High osmolarity glycerol response PtcB phosphatase is important for Aspergillus fumigatus virulence

Molecular Microbiology

Volumn 96, Issue 1, 2015, Pages 42-54

  Winkelströter, Lizziane K ^a   Bom, Vinícius Leite Pedro ^a   de Castro, Patrícia Alves ^a   Ramalho, Leandra Naira Zambelli ^a   Goldman, Maria Helena S ^a   Brown, Neil Andrew ^a   Rajendran, Ranjith ^b   Ramage, Gordon ^b   Bovier, Elodie ^a   dos Reis, Thaila Fernanda ^a   Savoldi, Marcela ^a   Hagiwara, Daisuke ^c   Goldman, Gustavo H ^a,d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b GLASGOW DENTAL HOSPITAL AND SCHOOL   (United Kingdom)

^c CHIBA UNIVERSITY   (Japan)

^d BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,3 GLUCAN; CHITIN; GLYCEROL; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN PTCB; PROTEIN SAKA; UNCLASSIFIED DRUG; BETA GLUCAN; BETA-1,3-GLUCAN; FUNGAL PROTEIN; PHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; BIOFILM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FUNGAL CELL WALL; FUNGAL METABOLISM; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS MUTANT; GENE EXPRESSION; GENE IDENTIFICATION; HIGH OSMOLARITY GLYCEROL RESPONSE; HISTOPATHOLOGY; LUNG ASPERGILLOSIS; MOUSE; MURINE MODEL; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGY; CELL WALL; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OSMOLARITY; PATHOGENICITY; PHYSIOLOGY; ULTRASTRUCTURE;

ASPERGILLUS FUMIGATUS; MURINAE;

ANIMALS; ASPERGILLUS FUMIGATUS; BETA-GLUCANS; BIOFILMS; CELL WALL; CHITIN; COMPUTATIONAL BIOLOGY; DISEASE MODELS, ANIMAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLYCEROL; MICE; MUTATION; OSMOLAR CONCENTRATION; PHOSPHORIC MONOESTER HYDROLASES; SIGNAL TRANSDUCTION;

EID: 84925388100     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12919     Document Type: Article

References (69)

