Home LiteratureArticle Details
PMID: 26179915 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Rho1- and Pkc1-dependent phosphorylation of the F-BAR protein Syp1 contributes to septin ring assembly.

Molecular biology of the cell ·Vol. 26 ·No. 18 ·2015-09-15 ·Pages 3245-62

Merlini L, Bolognesi A, Juanes MA, Vandermoere F, Courtellemont T, Pascolutti R, Séveno M, Barral Y, Piatti S

Abstract

In many cell types, septins assemble into filaments and rings at the neck of cellular appendages and/or at the cleavage furrow to help compartmentalize the plasma membrane and support cytokinesis. How septin ring assembly is coordinated with membrane remodeling and controlled by mechanical stress at these sites is unclear. Through a genetic screen, we uncovered an unanticipated link between the conserved Rho1 GTPase and its effector protein kinase C (Pkc1) with septin ring stability in yeast. Both Rho1 and Pkc1 stabilize the septin ring, at least partly through phosphorylation of the membrane-associated F-BAR protein Syp1, which colocalizes asymmetrically with the septin ring at the bud neck. Syp1 is displaced from the bud neck upon Pkc1-dependent phosphorylation at two serines, thereby affecting the rigidity of the new-forming septin ring. We propose that Rho1 and Pkc1 coordinate septin ring assembly with membrane and cell wall remodeling partly by controlling Syp1 residence at the bud neck.

MeSH Terms
Carrier Proteins/genetics,metabolism Cytokinesis/physiology Cytoskeleton/metabolism Gene Expression Regulation, Fungal Phosphorylation Protein Kinase C/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Septins/genetics,metabolism Signal Transduction rho GTP-Binding Proteins/genetics,metabolism
Chemicals
Carrier Proteins Saccharomyces cerevisiae Proteins Syp1 protein, S cerevisiae PKC1 protein, S cerevisiae Protein Kinase C Septins RHO1 protein, S cerevisiae rho GTP-Binding Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Merlini Laura
Centre de Recherche en Biochimie Macromoléculaire, 34293 Montpellier, France.
Bolognesi Alessio
Institute of Biochemistry, ETH Zurich, 8093 Zurich, Switzerland.
Juanes Maria Angeles
Centre de Recherche en Biochimie Macromoléculaire, 34293 Montpellier, France.
Vandermoere Franck
Functional Proteomic Platform, Institut de Génomique Fonctionnelle, 34094 Montpellier, France.
Courtellemont Thibault
Centre de Recherche en Biochimie Macromoléculaire, 34293 Montpellier, France.
Pascolutti Roberta
Centre de Recherche en Biochimie Macromoléculaire, 34293 Montpellier, France.
Séveno Martial
Functional Proteomic Platform, Institut de Génomique Fonctionnelle, 34094 Montpellier, France.
Barral Yves
Institute of Biochemistry, ETH Zurich, 8093 Zurich, Switzerland.
Piatti Simonetta
Centre de Recherche en Biochimie Macromoléculaire, 34293 Montpellier, France [email protected].
References (129)
129 references, click to expand
  1. Early-arriving Syp1p and Ede1p function in endocytic site placement and formation in budding yeast.
    Mol Biol Cell. 2009 Nov;20(22):4640-51 PMID: 19776351
  2. Phosphorylation-dependent regulation of septin dynamics during the cell cycle.
    Dev Cell. 2003 Mar;4(3):345-57 PMID: 12636916
  3. Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function.
    Mol Cell Biol. 2003 Apr;23(8):2762-77 PMID: 12665577
  4. Mid2p stabilizes septin rings during cytokinesis in fission yeast.
    J Cell Biol. 2003 Mar 31;160(7):1083-92 PMID: 12654901
  5. An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation.
    J Cell Biol. 2003 Mar 31;160(7):1093-103 PMID: 12668659
  6. Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast.
    J Cell Biol. 2003 Jun 23;161(6):1081-92 PMID: 12810699
  7. 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
  8. Receptor internalization in yeast requires the Tor2-Rho1 signaling pathway.
    Mol Biol Cell. 2003 Nov;14(11):4676-84 PMID: 14593073
  9. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae.
