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PMID: 8755864 Published · ppublish English Comparative Study Journal Article

Isolation of a gene involved in 1,3-beta-glucan synthesis in Aspergillus nidulans and purification of the corresponding protein.

Journal of bacteriology ·Vol. 178 ·No. 15 ·1996-08-00 ·Pages 4381-91

Kelly R, Register E, Hsu MJ, Kurtz M, Nielsen J

Abstract

Saccharomyces cerevisiae has two highly homologous genes, FKS1 and FKS2, which encode interchangeable putative catalytic subunits of 1,3-beta-glucan synthase (GS), an enzyme that synthesizes an essential polymer of the fungal cell wall. To determine if GS in Aspergillus species is similar, an FKS homolog, fksA, was cloned from Aspergillus nidulans by cross-hybridization, and the corresponding protein was purified. Sequence analysis revealed a 5,716-nucleotide coding region interrupted by two 56-bp introns. The fksA gene encodes a predicted peptide of 229 kDa, FksAp, that shows a remarkable degree of conservation in size, charge, amino acid identity, and predicted membrane topology with the S. cerevisiae FKS proteins (Fksps). FksAp exhibits 64 and 65% identity to Fks1p and Fks2p, respectively, and 79% similarity. Hydropathy analysis of FksAp suggests an integral membrane protein with 16 transmembrane helices that coincide with the transmembrane helices of the Saccharomyces Fksps. The sizes of the nontransmembrane domains are strikingly similar to those of Fks1p. The region of FksAp most homologous to the Saccharomyces FKS polypeptides is a large hydrophilic domain of 578 amino acids that is predicted to be cytoplasmic. This domain is 86% identical to the corresponding region of Fks1p and is a good candidate for the location of the catalytic site. Antibodies raised against a peptide derived from the FksAp sequence recognize a protein of approximately 200 kDa in crude membranes and detergent-solubilized active extracts. This protein is enriched approximately 300-fold in GS purified by product entrapment. Purified anti-FksAp immunoglobulin G immunodepletes nearly all of the GS activity in crude or purified extracts when Staphylococcus aureus cells are used to precipitate the antibodies, although it does not inhibit enzymatic activity when added to extracts. The purified GS is inhibited by echinocandins with a sensitivity equal to that displayed by whole cells. Thus, the product of fksA is important for the activity of highly purified preparations of GS, either as the catalytic subunit itself or as an associated copurifying subunit that mediates susceptibility of enzymatic activity to echinocandin inhibition.

