Home LiteratureArticle Details
PMID: 21209323 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Exo-endocytic trafficking and the septin-based diffusion barrier are required for the maintenance of Cdc42p polarization during budding yeast asymmetric growth.

Molecular biology of the cell ·Vol. 22 ·No. 5 ·2011-03-01 ·Pages 624-33

Orlando K, Sun X, Zhang J, Lu T, Yokomizo L, Wang P, Guo W

Abstract

Cdc42p plays a central role in asymmetric cell growth in yeast by controlling actin organization and vesicular trafficking. However, how Cdc42p is maintained specifically at the daughter cell plasma membrane during asymmetric cell growth is unclear. We have analyzed Cdc42p localization in yeast mutants defective in various stages of membrane trafficking by fluorescence microscopy and biochemical fractionation. We found that two separate exocytic pathways mediate Cdc42p delivery to the daughter cell. Defects in one of these pathways result in Cdc42p being rerouted through the other. In particular, the pathway involving trafficking through endosomes may couple Cdc42p endocytosis from, and subsequent redelivery to, the plasma membrane to maintain Cdc42p polarization at the daughter cell. Although the endo-exocytotic coupling is necessary for Cdc42p polarization, it is not sufficient to prevent the lateral diffusion of Cdc42p along the cell cortex. A barrier function conferred by septins is required to counteract the dispersal of Cdc42p and maintain its localization in the daughter cell but has no effect on the initial polarization of Cdc42p at the presumptive budding site before symmetry breaking. Collectively, membrane trafficking and septins function synergistically to maintain the dynamic polarization of Cdc42p during asymmetric growth in yeast.