    Yeast. 2004 Jun;21(8):661-70 PMID: 15197731
  10. Spatial coordination of cytokinetic events by compartmentalization of the cell cortex.
    Science. 2004 Jul 16;305(5682):393-6 PMID: 15256669
  11. Functional characterization of Dma1 and Dma2, the budding yeast homologues of Schizosaccharomyces pombe Dma1 and human Chfr.
    Mol Biol Cell. 2004 Aug;15(8):3796-810 PMID: 15146058
  12. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes.
    Yeast. 2004 Aug;21(11):947-62 PMID: 15334558
  13. A highly ordered ring of membrane-associated filaments in budding yeast.
    J Cell Biol. 1976 Jun;69(3):717-21 PMID: 773946
  14. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck.
    Mol Cell Biol. 1987 Oct;7(10):3678-87 PMID: 3316985
  15. Localization and possible functions of Drosophila septins.
    Mol Biol Cell. 1995 Dec;6(12):1843-59 PMID: 8590810
  16. The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast.
    EMBO J. 1996 Jan 2;15(1):83-91 PMID: 8598209
  17. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-beta-glucan synthase.
    Science. 1996 Apr 12;272(5259):279-81 PMID: 8602515
  18. Activation of yeast protein kinase C by Rho1 GTPase.
    J Biol Chem. 1996 Apr 19;271(16):9193-6 PMID: 8621575
  19. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
    Anal Chem. 1996 Mar 1;68(5):850-8 PMID: 8779443
  20. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae.
    EMBO J. 1996 Dec 2;15(23):6483-94 PMID: 8978675
  21. Signaling toward yeast 1,3-beta-glucan synthesis.
    Cell Struct Funct. 1996 Oct;21(5):395-402 PMID: 9118246
  22. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures.
    Genes Dev. 1997 Jun 15;11(12):1535-47 PMID: 9203580
  23. Role of Septin cytoskeleton in spine morphogenesis and dendrite development in neurons.
    Curr Biol. 2007 Oct 23;17(20):1752-8 PMID: 17935993
  24. The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology.
    Curr Biol. 2007 Oct 23;17(20):1746-51 PMID: 17935997
  25. The PAR-6 polarity protein regulates dendritic spine morphogenesis through p190 RhoGAP and the Rho GTPase.
    Dev Cell. 2008 Feb;14(2):216-26 PMID: 18267090
  26. Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth.
    Mol Biol Cell. 2008 Apr;19(4):1509-18 PMID: 18234840
  27. The septin family of GTPases: architecture and dynamics.
    Nat Rev Mol Cell Biol. 2008 Jun;9(6):478-89 PMID: 18478031
  28. An in vivo map of the yeast protein interactome.
    Science. 2008 Jun 13;320(5882):1465-70 PMID: 18467557
  29. A multidimensional chromatography technology for in-depth phosphoproteome analysis.
    Mol Cell Proteomics. 2008 Jul;7(7):1389-96 PMID: 18407956
  30. Septin stability and recycling during dynamic structural transitions in cell division and development.
    Curr Biol. 2008 Aug 26;18(16):1203-8 PMID: 18701287
  31. A novel septin-associated protein, Syp1p, is required for normal cell cycle-dependent septin cytoskeleton dynamics in yeast.
    Genetics. 2008 Nov;180(3):1445-57 PMID: 18791237
  32. Amoeboid T lymphocytes require the septin cytoskeleton for cortical integrity and persistent motility.
    Nat Cell Biol. 2009 Jan;11(1):17-26 PMID: 19043408
  33. Molecular mechanisms of membrane deformation by I-BAR domain proteins.
    Curr Biol. 2009 Jan 27;19(2):95-107 PMID: 19150238
  34. Existence of a novel clathrin-independent endocytic pathway in yeast that depends on Rho1 and formin.
    J Cell Biol. 2011 Nov 14;195(4):657-71 PMID: 22065638
  35. The F-BAR protein Syp1 negatively regulates WASp-Arp2/3 complex activity during endocytic patch formation.
    Curr Biol. 2009 Dec 15;19(23):1979-87 PMID: 19962315
  36. Understanding cytokinesis: lessons from fission yeast.
    Nat Rev Mol Cell Biol. 2010 Feb;11(2):149-55 PMID: 20094054
  37. An extensive circuitry for cell wall regulation in Candida albicans.
    PLoS Pathog. 2010 Feb;6(2):e1000752 PMID: 20140194
  38. Multiple functional domains of the yeast l,3-beta-glucan synthase subunit Fks1p revealed by quantitative phenotypic analysis of temperature-sensitive mutants.
