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Robust linkage between adherens junctions and the actomyosin cytoskeleton allows cells to change shape and move during morphogenesis without tearing tissues apart. The Drosophila multidomain protein Canoe and its mammalian homolog afadin are crucial for this, as in their absence many events of morphogenesis fail. To define the mechanism of action for Canoe, we are taking it apart. Canoe has five folded protein domains and a long intrinsically disordered region. The largest is the Dilute domain, which is shared by Canoe and myosin V. To define the roles of this domain in Canoe, we combined biochemical, genetic and cell biological assays. AlphaFold was used to predict its structure, providing similarities and contrasts with Myosin V. Biochemical data suggested one potential shared function - the ability to dimerize. We generated Canoe mutants with the Dilute domain deleted (CnoΔDIL). Surprisingly, they were viable and fertile. CnoΔDIL localized to adherens junctions and was enriched at junctions under tension. However, when its dose was reduced, CnoΔDIL did not provide fully wild-type function. Furthermore, canoeΔDIL mutants had defects in the orchestrated cell rearrangements of eye development. This reveals the robustness of junction-cytoskeletal connections during morphogenesis and highlights the power of natural selection to maintain protein structure.

Competing Interests: Competing interests The authors declare no competing or financial interests.

Titel:	The Dilute domain in Canoe is not essential for linking cell junctions to the cytoskeleton but supports morphogenesis robustness.
Autor/in / Beteiligte Person:	McParland, ED ; Butcher, TA ; Gurley, NJ ; Johnson, RI ; Slep, KC ; Peifer, M
Zeitschrift:	Journal of cell science, Jg. 137 (2024-03-15), Heft 6
Veröffentlichung:	Cambridge : Company of Biologists ; <i>Original Publication</i>: London., 2024
Medientyp:	academicJournal
ISSN:	1477-9137 (electronic)
DOI:	10.1242/jcs.261734
Schlagwort:	Animals Drosophila melanogaster genetics Drosophila melanogaster metabolism Cytoskeleton metabolism Intercellular Junctions metabolism Adherens Junctions metabolism Morphogenesis Cadherins metabolism Mammals metabolism Drosophila Proteins genetics Drosophila Proteins metabolism Myosin Type V metabolism
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article Language: English [J Cell Sci] 2024 Mar 15; Vol. 137 (6). <i>Date of Electronic Publication: </i>2024 Mar 21. MeSH Terms: Drosophila Proteins* / genetics ; Drosophila Proteins* / metabolism ; Myosin Type V* / metabolism ; Animals ; Drosophila melanogaster / genetics ; Drosophila melanogaster / metabolism ; Cytoskeleton / metabolism ; Intercellular Junctions / metabolism ; Adherens Junctions / metabolism ; Morphogenesis ; Cadherins / metabolism ; Mammals / metabolism Comments: Update of: bioRxiv. 2023 Oct 19;:. (PMID: 37905001) References: Mol Biol Cell. 2019 Jul 22;30(16):1938-1960. (PMID: 31188739) ; Dev Biol. 2021 Oct;478:173-182. (PMID: 34245727) ; Cell Tissue Res. 1999 Dec;298(3):397-404. (PMID: 10639730) ; Nat Commun. 2022 Aug 5;13(1):4562. (PMID: 35931706) ; Mol Biol Cell. 2023 Jan 1;34(1):ar7. (PMID: 36287827) ; Nat Commun. 