The Dos family of globin-related sensors using PAS domains to accommodate haem acting as the active site for sensing external signals

Advances in Microbial Physiology

Volumn 63, Issue , 2013, Pages 273-327

  Aono, Shigetoshi ^a  

^a OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

Author keywords

Aerotaxis; Chemotaxis; Diguanylate cyclase; EcDos; FixL; Haem based sensor; PAS domain; Phosphodiesterase; Two component system

Indexed keywords

GLOBIN; HEME; HEME OXYGENASE 2; HETERODIMER; NEURONAL PAS DOMAIN 2 PROTEIN; NUCLEOTIDE; PHOSPHODIESTERASE; PHOSPHODIESTERASE A1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BRUCELLA ABORTUS; CHEMOTAXIS; CONFORMATIONAL TRANSITION; DESULFOVIBRIO VULGARIS; DNA BINDING; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; GEOBACTER SULFURREDUCENS; GLUCONACETOBACTER XYLINUS; HYDROGEN BOND; LIGAND BINDING; LISTERIA MONOCYTOGENES; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PHYSIOLOGICAL PROCESS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; SECOND MESSENGER; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY; STREPTOCOCCUS MUTANS; TRANSCRIPTION REGULATION; ULTRAVIOLET SPECTROSCOPY;

AEROTAXIS; CHEMOTAXIS; DIGUANYLATE CYCLASE; ECDOS; FIXL; HAEM-BASED SENSOR; PAS DOMAIN; PHOSPHODIESTERASE; TWO-COMPONENT SYSTEM;

ALLOSTERIC REGULATION; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION; GLOBINS; HEME; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; SPECTRUM ANALYSIS;

EID: 84884187434     PISSN: 00652911     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407693-8.00007-8     Document Type: Chapter

References (177)

1. Agron P.G., Ditta G.S., Helinski D.R. Oxygen regulation of nifA transcription in vitro. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:3506-3510.
2. Airola M.V., Huh D., Sukomon N., Widom J., Sircar R., Borbat P.P., et al. Architecture of the soluble receptor Aer2 indicates an in-line mechanism for PAS and HAMP domain signaling. Journal of Molecular Biology 2013, 425:886-901.
3. Airola M.V., Watts K.J., Bilwes A.M., Crane B.R. Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 2010, 18:436-448.
4. 2-specific regulation of the ferrous heme-based sensor-kinase FixL from Sinorhizobium meliloti and its aberrant inactivation in the ferric form. Biochemical and Biophysical Research Communications 2003, 304:136-142.
5. Al Dahouk S., Loisel-Meyer S., Scholz H.C., Tomaso H., Kersten M., Harder A., et al. Proteomic analysis of Brucella suis under oxygen deficiency reveals flexibility in adaptive expression of various pathways. Proteomics 2009, 9:3011-3021.
6. Anantharaman V., Koonin E.V., Aravind L. Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. Journal of Molecular Biology 2001, 307:1271-1292.
7. Aono S. Biochemical and biophysical properties of the CO-sensing transcriptional activator CooA. Accounts of Chemical Research 2003, 36:825-831.
8. Aono S. Metal-containing sensor proteins sensing diatomic gas molecules. Dalton Transactions 2011, (24):3137-3146.
9. Aono S., Nakajima H., Saito K., Okada M. A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in Rhodospirillum rubrum. Biochemical and Biophysical Research Communications 1996, 228:752-756.
10. Aono S., Ohkubo K., Matsuo T., Nakajima H. Redox-controlled ligand exchange of the heme in the CO-sensing transcriptional activator CooA. The Journal of Biological Chemistry 1998, 273:25757-25764.
11. Aravind L., Ponting C.P. The GAF domain: An evolutionary link between diverse phototransducing proteins. Trends in Biochemical Sciences 1997, 22:458-459.
12. Baker S.C., Saunders N.F., Willis A.C., Ferguson S.J., Hajdu J., Fülöp V. Cytochrome cd1 structure: Unusual haem environments in a nitrite reductase and analysis of factors contributing to beta-propeller folds. Journal of Molecular Biology 1997, 269:440-455.
13. Balland V., Bouzhir-Sima L., Anxolabéhère-Mallart E., Boussac A., Vos M.H., Liebl U., et al. Functional implications of the propionate 7-arginine 220 interaction in the FixLH oxygen sensor from Bradyrhizobium japonicum. Biochemistry 2006, 45:2072-2084.
