The tumor suppressor APC differentially regulates multiple β-catenins through the function of axin and CKIα during C. elegans asymmetric stem cell divisions

Journal of Cell Science

Volumn 127, Issue 12, 2014, Pages 2771-2781

  Baldwin, Austin T ^a   Phillips, Bryan T ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

APC; C. elegans; SYS 1; Wnt; WRM 1; catenin

Indexed keywords

APC PROTEIN; APR 1 PROTEIN; AXIN; BETA CATENIN; CAENORHABDITIS ELEGANS PROTEIN; CASEIN KINASE IALPHA; KIN 19 PROTEIN; SYS 1 PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WRM 1 PROTEIN; CYTOSKELETON PROTEIN; KIN-19 PROTEIN, C ELEGANS; PROTEIN KINASE; PRY-1 PROTEIN, C ELEGANS; SYS-1 PROTEIN, C ELEGANS; TRANSCRIPTION FACTOR; WRM-1 PROTEIN, C ELEGANS;

ANIMAL CELL; ARTICLE; ASYMMETRIC CELL DIVISION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DAUGHTER CELL; GENE CONTROL; MICROTUBULE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STEM CELL; WNT SIGNALING PATHWAY; ACTIVE TRANSPORT; ANIMAL; CELL NUCLEUS; CELL POLARITY; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; ASYMMETRIC CELL DIVISION; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CELL POLARITY; CYTOSKELETAL PROTEINS; MICROTUBULES; PROTEIN KINASES; PROTEIN TRANSPORT; STEM CELLS; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84902440272     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.146514     Document Type: Article

References (50)

1. Banerjee, D., Chen, X., Lin, S. Y. and Slack, F. J. (2010). kin-19/casein kinase Ia has dual functions in regulating asymmetric division and terminal differentiation in C. elegans epidermal stem cells. Cell Cycle 9, 4748-4765.
2. Barth, A. I. M., Caro-Gonzalez, H. Y. and Nelson, W. J. (2008). Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin. Cell Dev. Biol. 19, 245-251.
3. Bellis, J., Duluc, I., Romagnolo, B., Perret, C., Faux, M. C., Dujardin, D., Formstone, C., Lightowler, S., Ramsay, R. G., Freund, J.-N. et al. (2012). The tumor suppressor Apc controls planar cell polarities central to gut homeostasis. J. Cell Biol. 198, 331-341.
4. Brocardo, M. and Henderson, B. R. (2008). APC shuttling to the membrane, nucleus and beyond. Trends Cell Biol. 18, 587-596.
5. Cicalese, A., Bonizzi, G., Pasi, C. E., Faretta, M., Ronzoni, S., Giulini, B., Brisken, C., Minucci, S., Di Fiore, P. P. and Pelicci, P. G. (2009). The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138, 1083-1095.
6. Clevers, H. and Nusse, R. (2012). Wnt/β-catenin signaling and disease. Cell 149, 1192-1205.
7. Gleason, J. E. and Eisenmann, D. M. (2010). Wnt signaling controls the stem cell-like asymmetric division of the epithelial seam cells during C. elegans larval development. Dev. Biol. 348, 58-66.
8. Gorrepati, L., Thompson, K. W. and Eisenmann, D. M. (2013). C. elegans GATA factors EGL-18 and ELT-6 function downstream of Wnt signaling to maintain the progenitor fate during larval asymmetric divisions of the seam cells. Development 140, 2093-2102.
9. 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.
10. Ha, N.-C., Tonozuka, T., Stamos, J. L., Choi, H.-J. and Weis, W. I. (2004). Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol. Cell 15, 511-521.
11. Habib, S. J., Chen, B.-C., Tsai, F.-C., Anastassiadis, K., Meyer, T., Betzig, E. and Nusse, R. (2013). A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339, 1445-1448.
12. Harterink, M., Kim, D. H., Middelkoop, T. C., Doan, T. D., van Oudenaarden, A. and Korswagen, H. C. (2011). Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein. Development 138, 2915-2924.
13. Horvitz, H. R. and Herskowitz, I. (1992). Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68, 237-255.
14. Huang, S., Shetty, P., Robertson, S. M. and Lin, R. (2007). Binary cell fate specification during C. elegans embryogenesis driven by reiterated reciprocal asymmetry of TCF POP-1 and its coactivator beta-catenin SYS-1. Development 134 2685-2695.
15. Huang, X., Tian, E., Xu, Y. and Zhang, H. (2009). The C. elegans engrailed homolog ceh-16 regulates the self-renewal expansion division of stem cell-like seam cells. Dev. Biol. 333, 337-347.
16. Hughes, S., Brabin, C., Appleford, P. J. and Woollard, A. (2013). CEH-20/Pbx and UNC-62/Meis function upstream of rnt-1/Runx to regulate asymmetric divisions of the C. elegans stem-like seam cells. Biology Open 6, 20134549.
17. Jackson, B. M. and Eisenmann, D. M. (2012). β-catenin-dependent Wnt signaling in C. elegans: teaching an old dog a new trick. Cold Spring Harb. Perspect. Biol. 4, a007948.
18. Kanamori, T., Inoue, T., Sakamoto, T., Gengyo-Ando, K., Tsujimoto, M., Mitani, S., Sawa, H., Aoki, J. and Arai, H. (2008). Beta-catenin asymmetry is regulated by PLA1 and retrograde traffic in C. elegans stem cell divisions. EMBO J. 27, 1647-1657.
19. Khramtsov, A. I., Khramtsova, G. F., Tretiakova, M., Huo, D., Olopade, O. I. and Goss, K. H. (2010). Wnt/beta-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am. J. Pathol. 176, 2911-2920.
20. Kidd, A. R., III, Miskowski, J. A., Siegfried, K. R., Sawa, H. and Kimble, J. (2005). A beta-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 121, 761-772.
21. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
22. Korswagen, H. C., Herman, M. A. and Clevers, H. C. (2000). Distinct betacatenins mediate adhesion and signalling functions in C. elegans. Nature 406, 527-532.
23. Korswagen, H. C., Coudreuse, D. Y. M., Betist, M. C., van de Water, S., Zivkovic, D. and Clevers, H. C. (2002). The Axin-like protein PRY-1 is a negative regulator of a canonical Wnt pathway in C. elegans. Genes Dev. 16, 1291-1302.
24. Lo, M.-C., Gay, F., Odom, R., Shi, Y. and Lin, R. (2004). Phosphorylation by the beta-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans. Cell 117, 95-106.
25. Lowry, R. (2010). VassarStats. Available at: http://vassarstats.net/index.html.
26. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
27. Min, K., Kang, J. and Lee, J. (2010). A modified feeding RNAi method for simultaneous knock-down of more than one gene in Caenorhabditis elegans. Biotechniques 48, 229-232.
28. Mizumoto, K. and Sawa, H. (2007). Cortical beta-catenin and APC regulate asymmetric nuclear beta-catenin localization during asymmetric cell division in C. elegans. Dev. Cell 12, 287-299.
29. Morrison, S. J. and Kimble, J. (2006). Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441, 1068-1074.
30. Nakamura, M., Zhou, X. Z. and Lu, K. P. (2001). Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr. Biol. 11, 1062-1067.
31. Nakamura, K., Kim, S., Ishidate, T., Bei, Y., Pang, K., Shirayama, M., Trzepacz, C., Brownell, D. R. and Mello, C. C. (2005). Wnt signaling drives WRM-1/beta-catenin asymmetries in early C. elegans embryos. Genes Dev. 19, 1749-1754.
32. Neufeld, K. L. (2009). Nuclear APC. Adv. Exp. Med. Biol. 656, 13-29.
33. Neufeld, K. L., Nix, D. A., Bogerd, H., Kang, Y., Beckerle, M. C., Cullen, B. R. and White, R. L. (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.
34. Neumüller, R. A. and Knoblich, J. A. (2009). Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23, 2675-2699.
35. Phillips, B. T. and Kimble, J. (2009). A new look at TCF and beta-catenin through the lens of a divergent C. elegans Wnt pathway. Dev. Cell 17, 27-34.
36. Phillips, B. T., Kidd, A. R., 3rd, King, R., Hardin, J. and Kimble, J. (2007). Reciprocal asymmetry of SYS-1/beta-catenin and POP-1/TCF controls asymmetric divisions in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104 3231-3236.
37. Powell, A. E., Shung, C.-Y., Saylor, K. W., Müllendorff, K. A., Weiss, J. B. and Wong, M. H. (2010). Lessons from development: A role for asymmetric stem cell division in cancer. Stem Cell Res. 4, 3-9.
38. Price, M. A. (2006). CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev. 20, 399-410.
39. Quyn, A. J., Appleton, P. L., Carey, F. A., Steele, R. J. C., Barker, N., Clevers, H., Ridgway, R. A., Sansom, O. J. and Näthke, I. S. (2010). Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 6, 175-181.
40. Ren, H. and Zhang, H. (2010). Wnt signaling controls temporal identities of seam cells in Caenorhabditis elegans. Dev. Biol. 345, 144-155.
41. Reya, T. and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434 843-850.
42. Rocheleau, C. E., Yasuda, J., Shin, T. H., Lin, R., Sawa, H., Okano, H., Priess, J. R., Davis, R. J. and Mello, C. C. (1999). WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 97, 717-726.
43. Rubinfeld, B., Tice, D. A. and Polakis, P. (2001). Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1e. J. Biol. Chem. 276, 39037-39045.
44. Sawa, H. (2012). Control of cell polarity and asymmetric division in C. elegans. Curr. Top. Dev. Biol. 101, 55-76.
45. Sugioka, K., Mizumoto, K. and Sawa, H. (2011). Wnt regulates spindle asymmetry to generate asymmetric nuclear β-catenin in C. elegans. Cell 146, 942-954.
46. Timmons, L., Court, D. L. and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
47. Wildwater, M., Sander, N., de Vreede, G. and van den Heuvel, S. (2011). Cell shape and Wnt signaling redundantly control the division axis of C. elegans epithelial stem cells. Development 138, 4375-4385.
48. Yamamoto, Y., Takeshita, H. and Sawa, H. (2011). Multiple Wnts redundantly control polarity orientation in Caenorhabditis elegans epithelial stem cells. PLoS Genet. 7, e1002308.
49. Yang, X.-D., Huang, S., Lo, M.-C., Mizumoto, K., Sawa, H., Xu, W., Robertson, S. and Lin, R. (2011). Distinct and mutually inhibitory binding by two divergent {beta}-catenins coordinates TCF levels and activity in C. elegans. Development 138 4255-4265.
50. Zumbrunn, J., Kinoshita, K., Hyman, A. A. and Näthke, I. S. (2001). Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 b phosphorylation. Curr. Biol. 11, 44-49.