Home LiteratureArticle Details
PMID: 14555471 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress.

Eukaryotic cell ·Vol. 2 ·No. 5 ·2003-10-00 ·Pages 886-900

Bulik DA, Olczak M, Lucero HA, Osmond BC, Robbins PW, Specht CA

Abstract

In Saccharomyces cerevisiae most chitin is synthesized by Chs3p, which deposits chitin in the lateral cell wall and in the bud-neck region during cell division. We have recently found that addition of glucosamine (GlcN) to the growth medium leads to a three- to fourfold increase in cell wall chitin levels. We compared this result to the increases in cellular chitin levels associated with cell wall stress and with treatment of yeast with mating pheromone. Since all three phenomena lead to increases in precursors of chitin, we hypothesized that chitin synthesis is at least in part directly regulated by the size of this pool. This hypothesis was strengthened by our finding that addition of GlcN to the growth medium causes a rapid increase in chitin synthesis without any pronounced change in the expression of more than 6,000 genes monitored with Affymetrix gene expression chips. In other studies we found that the specific activity of Chs3p is higher in the total membrane fractions from cells grown in GlcN and from mutants with weakened cell walls. Sucrose gradient analysis shows that Chs3p is present in an inactive form in what may be Golgi compartments but as an active enzyme in other intracellular membrane-bound vesicles, as well as in the plasma membrane. We conclude that Chs3p-dependent chitin synthesis in S. cerevisiae is regulated both by the levels of intermediates of the UDP-GlcNAc biosynthetic pathway and by an increase in the activity of the enzyme in the plasma membrane.