14. Balland V., Bouzhir-Sima L., Kiger L., Marden M.C., Vos M.H., Liebl U., et al. Role of arginine 220 in the oxygen sensor FixL from Bradyrhizobium japonicum. The Journal of Biological Chemistry 2005, 280:15279-15288.
15. Baraquet C., Théraulaz L., Iobbi-Nivol C., Méjean V., Jourlin-Castelli C. Unexpected chemoreceptors mediate energy taxis towards electron acceptors in Shewanella oneidensis. Molecular Microbiology 2009, 73:278-290.
16. Bauer C.E., Elsen S., Bird T.H. Mechanisms for redox control of gene expression. Annual Review of Microbiology 1999, 53:495-523.
17. Blair D.F. How bacteria sense and swim. Annual Review of Microbiology 1995, 49:489-522.
18. Boon E.M., Davis J.H., Tran R., Karow D.S., Huang S.H., Pan D., et al. Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta1 H-NOX domain. The Journal of Biological Chemistry 2006, 281:21892-21902.
19. Brem K.L., Gray H.B. Structurally engineered cytochromes with novel ligand-binding sites: Oxy and carbonmonoxy derivatives of semisynthetic horse heart Ala80 cytochrome c. Journal of the American Chemical Society 1993, 115:10382-103803.
20. Burnside K., Lembo A., de Los Reyes M., Iliuk A., Binhtran N.T., Connelly J.E., et al. Regulation of hemolysin expression and virulence of Staphylococcus aureus by a serine/threonine kinase and phosphatase. PLoS One 2010, 5:e11071. 10.1371/journal.pone.0011071.
21. Bush M., Ghosh T., Tucker N., Zhang X., Dixon R. Transcriptional regulation by the dedicated nitric oxide sensor, NorR: A route toward NO detoxification. Biochemical Society Transactions 2011, 39:289-293.
22. Carlson H.K., Vance R.E., Marletta M.A. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Molecular Microbiology 2010, 77:930-942.
23. Carrica Mdel C., Fernandez I., Martí M.A., Paris G., Goldbaum F.A. The NtrY/X two-component system of Brucella spp. acts as a redox sensor and regulates the expression of nitrogen respiration enzymes. Molecular Microbiology 2012, 85:39-50.
24. Catarino T., Pessanha M., De Candia A.G., Gouveia Z., Fernandes A.P., Pokkuluri P.R., et al. Probing the chemotaxis periplasmic sensor domains from Geobacter sulfurreducens by combined resonance Raman and molecular dynamic approaches: NO and CO sensing. The Journal of Physical Chemistry. B 2010, 114:11251-11260.
25. Chang A.L., Tuckerman J.R., Gonzalez G., Mayer R., Weinhouse H., Volman G., et al. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 2001, 40:3420-3426.
26. Cho H.Y., Cho H.J., Kim Y.M., Oh J.I., Kang B.S. Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. The Journal of Biological Chemistry 2009, 284:13057-13067.
27. Cotter P.A., Stibitz S. c-di-GMP-mediated regulation of virulence and biofilm formation. Current Opinion in Microbiology 2007, 10:17-23.
28. Da Re S., Schumacher J., Rousseau P., Fourment J., Ebel C., Kahn D. Phosphorylation-induced dimerization of the FixJ receiver domain. Molecular Microbiology 1999, 34:504-511.
29. 2 stretching modes in oxyhemoglobins. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:479-484.
30. D'Autréaux B., Tucker N.P., Dixon R., Spiro S. A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 2005, 437:769-772.
31. David M., Daveran M.L., Batut J., Dedieu A., Domergue O., Ghai J., et al. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 1998, 54:671-683.
32. Deckers H.M., Voordouw G. Identification of a large family of genes for putative chemoreceptor proteins in an ordered library of the Desulfovibrio vulgaris Hildenborough genome. Journal of Bacteriology 1994, 176:351-358.
33. Deckers H.M., Voordouw G. Membrane topology of the methyl-accepting chemotaxis protein DcrA from Desulfovibrio vulgaris Hildenborough. Antonie Van Leeuwenhoek 1994, 65:7-12.
34. Deckers H.M., Voordouw G. The dcr gene family of Desulfovibrio: Implications from the sequence of dcrH and phylogenetic comparison with other mcp genes. Antonie Van Leeuwenhoek 1996, 70:21-29.
35. Delgado-Nixon V.M., Gonzalez G., Gilles-Gonzalez M.A. Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 2000, 39:2685-2691.
