Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 2003 Mar 1;370(Pt 2):373–389. doi: 10.1042/BJ20021547

Archaeal protein kinases and protein phosphatases: insights from genomics and biochemistry.

Peter J Kennelly 1
PMCID: PMC1223194  PMID: 12444920

Abstract

Protein phosphorylation/dephosphorylation has long been considered a recent addition to Nature's regulatory arsenal. Early studies indicated that this molecular regulatory mechanism existed only in higher eukaryotes, suggesting that protein phosphorylation/dephosphorylation had emerged to meet the particular signal-transduction requirements of multicellular organisms. Although it has since become apparent that simple eukaryotes and even bacteria are sites of protein phosphorylation/dephosphorylation, the perception widely persists that this molecular regulatory mechanism emerged late in evolution, i.e. after the divergence of the contemporary phylogenetic domains. Only highly developed cells, it was reasoned, could afford the high 'overhead' costs inherent in the acquisition of dedicated protein kinases and protein phosphatases. The advent of genome sequencing has provided an opportunity to exploit Nature's phylogenetic diversity as a vehicle for critically examining this hypothesis. In tracing the origins and evolution of protein phosphorylation/dephosphorylation, the members of the Archaea, the so-called 'third domain of life', will play a critical role. Whereas several studies have demonstrated that archaeal proteins are subject to modification by covalent phosphorylation, relatively little is known concerning the identities of the proteins affected, the impact on their functional properties, or the enzymes that catalyse these events. However, examination of several archaeal genomes has revealed the widespread presence of several ostensibly 'eukaryotic' and 'bacterial' protein kinase and protein phosphatase paradigms. Similar findings of 'phylogenetic trespass' in members of the Eucarya (eukaryotes) and the Bacteria suggest that this versatile molecular regulatory mechanism emerged at an unexpectedly early point in development of 'life as we know it'.

Full Text

The Full Text of this article is available as a PDF (254.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams J. A. Kinetic and catalytic mechanisms of protein kinases. Chem Rev. 2001 Aug;101(8):2271–2290. doi: 10.1021/cr000230w. [DOI] [PubMed] [Google Scholar]
  2. Adler E., Donella-Deana A., Arigoni F., Pinna L. A., Stragler P. Structural relationship between a bacterial developmental protein and eukaryotic PP2C protein phosphatases. Mol Microbiol. 1997 Jan;23(1):57–62. doi: 10.1046/j.1365-2958.1997.1801552.x. [DOI] [PubMed] [Google Scholar]
  3. Aggen J. B., Nairn A. C., Chamberlin R. Regulation of protein phosphatase-1. Chem Biol. 2000 Jan;7(1):R13–R23. doi: 10.1016/s1074-5521(00)00069-7. [DOI] [PubMed] [Google Scholar]
  4. Aizawa S. I., Harwood C. S., Kadner R. J. Signaling components in bacterial locomotion and sensory reception. J Bacteriol. 2000 Mar;182(6):1459–1471. doi: 10.1128/jb.182.6.1459-1471.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Andersson S. G., Kurland C. G. Reductive evolution of resident genomes. Trends Microbiol. 1998 Jul;6(7):263–268. doi: 10.1016/s0966-842x(98)01312-2. [DOI] [PubMed] [Google Scholar]
  6. Angermayr Michaela, Roidl Andreas, Bandlow Wolfhard. Yeast Rio1p is the founding member of a novel subfamily of protein serine kinases involved in the control of cell cycle progression. Mol Microbiol. 2002 Apr;44(2):309–324. doi: 10.1046/j.1365-2958.2002.02881.x. [DOI] [PubMed] [Google Scholar]
  7. Bada Jeffrey L., Lazcano Antonio. Origin of life. Some like it hot, but not the first biomolecules. Science. 2002 Jun 14;296(5575):1982–1983. doi: 10.1126/science.1069487. [DOI] [PubMed] [Google Scholar]
  8. Barford D., Jia Z., Tonks N. K. Protein tyrosine phosphatases take off. Nat Struct Biol. 1995 Dec;2(12):1043–1053. doi: 10.1038/nsb1295-1043. [DOI] [PubMed] [Google Scholar]
  9. Barford D. Molecular mechanisms of the protein serine/threonine phosphatases. Trends Biochem Sci. 1996 Nov;21(11):407–412. doi: 10.1016/s0968-0004(96)10060-8. [DOI] [PubMed] [Google Scholar]
  10. Barton G. J., Cohen P. T., Barford D. Conservation analysis and structure prediction of the protein serine/threonine phosphatases. Sequence similarity with diadenosine tetraphosphatase from Escherichia coli suggests homology to the protein phosphatases. Eur J Biochem. 1994 Feb 15;220(1):225–237. doi: 10.1111/j.1432-1033.1994.tb18618.x. [DOI] [PubMed] [Google Scholar]