1. Adám, C., Erdei, E., Casado, C., Kovács, L., González, A., Majoros, L., etal. (2012) Protein phosphatase CaPpz1 is involved in cation homeostasis, cell wall integrity and virulence of Candida albicans. Microbiology 158: 1258-1267.
2. Andersen, J.N., Mortensen, O.H., Peters, G.H., Drake, P.G., Iversen, L.F., Olsen, O.H., etal. (2001) Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 21: 7117-7136.
3. Ariño, J., Casamayor, A., and González, A. (2011) Type 2C protein phosphatases in fungi. Eukaryot Cell 10: 21-33.
4. Bahn, Y.S. (2008) Master and commander in fungal pathogens: the two-component system and the HOG signaling pathway. Eukaryot Cell 7: 2017-2036.
5. Breitkreutz, A., Choi, H., Sharom, J.R., Boucher, L., Neduva, V., Larsen, B., etal. (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328: 1043-1046.
6. Brewster, J.L., and Gustin, M.C. (2014) Hog1: 20 years of discovery and impact. Sci Sign 7: re7.
7. ten Cate, J.M., Klis, F.M., Pereira-Cenci, T., Crielaard, W., and de Groot, P.W. (2009) Molecular and cellular mechanisms that lead to Candida biofilm formation. J Dent Res 88: 105-115.
8. Chung, D., Thammahong, A., Shepardson, K.M., Blosser, S.J., and Cramer, R.A. (2014) Endoplasmic reticulum localized PerA is required for cell wall integrity, azole drug resistance, and virulence in Aspergillus fumigatus. Mol Microbiol 92: 1279-1298.
9. Colot, H.H., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., etal. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103: 10352-10357.
10. Cuéllar-Cruz, M., López-Romero, E., Villagómez-Castro, J.C., and Ruiz-Baca, E. (2012) Candida species: new insights into biofilm formation. Future Microbiol 7: 755-771.
11. Dagenais, T.R., and Keller, N.P. (2009) Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin Microbiol Rev 22: 447-465.
12. Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Münch, K., and Kahmann, R. (2009) The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol Microbiol 73: 73-88.
13. Dinamarco, T.M., Freitas, F.Z., Almeida, R.S., Brown, N.A., dos Reis, T.F., Ramalho, L.N.Z., etal. (2012) Functional characterization of an Aspergillus fumigatus calcium transporter (PmcA) that is essential for fungal infection. PLoS ONE 7: e37591.
14. Du, Y., Shi, Y., Yang, J., Chen, X., Xue, M., Zhou, W., etal. (2013) A serine/threonine-protein phosphatase PP2A catalytic subunit is essential for asexual development and plant infection in Magnaporthe oryzae. Curr Genet 59: 33-41.
15. Erental, A., Harel, A., and Yarden, O. (2007) Type 2A phosphoprotein phosphatase is required for asexual development and pathogenesis of Sclerotinia sclerotiorum. Mol Plant Microbe Interact 20: 944-954.
16. Erlandsen, S.L., Kristich, C.J., Dunny, G.M., and Wells, C.L. (2004) High-resolution visualization of the microbial glycocalyx with low-voltage scanning electron microscopy: dependence on cationic dyes. J Histochem Cytochem 52: 1427-1435.
17. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
18. Feng, J., Zhao, J., Li, J., Zhang, L., and Jiang, L. (2010) Functional characterization of the PP2C phosphatase CaPtc2p in the human fungal pathogen Candida albicans. Yeast 27: 753-764.
19. Ghosh, A., Servin, J.A., Park, G., and Borkovich, K.A. (2014) Global analysis of serine/threonine and tyrosine protein phosphatase catalytic subunit genes in Neurospora crassa reveals interplay between phosphatases and the p38 mitogen-activated protein kinase. G3 (Bethesda) 4: 349-365.
20. Goldman, G.H., dos Reis Marques, E., Duarte Ribeiro, D.C., de Souza Bernardes, L.A., Quiapin, A.C., Vitorelli, P.M., etal. (2003) Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryot Cell 2: 34-48.
21. González, A., Ruiz, A., Serrano, R., Ariño, J., and Casamayor, A. (2006) Transcriptional profiling of the protein phosphatase 2C family in yeast provides insights into the unique functional roles of Ptc1. J Biol Chem 281: 35057-35069.
22. Graham, L.M., Tsoni, S.V., Willment, J.A., Williams, D.L., Taylor, P.R., Gordon, S., etal. (2006) Soluble Dectin-1 as a tool to detect beta-glucans. J Immunol Methods 314: 164-169.