MeSH Terms
Acetylglucosamine/analysis,pharmacology Cell Wall/metabolism Chitin/biosynthesis Chitin Synthase/genetics,metabolism Down-Regulation Fungal Proteins/metabolism Gene Deletion Gene Expression Profiling Gene Expression Regulation, Fungal Genotype Glucosamine/pharmacology Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing)/metabolism Lipoproteins/pharmacology Oligonucleotide Array Sequence Analysis Open Reading Frames/genetics Pheromones Pyrophosphatases/metabolism Saccharomyces cerevisiae/drug effects,genetics,metabolism Saccharomyces cerevisiae Proteins Subcellular Fractions/chemistry Up-Regulation Uridine Diphosphate N-Acetylglucosamine/analysis
Chemicals
Fungal Proteins Lipoproteins MFA2 protein, S cerevisiae Pheromones Saccharomyces cerevisiae Proteins Chitin Uridine Diphosphate N-Acetylglucosamine Chitin Synthase GFA1 protein, S cerevisiae Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing) Pyrophosphatases guanosine-diphosphatase Glucosamine Acetylglucosamine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Bulik Dorota A
Department of Molecular and Cell Biology, School of Dental Medicine, Boston University, Boston, Massachusetts 02118, USA.
Olczak Mariusz
Lucero Hector A
Osmond Barbara C
Robbins Phillips W
Specht Charles A
References (60)
60 references, click to expand
  1. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  2. Structure of the VHS domain of human Tom1 (target of myb 1): insights into interactions with proteins and membranes.
    Biochemistry. 2000 Sep 19;39(37):11282-90 PMID: 10985773
  3. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.
    J Cell Biol. 1996 Nov;135(3):597-610 PMID: 8909536
  4. Functional regulation of glutamine:fructose-6-phosphate aminotransferase 1 (GFAT1) of Drosophila melanogaster in a UDP-N-acetylglucosamine and cAMP-dependent manner.
    Biochem J. 2001 Dec 1;360(Pt 2):401-12 PMID: 11716769
  5. Characterization of the chitin biosynthesis process as a compensatory mechanism in the fks1 mutant of Saccharomyces cerevisiae.
    FEBS Lett. 2000 Jul 28;478(1-2):84-8 PMID: 10922474
  6. Phosphoinositides as regulators in membrane traffic.
    Science. 1996 Mar 15;271(5255):1533-9 PMID: 8599109
  7. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway.
    Mol Biol Cell. 1996 Dec;7(12):1909-19 PMID: 8970154
  8. The PROSITE database, its status in 2002.
    Nucleic Acids Res. 2002 Jan 1;30(1):235-8 PMID: 11752303
  9. 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
  10. The biosynthesis of glucosamine.
    Biochim Biophys Acta. 1953 Sep-Oct;12(1-2):15-22 PMID: 13115409
  11. Chitin synthases in yeast and fungi.
    EXS. 1999;87:55-69 PMID: 10906951
  12. Apparent inhibition of glycoprotein synthesis by S.cerevisiae mating pheromones.
    FEBS Lett. 1985 May 20;184(2):313-7 PMID: 3888669
  13. Functional discovery via a compendium of expression profiles.
    Cell. 2000 Jul 7;102(1):109-26 PMID: 10929718
  14. VHS domain marks a group of proteins involved in endocytosis and vesicular trafficking.
    FEBS Lett. 1998 Dec 4;440(3):255-7 PMID: 9872381
  15. Global analysis of protein activities using proteome chips.
    Science. 2001 Sep 14;293(5537):2101-5 PMID: 11474067
  16. Maintenance of cell integrity in the gas1 mutant of Saccharomyces cerevisiae requires the Chs3p-targeting and activation pathway and involves an unusual Chs3p localization.
    Yeast. 2002 Sep 30;19(13):1113-24 PMID: 12237852
  17. A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins.
    J Cell Biol. 2000 Oct 30;151(3):587-600 PMID: 11062260
  18. Cloning of the glutamine:fructose-6-phosphate amidotransferase gene from yeast. Pheromonal regulation of its transcription.
    J Biol Chem. 1989 May 25;264(15):8753-8 PMID: 2656689
  19. Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions.
    J Bacteriol. 2000 May;182(9):2428-37 PMID: 10762242
  20. Involvement of GFA1, which encodes glutamine-fructose-6-phosphate amidotransferase, in the activation of the chitin synthesis pathway in response to cell-wall defects in Saccharomyces cerevisiae.
    Eur J Biochem. 2002 Mar;269(6):1697-707 PMID: 11895440
  21. Developmental defects associated with glucosamine auxotrophy in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4351-5 PMID: 16592447
  22. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles.
    Science. 2000 Feb 4;287(5454):873-80 PMID: 10657304
  23. 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
  24. The yeast Chs4 protein stimulates the trypsin-sensitive activity of chitin synthase 3 through an apparent protein-protein interaction.
    Microbiology. 2000 Feb;146 ( Pt 2):385-91 PMID: 10708377
  25. Are yeast chitin synthases regulated at the transcriptional or the posttranslational level?
    Mol Cell Biol. 1994 Dec;14(12):7685-94 PMID: 7969112
  26. Sex, stress and integrity: the importance of MAP kinases in yeast.
    Curr Opin Genet Dev. 1994 Feb;4(1):90-5 PMID: 8193546
  27. Glc7p protein phosphatase inhibits expression of glutamine-fructose-6-phosphate transaminase from GFA1.
    J Biol Chem. 2000 Jun 16;275(24):18070-8 PMID: 10764753