  11. Bischoff K. M., Kennelly P. J. "In-gel" assay for identifying alternative nucleotide substrates for protein kinases. Anal Biochem. 1999 Jul 1;271(2):199–202. doi: 10.1006/abio.1999.4150. [DOI] [PubMed] [Google Scholar]
  12. Bork P., Brown N. P., Hegyi H., Schultz J. The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci. 1996 Jul;5(7):1421–1425. doi: 10.1002/pro.5560050720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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. 1989 May 5;264(13):7085–7088. [PubMed] [Google Scholar]
  14. Bourret Robert B., Stock Ann M. Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem. 2002 Jan 4;277(12):9625–9628. doi: 10.1074/jbc.R100066200. [DOI] [PubMed] [Google Scholar]
  15. Bray D. Protein molecules as computational elements in living cells. Nature. 1995 Jul 27;376(6538):307–312. doi: 10.1038/376307a0. [DOI] [PubMed] [Google Scholar]
  16. Brock T. D., Brock K. M., Belly R. T., Weiss R. L. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol. 1972;84(1):54–68. doi: 10.1007/BF00408082. [DOI] [PubMed] [Google Scholar]
  17. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. doi: 10.1126/science.273.5278.1058. [DOI] [PubMed] [Google Scholar]
  18. Burda P., Aebi M. The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta. 1999 Jan 6;1426(2):239–257. doi: 10.1016/s0304-4165(98)00127-5. [DOI] [PubMed] [Google Scholar]
  19. Cech T. R. The efficiency and versatility of catalytic RNA: implications for an RNA world. Gene. 1993 Dec 15;135(1-2):33–36. doi: 10.1016/0378-1119(93)90046-6. [DOI] [PubMed] [Google Scholar]
  20. Clancy C. E., Mendoza M. G., Naismith T. V., Kolman M. F., Egelhoff T. T. Identification of a protein kinase from Dictyostelium with homology to the novel catalytic domain of myosin heavy chain kinase A. J Biol Chem. 1997 May 2;272(18):11812–11815. doi: 10.1074/jbc.272.18.11812. [DOI] [PubMed] [Google Scholar]
  21. Cohen P. T., Cohen P. Discovery of a protein phosphatase activity encoded in the genome of bacteriophage lambda. Probable identity with open reading frame 221. Biochem J. 1989 Jun 15;260(3):931–934. doi: 10.1042/bj2600931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Cohen P. T. Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem Sci. 1997 Jul;22(7):245–251. doi: 10.1016/s0968-0004(97)01060-8. [DOI] [PubMed] [Google Scholar]
  23. Cohen P. Classification of protein-serine/threonine phosphatases: identification and quantitation in cell extracts. Methods Enzymol. 1991;201:389–398. doi: 10.1016/0076-6879(91)01035-z. [DOI] [PubMed] [Google Scholar]
  24. Condò I., Ruggero D., Reinhardt R., Londei P. A novel aminopeptidase associated with the 60 kDa chaperonin in the thermophilic archaeon Sulfolobus solfataricus. Mol Microbiol. 1998 Aug;29(3):775–785. doi: 10.1046/j.1365-2958.1998.00971.x. [DOI] [PubMed] [Google Scholar]
  25. Cozzone A. J. Protein phosphorylation in prokaryotes. Annu Rev Microbiol. 1988;42:97–125. doi: 10.1146/annurev.mi.42.100188.000525. [DOI] [PubMed] [Google Scholar]
  26. Daas P. J., Wassenaar R. W., Willemsen P., Theunissen R. J., Keltjens J. T., van der Drift C., Vogels G. D. Purification and properties of an enzyme involved in the ATP-dependent activation of the methanol:2-mercaptoethanesulfonic acid methyltransferase reaction in Methanosarcina barkeri. J Biol Chem. 1996 Sep 13;271(37):22339–22345. doi: 10.1074/jbc.271.37.22339. [DOI] [PubMed] [Google Scholar]
  27. Das A. K., Helps N. R., Cohen P. T., Barford D. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J. 1996 Dec 16;15(24):6798–6809. [PMC free article] [PubMed] [Google Scholar]
  28. Denu J. M., Dixon J. E. Protein tyrosine phosphatases: mechanisms of catalysis and regulation. Curr Opin Chem Biol. 1998 Oct;2(5):633–641. doi: 10.1016/s1367-5931(98)80095-1. [DOI] [PubMed] [Google Scholar]
  29. Doolittle R. F. The origins and evolution of eukaryotic proteins. Philos Trans R Soc Lond B Biol Sci. 1995 Sep 29;349(1329):235–240. doi: 10.1098/rstb.1995.0107. [DOI] [PubMed] [Google Scholar]
  30. Doolittle W. F. Lateral genomics. Trends Cell Biol. 1999 Dec;9(12):M5–M8. [PubMed] [Google Scholar]
  31. Eichler J. Novel glycoproteins of the halophilic archaeon Haloferax volcanii. Arch Microbiol. 2000 May-Jun;173(5-6):445–448. doi: 10.1007/s002030000152. [DOI] [PubMed] [Google Scholar]
  32. Elferink M. G., Albers S. V., Konings W. N., Driessen A. J. Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters. Mol Microbiol. 2001 Mar;39(6):1494–1503. doi: 10.1046/j.1365-2958.2001.02336.x. [DOI] [PubMed] [Google Scholar]
