Home LiteratureArticle Details
PMID: 18791237 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A novel septin-associated protein, Syp1p, is required for normal cell cycle-dependent septin cytoskeleton dynamics in yeast.

Genetics ·Vol. 180 ·No. 3 ·2008-11-00 ·Pages 1445-57

Qiu W, Neo SP, Yu X, Cai M

Abstract

Septins are a family of GTP-binding proteins whose heterooligomeric complex is the basic structural element of the septin filaments found in many eukaryotic organisms. In budding yeast, septins are mainly confined at the mother-daughter junction and are required for cell morphogenesis and division. Septins undergo assembly and disassembly in accordance with the progression of the cell cycle. In this report, we identified the yeast protein Syp1p as a new regulator of septin dynamics. Syp1p colocalizes with septins throughout most of the cell cycle. Syp1p interacts with the septin subunit Cdc10p and can be precipitated by Cdc10p and Cdc12p. In the syp1Delta mutant, both formation of a complete septin ring at the incipient bud site and disassembly of the septin ring in later stages of cell division are significantly delayed. In addition, overexpression of Syp1p causes marked acceleration of septin disassembly. The fluorescence recovery after photobleaching (FRAP) assay further showed that Syp1p promotes septin turnover in different cell cycle stages. These results suggest that Syp1p is involved in the regulation of cell cycle-dependent dynamics of the septin cytoskeleton in yeast.

