Vacuolar H +-ATPase plays a key role in cell wall biosynthesis of Aspergillus niger

Fungal Genetics and Biology

Volumn 49, Issue 4, 2012, Pages 284-293

  Schachtschabel, Doreen ^a   Arentshorst, Mark ^a   Lagendijk, Ellen L ^a   Ram, Arthur F J ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

Aspergillus; BafilomycinB 1; Cell wall; Stress response; V ATPase; Vacuole

Indexed keywords

ADENOSINE TRIPHOSPHATE; BAFILOMYCIN B1; CARBOXY TERMINAL TELOPEPTIDE; CASPOFUNGIN; MEPACRINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; ZINC ION;

ACIDIFICATION; AGSA GENE; ALLELE; ARTICLE; ASPERGILLUS NIGER; BIOSYNTHESIS; CELL VACUOLE; CELL WALL; CELLULAR STRESS RESPONSE; CODON; CONTROLLED STUDY; ENZYME ACTIVITY; FKSA GENE; FUNGAL CELL; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE MUTATION; GENETIC ANALYSIS; GENETIC COMPLEMENTATION; GENETIC REGULATION; HEAT SENSITIVITY; NONHUMAN; PHENOTYPE; PHIA GENE; PRIORITY JOURNAL; PROTON TRANSPORT; VMAD GENE;

AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; ASPERGILLUS NIGER; CELL WALL; ECHINOCANDINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENETIC COMPLEMENTATION TEST; GENETIC LOCI; HYPHAE; MACROLIDES; MOLECULAR SEQUENCE DATA; PHENOTYPE; POINT MUTATION; PROTON-TRANSLOCATING ATPASES; SEQUENCE ALIGNMENT; SEQUENCE DELETION; STRESS, PHYSIOLOGICAL; VACUOLES;

ASPERGILLUS; ASPERGILLUS NIGER; EUKARYOTA;

EID: 84859002520     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.12.008     Document Type: Article

References (63)