  33. Facchin Sonia, Sarno Stefania, Marin Oriano, Lopreiato Raffaele, Sartori Geppo, Pinna Lorenzo A. Acidophilic character of yeast PID261/BUD32, a putative ancestor of eukaryotic protein kinases. Biochem Biophys Res Commun. 2002 Sep 6;296(5):1366–1371. doi: 10.1016/s0006-291x(02)02090-9. [DOI] [PubMed] [Google Scholar]
  34. Fauman E. B., Cogswell J. P., Lovejoy B., Rocque W. J., Holmes W., Montana V. G., Piwnica-Worms H., Rink M. J., Saper M. A. Crystal structure of the catalytic domain of the human cell cycle control phosphatase, Cdc25A. Cell. 1998 May 15;93(4):617–625. doi: 10.1016/s0092-8674(00)81190-3. [DOI] [PubMed] [Google Scholar]
  35. Fauman E. B., Saper M. A. Structure and function of the protein tyrosine phosphatases. Trends Biochem Sci. 1996 Nov;21(11):413–417. doi: 10.1016/s0968-0004(96)10059-1. [DOI] [PubMed] [Google Scholar]
  36. Galinier A., Kravanja M., Engelmann R., Hengstenberg W., Kilhoffer M. C., Deutscher J., Haiech J. New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1823–1828. doi: 10.1073/pnas.95.4.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Goldman S., Hecht K., Eisenberg H., Mevarech M. Extracellular Ca2(+)-dependent inducible alkaline phosphatase from extremely halophilic archaebacterium Haloarcula marismortui. J Bacteriol. 1990 Dec;172(12):7065–7070. doi: 10.1128/jb.172.12.7065-7070.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Grabowski B., Kelman Z. Autophosphorylation of archaeal Cdc6 homologues is regulated by DNA. J Bacteriol. 2001 Sep;183(18):5459–5464. doi: 10.1128/JB.183.18.5459-5464.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Guan K. L., Dixon J. E. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science. 1990 Aug 3;249(4968):553–556. doi: 10.1126/science.2166336. [DOI] [PubMed] [Google Scholar]
  40. Hanks S. K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 1995 May;9(8):576–596. [PubMed] [Google Scholar]
  41. Hanks S. K., Lindberg R. A. Use of degenerate oligonucleotide probes to identify clones that encode protein kinases. Methods Enzymol. 1991;200:525–532. doi: 10.1016/0076-6879(91)00168-v. [DOI] [PubMed] [Google Scholar]
  42. Harris R. A., Popov K. M., Zhao Y., Kedishvili N. Y., Shimomura Y., Crabb D. W. A new family of protein kinases--the mitochondrial protein kinases. Adv Enzyme Regul. 1995;35:147–162. doi: 10.1016/0065-2571(94)00020-4. [DOI] [PubMed] [Google Scholar]
  43. Helmstaedt K., Krappmann S., Braus G. H. Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase. Microbiol Mol Biol Rev. 2001 Sep;65(3):404-21, table of contents. doi: 10.1128/MMBR.65.3.404-421.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Hess J. F., Oosawa K., Kaplan N., Simon M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell. 1988 Apr 8;53(1):79–87. doi: 10.1016/0092-8674(88)90489-8. [DOI] [PubMed] [Google Scholar]
  45. Hoch J. A. Two-component and phosphorelay signal transduction. Curr Opin Microbiol. 2000 Apr;3(2):165–170. doi: 10.1016/s1369-5274(00)00070-9. [DOI] [PubMed] [Google Scholar]
  46. Hon W. C., McKay G. A., Thompson P. R., Sweet R. M., Yang D. S., Wright G. D., Berghuis A. M. Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases. Cell. 1997 Jun 13;89(6):887–895. doi: 10.1016/s0092-8674(00)80274-3. [DOI] [PubMed] [Google Scholar]
  47. Hooft van Huijsduijnen R. Protein tyrosine phosphatases: counting the trees in the forest. Gene. 1998 Dec 28;225(1-2):1–8. doi: 10.1016/s0378-1119(98)00513-7. [DOI] [PubMed] [Google Scholar]
  48. Huse Morgan, Kuriyan John. The conformational plasticity of protein kinases. Cell. 2002 May 3;109(3):275–282. doi: 10.1016/s0092-8674(02)00741-9. [DOI] [PubMed] [Google Scholar]
  49. Igo M. M., Ninfa A. J., Stock J. B., Silhavy T. J. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev. 1989 Nov;3(11):1725–1734. doi: 10.1101/gad.3.11.1725. [DOI] [PubMed] [Google Scholar]
  50. Irmler A., Forchhammer K. A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. Proc Natl Acad Sci U S A. 2001 Oct 30;98(23):12978–12983. doi: 10.1073/pnas.231254998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Jeon Sung-Jong, Fujiwara Shinsuke, Takagi Masahiro, Tanaka Takeshi, Imanaka Tadayuki. Tk-PTP, protein tyrosine/serine phosphatase from hyperthermophilic archaeon Thermococcus kodakaraensis KOD1: enzymatic characteristics and identification of its substrate proteins. Biochem Biophys Res Commun. 2002 Jul 12;295(2):508–514. doi: 10.1016/s0006-291x(02)00705-2. [DOI] [PubMed] [Google Scholar]
