medigraphic.com
ISSN 2395-8723 (Electronic)
ISSN 1405-888X (Print)
TIP Revista Especializada en Ciencias Químico-Biológicas

2014, Number 1

<< Back Next >>

TIP Rev Esp Cienc Quim Biol 2014; 17 (1)

Los sistemas de dos componentes: circuitos moleculares versátiles

Barba-Ostria CA

Language: Spanish
References: 111
Page: 62-76
PDF size: 475.74 Kb.


ABSTRACT

To survive, organisms must adapt to sudden environmental changes that exert a selective pressure and therefore, their chances of survival depend on their ability to respond quickly and accurately. Adapting to these changes is closely linked to the correct perception and transmission of stimuli and the generation of appropriate responses. Two component systems (TCS) allow different bacteria, fungi, slime molds and plants to regulate their physiology according to the environmental conditions. In these molecular circuits, the mechanism of communication between modules is the consecutive phosphorylation of His and Asp residues located in sensor histidine kinase and response regulator protein pairs. This review highlights the most relevant features of TCS and their role in the perception and response to diverse stimuli. Finally, the differences between prokaryotic and eukaryotic TCS are illustrated using the osmotic response in Escherichia coli and Saccharomyces cerevisiae.


REFERENCES

  1. Stock, A.M., Robinson, V.L. & Goudreau, P.N. Two-Component Signal Transduction. Annual Review of Biochemistry 69, 183-215, doi:doi:10.1146/annurev.biochem.69.1.183 (2000).

  2. Grebe, T.W. & Stock, J.B. The histidine protein kinase superfamily. Adv. Microb. Physiol. 41, 139-227 (1999).

  3. Stock, J.B., Ninfa, A.J. & Stock, A.M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53, 450-490 (1989).

  4. Parkinson, J.S. & Kofoid, E.C. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26, 71-112, doi:10.1146/ annurev.ge.26.120192.000443 (1992).

  5. Hoch, J. & Silhavy, T.J. Two-Component Signal Transduction (ASM Press, 1995).

  6. Appleby, J.L., Parkinson, J.S. & Bourret, R.B. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86, 845-848, doi:S0092-8674(00)80158-0 [pii] (1996).

  7. Georgellis, D., Lynch, A.S.& Lin, E.C. In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli. J. Bacteriol. 179, 5429-5435 (1997).

  8. Álvarez, A.F. & Georgellis, D. In vitro and in vivo analysis of the ArcB/A redox signaling pathway. Methods Enzymol. 471, 205-228, doi:S0076-6879(10)71012-0 [pii]10.1016/S0076- 6879(10)71012-0 (2010).

  9. Peña-Sandoval, G.R. & Georgellis, D. The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. J. Bacteriol. 192, 1735-1739, doi:JB.01401-09 [pii]10.1128/JB.01401-09 (2010).

  10. Galperin, M.Y. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 13, 150-159, doi:10.1016/j.mib.2010.01.005S1369-5274(10)00010-X [pii] (2010).

  11. Gao, R., Mack, T.R. & Stock, A.M. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 32, 225-234, doi:S0968-0004(07)00058-8 [pii]10.1016/j.tibs.2007.03.002 (2007).

  12. Wadhams, G.H. & Armitage, J.P. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5, 1024-1037, doi:nrm1524 [pii]10.1038/nrm1524 (2004).

  13. Zhou, Y., Gottesman, S., Hoskins, J.R., Maurizi, M.R. & Wickner, S. The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev. 15, 627-637, doi:10.1101/ gad.864401 (2001).

  14. Bougdour, A., Cunning, C., Baptiste, P.J., Elliott, T. & Gottesman, S. Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol. Microbiol. 68, 298-313 (2008).

  15. Capra, E.J., Perchuk, B.S., Skerker, J.M. & Laub, M.T. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150, 222-232, doi:10.1016/j.cell.2012.05.033S0092-8674(12)00654-X [pii] (2012).

  16. Forst, S.A. & Roberts, D.L. Signal transduction by the EnvZ- OmpR phosphotransfer system in bacteria. Res. Microbiol. 145, 63-73 (1994).

