APC as a mobile scaffold: Regulation and function at the nucleus, centrosomes, and mitochondria

IUBMB Life

Volumn 64, Issue 3, 2012, Pages 209-214

  Lui, Christina ^a   Mills, Kate ^a   Brocardo, Mariana G ^a   Sharma, Manisha ^a   Henderson, Beric R ^a  

^a WESTMEAD HOSPITAL   (Australia)

Author keywords

APC; centrosome; mitochondria; nucleus; protein transport

Indexed keywords

APC PROTEIN; BETA CATENIN; DNA; NUCLEOPORIN; NUCLEOPORIN 153; NUCLEOPORIN 358; UNCLASSIFIED DRUG;

APOPTOSIS; CELL CYCLE ARREST; CELL MIGRATION; CELL NUCLEUS; CELL POLARITY; CELL SURVIVAL; CENTROSOME; DNA REPAIR; DNA REPLICATION; HUMAN; MITOCHONDRION; MITOSIS; MITOSIS SPINDLE; NUCLEAR EXPORT; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEOCYTOPLASMIC TRANSPORT; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CELL MOVEMENT; CELL NUCLEUS; CENTROSOME; HUMANS; MITOCHONDRIA;

EID: 84857250148     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.599     Document Type: Review

References (50)

1. Fodde, R., Smits, R., and, Clevers, H., (2001) APC, signal transduction and genetic instability in colorectal cancer. Nat. Rev. Cancer 1, 55-67. (Pubitemid 33741881)
2. Fodde, R., Kuipers, J., Rosenberg, C., Smits, R., Kielman, M., et al. (2001) Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat. Cell Biol. 3, 433-438. (Pubitemid 32288454)
3. Senda, T., Iizuka-Kogo, A., Onouchi, T., and, Shimomura, A., (2007) adenomatous polyposis coli (APC) plays multiple roles in the intestinal and colorectal epithelia. Med. Mol. Morphol. 40, 68-81. (Pubitemid 47305230)
4. Akiyama, T., and, Kawasaki, Y., (2006) Wnt signalling and the actin cytoskeleton. Oncogene 25, 7538-7544. (Pubitemid 44885753)
5. Nathke, I., (2006) Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat. Rev. Cancer 6, 967-974. (Pubitemid 44862681)
6. Polakis, P., (2007) The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45-51. (Pubitemid 46109296)
7. Brocardo, M., and, Henderson, B. R., (2008) APC shuttling to the membrane, nucleus and beyond. Trends Cell Biol. 18, 587-596.
8. Caldwell, C. M., and, Kaplan, K. B., (2009) The role of APC in mitosis and in chromosome instability. Adv. Exp. Med. Biol. 656, 51-64.
9. Henderson, B. R., and, Fagotto, F., (2002) The ins and outs of APC and beta-catenin nuclear transport. EMBO Rep. 3, 834-839. (Pubitemid 35154107)
10. Bahmanyar, S., Nelson, W. J., and, Barth, A. I., (2009) Role of APC and its binding partners in regulating microtubules in mitosis. Adv. Exp. Med. Biol. 656, 65-74.
11. Pease, J. C., and, Tirnauer, J. S., (2011) Mitotic spindle misorientation in cancer-out of alignment and into the fire. J. Cell Sci. 124, 1007-1016.
12. Henderson, B. R., (2000) Nuclear-cytoplasmic shuttling of APC regulates beta-catenin subcellular localization and turnover. Nat. Cell Biol. 2, 653-660.
13. Rosin-Arbesfeld, R., Townsley, F., and, Bienz, M., (2000) The APC tumour suppressor has a nuclear export function. Nature 406, 1009-1012.
14. Neufeld, K. L., Nix, D. A., Bogerd, H., Kang, Y., Beckerle, M. C., et al. (2000) Adenomatous polyposis coli protein contains two nuclear export signals and shuttles between the nucleus and cytoplasm. Proc. Natl. Acad. Sci. USA 97, 12085-12090.
15. Neufeld, K. L., (2009) Nuclear APC. Adv. Exp. Med. Biol. 656, 13-29.
16. Etienne-Manneville, S., (2009) APC in cell migration. Adv. Exp. Med. Biol. 656, 30-40.
