Stewart A, Leslie A, Pratt NR, Baty DU, Steele RJ et al. (2006). Relationship between point gene mutation, chromosomal abnormality, and tumour suppressor gene methylation status in colorectal adenomas. J Pathol 210: 344-350. (Pubitemid 44660513)
23. Kanter-Smoler G, Fritzell K, Rohlin A, Engwall Y, Hallberg B, Bergman A et al. (2008). Clinical characterization and the mutation spectrum in Swedish adenomatous polyposis families. BMC Med 6: 10.
24. Kaufmann A, Vogt S, Uhlhaas S, Stienen D, Kurth I, Hameister H et al. (2009). Analysis of rare APC variants at the mRNA level: six pathogenic mutations and literature review. J Mol Diagn 11: 131-139.
25. Kawaji H, Severin J, Lizio M, Waterhouse A, Katayama S, Irvine KM et al. (2009). The FANTOM web resource: from mammalian transcriptional landscape to its dynamic regulation. Genome Biol 10: R40.
26. Kohoutova M, Stekrova J, Jirasek V, Kapras J. (2002). APC germline mutations identified in Czech patients with familial adenomatous polyposis. Hum Mutat 19: 460-461.
27. Lambertz S, Ballhausen WG. (1993). Identification of an alternative 50 untranslated region of the adenomatous polyposis coli gene. Hum Genet 90: 650-652. (Pubitemid 23088076)
28. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A et al. (2006). TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-D110.
29. Miyoshi Y, Ando H, Nagase H, Nishisho I, Horii A, Miki Y et al. (1992). Germ-line mutations of the APC gene in 53 familial adenomatous polyposis patients. Proc Natl Acad Sci USA 89: 4452-4456.
30. Moisio AL, Jarvinen H, Peltomaki P. (2002). Genetic and clinical characterisation of familial adenomatous polyposis: a population based study. Gut 50: 845-850. (Pubitemid 34539048)
31. Mutoh M, Akasu T, Takahashi M, Niho N, Yoshida T, Sugimura T et al. (2006). Possible involvement of hyperlipidemia in increasing risk of colorectal tumor development in human familial adenoma-tous polyposis. Jpn J Clin Oncol 36: 166-171.
32. Nilbert M, Fernebro J, Kristoffersson U. (2000). Novel germline APC mutations in Swedish patients with familial adenomatous polyposis and Gardner syndrome. Scand J Gastroenterol 35: 1200-1203.
33. Palin K, Taipale J, Ukkonen E. (2006). Locating potential enhancer elements by comparative genomics using the EEL software. Nat Protoc 1: 368-374.
34. Phelps RA, Broadbent TJ, Stafforini DM, Jones DA. (2009a). New perspectives on APC control of cell fate and proliferation in colorectal cancer. Cell Cycle 8: 2549-2556.
35. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K et al. (2009b). A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137: 623-634.
36. Renkonen ET, Nieminen P, Abdel-Rahman WM, Moisio AL, Jarvela I, Arte S et al. (2005). Adenomatous polyposis families that screen APC mutation-negative by conventional methods are genetically heterogeneous. J Clin Oncol 23: 5651-5659.
37. Ripa R, Bisgaard ML, Bulow S, Nielsen FC. (2002). De novo mutations in familial adenomatous polyposis (FAP). Eur J Hum Genet 10: 631-637. (Pubitemid 35282413)
38. Romero-Gimenez J, Dopeso H, Blanco I, Guerra-Moreno A, Gonzalez S, Vogt S et al. (2008). Germline hypermethylation of the APC promoter is not a frequent cause of familial adenomatous polyposis in APC/MUTYH mutation negative families. Int J Cancer 122: 1422-1425. (Pubitemid 351287245)
39. Schouten JP, McElgunn CJ, Waaijer R, Zwijnenburg D, Diepvens F, Pals G. (2002). Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res 30: e57.
40. Segditsas S, Sieber OM, Rowan A, Setien F, Neale K, Phillips RK et al. (2008). Promoter hypermethylation leads to decreased APC mRNA expression in familial polyposis and sporadic colorectal tumours, but does not substitute for truncating mutations. Exp Mol Pathol 85: 201-206.
41. Sierra J, Yoshida T, Joazeiro CA, Jones KA. (2006). The APC tumor suppressor counteracts beta-catenin activation and H3K4 methyla-tion at Wnt target genes. Genes Dev 20: 586-600. (Pubitemid 43345324)
42. Solomon E, Voss R, Hall V, Bodmer WF, Jass JR, Jeffreys AJ et al. (1987). Chromosome 5 allele loss in human colorectal carcinomas. Nature 328: 616-619. (Pubitemid 17103961)
43. Stenson PD, Mort M, Ball EV, Howells K, Phillips AD, Thomas NS et al. (2009). The Human Gene Mutation Database: 2008 update. Genome Med 1: 13.
44. Tsuchiya T, Tamura G, Sato K, Endoh Y, Sakata K, Jin Z et al. (2000). Distinct methylation patterns of two APC gene promoters in normal and cancerous gastric epithelia. Oncogene 19: 3642-3646. (Pubitemid 30608485)
45. Venesio T, Balsamo A, Rondo-Spaudo M, Varesco L, Risio M, Ranzani GN. (2003). APC haploinsufficiency, but not CTNNB1 or CDH1 gene mutations, accounts for a fraction of familial adenomatous polyposis patients without APC truncating mutations. Lab Invest 83: 1859-1866. (Pubitemid 38018549)
46. Yan H, Dobbie Z, Gruber SB, Markowitz S, Romans K, Giardiello FM et al. (2002). Small changes in expression affect predisposition to tumorigenesis. Nat Genet 30: 25-26.