Testing hypotheses for the functions of APC family proteins using null and truncation alleles in Drosophila

Development

Volumn 133, Issue 12, 2006, Pages 2407-2418

  McCartney, Brooke M ^a   Price, Meredith H ^b   Webb, Rebecca L ^a   Hayden, Melissa A ^b   Holot, Lesley M ^a   Zhou, Mengning ^a   Bejsovec, Amy ^c   Peifer, Mark ^b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

catenin; Adherens junctions; Familial adenomatous polyposis; Mutation cluster region

Indexed keywords

APC PROTEIN; CADHERIN; WNT1 PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL DIVISION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; HYPOTHESIS; INSECT DEVELOPMENT; MALE; MUTANT; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINDLE CELL;

ALLELES; ANIMALS; ARMADILLO DOMAIN PROTEINS; CELL ADHESION; CELL NUCLEUS; CYTOSKELETAL PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; HUMANS; MALE; MITOTIC SPINDLE APPARATUS; MUTATION; OVARY; PHENOTYPE; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; WNT PROTEINS;

EID: 33745919542     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02398     Document Type: Article

References (64)

1. Ahmed, Y., Hayashi, S., Levine, A. and Wieschaus, E. (1998). Regulation of armadillo by a Drosophila APC inhibits neuronal apoptosis during retinal development. CelL 93, 1171-1182.
2. Ahmed, Y., Nouri, A. and Wieschaus, E. (2002). Drosophila Apc1 and Apc2 regulate Wingless transduction throughout development. Development 129, 1751-1762.
3. Akong, K., Grevengoed, E. E., Price, M. H., McCartney, B. M., Hayden, M. A., DeNofrio, J. C. and Peifer, M. (2002a). Drosophila APC2 and APC1 play overlapping roles in wingless signaling in the embryo and imaginal discs. Dev Biol 250, 91-100.
4. Akong, K., McCartney, B. M. and Peifer, M. (2002b). Drosophila APC2 and APC1 have overlapping roles in the larval brain despite their distinct intracellular localizations. Dev. Biol. 250, 71-90.
5. Albuquerque, C., Breukel, C., van der Luijt, R., Fidalgo, P., Lage, P., Slors, F. J., Leitao, C. N., Fodde, R. and Smits, R. (2002). The 'just-right' signaling model: APC somatic mutations are selected based on a specific level of activation of the β-catenin signaling cascade. Hum. Mol. Genet 11, 1549-1560.
6. Andreu, R, Colnot, S., Godard, C., Gad, S., Chafey, R, Niwa-Kawakita, M., Laurent-Puig, R, Kahn, A., Robine, S., Perret, C. et al. (2005). Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development 132, 1443-1451.
7. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
8. Cliffe, A., Hamada, F. and Bienz, M. (2003). A role of Dishevelled in relocating axin to the plasma membrane during wingless signaling. Curr. Biol. 13, 960-966.
9. Colnot, S., Decaens, T., Niwa-Kawakita, M., Godard, C., Hamard, G., Kahn, A., Giovannini, M. and Perret, C. (2004). Liver-targeted disruption of Apc in mice activates β-catenin signaling and leads to hepatocellular carcinomas. Proc. Natl. Acad. Sci. USA 101, 17216-17221.
10. Cox, R. T, Kirkpatrick, C. and Peifer, M. (1996). Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J. Cell Biol 134, 133-148.
11. Dikovskaya, D., Newton, I. P. and Nathke, I. S. (2004). The adenomatous polyposis coli protein is required for the formation of robust spindles formed in CSF Xenopus extracts. Mol. Biol. Cell 15, 2978-2991.
12. Etienne-Manneville, S. and Hall, A. (2003). Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756.
13. Fodde, R., Kulpers, J., Rosenberg, C., Smits, R., Kielman, M., Gaspar, C., van Es, J. H., Breukel, C., Wiegant, J., Giles, R. H. et al. (2001). Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3, 433-438.
14. Foe, V. E., Odell, G. M. and Edgar, B. A. (1993). Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In The Development of Drosophila, Vol. 1 (ed. M. Bate and A. Martinez-Arias), pp. 149-300. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press.
15. Gaspar, C. and Fodde, R. (2004). APC dosage effects in tumorigenesis and stem cell differentiation. Int. J. Dev Biol. 48, 377-386.
16. Godt, D. and Tepass, U. (1998). Drosophila oocyle localization is mediated by differential cadherin-based adhesion. Nature 395, 387-391.
17. Green, R. A. and Kaplan, K. B. (2003). Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J, Cell Biol. 163, 949-961.
