Home LiteratureArticle Details
PMID: 24798734 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Video-Audio Media

Plasma membrane phosphoinositide balance regulates cell shape during Drosophila embryo morphogenesis.

The Journal of cell biology ·Vol. 205 ·No. 3 ·2014-05-12 ·Pages 395-408

Reversi A, Loeser E, Subramanian D, Schultz C, De Renzis S

Abstract

Remodeling of cell shape during morphogenesis is driven by the coordinated expansion and contraction of specific plasma membrane domains. Loss of this coordination results in abnormal cell shape and embryonic lethality. Here, we show that plasma membrane lipid composition plays a key role in coordinating plasma membrane contraction during expansion. We found that an increase in PI(4,5)P2 levels caused premature actomyosin contraction, resulting in the formation of shortened cells. Conversely, acute depletion of PI(4,5)P2 blocked plasma membrane expansion and led to premature actomyosin disassembly. PI(4,5)P2-mediated contractility is counteracted by PI(3,4,5)P3 and the zygotic gene bottleneck, which acts by limiting myosin recruitment during plasma membrane expansion. Collectively, these data support a model in which the ratio of PI(4,5)P2/PI(3,4,5)P3 coordinates actomyosin contractility and plasma membrane expansion during tissue morphogenesis, thus ensuring proper cell shape.

