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PMID: 22018597 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Clathrin-mediated endocytosis in budding yeast.

Trends in cell biology ·Vol. 22 ·No. 1 ·2012-01-00 ·Pages 1-13

Weinberg J, Drubin DG

Abstract

Clathrin-mediated endocytosis in the budding yeast Saccharomyces cerevisiae involves the ordered recruitment, activity and disassembly of nearly 60 proteins at distinct sites on the plasma membrane. Two-color live-cell fluorescence microscopy has proven to be invaluable for in vivo analysis of endocytic proteins: identifying new components, determining the order of protein arrival and dissociation, and revealing even very subtle mutant phenotypes. Yeast genetics and functional genomics facilitate identification of complex interaction networks between endocytic proteins and their regulators. Quantitative datasets produced by these various analyses have made theoretical modeling possible. Here, we discuss recent findings on budding yeast endocytosis that have advanced our knowledge of how -60 endocytic proteins are recruited, perform their functions, are regulated by lipid and protein modifications, and are disassembled, all with remarkable regularity.

MeSH Terms
Animals Clathrin/pharmacology Endocytosis/drug effects Genome, Fungal Humans Protein Processing, Post-Translational Saccharomyces cerevisiae/drug effects,genetics Selection, Genetic
Chemicals
Clathrin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Weinberg Jasper
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3202, USA.
Drubin David G
References (108)
108 references, click to expand
  1. Rsp5p, a new link between the actin cytoskeleton and endocytosis in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 2002 Oct;22(20):6946-8 PMID: 12242276
  2. Expression of Vps1 I649K a self-assembly defective yeast dynamin, leads to formation of extended endocytic invaginations.
    Commun Integr Biol. 2011 Jan;4(1):115-7 PMID: 21509199
  3. Actin filament bundling by fimbrin is important for endocytosis, cytokinesis, and polarization in fission yeast.
    J Biol Chem. 2011 Jul 29;286(30):26964-77 PMID: 21642440
  4. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  5. Yeast actin patches are networks of branched actin filaments.
    J Cell Biol. 2004 Aug 30;166(5):629-35 PMID: 15337772
  6. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis.
    Cell. 1985 Apr;40(4):1001-9 PMID: 3886157
  7. Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells.
    Nat Cell Biol. 2011 Mar;13(3):331-7 PMID: 21297641
  8. Negative regulation of the actin-regulating kinase Prk1p by patch localization-induced autophosphorylation.
    Traffic. 2009 Jan;10(1):35-41 PMID: 18939955
  9. The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole.
    FEBS Lett. 1996 Jan 8;378(2):177-81 PMID: 8549828
  10. Multiple pathways regulate endocytic coat disassembly in Saccharomyces cerevisiae for optimal downstream trafficking.
    Traffic. 2008 May;9(5):848-59 PMID: 18298676
  11. The Rsp5 ubiquitin ligase binds to and ubiquitinates members of the yeast CIN85-endophilin complex, Sla1-Rvs167.
    J Biol Chem. 2004 Apr 16;279(16):16017-25 PMID: 14761940
  12. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.
    J Cell Biol. 1994 Apr;125(2):381-91 PMID: 8163554
  13. Dynamic phosphoregulation of the cortical actin cytoskeleton and endocytic machinery revealed by real-time chemical genetic analysis.
    J Cell Biol. 2003 Sep 1;162(5):765-72 PMID: 12952930
  14. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex.
    Mol Biol Cell. 1999 Oct;10(10):3521-38 PMID: 10512884
  15. Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae.
    Mol Biol Cell. 1994 Nov;5(11):1185-98 PMID: 7865884
  16. PtdIns(4,5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization.
    J Cell Biol. 2007 Apr 23;177(2):355-67 PMID: 17452534
  17. Functional genomic analysis reveals the utility of the I/LWEQ module as a predictor of protein:actin interaction.
    Biochem Biophys Res Commun. 1999 Dec 9;266(1):135-40 PMID: 10581178
  18. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces.
    J Cell Biol. 1984 Mar;98(3):922-33 PMID: 6365930
  19. The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton.
    Mol Biol Cell. 2003 Jul;14(7):2617-29 PMID: 12857851
  20. Specific sterols required for the internalization step of endocytosis in yeast.
    Mol Biol Cell. 1999 Nov;10(11):3943-57 PMID: 10564282
  21. Interaction of Sla2p's ANTH domain with PtdIns(4,5)P2 is important for actin-dependent endocytic internalization.
    Mol Biol Cell. 2005 Feb;16(2):717-30 PMID: 15574875
  22. 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
  23. Clathrin light chain directs endocytosis by influencing the binding of the yeast Hip1R homologue, Sla2, to F-actin.
    Mol Biol Cell. 2011 Oct;22(19):3699-714 PMID: 21849475
  24. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision.
