Home LiteratureArticle Details
PMID: 17065552 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

NPFXD-mediated endocytosis is required for polarity and function of a yeast cell wall stress sensor.

Molecular biology of the cell ·Vol. 18 ·No. 1 ·2007-01-00 ·Pages 57-65

Piao HL, Machado IM, Payne GS

Abstract

The actin-associated protein Sla1p, through its SHD1 domain, acts as an adaptor for the NPFX(1,2)D endocytic targeting signal in yeast. Here we report that Wsc1p, a cell wall stress sensor, depends on this signal-adaptor pair for endocytosis. Mutation of NPFDD in Wsc1p or expression of Sla1p lacking SHD1 blocked Wsc1p internalization. By live cell imaging, endocytically defective Wsc1p was not concentrated at sites of endocytosis. Polarized distribution of Wsc1p to regions of cell growth was lost in the absence of endocytosis. Mutations in genes necessary for endosome to Golgi traffic caused redistribution of Wsc1p from the cell surface to internal compartments, indicative of recycling. Inhibition of Wsc1p endocytosis caused defects in polarized deposition of the cell wall and increased sensitivity to perturbation of cell wall synthesis. Our results reveal that the NPFX(1,2)D-Sla1p system is responsible for directing Wsc1p into an endocytosis and recycling pathway necessary to maintain yeast cell wall polarity. The dynamic localization of Wsc1p, a sensor of the extracellular wall in yeast, resembles polarized distribution of certain extracellular matrix-sensing integrins through endocytic recycling.

