Trehalose 6-phosphate phosphatase is required for cell wall integrity and fungal virulence but not trehalose biosynthesis in the human fungal pathogen Aspergillus fumigatus

Molecular Microbiology

Volumn 77, Issue 4, 2010, Pages 891-911

  Puttikamonkul, Srisombat ^a   Willger, Sven D ^a   Grahl, Nora ^a   Perfect, John R ^b   Movahed, Navid ^a   Bothner, Brian ^a   Park, Steven ^c   Paderu, Padmaja ^c   Perlin, David S ^c   Cramer Jr , Robert A ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HEXOKINASE; MUTANT PROTEIN; OSMOTIC AGENT; PHOSPHATASE; TREHALOSE; TREHALOSE 6 PHOSPHATE PHOSPHATASE; UNCLASSIFIED DRUG; CULTURE MEDIUM; TREHALOSE-PHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASEXUAL REPRODUCTION; ASPERGILLUS FUMIGATUS; BIOACCUMULATION; BIOSYNTHESIS; CELL DESTRUCTION; CELL WALL; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE MUTATION; INCUBATION TEMPERATURE; LUNG ASPERGILLOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; DISEASE MODEL; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INVASIVE ASPERGILLOSIS; LUNG; METABOLISM; MICROBIOLOGY; MUTATION; PATHOLOGY; SURVIVAL ANALYSIS; VIRULENCE;

ASPERGILLUS FUMIGATUS; MURINAE;

ANIMALS; ASPERGILLUS FUMIGATUS; CELL WALL; CULTURE MEDIA; DISEASE MODELS, ANIMAL; INVASIVE PULMONARY ASPERGILLOSIS; LUNG; MICE; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; SURVIVAL ANALYSIS; TREHALOSE; VIRULENCE;

EID: 77955405132     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07254.x     Document Type: Article

References (82)