  17. Posas, F. et al. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86, 865-875 (1996).

  18. Álvarez, A.N.F., Rodríguez, C. & Georgellis, D. Ubiquinone and menaquinone electron-carriers represent the Ying and Yang in the redox regulation of the ArcB sensor kinase. Journal of Bacteriology, doi:10.1128/jb.00406-13 (2013).

  19. Georgellis, D., Kwon, O. & Lin, E.C. Quinones as the redox signal for the arc two-component system of bacteria. Science 292, 2314-2316, doi:10.1126/science.1059361292/5525/2314 [pii] (2001).

  20. Morigasaki, S., Shimada, K., Ikner, A., Yanagida, M. & Shiozaki, K. Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. Mol. Cell 30, 108-113 (2008).

  21. Groisman, E.A., Chiao, E., Lipps, C.J. & Heffron, F. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc. Natl. Acad. Sci. USA 86, 7077-7081 (1989).

  22. Ninfa, A.J. & Magasanik, B. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. USA 83, 5909-5913 (1986).

  23. Nohno, T., Noji, S., Taniguchi, S. & Saito, T. The narX and narL genes encoding the nitrate-sensing regulators of Escherichia coli are homologous to a family of prokaryotic two-component regulatory genes. Nucleic Acids Res. 17, 2947-2957 (1989).

  24. Lau, P.C. et al. A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc. Natl. Acad. Sci. USA 94, 1453-1458 (1997).

  25. Purcell, E.B., Siegal-Gaskins, D., Rawling, D.C., Fiebig, A. & Crosson, S. A photosensory two-component system regulates bacterial cell attachment. Proc. Natl. Acad. Sci. USA 104, 18241-18246, doi:0705887104 [pii]10.1073/pnas.0705887104 (2007).

  26. Blumenstein, A. et al. The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 15, 1833-1838, doi:S0960-9822(05)01020-1 [pii]10.1016/j. cub.2005.08.061 (2005).

  27. Jiang, M., Shao, W., Perego, M. & Hoch, J.A. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38, 535-542, doi:mmi2148 [pii] (2000).

  28. Perego, M. & Hoch, J.A. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 93, 1549-1553 (1996).

  29. Hutchings, M.I., Hong, H.J. & Buttner, M.J. The vancomycin resistance VanRS two-component signal transduction system of Streptomyces coelicolor. Molecular Microbiology 59, 923- 935, doi:doi:10.1111/j.1365-2958.2005.04953.x (2006).

  30. Bourret, R.B., Hess, J.F., Borkovich, K.A., Pakula, A.A. & Simon, M.I. Protein phosphorylation in chemotaxis and two- component regulatory systems of bacteria. J. Biol. Chem. 264, 7085-7088 (1989).

  31. Jagadeesan, S., Mann, P., Schink, C.W. & Higgs, P.I. A novel “four- component” two-component signal transduction mechanism regulates developmental progression in Myxococcus xanthus. J. Biol. Chem.284, 21435-21445, doi:M109.033415 [pii]10.1074/ jbc.M109.033415 (2009).

  32. Barba-Ostria, C., Lledias, F. & Georgellis, D. The Neurospora crassa DCC-1 Protein, a Putative Histidine Kinase, Is Required for Normal Sexual and Asexual Development and Carotenogenesis. Eukaryot. Cell 10, 1733-1739, doi:EC.05223-11 [pii]10.1128/ EC.05223-11 (2011).

  33. Cottarel, G. Mcs4, a two-component system response regulator homologue, regulates the Schizosaccharomyces pombe cell cycle control. Genetics 147, 1043-1051 (1997).

  34. Beier, D. & Gross, R. Regulation of bacterial virulence by two- component systems. Curr. Opin. Microbiol.9, 143-152 (2006).

  35. Nemecek, J.C., Wuthrich, M. & Klein, B.S. Global control of dimorphism and virulence in fungi. Science 312, 583-588, doi:312/5773/583 [pii]10.1126/science.1124105 (2006).

