Two distinct myosin II populations coordinate ovulatory contraction of the myoepithelial sheath in the<i>Caenorhabditis elegans</i>somatic gonad

Ono, Kanako; Ono, Shoichiro

doi:10.1091/mbc.e15-09-0648

Cited by 22 publications

(56 citation statements)

References 60 publications

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“…Defects in a host of other cytoskeletal components do lead to ovulation defects similar to the formin mutants (failed entry and broken oocytes), including mutation or knock-down of genes encoding tropomyosin (lev-11), members of the troponin complex (TnC pat-10, TnT mup-2, TnI tni-1, unc-27/tni-2), paramyosin (unc-15), muscle myosin heavy chains (myo-3, unc-54), nonmuscle myosin heavy and light chains (nmy-2 and mlc-4), b-integrin (pat-3), vinculin (deb-1), and AIP1 (unc-78, aipl-1) [Myers et al, 1996;Ono and Ono, 2004;Ono et al, 2007;Obinata et al, 2010;Ono and Ono, 2014;Ono and Ono, 2016]. However, these have all been implicated in regulating the contractions of the myoepithelial sheath cells, rather than defects of spermatheca function.…”

Section: Discussionmentioning

confidence: 99%

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

et al. 2016

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Formins are regulators of actin filament dynamics. We demonstrate here that two formins, FHOD-1 and EXC-6, are important in the nematode Caenorhabditis elegans for ovulation, during which actomyosin contractions push a maturing oocyte from the gonad arm into a distensible bag-like organ, the spermatheca. EXC-6, a homolog of the disease-associated mammalian formin INF2, is highly expressed in the spermatheca, where it localizes to cell-cell junctions and to circumferential actin filament bundles. Loss of EXC-6 does not noticeably affect the organization the actin filament bundles, and causes only a very modest increase in the population of junction-associated actin filaments. Despite absence of a strong cytoskeletal phenotype, approximately half of ovulations in exc-6 mutants exhibit extreme defects, including failure of the oocyte to enter the spermatheca, or breakage of the oocyte as the distal spermatheca entrance constricts during ovulation. Loss of FHOD-1 alone has little effect, and we cannot detect FHOD-1 in the spermatheca. However, combined loss of these formins in double fhod-1;exc-6 mutants results in profound ovulation defects, with significant slowing of the entry of oocytes into the spermatheca, and failure of nearly 80% of ovulations. We suggest that EXC-6 plays a role directly in the spermatheca, perhaps by modulating the ability of the spermatheca wall to rapidly accommodate an incoming oocyte, while FHOD-1 may play an indirect role relating to its known importance in the growth and function of the egg-laying muscles.

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Section: Discussionmentioning

confidence: 99%

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

et al. 2016

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“…Defects in a host of other cytoskeletal components do lead to ovulation defects similar to the formin mutants (failed entry and broken oocytes), including mutation or knock‐down of genes encoding tropomyosin ( lev‐11 ), members of the troponin complex (TnC pat‐10 , TnT mup‐2 , TnI tni‐1 , unc‐27/tni‐2 ), paramyosin ( unc‐15 ), muscle myosin heavy chains ( myo‐3 , unc‐54 ), nonmuscle myosin heavy and light chains ( nmy‐2 and mlc‐4 ), β‐integrin ( pat‐3 ), vinculin ( deb‐1 ), and AIP1 ( unc‐78 , aipl‐1 ) [Myers et al, ; Ono and Ono, ; Ono et al, ; Obinata et al, ; Ono and Ono, ; Ono and Ono, ]. However, these have all been implicated in regulating the contractions of the myoepithelial sheath cells, rather than defects of spermatheca function.…”