MeSH Terms
Amino Acid Sequence Aspergillus nidulans/drug effects,genetics,metabolism Base Sequence DNA, Fungal/genetics Echinocandins Enzyme Stability Fungal Proteins/genetics Genes, Fungal/drug effects Glucans/biosynthesis Glucosyltransferases/genetics,isolation & purification,metabolism Hot Temperature Membrane Proteins/genetics Molecular Sequence Data Peptides, Cyclic/pharmacology Precipitin Tests Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins Sequence Homology, Amino Acid Species Specificity beta-Glucans
Chemicals
DNA, Fungal Echinocandins Fungal Proteins Glucans Membrane Proteins Peptides, Cyclic Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins beta-Glucans beta-1,3-glucan Glucosyltransferases 1,3-beta-glucan synthase FKS1 protein, S cerevisiae GSC2 protein, S cerevisiae
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kelly R
Infectious Disease Research, Merck and Co., Rahway, New Jersey 07065, USA.
Register E
Hsu M J
Kurtz M
Nielsen J
References (49)
49 references, click to expand
  1. A zinc finger protein from Candida albicans is involved in sucrose utilization.
    J Bacteriol. 1992 Jan;174(1):222-32 PMID: 1729210
  2. Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum.
    Plant Mol Biol. 1990 Nov;15(5):673-83 PMID: 2151718
  3. An Aspergillus fumigatus alkaline protease mutant constructed by gene disruption is deficient in extracellular elastase activity.
    Mol Microbiol. 1992 Jun;6(12):1663-71 PMID: 1495393
  4. Vectors for generating nested deletions and facilitating subcloning G+C-rich DNA between Escherichia coli and Streptomyces sp.
    Gene. 1992 Sep 21;119(1):149-50 PMID: 1398085
  5. Antipneumocystis activity of water-soluble lipopeptide L-693,989 in rats.
    Antimicrob Agents Chemother. 1992 Sep;36(9):1964-70 PMID: 1416888
  6. Pneumocandins from Zalerion arboricola. I. Discovery and isolation.
    J Antibiot (Tokyo). 1992 Dec;45(12):1853-66 PMID: 1490876
  7. Predicting the topology of eukaryotic membrane proteins.
    Eur J Biochem. 1993 May 1;213(3):1333-40 PMID: 8099327
  8. Synthesis and antifungal activity of novel cationic pneumocandin B(o) derivatives.
    J Med Chem. 1994 Jan 21;37(2):222-5 PMID: 8295208
  9. Characterization of the 1,3-beta-glucan synthase of Aspergillus fumigatus.
    J Gen Microbiol. 1993 Dec;139(12):3071-8 PMID: 8126434
  10. Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution.
    Microbiol Rev. 1994 Mar;58(1):71-93 PMID: 8177172
  11. Characterization and cilofungin inhibition of solubilized Aspergillus fumigatus (1,3)-beta-D-glucan synthase.
    Antimicrob Agents Chemother. 1994 May;38(5):937-44 PMID: 8067773
  12. A Saccharomyces cerevisiae mutant with echinocandin-resistant 1,3-beta-D-glucan synthase.
    J Bacteriol. 1994 Sep;176(18):5686-96 PMID: 8083161
  13. (1,3) beta-Glucan synthase activity of Neurospora crassa: identification of a substrate-binding protein.
    Biochim Biophys Acta. 1994 Nov 11;1201(2):312-20 PMID: 7947947
  14. Morphological effects of lipopeptides against Aspergillus fumigatus correlate with activities against (1,3)-beta-D-glucan synthase.
    Antimicrob Agents Chemother. 1994 Jul;38(7):1480-9 PMID: 7979276
  15. A GTP-binding protein regulates the activity of (1-->3)-beta-glucan synthase, an enzyme directly involved in yeast cell wall morphogenesis.
    J Biol Chem. 1994 Dec 9;269(49):31267-74 PMID: 7983071
  16. Review: cell wall assembly in yeast.
    Yeast. 1994 Jul;10(7):851-69 PMID: 7985414
  17. Bidirectional gene transfer between Aspergillus fumigatus and Aspergillus nidulans.
    FEMS Microbiol Lett. 1994 Oct 1;122(3):227-31 PMID: 7988865
  18. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-D-glucan synthase.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12907-11 PMID: 7528927
  19. Identification of two cell cycle regulated genes affecting the beta 1,3-glucan content of cell walls in Saccharomyces cerevisiae.
    FEBS Lett. 1995 Jan 23;358(2):165-70 PMID: 7828729
  20. The yeast FKS1 gene encodes a novel membrane protein, mutations in which confer FK506 and cyclosporin A hypersensitivity and calcineurin-dependent growth.
    Gene. 1994 Dec 30;151(1-2):61-71 PMID: 7530227
  21. Increased antifungal activity of L-733,560, a water-soluble, semisynthetic pneumocandin, is due to enhanced inhibition of cell wall synthesis.
    Antimicrob Agents Chemother. 1994 Dec;38(12):2750-7 PMID: 7695257