MeSH Terms
Actomyosin/metabolism Animals Cell Membrane/metabolism Cell Shape Drosophila Proteins/genetics,metabolism Drosophila melanogaster/embryology,genetics,metabolism Embryo, Nonmammalian/metabolism HeLa Cells Humans Microfilament Proteins/genetics,metabolism Morphogenesis Myosin Type II/metabolism Phosphatidylinositol 4,5-Diphosphate/metabolism Phosphatidylinositols/metabolism RNA Interference Recombinant Fusion Proteins/metabolism Second Messenger Systems Transfection
Chemicals
Drosophila Proteins Microfilament Proteins Phosphatidylinositol 4,5-Diphosphate Phosphatidylinositols Recombinant Fusion Proteins bnk protein, Drosophila phosphoinositide-3,4,5-triphosphate Actomyosin Myosin Type II
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Reversi Alessandra
European Molecular Biology Laboratory (EMBL) Heidelberg, 69117 Heidelberg, Germany.
Loeser Eva
Subramanian Devaraj
Schultz Carsten
De Renzis Stefano
References (55)
55 references, click to expand
  1. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN.
    Cell. 1998 Oct 2;95(1):29-39 PMID: 9778245
  2. Challenges in studying phospholipid signaling.
    Nat Chem Biol. 2010 Jul;6(7):473-5 PMID: 20559309
  3. Prodrugs of biologically active phosphate esters.
    Bioorg Med Chem. 2003 Mar 20;11(6):885-98 PMID: 12614874
  4. The cytoskeleton and morphogenesis of the early Drosophila embryo.
    Curr Opin Cell Biol. 1995 Feb;7(1):18-22 PMID: 7755985
  5. Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells.
    Curr Biol. 2006 Jan 24;16(2):140-9 PMID: 16431366
  6. Mechanics of cytokinesis in eukaryotes.
    Curr Opin Cell Biol. 2010 Feb;22(1):50-6 PMID: 20031383
  7. Biomechanical regulation of contractility: spatial control and dynamics.
    Trends Cell Biol. 2012 Feb;22(2):61-81 PMID: 22119497
  8. Actin cytoskeleton. Through the bottleneck.
    Curr Biol. 1994 Jan 1;4(1):76-8 PMID: 7922320
  9. A local coupling model and compass parameter for eukaryotic chemotaxis.
    Dev Cell. 2005 Feb;8(2):215-27 PMID: 15691763
  10. Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila.
    Nat Commun. 2013;4:2244 PMID: 23921440
  11. Actin cortex mechanics and cellular morphogenesis.
    Trends Cell Biol. 2012 Oct;22(10):536-45 PMID: 22871642
  12. Forces driving epithelial spreading in zebrafish gastrulation.
    Science. 2012 Oct 12;338(6104):257-60 PMID: 23066079
  13. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster.
    Development. 1988 Nov;104(3):495-509 PMID: 3151484
  14. Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila.
    Development. 1990 Nov;110(3):851-63 PMID: 2088725
  15. src64 and tec29 are required for microfilament contraction during Drosophila cellularization.
    Development. 2004 Feb;131(4):863-71 PMID: 14736750
  16. The serendipity alpha gene encodes a membrane-associated protein required for the cellularization of the Drosophila embryo.
    Genes Dev. 1990 Jun;4(6):922-31 PMID: 2166703
  17. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels.
    Science. 2006 Dec 1;314(5804):1454-7 PMID: 16990515
  18. Modulation of membrane traffic by mechanical stimuli.
    Am J Physiol Renal Physiol. 2002 Feb;282(2):F179-90 PMID: 11788431
  19. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo.
    J Cell Biol. 2000 Aug 21;150(4):849-60 PMID: 10953008
  20. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42.
    Cell. 2007 Jan 26;128(2):383-97 PMID: 17254974
  21. bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo.
    Cell. 1993 Oct 22;75(2):373-85 PMID: 8402919
  22. Planar polarized actomyosin contractile flows control epithelial junction remodelling.
    Nature. 2010 Dec 23;468(7327):1110-4 PMID: 21068726
  23. Phosphoinositide signaling plays a key role in cytokinesis.
    J Cell Biol. 2006 Aug 14;174(4):485-90 PMID: 16908667
  24. Functional elements of the cytoskeleton in the early Drosophila embryo.
    Annu Rev Cell Biol. 1993;9:67-99 PMID: 8280474
  25. An Arf-GEF regulates antagonism between endocytosis and the cytoskeleton for Drosophila blastoderm development.
    Curr Biol. 2013 Nov 4;23(21):2110-20 PMID: 24120639
  26. Determinants of myosin II cortical localization during cytokinesis.
    Curr Biol. 2010 Jun 22;20(12):1080-5 PMID: 20541410
  27. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis.
    Curr Biol. 2003 Oct 28;13(21):1848-57 PMID: 14588240
  28. Pulsed contractions of an actin-myosin network drive apical constriction.
    Nature. 2009 Jan 22;457(7228):495-9 PMID: 19029882
  29. Phosphoinositides: tiny lipids with giant impact on cell regulation.
    Physiol Rev. 2013 Jul;93(3):1019-137 PMID: 23899561
  30. The molecular requirements for cytokinesis.
    Science. 2005 Mar 18;307(5716):1735-9 PMID: 15774750
  31. A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila.
    Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15050-5 PMID: 11742088
  32. Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells.
    J Cell Biol. 2006 Nov 6;175(3):377-82 PMID: 17088424
  33. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis.
    Nat Cell Biol. 2011 Aug 14;13(9):1124-31 PMID: 21841790
  34. A putative modular domain present in diverse signaling proteins.
    Cell. 1993 May 21;73(4):629-30 PMID: 8500161
  35. Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling.
    Development. 2005 Apr;132(7):1675-86 PMID: 15743877
  36. PIP3, PIP2, and cell movement--similar messages, different meanings?
    Dev Cell. 2001 Dec;1(6):743-7 PMID: 11740936
  37. Protein translocation as a tool: The current rapamycin story.
    FEBS Lett. 2012 Jul 16;586(15):2097-105 PMID: 22584056
  38. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis.
    Curr Biol. 2005 Aug 9;15(15):1407-12 PMID: 16085494
  39. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos.
    Mol Biol Cell. 2004 Feb;15(2):838-50 PMID: 14657248
  40. How actin gets the PIP.
    Sci Signal. 2012 Feb 28;5(213):pe7 PMID: 22375053
  41. Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization.
    Dev Cell. 2008 May;14(5):775-86 PMID: 18477459
  42. Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells.
    Nat Cell Biol. 2006 Sep;8(9):963-70 PMID: 16921364
  43. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization.
    J Cell Biol. 2000 Nov 13;151(4):905-18 PMID: 11076973
  44. Myosin II dynamics are regulated by tension in intercalating cells.
    Dev Cell. 2009 Nov;17(5):736-43 PMID: 19879198
  45. PIP2 hydrolysis and calcium release are required for cytokinesis in Drosophila spermatocytes.
    Curr Biol. 2005 Aug 9;15(15):1401-6 PMID: 16085493
  46. Lifeact: a versatile marker to visualize F-actin.
    Nat Methods. 2008 Jul;5(7):605-7 PMID: 18536722
  47. Apical domain polarization localizes actin-myosin activity to drive ratchet-like apical constriction.
    Nat Cell Biol. 2013 Aug;15(8):926-36 PMID: 23831726
  48. Developmental control of cell morphogenesis: a focus on membrane growth.
    Nat Cell Biol. 2003 Feb;5(2):103-8 PMID: 12563275
  49. Phosphoinositides specify polarity during epithelial organ development.
    Cell. 2007 Jan 26;128(2):239-40 PMID: 17254962
  50. Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos.
    Development. 1988 Nov;104(3):483-93 PMID: 3256473
  51. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers.
    Mol Cell Biol. 1999 Oct;19(10):6845-57 PMID: 10490623
  52. PIP(2) and proteins: interactions, organization, and information flow.
    Annu Rev Biophys Biomol Struct. 2002;31:151-75 PMID: 11988466
  53. Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading.
    Proc Natl Acad Sci U S A. 2011 Aug 30;108(35):14467-72 PMID: 21808040
  54. Membrane-permeant phosphoinositide derivatives as modulators of growth factor signaling and neurite outgrowth.
    Chem Biol. 2009 Nov 25;16(11):1190-6 PMID: 19942142
  55. The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization.
    Dev Cell. 2013 Dec 23;27(6):648-55 PMID: 24316147
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
DOI
10.1083/jcb.201309079
Published
2014-05-12
Epub
2014-00-05
Pages
395-408
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC4018783
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.201309079 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2