1. +-ATPase. Yeast 1993, 9:175-184.
2. Bagar T., Altenbach K., Read N.D., Bencina M. Live-Cell imaging and measurement of intracellular pH in filamentous fungi using a genetically encoded ratiometric probe. Eukaryot. Cell 2009, 8:703-712.
3. +-ATPase membrane sector. J. Biol. Chem. 1993, 268:12749-12757.
4. Bennett J.W., Lasure L.L. Growth media. More Gene Manipulations in Fungi 1991, 441-458. Academic Press, San Diego. J.W. Bennett, L.L. Lasure (Eds.).
5. Bernard M., Latge J.P. Aspergillus fumigatus cell wall: composition and biosynthesis. Med. Mycol. 2001, 39:9-17.
6. Borges-Walmsley M.I., Chen D.L., Shu X.H., Walmsley A.R. The pathobiology of Paracoccidioides brasiliensis. Trends Microbiol. 2002, 10:80-87.
7. Bos C.J., Debets A.J., Swart K., Huybers A., Kobus G., Slakhorst S.M. Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger. Curr. Genet. 1988, 14:437-443.
8. Bowman E.J., Siebers A., Altendorf K. Bafilomycins - a class of inhibitors of membrane ATPases form microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 1988, 85:7972-7976.
9. +-ATPase, causes severe morphological changes in Neurospora crassa. J. Biol. Chem. 2000, 275:167-176.
10. Carvalho N., Arentshorst M., Kwon M.J., Meyer V., Ram A.F.J. Expanding the ku70 toolbox for filamentous fungi: establishment of complementation vectors and recipient strains for advanced gene analyses. Appl. Microbiol. Biotechnol. 2010, 87:1463-1473.
11. Cipriano D.J., Wang Y., Bond S., Hinton A., Jefferies K.C., Qi J., Forgac M. Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta-Bioenerg. 2008, 1777:599-604.
12. Damveld R.A., Arentshorst M., Franken A., vanKuyk P.A., Klis F.M., van den Hondel C.A., Ram A.F. The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol. Microbiol. 2005, 58:305-319.
13. Damveld R.A., vanKuyk P.A., Arentshorst M., Klis F.M., Van den Hondel C.A., Ram A.F. Expression of agsA, one of five 1,3-alpha-d-glucan synthase-encoding genes in Aspergillus niger, is induced in response to cell wall stress. Fungal Genet. Biol. 2005, 42:165-177.
14. Damveld R.A., Franken A., Arentshorst M., Punt P.J., Klis F.M., van den Hondel C.A., Ram A.F. A novel screening method for cell wall mutants in Aspergillus niger identifies UDP-galactopyranose mutase as an important protein in fungal cell wall biosynthesis. Genetics 2008, 178:873-881.
15. de Ruiter-Jacobs Y.M., Broekhuijsen M., Unkles S.E., Campbell E.I., Kinghorn J.R., Contreras R., Pouwels P.H., van den Hondel C.A. A gene-transfer system based on the homologues pyrG genes and efficient expression of bacterial genes in Aspergillus oryzae. Curr. Genet. 1989, 16:159-163.
16. Drose S., Bindseil K.U., Bowman E.J., Siebers A., Zeeck A., Altendorf K. Inhibitory effect of modified bafilomycins and concanamycins on P-type and V-type adenosine-triphosphatases. Biochemistry 1993, 32:3902-3906.
17. +-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism. Mol. Gen. Genet. 1993, 241:447-456.
18. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 2007, 8:917-929.
19. Franzot S.P., Casadevall A. Pneumocandin L-743, 872 enhances the activities of amphotericin B and fluconazole against Cryptococcus neoformans in vitro. Antimicrobiol. Agents Chemother. 1997, 41:331-336.
20. Gastebois A., Clavaud C., Aimanianda V., Latgé J.P. Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Fut. Microbiol. 2009, 4:583-595.
21. Gomori G. Histochemical demonstration of sites of choline esterase activity. Proc. Soc. Exp. Biol. Med. 1948, 68:354-358.
22. Inoue H., Nojima H., Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene 1990, 96:23-28.
23. Kelly J.M., Hynes M.J. Transformation of Aspergillus niger by the amdS gene of Aspergillus nidulans. EMBO J. 1985, 4:475-479.
24. Klis F.M., Mol P., Hellingwerf K., Brul S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2002, 26:239-256.
25. Klis F.M., Boorsma A., De Groot P.W.J. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202.
26. +-ATPase during alkaline pH mediated growth of Aspergillus oryzae. FEMS Microbiol. Lett. 2002, 209:277-282.
27. Lagorce A., Hauser N.C., Labourdette D., Rodriguez C., Martin-Yken H., Arroyo J., Hoheisel J.D., François J. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:20345-20357.
28. Loussert C., Schmitt C., Prevost M.C., Balloy V., Fadel E., Philippe B., Kauffmann-Lacroix C., Latgé J.P., Beauvais A. In vivo biofilm composition of Aspergillus fumigatus. Cell. Microbiol. 2010, 12:405-410.
29. Marcireau C., Guilloton M., Karst F. In vivo effects of fenpropimorph on yeast Saccharomyces cerevisiae and determination of the molecular basis of antifungal property. Antimicrobiol. Agents Chemother. 1990, 34:989-993.
30. McIlvaine T.C. A buffer solution for colorimetric comparison. J. Biol. Chem. 1921, 49:183-186.
31. Melin P., Schnürer J., Wagner E.G.H. Changes in Aspergillus nidulans gene expression induced by bafilomycin, a Streptomyces-produced antibiotic. Microbiology 1999, 145:1115-1122.
32. Melin P., Schnürer J., Wagner E.G.H. Disruption of the gene encoding the V-ATPase subunit A results in inhibition of normal growth and abolished sporulation in Aspergillus nidulans. Microbiol.-Sgm. 2004, 150:743-748.
33. Merzendorfer H., Reineke S., Zhao X.F., Jacobmeier B., Harvey W.R., Wieczorek H. The multigene family of the tobacco hornworm V-ATPase: novel subunits A, C, D, H, and putative isoforms. Biochem. Biophys. Acta-Biomem. 2000, 1467:369-379.
34. Meyer V., Damveld R.A., Arentshorst M., Stahl U., van den Hondel C.A., Ram A.F. Survival in the presence of antifungals - Genome-wide expression profiling of Aspergillus niger in response to sublethal concentrations of caspofungin and fenpropimorph. J. Biol. Chem. 2007, 282:32935-32948.