2021 Sep 7;12(1):5315. (PMID: 34493720) ; J Cell Biol. 2021 Dec 6;220(12):. (PMID: 34762121) ; Adv Biol Regul. 2021 Jan;79:100787. (PMID: 33541831) ; Dev Cell. 2005 Apr;8(4):493-504. (PMID: 15809032) ; Sci Adv. 2022 Dec 9;8(49):eadd4187. (PMID: 36490350) ; J Biol Chem. 2013 Nov 22;288(47):34131-34145. (PMID: 24097982) ; Cold Spring Harb Perspect Biol. 2018 Aug 1;10(8):. (PMID: 28778874) ; Mol Biol Cell. 2013 Apr;24(7):945-63. (PMID: 23363604) ; Mol Biol Cell. 2011 Jun 15;22(12):2010-30. (PMID: 21508316) ; Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9064-9. (PMID: 10922060) ; Sci Adv. 2020 Nov 6;6(45):. (PMID: 33158857) ; Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11314-9. (PMID: 23798443) ; Proc Natl Acad Sci U S A. 2013 Dec 17;110(51):20443-8. (PMID: 24248336) ; J Vis Exp. 2019 Mar 15;(145):. (PMID: 30933080) ; PLoS One. 2023 Aug 3;18(8):e0289224. (PMID: 37535684) ; J Biol Chem. 2011 Dec 16;286(50):43537-48. (PMID: 22027834) ; J Biol Chem. 2016 Jun 24;291(26):13571-9. (PMID: 27129208) ; J Cell Biol. 2004 Oct 11;167(1):135-47. (PMID: 15479740) ; Nucleic Acids Res. 2022 Jul 5;50(W1):W276-W279. (PMID: 35412617) ; J Cell Biol. 1999 May 3;145(3):539-49. (PMID: 10225955) ; Elife. 2016 Sep 13;5:. (PMID: 27623148) ; J Cell Sci. 2018 Mar 26;131(6):. (PMID: 29507112) ; Genetics. 2003 Sep;165(1):159-69. (PMID: 14504224) ; Development. 2003 Nov;130(22):5413-23. (PMID: 14507782) ; Nat Cell Biol. 2015 Aug;17(8):955-63. (PMID: 26121555) ; Nature. 2021 Aug;596(7873):583-589. (PMID: 34265844) ; Wilehm Roux Arch Dev Biol. 1984 Sep;193(5):283-295. (PMID: 28305338) ; Nucleic Acids Res. 2022 Jan 7;50(D1):D439-D444. (PMID: 34791371) ; J Biol Chem. 2003 Feb 7;278(6):4103-11. (PMID: 12446711) ; Dev Cell. 2019 Aug 5;50(3):313-326.e5. (PMID: 31353315) ; Development. 2020 Sep 11;147(17):. (PMID: 32917667) ; Genes Cells. 2018 Mar;23(3):185-199. (PMID: 29431241) ; J Cell Biol. 2009 Jul 13;186(1):57-73. (PMID: 19596848) ; Science. 2020 Nov 27;370(6520):. (PMID: 33243859) ; PLoS One. 2009 Sep 15;4(9):e7008. (PMID: 19753121) ; J Cell Biol. 1997 Oct 20;139(2):517-28. (PMID: 9334353) ; Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3312-7. (PMID: 17360644) ; J Cell Biol. 2016 Apr 25;213(2):243-60. (PMID: 27114502) ; Development. 2018 Jan 26;145(2):. (PMID: 29361565) ; Mol Biol Cell. 2011 Jul 15;22(14):2491-508. (PMID: 21613546) ; Development. 1997 Jul;124(14):2671-80. (PMID: 9226438) Grant Information: R15 GM114729 United States GM NIGMS NIH HHS; R35 GM118096 United States GM NIGMS NIH HHS; NIH R35 GM118096 United States GM NIGMS NIH HHS; R15 GM114729 United States NH NIH HHS Contributed Indexing: Keywords: Drosophila; Adherens junction; Afadin; Cadherin; Canoe; Morphogenesis Substance Nomenclature: 0 (Drosophila Proteins) ; EC 3.6.1.- (Myosin Type V) ; 0 (Cadherins) Entry Date(s): Date Created: 20240207 Date Completed: 20240322 Latest Revision: 20240425 Update Code: 20240425 PubMed Central ID: PMC11006394

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The Dilute domain in Canoe is not essential for linking cell junctions to the cytoskeleton but supports morphogenesis robustness.