Histidine phosphotransfer proteins in fungal two-component signal transduction pathways

Eukaryotic Cell

Volumn 12, Issue 8, 2013, Pages 1052-1060

  Fassler, Jan S ^a   West, Ann H ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; DNA BINDING PROTEIN; HISTIDINE; PROTEIN KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE; YPD1 PROTEIN, S CEREVISIAE;

AMINO ACID SEQUENCE; CRYPTOCOCCUS NEOFORMANS; GENETICS; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; CRYPTOCOCCUS NEOFORMANS; DNA-BINDING PROTEINS; HISTIDINE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84880795175     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00083-13     Document Type: Review

References (99)

1. MacRitchie DM, Buelow DR, Price NL, Raivio TL. 2008. Twocomponent signaling and gram negative envelope stress response systems. Adv. Exp. Med. Biol. 631:80-110.
2. Whistler CA, Corbell NA, Sarniguet A, Ream W, Loper JE. 1998. The two-component regulators GacS and GacA influence accumulation of the stationary-phase sigma factor sigmaS and the stress response in Pseudomonas fluorescens Pf-5. J. Bacteriol. 180:6635-6641.
3. Martinez-Wilson HF, Tamayo R, Tischler AD, Lazinski DW, Camilli A. 2008. The Vibrio cholerae hybrid sensor kinase VieS contributes to motility and biofilm regulation by altering the cyclic diguanylate level. J. Bacteriol. 190:6439-6447.
4. Hickman JW, Tifrea DF, Harwood CS. 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. U. S. A. 102:14422-14427.
5. Cotter PA, Stibitz S. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10:17-23.
6. Ohta N, Lane T, Ninfa EG, Sommer JM, Newton A. 1992. A histidine protein kinase homologue required for regulation of bacterial cell division and differentiation. Proc. Natl. Acad. Sci. U. S. A. 89:10297-10301.
7. Hoch JA. 1993. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu. Rev. Microbiol. 47:441-465.
8. Ulrich LE, Zhulin IB. 2010. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res. 38:D401-D407.
9. Ninfa EG, Atkinson MR, Kamberov ES, Ninfa AJ. 1993. Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): trans-phosphorylation between subunits. J. Bacteriol. 175:7024-7032.
10. Swanson RV, Bourret RB, Simon MI. 1993. Intermolecular complementation of the kinase activity of CheA. Mol. Microbiol. 8:435-441.
11. Wolfe AJ, Stewart RC. 1993. The short form of the CheA protein restores kinase activity and chemotactic ability to kinase-deficient mutants. Proc. Natl. Acad. Sci. U. S. A. 90:1518-1522.
12. Yang Y, Inouye M. 1993. Requirement of both kinase and phosphatase activities of an Escherichia coli receptor (Taz1) for ligand-dependent signal transduction. J. Mol. Biol. 231:335-342.
13. McEvoy MM, Dahlquist FW. 1997. Phosphohistidines in bacterial signaling. Curr. Opin. Struct. Biol. 7:793-797.
14. Alex LA, Simon MI. 1994. Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. Trends Genet. 10:133-138.
15. Stock AM, Robinson VL, Goudreau PN. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215.
16. Tsuzuki M, Ishige K, Mizuno T. 1995. Phosphotransfer circuitry of the putative multi-signal transducer, ArcB, of Escherichia coli: in vitro studies with mutants. Mol. Microbiol. 18:953-962.
17. Santos JL, Shiozaki K. 2001. Fungal histidine kinases. Sci. STKE 2001(98):re1.
18. Schaller GE, Shiu SH, Armitage JP. 2011. Two-component systems and their co-option for eukaryotic signal transduction. Curr. Biol. 21:R320-R330.
19. Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC, Saito H. 1996. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86:865-875.
20. Li D, Agrellos OA, Calderone R. 2010. Histidine kinases keep fungi safe and vigorous. Curr. Opin. Microbiol. 13:424-430.
21. Selitrennikoff CP, Alex L, Miller TK, Clemons KV, Simon MI, Stevens DA. 2001. COS-l, a putative two-component histidine kinase of Candida albicans, is an in vivo virulence factor. Med. Mycol. 39:69-74.