Section: Discussionmentioning

confidence: 99%

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

et al. 2016

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Formins are regulators of actin filament dynamics. We demonstrate here that two formins, FHOD‐1 and EXC‐6, are important in the nematode Caenorhabditis elegans for ovulation, during which actomyosin contractions push a maturing oocyte from the gonad arm into a distensible bag‐like organ, the spermatheca. EXC‐6, a homolog of the disease‐associated mammalian formin INF2, is highly expressed in the spermatheca, where it localizes to cell‐cell junctions and to circumferential actin filament bundles. Loss of EXC‐6 does not noticeably affect the organization the actin filament bundles, and causes only a very modest increase in the population of junction‐associated actin filaments. Despite absence of a strong cytoskeletal phenotype, approximately half of ovulations in exc‐6 mutants exhibit extreme defects, including failure of the oocyte to enter the spermatheca, or breakage of the oocyte as the distal spermatheca entrance constricts during ovulation. Loss of FHOD‐1 alone has little effect, and we cannot detect FHOD‐1 in the spermatheca. However, combined loss of these formins in double fhod‐1;exc‐6 mutants results in profound ovulation defects, with significant slowing of the entry of oocytes into the spermatheca, and failure of nearly 80% of ovulations. We suggest that EXC‐6 plays a role directly in the spermatheca, perhaps by modulating the ability of the spermatheca wall to rapidly accommodate an incoming oocyte, while FHOD‐1 may play an indirect role relating to its known importance in the growth and function of the egg‐laying muscles. © 2016 The Authors. Cytoskeleton Published by Wiley Periodicals, Inc.

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“…Since GFP::NMY-1 labels only the heavy chain of myosin (Piekny, Johnson, Cham, & Mains, 2003;Wirshing & Cram, 2017), we asked if these myosin foci were functional nonmuscle myosin hexamers (Conti & Adelstein, 2008). We used labeled myosin regulatory light chain (MRLC), GFP::MLC-4 (Kelley et al, 2018;K. Ono & Ono, 2016;Shelton, Carter, Ellis, & Bowerman, 1999), and stained F-actin with phalloidin to show that the MRLC is also associated with the nucleus in fln-1 animals, but not in wild type animals ( Figure 3D).…”

Section: Myosin Forms Perinuclear Foci In Fln-1 Animalsmentioning

confidence: 99%

“…(Wirshing & Cram, 2017). UN1953 was generating by crossing UN0810 fln-1(tm545) (Kovacevic & Cram, 2010) with EU573 orEx2 [mlc-4p::mlc-4::GFP::unc-54 3'UTR + rol-6(su1006)] (K. Ono & Ono, 2016). WBM875 [Y38F2AR.9(wbm3[eGFP::Sec61b])IV] was a gift from the Mair lab and used to label the endoplasmic reticulum.…”

Section: Nematode Maintenance and Strain Generationmentioning

confidence: 99%

FLN-1/Filamin is required to anchor the actomyosin cytoskeleton and for global organization of sub-cellular organelles in a contractile tissue

Kelley

Triplett

Mallick

et al. 2020

Preprint

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AbstractActomyosin networks are organized in space, direction, size, and connectivity to produce coordinated contractions across cells. We use the C. elegans spermatheca, a tube composed of contractile myoepithelial cells, to study how actomyosin structures are organized. FLN-1/filamin is required for the formation and stabilization of a regular array of parallel, contractile, actomyosin fibers in this tissue. Loss of fln-1 results in the detachment of actin fibers from the basal surface, which then accumulate along the cell junctions and are stabilized by spectrin. In addition, actin and myosin are captured at the nucleus by the linker of nucleoskeleton and cytoskeleton complex (LINC) complex, where they form large foci. Nuclear positioning and morphology, distribution of the endoplasmic reticulum and the mitochondrial network are also disrupted. These results demonstrate that filamin is required to prevent large actin bundle formation and detachment, to prevent excess nuclear localization of actin and myosin, and to ensure correct positioning of organelles.

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Two distinct myosin II populations coordinate ovulatory contraction of the myoepithelial sheath in theCaenorhabditis eleganssomatic gonad

Cited by 22 publications

References 60 publications

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

INF2‐ and FHOD‐related formins promote ovulation in the somatic gonad of C. elegans

FLN-1/Filamin is required to anchor the actomyosin cytoskeleton and for global organization of sub-cellular organelles in a contractile tissue

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