  52. Johnson L. N., Lewis R. J. Structural basis for control by phosphorylation. Chem Rev. 2001 Aug;101(8):2209–2242. doi: 10.1021/cr000225s. [DOI] [PubMed] [Google Scholar]
  53. Johnson L. N., Noble M. E., Owen D. J. Active and inactive protein kinases: structural basis for regulation. Cell. 1996 Apr 19;85(2):149–158. doi: 10.1016/s0092-8674(00)81092-2. [DOI] [PubMed] [Google Scholar]
  54. Johnston M. The complete code for a eukaryotic cell. Genome sequencing. Curr Biol. 1996 May 1;6(5):500–503. doi: 10.1016/s0960-9822(02)00526-2. [DOI] [PubMed] [Google Scholar]
  55. Jung K. H., Spudich E. N., Trivedi V. D., Spudich J. L. An archaeal photosignal-transducing module mediates phototaxis in Escherichia coli. J Bacteriol. 2001 Nov;183(21):6365–6371. doi: 10.1128/JB.183.21.6365-6371.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Kawarabayasi Y., Hino Y., Horikawa H., Yamazaki S., Haikawa Y., Jin-no K., Takahashi M., Sekine M., Baba S., Ankai A. Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 1999 Apr 30;6(2):83-101, 145-52. doi: 10.1093/dnares/6.2.83. [DOI] [PubMed] [Google Scholar]
  57. Kawarabayasi Y., Sawada M., Horikawa H., Haikawa Y., Hino Y., Yamamoto S., Sekine M., Baba S., Kosugi H., Hosoyama A. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res. 1998 Apr 30;5(2):55–76. doi: 10.1093/dnares/5.2.55. [DOI] [PubMed] [Google Scholar]
  58. Kawashima T., Amano N., Koike H., Makino S., Higuchi S., Kawashima-Ohya Y., Watanabe K., Yamazaki M., Kanehori K., Kawamoto T. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14257–14262. doi: 10.1073/pnas.97.26.14257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Keener J., Kustu S. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci U S A. 1988 Jul;85(14):4976–4980. doi: 10.1073/pnas.85.14.4976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Kennelly P. J., Krebs E. G. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J Biol Chem. 1991 Aug 25;266(24):15555–15558. [PubMed] [Google Scholar]
  61. Kennelly P. J., Oxenrider K. A., Leng J., Cantwell J. S., Zhao N. Identification of a serine/threonine-specific protein phosphatase from the archaebacterium Sulfolobus solfataricus. J Biol Chem. 1993 Mar 25;268(9):6505–6510. [PubMed] [Google Scholar]
  62. Kennelly P. J., Potts M. Fancy meeting you here! A fresh look at "prokaryotic" protein phosphorylation. J Bacteriol. 1996 Aug;178(16):4759–4764. doi: 10.1128/jb.178.16.4759-4764.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Kennelly P. J. Protein phosphatases--a phylogenetic perspective. Chem Rev. 2001 Aug;101(8):2291–2312. doi: 10.1021/cr0002543. [DOI] [PubMed] [Google Scholar]
  64. Kennelly Peter J. Protein kinases and protein phosphatases in prokaryotes: a genomic perspective. FEMS Microbiol Lett. 2002 Jan 2;206(1):1–8. doi: 10.1111/j.1574-6968.2002.tb10978.x. [DOI] [PubMed] [Google Scholar]
  65. Kim D., Forst S. Genomic analysis of the histidine kinase family in bacteria and archaea. Microbiology. 2001 May;147(Pt 5):1197–1212. doi: 10.1099/00221287-147-5-1197. [DOI] [PubMed] [Google Scholar]
  66. Klenk H. P., Clayton R. A., Tomb J. F., White O., Nelson K. E., Ketchum K. A., Dodson R. J., Gwinn M., Hickey E. K., Peterson J. D. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997 Nov 27;390(6658):364–370. doi: 10.1038/37052. [DOI] [PubMed] [Google Scholar]
  67. Koretke K. K., Lupas A. N., Warren P. V., Rosenberg M., Brown J. R. Evolution of two-component signal transduction. Mol Biol Evol. 2000 Dec;17(12):1956–1970. doi: 10.1093/oxfordjournals.molbev.a026297. [DOI] [PubMed] [Google Scholar]
  68. Krupa A., Srinivasan N. Lipopolysaccharide phosphorylating enzymes encoded in the genomes of Gram-negative bacteria are related to the eukaryotic protein kinases. Protein Sci. 2002 Jun;11(6):1580–1584. doi: 10.1110/ps.3560102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. LaPorte D. C. The isocitrate dehydrogenase phosphorylation cycle: regulation and enzymology. J Cell Biochem. 1993 Jan;51(1):14–18. doi: 10.1002/jcb.240510104. [DOI] [PubMed] [Google Scholar]
  70. Leng J., Cameron A. J., Buckel S., Kennelly P. J. Isolation and cloning of a protein-serine/threonine phosphatase from an archaeon. J Bacteriol. 1995 Nov;177(22):6510–6517. doi: 10.1128/jb.177.22.6510-6517.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Leonard C. J., Aravind L., Koonin E. V. Novel families of putative protein kinases in bacteria and archaea: evolution of the "eukaryotic" protein kinase superfamily. Genome Res. 1998 Oct;8(10):1038–1047. doi: 10.1101/gr.8.10.1038. [DOI] [PubMed] [Google Scholar]
