The pleiotropic phenotype of Apc mutations in the mouse: Allele specificity and effects of the genetic background

Genetics

Volumn 180, Issue 1, 2008, Pages 601-609

  Halberg, Richard B ^a   Chen, Xiaodi ^a   Amos Landgraf, James M ^a   White, Alanna ^a   Rasmussen, Kristin ^a   Clipson, Linda ^a   Pasch, Cheri ^a   Sullivan, Ruth ^b   Pitot, Henry C ^a   Dove, William F ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; PROTEIN P21; PROTEIN P53;

ADENOMATOUS POLYP; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FAMILIAL POLYPOSIS; FEMALE; GENE FREQUENCY; GENE FUNCTION; GENE MUTATION; GENETIC VARIABILITY; HEREDITY; HISTOPATHOLOGY; INTESTINE TUMOR; MALE; MOUSE; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; ANIMAL; COLON POLYPOSIS; CROSS BREEDING; GENE EXPRESSION REGULATION; GENETICS; HOMOZYGOTE; HUMAN; MOUSE MUTANT; MUTATION; PANCREAS TUMOR; TUMOR SUPPRESSOR GENE;

MUS;

ADENOMATOUS POLYPOSIS COLI; ADENOMATOUS POLYPOSIS COLI PROTEIN; ALLELES; ANIMALS; CROSSES, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, APC; HOMOZYGOTE; HUMANS; INTESTINAL NEOPLASMS; MICE; MICE, KNOCKOUT; MUTATION; PANCREATIC NEOPLASMS; PHENOTYPE;

EID: 56049110529     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.091967     Document Type: Article

References (64)