  36. Stepanova, A.N. & Alonso, J.M. Arabidopsis ethylene signaling pathway. Sci. STKE 2005, cm4, doi:stke.2762005cm4 [pii]10.1126/stke.2762005cm4 (2005).

  37. Oka, A., Sakai, H. & Iwakoshi, S. His-Asp phosphorelay signal transduction in higher plants: receptors and response regulators for cytokinin signaling in Arabidopsis thaliana. Genes Genet. Syst. 77, 383-391 (2002).

  38. Hwang, I. & Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383-389, doi:10.1038/3509650035096500 [pii] (2001).

  39. Yeh, K.C. & Lagarias, J.C. Eukaryotic phytochromes: light- regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. USA 95, 13976-13981 (1998).

  40. Matsushika, A., Makino, S., Kojima, M. & Mizuno, T. Circadian waves of expression of the APRR1/TOC1 family of pseudo- response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol.41, 1002-1012 (2000).

  41. Makino, S. et al. Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 41, 791-803 (2000).

  42. Ninfa, A.J. et al. Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proceedings of the National Academy of Sciences 85, 5492- 5496 (1988).

  43. Yamamoto, K. et al. Functional characterization in vitro of all twocomponent signal transduction systems from Escherichia coli. J. Biol. Chem.280, 1448-1456, doi:M410104200 [pii]10.1074/ jbc.M410104200 (2005).

  44. Skerker, J.M., Prasol, M.S., Perchuk, B.S., Biondi, E.G. & Laub, M.T. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system- level analysis. PLoS Biol 3, e334, doi:05-PLBI-RA-0427R2 [pii]10.1371/journal.pbio.0030334 (2005).

  45. Wanner, B.L. Is cross regulation by phosphorylation of two- component response regulator proteins important in bacteria? J. Bacteriol. 174, 2053-2058 (1992).

  46. Galperin, M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5, 35, doi:1471-2180-5-35 [pii]10.1186/1471-2180-5-35 (2005).

  47. Ulrich, L.E. & Zhulin, I.B. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res.38, D401-407, doi:10.1093/nar/gkp940gkp940 [pii] (2010).

  48. Leonardo, M.R. & Forst, S. Re-examination of the role of the periplasmic domain of EnvZ in sensing of osmolarity signals in Escherichia coli. Mol. Microbiol. 22, 405-413 (1996).

  49. Forst, S., Comeau, D., Norioka, S. & Inouye, M. Localization and membrane topology of EnvZ, a protein involved in osmoregulation of OmpF and OmpC in Escherichia coli. J. Biol. Chem. 262, 16433-16438 (1987).

  50. Roberts, D.L., Bennett, D.W. & Forst, S.A. Identification of the site of phosphorylation on the osmosensor, EnvZ, of Escherichia coli. J. Biol. Chem. 269, 8728-8733 (1994).

  51. Delgado, J., Forst, S., Harlocker, S. & Inouye, M. Identification of a phosphorylation site and functional analysis of conserved aspartic acid residues of OmpR, a transcriptional activator for ompF and ompC in Escherichia coli. Mol. Microbiol. 10, 1037-1047 (1993).

  52. Head, C.G., Tardy, A. & Kenney, L.J. Relative binding affinities of OmpR and OmpR-phosphate at the ompF and ompC regulatory sites. J. Mol. Biol. 281, 857-870, doi:S0022-2836(98)91985-4 [pii]10.1006/jmbi.1998.1985 (1998).

  53. Yoshida, T., Qin, L., Egger, L.A. & Inouye, M. Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J. Biol. Chem. 281, 17114-17123, doi:M602112200 [pii]10.1074/jbc.M602112200 (2006).

  54. Ferrario, M. et al. The leucine-responsive regulatory protein of Escherichia coli negatively regulates transcription of ompC and micF and positively regulates translation of ompF. J. Bacteriol. 177, 103-113 (1995).