  72. Levitzki A., Gazit A. Tyrosine kinase inhibition: an approach to drug development. Science. 1995 Mar 24;267(5205):1782–1788. doi: 10.1126/science.7892601. [DOI] [PubMed] [Google Scholar]
  73. Li Y., Strohl W. R. Cloning, purification, and properties of a phosphotyrosine protein phosphatase from Streptomyces coelicolor A3(2). J Bacteriol. 1996 Jan;178(1):136–142. doi: 10.1128/jb.178.1.136-142.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Lim Wendell A. The modular logic of signaling proteins: building allosteric switches from simple binding domains. Curr Opin Struct Biol. 2002 Feb;12(1):61–68. doi: 10.1016/s0959-440x(02)00290-7. [DOI] [PubMed] [Google Scholar]
  75. Liu J., Rosen B. P. Ligand interactions of the ArsC arsenate reductase. J Biol Chem. 1997 Aug 22;272(34):21084–21089. doi: 10.1074/jbc.272.34.21084. [DOI] [PubMed] [Google Scholar]
  76. Lohse D. L., Denu J. M., Dixon J. E. Insights derived from the structures of the Ser/Thr phosphatases calcineurin and protein phosphatase 1. Structure. 1995 Oct 15;3(10):987–990. doi: 10.1016/s0969-2126(01)00234-9. [DOI] [PubMed] [Google Scholar]
  77. Lower B. H., Bischoff K. M., Kennelly P. J. The archaeon Sulfolobus solfataricus contains a membrane-associated protein kinase activity that preferentially phosphorylates threonine residues in vitro. J Bacteriol. 2000 Jun;182(12):3452–3459. doi: 10.1128/jb.182.12.3452-3459.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Lower Brian H., Kennelly Peter J. The membrane-associated protein-serine/threonine kinase from Sulfolobus solfataricus is a glycoprotein. J Bacteriol. 2002 May;184(10):2614–2619. doi: 10.1128/JB.184.10.2614-2619.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Lübben M., Schäfer G. Chemiosmotic energy conversion of the archaebacterial thermoacidophile Sulfolobus acidocaldarius: oxidative phosphorylation and the presence of an F0-related N,N'-dicyclohexylcarbodiimide-binding proteolipid. J Bacteriol. 1989 Nov;171(11):6106–6116. doi: 10.1128/jb.171.11.6106-6116.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. MILLER S. L. A production of amino acids under possible primitive earth conditions. Science. 1953 May 15;117(3046):528–529. doi: 10.1126/science.117.3046.528. [DOI] [PubMed] [Google Scholar]
  81. MacKintosh C., MacKintosh R. W. Inhibitors of protein kinases and phosphatases. Trends Biochem Sci. 1994 Nov;19(11):444–448. doi: 10.1016/0968-0004(94)90127-9. [DOI] [PubMed] [Google Scholar]
  82. Maehama T., Dixon J. E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem. 1998 May 29;273(22):13375–13378. doi: 10.1074/jbc.273.22.13375. [DOI] [PubMed] [Google Scholar]
  83. Mai B., Frey G., Swanson R. V., Mathur E. J., Stetter K. O. Molecular cloning and functional expression of a protein-serine/threonine phosphatase from the hyperthermophilic archaeon Pyrodictium abyssi TAG11. J Bacteriol. 1998 Aug;180(16):4030–4035. doi: 10.1128/jb.180.16.4030-4035.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Martell K. J., Angelotti T., Ullrich A. The "VH1-like" dual-specificity protein tyrosine phosphatases. Mol Cells. 1998 Feb 28;8(1):2–11. [PubMed] [Google Scholar]
  85. Mattevi A., Rizzi M., Bolognesi M. New structures of allosteric proteins revealing remarkable conformational changes. Curr Opin Struct Biol. 1996 Dec;6(6):824–829. doi: 10.1016/s0959-440x(96)80013-3. [DOI] [PubMed] [Google Scholar]
  86. Millward T. A., Zolnierowicz S., Hemmings B. A. Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem Sci. 1999 May;24(5):186–191. doi: 10.1016/s0968-0004(99)01375-4. [DOI] [PubMed] [Google Scholar]
  87. Min K. T., Hilditch C. M., Diederich B., Errington J., Yudkin M. D. Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell. 1993 Aug 27;74(4):735–742. doi: 10.1016/0092-8674(93)90520-z. [DOI] [PubMed] [Google Scholar]
  88. Missiakas D., Raina S. Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli: role of two new phosphoprotein phosphatases PrpA and PrpB. EMBO J. 1997 Apr 1;16(7):1670–1685. doi: 10.1093/emboj/16.7.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Moens S., Vanderleyden J. Glycoproteins in prokaryotes. Arch Microbiol. 1997 Sep;168(3):169–175. doi: 10.1007/s002030050484. [DOI] [PubMed] [Google Scholar]
  90. Monod J. From enzymatic adaptation to allosteric transitions. Science. 1966 Oct 28;154(3748):475–483. doi: 10.1126/science.154.3748.475. [DOI] [PubMed] [Google Scholar]