35. Meyer V., Ram A.F., Punt P.J. Genetics, genetic manipulation and approaches to strain improvement of filamentous fungi. Manual of Industrial Microbiology and Biotechnology 2010, 318-329. Wiley, NY. third ed. A.L. Demain, J. Davis (Eds.).
36. Miura G.I., Froelick G.J., Marsh D.J., Stark K.L., Palmiter R.D. The d subunit of the vacuolar ATPase (Atp6d) is essential for embryonic development. Transgenic Res. 2003, 12:131-133.
37. Netea M.G., Gow N.A., Munro C.A., Bates S., Collins C., Ferwerda G., Hobson R.P., Bertram G., Hughes H.B., Jansen T., Jacobs L., Buurman E.T., Gijzen K., Williams D.L., Torensma R., McKinnon A., MacCallum D.M., Odds F.C., Van der Meer J.W., Brown A.J., Kullberg B.J. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 2006, 116:1642-1650.
38. +-ATPases - nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 2002, 3:94-103.
39. Nishi T., Nishi S.K., Forgac M. Expression and function of the mouse V-ATPase d subunit isoforms. J. Biol. Chem. 2003, 278:46396-46402.
40. Ostling S., Virtama P. A modified preparation of the universal buffer described by Teorell and Stenhangen. Acta Physiol. Scan. 1946, 11:289-293.
41. Owegi M.A., Pappas D.L., Finch M.W., Bilbo S.A., Resendiz C.A., Jacquemin L.J., Warrier A., Trombley J.D., McCulloch K.M., Margalef K.L., Mertz M.J., Storms J.M., Damin C.A., Parra K.J. Identification of a domain in the V0 subunit d that is critical for coupling of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 2006, 281:30001-30014.
42. Perzov N., Padler-Karavani V., Nelson H., Nelson N. Characterization of yeast V-ATPase mutants lacking Vph1p or Stv1p and the effect on endocytosis. J. Exp. Biol. 2002, 205:1209-1219.
43. Poltermann S., Nguyen M., Günther J., Wendland J., Härtl A., Künkel W., Zipfel P.F., Eck R. The putative vacuolar ATPase subunit Vma7p of Candida albicans is involved in vacuole acidification, hyphal development and virulence. Microbiol. Sgm. 2005, 151:1645-1655.
44. Punt P.J., Schuren F.H., Lehmbeck J., Christensen T., Hjort C., van den Hondel C.A. Characterization of the Aspergillus niger prtT, a unique regulator of extracellular protease encoding genes. Fungal Genet. Biol. 2008, 45:1591-1599.
45. Ram A.F., Klis F.M. Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat. Prot. 2006, 1:2253-2256.
46. Ram A.F., Arentshorst M., Damveld R.A., vanKuyk P.A., Klis F.M., van den Hondel C.A. The cell wall stress response in Aspergillus niger involves increased expression of the glutamine: fructose-6-phosphate amidotrans-ferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiol.-Sgm. 2004, 150:3315-3326.
47. Rispail N., Soanes D.M., Ant C., Czajkowski R., Grünler A., Huguet R., Perez-Nadales E., Poli A., Sartorel E., Valiante V., Yang M., Beffa R., Brakhage A.A., Gow N.A., Kahmann R., Lebrun M.H., Lenasi H., Perez-Martin J., Talbot N.J., Wendland J., Di Pietro A. Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 2009, 46:287-298.
48. Sambade M., Alba M., Smardon A.M., West R.W., Kane P.M. Genomic screen for yeast vacuolar membrane ATPase mutants. Genetics 2005, 170:1539-1551.
49. Sambrook J., Russel D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Habor Laboratory Press, NY.
50. Schumacher K., Krebs M. The V-ATPase: small cargo, large effects. Curr. Opin. Plant Biol. 2010, 13:724-730.
51. Shapiro R.S., Robbins N., Cowen L.E. Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol. Mol. Biol. Rev. 2011, 75:213-267.
52. +-ATPase d2 subunit: molecular characterization, developmental regulation, and localization to specialized proton pumps in kidney and bone. J. Am. Soc. Neph. 2005, 16:1245-1256.
53. Smits G.J., Kapteyn J.C., van den Ende H., Klis F.M. Cell wall dynamics in yeast. Curr. Opin. Microbiol. 1999, 2:348-352.
54. Sun-Wada G.H., Wada Y. Vacuolar-type proton pump ATPases: roles of subunit isoforms in physiology and pathology. Histol. Histopathol. 2010, 25:1611-1620.
55. Sun-Wada G.H., Yoshimizu T., Imai-Senga Y., Wada Y., Futai M. Diversity of mouse proton-translocating ATPase: presence of multiple isoforms of the C, d and G subunits. Gene 2003, 302:147-153.
56. Toei M., Saum R., Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry 2010, 49:4715-4723.
57. van Gorcom R.F., van den Hondel C.A. Expression analysis vectors for Aspergillus niger. Nucl. Acids Res. 1988, 16:9052.
58. van Leeuwen M.R., Smant W., de Boer W., Dijksterhuis J. Filipin is a reliable in situ marker of ergosterol in the plasma membrane of germinating conidia (spores) of Penicillium discolor and stains intensively at the site of germ tube formation. J. Microbiol. Meth. 2008, 74:64-73.
59. Verdoes J.C., Punt P.J., Berg P., Debets F., Stouthamer A.H., van den Hondel C.A. Characterization of an efficient gene cloning strategy for Aspergillus niger based on an autonomously replicating plasmid: cloning of the nicB gene of A. Niger. Gene 1994, 146:159-165.
60. +-ATPase from chromaffin granules. J. Biol. Chem. 1988, 263:17638-17642.
61. Wang K., Ussery D.W., Brunak S. Analysis and prediction of gene splice sites in four Aspergillus genomes. Fungal Genet. Biol. Suppl. 2009, 1:S14-8.
62. Watson P.F., Rose M.E., Ellis S.W., England H., Kelly S.L. Defective sterol C5-6 desaturation and azole resistance. a new hypothesis for the mode of action of azole antifungals. Biochem. Biophys. Res. Commun. 1989, 164:1170-1175.
63. Zhang Y.Q., Gamarra S., Garcia-Effron G., Park S., Perlin D.S., Rao R. Requirement of ergosterol in V-ATPase function underlies antifungal activity of azole drugs. PLoS Path. 2010, 6:13.