36. Desbois A. Resonance Raman spectroscopy of c-type cytochromes. Biochimie 1994, 76:693-707.
37. Dioum E.M., Rutter J., Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.A., McKnight S.L. NPAS2: A gas-responsive transcription factor. Science 2002, 298:2385-2397.
38. Dolla A., Fu R., Brumlik M.J., Voordouw G. Nucleotide sequence of dcrA, a Desulfovibrio vulgaris Hildenborough chemoreceptor gene, and its expression in Escherichia coli. Journal of Bacteriology 1992, 174:1726-1733.
39. Dunham C.M., Dioum E.M., Tuckerman J.R., Gonzalez G., Scott W.G., Gilles-Gonzalez M.A. A distal arginine in oxygen-sensing heme-PAS domains is essential to ligand binding, signal transduction, and structure. Biochemistry 2003, 42:7701-7708.
40. El-Mashtoly S.F., Nakashima S., Tanaka A., Shimizu T., Kitagawa T. Roles of Arg-97 and Phe-113 in regulation of distal ligand binding to heme in the sensor domain of Ec DOS protein. Resonance Raman and mutation study. The Journal of Biological Chemistry 2008, 283:19000-19100.
41. El-Mashtoly S.F., Takahashi H., Shimizu T., Kitagawa T. Ultraviolet resonance Raman evidence for utilization of the heme 6-propionate hydrogen-bond network in signal transmission from heme to protein in Ec DOS protein. Journal of the American Chemical Society 2007, 129:3556-3563.
42. Erbil W.K., Price M.S., Wemmer D.E., Marletta M.A. A structural basis for H-NOX signaling in Shewanella oneidensis by trapping a histidine kinase inhibitory conformation. Proceedings of the National Academy of Sciences of the United States of the America 2009, 106:19753-19760.
43. Fischer H.M. Genetic regulation of nitrogen fixation in rhizobia. Microbiological Reviews 1994, 58:352-386.
44. Fu R., Voordouw G. Targeted gene-replacement mutagenesis of dcrA, encoding an oxygen sensor of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Microbiology (Reading, England) 1997, 143:1815-1826.
45. Fu R., Wall J.D., Voordouw G. DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. Journal of Bacteriology 1994, 176:344-350.
46. Fülöp V., Moir J.W., Ferguson S.J., Hajdu J. The anatomy of a bifunctional enzyme: Structural basis for reduction of oxygen to water and synthesis of nitric oxide by cytochrome cd1. Cell 1995, 81:369-377.
47. Gilles-Gonzalez M.A. Oxygen signal transduction. IUBMB Life 2001, 51:165-173.
48. Gilles-Gonzalez M.A., Caceres A.I., Sousa E.H., Tomchick D.R., Brautigam C., Gonzalez C., et al. A proximal arginine R206 participates in switching of the Bradyrhizobium japonicum FixL oxygen sensor. Journal of Molecular Biology 2006, 360:80-89.
49. Gilles-Gonzalez M.A., Ditta G.S., Helinski D.R. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 1991, 350:170-172.
50. Gilles-Gonzalez M.A., Gonzalez G. Regulation of the kinase activity of heme protein FixL from the two-component system FixL/FixJ of Rhizobium meliloti. The Journal of Biological Chemistry 1993, 268:16293-16297.
51. Gilles-Gonzalez M.A., Gonzalez G. Heme-based sensors: Defining characteristics, recent developments, and regulatory hypotheses. Journal of Inorganic Biochemistry 2005, 99:1-22.
52. Gilles-González M.A., González G., Perutz M.F. Kinase activity of oxygen sensor FixL depends on the spin state of its heme iron. Biochemistry 1995, 34:232-236.
53. Gilles-Gonzalez M.A., Gonzalez G., Perutz M.F., Kiger L., Marden M.C., Poyart C. Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 1994, 33:8067-8073.
54. Gong W., Hao B., Chan M.K. New mechanistic insights from structural studies of the oxygen-sensing domain of Bradyrhizobium japonicum FixL. Biochemistry 2000, 39:3955-3962.
55. Gong W., Hao B., Mansy S.S., Gonzalez G., Gilles-Gonzalez M.A., Chan M.K. Structure of a biological oxygen sensor: A new mechanism for heme-driven signal transduction. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:15177-15182.
56. Gottfried D.S., Peterson E.S., Sheikh A.G., Wang J., Yang M., Friedman J.M. Evidence for damped hemoglobin dynamics in a room temperature trehalose glass. The Journal of Physical Chemistry 1996, 100:12034-12042.