    J Cell Biol. 2011 Jan 10;192(1):111-9 PMID: 21200030
  25. Coronin switches roles in actin disassembly depending on the nucleotide state of actin.
    Mol Cell. 2009 May 15;34(3):364-74 PMID: 19450534
  26. Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast.
    Curr Biol. 2010 Aug 24;20(16):1415-22 PMID: 20705466
  27. Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast.
    EMBO J. 2001 Dec 3;20(23):6783-92 PMID: 11726514
  28. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity.
    Dev Cell. 2006 Jul;11(1):33-46 PMID: 16824951
  29. The yeast dynamin-related GTPase Vps1p functions in the organization of the actin cytoskeleton via interaction with Sla1p.
    J Cell Sci. 2004 Aug 1;117(Pt 17):3839-53 PMID: 15265985
  30. Negative regulation of yeast WASp by two SH3 domain-containing proteins.
    Curr Biol. 2003 Jun 17;13(12):1000-8 PMID: 12814545
  31. Actin and septin ultrastructures at the budding yeast cell cortex.
    Mol Biol Cell. 2005 Jan;16(1):372-84 PMID: 15525671
  32. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants.
    EMBO J. 1994 Jul 15;13(14):3261-71 PMID: 8045256
  33. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits.
    Dev Cell. 2009 Dec;17(6):811-22 PMID: 20059951
  34. The WASP homologue Las17 activates the novel actin-regulatory activity of Ysc84 to promote endocytosis in yeast.
    Mol Biol Cell. 2009 Mar;20(6):1618-28 PMID: 19158382
  35. Modeling vesicle traffic reveals unexpected consequences for Cdc42p-mediated polarity establishment.
    Curr Biol. 2011 Feb 8;21(3):184-94 PMID: 21277209
  36. Dissecting BAR domain function in the yeast Amphiphysins Rvs161 and Rvs167 during endocytosis.
    Mol Biol Cell. 2010 Sep 1;21(17):3054-69 PMID: 20610658
  37. Reconstitution and protein composition analysis of endocytic actin patches.
    Curr Biol. 2010 Nov 9;20(21):1890-9 PMID: 21035341
  38. A "primer"-based mechanism underlies branched actin filament network formation and motility.
    Curr Biol. 2010 Mar 9;20(5):423-8 PMID: 20188562
  39. The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis.
    Microbiol Rev. 1995 Jun;59(2):304-22 PMID: 7603412
  40. Eisosomes mark static sites of endocytosis.
    Nature. 2006 Feb 23;439(7079):998-1003 PMID: 16496001
  41. The ubiquitin-interacting motifs target the endocytic adaptor protein epsin for ubiquitination.
    Curr Biol. 2002 Jul 9;12(13):1112-6 PMID: 12121618
  42. Cargo and dynamin regulate clathrin-coated pit maturation.
    PLoS Biol. 2009 Mar 17;7(3):e57 PMID: 19296720
  43. FINE STRUCTURE IN FROZEN-ETCHED YEAST CELLS.
    J Cell Biol. 1963 Jun 1;17(3):609-28 PMID: 19866628
  44. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis.
    PLoS Biol. 2011 Mar;9(3):e1000604 PMID: 21445324
  45. Synaptojanin family members are implicated in endocytic membrane traffic in yeast.
    J Cell Sci. 1998 Nov;111 ( Pt 22):3347-56 PMID: 9788876
  46. Furrow-like invaginations of the yeast plasma membrane correspond to membrane compartment of Can1.
    J Cell Sci. 2009 Aug 15;122(Pt 16):2887-94 PMID: 19638406
  47. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast.
    J Cell Biol. 1995 Mar;128(5):779-92 PMID: 7533169
  48. Regulation of clathrin adaptor function in endocytosis: novel role for the SAM domain.
    EMBO J. 2010 Mar 17;29(6):1033-44 PMID: 20150898
  49. Distinct roles for Arp2/3 regulators in actin assembly and endocytosis.
    PLoS Biol. 2008 Jan;6(1):e1 PMID: 18177206
  50. The mechanochemistry of endocytosis.
    PLoS Biol. 2009 Sep;7(9):e1000204 PMID: 19787029
  51. Vrp1p-Las17p interaction is critical for actin patch polarization but is not essential for growth or fluid phase endocytosis in S. cerevisiae.
