Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis
K.A. Edwards, D.P. Kiehart
Development 1996 122: 1499-1511;
K.A. Edwards
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
D.P. Kiehart
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

Morphogenesis is characterized by orchestrated changes in the shape and position of individual cells. Many of these movements are thought to be powered by motor proteins. However, in metazoans, it is often difficult to match specific motors with the movements they drive. The nonmuscle myosin II heavy chain (MHC encoded by zipper is required for cell sheet movements in Drosophila embryos. To determine if myosin II is required for other processes, we examined the phenotypes of strong and weak larval lethal mutations in spaghetti squash (sqh), which encodes the nonmuscle myosin II regulatory light chain (RLC). sqh mutants can be rescued to adulthood by daily induction of a sqh cDNA transgene driven by the hsp70 promoter. By transiently ceasing induction of the cDNA, we depleted RLC at specific times during development. When RLC is transiently depleted in larvae, the resulting adult phenotypes demonstrate that RLC is required in a stage-specific fashion for proper development of eye and leg imaginal discs. When RLC is depleted in adult females, oogenesis is reversibly disrupted. Without RLC induction, developing egg chambers display a succession of phenotypes that demonstrate roles for myosin II in morphogenesis of the interfollicular stalks, three morphologically and mechanistically distinct types of follicle cell migration, and completion of nurse cell cytoplasm transport (dumping). Finally, we show that in sqh mutant tissues, MHC is abnormally localized in punctate structures that do not contain appreciable amounts of filamentous actin or the myosin tail-binding protein p127. This suggests that sqh mutant phenotypes are chiefly caused by sequestration of myosin into inactive aggregates. These results show that myosin II is responsible for a surprisingly diverse array of cell shape changes throughout development.