  91. Mushegian A. R., Koonin E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10268–10273. doi: 10.1073/pnas.93.19.10268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Ng W. V., Kennedy S. P., Mahairas G. G., Berquist B., Pan M., Shukla H. D., Lasky S. R., Baliga N. S., Thorsson V., Sbrogna J. Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12176–12181. doi: 10.1073/pnas.190337797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Nilsson I., Hoffmann I. Cell cycle regulation by the Cdc25 phosphatase family. Prog Cell Cycle Res. 2000;4:107–114. doi: 10.1007/978-1-4615-4253-7_10. [DOI] [PubMed] [Google Scholar]
  94. Olsen G. J., Woese C. R. Ribosomal RNA: a key to phylogeny. FASEB J. 1993 Jan;7(1):113–123. doi: 10.1096/fasebj.7.1.8422957. [DOI] [PubMed] [Google Scholar]
  95. Osorio G., Jerez C. A. Adaptive response of the archaeon Sulfolobus acidocaldarius BC65 to phosphate starvation. Microbiology. 1996 Jun;142(Pt 6):1531–1536. doi: 10.1099/13500872-142-6-1531. [DOI] [PubMed] [Google Scholar]
  96. Oxenrider K. A., Kennelly P. J. A protein-serine phosphatase from the halophilic archaeon Haloferax volcanii. Biochem Biophys Res Commun. 1993 Aug 16;194(3):1330–1335. doi: 10.1006/bbrc.1993.1970. [DOI] [PubMed] [Google Scholar]
  97. Oxenrider K. A., Rasche M. E., Thorsteinsson M. V., Kennelly P. J. Inhibition of an archaeal protein phosphatase activity by okadaic acid, microcystin-LR, or calyculin A. FEBS Lett. 1993 Oct 4;331(3):291–295. doi: 10.1016/0014-5793(93)80355-x. [DOI] [PubMed] [Google Scholar]
  98. Perego M. Kinase-phosphatase competition regulates Bacillus subtilis development. Trends Microbiol. 1998 Sep;6(9):366–370. doi: 10.1016/s0966-842x(98)01350-x. [DOI] [PubMed] [Google Scholar]
  99. Perutz M. F. Mechanisms of cooperativity and allosteric regulation in proteins. Q Rev Biophys. 1989 May;22(2):139–237. doi: 10.1017/s0033583500003826. [DOI] [PubMed] [Google Scholar]
  100. Peterson J. D., Umayam L. A., Dickinson T., Hickey E. K., White O. The Comprehensive Microbial Resource. Nucleic Acids Res. 2001 Jan 1;29(1):123–125. doi: 10.1093/nar/29.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Pinna L. A. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim Biophys Acta. 1990 Sep 24;1054(3):267–284. doi: 10.1016/0167-4889(90)90098-x. [DOI] [PubMed] [Google Scholar]
  102. Plowman G. D., Sudarsanam S., Bingham J., Whyte D., Hunter T. The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13603–13610. doi: 10.1073/pnas.96.24.13603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Ponting C. P., Aravind L., Schultz J., Bork P., Koonin E. V. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol. 1999 Jun 18;289(4):729–745. doi: 10.1006/jmbi.1999.2827. [DOI] [PubMed] [Google Scholar]
  104. Potts M., Sun H., Mockaitis K., Kennelly P. J., Reed D., Tonks N. K. A protein-tyrosine/serine phosphatase encoded by the genome of the cyanobacterium Nostoc commune UTEX 584. J Biol Chem. 1993 Apr 15;268(11):7632–7635. [PubMed] [Google Scholar]
  105. Ramponi G., Stefani M. Structural, catalytic, and functional properties of low M(r), phosphotyrosine protein phosphatases. Evidence of a long evolutionary history. Int J Biochem Cell Biol. 1997 Feb;29(2):279–292. doi: 10.1016/s1357-2725(96)00109-4. [DOI] [PubMed] [Google Scholar]
  106. Reichard Peter. Ribonucleotide reductases: the evolution of allosteric regulation. Arch Biochem Biophys. 2002 Jan 15;397(2):149–155. doi: 10.1006/abbi.2001.2637. [DOI] [PubMed] [Google Scholar]
  107. Reizer J., Hoischen C., Titgemeyer F., Rivolta C., Rabus R., Stülke J., Karamata D., Saier M. H., Jr, Hillen W. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol. 1998 Mar;27(6):1157–1169. doi: 10.1046/j.1365-2958.1998.00747.x. [DOI] [PubMed] [Google Scholar]
  108. Reizer J., Reizer A., Perego M., Saier M. H., Jr Characterization of a family of bacterial response regulator aspartyl-phosphate (RAP) phosphatases. Microb Comp Genomics. 1997;2(2):103–111. doi: 10.1089/omi.1.1997.2.103. [DOI] [PubMed] [Google Scholar]
  109. Roach P. J. Multisite and hierarchal protein phosphorylation. J Biol Chem. 1991 Aug 5;266(22):14139–14142. [PubMed] [Google Scholar]
  110. Rubin G. M., Yandell M. D., Wortman J. R., Gabor Miklos G. L., Nelson C. R., Hariharan I. K., Fortini M. E., Li P. W., Apweiler R., Fleischmann W. Comparative genomics of the eukaryotes. Science. 2000 Mar 24;287(5461):2204–2215. doi: 10.1126/science.287.5461.2204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Rudolph J., Oesterhelt D. Chemotaxis and phototaxis require a CheA histidine kinase in the archaeon Halobacterium salinarium. EMBO J. 1995 Feb 15;14(4):667–673. doi: 10.1002/j.1460-2075.1995.tb07045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Rudolph J., Oesterhelt D. Deletion analysis of the che operon in the archaeon Halobacterium salinarium. J Mol Biol. 1996 May 17;258(4):548–554. doi: 10.1006/jmbi.1996.0267. [DOI] [PubMed] [Google Scholar]