57. 2 sensing and ligand discrimination by the FixL heme domain of Bradyrhizobium japonicum. Biochemistry 2002, 41:12952-12958.
58. Heikaus C.C., Pandit J., Klevit R.E. Cyclic nucleotide binding GAF domains from phosphodiesterases: Structural and mechanistic insights. Structure 2009, 17:1551-1557.
59. Henry J.T., Crosson S. Ligand-binding PAS domains in a genomic, cellular, and structural context. Annual Review of Microbiology 2011, 65:261-286.
60. Hiruma Y., Kikuchi A., Tanaka A., Shiro Y., Mizutani Y. Resonance Raman observation of the structural dynamics of FixL on signal transduction and ligand discrimination. Biochemistry 2007, 46:6086-6096.
61. Honaker R.W., Dhiman R.K., Narayanasamy P., Crick D.C., Voskuil M.I. DosS responds to a reduced electron transport system to induce the Mycobacterium tuberculosis DosR regulon. Journal of Bacteriology 2010, 192:6447-6455.
62. Hong C.S., Kuroda A., Takiguchi N., Ohtake H., Kato J. Expression of Pseudomonas aeruginosa aer-2, one of two aerotaxis transducer genes, is controlled by RpoS. Journal of Bacteriology 2005, 187:1533-1535.
63. Hong C.S., Shitashiro M., Kuroda A., Ikeda T., Takiguchi N., Ohtake H., et al. Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa. FEMS Microbiology Letters 2004, 231:247-252.
64. Hou S., Larsen R.W., Boudko D., Riley C.W., Karatan E., Zimmer M., et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 2000, 403:540-544.
65. Hu S., Morris I.K., Singh J.P., Smith K.M., Spiro T.G. Complete assignment of cytochrome-c resonance Raman spectra via enzymatic reconstitution with isotopically-labeled hemes. Journal of the American Chemical Society 1993, 115:12446-12458.
66. Hu S.Z., Smith K.M., Spiro T.G. Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin. Journal of the American Chemical Society 1996, 118:12638-12646.
67. Ioanoviciu A., Meharenna Y.T., Poulos T.L., Ortiz de Montellano P.R. DevS oxy complex stability identifies this heme protein as a gas sensor in Mycobacterium tuberculosis dormancy. Biochemistry 2009, 48:5839-5848.
68. Ioanoviciu A., Yukl E.T., Moënne-Loccoz P., Ortiz de Montellano P.R. DevS, a heme-containing two-component oxygen sensor of Mycobacterium tuberculosis. Biochemistry 2007, 46:4250-4260.
69. Ishida M.L., Assumpção M.C., Machado H.B., Benelli E.M., Souza E.M., Pedrosa F.O. Identification and characterization of the two-component NtrY/NtrX regulatory system in Azospirillum brasilense. Brazilian Journal of Medical and Biological Research 2002, 35:651-661.
70. Ishida M., Ueha T., Sagami I. Effects of mutations in the heme domain on the transcriptional activity and DNA-binding activity of NPAS2. Biochemical and Biophysical Research Communications 2008, 368:292-297.
71. 2. Biochemistry 2008, 47:8874-8884.
72. Ito S., Araki Y., Tanaka A., Igarashi J., Wada T., Shimizu T. Role of Phe113 at the distal side of the heme domain of an oxygen-sensor (Ec DOS) in the characterization of the heme environment. Journal of Inorganic Biochemistry 2009, 103:989-996.
73. Ito S., Igarashi J., Shimizu T. The FG loop of a heme-based gas sensor enzyme, Ec DOS, functions in heme binding, autoxidation and catalysis. Journal of Inorganic Biochemistry 2009, 103:1380-1385.
74. Iyer L.M., Anantharaman V., Aravind L. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics 2003, 4:5. 10.1186/1471-2164-4-5.
75. Jasaitis A., Hola K., Bouzhir-Sima L., Lambry J.C., Balland V., Vos M.H., et al. Role of distal arginine in early sensing intermediates in the heme domain of the oxygen sensor FixL. Biochemistry 2006, 45:6018-6026.
76. Jenal U. Cyclic di-guanosine-monophosphate comes of age: A novel secondary messenger involved in modulating cell surface structures in bacteria?. Current Opinion in Microbiology 2004, 7:185-191.