22. Kruppa M, Krom BP, Chauhan N, Bambach AV, Cihlar RL, Calderone RA. 2004. The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot. Cell 3:1062-1065.
23. Bahn YS, Kojima K, Cox GM, Heitman J. 2006. A unique fungal twocomponent system regulates stress responses, drug sensitivity, sexual development, and virulence of Cryptococcus neoformans. Mol. Biol. Cell 17: 3122-3135.
24. Boyce KJ, Schreider L, Kirszenblat L, Andrianopoulos A. 2011. The two-component histidine kinases DrkA and SlnA are required for in vivo growth in the human pathogen Penicillium marneffei. Mol. Microbiol. 82:1164-1184.
25. Wang F, Tao J, Qian Z, You S, Dong H, Shen H, Chen X, Tang S, Ren S. 2009. A histidine kinase PmHHK1 regulates polar growth, sporulation and cell wall composition in the dimorphic fungus Penicillium marneffei. Mycol. Res. 113:915-923.
26. Nemecek JC, Wuthrich M, Klein BS. 2006. Global control of dimorphism and virulence in fungi. Science 312:583-588.
27. Ochiai N, Tokai T, Nishiuchi T, Takahashi-Ando N, Fujimura M, Kimura M. 2007. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem. Biophys. Res. Commun. 363:639-644.
28. Rispail N, Di Pietro A. 2010. The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum. Mol. Plant Pathol. 11:395-407.
29. Ma Z, Luo Y, Michailides T. 2006. Molecular characterization of the two-component histidine kinase gene from Monilinia fructicola. Pest Manag. Sci. 62:991-998.
30. Cui W, Beever RE, Parkes SL, Weeds PL, Templeton MD. 2002. An osmosensing histidine kinase mediates dicarboximide fungicide resistance in Botryotinia fuckeliana (Botrytis cinerea). Fungal Genet. Biol. 36: 187-198.
31. Oshima M, Fujimura M, Banno S, Hashimoto C, Motoyama T, Ichiishi A, Yamaguchi I. 2002. A point mutation in the two-component histidine kinase BcOS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology 92:75-80.
32. Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pecheur P, Kunduru AR, Leroux P, Legendre L. 2006. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant Microbe Interact. 19:1042-1050.
33. Cho Y, Kim KH, La Rota M, Scott D, Santopietro G, Callihan M, Mitchell TK, Lawrence CB. 2009. Identification of novel virulence factors associated with signal transduction pathways in Alternaria brassicicola. Mol. Microbiol. 72:1316-1333.
34. Dry IB, Yuan KH, Hutton DG. 2004. Dicarboximide resistance in field isolates of Alternaria alternata is mediated by a mutation in a twocomponent histidine kinase gene. Fungal Genet. Biol. 41:102-108.
35. Oide S, Liu J, Yun SH, Wu D, Michev A, Choi MY, Horwitz BA, Turgeon BG. 2010. Histidine kinase two-component response regulator proteins regulate reproductive development, virulence, and stress responses of the fungal cereal pathogens Cochliobolus heterostrophus and Gibberella zeae. Eukaryot. Cell 9:1867-1880.
36. Lu JM, Deschenes RJ, Fassler JS. 2003. Saccharomyces cerevisiae histidine phosphotransferase Ypd1p shuttles between the nucleus and cytoplasm for SLN1-dependent phosphorylation of Ssk1p and Skn7p. Eukaryot. Cell 2:1304-1314.
37. Geer LY, Domrachev M, Lipman DJ, Bryant SH. 2002. CDART: protein homology by domain architecture. Genome Res. 12:1619-1623.
38. Horie T, Tatebayashi K, Yamada R, Saito H. 2008. Phosphorylated Ssk1 prevents unphosphorylated Ssk1 from activating the Ssk2 mitogenactivated protein kinase kinase kinase in the yeast high-osmolarity glycerol osmoregulatory pathway. Mol. Cell. Biol. 28:5172-5183.