17. Kennell, J., and, Cadigan, K. M., (2009) APC and beta-catenin degradation. Adv. Exp. Med. Biol. 656, 1-12.
18. Galea, M. A., Eleftheriou, A., and, Henderson, B. R., (2001) ARM domain-dependent nuclear import of adenomatous polyposis coli protein is stimulated by the B56 alpha subunit of protein phosphatase 2A. J. Biol. Chem. 276, 45833-45839.
19. Brocardo, M., Nathke, I. S., and, Henderson, B. R., (2005) Redefining the subcellular location and transport of APC: new insights using a panel of antibodies. EMBO Rep. 6, 184-190. (Pubitemid 40309417)
20. Zhang, F., White, R. L., and, Neufeld, K. L., (2000) Phosphorylation near nuclear localization signal regulates nuclear import of adenomatous polyposis coli protein. Proc. Natl. Acad. Sci. USA 97, 12577-12582.
21. Dikovskaya, D., Li, Z., Newton, I. P., Davidson, I., Hutchins, J. R., et al. (2010) Microtubule assembly by the Apc protein is regulated by importin-beta-RanGTP. J. Cell Sci. 123, 736-746.
22. Neufeld, K. L., and, White, R. L., (1997) Nuclear and cytoplasmic localizations of the adenomatous polyposis coli protein. Proc. Natl. Acad. Sci. USA 94, 3034-3039. (Pubitemid 27157259)
23. Deka, J., Herter, P., Sprenger-Haussels, M., Koosch, S., Franz, D., et al. (1999) The APC protein binds to A/T rich DNA sequences. Oncogene 18, 5654-5661. (Pubitemid 29497600)
24. Schneikert, J., and, Behrens, J., (2006) Truncated APC is required for cell proliferation and DNA replication. Int. J. Cancer 119, 74-79.
25. Brocardo, M. G., Borowiec, J. A., and, Henderson, B. R., (2011) Adenomatous polyposis coli protein regulates the cellular response to DNA replication stress. Int. J. Biochem. Cell Biol. 43, 1354-1364.
26. Qian, J., Sarnaik, A. A., Bonney, T. M., Keirsey, J., Combs, K. A., et al. (2008) The APC tumor suppressor inhibits DNA replication by directly binding to DNA via its carboxyl terminus. Gastroenterology 135, 152-162. (Pubitemid 351899022)
27. Kouzmenko, A. P., Takeyama, K., Kawasaki, Y., Akiyama, T., and, Kato, S., (2008) Truncation mutations abolish chromatin-associated activities of adenomatous polyposis coli. Oncogene 27, 4888-4899.
28. Feng, J., Wakeman, T., Yong, S., Wu, X., Kornbluth, S., et al. (2009) Protein phosphatase 2A-dependent dephosphorylation of replication protein A is required for the repair of DNA breaks induced by replication stress. Mol. Cell Biol. 29, 5696-5709.
29. Narayan, S., Jaiswal, A. S., and, Balusu, R., (2005) Tumor suppressor APC blocks DNA polymerase beta-dependent strand displacement synthesis during long patch but not short patch base excision repair and increases sensitivity to methylmethane sulfonate. J. Biol. Chem. 280, 6942-6949. (Pubitemid 40341250)
30. Jaiswal, A. S., and, Narayan, S., (2008) A novel function of adenomatous polyposis coli (APC) in regulating DNA repair. Cancer Lett. 271, 272-280.
31. Chen, T., Yang, I., Irby, R., Shain, K. H., Wang, H. G., et al. (2003) Regulation of caspase expression and apoptosis by adenomatous polyposis coli. Cancer Res. 63, 4368-4374. (Pubitemid 36951005)
32. Collin, L., Schlessinger, K., and, Hall, A., (2008) APC nuclear membrane association and microtubule polarity. Biol. Cell 100, 243-252. (Pubitemid 351517087)
33. Ball, J. R., and, Ullman, K. S., (2005) Versatility at the nuclear pore complex: lessons learned from the nucleoporin Nup153. Chromosoma 114, 319-330. (Pubitemid 41662801)