1. Aisaka, K. Masuda, T. (1995) Production of trehalose phosphorylase by Catellatospora ferruginea. FEMS Microbiol Lett 131 : 47 51.
2. Aisaka, K., Masuda, T., Chikamune, T. Kamitori, K. (1998) Purification and characterization of trehalose phosphorylase from Catellatospora ferruginea. Biosci Biotechnol Biochem 62 : 782 787.
3. Al-Bader, N., Vanier, G., Liu, H., Gravelat, F.N., Urb, M., Hoareau, C.M., et al. (2010) The role of trehalose biosynthesis in Aspergillus fumigatus development, stress response and virulence. Infect Immun doi:10.1128/IAI.00813- 09.
4. Anderson, P.J., Karageuzian, L.N., Cheng, H.M. Epstein, D.L. (1984) Hexokinase of calf trabecular meshwork. Invest Ophthalmol Vis Sci 25 : 1258 1261.
5. Aufauvre-Brown, A., Mellado, E., Gow, N.A.R. Holden, D.W. (1997) Aspergillus fumigatus chsE: a gene related to CHS3 of saccharomyces cerevisiae and important for hyphal growth and conidiophore development but not pathogenicity. Fungal Genet Biol 21 : 141 152.
6. Avonce, N., Mendoza-Vargas, A., Morett, E. Iturriaga, G. (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6 : 109 123.
7. Bell, W., Sun, W., Hohmann, S., Wera, S., Reinders, A., De Virgilio, C., et al. (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273 : 33311 33319.
8. Belocopitow, E. Marechal, L.R. (1970) Trehalose phosphorylase from Euglena gracilis. Biochim Biophys Acta 198 : 151 154.
9. Belocopitow, E. Marechal, L.R. (1974) Metabolism of trehalose in Euglena gracilis. Partial purification and some properties of phosphoglucomutase acting on beta-glucose 1-phosphate. Eur J Biochem 46 : 631 637.
10. Bergmeyer, H.U., Grassl, M. Walter, H.E. (1983) Hexokinase. In Methods of Enzymatic Analysis, Vol. II, 3rd edn. Bergmeyer, H.U. (ed.). Deerfield Beach, FL : Verlag Chemie, pp. 222 223.
11. Bernard, M. Latge, J.P. (2001) Aspergillus fumigatus cell wall: composition and biosynthesis. Med Mycol 39 (Suppl. 1 9 17.
12. Blazquez, M.A., Lagunas, R., Gancedo, C. Gancedo, J.M. (1993) Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett 329 : 51 54.
13. Blazquez, M.A., Stucka, R., Feldmann, H. Gancedo, C. (1994) Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. J Bacteriol 176 : 3895 3902.
14. Borgia, P.T. Dodge, C.L. (1992) Characterization of Aspergillus nidulans mutants deficient in cell wall chitin or glucan. J Bacteriol 174 : 377 383.
15. Borgia, P.T., Miao, Y. Dodge, C.L. (1996) The orlA gene from Aspergillus nidulans encodes a trehalose-6-phosphate phosphatase necessary for normal growth and chitin synthesis at elevated temperatures. Mol Microbiol 20 : 1287 1296.
16. Brun, Y.F., Dennis, C.G., Greco, W.R., Bernacki, R.J., Pera, P.J., Bushey, J.J., et al. (2007) Modeling the combination of amphotericin B, micafungin, and nikkomycin Z against Aspergillus fumigatus in vitro using a novel response surface paradigm. Antimicrob Agents Chemother 51 : 1804 1812.
17. Cabib, E. Leloir, L.F. (1958) The biosynthesis of trehalose phosphate. J Biol Chem 231 : 259 275.
18. Cao, Y., Wang, Y., Dai, B., Wang, B., Zhang, H., Zhu, Z., et al. (2008) Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol Pharm Bull 31 : 421 425.
19. Cramer, R.A., Jr., Gamcsik, M.P., Brooking, R.M., Najvar, L.K., Kirkpatrick, W.R., Patterson, T.F., et al. (2006) Disruption of a nonribosomal peptide synthetase in Aspergillus fumigatus eliminates gliotoxin production. Eukaryot Cell 5 : 972 980.
20. Cramer, R.A., Jr., Perfect, B.Z., Pinchai, N., Park, S., Perlin, D.S., Asfaw, Y.G., et al. (2008) Calcineurin target CrzA regulates conidial germination, hyphal growth, and pathogenesis of Aspergillus fumigatus. Eukaryot Cell 7 : 1085 1097.
21. Crowe, J.H., Hoekstra, F.A. Crowe, L.M. (1992) Anhydrobiosis. Annu Rev Physiol 54 : 579 599.
22. De Virgilio, C., Burckert, N., Bell, W., Jeno, P., Boller, T. Wiemken, A. (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212 : 315 323.
23. Eis, C. Nidetzky, B. (1999) Characterization of trehalose phosphorylase from Schizophyllum commune. Biochem J 341 (Part 2 385 393.
24. Ejzykowicz, D.E., Cunha, M.M., Rozental, S., Solis, N.V., Gravelat, F.N., Sheppard, D.C. Filler, S.G. (2009) The Aspergillus fumigatus transcription factor Ace2 governs pigment production, conidiation and virulence. Mol Microbiol 72 : 155 169.
25. Elbein, A.D., Pan, Y.T., Pastuszak, I. Carroll, D. (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13 : R17 R27.
26. Elliott, B., Haltiwanger, R.S. Futcher, B. (1996) Synergy between trehalose and Hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 144 : 923 933.
27. d'Enfert, C. (1996) Selection of multiple disruption events in Aspergillus fumigatus using the orotidine-5′-decarboxylase gene, pyrG, as a unique transformation marker. Curr Genet 30 : 76 82.