39. Posas F, Saito H. 1998. Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17: 1385-1394.
40. Brown JL, Bussey H, Stewart RC. 1994. Yeast Skn7p functions in a eukaryotic two-component regulatory pathway. EMBO J. 13:5186-5194.
41. Raitt DC, Johnson AL, Erkine AM, Makino K, Morgan B, Gross DS, Johnston LH. 2000. The Skn7 response regulator of Saccharomyces cerevisiae interacts with Hsf1 in vivo and is required for the induction of heat shock genes by oxidative stress. Mol. Biol. Cell 11:2335-2347.
42. Hwang I, Sheen J. 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383-389.
43. Tanaka Y, Suzuki T, Yamashino T, Mizuno T. 2004. Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 68:462-465.
44. Punwani JA, Hutchison CE, Schaller GE, Kieber JJ. 2010. The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J. 62:473-482.
45. Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T. 2000. Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 41:791-803.
46. Wuichet K, Cantwell BJ, Zhulin IB. 2010. Evolution and phyletic distribution of two-component signal transduction systems. Curr. Opin. Microbiol. 13:219-225.
47. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605-618.
48. Maeda T, Wurgler-Murphy SM, Saito H. 1994. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369:242-245.
49. Brown JL, North S, Bussey H. 1993. SKN7, a yeast multicopy suppressor of a mutation affecting cell wall beta-glucan assembly, encodes a product with domains homologous to prokaryotic two-component regulators and to heat shock transcription factors. J. Bacteriol. 175:6908-6915.
50. Aoyama K, Mitsubayashi Y, Aiba H, Mizuno T. 2000. Spy1, a histidinecontaining phosphotransfer signaling protein, regulates the fission yeast cell cycle through the Mcs4 response regulator. J. Bacteriol. 182:4868-4874.
51. Calera JA, Herman D, Calderone R. 2000. Identification of YPD1, a gene of Candida albicans which encodes a two-component phosphohistidine intermediate protein. Yeast 16:1053-1059.
52. Azuma N, Kanamaru K, Matsushika A, Yamashino T, Mizuno T, Kato M, Kobayashi T. 2007. In vitro analysis of His-Asp phosphorelays in Aspergillus nidulans: the first direct biochemical evidence for the existence of His-Asp phosphotransfer systems in filamentous fungi. Biosci. Biotechnol. Biochem. 71:2493-2502.
53. Tan H, Janiak-Spens F, West AH. 2007. Functional characterization of the phosphorelay protein Mpr1p from Schizosaccharomyces pombe. FEMS Yeast Res. 7:912-921.
54. Lee JW, Ko YJ, Kim SY, Bahn YS. 2011. Multiple roles of Ypd1 phosphotransfer protein in viability, stress response, and virulence factor regulation in Cryptococcus neoformans. Eukaryot. Cell 10:998-1002.
55. Nguyen AN, Lee A, Place W, Shiozaki K. 2000. Multistep phosphorelay proteins transmit oxidative stress signals to the fission yeast stressactivated protein kinase. Mol. Biol. Cell 11:1169-1181.
56. Chang WT, Thomason PA, Gross JD, Neweil PC. 1998. Evidence that the RdeA protein is a component of a multistep phosphorelay modulating rate of development in Dictyostelium. EMBO J. 17:2809-2816.
57. Ohmiya R, Kato C, Yamada H, Aiba H, Mizuno T. 1999. A fission yeast gene (prr1(+)) that encodes a response regulator implicated in oxidative stress response. J. Biochem. 125:1061-1066.
58. Quinn J, Malakasi P, Smith DA, Cheetham J, Buck V, Millar JB, Morgan BA. 2011. Two-component mediated peroxide sensing and signal transduction in fission yeast. Antioxid. Redox Signal. 15:153-165.
59. Banno S, Noguchi R, Yamashita K, Fukumori F, Kimura M, Yamaguchi I, Fujimura M. 2007. Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in Neurospora crassa. Curr. Genet. 51:197-208.
60. Vargas-Perez I, Sanchez O, Kawasaki L, Georgellis D, Aguirre J. 2007. Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryot. Cell 6:1570-1583.
