Home LiteratureArticle Details
PMID: 10679005 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Sbe2p and sbe22p, two homologous Golgi proteins involved in yeast cell wall formation.

Molecular biology of the cell ·Vol. 11 ·No. 2 ·2000-02-00 ·Pages 435-52

Santos B, Snyder M

Abstract

The cell wall of fungal cells is important for cell integrity and cell morphogenesis and protects against harmful environmental conditions. The yeast cell wall is a complex structure consisting mainly of mannoproteins, glucan, and chitin. The molecular mechanisms by which the cell wall components are synthesized and transported to the cell surface are poorly understood. We have identified and characterized two homologous yeast proteins, Sbe2p and Sbe22p, through their suppression of a chs5 spa2 mutant strain defective in chitin synthesis and cell morphogenesis. Although sbe2 and sbe22 null mutants are viable, sbe2 sbe22 cells display several phenotypes indicative of defects in cell integrity and cell wall structure. First, sbe2 sbe22 cells display a sorbitol-remediable lysis defect at 37 degrees C and are hypersensitive to SDS and calcofluor. Second, electron microscopic analysis reveals that sbe2 sbe22 cells have an aberrant cell wall structure with a reduced mannoprotein layer. Finally, immunofluorescence experiments reveal that in small-budded cells, sbe2 sbe22 mutants mislocalize Chs3p, a protein involved in chitin synthesis. In addition, sbe2 sbe22 diploids have a bud-site selection defect, displaying a random budding pattern. A Sbe2p-GFP fusion protein localizes to cytoplasmic patches, and Sbe2p cofractionates with Golgi proteins. Deletion of CHS5, which encodes a Golgi protein involved in the transport of Chs3p to the cell periphery, is lethal in combination with disruption of SBE2 and SBE22. Thus, we suggest a model in which Sbe2p and Sbe22p are involved in the transport of cell wall components from the Golgi apparatus to the cell surface periphery in a pathway independent of Chs5p.