MeSH Terms
Cell Membrane/metabolism Cell Polarity Diffusion Endocytosis Exocytosis Models, Biological Mutation/genetics Protein Transport Saccharomyces cerevisiae/cytology,growth & development,metabolism Secretory Vesicles/metabolism Septins/metabolism cdc42 GTP-Binding Protein, Saccharomyces cerevisiae/metabolism
Chemicals
Septins cdc42 GTP-Binding Protein, Saccharomyces cerevisiae
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Orlando Kelly
Department of Biology, University of Pennsylvania, Philadelphia, PA 19096 College of Life Sciences, Nankai University, Tianjin, 300071, China.
Sun Xiaoli
Zhang Jian
Lu Tu
Yokomizo Lauren
Wang Puyue
Guo Wei
References (57)
57 references, click to expand
  1. Opposing roles for actin in Cdc42p polarization.
    Mol Biol Cell. 2005 Mar;16(3):1296-304 PMID: 15616194
  2. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Jun;9(6):1565-76 PMID: 9614194
  3. EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration.
    J Cell Sci. 2007 Mar 1;120(Pt 5):802-14 PMID: 17284518
  4. Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity.
    Cell. 2007 Apr 20;129(2):411-22 PMID: 17448998
  5. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase.
    Science. 2003 Feb 21;299(5610):1231-5 PMID: 12560471
  6. Central roles of small GTPases in the development of cell polarity in yeast and beyond.
    Microbiol Mol Biol Rev. 2007 Mar;71(1):48-96 PMID: 17347519
  7. Pep12p is a multifunctional yeast syntaxin that controls entry of biosynthetic, endocytic and retrograde traffic into the prevacuolar compartment.
    Traffic. 2000 Mar;1(3):259-69 PMID: 11208109
  8. 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
  9. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  10. Saccharomyces cerevisiae Cdc42p localizes to cellular membranes and clusters at sites of polarized growth.
    Eukaryot Cell. 2002 Jun;1(3):458-68 PMID: 12455994
  11. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity.
    Mol Biol Cell. 1993 Dec;4(12):1307-16 PMID: 8167411
  12. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling.
    Curr Biol. 2003 Sep 16;13(18):1636-40 PMID: 13678596
  13. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):54-105 PMID: 10066831
  14. Polarized growth in budding yeast in the absence of a localized formin.
    Mol Biol Cell. 2009 May;20(10):2540-8 PMID: 19297522
  15. Singularity in polarization: rewiring yeast cells to make two buds.
    Cell. 2009 Nov 13;139(4):731-43 PMID: 19914166
  16. Cdc42--the centre of polarity.
    J Cell Sci. 2004 Mar 15;117(Pt 8):1291-300 PMID: 15020669
  17. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling.
    J Cell Biol. 2004 Sep 13;166(6):889-900 PMID: 15353546
  18. Parallel secretory pathways to the cell surface in yeast.
    J Cell Biol. 1995 Oct;131(2):297-310 PMID: 7593160
  19. A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway.
    J Cell Biol. 2002 Jan 21;156(2):271-85 PMID: 11807092
  20. Symmetry breaking in the life cycle of the budding yeast.
    Cold Spring Harb Perspect Biol. 2009 Sep;1(3):a003384 PMID: 20066112
  21. Multiple sorting pathways between the late Golgi and the vacuole in yeast.
    Biochim Biophys Acta. 1998 Aug 14;1404(1-2):211-30 PMID: 9714809
  22. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.
    J Cell Biol. 1996 Nov;135(3):597-610 PMID: 8909536
  23. Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane.
    J Cell Biol. 1995 Apr;129(1):35-46 PMID: 7698993
  24. Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):230-47 PMID: 9529893
  25. Membrane organization and dynamics in cell polarity.
    Cold Spring Harb Perspect Biol. 2009 Nov;1(5):a001321 PMID: 20066116
  26. Scaffold-mediated symmetry breaking by Cdc42p.
    Nat Cell Biol. 2003 Dec;5(12):1062-70 PMID: 14625559
  27. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.
    Cell. 1980 Aug;21(1):205-15 PMID: 6996832
  28. Exo70p mediates the secretion of specific exocytic vesicles at early stages of the cell cycle for polarized cell growth.
    J Cell Biol. 2007 Mar 12;176(6):771-7 PMID: 17339375
  29. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization.
    EMBO J. 2002 Apr 2;21(7):1565-76 PMID: 11927541
  30. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42.
    J Cell Biol. 2008 Jan 14;180(1):145-58 PMID: 18195105
  31. Integrin trafficking and the control of cell migration.
    Traffic. 2006 Jan;7(1):14-21 PMID: 16445683
  32. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae.
    J Cell Biol. 1993 Jan;120(1):55-65 PMID: 8380177
  33. Moving membrane up to the front of migrating cells.
    Cell. 1996 May 17;85(4):465-7 PMID: 8653781
  34. Palmitoylated Ras proteins traffic through recycling endosomes to the plasma membrane during exocytosis.
    J Cell Biol. 2010 Oct 4;191(1):23-9 PMID: 20876282
  35. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration.
    Cell. 2008 Jul 11;134(1):135-47 PMID: 18614017
  36. Dual modes of cdc42 recycling fine-tune polarized morphogenesis.
    Dev Cell. 2009 Dec;17(6):823-35 PMID: 20059952
  37. Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis.
    Am J Physiol Cell Physiol. 2008 Aug;295(2):C545-56 PMID: 18579802
  38. Mechanisms of polarized growth and organelle segregation in yeast.
    Annu Rev Cell Dev Biol. 2004;20:559-91 PMID: 15473852
  39. Rvs161p and Rvs167p, the two yeast amphiphysin homologs, function together in vivo.
    J Biol Chem. 2001 Feb 23;276(8):6016-22 PMID: 11096097
  40. Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling.
    J Cell Biol. 2007 Apr 9;177(1):115-25 PMID: 17420293
  41. Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae.
    J Cell Biol. 1997 Jun 30;137(7):1469-82 PMID: 9199164
  42. Homologues of oxysterol-binding proteins affect Cdc42p- and Rho1p-mediated cell polarization in Saccharomyces cerevisiae.
    Traffic. 2006 Sep;7(9):1224-42 PMID: 17004323
  43. The exocyst complex in polarized exocytosis.
    Curr Opin Cell Biol. 2009 Aug;21(4):537-42 PMID: 19473826
  44. Cdc42p functions at the docking stage of yeast vacuole membrane fusion.
    EMBO J. 2001 Oct 15;20(20):5657-65 PMID: 11598009
  45. NPFXD-mediated endocytosis is required for polarity and function of a yeast cell wall stress sensor.
    Mol Biol Cell. 2007 Jan;18(1):57-65 PMID: 17065552
  46. Restriction of copper export in Saccharomyces cerevisiae to a late Golgi or post-Golgi compartment in the secretory pathway.
    J Biol Chem. 1997 Oct 10;272(41):25787-93 PMID: 9325307
  47. Dynamin and clathrin are required for the biogenesis of a distinct class of secretory vesicles in yeast.
    EMBO J. 2002 Feb 15;21(4):602-14 PMID: 11847108
  48. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity.
    Cold Spring Harb Perspect Biol. 2009 Jul;1(1):a000513 PMID: 20066074
  49. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex.
    Curr Biol. 2008 Nov 25;18(22):1719-26 PMID: 19013066
  50. Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin beta1 to control cell migration.
    Dev Cell. 2005 Nov;9(5):663-73 PMID: 16256741
  51. Widely conserved signaling pathways in the establishment of cell polarity.
    Cold Spring Harb Perspect Biol. 2009 Aug;1(2):a001370 PMID: 20066082
  52. Cyclical regulation of the exocyst and cell polarity determinants for polarized cell growth.
    Mol Biol Cell. 2005 Mar;16(3):1500-12 PMID: 15647373
  53. RalA-exocyst complex regulates integrin-dependent membrane raft exocytosis and growth signaling.
    Curr Biol. 2010 Jan 12;20(1):75-9 PMID: 20005108
  54. Scd5p and clathrin function are important for cortical actin organization, endocytosis, and localization of sla2p in yeast.
    Mol Biol Cell. 2002 Aug;13(8):2607-25 PMID: 12181333
  55. 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
  56. Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast.
    Mol Biol Cell. 1996 Apr;7(4):579-94 PMID: 8730101
  57. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking.
    EMBO J. 2001 Oct 15;20(20):5650-6 PMID: 11598008
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.E10-06-0484
Published
2011-03-01
Epub
2011-00-05
Pages
624-33
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC3046059
Subset
IM
Grants
NIGMS NIH HHS · R01 GM064690 · United States
NIGMS NIH HHS · GM64690 · United States
External Links
PubMed source DOI: 10.1091/mbc.E10-06-0484 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