    Biochim Biophys Acta. 2010 Dec;1803(12):1332-46 PMID: 20816901
  52. Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway.
    J Cell Biol. 2010 Mar 22;188(6):769-77 PMID: 20231387
  53. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A.
    J Cell Biol. 1997 Apr 21;137(2):399-416 PMID: 9128251
  54. A proteomics approach to understanding protein ubiquitination.
    Nat Biotechnol. 2003 Aug;21(8):921-6 PMID: 12872131
  55. Down regulation of the alpha-factor pheromone receptor in S. cerevisiae.
    Cell. 1986 Aug 1;46(3):345-53 PMID: 3015412
  56. Harnessing actin dynamics for clathrin-mediated endocytosis.
    Nat Rev Mol Cell Biol. 2006 Jun;7(6):404-14 PMID: 16723976
  57. Actin and fimbrin are required for the internalization step of endocytosis in yeast.
    EMBO J. 1993 Jul;12(7):2855-62 PMID: 8335001
  58. Characterization of the yeast amphiphysins Rvs161p and Rvs167p reveals roles for the Rvs heterodimer in vivo.
    Mol Biol Cell. 2006 Mar;17(3):1306-21 PMID: 16394103
  59. Clathrin-mediated endocytosis in AP-2-depleted cells.
    J Cell Biol. 2003 Sep 1;162(5):909-18 PMID: 12952941
  60. Functional organization of the yeast proteome by systematic analysis of protein complexes.
    Nature. 2002 Jan 10;415(6868):141-7 PMID: 11805826
  61. Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5793-8 PMID: 16574772
  62. 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
  63. Interaction between Epsin/Yap180 adaptors and the scaffolds Ede1/Pan1 is required for endocytosis.
    Mol Biol Cell. 2008 Jul;19(7):2936-48 PMID: 18448668
  64. Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane.
    J Cell Biol. 2008 Mar 24;180(6):1219-32 PMID: 18347067
  65. Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface.
    Cell. 2008 Nov 14;135(4):714-25 PMID: 18976803
  66. 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
  67. Phosphoregulation of Arp2/3-dependent actin assembly during receptor-mediated endocytosis.
    Nat Cell Biol. 2005 Mar;7(3):246-54 PMID: 15711538
  68. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis.
    Nat Cell Biol. 2011 Aug 14;13(9):1124-31 PMID: 21841790
  69. FCHo proteins are nucleators of clathrin-mediated endocytosis.
    Science. 2010 Jun 4;328(5983):1281-4 PMID: 20448150
  70. Plasma membrane microdomains regulate turnover of transport proteins in yeast.
    J Cell Biol. 2008 Dec 15;183(6):1075-88 PMID: 19064668
  71. WW domains of Rsp5p define different functions: determination of roles in fluid phase and uracil permease endocytosis in Saccharomyces cerevisiae.
    Genetics. 2001 Jan;157(1):91-101 PMID: 11139494
  72. Cryopreparation of biological specimens for immunoelectron microscopy.
    Ann Anat. 2009 Jun;191(3):231-47 PMID: 19264467
  73. Pil1 controls eisosome biogenesis.
    Mol Biol Cell. 2009 Feb;20(3):809-18 PMID: 19037108
  74. The function of yeast epsin and Ede1 ubiquitin-binding domains during receptor internalization.
    Traffic. 2010 Jan;11(1):151-60 PMID: 19903324
  75. 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
  76. Novel function of clathrin light chain in promoting endocytic vesicle formation.
    Mol Biol Cell. 2006 Oct;17(10):4343-52 PMID: 16870700
  77. Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae.
    EMBO J. 2000 Jun 15;19(12):2824-33 PMID: 10856228
  78. Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis.
    J Biol Chem. 1998 Jun 19;273(25):15779-86 PMID: 9624177
  79. A role for the dynamin-like protein Vps1 during endocytosis in yeast.
    J Cell Sci. 2010 Oct 15;123(Pt 20):3496-506 PMID: 20841380
  80. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  81. An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast.
    J Cell Sci. 2003 Jun 15;116(Pt 12):2551-64 PMID: 12734398
  82. 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
  83. Clathrin is important for normal actin dynamics and progression of Sla2p-containing patches during endocytosis in yeast.
