A Compound PCP Scheme Underlies Sequential Rosettes-based Cell Intercalation

Overview

Journal Development

Specialty Biology

Date 2023 Mar 28

PMID 36975724

Authors

Yichi Xu

Yunsheng Cheng

Allison T Chen

Zhirong Bao

Affiliations

Soon will be listed here.

Abstract

The formation of sequential rosettes is a type of collective cell behavior recently discovered in the Caenorhabditis elegans embryo that mediates directional cell migration through sequential formation and resolution of multicellular rosettes involving the migrating cell and its neighboring cells along the way. Here, we show that a planar cell polarity (PCP)-based polarity scheme regulates sequential rosettes, which is distinct from the known mode of PCP regulation in multicellular rosettes during the process of convergent extension. Specifically, non-muscle myosin (NMY) localization and edge contraction are perpendicular to that of Van Gogh as opposed to colocalizing with Van Gogh. Further analyses suggest a two-component polarity scheme: one being the canonical PCP pathway with MIG-1/Frizzled and VANG-1/Van Gogh localized to the vertical edges, the other being MIG-1/Frizzled and NMY-2 localized to the midline/contracting edges. The NMY-2 localization and contraction of the midline edges also required LAT-1/Latrophilin, an adhesion G protein-coupled receptor that has not been shown to regulate multicellular rosettes. Our results establish a distinct mode of PCP-mediated cell intercalation and shed light on the versatile nature of the PCP pathway.

References

Harrell J, Goldstein B . Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators. Dev Biol. 2010; 350(1):1-12. PMC: 3022094. DOI: 10.1016/j.ydbio.2010.09.012. View

Ghenea S, Boudreau J, Lague N, Chin-Sang I . The VAB-1 Eph receptor tyrosine kinase and SAX-3/Robo neuronal receptors function together during C. elegans embryonic morphogenesis. Development. 2005; 132(16):3679-90. DOI: 10.1242/dev.01947. View

Axelrod J . Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 2001; 15(10):1182-7. PMC: 313798. DOI: 10.1101/gad.890501. View

Moore J, Du Z, Bao Z . Systematic quantification of developmental phenotypes at single-cell resolution during embryogenesis. Development. 2013; 140(15):3266-74. PMC: 3931741. DOI: 10.1242/dev.096040. View

Bao Z, Murray J, Boyle T, Ooi S, Sandel M, Waterston R . Automated cell lineage tracing in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2006; 103(8):2707-12. PMC: 1413828. DOI: 10.1073/pnas.0511111103. View

Williams M, Solnica-Krezel L . Cellular and molecular mechanisms of convergence and extension in zebrafish. Curr Top Dev Biol. 2020; 136:377-407. PMC: 9306301. DOI: 10.1016/bs.ctdb.2019.08.001. View

Ambegaonkar A, Pan G, Mani M, Feng Y, Irvine K . Propagation of Dachsous-Fat planar cell polarity. Curr Biol. 2012; 22(14):1302-8. PMC: 3418676. DOI: 10.1016/j.cub.2012.05.049. View

Shah P, Santella A, Jacobo A, Siletti K, Hudspeth A, Bao Z . An In Toto Approach to Dissecting Cellular Interactions in Complex Tissues. Dev Cell. 2017; 43(4):530-540.e4. PMC: 5728429. DOI: 10.1016/j.devcel.2017.10.021. View

Walck-Shannon E, Lucas B, Chin-Sang I, Reiner D, Kumfer K, Cochran H . CDC-42 Orients Cell Migration during Epithelial Intercalation in the Caenorhabditis elegans Epidermis. PLoS Genet. 2016; 12(11):e1006415. PMC: 5127194. DOI: 10.1371/journal.pgen.1006415. View

10.

Brittle A, Thomas C, Strutt D . Planar polarity specification through asymmetric subcellular localization of Fat and Dachsous. Curr Biol. 2012; 22(10):907-14. PMC: 3362735. DOI: 10.1016/j.cub.2012.03.053. View

11.

Butler M, Wallingford J . Planar cell polarity in development and disease. Nat Rev Mol Cell Biol. 2017; 18(6):375-388. PMC: 5826606. DOI: 10.1038/nrm.2017.11. View

12.

Bao Z, Murray J . Mounting Caenorhabditis elegans embryos for live imaging of embryogenesis. Cold Spring Harb Protoc. 2011; 2011(9). DOI: 10.1101/pdb.prot065599. View

13.

George S, Ding M, Moseley S, Lynch A, Chisholm A . The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans. Cell. 2000; 99(7):781-90. DOI: 10.1016/s0092-8674(00)81675-x. View

14.

Pan C, Howell J, Clark S, Hilliard M, Cordes S, Bargmann C . Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell. 2006; 10(3):367-77. DOI: 10.1016/j.devcel.2006.02.010. View

15.

Langenhan T, Promel S, Mestek L, Esmaeili B, Waller-Evans H, Hennig C . Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev Cell. 2009; 17(4):494-504. PMC: 2819344. DOI: 10.1016/j.devcel.2009.08.008. View

16.

Williams M, Yen W, Lu X, Sutherland A . Distinct apical and basolateral mechanisms drive planar cell polarity-dependent convergent extension of the mouse neural plate. Dev Cell. 2014; 29(1):34-46. PMC: 4120093. DOI: 10.1016/j.devcel.2014.02.007. View

17.

Koca Y, Collu G, Mlodzik M . Wnt-frizzled planar cell polarity signaling in the regulation of cell motility. Curr Top Dev Biol. 2022; 150:255-297. PMC: 9870057. DOI: 10.1016/bs.ctdb.2022.03.006. View

18.

Cravo J, van den Heuvel S . Tissue polarity and PCP protein function: C. elegans as an emerging model. Curr Opin Cell Biol. 2019; 62:159-167. DOI: 10.1016/j.ceb.2019.11.004. View

19.

Bernadskaya Y, Wallace A, Nguyen J, Mohler W, Soto M . UNC-40/DCC, SAX-3/Robo, and VAB-1/Eph polarize F-actin during embryonic morphogenesis by regulating the WAVE/SCAR actin nucleation complex. PLoS Genet. 2012; 8(8):e1002863. PMC: 3410845. DOI: 10.1371/journal.pgen.1002863. View

20.

Huebner R, Wallingford J . Coming to Consensus: A Unifying Model Emerges for Convergent Extension. Dev Cell. 2018; 46(4):389-396. PMC: 6140352. DOI: 10.1016/j.devcel.2018.08.003. View