77. Jenal U., Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annual Review of Genetics 2006, 40:385-407.
78. Jung K., Fried L., Behr S., Heermann R. Histidine kinases and response regulators in networks. Current Opinion in Microbiology 2011, 15:118-124.
79. Karatan E., Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiology and Molecular Biology Review 2009, 73:310-347.
80. Karow D.S., Pan D., Tran R., Pellicena P., Presley A., Mathies R.A., et al. Spectroscopic characterization of the soluble guanylate cyclase-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis. Biochemistry 2004, 43:10203-10211.
81. Kerby R.L., Youn H., Roberts G.P. RcoM: A new single-component transcriptional regulator of CO metabolism in bacteria. Journal of Bacteriology 2008, 190:3336-3343.
82. Key J., Moffat K. Crystal structures of deoxy and CO-bound bjFixLH reveal details of ligand recognition and signaling. Biochemistry 2005, 44:4627-4635.
83. Kim M.J., Park K.J., Ko I.J., Kim Y.M., Oh J.I. Different roles of DosS and DosT in the hypoxic adaptation of Mycobacteria. Journal of Bacteriology 2010, 192:4868-4875.
84. King G.M., Weber C.F. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nature Reviews. Microbiology 2007, 5:107-118.
85. King D.P., Zhao Y., Sangoram A.M., Wilsbacher L.D., Tanaka M., Antoch M.P., et al. Positional cloning of the mouse circadian clock gene. Cell 1997, 89:641-653.
86. Kirby J.R. Chemotaxis-like regulatory systems: Unique roles in diverse bacteria. Annual Review of Microbiology 2009, 63:45-59.
87. 2 complex of YddV, a globin-coupled heme-based oxygen sensor diguanylate cyclase. Biochemistry 2010, 49:10381-10393.
88. Kobayashi K., Tanaka A., Takahashi H., Igarashi J., Ishitsuka Y., Yokota N., et al. Catalysis and oxygen binding of Ec DOS: A haem-based oxygen-sensor enzyme from Escherichia coli. Journal of Biochemistry 2010, 148:693-703.
89. Komori H., Inagaki S., Yoshioka S., Aono S., Higuchi Y. Crystal structure of CO-sensing transcription activator CooA bound to exogenous ligand imidazole. Journal of Molecular Biology 2007, 367:864-871.
90. Kruglik S.G., Jasaitis A., Hola K., Yamashita T., Liebl U., Martin J.L., et al. Subpicosecond oxygen trapping in the heme pocket of the oxygen sensor FixL observed by time-resolved resonance Raman spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7408-7413.
91. Kumar A., Toledo J.C., Patel R.P., Lancaster J.R., Steyn A.J. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11568-11573.
92. Kurokawa H., Lee D.S., Watanabe M., Sagami I., Mikami B., Raman C.S., et al. A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. The Journal of Biological Chemistry 2004, 279:20186-20193.
93. Lanzilotta W.N., Schuller D.J., Thorsteinsson M.V., Kerby R.L., Roberts G.P., Poulos T.L. Structure of the CO sensing transcription activator CooA. Natural Structural Biology 2000, 7:876-880.
94. Lechauve C., Bouzhir-Sima L., Yamashita T., Marden M.C., Vos M.H., Liebl U., et al. Heme ligand binding properties and intradimer interactions in the full-length sensor protein dos from Escherichia coli and its isolated heme domain. The Journal of Biological Chemistry 2009, 284:36146-36159.
95. 2- and NO-sensing mechanism through the DevSR two-component system in Mycobacterium smegmatis. Journal of Bacteriology 2008, 190:6795-6804.
96. Liebl U., Bouzhir-Sima L., Negrerie M., Martin J.L., Vos M.H. Ultrafast ligand rebinding in the heme domain of the oxygen sensors FixL and Dos: General regulatory implications for heme-based sensors. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:12771-12776.
97. Londer Y.Y., Dementieva I.S., D'Ausilio C.A., Pokkuluri P.R., Schiffer M. Characterization of a c-type heme-containing PAS sensor domain from Geobacter sulfurreducens representing a novel family of periplasmic sensors in Geobacteraceae and other bacteria. FEMS Microbiology Letters 2006, 258:173-181.
98. Lukat-Rodgers G.S., Rexine J.L., Rodgers K.R. Heme speciation in alkaline ferric FixL and possible tyrosine involvement in the signal transduction pathway for regulation of nitrogen fixation. Biochemistry 1998, 37:13543-13552.