  22. Nikkomycin Z supersensitivity of an echinocandin-resistant mutant of Saccharomyces cerevisiae.
    Antimicrob Agents Chemother. 1995 Jan;39(1):200-7 PMID: 7695307
  23. Calcineurin, the Ca2+/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H(+)-ATPase.
    Mol Cell Biol. 1995 Aug;15(8):4103-14 PMID: 7542741
  24. Evaluation of water-soluble pneumocandin analogs L-733560, L-705589, and L-731373 with mouse models of disseminated aspergillosis, candidiasis, and cryptococcosis.
    Antimicrob Agents Chemother. 1995 May;39(5):1077-81 PMID: 7625792
  25. Characterization and gene cloning of 1,3-beta-D-glucan synthase from Saccharomyces cerevisiae.
    Eur J Biochem. 1995 Aug 1;231(3):845-54 PMID: 7649185
  26. Differential expression and function of two homologous subunits of yeast 1,3-beta-D-glucan synthase.
    Mol Cell Biol. 1995 Oct;15(10):5671-81 PMID: 7565718
  27. Papulacandin B resistance in budding and fission yeasts: isolation and characterization of a gene involved in (1,3)beta-D-glucan synthesis in Saccharomyces cerevisiae.
    J Bacteriol. 1995 Oct;177(20):5732-9 PMID: 7592316
  28. Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae.
    Microbiol Rev. 1995 Sep;59(3):345-86 PMID: 7565410
  29. Aerosol and parenteral pneumocandins are effective in a rat model of pulmonary aspergillosis.
    Antimicrob Agents Chemother. 1995 Aug;39(8):1784-9 PMID: 7486919
  30. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis.
    Science. 1996 Apr 12;272(5259):277-9 PMID: 8602514
  31. 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
  32. In vitro activity of 1,3-beta-D-glucan synthase requires the GTP-binding protein Rho1.
    J Biol Chem. 1996 Jun 14;271(24):14604-9 PMID: 8662910
  33. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  34. Regulation of fungal cell wall growth: a guanine nucleotide-binding, proteinaceous component required for activity of (1----3)-beta-D-glucan synthase.
    Proc Natl Acad Sci U S A. 1986 Aug;83(16):5808-12 PMID: 2942941
  35. Progressive sequence alignment as a prerequisite to correct phylogenetic trees.
    J Mol Evol. 1987;25(4):351-60 PMID: 3118049
  36. The unique histone H2A gene of Aspergillus nidulans contains three introns.
    Gene. 1987;58(1):59-66 PMID: 3319784
  37. The antigenic index: a novel algorithm for predicting antigenic determinants.
    Comput Appl Biosci. 1988 Mar;4(1):181-6 PMID: 2454713
  38. Sequences important for gene expression in filamentous fungi.
    Yeast. 1986 Dec;2(4):229-36 PMID: 3333455
  39. Predicting the orientation of eukaryotic membrane-spanning proteins.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5786-90 PMID: 2762295
  40. Identification of lysine 15 at the active site in Escherichia coli glycogen synthase. Conservation of Lys-X-Gly-Gly sequence in the bacterial and mammalian enzymes.
    J Biol Chem. 1990 Feb 5;265(4):2086-90 PMID: 2105316
  41. Identification of the uridine 5'-diphosphoglucose (UDP-Glc) binding subunit of cellulose synthase in Acetobacter xylinum using the photoaffinity probe 5-azido-UDP-Glc.
    J Biol Chem. 1990 Mar 25;265(9):4782-4 PMID: 2138620
  42. Fungal cell wall synthesis: the construction of a biological structure.
    Microbiol Sci. 1988 Dec;5(12):370-5 PMID: 3079180
  43. Treatment of Pneumocystis carinii pneumonia with 1,3-beta-glucan synthesis inhibitors.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5950-4 PMID: 2198575
  44. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  45. Genetic organization of the cellulose synthase operon in Acetobacter xylinum.
    Proc Natl Acad Sci U S A. 1990 Oct;87(20):8130-4 PMID: 2146681
  46. Isolation of the GSY1 gene encoding yeast glycogen synthase and evidence for the existence of a second gene.
    J Biol Chem. 1990 Dec 5;265(34):20879-86 PMID: 2123485
  47. Sequence, organization and expression of the core histone genes of Aspergillus nidulans.
    Mol Gen Genet. 1990 Jul;222(2-3):416-24 PMID: 2274040
  48. Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans.
    Nucleic Acids Res. 1991 Jun 11;19(11):3105-9 PMID: 2057366
  49. Characterization of Aspergillus nidulans mutants deficient in cell wall chitin or glucan.
    J Bacteriol. 1992 Jan;174(2):377-83 PMID: 1729232
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-08-00
Pages
4381-91
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC178203
Subset
IM
Databases
GENBANK
U51272
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