1. ABRAHAM, S. C., T. T. WU, D. S. KLIMSTRA, L. S. FINN, J. H. LEE et al., 2001 Distinctive molecular genetic alterations in sporadic and familial adenomatous polyposis-associated pancreatoblastomas: frequent alterations in the APC/beta-catenin pathway and chromosome 11p. Am. J. Pathol. 159: 1619-1627.
2. ABRAHAM, S. C., T. T. WU, R. H. HRUBAN, J. H. LEE, C. J. YEO et al., 2002 Genetic and immunohistochemical analysis of pancreatic acinar cell carcinoma: frequent allelic loss on chromosome 11p and alterations in the APC/beta-catenin pathway. Am. J. Pathol. 160: 953-962.
3. ALBUQUERQUE, C., C. BREUKEL, L. R. VAN DER LUIJT, P. FIDALGO, P. LAGE et al., 2002 The 'just-right' signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Hum. Mol. Genet. 11: 1549-1560.
4. BARAN, A. A., K. A. SILVERMAN, J. ZESKAND, R. KORATKAR, A. PALMER et al., 2007 The modifier of Min 2 (Mom2) locus: embryonic lethality of a mutation in the Atp5a1 gene suggests a novel mechanism of polyp suppression. Genome Res. 17: 566-576.
5. BERTARIO, L., A. RUSSO, P. SALA, M. EBOLI, M. GIAROLA et al., 2001 Genotype and phenotype factors as determinants of desmoid tumors in patients with familial adenomatous polyposis. Int. J. Cancer 95: 102-107.
6. BERTARIO, L., A. RUSSO, P. SALA, L. VARESCO, M. GIAROLA et al., 2003 Multiple approach to the exploration of genotype-phenotype correlations in familial adenomatous polyposis. J. Clin. Oncol. 21: 1698-1707.
7. CHEN, T., J. TURNER, S. MCCARTHY, M. SCALTRITI, S. BETTUZZI et al., 2004 Clusterin-mediated apoptosis is regulated by adenomatous polyposis coli and is p21 dependent but p53 independent. Cancer Res. 64: 7412-7419.
8. CLARKE, A. R., M. C. CUMMINGS and D. J. HARRISON, 1995 Interaction between murine germline mutations in p53 and APC predisposes to pancreatic neoplasia but not to increased intestinal malignancy. Oncogene 11: 1913-1920.
9. CORMIER, R. T., and W. F. DOVE, 2000 Dnmt1N/+ reduces the net growth rate and multiplicity of intestinal adenomas in C57BL/ 6-multiple intestinal neoplasia (Min)/+ mice independently of p53 but demonstrates strong synergy with the modifier of Min 1(AKR) resistance allele. Cancer Res. 60: 3965-3970.
10. CRONER, R. S., W. M. BRUECKL, B. REINGRUBER, W. HOHENBERGER and K. GUENTHER, 2005 Age and manifestation related symptoms in familial adenomatous polyposis. BMC Cancer 5: 24.
11. DE VRIES, A., E. R. FLORES, B. MIRANDA, H. M. HSIEH, C. T. VANOOSTROM et al., 2002 Targeted point mutations of p53 lead to dominant-negative inhibition of wild-type p53 function. Proc. Natl. Acad. Sci. USA 99: 2948-2953.
12. DONEHOWER, L. A., M. HARVEY, B. L. SLAGLE, M. J. MCARTHUR, C. A. MONTGOMERY, JR. et al., 1992 Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
13. DONG, M., G. MA, W. TU, K. J. GUO, Y. L. TIAN et al., 2005 Clinicopathological significance of p53 and mdm2 protein expression in human pancreatic cancer. World J. Gastroenterol. 11: 2162-2165.
14. ENOMOTO, M., M. KONISHI, T. IWAMA, J. UTSUNOMIYA, K. I. SUGIHARA et al., 2000 The relationship between frequencies of extracolonic manifestations and the position of APC germline mutation in patients with familial adenomatous polyposis. Jpn. J. Clin. Oncol. 30: 82-88.
15. ERDMAN, S. H., N. A. IGNATENKO, M. B. POWELL, K. A. BLOHM-MANGONE, H. HOLUBEC et al., 1999 APC-dependent changes in expression of genes influencing polyamine metabolism, and consequences for gastrointestinal carcinogenesis, in the Min mouse. Carcinogenesis 20: 1709-1713.
16. FEARON, E. R., 1997 Human cancer syndromes: clues to the origin and nature of cancer. Science 278: 1043-1050.
17. GARBER, J. E., and K. OFFIT, 2005 Hereditary cancer predisposition syndromes. J. Clin. Oncol. 23: 276-292.
18. GIARDIELLO, F. M., G. J. OFFERHAUS, D. H. LEE, A. J. KRUSH, A. C. TERSMETTE et al., 1993 Increased risk of thyroid and pancreatic carcinoma in familial adenomatous polyposis. Gut 34: 1394-1396.