  55. Olivera, B.C., Ugalde, E. & Martínez-Antonio, A. Regulatory dynamics of standard two-component systems in bacteria. J. Theor. Biol. 264, 560-569, doi:10.1016/j.jtbi.2010.02.00 8S0022-5193(10)00075-5 [pii] (2010).

  56. Mitrophanov, A.Y. & Groisman, E.A. Signal integration in bacterial two-component regulatory systems. Genes Dev.22, 2601-2611, doi:10.1101/gad.170030822/19/2601 [pii] (2008).

  57. Burkholder, W.F., Kurtser, I. & Grossman, A.D. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104, 269-279, doi:S0092-8674(01)00211-2 [pii] (2001).

  58. Wang, L., Grau, R., Perego, M. & Hoch, J.A. A novel histidine kinase inhibitor regulating development in Bacillus subtilis. Genes Dev. 11, 2569-2579 (1997).

  59. Perego, M. & Brannigan, J.A. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22, 1541-1547, doi:S0196-9781(01)00490-9 [pii] (2001).

  60. Smits, W.K. et al. Temporal separation of distinct differentiation pathways by a dual specificity Rap-Phr system in Bacillus subtilis. Mol. Microbiol. 65, 103-120, doi:MMI5776 [pii]10.1111/j.1365-2958.2007.05776.x (2007).

  61. Kato, A. & Groisman, E.A. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev. 18, 2302- 2313, doi:10.1101/gad.123080418/18/2302 [pii] (2004).

  62. Kato, A., Latifi, T. & Groisman, E.A. Closing the loop: the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc. Natl. Acad. Sci. USA 100, 4706-4711, doi:10.1073/ pnas.08368371000836837100 [pii] (2003).

  63. Kox, L.F., Wosten, M.M. & Groisman, E.A. A small protein that mediates the activation of a two-component system by another two-component system. EMBO J.19, 1861-1872, doi:10.1093/ emboj/19.8.1861 (2000).

  64. Eguchi, Y. et al. B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proc. Natl. Acad. Sci. USA104, 18712-18717, doi:0705768104 [pii]10.1073/pnas.0705768104 (2007).

  65. Pratt, L.A., Hsing, W., Gibson, K.E. & Silhavy, T.J. From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol. Microbiol. 20, 911-917 (1996).

  66. Romling, U., Sierralta, W.D., Eriksson, K. & Normark, S. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol 28, 249-264 (1998).

  67. Hung, D.L., Raivio, T.L., Jones, C.H., Silhavy, T.J. & Hultgren, S.J. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20, 1508-1518, doi:10.1093/emboj/20.7.1508 (2001).

  68. Dorel, C., Vidal, O., Prigent-Combaret, C., Vallet, I. & Lejeune, P. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett.178, 169-175, doi:S0378-1097(99)00347-X [pii] (1999).

  69. Jubelin, G. et al. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187, 2038-2049, doi:187/6/2038 [pii]10.1128/ JB.187.6.2038-2049.2005 (2005).

  70. Prigent-Combaret, C. et al. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183, 7213-7223, doi:10.1128/JB.183.24.7213-7223.2001 (2001).

  71. Prigent-Combaret, C., Vidal, O., Dorel, C. & Lejeune, P. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181, 5993-6002 (1999).

  72. Majdalani, N. & Gottesman, S. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59, 379-405, doi:10.1146/annurev.micro.59.050405.101230 (2005).

  73. Majdalani, N., Heck, M., Stout, V. & Gottesman, S. Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J. Bacteriol. 187, 6770-6778, doi:187/19/6770 [pii]10.1128/ JB.187.19.6770-6778.2005 (2005).

  74. Ferrieres, L. & Clarke, D.J. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol. Microbiol. 50, 1665-1682, doi:3815 [pii] (2003).

  75. Vianney, A. et al. Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151, 2487-2497, doi:151/7/2487 [pii]10.1099/mic.0.27913-0 (2005).

  76. Gerstel, U. & Romling, U. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res. Microbiol. 154, 659-667, doi:S0923-2508(03)00199-2 [pii]10.1016/j. resmic.2003.08.005 (2003).