18. Green, R. A., Wollman, R. and Kaplan, K. B. (2005). APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol. Biol. Cell 16, 4609-4622.
19. Grigliatti, T A. (1998). Mutagenesis. In Drosophila: A Practical Approach (ed. D. B. Roberts), pp. 55-84. Oxford: Oxford University Press.
20. Hamada, F. and Bienz, M. (2002). A Drosophila APC tumour suppressor homologue functions in cellular adhesion. Nat. Cell Biol. 4, 208-213.
21. Hayashi, S., Rubinfeld, B., Souza, B., Polakis, R, Wieschaus, E. and Levine, A. J. (1997). A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates β-catenin but its zygotic expression is not essential for the regulation of Armadillo. Proc. Natl. Acad. Sci. USA 94, 242-247.
22. Huber, A. H., Nelson, W. J. and Weis, W. I. (1997). Three-dimensional structure of the armadillo repeat region of β-catenin. Cell 90, 871-882.
23. Kaplan, K. B., Burds, A. A., Swedlow, J. R., Bekir, S. S., Sorger, P. K. and Nathke, I. S. (2001). A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol. 3, 429-432.
24. Kawasaki, Y., Sato, R. and Akiyama, T. (2003). Mutated APC and Asef are involved in the migration of colorectal tumour cells. Nat. Cell Biol 5, 211-215.
25. Kleiman, M. F., Rindapaa, M., Gaspar, C., van Poppel, N., Breukel, C., van Leeuwen, S., Taketo, M. M., Roberts, S., Smits, R. and Fodde, R. (2002). Apc modulates embryonic stem-cell differentiation by controlling the dosage of β-catenin signaling. Nat. Genet 32, 594-605.
26. Kim, K. M., Calabrese, P., Tavare, S. and Shibata, D. (2004). Enhanced stem cell survival in familial adenomatous polyposis. Am. J. Pathol. 164, 1369-1377.
27. Laken, S. J., Papadopoulos, N., Petersen, G. M., Gruber, S. B., Hamilton, S. R., Giardiello, F. M., Brensinger, J. D., Vogelstein, B. and Kinzler, K. W. (1999). Analysis of masked mutations in familial adenomatous polyposis. Proc. Natl. Acad. Sci. USA 96, 2322-2326.
28. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev Cell Dev Biol. 20, 781-810.
29. Lu, B., Roegiers, F., Jan. L. Y. and Jan, Y. N. (2001). Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 409, 522-525.
30. McCartney, B. M., Dierick. H. A., Kirkpatrick, C., Moline, M. M., Baas, A., Peifer, M. and Bejsovec, A. (1999). Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis. J. Cell Biol. 146, 1303-1318.
31. McCartney, B. M., McEwen, D. G., Grevengoed, E., Maddox, P., Bejsovec, A. and Peifer, M. (2001). Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin. Nat. Cell Biol. 3, 933-938.
32. McEwen, D. G., Cox, R. T. and Peifer, M. (2000). The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning. Development 127, 3607-3617.
33. Moser, A. R., Shoemaker, A. R., Connelly, C. S., Clipson, L, Gould, K. A., Luongo, C., Dove, W. F., Siggers, P. H. and Gardner, R. L. (1995). Homozygosity for the Min allele of Apc results in disruption of mouse development prior to gastrulation. Dev Dyn. 203, 422-433.
34. Munemitsu, S., Albert, I., Souza, B., Rubinfeld, B. and Polakis, P. (1995), Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA 92, 3046-3050.
35. Nakagawa, H., Murata, Y., Koyama, K., Fujiyama, A., Miyoshi, Y., Monden, M., Akiyama, T. and Nakamura, Y. (1998). Identification of a brain-specific APC homologue, APCL, and its interaction with β-catenin. Cancer Res. 58, 5176-5181.
36. Nathke, I. S. (2004). The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu. Rev. Cell Dev Bial. 20, 337-366.
37. Oshima, M., Oshima, H., Kitagawa, K., Kobayashi, M., Itakura, C. and Taketo, M. (1995a). Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc. Natl. Acad. Sci. USA 92, 4482-4486
38. Oshima, M., Oshima, H., Kobayashi, M., Tsutsumi, M. and Taketo, M. M. (1995b). Evidence against dominant negative mechanisms of intestinal polyp formation by Apc gene mutations. Cancer Res. 55, 2719-2722.
39. Pazdera, T. M., Janardhan, R and Minden, J. S. (1998). Patterned epidermal cell death in wild-type and segment polarity mutant Drosophila embryos. Development 125, 3427-3436.
40. Peifer, M., Orsulic, S., Sweeton, D. and Wieschaus, E. (1993). A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118, 1191-1207.
41. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994). wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369-380.
42. Polakis, P. (2000). Wnt signaling and cancer. Genes Dev 14, 1837-1851.
43. Sansom, O. J., Reed, K. R., Hayes, A. J., Ireland, H., Brinkmann, H., Newton, I. P., Batlle, E., Simon-Assmann, R, Clevers, H., Nathke, I. S. et al. (2004). Loss of Apc in vivo immediately perturbs Writ signaling, differentiation, and migration. Genes Dev 18, 1385-1390.
44. Shi, S. H., Cheng, T., Jan, L. Y. and Jan, Y. N. (2004). APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14, 2025-2032.
45. Shibata, H., Toyama, K., Shioya, H., Ito, M., Hirota, M., Hasegawa, S., Matsumoto, H., Takano, H., Akiyama, T, Toyoshima, K. et al. (1997). Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278, 120-123.
46. Sieber, O. M., Heinimann, K., Gorman, P., Lamlum, H., Crabtree, M., Simpson, C. A., Davies, D., Neale, K., Hodgson, S. V., Roylance, R. R. et al. (2002a). Analysis of chromosomal instability in human colorectal adenomas with two mutational hits at APC. Proc. Natl. Acad Sci. USA 99, 16910-16915.
47. Sieber, O. M., Lamlum, H., Crabtree, M. D., Rowan, A. J., Barclay, E., Lipton, L, Hodgson, S., Thomas, H. J., Neale, K., Phillips, R. K. et al. (2002b), 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.
48. Siegfried, E., Chou, T. B. and Perrimon, N. (1992). wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167-1179.
49. Siegfried, E., Wilder, E. L. and Perrimon, N. (1994). Components of wingless signalling in Drosophila. Nature 367, 76-80.
50. Smits, R., Kleiman, M. F., Breukel, C., Zurcher, C., Neufeld, K., Jagmohan-Changur, S., Hofland, N., van Dijk, J., White, R., Edelmann, W. et al. (1999). Apc1638T. a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumarigenesis and development. Genes Dev 13, 1309-1321.
51. Su. L. K., Burrell, M., Hill, D. E., Gyuris, J., Brent, R., Wiltshire, R., Trent J., Vagelstein, B. and Kinzler, K. W. (1995). APC binds to the novel protein EB1. Cancer Res. 55, 2972-2977.
52. Sullivan, W., Fogarty, P. and Theurkauf, W. (1993). Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development 118, 1245-1254.
53. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L, Torok, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10, 672-685.
54. Tighe, A., Johnson, V. L, Albertella, M. and Taylor, S. S. (2001). Aneuploid colon cancer cells have a robust spindle checkpoint. EMBO Rep. 2, 609-614.
55. Tolwinski, N. S., Wehrli, M., Rives, A., Erdeniz, N., DiNardo, S. and Wieschaus, E. (2003). Wg/Wnt signal can be transmitted through arrow/ LRP5,6 and Axin independently of Zw3/Gsk3beta activity. Dev Cell 4, 407-418.
56. Townsley, F. M. and Bienz, M. (2000). Actin-dependent membrane association of a Drosophila epithelial APC protein and its effect on junctional Armadillo. Curr. Biol. 10, 1339-1348.
57. van Es, J. H., Kirkpatrick, C., van de Wetering, M., Molenaar, M., Miles, A., Kuipers, J., Destree, O., Peifer, M. and Clevers, H. (1999). Identification of APC2, a homologue of the adenomatous polyposis coli tumour suppressor. Curr. Biol. 9, 105-108.
58. Wen, Y., Eng, C. H., Schmoranzer, J., Cabrera-Poch, N., Morris, E. J., Chen, M., Wallar, B. J., Alberts, A. S. and Gundersen, G. G. (2004). EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6, 820-830.
59. Wieschaus, E. and Nusslein-Volhard, C. (1998). Looking at embryos, In Drosophila: A Practical Approach(ed. D. B. Roberts), pp. 179-214. Oxford: Oxford University Press.
60. Yamanaka, H., Hashimoto, N., Koyama, K., Nakagawa, H., Nakamura, Y. and Noguchi, K. (2002). Expression of Apc2 during mouse development. Brain Res. Gene Expr. Patterns 1, 107-114.
61. Yamashita, Y. M., Jones, D. L. and Fuller, M. T. (2003). Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301, 1547-1550.
62. Yu, X. and Bienz, M. (1999). Ubiquitous expression of a Drosophila adenomatous polyposis coli homolog and its localization in cortical actin caps. Mech. Dev 84, 69-73.
63. Yu, X., Waltzer, L. and Bienz, M. (1999). A new Drosophila APC homologue associated with adhesive zones of epithelial cells. Nat. Cell Biol. 1, 144-151.
64. Zhou, F. Q., Zhou, J., Dedhar, S., Wu, Y. H. and Snider, W. D. (2004). NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42, 897-912.