23. Greenberger, P.A. (2002) Allergic bronchopulmonary aspergillosis. J Allergy Clin Immunol 110: 685-692.
24. Hagiwara, D., Takahashi-Nakaguchi, A., Toyotome, T., Yoshimi, A., Abe, K., Kamei, K., etal. (2013) NikA/TcsC histidine kinase is involved in conidiation, hyphal morphology, and responses to osmotic stress and antifungal chemicals in Aspergillus fumigatus. PLoS ONE 8: e80881.
25. Hamel, L.P., Nicole, M.C., Duplessis, S., and Ellis, B.E. (2012) Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 24: 1327-1351.
26. Herrera-Estrella, A., Goldman, G.H., and Van Montagu, M. (1990) High-efficiency transformation system for the biocontrol agents, Trichoderma spp. Mol Microbiol 4: 839-843.
27. Jacoby, T., Flanagan, H., Faykin, A., Seto, A.G., Mattison, C., and Ota, I. (1997) Two protein-tyrosine phosphatases inactivate the osmotic stress response pathway in yeast by targeting the mitogen-activated protein kinase, Hog1. J Biol Chem 272: 17749-17755.
28. Jiang, J., Yun, Y., Yang, Q., Shim, W.B., Wang, Z., etal. (2011) A type 2C protein phosphatase, FgPtc3 is involved in cell wall integrity, lipid metabolism, and virulence in Fusarium graminearum. PLoS ONE 6: e25311.
29. Kafer, E. (1977) Meiotic and mitotic recombination in Aspergilllus and its chromosomal aberrations. Adv Genet 19: 33-131.
30. Lee, K.T., Byun, H.J., Jung, K.W., Hong, J., Cheong, E., and Bahn, Y.S. (2014) Distinct and redundant roles of protein tyrosine phosphatases Ptp1 and Ptp2 in governing the differentiation and pathogenicity of Cryptococcus neoformans. Eukaryot Cell 13: 796-812.
31. Ma, D., and Li, R. (2013) Current understanding of HOG-MAPK pathway in Aspergillus fumigatus. Mycopathologia 175: 13-23.
32. Martín, H., Flández, M., Nombela, C., and Molina, M. (2005) Protein phosphatases in MAPK signalling: we keep learning from yeast. Mol Microbiol 58: 6-16.
33. Mattison, C.P., Spencer, S.S., Kresge, K.A., Lee, J., and Ota, I.M. (1999) 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 19: 7651-7660.
34. May, G.S. (2008) Mitogen-activated protein kinase pathways in Aspergilli. In The Aspergilli. Genomics, Medical Aspects, Biotechnology, and Research Methods. Goldman, G.H., and Osmani, S.A. (eds). Boca Raton, FL: CRC Press, pp. 121-127.
35. Monge, R.A., Román, E., Nombela, C., and Pla, J. (2006) The MAP kinase signal transduction network in Candida albicans. Microbiology 152: 905-912.
36. Moorhead, G.B., Trinkle-Mulcahy, L., and Ulke-Lemee, A. (2007) Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol 8: 234-244.
37. Moorhead, G.B., De Wever, V., Templeton, G., and Kerk, D. (2009) Evolution of protein phosphatases in plants and animals. Biochem J 417: 401-409.
38. Mowat, E., Butcher, J., Lang, S., Williams, C., and Ramage, G. (2007) Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol 56: 1205-1212.
39. Muszkieta, L., Carrion Sde, J., Robinet, P., Beau, R., Elbim, C., Pearlman, E., etal. (2014) The protein phosphatase PhzA of A.fumigatus is involved in oxidative stress tolerance and fungal virulence. Fungal Genet Biol 66: 79-85.
40. Pao, L.I., Badour, K., Siminovitch, K.A., and Neel, B.G. (2007) Nonreceptor protein-tyrosine phosphatases in immune cell signaling. Annu Rev Immunol 25: 473-523.
41. Pearson, G., Robinson, F., Beers Gibson, T., Xu, B.E., Karandikar, M., Berman, K., etal. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22: 153-183.
42. Reyes, G., Romans, A., Nguyen, C.K., and May, G.S. (2006) Novel mitogen-activated protein kinase MpkC of Aspergillus fumigatus is required for utilization of polyalcohol sugars. Eukaryot Cell 5: 1934-1940.
43. Rispail, N., Soanes, D.M., Ant, C., Czajkowski, R., Grünler, A., Huguet, R., etal. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet Biol 46: 287-298.
44. Román, E., Arana, D.M., Nombela, C., Alonso-Monge, R., and Pla, J. (2007) MAP kinase pathways as regulators of fungal virulence. Trends Microbiol 15: 181-190.
45. Saito, H., and Posas, F. (2012) Response to Hyperosmotic Stress. Genetics 192: 289-318.