  77. Gerstel, U., Park, C. & Romling, U. Complex regulation of csgD promoter activity by global regulatory proteins. Mol. Microbiol. 49, 639-654, doi:3594 [pii] (2003).

  78. Arnqvist, A., Olsen, A. & Normark, S. Sigma S-dependent growth- phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS. Mol. Microbiol. 13, 1021- 1032 (1994).

  79. Cunin, R., Glansdorff, N., Pierard, A. & Stalon, V. Biosynthesis and metabolism of arginine in bacteria. Microbiol. Rev. 50, 314-352 (1986).

  80. Burne, R.A. & Marquis, R.E. Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol. Lett. 193, 1-6, doi:S0378-1097(00)00438-9 [pii] (2000).

  81. Liu, Y., Dong, Y., Chen, Y.Y. & Burne, R.A. Environmental and growth phase regulation of the Streptococcus gordonii arginine deiminase genes. Appl. Environ. Microbiol. 74, 5023-5030, doi:10.1128/AEM.00556-08AEM.00556-08 [pii] (2008).

  82. Liu, Y. & Burne, R.A. Multiple two-component systems modulate alkali generation in Streptococcus gordonii in response to environmental stresses. J. Bacteriol. 191, 7353-7362, doi:10.1128/JB.01053-09JB.01053-09 [pii] (2009).

  83. Loomis, W. F., Shaulsky, G. & Wang, N. Histidine kinases in signal transduction pathways of eukaryotes. J. Cell Sci. 110 ( Pt 10), 1141-1145 (1997).

  84. Wurgler-Murphy, S.M. & Saito, H. Two-component signal transducers and MAPK cascades. Trends Biochem. Sci. 22, 172-176, doi:S0968000497010360 [pii] (1997).

  85. Urao, T., Yamaguchi-Shinozaki, K. & Shinozaki, K. Two- component systems in plant signal transduction. Trends Plant Sci. 5, 67-74, doi:S1360-1385(99)01542-3 [pii] (2000).

  86. Catlett, N.L., Yoder, O.C. & Turgeon, B.G. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell 2, 1151-1161 (2003).

  87. Wuichet, K., Cantwell, B.J. & Zhulin, I.B. Evolution and phyletic distribution of two-component signal transduction systems. Curr. Opin. Microbiol. 13, 219-225, doi:10.1016/j.mib.2009. 12.011S1369-5274(10)00002-0 [pii] (2010).

  88. Schaller, G.E., Shiu, S.H. & Armitage, J.P. Two-component systems and their co-option for eukaryotic signal transduction. Curr. Biol. 21, R320-330, doi:S0960-9822(11)00236-3 [pii]10.1016/j.cub.2011.02.045 (2011).

  89. Borkovich, K.A. et al. Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism. Microbiol. Mol. Biol. Rev.68, 1-108, doi:10.1128/mmbr.68.1.1-108.2004 (2004).

  90. Lu, J.M., Deschenes, R.J. & Fassler, J.S. Saccharomyces cerevisiae histidine phosphotransferase Ypd1p shuttles between the nucleus and cytoplasm for SLN1-dependent phosphorylation of Ssk1p and Skn7p. Eukaryot. Cell 2, 1304-1314 (2003).

  91. Maeda, T., Wurgler-Murphy, S.M. & Saito, H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242-245, doi:10.1038/369242a0 (1994).

  92. Bahn, Y.S. Master and commander in fungal pathogens: the two- component system and the HOG signaling pathway. Eukaryot. Cell 7, 2017-2036, doi:10.1128/EC.00323-08EC.00323-08 [pii] (2008).

  93. Catlett, N.L., Yoder, O.C. & Turgeon, B.G. Whole-Genome Analysis of Two-Component Signal Transduction Genes in Fungal Pathogens. Eukaryotic Cell 2, 1151-1161, doi:10.1128/ ec.2.6.1151-1161.2003 (2003).