28. d'Enfert, C. Fontaine, T. (1997) Molecular characterization of the Aspergillus nidulans treA gene encoding an acid trehalase required for growth on trehalose. Mol Microbiol 24 : 203 216.
29. Erjavec, Z., Kluin-Nelemans, H. Verweij, P.E. (2009) Trends in invasive fungal infections, with emphasis on invasive aspergillosis. Clin Microbiol Infect 15 : 625 633.
30. Fillinger, S., Chaveroche, M.K., van Dijck, P., de Vries, R., Ruijter, G., Thevelein, J. d'Enfert, C. (2001) Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147 : 1851 1862. (Pubitemid 32684927)
31. Flipphi, M., Sun, J., Robellet, X., Karaffa, L., Fekete, E., Zeng, A.P. Kubiecek, C.P. (2009) Biodiversity and evolution of primary carbon metabolism in Aspergillus nidulans and other Aspergillus spp. Fungal Genet Biol 46 (Suppl. 1 S19 S44.
32. Foster, A.J., Jenkinson, J.M. Talbot, N.J. (2003) Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J 22 : 225 235.
33. Gancedo, C. Flores, C.L. (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4 : 351 359.
34. Han, S.E., Kwon, H.B., Lee, S.B., Yi, B.Y., Murayama, I., Kitamoto, Y. Byun, M.O. (2003) Cloning and characterization of a gene encoding trehalose phosphorylase (TP) from Pleurotus sajor-caju. Protein Expr Purif 30 : 194 202.
35. Harris, J.L. (1986) Modified method for fungal slide culture. J Clin Microbiol 24 : 460 461.
36. Hottiger, T., De Virgilio, C., Hall, M.N., Boller, T. Wiemken, A. (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur J Biochem 219 : 187 193.
37. Huppert, M., Oliver, D.J. Sun, S.H. (1978) Combined methenamine-silver nitrate and hematoxylin & eosin stain for fungi in tissues. J Clin Microbiol 8 : 598 603.
38. Ishihara, R., Taketani, S., Sasai-Takedatsu, M., Adachi, Y., Kino, M., Furuya, A., et al. (2000) ELISA for urinary trehalase with monoclonal antibodies: a technique for assessment of renal tubular damage. Clin Chem 46 : 636 643.
39. Johnson, E.A. (1946) An Improved Slide Culture Technique for the Study and Identification of Pathogenic Fungi. J Bacteriol 51 : 689 694.
40. Kandror, O., DeLeon, A. Goldberg, A.L. (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99 : 9727 9732.
41. Kane, S.M. Roth, R. (1974) Carbohydrate metabolism during ascospore development in yeast. J Bacteriol 118 : 8 14.
42. Kaur, R., Ma, B. Cormack, B.P. (2007) A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci USA 104 : 7628 7633.
43. Kitamoto, Y., Osaki, N., Tanaka, H., Sasaki, H. Mori, N. (2000) Purification and properties of a-glucose 1-phosphate-forming trehalose phosphorylase from basidiomycete, Pleurotus ostreatus. Mycoscience 41 : 607 613.
44. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 : 402 408.
45. Lockington, R.A., Borlace, G.N. Kelly, J.M. (1997) Pyruvate decarboxylase and anaerobic survival in Aspergillus nidulans. Gene 191 : 61 67.
46. Lunn, J.E., Feil, R., Hendriks, J.H., Gibon, Y., Morcuende, R., Osuna, D., et al. (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397 : 139 148.
47. Mabey, J.E., Anderson, M.J., Giles, P.F., Miller, C.J., Attwood, T.K., Paton, N.W., et al. (2004) CADRE: the Central Aspergillus Data REpository. Nucleic Acids Res 32 : D401 D405.
48. Mellado, E., Aufauvre-Brown, A., Gow, N.A. Holden, D.W. (1996) The Aspergillus fumigatus chsC and chsG genes encode class III chitin synthases with different functions. Mol Microbiol 20 : 667 679.
49. Mellado, E., Dubreucq, G., Mol, P., Sarfati, J., Paris, S., Diaquin, M., et al. (2003) Cell wall biogenesis in a double chitin synthase mutant (chsG-/chsE-) of Aspergillus fumigatus. Fungal Genet Biol 38 : 98 109.
50. Morgenstern, D.E., Gifford, M.A., Li, L.L., Doerschuk, C.M. Dinauer, M.C. (1997) Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J Exp Med 185 : 207 218.
51. Munro, C.A. Gow, N.A. (2001) Chitin synthesis in human pathogenic fungi. Med Mycol 39 (Suppl. 1 41 53.
52. Murray, I.A., Coupland, K., Smith, J.A., Ansell, I.D. Long, R.G. (2000) Intestinal trehalase activity in a UK population: establishing a normal range and the effect of disease. Br J Nutr 83 : 241 245.
53. Ngamskulrungroj, P., Himmelreich, U., Breger, J.A., Wilson, C., Chayakulkeeree, M., Krockenberger, M.B., et al. (2009) The trehalose synthesis pathway is an integral part of the virulence composite for Cryptococcus gattii. Infect Immun 77 : 4584 4596.
54. Ni, M. Yu, J.H. (2007) A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS ONE 2 : e970.
55. Nwaka, S., Mechler, B., Destruelle, M. Holzer, H. (1995) Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Lett 360 : 286 290.