    Genetics. 2010 Apr;184(4):1013-24 PMID: 20124029
  39. A global protein kinase and phosphatase interaction network in yeast.
    Science. 2010 May 21;328(5981):1043-6 PMID: 20489023
  40. Conquering the complex world of human septins: implications for health and disease.
    Clin Genet. 2010 Jun;77(6):511-24 PMID: 20236126
  41. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins.
    J Cell Biol. 1999 Nov 29;147(5):981-94 PMID: 10579719
  42. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP.
    Curr Biol. 1999 Dec 16-30;9(24):1458-67 PMID: 10607590
  43. Phosphorylation of a new brain-specific septin, G-septin, by cGMP-dependent protein kinase.
    J Biol Chem. 2000 Apr 7;275(14):10047-56 PMID: 10744683
  44. 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
  45. Gic2p may link activated Cdc42p to components involved in actin polarization, including Bni1p and Bud6p (Aip3p).
    Mol Cell Biol. 2000 Sep;20(17):6244-58 PMID: 10938101
  46. The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis.
    J Cell Sci. 2000 Nov;113 Pt 21:3825-37 PMID: 11034910
  47. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization.
    J Mol Biol. 2010 Dec 10;404(4):711-31 PMID: 20951708
  48. Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast.
    Sci Signal. 2010;3(153):rs4 PMID: 21177495
  49. Septin structure and function in yeast and beyond.
    Trends Cell Biol. 2011 Mar;21(3):141-8 PMID: 21177106
  50. Septin filament formation is essential in budding yeast.
    Dev Cell. 2011 Apr 19;20(4):540-9 PMID: 21497764
  51. Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis.
    Genes Dev. 2011 Apr 15;25(8):875-88 PMID: 21498574
  52. Atypical protein kinase C controls sea urchin ciliogenesis.
    Mol Biol Cell. 2011 Jun 15;22(12):2042-53 PMID: 21508313
  53. Evidence that a septin diffusion barrier is dispensable for cytokinesis in budding yeast.
    Biol Chem. 2011 Aug;392(8-9):813-29 PMID: 21824009
  54. Functional organization of the yeast proteome by systematic analysis of protein complexes.
    Nature. 2002 Jan 10;415(6868):141-7 PMID: 11805826
  55. Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p.
    J Cell Biol. 2002 Jan 21;156(2):315-26 PMID: 11807094
  56. Aspergillus nidulans septin AspB plays pre- and postmitotic roles in septum, branch, and conidiophore development.
    Mol Biol Cell. 2002 Jan;13(1):110-8 PMID: 11809826
  57. The Rho-GAP Bem2p plays a GAP-independent role in the morphogenesis checkpoint.
    EMBO J. 2002 Aug 1;21(15):4012-25 PMID: 12145202
  58. Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 2002 Oct;22(19):6906-20 PMID: 12215547
  59. 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
  60. Mechanisms for concentrating Rho1 during cytokinesis.
    Genes Dev. 2009 Apr 1;23(7):810-23 PMID: 19339687
  61. Septins and the lateral compartmentalization of eukaryotic membranes.
    Dev Cell. 2009 Apr;16(4):493-506 PMID: 19386259
  62. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution.
    Science. 2009 Sep 25;325(5948):1682-6 PMID: 19779198
  63. Global analysis of the yeast osmotic stress response by quantitative proteomics.
    Mol Biosyst. 2009 Nov;5(11):1337-46 PMID: 19823750
  64. Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation.
    EMBO J. 2009 Oct 21;28(20):3103-16 PMID: 19713939
  65. F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis.
    J Neurosci. 2009 Oct 21;29(42):13315-27 PMID: 19846719
  66. Budding yeast dma proteins control septin dynamics and the spindle position checkpoint by promoting the recruitment of the Elm1 kinase to the bud neck.
    PLoS Genet. 2012;8(4):e1002670 PMID: 22570619
  67. Proteasomal degradation resolves competition between cell polarization and cellular wound healing.
    Cell. 2012 Jul 6;150(1):151-64 PMID: 22727045
  68. Rapid redistribution of phosphatidylinositol-(4,5)-bisphosphate and septins during the Candida albicans response to caspofungin.