MeSH Terms
Amino Acid Sequence Benzenesulfonates/metabolism Cell Division Cell Polarity Cell Wall/metabolism,ultrastructure Chitin Synthase/analysis,genetics Cytoplasm/chemistry Cytoskeletal Proteins Epistasis, Genetic Fungal Proteins/analysis,genetics Genes, Fungal/genetics,physiology Genes, Lethal/genetics Glucan 1,3-beta-Glucosidase Glycoside Hydrolases/metabolism Golgi Apparatus/chemistry,metabolism Membrane Glycoproteins/chemistry,genetics,metabolism Molecular Sequence Data Mutation/genetics Saccharomyces cerevisiae/cytology,genetics,growth & development,metabolism Saccharomyces cerevisiae Proteins Sequence Homology, Amino Acid Sodium Dodecyl Sulfate/metabolism Suppression, Genetic/genetics Vesicular Transport Proteins beta-Fructofuranosidase beta-Glucosidase/metabolism
Chemicals
Benzenesulfonates Cytoskeletal Proteins Fungal Proteins Membrane Glycoproteins SBE2 protein, S cerevisiae SBE22 protein, S cerevisiae SPA2 protein, S cerevisiae Saccharomyces cerevisiae Proteins Vesicular Transport Proteins Sodium Dodecyl Sulfate C.I. Fluorescent Brightening Agent 28 CHS5 protein, S cerevisiae Chitin Synthase Glycoside Hydrolases beta-Glucosidase beta-Fructofuranosidase Glucan 1,3-beta-Glucosidase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Santos B
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520-8103, USA.
Snyder M
References (76)
76 references, click to expand
  1. 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
  2. Parallel secretory pathways to the cell surface in yeast.
    J Cell Biol. 1995 Oct;131(2):297-310 PMID: 7593160
  3. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1991 Jul;114(1):111-23 PMID: 2050738
  4. The role of Myo2, a yeast class V myosin, in vesicular transport.
    J Cell Biol. 1995 Mar;128(6):1055-68 PMID: 7896871
  5. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.
    J Cell Biol. 1996 Nov;135(3):597-610 PMID: 8909536
  6. The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway.
    EMBO J. 1994 Oct 17;13(20):4896-907 PMID: 7957057
  7. Isolation, characterization, and properties of Saccharomyces cerevisiae mnn mutants with nonconditional protein glycosylation defects.
    Methods Enzymol. 1990;185:440-70 PMID: 2199792
  8. The high osmolarity glycerol response (HOG) MAP kinase pathway controls localization of a yeast golgi glycosyltransferase.
    J Cell Biol. 1998 Nov 16;143(4):935-46 PMID: 9817752
  9. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1995 May;129(3):751-65 PMID: 7730409
  10. Chs7p, a new protein involved in the control of protein export from the endoplasmic reticulum that is specifically engaged in the regulation of chitin synthesis in Saccharomyces cerevisiae.
    J Cell Biol. 1999 Jun 14;145(6):1153-63 PMID: 10366589
  11. Cell polarity and morphogenesis in budding yeast.
    Annu Rev Microbiol. 1998;52:687-744 PMID: 9891811
  12. The contribution of the O-glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild-type cells and beta 1,6-glucan-deficient mutants.
    Mol Microbiol. 1999 Mar;31(6):1835-44 PMID: 10209754
  13. A synthetic lethal screen identifies SLK1, a novel protein kinase homolog implicated in yeast cell morphogenesis and cell growth.
    Mol Cell Biol. 1992 Mar;12(3):1162-78 PMID: 1545797
  14. Immunofluorescence methods for yeast.
    Methods Enzymol. 1991;194:565-602 PMID: 2005809
  15. 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
  16. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway.
    Cell. 1990 May 18;61(4):723-33 PMID: 2188733
  17. Selection of polarized growth sites in yeast.
    Trends Cell Biol. 1996 Nov;6(11):434-41 PMID: 15157515
  18. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating.
    J Cell Biol. 1990 Oct;111(4):1451-64 PMID: 2211820
  19. Localization of components involved in protein transport and processing through the yeast Golgi apparatus.
    J Cell Biol. 1991 Jan;112(1):27-37 PMID: 1986005
  20. 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
  21. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole.
    Cell. 1982 Sep;30(2):439-48 PMID: 6754086
  22. Identification of the MNN2 and MNN5 mannosyltransferases required for forming and extending the mannose branches of the outer chain mannans of Saccharomyces cerevisiae.
    J Biol Chem. 1998 Oct 9;273(41):26836-43 PMID: 9756928
  23. Identification of three mannoproteins in the cell wall of Saccharomyces cerevisiae.
    J Bacteriol. 1995 Jun;177(11):3104-10 PMID: 7768807
  24. Beta-D-fructofuranoside fructohydrolase from yeast.
    Methods Enzymol. 1975;42:504-11 PMID: 237205
  25. Increase in chitin as an essential response to defects in assembly of cell wall polymers in the ggp1delta mutant of Saccharomyces cerevisiae.
    J Bacteriol. 1997 Jan;179(2):463-9 PMID: 8990299
  26. SLK1, a yeast homolog of MAP kinase activators, has a RAS/cAMP-independent role in nutrient sensing.
    Mol Gen Genet. 1994 May 10;243(3):286-96 PMID: 8190082
  27. 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
  28. BED1, a gene encoding a galactosyltransferase homologue, is required for polarized growth and efficient bud emergence in Saccharomyces cerevisiae.
    J Cell Biol. 1996 Jan;132(1-2):137-51 PMID: 8567719
  29. Prediction and analysis of coiled-coil structures.
    Methods Enzymol. 1996;266:513-25 PMID: 8743703
  30. Localization of proteins to the Golgi apparatus.
    Trends Cell Biol. 1998 Jan;8(1):11-5 PMID: 9695801
  31. HKR1 encodes a cell surface protein that regulates both cell wall beta-glucan synthesis and budding pattern in the yeast Saccharomyces cerevisiae.
    J Bacteriol. 1996 Jan;178(2):477-83 PMID: 8550469
  32. Isolation of new temperature-sensitive mutants of Saccharomyces cerevisiae deficient in mannose outer chain elongation.
    Yeast. 1992 Jul;8(7):535-47 PMID: 1523886
  33. Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae.
    Yeast. 1995 Oct;11(13):1265-74 PMID: 8553697
  34. 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