MeSH Terms
Cell Cycle/physiology Cell Cycle Proteins/genetics,metabolism Cell Division Cellular Structures Cytoskeletal Proteins/genetics,metabolism Cytoskeleton/physiology Fluorescence Recovery After Photobleaching GTP Phosphohydrolases/genetics,metabolism Gene Expression Regulation, Fungal Green Fluorescent Proteins/metabolism Membrane Proteins/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Schizosaccharomyces/genetics Two-Hybrid System Techniques
Chemicals
CDC12 protein, S cerevisiae Cell Cycle Proteins Cytoskeletal Proteins Membrane Proteins Saccharomyces cerevisiae Proteins Green Fluorescent Proteins CDC10 protein, S cerevisiae GTP Phosphohydrolases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Qiu Wenjie
Institute of Molecular and Cell Biology, Singapore 138673, Republic of Singapore.
Neo Suat Peng
Yu Xianwen
Cai Mingjie
References (41)
41 references, click to expand
  1. Molecular genetic analysis of Rts1p, a B' regulatory subunit of Saccharomyces cerevisiae protein phosphatase 2A.
    Mol Cell Biol. 1997 Jun;17(6):3242-53 PMID: 9154823
  2. Septins: cytoskeletal polymers or signalling GTPases?
    Trends Cell Biol. 1999 Oct;9(10):387-94 PMID: 10481176
  3. Some assembly required: yeast septins provide the instruction manual.
    Trends Cell Biol. 2005 Aug;15(8):414-24 PMID: 16009555
  4. Regulation of yeast actin cytoskeleton-regulatory complex Pan1p/Sla1p/End3p by serine/threonine kinase Prk1p.
    Mol Biol Cell. 2001 Dec;12(12):3759-72 PMID: 11739778
  5. The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis.
    J Cell Sci. 2001 Apr;114(Pt 7):1379-86 PMID: 11257003
  6. 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
  7. Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p.
    J Cell Biol. 2002 Jan 21;156(2):315-26 PMID: 11807094
  8. A Bni4-Glc7 phosphatase complex that recruits chitin synthase to the site of bud emergence.
    Mol Biol Cell. 2003 Jan;14(1):26-39 PMID: 12529424
  9. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function.
    J Cell Biol. 1998 Nov 2;143(3):719-36 PMID: 9813093
  10. Spatial coordination of cytokinetic events by compartmentalization of the cell cortex.
    Science. 2004 Jul 16;305(5682):393-6 PMID: 15256669
  11. Cell cycle control of septin ring dynamics in the budding yeast.
    Microbiology (Reading). 2001 Jun;147(Pt 6):1437-1450 PMID: 11390675
  12. Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution.
    J Cell Biol. 1998 Dec 28;143(7):1947-60 PMID: 9864366
  13. Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4.
    J Cell Biol. 2004 Mar 1;164(5):701-15 PMID: 14993234
  14. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1857-70 PMID: 8657162
  15. Structural insight into filament formation by mammalian septins.
    Nature. 2007 Sep 20;449(7160):311-5 PMID: 17637674
  16. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis.
    Exp Cell Res. 1971 Dec;69(2):265-76 PMID: 4950437
  17. Functional analysis of the interaction between Afr1p and the Cdc12p septin, two proteins involved in pheromone-induced morphogenesis.
    Mol Biol Cell. 1997 Jun;8(6):987-98 PMID: 9201710
  18. Components required for cytokinesis are important for bud site selection in yeast.
    J Cell Biol. 1993 Jul;122(2):373-86 PMID: 8320260
  19. Localization of Saccharomyces cerevisiae protein phosphatase 2A subunits throughout mitotic cell cycle.
    Mol Biol Cell. 2002 Oct;13(10):3477-92 PMID: 12388751
  20. Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth.
    J Cell Biol. 2005 Jun 20;169(6):897-908 PMID: 15967812
  21. Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae.
    Mol Biol Cell. 2004 Dec;15(12):5329-45 PMID: 15371547
  22. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae.
    Mol Cell Biol. 2000 Jun;20(11):4049-61 PMID: 10805747
  23. Chemical genetic analysis of the budding-yeast p21-activated kinase Cla4p.
    Nat Cell Biol. 2000 Oct;2(10):677-85 PMID: 11025657
  24. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier.
    Science. 2000 Oct 13;290(5490):341-4 PMID: 11030653
  25. Suppression of the profilin-deficient phenotype by the RHO2 signaling pathway in Saccharomyces cerevisiae.
    Genetics. 2000 Oct;156(2):579-92 PMID: 11014808
  26. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast.
    Genes Dev. 1999 Jan 15;13(2):176-87 PMID: 9925642
  27. Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae.
    Mol Biol Cell. 2004 Oct;15(10):4568-83 PMID: 15282341
  28. Cytokinesis in budding yeast: the relationship between actomyosin ring function and septum formation.
    Cell Struct Funct. 2001 Dec;26(6):529-37 PMID: 11942606
  29. Structural insights into yeast septin organization from polarized fluorescence microscopy.
    Nature. 2006 Sep 28;443(7110):466-9 PMID: 17006515
  30. The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast.
    Mol Biol Cell. 2003 Oct;14(10):4051-66 PMID: 14517318
  31. Phosphorylation-dependent regulation of septin dynamics during the cell cycle.
    Dev Cell. 2003 Mar;4(3):345-57 PMID: 12636916
  32. The Saccharomyces cerevisiae Arf3 protein is involved in actin cable and cortical patch formation.
    FEMS Yeast Res. 2007 Sep;7(6):782-95 PMID: 17425670
  33. The phosphotyrosyl phosphatase activator, Ncs1p (Rrd1p), functions with Cla4p to regulate the G(2)/M transition in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Jan;21(2):488-500 PMID: 11134337
  34. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall.
    J Cell Biol. 1997 Oct 6;139(1):75-93 PMID: 9314530
  35. The septins: roles in cytokinesis and other processes.
    Curr Opin Cell Biol. 1996 Feb;8(1):106-19 PMID: 8791410
  36. The morphogenesis checkpoint: how yeast cells watch their figures.
    Curr Opin Cell Biol. 2003 Dec;15(6):648-53 PMID: 14644188
  37. Here come the septins: novel polymers that coordinate intracellular functions and organization.
    J Cell Sci. 2006 Jan 1;119(Pt 1):4-10 PMID: 16371649
  38. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast.
    Mol Cell. 2000 May;5(5):841-51 PMID: 10882120
  39. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast.
    Genes Dev. 1995 Aug 1;9(15):1817-30 PMID: 7649470
  40. Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site.
    Mol Biol Cell. 2006 Mar;17(3):1110-25 PMID: 16371506
  41. Phosphorylation of the septin cdc3 in g1 by the cdc28 kinase is essential for efficient septin ring disassembly.
    Cell Cycle. 2002 Jan;1(1):42-9 PMID: 12429908
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2008-11-00
Epub
2008-00-14
Pages
1445-57
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC2581947
Subset
IM
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]