99. Marina A., Waldburger C.D., Hendrickson W.A. Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO Journal 2005, 24:4247-4259.
100. Marvin K.A., Kerby R.L., Youn H., Roberts G.P., Burstyn J.N. The transcription regulator RcoM-2 from Burkholderia xenovorans is a cysteine-ligated hemoprotein that undergoes a redox-mediated ligand switch. Biochemistry 2008, 47:9016-9028.
101. Miyatake H., Kanai M., Adachi S., Nakamura H., Tamura K., Tanida H., et al. Dynamic light-scattering and preliminary crystallographic studies of the sensor domain of the haem-based oxygen sensor FixL from Rhizobium meliloti. Acta Crystallographica. Section D, Biological Crystallography 1999, 55:1215-1218.
102. Miyatake H., Mukai M., Adachi S., Nakamura H., Tamura K., Iizuka T., et al. Iron coordination structures of oxygen sensor FixL characterized by Fe K-edge extended X-ray absorption fine structure and resonance Raman spectroscopy. The Journal of Biological Chemistry 1999, 274:23176-23184.
103. Miyatake H., Mukai M., Park S.Y., Adachi S., Tamura K., Nakamura H., et al. Sensory mechanism of oxygen sensor FixL from Rhizobium meliloti: Crystallographic, mutagenesis and resonance Raman spectroscopic studies. Journal of Molecular Biology 2000, 301:415-431.
104. Möglich A., Ayers R.A., Moffat K. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 2009, 17:1282-1294.
105. Monson E.K., Ditta G.S., Helinski D.R. The oxygen sensor protein, FixL, of Rhizobium meliloti. Role of histidine residues in heme binding, phosphorylation, and signal transduction. The Journal of Biological Chemistry 1995, 270:5243-5250.
106. Mukai M., Nakamura K., Nakamura H., Iizuka T., Shiro Y. Roles of Ile209 and Ile210 on the heme pocket structure and regulation of histidine kinase activity of oxygen sensor FixL from Rhizobium meliloti. Biochemistry 2000, 39:13810-13816.
107. Mukai M., Savard P.Y., Ouellet H., Guertin M., Yeh S.R. Unique ligand-protein interactions in a new truncated hemoglobin from Mycobacterium tuberculosis. Biochemistry 2002, 41:3897-3905.
108. Mukaiyama Y., Uchida T., Sato E., Sasaki A., Sato Y., Igarashi J., et al. Spectroscopic and DNA-binding characterization of the isolated heme-bound basic helix-loop-helix-PAS-A domain of neuronal PAS protein 2 (NPAS2), a transcription activator protein associated with circadian rhythms. FEBS Journal 2006, 273:2528-2539.
109. Nakajima H., Honma Y., Tawara T., Kato T., Park S.Y., Miyatake H., et al. Redox properties and coordination structure of the heme in the CO-sensing transcriptional activator CooA. The Journal of Biological Chemistry 2001, 276:7055-7061.
110. Nakajima H., Takatani N., Yoshimitsu K., Itoh M., Aono S., Takahashi Y., et al. The role of the Fe-S cluster in the sensory domain of nitrogenase transcriptional activator VnfA from Azotobacter vinelandii. FEBS Journal 2010, 277:817-832.
111. Nakamura H., Kumita H., Imai K., Iizuka T., Shiro Y. ADP reduces the oxygen-binding affinity of a sensory histidine kinase, FixL: The possibility of an enhanced reciprocating kinase reaction. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:2742-2746.
112. Nioche P., Berka V., Vipond J., Minton N., Tsai A.L., Raman C.S. Femtomolar sensitivity of a NO sensor from Clostridium botulinum. Science 2004, 306:1550-1553.
113. Nuernberger P., Lee K.F., Bonvalet A., Bouzhir-Sima L., Lambry J.C., Liebl U., et al. Strong ligand-protein interactions revealed by ultrafast infrared spectroscopy of CO in the heme pocket of the oxygen sensor FixL. Journal of the American Chemical Society 2011, 133:17110-17113.
114. Olea C., Boon E.M., Pellicena P., Kuriyan J., Marletta M.A. Probing the function of heme distortion in the H-NOX family. ACS Chemical Biology 2008, 3:703-710.
115. Olea C., Herzik M.A., Kuriyan J., Marletta M.A. Structural insights into the molecular mechanism of H-NOX activation. Protein Science 2010, 19:881-887.