MeSH Terms
Amino Acid Motifs Carrier Proteins/metabolism Cell Membrane/metabolism Cell Polarity Cell Wall/metabolism,ultrastructure Cytoskeletal Proteins Endocytosis Membrane Proteins/chemistry,metabolism Peptide Fragments/chemistry,metabolism Protein Binding Protein Structure, Tertiary Protein Transport Saccharomyces cerevisiae/cytology,ultrastructure Saccharomyces cerevisiae Proteins/chemistry,metabolism Signal Transduction
Chemicals
Carrier Proteins Cytoskeletal Proteins Membrane Proteins Peptide Fragments SLA1 protein, S cerevisiae SLG1 protein, S cerevisiae Saccharomyces cerevisiae Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Piao Hai Lan
Department of Biological Chemistry, David Geffen School of Medicine, University of California-Los Angeles, Los Angeles, CA 90095, USA.
Machado Iara M P
Payne Gregory S
References (56)
56 references, click to expand
  1. Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis.
    J Cell Biol. 2002 Apr 15;157(2):315-26 PMID: 11940605
  2. Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics.
    J Cell Sci. 2002 Apr 15;115(Pt 8):1703-15 PMID: 11950888
  3. Insights from yeast endosomes.
    Curr Opin Cell Biol. 2002 Aug;14(4):454-62 PMID: 12383796
  4. Receptor downregulation and multivesicular-body sorting.
    Nat Rev Mol Cell Biol. 2002 Dec;3(12):893-905 PMID: 12461556
  5. Vps10p cycles between the TGN and the late endosome via the plasma membrane in clathrin mutants.
    Mol Biol Cell. 2002 Dec;13(12):4296-307 PMID: 12475953
  6. Regulated portals of entry into the cell.
    Nature. 2003 Mar 6;422(6927):37-44 PMID: 12621426
  7. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins.
    Annu Rev Cell Dev Biol. 2003;19:141-72 PMID: 14570567
  8. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  9. The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling.
    Eukaryot Cell. 2003 Dec;2(6):1200-10 PMID: 14665455
  10. The biogenesis of multivesicular endosomes.
    Nat Rev Mol Cell Biol. 2004 Apr;5(4):317-23 PMID: 15071556
  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. Disruption of YHC8, a member of the TSR1 gene family, reveals its direct involvement in yeast protein translocation.
    J Biol Chem. 1999 Apr 16;274(16):11296-302 PMID: 10196219
  13. Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae.
    Mol Cell Biol. 1999 Jun;19(6):3969-76 PMID: 10330137
  14. Saccharomyces cerevisiae mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway.
    J Bacteriol. 1999 Jun;181(11):3330-40 PMID: 10348843
  15. Cell wall stress depolarizes cell growth via hyperactivation of RHO1.
    J Cell Biol. 1999 Oct 4;147(1):163-74 PMID: 10508863
  16. Ubiquitin and endocytic internalization in yeast and animal cells.
    Biochim Biophys Acta. 2004 Nov 29;1695(1-3):89-111 PMID: 15571811
  17. 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
  18. Cell wall integrity signaling in Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 2005 Jun;69(2):262-91 PMID: 15944456
  19. Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane.
    Biochim Biophys Acta. 2005 Jul 10;1744(3):415-37 PMID: 15922462
  20. 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
  21. A modular design for the clathrin- and actin-mediated endocytosis machinery.
    Cell. 2005 Oct 21;123(2):305-20 PMID: 16239147
  22. Integrin trafficking and the control of cell migration.
    Traffic. 2006 Jan;7(1):14-21 PMID: 16445683
  23. Cargo- and compartment-selective endocytic scaffold proteins.
    Biochem J. 2004 Oct 1;383(Pt 1):1-11 PMID: 15219178
  24. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  25. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  26. Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae.
    J Cell Biol. 1992 Aug;118(3):531-40 PMID: 1322413
  27. Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors.
    J Cell Biol. 1993 Jul;122(1):53-65 PMID: 8391002
  28. Continued functioning of the secretory pathway is essential for ribosome synthesis.
    Mol Cell Biol. 1994 Apr;14(4):2493-502 PMID: 8139552
  29. The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast.
    Mol Biol Cell. 1994 Sep;5(9):1023-37 PMID: 7841519
  30. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast.
    J Cell Biol. 1995 Mar;128(5):779-92 PMID: 7533169
  31. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response.
    Genes Dev. 1995 Jul 1;9(13):1559-71 PMID: 7628692
  32. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae.
    J Cell Biol. 1995 Nov;131(3):603-17 PMID: 7593183
  33. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis.
    Cell. 1996 Jan 26;84(2):277-87 PMID: 8565073
  34. 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
  35. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis.
    Science. 1996 Apr 12;272(5259):277-9 PMID: 8602514
  36. 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
  37. Moving membrane up to the front of migrating cells.
    Cell. 1996 May 17;85(4):465-7 PMID: 8653781
  38. Ubiquitination of the yeast a-factor receptor.
    J Cell Biol. 1996 Aug;134(3):661-74 PMID: 8707846
  39. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.
    Genetics. 1996 Dec;144(4):1425-36 PMID: 8978031
  40. The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae.
    J Cell Biol. 1996 Dec;135(6 Pt 2):1789-800 PMID: 8991091
  41. A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator.
    EMBO J. 1997 Aug 15;16(16):4924-37 PMID: 9305635
  42. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13804-9 PMID: 9391108
  43. The use of dimethylsulfoxide for fixation of yeasts for electron microscopy.
    Biotech Histochem. 1997 Sep;72(5):268-72 PMID: 9408587
  44. A screen for upstream components of the yeast protein kinase C signal transduction pathway identifies the product of the SLG1 gene.
    Mol Gen Genet. 1998 Apr;258(1-2):148-55 PMID: 9613583
  45. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  46. Pan1p, End3p, and S1a1p, three yeast proteins required for normal cortical actin cytoskeleton organization, associate with each other and play essential roles in cell wall morphogenesis.
    Mol Cell Biol. 2000 Jan;20(1):12-25 PMID: 10594004
  47. An unexpected link between the secretory path and the organization of the nucleus.
    J Biol Chem. 1999 Nov 19;274(47):33785-9 PMID: 10559272
  48. Sla1p is a functionally modular component of the yeast cortical actin cytoskeleton required for correct localization of both Rho1p-GTPase and Sla2p, a protein with talin homology.
    Mol Biol Cell. 1999 Apr;10(4):1061-75 PMID: 10198057
  49. Polarization of cell growth in yeast.
    J Cell Sci. 2000 Feb;113 ( Pt 4):571-85 PMID: 10652251
  50. Repression of ribosome and tRNA synthesis in secretion-defective cells is signaled by a novel branch of the cell integrity pathway.
    Mol Cell Biol. 2000 Jun;20(11):3843-51 PMID: 10805727
  51. Ric1p and Rgp1p form a complex that catalyses nucleotide exchange on Ypt6p.
    EMBO J. 2000 Sep 15;19(18):4885-94 PMID: 10990452
  52. Recycling of the yeast a-factor receptor.
    J Cell Biol. 2000 Oct 30;151(3):731-8 PMID: 11062272
  53. Ric1p and the Ypt6p GTPase function in a common pathway required for localization of trans-Golgi network membrane proteins.
    Mol Biol Cell. 2001 Jan;12(1):13-26 PMID: 11160819
  54. The arrest of secretion response in yeast: signaling from the secretory path to the nucleus via Wsc proteins and Pkc1p.
    Mol Cell. 2001 Aug;8(2):281-9 PMID: 11545731
  55. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting.
    EMBO J. 2001 Sep 17;20(18):5176-86 PMID: 11566881
  56. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis.
    Nat Cell Biol. 2002 May;4(5):389-93 PMID: 11988742
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2007-01-00
Epub
2006-00-25
Pages
57-65
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1751320
Subset
IM
Grants
NIGMS NIH HHS · R01 GM039040 · United States
NIGMS NIH HHS · GM39040 · 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: product@genelibs.com