56. Panneman, H., Ruijter, G.J., van den Broeck, H.C. Visser, J. (1998) Cloning and biochemical characterisation of Aspergillus niger hexokinase - the enzyme is strongly inhibited by physiological concentrations of trehalose 6-phosphate. Eur J Biochem 258 : 223 232.
57. Perlin, D.S. Mellado, E. (2008) Antifungal mechanisms of action and resistance. In Aspergillus fumigatus and Aspergillosis. Latge, J.-P. Steinbach, W.J. (eds). Washington, DC : ASM Press, p. 568.
58. Petzold, E.W., Himmelreich, U., Mylonakis, E., Rude, T., Toffaletti, D., Cox, G.M., et al. (2006) Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect Immun 74 : 5877 5887.
59. Pollock, J.D., Williams, D.A., Gifford, M.A., Li, L.L., Du, X., Fisherman, J., et al. (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9 : 202 209.
60. Ram, A.F. Klis, F.M. (2006) Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1 : 2253 2256.
61. Reinders, A., Burckert, N., Hohmann, S., Thevelein, J.M., Boller, T., Wiemken, A. De Virgilio, C. (1997) Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Mol Microbiol 24 : 687 695.
62. Saito, K., Kase, T., Takahashi, E. Horinouchi, S. (1998a) Purification and characterization of a trehalose synthase from the basidiomycete grifola frondosa. Appl Environ Microbiol 64 : 4340 4345.
63. Saito, K., Yamazaki, H., Ohnishi, Y., Fujimoto, S., Takahashi, E. Horinouchi, S. (1998b) Production of trehalose synthase from a basidiomycete, Grifola frondosa, in Escherichia coli. Appl Microbiol Biotechnol 50 : 193 198. (Pubitemid 28414540)
64. Sano, F., Asakawa, N., Inoue, Y. Sakurai, M. (1999) A dual role for intracellular trehalose in the resistance of yeast cells to water stress. Cryobiology 39 : 80 87.
65. Shimizu, K. Keller, N.P. (2001) Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157 : 591 600.
66. Shinohara, M.L., Correa, A., Bell-Pedersen, D., Dunlap, J.C. Loros, J.J. (2002) Neurospora clock-controlled gene 9 (ccg-9) encodes trehalose synthase: circadian regulation of stress responses and development. Eukaryot Cell 1 : 33 43.
67. Singer, M.A. Lindquist, S. (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16 : 460 468.
68. Snelders, E., van der Lee, H.A., Kuijpers, J., Rijs, A.J., Varga, J., Samson, R.A., et al. (2008) Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med 5 : e219.
69. Sur, I.P., Lobo, Z. Maitra, P.K. (1994) Analysis of PFK3 - a gene involved in particulate phosphofructokinase synthesis reveals additional functions of TPS2 in Saccharomyces cerevisiae. Yeast 10 : 199 209.
70. Thevelein, J.M. (1984) Regulation of trehalose mobilization in fungi. Microbiol Rev 48 : 42 59.
71. Thevelein, J.M. Hohmann, S. (1995) Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem Sci 20 : 3 10.
72. Van Dijck, P., De Rop, L., Szlufcik, K., Ael, E.V. Thevelein, J.M. (2002) Disruption of the Candida albicans TPS2 gene encoding trehalose-6-phosphate phosphatase decreases infectivity without affecting hypha formation. Infect Immun 70 : 1772 1782.
73. Varkey, J.B. Perfect, J.R. (2008) Rare and emerging fungal pulmonary infections. Semin Respir Crit Care Med 29 : 121 131.
74. Verweij, P.E., Mellado, E. Melchers, W.J. (2007) Multiple-triazole- resistant aspergillosis. N Engl J Med 356 : 1481 1483.
75. Vuorio, O.E., Kalkkinen, N. Londesborough, J. (1993) Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. Eur J Biochem 216 : 849 861.
76. Wannet, W.J., Op den Camp, H.J., Wisselink, H.W., van der Drift, C., Van Griensven, L.J. Vogels, G.D. (1998) Purification and characterization of trehalose phosphorylase from the commercial mushroom Agaricus bisporus. Biochim Biophys Acta 1425 : 177 188.
77. White, T.C., Marr, K.A. Bowden, R.A. (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11 : 382 402.
78. Willger, S.D., Puttikamonkul, S., Kim, K.H., Burritt, J.B., Grahl, N., Metzler, L.J., et al. Jr (2008) A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus. PLoS Pathog 4 : e1000200.
79. Wilson, R.A., Jenkinson, J.M., Gibson, R.P., Littlechild, J.A., Wang, Z.Y. Talbot, N.J. (2007) Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J 26 : 3673 3685.
80. Yelton, M.M., Hamer, J.E. Timberlake, W.E. (1984) Transformation of Aspergillus nidulans by using a trpC plasmid. Proc Natl Acad Sci USA 81 : 1470 1474.
81. Zaragoza, O., Blazquez, M.A. Gancedo, C. (1998) Disruption of the Candida albicans TPS1 gene encoding trehalose-6-phosphate synthase impairs formation of hyphae and decreases infectivity. J Bacteriol 180 : 3809 3815.
82. Zaragoza, O., de Virgilio, C., Ponton, J. Gancedo, C. (2002) Disruption in Candida albicans of the TPS2 gene encoding trehalose-6-phosphate phosphatase affects cell integrity and decreases infectivity. Microbiology 148 : 1281 1290.