Home LiteratureArticle Details
PMID: 19297522 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Polarized growth in budding yeast in the absence of a localized formin.

Molecular biology of the cell ·Vol. 20 ·No. 10 ·2009-05-00 ·Pages 2540-8

Gao L, Bretscher A

Abstract

Polarity is achieved partly through the localized assembly of the cytoskeleton. During growth in budding yeast, the bud cortex and neck localized formins Bni1p and Bnr1p nucleate and assemble actin cables that extend along the bud-mother axis, providing tracks for secretory vesicle delivery. Localized formins are believed to determine the location and polarity of cables, hence growth. However, yeast expressing the nonlocalized actin nucleating/assembly formin homology (FH) 1-FH2 domains of Bnr1p or Bni1p as the sole formin grow well. Although cables are significantly disorganized, analysis of directed transport of secretory vesicles is still biased toward the bud, reflecting a bias in correctly oriented cables, thereby permitting polarized growth. Myosin II, localized at the bud neck, contributes to polarized growth as a mutant unable to interact with F-actin further compromises growth in cells with an unlocalized formin but not with a localized formin. Our results show that multiple mechanisms contribute to cable orientation and polarized growth, with localized formins and myosin II being two major contributors.

MeSH Terms
Actins/metabolism Cell Polarity Cytoskeletal Proteins/chemistry,metabolism Cytoskeleton/metabolism Microbial Viability Microfilament Proteins/chemistry,metabolism Myosin Heavy Chains/metabolism Myosin Type II/metabolism Myosin Type V/metabolism Peptide Fragments/metabolism Protein Structure, Tertiary Protein Transport Saccharomyces cerevisiae Proteins/chemistry,metabolism Saccharomycetales/cytology,growth & development Secretory Vesicles/metabolism
Chemicals
Actins BNR1 protein, S cerevisiae Bni1 protein, S cerevisiae Cytoskeletal Proteins MYO2 protein, S cerevisiae Microfilament Proteins Peptide Fragments Saccharomyces cerevisiae Proteins Myosin Type II Myosin Type V Myosin Heavy Chains
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gao Lina
Department of Molecular Biology and Genetics, Weill Institute for Cell and Molecular Biology, Weill Hall, Cornell University, Ithaca, NY 14853, USA.
Bretscher Anthony
References (38)
38 references, click to expand
  1. Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 May;9(5):1221-33 PMID: 9571251
  2. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast.
    Mol Biol Cell. 2004 Nov;15(11):4971-89 PMID: 15371545
  3. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6.
    J Biol Chem. 2005 Jul 29;280(30):28023-33 PMID: 15923184
  4. The ARP2/3 complex: an actin nucleator comes of age.
    Nat Rev Mol Cell Biol. 2006 Oct;7(10):713-26 PMID: 16990851
  5. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast.
    Nat Cell Biol. 2002 Jan;4(1):32-41 PMID: 11740490
  6. Actin cable dynamics in budding yeast.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):751-6 PMID: 11805329
  7. Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast.
    J Cell Biol. 2006 Dec 18;175(6):957-69 PMID: 17178912
  8. Polarization of cell growth in yeast.
    J Cell Sci. 2000 Feb;113 ( Pt 4):571-85 PMID: 10652251
  9. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  10. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast.
    J Cell Biol. 1998 Dec 28;143(7):1931-45 PMID: 9864365
  11. An actin nucleation mechanism mediated by Bni1 and profilin.
    Nat Cell Biol. 2002 Aug;4(8):626-31 PMID: 12134165
  12. Adaptation of core mechanisms to generate cell polarity.
    Nature. 2003 Apr 17;422(6933):766-74 PMID: 12700771
  13. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast.
    Mol Biol Cell. 2005 Nov;16(11):5346-55 PMID: 16148042
  14. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6181-6 PMID: 9600938
  15. Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae.
    Mol Biol Cell. 2000 Feb;11(2):593-611 PMID: 10679017
  16. Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables.
    Mol Biol Cell. 2007 May;18(5):1826-38 PMID: 17344480
  17. Pheromone-induced polarization is dependent on the Fus3p MAPK acting through the formin Bni1p.
    J Cell Biol. 2004 Apr;165(1):99-109 PMID: 15067022
  18. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae.
    J Cell Biol. 2004 Nov 8;167(3):519-30 PMID: 15534003
  19. Rho1 directs formin-mediated actin ring assembly during budding yeast cytokinesis.
    Curr Biol. 2002 Oct 29;12(21):1864-70 PMID: 12419188
  20. The yeast actin cytoskeleton: from cellular function to biochemical mechanism.
    Microbiol Mol Biol Rev. 2006 Sep;70(3):605-45 PMID: 16959963
  21. Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis.
    J Cell Biol. 1998 Jan 26;140(2):355-66 PMID: 9442111
  22. Harnessing actin dynamics for clathrin-mediated endocytosis.
    Nat Rev Mol Cell Biol. 2006 Jun;7(6):404-14 PMID: 16723976
  23. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis.
    J Cell Biol. 1998 Sep 7;142(5):1301-12 PMID: 9732290
  24. Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Oct 23;273(43):28341-5 PMID: 9774458
  25. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length.
    J Cell Biol. 2002 Jan 7;156(1):35-9 PMID: 11781333
  26. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae.
    J Cell Biol. 1984 Mar;98(3):934-45 PMID: 6365931
  27. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting.
    J Cell Biol. 1999 Nov 15;147(4):791-808 PMID: 10562281
  28. Role of formins in actin assembly: nucleation and barbed-end association.
    Science. 2002 Jul 26;297(5581):612-5 PMID: 12052901
  29. Yeast formins regulate cell polarity by controlling the assembly of actin cables.
    Nat Cell Biol. 2002 Jan;4(1):42-50 PMID: 11740491
  30. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  31. Two components of actin-based retrograde flow in sea urchin coelomocytes.
    Mol Biol Cell. 1999 Dec;10(12):4075-90 PMID: 10588644
  32. Mechanisms of polarized growth and organelle segregation in yeast.
    Annu Rev Cell Dev Biol. 2004;20:559-91 PMID: 15473852
  33. An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae.
    Oncogene. 1999 Nov 25;18(50):7046-54 PMID: 10597305
  34. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Feb;21(3):827-39 PMID: 11154270
  35. Retrograde flow and myosin II activity within the leading cell edge deliver F-actin to the lamella to seed the formation of graded polarity actomyosin II filament bundles in migrating fibroblasts.
    Mol Biol Cell. 2008 Nov;19(11):5006-18 PMID: 18799629
  36. Purification and characterization of the Saccharomyces cerevisiae BGL2 gene product, a cell wall endo-beta-1,3-glucanase.
    J Bacteriol. 1993 Apr;175(7):2102-6 PMID: 8458852
  37. Mechanism and function of formins in the control of actin assembly.
    Annu Rev Biochem. 2007;76:593-627 PMID: 17373907
  38. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches.
    J Cell Biol. 1998 Sep 21;142(6):1501-17 PMID: 9744880
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.e09-03-0194
Published
2009-05-00
Epub
2009-00-18
Pages
2540-8
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2682595
Subset
IM
Grants
NIGMS NIH HHS · R01 GM039066 · United States
NIGMS NIH HHS · GM39066 · United States
External Links
PubMed source DOI: 10.1091/mbc.e09-03-0194 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: product@genelibs.com

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