19. GOULD, K. A., W. F. DIETRICH, N. BORENSTEIN, E. S. LANDER and W. F. DOVE, 1996 Mom1 is a semi-dominant modifier of intestinal adenoma size and multiplicity in Min/+ mice. Genetics 144: 1769-1776.
20. GRODEN, J., A. THLIVERIS, W. SAMOWITZ, M. CARLSON, L. GELBERT et al., 1991 Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66: 589-600.
21. GURBUZ, A. K., F. M. GIARDIELLO, G. M. PETERSEN, A. J. KRUSH, G. J. OFFERHAUS et al., 1994 Desmoid tumours in familial adenomatous polyposis. Gut 35: 377-381.
22. HAIGIS, K. M., and W. F. DOVE, 2003 A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat. Genet. 33: 33-39.
23. HAIGIS, K. M., J. G. CAYA, M. REICHELDERFER and W. F. DOVE, 2002 Intestinal adenomas can develop with a stable karyotype and stablemicrosatellites. Proc. Natl. Acad. Sci. USA 99: 8927-8931.
24. HAIGIS, K. M., P. D. HOFF, A. WHITE, A. R. SHOEMAKER, R. B. HALBERG et al., 2004 Tumor regionality in the mouse intestine reflects the mechanism of loss of Apc function. Proc. Natl. Acad. Sci. USA 101: 9769-9773.
25. HALBERG, R. B., D. S. KATZUNG, P. D. HOFF, A. R. MOSER, C. E. COLE et al., 2000 Tumorigenesis in the multiple intestinal neoplasia mouse: redundancy of negative regulators and specificity of modifiers. Proc. Natl. Acad. Sci. USA 97: 3461-3466.
26. HARRIS, S. L., and A. J. LEVINE, 2005 The p53 pathway: positive and negative feedback loops. Oncogene 24: 2899-2908.
27. HARTWELL, L., 2004 Genetics. Robust interactions. Science 303: 774-775.
28. HIRATA, A., T. TSUKAMOTO, M. YAMAMOTO, H. SAKAI, T. YANAI et al., 2005 Organ-specific susceptibility of p53 knockout mice to N-bis(2-hydroxypropyl)nitrosamine carcinogenesis. Cancer Lett. 238: 271-283.
29. JACKS, T., L. REMINGTON, B. O. WILLIAMS, E. M. SCHMITT, S. HALACHMI et al., 1994 Tumor spectrum analysis in p53-mutant mice. Curr. Biol. 4: 1-7.
30. KEMP, C. J., L. A. DONEHOWER, A. BRADLEY and A. BALMAIN, 1993 Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74: 813-822.
31. KINZLER, K. W., M. C. NILBERT, L.-K. SU, B. VOGELSTEIN, T. M. BRYAN et al., 1991 Identification of FAP locus genes from chromosome 5q21. Science 253: 661-665.
32. KUCHERLAPATI, M., A. NGUYEN, M. KURAGUCHI, K. YANG, K. FAN et al., 2007 Tumor progression in Apc(1638N) mice with Exo1 and Fen1 deficiencies. Oncogene 26: 6297-6306.
33. KURAGUCHI, M., X. P. WANG, R. T. BRONSON, R. ROTHENBERG, N. Y. OHENE-BAAH et al., 2006 Adenomatous polyposis coli (APC) is required for normal development of skin and thymus. PLoS Genet. 2: 1362-1374.
34. LI, F. P., and J. F. FRAUMENI, JR., 1969 Soft-tissue sarcomas, breast cancer, and other neoplasms. A familial syndrome? Ann. Intern. Med. 71: 747-752.
35. + in intestinal adenomas from Min mice. Cancer Res. 54: 5947-5952.
36. MALKIN, D., F. P. LI, L. C. STRONG, J. F. FRAUMENI, JR., C. E. NELSON et al., 1990 Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 250: 1233-1238.
37. MARTINEZ, M. E., T. G. O'BRIEN, K. E. FULTZ, N. BABBAR, H. YERUSHALMI et al., 2003 Pronounced reduction in adenoma recurrence associated with aspirin use and a polymorphism in the ornithine decarboxylase gene. Proc. Natl. Acad. Sci. USA 100: 7859-7864.
38. MATUSHANSKY, I., R. G. MAKI and C. C. CARDO, 2008 A context dependent role for Wnt signaling in tumorigenesis and stem cells. Cell Cycle 7: 720-724.
39. MOSER, A. R., H. C. PITOT and W. F. DOVE, 1990 A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247: 322-324.
40. MOSER, A. R., A. R. SHOEMAKER, C. S. CONNELLY, L. CLIPSON, K. A. GOULD et al., 1995 Homozygosity for the Min allele of Apc results in disruption of mouse development prior to gastrulation. Dev. Dyn. 203: 422-433.
41. NACHT, M., A. STRASSER, Y. R. CHAN, A. W. HARRIS, M. SCHLISSEL et al., 1996 Mutations in the p53 and SCID genes cooperate in tumorigenesis. Genes Dev. 10: 2055-2066.
42. NAGY, R., K. SWEET and C. ENG, 2004 Highly penetrant hereditary cancer syndromes. Oncogene 23: 6445-6470.
