Filopodia-like Actin Cables Position Nuclei in Association with Perinuclear Actin in Drosophila Nurse Cells

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2013 Oct 5

PMID 24091012

Citations 42

Authors

Sven Huelsmann

Jari Ylanne

Nicholas H Brown

Affiliations

Soon will be listed here.

Abstract

Controlling the position of the nucleus is vital for a number of cellular processes from yeast to humans. In Drosophila nurse cells, nuclear positioning is crucial during dumping, when nurse cells contract and expel their contents into the oocyte. We provide evidence that in nurse cells, continuous filopodia-like actin cables, growing from the plasma membrane and extending to the nucleus, achieve nuclear positioning. These actin cables move nuclei away from ring canals. When nurse cells contract, actin cables associate laterally with the nuclei, in some cases inducing nuclear turning so that actin cables become partially wound around the nuclei. Our data suggest that a perinuclear actin meshwork connects actin cables to nuclei via actin-crosslinking proteins such as the filamin Cheerio. We provide a revised model for how actin structures position nuclei in nurse cells, employing evolutionary conserved machinery.

Citing Articles

Filamin protects myofibrils from contractile damage through changes in its mechanosensory region.

Fisher L, Carriqui-Madronal B, Mulder T, Huelsmann S, Schock F, Gonzalez-Morales N PLoS Genet. 2024; 20(6):e1011101.

PMID: 38905299 PMC: 11221683. DOI: 10.1371/journal.pgen.1011101.

Principles of organelle positioning in motile and non-motile cells.

Kroll J, Renkawitz J EMBO Rep. 2024; 25(5):2172-2187.

PMID: 38627564 PMC: 11094012. DOI: 10.1038/s44319-024-00135-4.

Basal actomyosin pulses expand epithelium coordinating cell flattening and tissue elongation.

Li S, Liu Z, Li H, Zhou S, Liu J, Sun N Nat Commun. 2024; 15(1):3000.

PMID: 38589403 PMC: 11001887. DOI: 10.1038/s41467-024-47236-1.

JAK-STAT-dependent contact between follicle cells and the oocyte controls Drosophila anterior-posterior polarity and germline development.

Mallart C, Netter S, Chalvet F, Claret S, Guichet A, Montagne J Nat Commun. 2024; 15(1):1627.

PMID: 38388656 PMC: 10883949. DOI: 10.1038/s41467-024-45963-z.

New mutant alleles for Spargel/dPGC-1 highlights the function of Spargel RRM domain in oogenesis and expands the role of Spargel in embryogenesis and intracellular transport.

Roy S, Nagarajan S, Jalal M, Basar M, Duttaroy A G3 (Bethesda). 2023; 13(9).

PMID: 37369430 PMC: 10468312. DOI: 10.1093/g3journal/jkad142.

References

Faix J, Breitsprecher D, Stradal T, Rottner K . Filopodia: Complex models for simple rods. Int J Biochem Cell Biol. 2009; 41(8-9):1656-64. DOI: 10.1016/j.biocel.2009.02.012. View

Wheatley S, Kulkarni S, Karess R . Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development. 1995; 121(6):1937-46. DOI: 10.1242/dev.121.6.1937. View

Burke B, Roux K . Nuclei take a position: managing nuclear location. Dev Cell. 2009; 17(5):587-97. DOI: 10.1016/j.devcel.2009.10.018. View

Oda H, Uemura T, Takeichi M . Phenotypic analysis of null mutants for DE-cadherin and Armadillo in Drosophila ovaries reveals distinct aspects of their functions in cell adhesion and cytoskeletal organization. Genes Cells. 1997; 2(1):29-40. DOI: 10.1046/j.1365-2443.1997.d01-284.x. View

Rodesch C, Pettus J, Nagoshi R . The Drosophila ovarian tumor gene is required for the organization of actin filaments during multiple stages in oogenesis. Dev Biol. 1997; 190(2):153-64. DOI: 10.1006/dbio.1997.8697. View