    Antimicrob Agents Chemother. 2012 Sep;56(9):4614-24 PMID: 22687514
  69. Cytokinesis in animal cells.
    Annu Rev Cell Dev Biol. 2012;28:29-58 PMID: 22804577
  70. Robust polarity establishment occurs via an endocytosis-based cortical corralling mechanism.
    J Cell Biol. 2013 Feb 18;200(4):407-18 PMID: 23401000
  71. Coupling of septins to the axial landmark by Bud4 in budding yeast.
    J Cell Sci. 2013 Mar 1;126(Pt 5):1218-26 PMID: 23345395
  72. Daughter cell identity emerges from the interplay of Cdc42, septins, and exocytosis.
    Dev Cell. 2013 Jul 29;26(2):148-61 PMID: 23906065
  73. Drosophila F-BAR protein Syndapin contributes to coupling the plasma membrane and contractile ring in cytokinesis.
    Open Biol. 2013 Aug;3(8):130081 PMID: 23926047
  74. Membrane-sculpting BAR domains generate stable lipid microdomains.
    Cell Rep. 2013 Sep 26;4(6):1213-23 PMID: 24055060
  75. A visual screen of protein localization during sporulation identifies new components of prospore membrane-associated complexes in budding yeast.
    Eukaryot Cell. 2014 Mar;13(3):383-91 PMID: 24390141
  76. A cell-signaling network temporally resolves specific versus promiscuous phosphorylation.
    Cell Rep. 2015 Feb 24;10(7):1202-14 PMID: 25704821
  77. Mechanical stress and network structure drive protein dynamics during cytokinesis.
    Curr Biol. 2015 Mar 2;25(5):663-70 PMID: 25702575
  78. Polarity proteins control ciliogenesis via kinesin motor interactions.
    Curr Biol. 2004 Aug 24;14(16):1451-61 PMID: 15324661
  79. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site.
    J Cell Biol. 1991 Feb;112(4):535-44 PMID: 1993729
  80. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
  81. MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C.
    Mol Cell Biol. 1993 May;13(5):3076-83 PMID: 8386320
  82. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins.
    Cell. 1994 May 6;77(3):371-9 PMID: 8181057
  83. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae.
    J Cell Biol. 1994 Jun;125(5):1077-93 PMID: 8195291
  84. Protein kinase C in yeast. Characteristics of the Saccharomyces cerevisiae PKC1 gene product.
    J Biol Chem. 1994 Jun 17;269(24):16821-8 PMID: 8207004
  85. Different domains of the essential GTPase Cdc42p required for growth and development of Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Jan;21(1):235-48 PMID: 11113198
  86. 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
  87. Spatial regulation of the exocyst complex by Rho1 GTPase.
    Nat Cell Biol. 2001 Apr;3(4):353-60 PMID: 11283608
  88. Cell cycle control of septin ring dynamics in the budding yeast.
    Microbiology. 2001 Jun;147(Pt 6):1437-50 PMID: 11390675
  89. An E3-like factor that promotes SUMO conjugation to the yeast septins.
    Cell. 2001 Sep 21;106(6):735-44 PMID: 11572779
  90. Borg proteins control septin organization and are negatively regulated by Cdc42.
    Nat Cell Biol. 2001 Oct;3(10):861-6 PMID: 11584266
  91. The guanine nucleotide-binding switch in three dimensions.
    Science. 2001 Nov 9;294(5545):1299-304 PMID: 11701921
  92. Mammalian septins: dynamic heteromers with roles in cellular morphogenesis and compartmentalization.
    J Pathol. 2012 Jan;226(2):287-99 PMID: 21990096
  93. Universal and confident phosphorylation site localization using phosphoRS.
    J Proteome Res. 2011 Dec 2;10(12):5354-62 PMID: 22073976
  94. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway.
    Genetics. 2011 Dec;189(4):1145-75 PMID: 22174182
  95. Septins at a glance.
    J Cell Sci. 2011 Dec 15;124(Pt 24):4141-6 PMID: 22247190
  96. Septins: the fourth component of the cytoskeleton.
    Nat Rev Mol Cell Biol. 2012 Mar;13(3):183-94 PMID: 22314400
  97. The septin AspB in Aspergillus nidulans forms bars and filaments and plays roles in growth emergence and conidiation.