  94. Jones, C.A., Greer-Phillips, S.E. & Borkovich, K.A. The Response Regulator RRG-1 Functions Upstream of a Mitogen-activated Protein Kinase Pathway Impacting Asexual Development, Female Fertility, Osmotic Stress, and Fungicide Resistance in Neurospora crassa. Mol. Biol. Cell18, 2123-2136, doi:10.1091/ mbc.E06-03-0226 (2007).

  95. Chang, C., Kwok, S.F., Bleecker, A.B. & Meyerowitz, E.M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262, 539-544 (1993).

  96. Hua, J., Chang, C., Sun, Q. & Meyerowitz, E.M. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269, 1712-1714 (1995).

  97. He, X.J., Mulford, K.E. & Fassler, J.S. Oxidative stress function of the Saccharomyces cerevisiae Skn7 receiver domain. Eukaryot. Cell 8, 768-778, doi:10.1128/EC.00021-09EC.00021-09 [pii] (2009).

  98. Li, S. et al. The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J. 17, 6952-6962, doi:10.1093/emboj/17.23.6952 (1998).

  99. Thomason, P.A. et al. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J. 17, 2838-2845, doi:10.1093/emboj/17.10.2838 (1998).

  100. Oehme, F. & Schuster, S.C. Osmotic stress-dependent serine phosphorylation of the histidine kinase homologue DokA. BMC Biochem. 2, 2 (2001).

  101. Grefen, C. & Harter, K. Plant two-component systems: principles, functions, complexity and cross talk. Planta 219, 733-742 (2004).

  102. Mizuno, T. Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci. Biotechnol. Biochem. 69, 2263-2276 (2005).

  103. Morgan, B.A. et al. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16, 1035-1044, doi:10.1093/emboj/16.5.1035 (1997).

  104. Morgan, B.A., Bouquin, N., Merrill, G.F. & Johnston, L.H. A yeast transcription factor bypassing the requirement for SBF and DSC1/MBF in budding yeast has homology to bacterial signal transduction proteins. EMBO J. 14, 5679-5689 (1995).

  105. Janiak-Spens, F., Cook, P.F. & West, A.H. Kinetic analysis of YPD1-dependent phosphotransfer reactions in the yeast osmoregulatory phosphorelay system. Biochemistry 44, 377- 386, doi:10.1021/bi048433s (2005).

  106. Horie, T., Tatebayashi, K., Yamada, R. & Saito, H. Phosphorylated Ssk1 prevents unphosphorylated Ssk1 from activating the Ssk2 mitogen-activated protein kinase kinase kinase in the yeast high-osmolarity glycerol osmoregulatory pathway. Mol. Cell Biol. 28, 5172-5183, doi:MCB.00589-08 [pii]10.1128/ MCB.00589-08 (2008).

  107. Kaserer, A.O., Andi, B., Cook, P.F. & West, A.H. Effects of osmolytes on the SLN1-YPD1-SSK1 phosphorelay system from Saccharomyces cerevisiae. Biochemistry 48, 8044-8050, doi:10.1021/bi900886g (2009).

  108. Kaserer, A.O., Andi, B., Cook, P.F. & West, A.H. Kinetic studies of the yeast His-Asp phosphorelay signaling pathway. Methods Enzymol. 471, 59-75, doi:S0076-6879(10)71004-1 [pii]10.1016/S0076-6879(10)71004-1 (2010).

  109. Fassler, J.S. & West, A.H. Genetic and biochemical analysis of the SLN1 pathway in Saccharomyces cerevisiae. Methods Enzymol. 471, 291-317, doi:S0076-6879(10)71016-8 [pii]10.1016/ S0076-6879(10)71016-8 (2010).

  110. Dziarski, R., Kashyap, D.R. & Gupta, D. Mammalian peptidoglycan recognition proteins kill bacteria by activating two-component systems and modulate microbiome and inflammation. Microb. Drug Resist.18, 280-285, doi:10.1089/mdr.2012.0002 (2012).

  111. Kashyap, D.R. et al. Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nat. Med. 17, 676-683, doi:10.1038/nm.2357nm.2357 [pii] (2011).




2020     |     www.medigraphic.com