34. Murawala, P., Tripathi, M. M., Vyas, P., Salunke, A., and, Joseph, J., (2009) Nup358 interacts with APC and plays a role in cell polarization. J. Cell Sci. 122, 3113-3122.
35. Kaplan, K. B., Burds, A. A., Swedlow, J. R., Bekir, S. S., Sorger, P. K., et al. (2001) A role for the adenomatous polyposis coli protein in chromosome segregation. Nat. Cell Biol. 3, 429-432. (Pubitemid 32288453)
36. Etienne-Manneville, S., and, Hall, A., (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756. (Pubitemid 36227627)
37. Wang, Y., Azuma, Y., Friedman, D. B., Coffey, R. J., and, Neufeld, K. L., (2009) Novel association of APC with intermediate filaments identified using a new versatile APC antibody. BMC Cell Biol. 10, 75.
38. Coffinier, C., Fong, L. G., and, Young, S. G., (2010) LINCing lamin B2 to neuronal migration: growing evidence for cell-specific roles of B-type lamins. Nucleus 1, 407-411.
39. Louie, R. K., Bahmanyar, S., Siemers, K. A., Votin, V., Chang, P., et al. (2004) Adenomatous polyposis coli and EB1 localize in close proximity of the mother centriole and EB1 is a functional component of centrosomes. J. Cell. Sci. 117, 1117-1128. (Pubitemid 38456093)
40. 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. (Pubitemid 32707708)
41. Splinter, D., Tanenbaum, M. E., Lindqvist, A., Jaarsma, D., Flotho, A., et al. (2010) Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 8, e1000350.
42. Bolhy, S., Bouhlel, I., Dultz, E., Nayak, T., Zuccolo, M., et al. (2011) A Nup133-dependent NPC-anchored network tethers centrosomes to the nuclear envelope in prophase. J. Cell Biol. 192, 855-871.
43. Fukasawa, K., (2007) Oncogenes and tumour suppressors take on centrosomes. Nat. Rev. Cancer 7, 911-924. (Pubitemid 350165854)
44. Dikovskaya, D., Schiffmann, D., Newton, I. P., Oakley, A., Kroboth, K., et al. (2007) Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176, 183-195. (Pubitemid 46143259)
45. Steigerwald, K., Behbehani, G. K., Combs, K. A., Barton, M. C., and, Groden, J., (2005) The APC tumor suppressor promotes transcription-independent apoptosis in vitro. Mol. Cancer Res. 3, 78-89. (Pubitemid 40271138)
46. Tighe, A., Johnson, V. L., and, Taylor, S. S., (2004) Truncating APC mutations have dominant effects on proliferation, spindle checkpoint control, survival and chromosome stability. J. Cell Sci. 117, 6339-6353. (Pubitemid 40214561)
47. Qian, J., Steigerwald, K., Combs, K. A., Barton, M. C., and, Groden, J., (2007) Caspase cleavage of the APC tumor suppressor and release of an amino-terminal domain is required for the transcription-independent function of APC in apoptosis. Oncogene 26, 4872-4876. (Pubitemid 47093166)
48. Schneikert, J., Grohmann, A., and, Behrens, J., (2007) Truncated APC regulates the transcriptional activity of beta-catenin in a cell cycle dependent manner. Hum. Mol. Genet. 16, 199-209. (Pubitemid 46179002)
49. Brocardo, M., Lei, Y., Tighe, A., Taylor, S. S., Mok, M. T., et al. (2008) Mitochondrial targeting of adenomatous polyposis coli protein is stimulated by truncating cancer mutations: regulation of Bcl-2 and implications for cell survival. J. Biol. Chem. 283, 5950-5959.
50. Qian, J., Perchiniak, E. M., Sun, K., and, Groden, J., (2010) The mitochondrial protein hTID-1 partners with the caspase-cleaved adenomatous polyposis cell tumor suppressor to facilitate apoptosis. Gastroenterology 138, 1418-1428.