    Eukaryot Cell. 2012 Mar;11(3):311-23 PMID: 22247265
  98. SEPT12 mutations cause male infertility with defective sperm annulus.
    Hum Mutat. 2012 Apr;33(4):710-9 PMID: 22275165
  99. A link between mitotic entry and membrane growth suggests a novel model for cell size control.
    J Cell Biol. 2012 Apr 2;197(1):89-104 PMID: 22451696
  100. Saccharomyces cerevisiae PKC1 encodes a protein kinase C (PKC) homolog with a substrate specificity similar to that of mammalian PKC.
    J Biol Chem. 1994 Jun 17;269(24):16829-36 PMID: 8207005
  101. Conditional lethality of a yeast strain expressing human RHOA in place of RHO1.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9317-21 PMID: 7937763
  102. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-D-glucan synthase.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12907-11 PMID: 7528927
  103. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae.
    Cell Mol Biol Res. 1994;40(3):229-39 PMID: 7874200
  104. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  105. A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae.
    EMBO J. 1995 Dec 1;14(23):5931-8 PMID: 8846785
  106. Subcellular membrane curvature mediated by the BAR domain superfamily proteins.
    Semin Cell Dev Biol. 2010 Jun;21(4):340-9 PMID: 19963073
  107. Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling.
    Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11805-10 PMID: 20547860
  108. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution.
    Science. 2010 Jul 23;329(5990):436-9 PMID: 20558667
  109. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis.
    Science. 2010 Sep 10;329(5997):1337-40 PMID: 20671153
  110. Cell biology. Septins at the nexus.
    Science. 2010 Sep 10;329(5997):1289-90 PMID: 20829470
  111. 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
  112. PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells.
    Eur J Biochem. 1998 Aug 15;256(1):201-11 PMID: 9746365
  113. 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
  114. 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
  115. 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
  116. Budding yeast Bub2 is localized at spindle pole bodies and activates the mitotic checkpoint via a different pathway from Mad2.
    J Cell Biol. 1999 May 31;145(5):979-91 PMID: 10352016
  117. 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
  118. Functional interdependence between septin and actin cytoskeleton.
    BMC Cell Biol. 2004 Nov 12;5(1):43 PMID: 15541171
  119. Molecular analysis reveals localization of Saccharomyces cerevisiae protein kinase C to sites of polarized growth and Pkc1p targeting to the nucleus and mitotic spindle.
    Eukaryot Cell. 2005 Jan;4(1):36-45 PMID: 15643058
  120. The Sept4 septin locus is required for sperm terminal differentiation in mice.
    Dev Cell. 2005 Mar;8(3):353-64 PMID: 15737931
  121. The molecular requirements for cytokinesis.
    Science. 2005 Mar 18;307(5716):1735-9 PMID: 15774750
  122. ACE2, CBK1, and BUD4 in budding and cell separation.
    Eukaryot Cell. 2005 Jun;4(6):1018-28 PMID: 15947194
  123. Mad3/BubR1 phosphorylation during spindle checkpoint activation depends on both Polo and Aurora kinases in budding yeast.
    Cell Cycle. 2005 Jul;4(7):972-80 PMID: 15970700
  124. Cytokinesis: welcome to the Rho zone.
    Trends Cell Biol. 2005 Dec;15(12):651-8 PMID: 16243528
  125. 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
  126. Polo-like kinase Cdc5 controls the local activation of Rho1 to promote cytokinesis.
    Science. 2006 Jul 7;313(5783):108-11 PMID: 16763112
  127. AgSwe1p regulates mitosis in response to morphogenesis and nutrients in multinucleated Ashbya gossypii cells.
    Mol Biol Cell. 2006 Oct;17(10):4494-512 PMID: 16899511
  128. Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae.
    J Proteome Res. 2007 Mar;6(3):1190-7 PMID: 17330950
  129. Sept12 is a component of the mammalian sperm tail annulus.
    Cell Motil Cytoskeleton. 2007 Oct;64(10):794-807 PMID: 17685441
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.E15-06-0366
Email
[email protected]
Published
2015-09-15
Epub
2015-00-15
Pages
3245-62
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC4569315
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.E15-06-0366 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