  113. Rudolph J., Tolliday N., Schmitt C., Schuster S. C., Oesterhelt D. Phosphorylation in halobacterial signal transduction. EMBO J. 1995 Sep 1;14(17):4249–4257. doi: 10.1002/j.1460-2075.1995.tb00099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Ruepp A., Graml W., Santos-Martinez M. L., Koretke K. K., Volker C., Mewes H. W., Frishman D., Stocker S., Lupas A. N., Baumeister W. The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature. 2000 Sep 28;407(6803):508–513. doi: 10.1038/35035069. [DOI] [PubMed] [Google Scholar]
  115. Saito H. Histidine phosphorylation and two-component signaling in eukaryotic cells. Chem Rev. 2001 Aug;101(8):2497–2509. doi: 10.1021/cr000243+. [DOI] [PubMed] [Google Scholar]
  116. Sala-Newby G. B., Campbell A. K. Engineering a bioluminescent indicator for cyclic AMP-dependent protein kinase. Biochem J. 1991 Nov 1;279(Pt 3):727–732. doi: 10.1042/bj2790727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Sanwal B. D. Allosteric controls of amphilbolic pathways in bacteria. Bacteriol Rev. 1970 Mar;34(1):20–39. doi: 10.1128/br.34.1.20-39.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Schäffer C., Messner P. Glycobiology of surface layer proteins. Biochimie. 2001 Jul;83(7):591–599. doi: 10.1016/s0300-9084(01)01299-8. [DOI] [PubMed] [Google Scholar]
  119. Shaw K. J., Rather P. N., Hare R. S., Miller G. H. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol Rev. 1993 Mar;57(1):138–163. doi: 10.1128/mr.57.1.138-163.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. She Q., Singh R. K., Confalonieri F., Zivanovic Y., Allard G., Awayez M. J., Chan-Weiher C. C., Clausen I. G., Curtis B. A., De Moors A. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A. 2001 Jun 26;98(14):7835–7840. doi: 10.1073/pnas.141222098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Shi L., Bischoff K. M., Kennelly P. J. The icfG gene cluster of Synechocystis sp. strain PCC 6803 encodes an Rsb/Spo-like protein kinase, protein phosphatase, and two phosphoproteins. J Bacteriol. 1999 Aug;181(16):4761–4767. doi: 10.1128/jb.181.16.4761-4767.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Shi L., Carmichael W. W., Kennelly P. J. Cyanobacterial PPP family protein phosphatases possess multifunctional capabilities and are resistant to microcystin-LR. J Biol Chem. 1999 Apr 9;274(15):10039–10046. doi: 10.1074/jbc.274.15.10039. [DOI] [PubMed] [Google Scholar]
  123. Shi L., Potts M., Kennelly P. J. The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol Rev. 1998 Oct;22(4):229–253. doi: 10.1111/j.1574-6976.1998.tb00369.x. [DOI] [PubMed] [Google Scholar]
  124. Skorko R. Polyphosphate as a source of phosphoryl group in protein modification in the archaebacterium Sulfolobus acidocaldarius. Biochimie. 1989 Sep-Oct;71(9-10):1089–1093. doi: 10.1016/0300-9084(89)90115-6. [DOI] [PubMed] [Google Scholar]
  125. Skórko R. Protein phosphorylation in the archaebacterium Sulfolobus acidocaldarius. Eur J Biochem. 1984 Dec 17;145(3):617–622. doi: 10.1111/j.1432-1033.1984.tb08601.x. [DOI] [PubMed] [Google Scholar]
  126. Smith D. R., Doucette-Stamm L. A., Deloughery C., Lee H., Dubois J., Aldredge T., Bashirzadeh R., Blakely D., Cook R., Gilbert K. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol. 1997 Nov;179(22):7135–7155. doi: 10.1128/jb.179.22.7135-7155.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Smith S. C., Kennelly P. J., Potts M. Protein-tyrosine phosphorylation in the Archaea. J Bacteriol. 1997 Apr;179(7):2418–2420. doi: 10.1128/jb.179.7.2418-2420.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Solow B., Bischoff K. M., Zylka M. J., Kennelly P. J. Archael phosphoproteins. Identification of a hexosephosphate mutase and the alpha-subunit of succinyl-CoA synthetase in the extreme acidothermophile Sulfolobus solfataricus. Protein Sci. 1998 Jan;7(1):105–111. doi: 10.1002/pro.5560070111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Solow B., Young J. C., Kennelly P. J. Gene cloning and expression and characterization of a toxin-sensitive protein phosphatase from the methanogenic archaeon Methanosarcina thermophila TM-1. J Bacteriol. 1997 Aug;179(16):5072–5075. doi: 10.1128/jb.179.16.5072-5075.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Spudich E. N., Spudich J. L. Photosensitive phosphoproteins in Halobacteria: regulatory coupling of transmembrane proton flux and protein dephosphorylation. J Cell Biol. 1981 Dec;91(3 Pt 1):895–900. doi: 10.1083/jcb.91.3.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Spudich J. L., Stoeckenius W. Light-regulated retinal-dependent reversible phosphorylation of Halobacterium proteins. J Biol Chem. 1980 Jun 25;255(12):5501–5503. [PubMed] [Google Scholar]