Roper K, Mao Y, Brown N . Contribution of sequence variation in Drosophila actins to their incorporation into actin-based structures in vivo. J Cell Sci. 2005; 118(Pt 17):3937-48. DOI: 10.1242/jcs.02517. View

Sokol N, Cooley L . Drosophila filamin encoded by the cheerio locus is a component of ovarian ring canals. Curr Biol. 1999; 9(21):1221-30. DOI: 10.1016/s0960-9822(99)80502-8. View

Riedl J, Crevenna A, Kessenbrock K, Yu J, Neukirchen D, Bista M . Lifeact: a versatile marker to visualize F-actin. Nat Methods. 2008; 5(7):605-7. PMC: 2814344. DOI: 10.1038/nmeth.1220. View

Cooley L . The villin-like protein encoded by the Drosophila quail gene is required for actin bundle assembly during oogenesis. Cell. 1994; 78(2):291-301. DOI: 10.1016/0092-8674(94)90298-4. View

10.

Lyulcheva E, Taylor E, Michael M, Vehlow A, Tan S, Fletcher A . Drosophila pico and its mammalian ortholog lamellipodin activate serum response factor and promote cell proliferation. Dev Cell. 2008; 15(5):680-90. PMC: 2691947. DOI: 10.1016/j.devcel.2008.09.020. View

11.

Manor U, Kachar B . Dynamic length regulation of sensory stereocilia. Semin Cell Dev Biol. 2008; 19(6):502-10. PMC: 2650238. DOI: 10.1016/j.semcdb.2008.07.006. View

12.

Riparbelli M, Gigliotti S, Callaini G . The Drosophila nucleoporin gene nup154 is required for correct microfilament dynamics and cell death during oogenesis. Cell Motil Cytoskeleton. 2007; 64(8):590-604. DOI: 10.1002/cm.20206. View

13.

Sokol N, Cooley L . Drosophila filamin is required for follicle cell motility during oogenesis. Dev Biol. 2003; 260(1):260-72. DOI: 10.1016/s0012-1606(03)00248-3. View

14.

Doherty J, Rossing M, Cushing-Haugen K, Chen C, Van Den Berg D, Wu A . ESR1/SYNE1 polymorphism and invasive epithelial ovarian cancer risk: an Ovarian Cancer Association Consortium study. Cancer Epidemiol Biomarkers Prev. 2010; 19(1):245-50. PMC: 2863004. DOI: 10.1158/1055-9965.EPI-09-0729. View

15.

Luxton G, Gomes E, Folker E, Vintinner E, Gundersen G . Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science. 2010; 329(5994):956-9. PMC: 3938394. DOI: 10.1126/science.1189072. View

16.

Haruta T, Warrior R, Yonemura S, Oda H . The proximal half of the Drosophila E-cadherin extracellular region is dispensable for many cadherin-dependent events but required for ventral furrow formation. Genes Cells. 2010; 15(3):193-208. DOI: 10.1111/j.1365-2443.2010.01389.x. View

17.

Kovacs E, Goodwin M, Ali R, Paterson A, Yap A . Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol. 2002; 12(5):379-82. DOI: 10.1016/s0960-9822(02)00661-9. View

18.

Gay O, Gilquin B, Nakamura F, Jenkins Z, McCartney R, Krakow D . RefilinB (FAM101B) targets filamin A to organize perinuclear actin networks and regulates nuclear shape. Proc Natl Acad Sci U S A. 2011; 108(28):11464-9. PMC: 3136255. DOI: 10.1073/pnas.1104211108. View

19.

Petrella L, Smith-Leiker T, Cooley L . The Ovhts polyprotein is cleaved to produce fusome and ring canal proteins required for Drosophila oogenesis. Development. 2007; 134(4):703-12. DOI: 10.1242/dev.02766. View

20.

Cant K, Cooley L . Single amino acid mutations in Drosophila fascin disrupt actin bundling function in vivo. Genetics. 1996; 143(1):249-58. PMC: 1207258. DOI: 10.1093/genetics/143.1.249. View