  35. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer.
    Curr Biol. 1996 Feb 1;6(2):178-82 PMID: 8673464
  36. The SPA2 protein of yeast localizes to sites of cell growth.
    J Cell Biol. 1989 Apr;108(4):1419-29 PMID: 2647769
  37. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles.
    J Cell Biol. 1991 May;113(3):539-51 PMID: 2016335
  38. Yeast actin cytoskeleton mutants accumulate a new class of Golgi-derived secretary vesicle.
    Mol Biol Cell. 1997 Aug;8(8):1481-99 PMID: 9285820
  39. CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae.
    J Cell Biol. 1991 Jul;114(1):101-9 PMID: 2050737
  40. Multi-protein complexes in the cis Golgi of Saccharomyces cerevisiae with alpha-1,6-mannosyltransferase activity.
    EMBO J. 1998 Jan 15;17(2):423-34 PMID: 9430634
  41. Demonstration of a fibrillar component in the cell wall of the yeast Saccharomyces cerevisiae and its chemical nature.
    J Cell Biol. 1974 Jul;62(1):66-76 PMID: 4135002
  42. Glycoprotein biosynthesis in Saccharomyces cerevisiae: ngd29, an N-glycosylation mutant allelic to och1 having a defect in the initiation of outer chain formation.
    FEBS Lett. 1995 Aug 14;370(1-2):41-5 PMID: 7649302
  43. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  44. Cell wall integrity modulates RHO1 activity via the exchange factor ROM2.
    EMBO J. 1998 Apr 15;17(8):2235-45 PMID: 9545237
  45. Maturation of the yeast plasma membrane [H+]ATPase involves phosphorylation during intracellular transport.
    J Cell Biol. 1991 Oct;115(2):289-95 PMID: 1833410
  46. Location of mannan and chitin on thin sections of budding yeasts with gold markers.
    Arch Microbiol. 1977 Oct 24;115(1):1-7 PMID: 337918
  47. Isolation of new nonconditional Saccharomyces cerevisiae mutants defective in asparagine-linked glycosylation.
    Glycobiology. 1997 Jun;7(4):487-97 PMID: 9184829
  48. Yeast Kex1p is a Golgi-associated membrane protein: deletions in a cytoplasmic targeting domain result in mislocalization to the vacuolar membrane.
    J Cell Biol. 1992 Dec;119(6):1459-68 PMID: 1469044
  49. Order of events in the yeast secretory pathway.
    Cell. 1981 Aug;25(2):461-9 PMID: 7026045
  50. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1991 May;113(3):527-38 PMID: 2016334
  51. Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae.
    Microbiol Rev. 1995 Sep;59(3):345-86 PMID: 7565410
  52. The hypo-osmolarity-sensitive phenotype of the Saccharomyces cerevisiae hpo2 mutant is due to a mutation in PKC1, which regulates expression of beta-glucanase.
    Mol Gen Genet. 1994 Mar;242(6):641-8 PMID: 8152414
  53. Altered extent of cross-linking of beta1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall beta1,3-glucan content.
    J Bacteriol. 1997 Oct;179(20):6279-84 PMID: 9335273
  54. A yeast protein similar to bacterial two-component regulators.
    Science. 1993 Oct 22;262(5133):566-9 PMID: 8211183
  55. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1858-62 PMID: 377286
  56. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 Jul 11;21(14):3329-30 PMID: 8341614
  57. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1981 Jun;89(3):395-405 PMID: 7019215
  58. Identification of the bud emergence gene BEM4 and its interactions with rho-type GTPases in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Aug;16(8):4387-95 PMID: 8754839
  59. Role of small G proteins in yeast cell polarization and wall biosynthesis.
    Annu Rev Biochem. 1998;67:307-33 PMID: 9759491
  60. The syntaxin Tlg1p mediates trafficking of chitin synthase III to polarized growth sites in yeast.
    Mol Biol Cell. 1998 Dec;9(12):3383-97 PMID: 9843576
  61. The septins: roles in cytokinesis and other processes.
    Curr Opin Cell Biol. 1996 Feb;8(1):106-19 PMID: 8791410
  62. The Spa2-related protein, Sph1p, is important for polarized growth in yeast.
    J Cell Sci. 1998 Feb;111 ( Pt 4):479-94 PMID: 9443897
  63. Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae.
    Genetics. 1997 Oct;147(2):435-50 PMID: 9335584
  64. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.
    Cell. 1980 Aug;21(1):205-15 PMID: 6996832
  65. The Saccharomyces cerevisiae protein Mnn10p/Bed1p is a subunit of a Golgi mannosyltransferase complex.
    J Biol Chem. 1999 Mar 5;274(10):6579-85 PMID: 10037752
  66. Effect of calcofluor white on chitin synthases from Saccharomyces cerevisiae.
    J Bacteriol. 1988 Apr;170(4):1945-9 PMID: 2965145
  67. MNN6, a member of the KRE2/MNT1 family, is the gene for mannosylphosphate transfer in Saccharomyces cerevisiae.
    J Biol Chem. 1997 Jul 18;272(29):18117-24 PMID: 9218445
  68. A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white.
    Yeast. 1994 Aug;10(8):1019-30 PMID: 7992502
  69. Cloning of genes related to exo-beta-glucanase production in Saccharomyces cerevisiae: characterization of an exo-beta-glucanase structural gene.
    Gene. 1986;47(2-3):245-59 PMID: 3104142
  70. SBF cell cycle regulator as a target of the yeast PKC-MAP kinase pathway.
    Science. 1997 Mar 21;275(5307):1781-4 PMID: 9065400
  71. A two-component system that regulates an osmosensing MAP kinase cascade in yeast.
    Nature. 1994 May 19;369(6477):242-5 PMID: 8183345
  72. CHS5, a gene involved in chitin synthesis and mating in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 May;17(5):2485-96 PMID: 9111317
  73. Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p.
    J Cell Biol. 1997 Jan 13;136(1):95-110 PMID: 9008706
  74. 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
  75. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  76. Components required for cytokinesis are important for bud site selection in yeast.
    J Cell Biol. 1993 Jul;122(2):373-86 PMID: 8320260
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2000-02-00
Pages
435-52
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC14784
Subset
IM
Grants
NIGMS NIH HHS · R01 GM036494 · United States
NIGMS NIH HHS · GM36494 · 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