  28. Loss of the plasma membrane-bound protein Gas1p in Saccharomyces cerevisiae results in the release of beta1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity.
    J Bacteriol. 1998 Mar;180(6):1418-24 PMID: 9515908
  29. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae.
    Cell Mol Biol Res. 1994;40(3):229-39 PMID: 7874200
  30. Glucosamine metabolism. V. Enzymatic synthesis of glucosamine 6-phosphate.
    J Biol Chem. 1960 May;235:1265-73 PMID: 13827775
  31. A glutamine synthetase mutant of Saccharomyces cerevisiae shows defect in cell wall.
    J Gen Appl Microbiol. 1997 Jun;43(3):157-162 PMID: 12501331
  32. 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
  33. Dynamics of cell wall structure in Saccharomyces cerevisiae.
    FEMS Microbiol Rev. 2002 Aug;26(3):239-56 PMID: 12165426
  34. The genomics of yeast responses to environmental stress and starvation.
    Funct Integr Genomics. 2002 Sep;2(4-5):181-92 PMID: 12192591
  35. A guanosine diphosphatase enriched in Golgi vesicles of Saccharomyces cerevisiae. Purification and characterization.
    J Biol Chem. 1990 Nov 5;265(31):19351-5 PMID: 2172253
  36. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis.
    Mol Cell Biol. 1992 Apr;12(4):1764-76 PMID: 1532231
  37. Functional characterization of the YUR1, KTR1, and KTR2 genes as members of the yeast KRE2/MNT1 mannosyltransferase gene family.
    J Biol Chem. 1996 May 3;271(18):11001-8 PMID: 8631921
  38. Oligomeric structure and regulation of Candida albicans glucosamine-6-phosphate synthase.
    J Biol Chem. 1999 Feb 12;274(7):4000-8 PMID: 9933591
  39. The yeast cell wall and septum as paradigms of cell growth and morphogenesis.
    J Biol Chem. 2001 Jun 8;276(23):19679-82 PMID: 11309404
  40. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway.
    Mol Microbiol. 1999 Dec;34(5):1049-57 PMID: 10594829
  41. Differential regulation of the cell wall integrity mitogen-activated protein kinase pathway in budding yeast by the protein tyrosine phosphatases Ptp2 and Ptp3.
    Mol Cell Biol. 1999 Nov;19(11):7651-60 PMID: 10523653
  42. Subcellular localization of the yeast proteome.
    Genes Dev. 2002 Mar 15;16(6):707-19 PMID: 11914276
  43. Up-regulation of genes encoding glycosylphosphatidylinositol (GPI)-attached proteins in response to cell wall damage caused by disruption of FKS1 in Saccharomyces cerevisiae.
    Mol Gen Genet. 2000 Sep;264(1-2):64-74 PMID: 11016834
  44. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.
    Science. 1999 Aug 6;285(5429):901-6 PMID: 10436161
  45. A nonradioactive, high throughput assay for chitin synthase activity.
    Anal Biochem. 2002 Jun 1;305(1):97-105 PMID: 12018950
  46. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae.
    Nucleic Acids Res. 1990 May 25;18(10):3091-2 PMID: 2190191
  47. A new method for quantitative determination of polysaccharides in the yeast cell wall. Application to the cell wall defective mutants of Saccharomyces cerevisiae.
    Yeast. 1998 Oct;14(14):1297-306 PMID: 9802208
  48. Chitin synthesis in a gas1 mutant of Saccharomyces cerevisiae.
    J Bacteriol. 2000 Sep;182(17):4752-7 PMID: 10940014
  49. Cloning and expression of two chitin deacetylase genes of Saccharomyces cerevisiae.
    Yeast. 1997 Mar 30;13(4):327-36 PMID: 9133736
  50. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins.
    Dev Cell. 2002 Mar;2(3):283-94 PMID: 11879634
  51. 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
  52. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  53. Uridine diphosphate-glucose transport into the endoplasmic reticulum of Saccharomyces cerevisiae: in vivo and in vitro evidence.
    Mol Biol Cell. 1999 Apr;10(4):1019-30 PMID: 10198054
  54. Glucosamine-6-phosphate synthase from Escherichia coli: determination of the mechanism of inactivation by N3-fumaroyl-L-2,3-diaminopropionic derivatives.
    Biochemistry. 1990 Apr 17;29(15):3668-76 PMID: 2111163
  55. Chitin synthase III: synthetic lethal mutants and "stress related" chitin synthesis that bypasses the CSD3/CHS6 localization pathway.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11206-10 PMID: 10500155
  56. Solubilization and partial purification of yeast chitin synthetase. Confirmation of the zymogenic nature of the enzyme.
    J Biol Chem. 1978 Jun 25;253(12):4419-25 PMID: 350873
  57. The genetic complexity of chitin synthesis in fungi.
    Curr Genet. 2002 Sep;41(6):367-78 PMID: 12228806
  58. Localized deposition of chitin on the yeast cell surface in response to mating pheromone.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):645-9 PMID: 16592617
  59. 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
  60. 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
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
Published
2003-10-00
Pages
886-900
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC219353
Subset
IM
Grants
NIGMS NIH HHS · GM31318 · United States
NIGMS NIH HHS · R01 GM031318 · United States
NIAID NIH HHS · AI44070 · United States
NIAID NIH HHS · R01 AI025780 · United States
NIAID NIH HHS · AI25780 · United States
NIAID NIH HHS · R01 AI044070 · 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]