116. Osterberg S., Skärfstad E., Shingler V. The sigma-factor FliA, ppGpp and DksA coordinate transcriptional control of the aer2 gene of Pseudomonas putida. Environmental Microbiology 2010, 12:1439-1451.
117. Ouellet Y., Milani M., Couture M., Bolognesi M., Guertin M. Ligand interactions in the distal heme pocket of Mycobacterium tuberculosis truncated hemoglobin N: Roles of TyrB10 and GlnE11 residues. Biochemistry 2006, 45:8770-8781.
118. Park H., Suquet C., Satterlee J.D., Kang C. Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH). Biochemistry 2004, 43:2738-2746.
119. Pawlowski K., Klosse U., de Bruijn F.J. Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Molecular and General Genetics 1991, 231:124-138.
120. Pesavento C., Hengge R. Bacterial nucleotide-based second messengers. Current Opinion in Microbiology 2009, 12:170-176.
121. Peterson E.S., Friedman J.M., Chien E.Y., Sligar S.G. Functional implications of the proximal hydrogen-bonding network in myoglobin: A resonance Raman and kinetic study of Leu89, Ser92, His97, and F-helix swap mutants. Biochemistry 1998, 37:12301-12319.
122. Podust L.M., Ioanoviciu A., Ortiz de Montellano P.R. 2.3Å X-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis. Biochemistry 2008, 47:12523-12531.
123. Pokkuluri P.R., Pessanha M., Londer Y.Y., Wood S.J., Duke N.E., Wilton R., et al. Structures and solution properties of two novel periplasmic sensor domains with c-type heme from chemotaxis proteins of Geobacter sulfurreducens: Implications for signal transduction. Journal of Molecular Biology 2008, 377:1498-1517.
124. Ragsdale S.W. Life with carbon monoxide. Critical Reviews in Biochemistry and Molecular Biology 2004, 39:165-195.
125. Rao F., Ji Q., Soehano I., Liang Z.X. Unusual heme-binding PAS domain from YybT family proteins. Journal of Bacteriology 2011, 193:1543-1551.
126. Rao F., See R.Y., Zhang D., Toh D.C., Ji Q., Liang Z.X. YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. The Journal of Biological Chemistry 2010, 285:473-482.
127. Reick M., Garcia J.A., Dudley C., McKnight S.L. NPAS2: An analog of clock operative in the mammalian forebrain. Science 2001, 293:506-509.
128. Reyrat J.M., David M., Batut J., Boistard P. FixL of Rhizobium meliloti enhances the transcriptional activity of a mutant FixJD54N protein by phosphorylation of an alternate residue. Journal of Bacteriology 1994, 176:1969-1976.
129. Reyrat J.M., David M., Blonski C., Boistard P., Batut J. Oxygen-regulated in vitro transcription of Rhizobium meliloti nifA and fixK genes. Journal of Bacteriology 1993, 175:6867-6872.
130. Roberts G.P., Kerby R.L., Youn H., Conrad M. CooA, a paradigm for gas sensing regulatory proteins. Journal of Inorganic Biochemistry 2005, 99:280-292.
131. Römling U., Amikam D. Cyclic di-GMP as a second messenger. Current Opinion in Microbiology 2006, 9:218-228.
132. Römling U., Gomelsky M., Galperin M. C-di-GMP: The dawning of a novel bacterial signaling system. Molecular Microbiology 2005, 57:629-639.
133. Roop R.M., Caswell C.C. Redox-responsive regulation of denitrification genes in Brucella. Molecular Microbiology 2012, 85:5-7.
134. Saini D.K., Malhotra V., Dey D., Pant N., Das T.K., Tyagi J.S. DevR-DevS is a bona fide two-component system of Mycobacterium tuberculosis that is hypoxia-responsive in the absence of the DNA-binding domain of DevR. Microbiology (Reading, England) 2004, 150:865-875.
135. Sarand I., Osterberg S., Holmqvist S., Holmfeldt P., Skärfstad E., Parales R.E., et al. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environmental Microbiology 2008, 10:1320-1334.
136. Sardiwal S., Kendall S.L., Movahedzadeh F., Rison S.C., Stoker N.G., Djordjevic S.A. GAF domain in the hypoxia/NO-inducible Mycobacterium tuberculosis DosS protein binds haem. Journal of Molecular Biology 2005, 353:929-936.
137. Sasakura Y., Yoshimura-Suzuki T., Kurokawa H., Shimizu T. Structure-function relationships of EcDOS, a heme-regulated phosphodiesterase from Escherichia coli. Accounts of Chemical Research 2006, 39:37-43.