Reference

    1. Bement W. M.,
    2. Forscher P.,
    3. Mooseker M. S.
    (1993) A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol 121, 565–578
    OpenUrlAbstract/FREE Full Text
    1. Chen P.,
    2. Ostrow B. D.,
    3. Tafuri S. R.,
    4. Chisholm R. L.
    (1994) Targeted disruption of the Dictyostelium RMLC gene produces cells defective in cytokinesis and development. J. Cell Biol 127, 1933–1944
    OpenUrlAbstract/FREE Full Text
    1. Cheney R. E.,
    2. Riley M. A.,
    3. Mooseker M. S.
    (1993) Phylogenetic analysis of the myosin superfamily. Cell Motility and the Cytoskeleton 24, 215–233
    OpenUrlCrossRefPubMedWeb of Science
    1. Condic M. L.,
    2. Fristrom D.,
    3. Fristrom J. W.
    (1991) Apical cell shape changes during Drosophila imaginal leg disc elongation: a novel morphogenetic mechanism. Development 111, 23–33
    OpenUrlAbstract
    1. DeLozanne A.,
    2. Spudich J.
    (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236, 1086–1091
    OpenUrlAbstract/FREE Full Text
    1. Doolittle K. W.,
    2. Reddy I.,
    3. McNally J. G.
    (1995) 3D analysis of cell movement during normal and myosin-II-null cell morphogenesis in Dictyostelium. Dev. Biol 167, 118–129
    OpenUrlCrossRefPubMedWeb of Science
    1. Gatti M.,
    2. Baker B. S.
    (1989) Genes controlling essential cell-cycle functions in Drosophila melanogaster. Genes Dev 3, 438–453
    OpenUrlAbstract/FREE Full Text
    1. Hall A.
    (1994) Small GTP-Binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol 10, 31–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Harden N.,
    2. Loh H. Y.,
    3. Chia W.,
    4. Lim L.
    (1995) A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila. Development 121, 903–914
    OpenUrlAbstract
    1. Harrington W. F.,
    2. Rodgers M. E.
    (1984) Myosin. Annu. Rev Biochem 53, 35–73
    OpenUrlCrossRefPubMedWeb of Science
    1. Karess R. E.,
    2. Chang X.-j.,
    3. Edwards K. A.,
    4. Kulkarni S.,
    5. Aguilera I.,
    6. Kiehart D. P.
    (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177–1189
    OpenUrlCrossRefPubMedWeb of Science
    1. Ketchum A. S.,
    2. Stewart C. T.,
    3. Stewart M.,
    4. Kiehart D. P.
    (1990) Complete sequence of the Drosophila nonmuscle myosin heavy chain transcript: Conserved sequences in the myosin tail and differential splicing in the 5untranslated sequence. Proc. Natl. Acad. Sci. USA 87, 6316–6320
    OpenUrlAbstract/FREE Full Text
    1. Kiehart D. P.,
    2. Feghali R.
    (1986) Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol 103, 1517–1525
    OpenUrlAbstract/FREE Full Text
    1. Kiehart D. P.,
    2. Lutz M. S.,
    3. Chan D.,
    4. Ketchum A. S.,
    5. Laymon R. A.,
    6. Nguyen B.,
    7. Goldstein L. S. B.
    (1989) Identification of the gene for fly non-muscle myosin heavy chain: Drosophila myosin heavy chains are encoded by a gene family. EMBO J 8, 913–922
    OpenUrlPubMedWeb of Science
    1. Leptin M.,
    2. Casal J.,
    3. Grunewald B.,
    4. Reuter R.
    (1992) Mechanisms of early Drosophila mesoderm formation. In Gastrulation (ed. C. Stern and P. Ingham). Development 1992, 23–31
    1. Lin H.,
    2. Yue L.,
    3. Spradling A. C.
    (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947–956
    OpenUrlAbstract
    1. Lin H.,
    2. Spradling A. C.
    (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet 16, 6–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Lundell M. J.,
    2. Hirsh J.
    (1994) A new visible light DNA fluorochrome for confocal microscopy. Biotechniques 16, 434–440
    OpenUrlPubMed
    1. Mabuchi I.,
    2. Okuno M.
    (1977) The effect of myosin antibody on the division of starfish blastomeres. JCell Biol 74, 251–263
    OpenUrlAbstract/FREE Full Text
    1. Mahajan-Miklos S.,
    2. Cooley L.
    (1994) Intercellular cytoplasm transport during Drosophila oogenesis. Dev. Biol 165, 336–351
    OpenUrlCrossRefPubMedWeb of Science
    1. Mansfield S. G.,
    2. Al-Shirawi D. Y.,
    3. Ketchum A. S.,
    4. Newbern E. C.,
    5. Kiehart D. P.
    (1996) Molecular organization and alternative splicing in zipper, the gene that encodes the Drosophila nonmuscle myosin II heavy chain. J. Mol. Biol 255, 98–109
    OpenUrlCrossRefPubMedWeb of Science
    1. Martin P.,
    2. Dickson M. C.,
    3. Millan F. A.,
    4. Akhurst R. J.
    (1993) Rapid induction and clearance of TGF1 is an early response to wounding in the mouse embryo. Dev Genet 14, 225–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Montell D. J.,
    2. Rorth P.,
    3. Spradling A. C.
    (1992) slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71, 51–62
    OpenUrlCrossRefPubMedWeb of Science
    1. Morgan N. S.,
    2. Skovronsky D. M.,
    3. Artavanis-Tsakonas S.,
    4. Mooseker M. S.
    (1994) The molecular cloning and characterization of Drosophila melanogaster Myosin-IA and Myosin-IB. J. Mol. Biol 239, 347–356
    OpenUrlCrossRefPubMedWeb of Science
    1. Pesacreta T. C.,
    2. Byers T. J.,
    3. Dubreuil R.,
    4. Kiehart D. P.,
    5. Branton D.
    (1989) Drosophila spectrin: the membrane skeleton during embryogenesis. J. Cell Biol 108, 1697–1709
    OpenUrlAbstract/FREE Full Text
    1. Rayment I.,
    2. Rypniewski W. R.,
    3. Schmidt-Base K.,
    4. Smith R.,
    5. Tomchick D. R.,
    6. Benning M. M.,
    7. Winkelmann D. A.,
    8. Wesenberg G.,
    9. Holden H. M.
    (1993) Three-dimensional structure of myosin subfragment-1: A molecular motor. Science 261, 50–58
    OpenUrlAbstract/FREE Full Text
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P-element transposase in Drosophilamelanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Springer M. L.,
    2. Patterson B.,
    3. Spudich J. A.
    (1994) Stage-specific requirement for myosin II during Dictyostelium development. Development 120, 2651–2660
    OpenUrlAbstract/FREE Full Text
    1. Strand D.,
    2. Raska I.,
    3. Mechler B. M.
    (1994) The Drosophila lethal(2)giant larvae tumor suppressor protein is a component of the cytoskeleton. J. Cell Biol 127, 1345–1360
    OpenUrlAbstract/FREE Full Text
    1. Strand D.,
    2. Jakobs R.,
    3. Merdes G.,
    4. Neumann B.,
    5. Kalmes A.,
    6. Heid H. W.,
    7. Husmann I.,
    8. Mechler B. M.
    (1994) The Drosophila lethal(2)giant larvae tumor suppressor forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol 127, 1361–1373
    OpenUrlAbstract/FREE Full Text
    1. Thummel C. S.,
    2. Pirotta V.
    (1992) New pCaSpeR P element vectors. Dros. Inf. Serv 71, 150–.
    OpenUrl
    1. Trybus K. M.,
    2. Waller G. S.,
    3. Chatman T. A.
    (1994) Coupling of ATPase activity and motility in smooth muscle myosin is mediated by the regulatory light chain. J. Cell Biol 124, 963–969
    OpenUrlAbstract/FREE Full Text
    1. Twombly V.,
    2. Blackman R. K.,
    3. Jin H.,
    4. Graff J.M.,
    5. Padgett R.W.,
    6. Gelbart W.M.
    (1996) The TGF-signaling pathway is essential for Drosophila oogenesis. Development 122, 1555–1565
    OpenUrlAbstract
    1. Uyeda T. Q. P.,
    2. Spudich J. A.
    (1993) A functional recombinant myosin II lacking a regulatory light chain-binding site. Science 262, 1867–1870
    OpenUrlAbstract/FREE Full Text
    1. von Kalm L.,
    2. Fristrom D.,
    3. Fristrom J.
    (1995) The making of a fly leg: a model for epithelial morphogenesis. BioEssays 17, 693–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Warrick H. M.,
    2. Spudich J. A.
    (1987) Myosin structure and function in cell motility. Annu. Rev. Cell Biol 3, 379–421
    OpenUrlCrossRefWeb of Science
    1. Wheatley S.,
    2. Kulkarni S.,
    3. Karess R.
    (1995) Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937–1946
    OpenUrlAbstract
    1. Xie X.,
    2. Harrison D. H.,
    3. Schlichting I.,
    4. Sweet R. M.,
    5. Kalabokis V. N.,
    6. Szent-Gyorgyi A. G.,
    7. Cohen C.
    (1994). Structure of the regulatory domain of scallop myosin at 2.8 angstrom resolution. Nature 368, 306–312
    OpenUrlCrossRefPubMed
    1. Young P. E.,
    2. Pesacreta T. C.,
    3. Kiehart D. P.
    (1991) Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 111, 1–14
    OpenUrlAbstract
    1. Young P. E.,
    2. Richman A. M.,
    3. Ketchum A. S.,
    4. Kiehart D. P.
    (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7, 29–41
    OpenUrlAbstract/FREE Full Text
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
Share
JOURNAL ARTICLES
Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis
K.A. Edwards, D.P. Kiehart
Development 1996 122: 1499-1511;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis
K.A. Edwards, D.P. Kiehart
Development 1996 122: 1499-1511;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Non-imprinted Igf2r expression decreases growth and rescues the Tme mutation in mice
  • The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium
  • REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.


Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?


Primer – Principles and applications of optogenetics in developmental biology

Schematic demonstrating the approaches to controlling protein activity using optogenetics.

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.


preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.


Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.


Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2019   The Company of Biologists Ltd   Registered Charity 277992