46. Saito, H., and Tatebayashi, K. (2004) Regulation of the osmoregulatory HOG MAPK cascade in yeast. J Biochem 136: 267-272.
47. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
48. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory, Cold Spring Harbor.
49. Sanvoisin, J., and Gani, D. (2001) Protein phosphatase 1 catalyses the direct hydrolytic cleavage of phosphate monoester in a ternary complex mechanism. Bioorg Med Chem Lett 11: 471-474.
50. Schiestl, R.H., and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16: 339-346.
51. Shepardson, K.M., Ngo, L.Y., Aimanianda, V., Latge, J.P., Barker, B.M., Blosser, S.J., etal. (2013) Hypoxia enhances innate immune activation to Aspergillus fumigatus through cell wall modulation. Microbes Infect 15: 259-269.
52. Shi, Y. (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139: 468-484.
53. Shin, J.H., Kim, J.E., Malapi-Wight, M., Choi, Y.E., Shaw, B.D., and Shim, W.-B. (2013) Protein phosphatase 2A regulatory subunits perform distinct functional roles in the maize pathogen Fusarium verticillioides. Mol Plant Pathol 14: 518-529.
54. Shopova, I., Bruns, S., Thywissen, A., Kniemeyerm, O., Brakhage, A.A., and Hillmann, F. (2013) Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus. Front Microbiol 4: 141.
55. Son, S., and Osmani, S.A. (2009) Analysis of all protein phosphatase genes in Aspergillus nidulans identifies a new mitotic regulator, fcp1. Eukaryot Cell 8: 573-585.
56. Steinbach, W.J., Reedy, J.L., Cramer, R.A., Jr, Perfect, J.R., and Heitman, J. (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiol 5: 418-430.
57. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: molecular evolutionary genetic analysis version 6.0. Mol Biol Evol 30: 2725-2729.
58. Valiante, V., Heinekamp, T., Jain, R., Hartl, A., and Brakhage, A.A. (2008) The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet Biol 45: 618-627.
59. Valiante, V., Jain, R., Heinekamp, T., and Brakhage, A.A. (2009) The MpkA MAP kinase module regulates cell wall integrity signaling and pyomelanin formation in Aspergillus fumigatus. Fungal Genet Biol 46: 909-918.
60. Warmka, J., Hanneman, J., Lee, J., Amin, D., and Ota, I. (2001) Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Mol Cell Biol 21: 51-60.
61. Williams, N.H. (2004) Models for biological phosphoryl transfer. Biochim Biophys Acta 1697: 279-287.
62. Wong Sak Hoi, J., Lamarre, C., Beau, R., Meneau, I., Berepiki, A., Barre, A., etal. (2011) A novel family of dehydrin-like proteins is involved in stress response in the human fungal pathogen Aspergillus fumigatus. Mol Biol Cell 22: 1896-1906.
63. Wurgler-Murphy, S.M., Maeda, T., Witten, E.A., and Saito, H. (1997) Regulation of the Saccharomyces cerevisiae HOG1 mitogen activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol Cell Biol 17: 1289-1297.
64. Xue, T., Nguyen, C.K., Romans, A., and May, G.S. (2004) A mitogen-activated protein kinase that senses nitrogen regulates conidial germination and growth in Aspergillus fumigatus. Eukaryot Cell 3: 557-560.
65. Yang, Q., Yu, F., Yin, Y., and Ma, Z. (2013a) Involvement of protein tyrosine phosphatases BcPtpA and BcPtpB in regulation of vegetative development, virulence and multi-stress tolerance in Botrytis cinerea. PLoS ONE 8: e61307.
66. Yang, Q., Jiang, J., Mayr, C., Hahn, M., and Ma, Z. (2013b) Involvement of two type 2C protein phosphatases BcPtc1 and BcPtc3 in the regulation of multiple stress tolerance and virulence of Botrytis cinerea. Environ Microbiol 15: 2696-2711.
67. Yu, F., Gu, Q., Yun, Y., Yin, Y., Xu, J.R., Shim, W.-B., etal. (2014) The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytol 203: 219-232.
68. Zhang, M., Liu, J., Kim, Y., Dixon, J.E., Pfaff, S.L., Gill, G.N., etal. (2010) Structural and functional analysis of the phosphoryl transfer reaction mediated by the human small C-terminal domain phosphatase, Scp1. Protein Sci 19: 974-986.
69. Zuckerkandl, E., and Pauling, L. (1965) Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins. Bryson, V., and Vogel, H.J. (eds). New York, NY: Academic Press, pp. 97-166.