43. NIGRO, J. M., S. J. BAKER, A. C. PREISINGER, J. M. JESSUP, R. HOSTETTER et al., 1989 Mutations in the p53 gene occur in diverse human tumour types. Nature 342: 705-708.
44. NISHISHO, I., Y. NAKAMURA, Y. MIYOSHI, Y. MIKI, H. ANDO et al., 1991 Mutation of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 253: 665-668.
45. OGINO, S., M. BRAHMANDAM, T. KAWASAKI, G. J. KIRKNER, M. LODA et al., 2006 Epigenetic profiling of synchronous colorectal neoplasias by quantitative DNA methylation analysis. Mod. Pathol. 19: 1083-1090.
46. Δ716 knockout mice. Cancer Res. 57: 1644-1649.
47. REILLY, K. M., D. A. LOISEL, R. T. BRONSON, M. E. MCLAUGHLIN and T. JACKS, 2000 Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat. Genet. 26: 109-113.
48. ROWAN, A. J., H. LAMLUM, M. ILYAS, J. WHEELER, J. STRAUB et al., 2000 APC mutations in sporadic colorectal tumors: a mutational "hotspot" and interdependence of the "two hits." Proc. Natl. Acad. Sci. USA 97: 3352-3357.
49. SAKAI, H., T. TSUKAMOTO, M. YAMAMOTO, N. SHIRAI, T. IIDAKA et al., 2003 High susceptibility of nullizygous p53 knockout mice to colorectal tumor induction by 1,2-dimethylhydrazine. J. Cancer Res. Clin. Oncol. 129: 335-340.
50. SAMOWITZ, W. S., A. THLIVERIS, L. N. SPIRIO and R. WHITE, 1995 Alternatively spliced adenomatous polyposis coli (APC) gene transcripts that delete exons mutated in attenuated APC. Cancer Res. 55: 3732-3734.
51. SHIBATA, H., K. TOYAMA, H. SHIOYA, M. ITO, M. HIROTA et al., 1997 Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278: 120-123.
52. SHIRAI, N., T. TSUKAMOTO, M. YAMAMOTO, T. IIDAKA, H. SAKAI et al., 2002 Elevated susceptibility of the p53 knockout mouse esophagus to methyl-N-amylnitrosamine carcinogenesis. Carcinogenesis 23: 1541-1547.
53. Min/+ mice. Proc. Natl. Acad. Sci. USA 95: 10826-10831.
54. SIEBER, O. M., H. LAMLUM, M. D. CRABTREE, A. J. ROWAN, E. BARCLAY et al., 2002 Whole-gene APC deletions cause classical familial adenomatous polyposis, but not attenuated polyposis or "multiple" colorectal adenomas. Proc. Natl. Acad. Sci. USA 99: 2954-2958.
55. SMITS, R., W. VANOORDT, A. LUZ, C. ZURCHER, S. JAGMOHAN-CHANGUR et al., 1998 Apc1638N: a mouse model for familial adenomatous polyposis-associated desmoid tumors and cutaneous cysts. Gastroenterology 114: 275-283.
56. SMITS, R., M. F. KIELMAN, C. BREUKEL, C. ZURCHER, K. NEUFELD et al., 1999 Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Genes Dev. 13: 1309-1321.
57. SOLOMON, E., R. VOSS, V. HALL, W. F. BODMER, J. R. JASS et al., 1987 Chromosome 5 allele loss in human colorectal carcinomas. Nature 328: 616-619.
58. SOUSSI, T., and C. BEROUD, 2001 Assessing TP53 status in human tumours to evaluate clinical outcome. Nat. Rev. Cancer 1: 233-240.
59. SU, L. K., K. W. KINZLER, B. VOGELSTEIN, A. C. PREISINGER, A. R. MOSER et al., 1992 Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256: 668-670.
60. THLIVERIS, A., W. SAMOWITZ, N. MATSUNAMI, J. GRODEN and R. WHITE, 1994 Demonstration of promoter activity and alternative splicing in the region 5′ to exon 1 of the APC gene. Cancer Res. 54: 2991-2995.
61. XU, Y., E. M. YANG, J. BRUGAROLAS, T. JACKS and D. BALTIMORE, 1998 Involvement of p53 and p21 in cellular defects and tumorigenesis in Atm-/- mice. Mol. Cell. Biol. 18: 4385-4390.
62. YAMAMOTO, M., T. TSUKAMOTO, H. SAKAI, N. SHIRAI, H. OHGAKI et al., 2000 p53 knockout mice (-/-) are more susceptible than (+/-) or (+/+) mice to N-methyl-N-nitrosourea stomach carcinogenesis. Carcinogenesis 21: 1891-1897.
63. YANG, K., W. EDELMANN, K. FAN, K. LAU, V. R. KOLLI et al., 1997 A mouse model of human familial adenomatous polyposis. J. Exp. Zool. 277: 245-254.
64. YANG, W. C., J. MATHEW, A. VELCICH, W. EDELMANN, R. KUCHERLAPATI et al., 2001 Targeted inactivation of the p21WAF1/cip1 gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a Western-style high-risk diet by altering cell maturation in the intestinal mucosa. Cancer Res. 61: 565-569.