  132. Stadtman E. R. Allosteric regulation of enzyme activity. Adv Enzymol Relat Areas Mol Biol. 1966;28:41–154. doi: 10.1002/9780470122730.ch2. [DOI] [PubMed] [Google Scholar]
  133. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Szathmáry E. The origin of the genetic code: amino acids as cofactors in an RNA world. Trends Genet. 1999 Jun;15(6):223–229. doi: 10.1016/s0168-9525(99)01730-8. [DOI] [PubMed] [Google Scholar]
  135. Takagi T., Moore C. R., Diehn F., Buratowski S. An RNA 5'-triphosphatase related to the protein tyrosine phosphatases. Cell. 1997 Jun 13;89(6):867–873. doi: 10.1016/s0092-8674(00)80272-x. [DOI] [PubMed] [Google Scholar]
  136. Taylor G. S., Maehama T., Dixon J. E. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8910–8915. doi: 10.1073/pnas.160255697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Taylor S. S., Knighton D. R., Zheng J., Sowadski J. M., Gibbs C. S., Zoller M. J. A template for the protein kinase family. Trends Biochem Sci. 1993 Mar;18(3):84–89. doi: 10.1016/0968-0004(93)80001-r. [DOI] [PubMed] [Google Scholar]
  138. Treuner-Lange A., Ward M. J., Zusman D. R. Pph1 from Myxococcus xanthus is a protein phosphatase involved in vegetative growth and development. Mol Microbiol. 2001 Apr;40(1):126–140. doi: 10.1046/j.1365-2958.2001.02362.x. [DOI] [PubMed] [Google Scholar]
  139. Virshup D. M. Protein phosphatase 2A: a panoply of enzymes. Curr Opin Cell Biol. 2000 Apr;12(2):180–185. doi: 10.1016/s0955-0674(99)00074-5. [DOI] [PubMed] [Google Scholar]
  140. Wang J. Y., Koshland D. E., Jr Evidence for protein kinase activities in the prokaryote Salmonella typhimurium. J Biol Chem. 1978 Nov 10;253(21):7605–7608. [PubMed] [Google Scholar]
  141. Weiss V., Magasanik B. Phosphorylation of nitrogen regulator I (NRI) of Escherichia coli. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8919–8923. doi: 10.1073/pnas.85.23.8919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Weng G., Bhalla U. S., Iyengar R. Complexity in biological signaling systems. Science. 1999 Apr 2;284(5411):92–96. doi: 10.1126/science.284.5411.92. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Westheimer F. H. Why nature chose phosphates. Science. 1987 Mar 6;235(4793):1173–1178. doi: 10.1126/science.2434996. [DOI] [PubMed] [Google Scholar]
  144. Woese Carl R. On the evolution of cells. Proc Natl Acad Sci U S A. 2002 Jun 19;99(13):8742–8747. doi: 10.1073/pnas.132266999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Wu J., Ohta N., Zhao J. L., Newton A. A novel bacterial tyrosine kinase essential for cell division and differentiation. Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13068–13073. doi: 10.1073/pnas.96.23.13068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Yang X., Kang C. M., Brody M. S., Price C. W. Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 1996 Sep 15;10(18):2265–2275. doi: 10.1101/gad.10.18.2265. [DOI] [PubMed] [Google Scholar]
  147. Yeh K. C., Lagarias J. C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13976–13981. doi: 10.1073/pnas.95.23.13976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Zegers I., Martins J. C., Willem R., Wyns L., Messens J. Arsenate reductase from S. aureus plasmid pI258 is a phosphatase drafted for redox duty. Nat Struct Biol. 2001 Oct;8(10):843–847. doi: 10.1038/nsb1001-843. [DOI] [PubMed] [Google Scholar]
  149. Zhang W., Inouye M., Inouye S. Reciprocal regulation of the differentiation of Myxococcus xanthus by Pkn5 and Pkn6, eukaryotic-like Ser/Thr protein kinases. Mol Microbiol. 1996 Apr;20(2):435–447. doi: 10.1111/j.1365-2958.1996.tb02630.x. [DOI] [PubMed] [Google Scholar]
  150. Zhang Z. Y. Structure, mechanism, and specificity of protein-tyrosine phosphatases. Curr Top Cell Regul. 1997;35:21–68. doi: 10.1016/s0070-2137(97)80002-7. [DOI] [PubMed] [Google Scholar]
  151. de Duve C. The birth of complex cells. Sci Am. 1996 Apr;274(4):50–57. doi: 10.1038/scientificamerican0496-50. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES