Home LiteratureArticle Details
PMID: 19154724 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Cell polarity determinants establish asymmetry in MEN signaling.

Developmental cell ·Vol. 16 ·No. 1 ·2009-01-00 ·Pages 132-45

Monje-Casas F, Amon A

Abstract

Components of the mitotic exit network (MEN), a signaling pathway that triggers exit from mitosis, localize to the spindle pole body (SPB) that migrates into the daughter cell during anaphase but are largely absent from the SPB that remains in the mother cell. Through the analysis of one of the determinants of this asymmetry, Bfa1, we find that the machinery responsible for establishing cell polarity and cytoplasmic microtubules collaborate to establish MEN asymmetry. In cells defective in the Cdc42 signaling pathway or the formin Bni1, Bfa1 localizes to both SPBs. The quantitative analysis of Bfa1 localization further shows that Bfa1 can associate with both SPBs in a transient and highly dynamic fashion, but the protein is stabilized on the SPB that migrates into the daughter cell during anaphase through microtubule-bud cortex interactions. Our results indicate that mother-daughter cell asymmetry determinants establish MEN signaling asymmetry through microtubule-bud cortex interactions.

MeSH Terms
Actins/metabolism Cell Cycle/physiology Cell Cycle Proteins/genetics,metabolism Cell Polarity/physiology Cytoskeletal Proteins/genetics,metabolism Cytoskeleton/metabolism Microtubules/metabolism Monomeric GTP-Binding Proteins/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Signal Transduction/physiology Spindle Apparatus/metabolism Tubulin/genetics,metabolism
Chemicals
Actins BFA1 protein, S cerevisiae BUB2 protein, S cerevisiae Cell Cycle Proteins Cytoskeletal Proteins Recombinant Fusion Proteins Saccharomyces cerevisiae Proteins TEM1 protein, S cerevisiae Tubulin Monomeric GTP-Binding Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Monje-Casas Fernando
David H. Koch Institute for Integrative Cancer Research and Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
Amon Angelika
References (58)
58 references, click to expand
  1. 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
  2. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae.
    J Biol Chem. 1995 Jan 13;270(2):626-30 PMID: 7822288
  3. Characterization of the CDC10 product and the timing of events of the budding site of Saccharomyces cerevisiae.
    Mol Cells. 2001 Aug 31;12(1):77-83 PMID: 11561733
  4. The role of actin in spindle orientation changes during the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1999 Sep 6;146(5):1019-32 PMID: 10477756
  5. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis.
    Science. 1997 Apr 4;276(5309):118-22 PMID: 9082982
  6. Bifurcation of the mitotic checkpoint pathway in budding yeast.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4989-94 PMID: 10220406
  7. Asymmetric spindle pole localization of yeast Cdc15 kinase links mitotic exit and cytokinesis.
    Curr Biol. 2001 Mar 6;11(5):345-50 PMID: 11267871
  8. Regulation of septin organization and function in yeast.
    Trends Cell Biol. 2003 Aug;13(8):403-9 PMID: 12888292
  9. Localization of Bud2p, a GTPase-activating protein necessary for programming cell polarity in yeast to the presumptive bud site.
    Genes Dev. 1999 Aug 1;13(15):1912-7 PMID: 10444589
  10. Cla4p, a Saccharomyces cerevisiae Cdc42p-activated kinase involved in cytokinesis, is activated at mitosis.
    Mol Cell Biol. 1997 Sep;17(9):5067-76 PMID: 9271384
  11. Disappearance of the budding yeast Bub2-Bfa1 complex from the mother-bound spindle pole contributes to mitotic exit.
    J Cell Biol. 2006 Jan 30;172(3):335-46 PMID: 16449187
  12. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis.
    Mol Cell Biol. 1998 Jul;18(7):4053-69 PMID: 9632790
  13. 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
  14. 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
  15. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae.
    EMBO J. 1997 May 15;16(10):2745-55 PMID: 9184220
  16. Mitosis in living budding yeast: anaphase A but no metaphase plate.
    Science. 1997 Jul 25;277(5325):574-8 PMID: 9228009
  17. 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
  18. Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex.
    EMBO J. 2001 Nov 15;20(22):6359-70 PMID: 11707407
  19. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states.
    J Cell Sci. 2000 Feb;113 ( Pt 3):365-75 PMID: 10639324
  20. The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit.
    Mol Biol Cell. 2004 Apr;15(4):1519-32 PMID: 14718561
  21. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae.
    Yeast. 2004 Jun;21(8):661-70 PMID: 15197731
  22. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septum-inducing protein kinase Cdc7p.
    Genes Dev. 1998 Jan 1;12(1):84-94 PMID: 9420333
  23. Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae.
    Mol Biol Cell. 2000 Feb;11(2):593-611 PMID: 10679017
  24. Rho family members: activators of MAP kinase cascades.
    Cell. 1995 Aug 25;82(4):527-9 PMID: 7664330
  25. 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
  26. Cdk1-Clb4 controls the interaction of astral microtubule plus ends with subdomains of the daughter cell cortex.
    Genes Dev. 2004 Jul 15;18(14):1709-24 PMID: 15256500
  27. Functional characterization of the Cdc42p binding domain of yeast Ste20p protein kinase.
    EMBO J. 1997 Jan 2;16(1):83-97 PMID: 9009270
  28. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus.
    Nature. 1999 Apr 29;398(6730):818-23 PMID: 10235265
  29. Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast.
    Mol Biol Cell. 2001 Sep;12(9):2870-80 PMID: 11553724
  30. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints.
    Cell. 2001 Nov 30;107(5):655-65 PMID: 11733064
  31. 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
  32. Dissection of septin actin interactions using actin overexpression in Saccharomyces cerevisiae.
    Mol Microbiol. 2004 Jul;53(2):469-83 PMID: 15228528
  33. A mechanism for coupling exit from mitosis to partitioning of the nucleus.
    Cell. 2000 Jul 7;102(1):21-31 PMID: 10929710
  34. Kin4 kinase delays mitotic exit in response to spindle alignment defects.
    Mol Cell. 2005 Jul 22;19(2):209-21 PMID: 16039590
  35. Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate bud cortex interactions.
    EMBO J. 2003 Feb 3;22(3):438-49 PMID: 12554645
  36. The protein kinase Kin4 inhibits exit from mitosis in response to spindle position defects.
    Mol Cell. 2005 Jul 22;19(2):223-34 PMID: 16039591
  37. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation.
    Mol Cell. 1998 Dec;2(6):709-18 PMID: 9885559
  38. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae.
    EMBO J. 1996 Nov 15;15(22):6060-8 PMID: 8947028
  39. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle.
    Cell. 1994 Jul 1;77(7):1037-50 PMID: 8020094
  40. The Bub2p spindle checkpoint links nuclear migration with mitotic exit.
    Mol Cell. 2000 Jul;6(1):1-10 PMID: 10949022
  41. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex.
    Cell. 1999 Apr 16;97(2):233-44 PMID: 10219244
  42. Polarization of cell growth in yeast.
    J Cell Sci. 2000 Feb;113 ( Pt 4):571-85 PMID: 10652251
  43. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation.
    Annu Rev Genet. 2004;38:203-32 PMID: 15568976
  44. Cdc14-regulated midzone assembly controls anaphase B.
    J Cell Biol. 2007 Jun 18;177(6):981-93 PMID: 17562791
  45. Yeast formins regulate cell polarity by controlling the assembly of actin cables.
    Nat Cell Biol. 2002 Jan;4(1):42-50 PMID: 11740491
  46. Timing is everything: regulation of mitotic exit and cytokinesis by the MEN and SIN.
    Trends Cell Biol. 2001 Feb;11(2):89-95 PMID: 11166217
  47. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4463-8 PMID: 9114012
  48. 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
  49. A morphogenesis checkpoint monitors the actin cytoskeleton in yeast.
    J Cell Biol. 1998 Sep 21;142(6):1487-99 PMID: 9744879
  50. Nud1p links astral microtubule organization and the control of exit from mitosis.
    EMBO J. 2000 Dec 1;19(23):6475-88 PMID: 11101520
  51. Linked for life: temporal and spatial coordination of late mitotic events.
    Curr Opin Cell Biol. 2004 Feb;16(1):41-8 PMID: 15037303
  52. Mitotic spindle: laser microsurgery in yeast cells.
    Curr Biol. 2004 Sep 21;14(18):R748-50 PMID: 15380083
  53. Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants.
    Mol Biol Cell. 2000 Nov;11(11):3949-61 PMID: 11071919
  54. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast.
    EMBO J. 1996 Dec 16;15(24):7046-59 PMID: 9003780
  55. Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast.
    J Cell Biol. 1999 Mar 22;144(6):1203-18 PMID: 10087264
  56. Localization of core spindle pole body (SPB) components during SPB duplication in Saccharomyces cerevisiae.
    J Cell Biol. 1999 May 17;145(4):809-23 PMID: 10330408
  57. Multistep and multimode cortical anchoring of tea1p at cell tips in fission yeast.
    EMBO J. 2005 Nov 2;24(21):3690-9 PMID: 16222337
  58. Septins: a ring to part mother and daughter.
    Curr Genet. 2002 Jun;41(3):123-31 PMID: 12111093
Article Info
Journal
Developmental cell
Abbr.
Dev Cell
ISSN
1878-1551
Published
2009-01-00
Pages
132-45
Language
English
Region
United States
NLM ID
101120028
PMCID
PMC2713012
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · R29 GM056800 · United States
NIGMS NIH HHS · R01 GM056800 · United States
NIGMS NIH HHS · GM056800 · United States
NIGMS NIH HHS · R01 GM056800-14 · United States
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]