    Traffic. 2006 May;7(5):574-88 PMID: 16643280
  84. Quantitative analysis of the mechanism of endocytic actin patch assembly and disassembly in fission yeast.
    Mol Biol Cell. 2010 Aug 15;21(16):2894-904 PMID: 20587778
  85. Endocytic vesicle scission by lipid phase boundary forces.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10277-10282 PMID: 16801551
  86. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis.
    Cell. 2010 Feb 19;140(4):540-53 PMID: 20178746
  87. Differential requirements for actin during yeast and mammalian endocytosis.
    Nat Cell Biol. 2009 Aug;11(8):1039-42 PMID: 19597484
  88. Multiple functions of sterols in yeast endocytosis.
    Mol Biol Cell. 2002 Aug;13(8):2664-80 PMID: 12181337
  89. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis.
    Cell. 1996 Jan 26;84(2):277-87 PMID: 8565073
  90. Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast.
    J Cell Sci. 2011 Feb 1;124(Pt 3):328-37 PMID: 21224391
  91. Mathematical modeling of endocytic actin patch kinetics in fission yeast: disassembly requires release of actin filament fragments.
    Mol Biol Cell. 2010 Aug 15;21(16):2905-15 PMID: 20587776
  92. Negative regulation of yeast Eps15-like Arp2/3 complex activator, Pan1p, by the Hip1R-related protein, Sla2p, during endocytosis.
    Mol Biol Cell. 2007 Feb;18(2):658-68 PMID: 17151356
  93. Endocytose and degradation of the uracil permease of S. cerevisiae under stress conditions: possible role of ubiquitin.
    Folia Microbiol (Praha). 1994;39(6):554-7 PMID: 8550022
  94. A yeast killer toxin screen provides insights into a/b toxin entry, trafficking, and killing mechanisms.
    Dev Cell. 2009 Oct;17(4):552-60 PMID: 19853568
  95. The yeast Epsin Ent1 is recruited to membranes through multiple independent interactions.
    J Biol Chem. 2003 Mar 21;278(12):10737-43 PMID: 12529323
  96. Characterization of dip1p reveals a switch in Arp2/3-dependent actin assembly for fission yeast endocytosis.
    Curr Biol. 2011 Jun 7;21(11):905-16 PMID: 21620704
  97. In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast.
    Dev Cell. 2005 Jul;9(1):87-98 PMID: 15992543
  98. Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1707-16 PMID: 8276891
  99. Regulators of yeast endocytosis identified by systematic quantitative analysis.
    J Cell Biol. 2009 Jun 15;185(6):1097-110 PMID: 19506040
  100. The yeast dynamin-like protein Vps1:vps1 mutations perturb the internalization and the motility of endocytic vesicles and endosomes via disorganization of the actin cytoskeleton.
    Eur J Cell Biol. 2010 Jul;89(7):499-508 PMID: 20189679
  101. Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission.
    Dev Cell. 2011 Feb 15;20(2):206-18 PMID: 21316588
  102. Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins.
    PLoS Biol. 2009 Oct;7(10):e1000218 PMID: 19841731
  103. Yeast Arf3p modulates plasma membrane PtdIns(4,5)P2 levels to facilitate endocytosis.
    Traffic. 2008 Apr;9(4):559-73 PMID: 18208507
  104. 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
  105. 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
  106. Ubiquitination screen using protein microarrays for comprehensive identification of Rsp5 substrates in yeast.
    Mol Syst Biol. 2007;3:116 PMID: 17551511
  107. Ubiquitin binds to and regulates a subset of SH3 domains.
    Mol Cell. 2007 Jan 26;25(2):273-84 PMID: 17244534
  108. Lsb5p interacts with actin regulators Sla1p and Las17p, ubiquitin and Arf3p to couple actin dynamics to membrane trafficking processes.
    Biochem J. 2005 May 1;387(Pt 3):649-58 PMID: 15651983
Article Info
Journal
Trends in cell biology
Abbr.
Trends Cell Biol
ISSN
1879-3088
Published
2012-01-00
Epub
2011-00-20
Pages
1-13
Language
English
Region
England
NLM ID
9200566
PMCID
PMC3253927
Subset
IM
Grants
NIGMS NIH HHS · R01 GM042759 · United States
NIGMS NIH HHS · R01 GM050399-16 · United States
NIGMS NIH HHS · GM R01 50399 · United States
NIGMS NIH HHS · R01 GM042759-17 · United States
NIGMS NIH HHS · R01 GM050399 · United States
NIGMS NIH HHS · GM R01 42759 · United States
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