61. Nemecek JC, Wüthrich M, Klein BS. 2007. Detection and measurement of two-component systems that control dimorphism and virulence in fungi. Methods Enzymol. 422:465-487.
62. Xu Q, Nguyen V, West AH. 1999. Purification, crystallization and preliminary X-ray diffraction analysis of the yeast phosphorelay protein YPD1. Acta Crystallogr. D Biol. Crystallogr. 55:291-293.
63. Janiak-Spens F, West AH. 2000. Functional roles of conserved amino acid residues surrounding the phosphorylatable histidine of the yeast phosphorelay protein YPD1. Mol. Microbiol. 37:136-144.
64. Fassler JS, West AH. 2010. Genetic and biochemical analysis of the SLN1 pathway in Saccharomyces cerevisiae. Methods Enzymol. 471:291-317.
65. Janiak-Spens F, Sparling DP, West AH. 2000. Novel role for an HPt domain in stabilizing the phosphorylated state of a response regulator domain. J. Bacteriol. 182:6673-6678.
66. Porter SW, West AH. 2005. A common docking site for response regulators on the yeast phosphorelay protein YPD1. Biochim. Biophys. Acta 1748:138-145.
67. Porter SW, Xu Q, West AH. 2003. Ssk1p response regulator binding surface on histidine-containing phosphotransfer protein Ypd1p. Eukaryot. Cell 2:27-33.
68. Ault AD. 2001. Analysis of the molecular mechanisms of signaling by Sln1, part of a two-component phosphorelay pathway in Saccharomyces cerevisiae. University of Iowa, Iowa City, IA.
69. Hiramoto F, Nomura N, Furumai T, Igarashi Y, Oki T. 2003. Pradimicin- resistance of yeast is caused by a point mutation of the histidinecontaining phosphotransfer protein Ypd1. J. Antibiot. (Tokyo) 56:1053-1057.
70. Fassler JS, Gray WM, Malone CL, Tao W, Lin H, Deschenes RJ. 1997. Activated alleles of yeast SLN1 increase Mcm1-dependent reporter gene expression and diminish signaling through the Hog1 osmosensing pathway. J. Biol. Chem. 272:13365-13371.
71. Barrett JF, Goldschmidt RM, Lawrence LE, Foleno B, Chen R, Demers JP, Johnson S, Kanojia R, Fernandez J, Bernstein J, Licata L, Donetz A, Huang S, Hlasta DJ, Macielag MJ, Ohemeng K, Frechette R, Frosco MB, Klaubert DH, Whiteley JM, Wang L, Hoch JA. 1998. Antibacterial agents that inhibit two-component signal transduction systems. Proc. Natl. Acad. Sci. U. S. A. 95:5317-5322.
72. Barrett JF, Hoch JA. 1998. Two-component signal transduction as a target for microbial anti-infective therapy. Antimicrob. Agents Chemother. 42:1529-1536.
73. Foster JE, Sheng Q, McClain JR, Bures M, Nicas TI, Henry K, Winkler ME, Gilmour R. 2004. Kinetic and mechanistic analyses of new classes of inhibitors of two-component signal transduction systems using a coupled assay containing HpkA-DrrA from Thermotoga maritima. Microbiology 150:885-896.
74. Sugahara H, Kondo T, Okada M, Ikeda Y, Kaida K, Fudou R, Mizuno T, Sakagami Y. 2008. Articulospora sp. produces Art1, an inhibitor of bacterial histidine kinase. Biosci. Biotechnol. Biochem. 72:2521-2525.
75. Deschenes RJ, Lin H, Ault AD, Fassler JS. 1999. Antifungal properties and target evaluation of three putative bacterial histidine kinase inhibitors. Antimicrob. Agents Chemother. 43:1700-1703.
76. Gotoh Y, Eguchi Y, Watanabe T, Okamoto S, Doi A, Utsumi R. 2010. Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr. Opin. Microbiol. 13:232-239.
