Reciprocal Asymmetry of SYS-1/beta-catenin and POP-1/TCF Controls Asymmetric Divisions in Caenorhabditis Elegans

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2007 Feb 14

PMID 17296929

Citations 70

Authors

Bryan T Phillips

Ambrose R Kidd 3rd

Ryan King

Jeff Hardin

Judith Kimble

Affiliations

Soon will be listed here.

Abstract

beta-Catenins are conserved regulators of metazoan development that function with TCF DNA-binding proteins to activate transcription. In Caenorhabditis elegans, SYS-1/beta-catenin and POP-1/TCF regulate several asymmetric divisions, including that of the somatic gonadal precursor cell (SGP). In the distal but not the proximal SGP daughter, SYS-1/beta-catenin and POP-1/TCF transcriptionally activate ceh-22 to specify the distal fate. Here, we investigate the distribution of SYS-1/beta-catenin and its regulation. Using a rescuing transgene, VNS::SYS-1, which fuses VENUS fluorescent protein to SYS-1, we find more VNS::SYS-1 in distal than proximal SGP daughters, a phenomenon we call "SYS-1 asymmetry." In addition, SYS-1 asymmetry is seen in many other tissues, consistent with the idea that SYS-1 regulates asymmetric divisions broadly during C. elegans development. In particular, SYS-1 is more abundant in E than MS, and SYS-1 is critical for the endodermal fate. In all cases, SYS-1 is reciprocal to POP-1 asymmetry: cells with higher SYS-1 have lower POP-1, and vice versa. SYS-1 asymmetry is controlled posttranslationally and relies on frizzled and dishevelled homologs, which also control POP-1 asymmetry. Therefore, upstream regulators modulate the SYS-1 to POP-1 ratio by increasing SYS-1 and decreasing POP-1 within the same cell. By contrast, SYS-1 asymmetry does not rely on WRM-1, which appears specialized for POP-1 asymmetry. We suggest a two-pronged pathway for control of SYS-1:POP-1, which can robustly accomplish differential gene expression in daughters of an asymmetric cell division.

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References

Maduro M, Kasmir J, Zhu J, Rothman J . The Wnt effector POP-1 and the PAL-1/Caudal homeoprotein collaborate with SKN-1 to activate C. elegans endoderm development. Dev Biol. 2005; 285(2):510-23. DOI: 10.1016/j.ydbio.2005.06.022. View

Bischoff M, Schnabel R . A posterior centre establishes and maintains polarity of the Caenorhabditis elegans embryo by a Wnt-dependent relay mechanism. PLoS Biol. 2006; 4(12):e396. PMC: 1637133. DOI: 10.1371/journal.pbio.0040396. View

Lam N, Chesney M, Kimble J . Wnt signaling and CEH-22/tinman/Nkx2.5 specify a stem cell niche in C. elegans. Curr Biol. 2006; 16(3):287-95. PMC: 1637041. DOI: 10.1016/j.cub.2005.12.015. View

Goldstein B, Takeshita H, Mizumoto K, Sawa H . Wnt signals can function as positional cues in establishing cell polarity. Dev Cell. 2006; 10(3):391-6. PMC: 2221774. DOI: 10.1016/j.devcel.2005.12.016. View

Wu M, Herman M . A novel noncanonical Wnt pathway is involved in the regulation of the asymmetric B cell division in C. elegans. Dev Biol. 2006; 293(2):316-29. DOI: 10.1016/j.ydbio.2005.12.024. View

Walston T, Hardin J . Wnt-dependent spindle polarization in the early C. elegans embryo. Semin Cell Dev Biol. 2006; 17(2):204-13. DOI: 10.1016/j.semcdb.2006.04.005. View

Barrow J . Wnt/PCP signaling: a veritable polar star in establishing patterns of polarity in embryonic tissues. Semin Cell Dev Biol. 2006; 17(2):185-93. DOI: 10.1016/j.semcdb.2006.04.002. View

Walston T, Guo C, Proenca R, Wu M, Herman M, Hardin J . mig-5/Dsh controls cell fate determination and cell migration in C. elegans. Dev Biol. 2006; 298(2):485-97. DOI: 10.1016/j.ydbio.2006.06.053. View

Zhu X, Joh K, Hedgecock E, Hori K . Identification of epi-1 locus as a laminin alpha chain gene in the nematode Caenorhabditis elegans and characterization of epi-1 mutant alleles. DNA Seq. 2000; 10(4-5):207-17. DOI: 10.3109/10425179909033950. View

10.

Whangbo J, Harris J, Kenyon C . Multiple levels of regulation specify the polarity of an asymmetric cell division in C. elegans. Development. 2000; 127(21):4587-98. DOI: 10.1242/dev.127.21.4587. View

11.

Eisenmann D, Kim S . Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. Genetics. 2000; 156(3):1097-116. PMC: 1461321. DOI: 10.1093/genetics/156.3.1097. View

12.

Miskowski J, Li Y, Kimble J . The sys-1 gene and sexual dimorphism during gonadogenesis in Caenorhabditis elegans. Dev Biol. 2001; 230(1):61-73. DOI: 10.1006/dbio.2000.9998. View

13.

Herman M . C. elegans POP-1/TCF functions in a canonical Wnt pathway that controls cell migration and in a noncanonical Wnt pathway that controls cell polarity. Development. 2001; 128(4):581-90. DOI: 10.1242/dev.128.4.581. View

14.

Siegfried K, Kimble J . POP-1 controls axis formation during early gonadogenesis in C. elegans. Development. 2002; 129(2):443-53. DOI: 10.1242/dev.129.2.443. View

15.

van Noort M, Clevers H . TCF transcription factors, mediators of Wnt-signaling in development and cancer. Dev Biol. 2002; 244(1):1-8. DOI: 10.1006/dbio.2001.0566. View

16.

Korswagen H, Coudreuse D, Betist M, van de Water S, Zivkovic D, Clevers H . The Axin-like protein PRY-1 is a negative regulator of a canonical Wnt pathway in C. elegans. Genes Dev. 2002; 16(10):1291-302. PMC: 186271. DOI: 10.1101/gad.981802. View

17.

Herman M . Control of cell polarity by noncanonical Wnt signaling in C. elegans. Semin Cell Dev Biol. 2002; 13(3):233-41. DOI: 10.1016/s1084-9521(02)00051-4. View

18.

Maduro M, Lin R, Rothman J . Dynamics of a developmental switch: recursive intracellular and intranuclear redistribution of Caenorhabditis elegans POP-1 parallels Wnt-inhibited transcriptional repression. Dev Biol. 2002; 248(1):128-42. DOI: 10.1006/dbio.2002.0721. View

19.

van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A . The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 2002; 111(2):241-50. DOI: 10.1016/s0092-8674(02)01014-0. View

20.

Reya T, Duncan A, Ailles L, Domen J, Scherer D, Willert K . A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003; 423(6938):409-14. DOI: 10.1038/nature01593. View