77. Buschart A, Gremmer K, El-Mowafy M, van den Heuvel J, Mueller PP, Bilitewski U. 2012. A novel functional assay for fungal histidine kinases group III reveals the role of HAMP domains for fungicide sensitivity. J. Biotechnol. 157:268-277.
78. Tebbets B, Stewart D, Lawry S, Nett J, Nantel A, Andes D, Klein BS. 2012. Identification and characterization of antifungal compounds using a Saccharomyces cerevisiae reporter bioassay. PLoS One 7:e36021. doi:10.1371/journal.pone.0036021.
79. Epand RM, Vogel HJ. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462:11-28.
80. Tossi A, Sandri L, Giangaspero A. 2000. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55:4-30.
81. Hancock RE, Lehrer R. 1998. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16:82-88.
82. Zasloff M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395.
83. Bobek LA, Situ H. 2003. MUC7 20-mer: investigation of antimicrobial activity, secondary structure, and possible mechanism of antifungal action. Antimicrob. Agents Chemother. 47:643-652.
84. Satyanarayana J, Situ H, Narasimhamurthy S, Bhayani N, Bobek LA, Levine MJ. 2000. Divergent solid-phase synthesis and candidacidal activity ofMUC7D1, a 51-residue histidine-rich N-terminal domain of human salivary mucin MUC7. J. Pept. Res. 56:275-282.
85. Hancock RE. 1997. Peptide antibiotics. Lancet 349:418-422.
86. Hancock RE, Rozek A. 2002. Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206:143-149.
87. Garibotto FM, Garro AD, Masman MF, Rodriguez AM, Luiten PG, Raimondi M, Zacchino SA, Somlai C, Penke B, Enriz RD. 2010. New small-size peptides possessing antifungal activity. Bioorg. Med. Chem. 18:158-167.
88. Grimaldi M, De Rosa M, Di Marino S, Scrima M, Posteraro B, Sanguinetti M, Fadda G, Soriente A, D'Ursi AM. 2010. Synthesis of new antifungal peptides selective against Cryptococcus neoformans. Bioorg. Med. Chem. 18:7985-7990.
89. Arkin MR, Whitty A. 2009. The road less traveled: modulating signal transduction enzymes by inhibiting their protein-protein interactions. Curr. Opin. Chem. Biol. 13:284-290.
90. Neduva V, Russell RB. 2006. Peptides mediating interaction networks: new leads at last. Curr. Opin. Biotechnol. 17:465-471.
91. Xu Q, Porter SW, West AH. 2003. The yeast YPD1/SLN1 complex: insights into molecular recognition in two-component signaling systems. Structure 11:1569-1581.
92. Zhao X, Copeland DM, Soares AS, West AH. 2008. Crystal structure of a complex between the phosphorelay protein YPD1 and the response regulator domain of SLN1 bound to a phosphoryl analog. J. Mol. Biol. 375: 1141-1151.
93. Edgar RC. 2004. Local homology recognition and distance measures in linear time using compressed amino acid alphabets. Nucleic Acids Res. 32:380-385.
94. Nicholas KB, Nicholas HBJ, Deerfield DWI. 1997. GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4:14.
95. Song HK, Lee JY, Lee MG, Moon J, Min K, Yang JK, Suh SW. 1999. Insights into eukaryotic multistep phosphorelay signal transduction revealed by the crystal structure of Ypd1p from Saccharomyces cerevisiae. J. Mol. Biol. 293:753-761.
96. Xu Q, West AH. 1999. Conservation of structure and function among histidine-containing phosphotransfer (HPt) domains as revealed by the crystal structure of YPD1. J. Mol. Biol. 292:1039-1050.
97. Ochiai N, Fujimura M, Motoyama T, Ichiishi A, Usami R, Horikoshi K, Yamaguchi I. 2001. Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa. Pest Manag. Sci. 57:437-442.
98. Xu D, Jiang B, Ketela T, Lemieux S, Veillette K, Martel N, Davison J, Sillaots S, Trosok S, Bachewich C, Bussey H, Youngman P, Roemer T. 2007. Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog. 3:e92. doi:10.1371 /journal.ppat.0030092.
99. Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K. 2005. Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol. Microbiol. 56:1246-1261.