138. Sato A., Sasakura Y., Sugiyama S., Sagami I., Shimizu T., Mizutani Y., et al. Stationary and time-resolved resonance Raman spectra of His77 and Met95 mutants of the isolated heme domain of a direct oxygen sensor from Escherichia coli. The Journal of Biological Chemistry 2002, 277:32650-32658.
139. Sawai H., Sugimoto H., Shiro Y., Ishikawa H., Mizutani Y., Aono S. Structural basis for oxygen sensing and signal transduction of the heme-based sensor protein Aer2 from Pseudomonas aeruginosa. Chemical Communications 2012, 48:6523-6525.
140. Sawai H., Yamanaka M., Sugimoto H., Shiro Y., Aono S. Structural basis for the transcriptional regulation of heme homeostasis in Lactococcus lactis. The Journal of Biological Chemistry 2012, 287:30755-30768.
141. Sawai H., Yoshioka S., Uchida T., Hyodo M., Hayakawa Y., Ishimori K., et al. Molecular oxygen regulates the enzymatic activity of a heme-containing diguanylate cyclase (HemDGC) for the synthesis of cyclic di-GMP. Biochimica et Biophysica Acta 2009, 1804:166-172.
142. Sciotti M.A., Chanfon A., Hennecke H., Fischer H.M. Disparate oxygen responsiveness of two regulatory cascades that control expression of symbiotic genes in Bradyrhizobium japonicum. Journal of Bacteriology 2003, 185:5639-5642.
143. Seshasayee A.S., Fraser G.M., Luscombe N.M. Comparative genomics of cyclic-di-GMP signaling in bacteria: Post-translational regulation and catalytic activity. Nucleic Acids Research 2010, 38:5970-5981.
144. Silva M.A., Lucas T.G., Salgueiro C.A., Gomes C.M. Protein folding modulates the swapped dimerization mechanism of methyl-accepting chemotaxis heme sensors. PLoS One 2012, 7:e46328. 10.1371/journal.pone.0046328.
145. Smith A.T., Marvin K.A., Freeman K.M., Kerby R.L., Roberts G.P., Burstyn J.N. Identification of Cys94 as the distal ligand to the Fe(III) heme in the transcriptional regulator RcoM-2 from Burkholderia xenovorans. Journal of Biological Inorganic Chemistry 2012, 17:1071-1082.
146. 2-fixation gene expression within the alfalfa root nodule. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:3759-3763.
147. Sousa E.H., Gonzalez G., Gilles-Gonzalez M.A. Oxygen blocks the reaction of the FixL-FixJ complex with ATP but does not influence binding of FixJ or ATP to FixL. Biochemistry 2005, 44:15359-15365.
148. Sousa E.H., Tuckerman J.R., Gondim A.C., Gonzalez G., Gilles-Gonzalez M.A. Signal transduction and phosphoryl transfer by a FixL hybrid kinase with low oxygen affinity: Importance of the vicinal PAS domain and receiver aspartate. Biochemistry 2013, 52:456-465.
149. Sousa E.H., Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.A. DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Science 2007, 16:1708-1719.
150. Stock J.B., Lukat G.S., Stock A.M. Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annual Review of Biophysics and Biophysical Chemistry 1991, 20:109-136.
151. Szurmant H., Ordal G.W. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiology and Molecular Biology Reviews 2004, 68:301-319.
152. Tamayo R., Pratt J.T., Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annual Review of Microbiology 2007, 61:131-148.
153. Tan E., Rao F., Pasunooti S., Pham T.H., Soehano I., Turner M.S., et al. Solution structure of the PAS domain of a thermophilic YybT homolog reveals a potential ligand-binding site. The Journal of Biological Chemistry 2013, 288:11949-11959.
154. 2 sensing: A single convergent structure of the heme moiety is relevant to the downregulation of kinase activity. Biochemistry 2006, 45:2515-2523.
155. Tanaka A., Shimizu T. Ligand binding to the Fe(III)-protoporphyrin IX complex of phosphodiesterase from Escherichia coli (Ec DOS) markedly enhances catalysis of cyclic di-GMP: Roles of Met95, Arg97, and Phe113 of the putative heme distal side in catalytic regulation and ligand binding. Biochemistry 2008, 47:13438-13446.
156. Tanaka A., Takahashi H., Shimizu T. Critical role of the heme axial ligand, Met95, in locking catalysis of the phosphodiesterase from Escherichia coli (Ec DOS) toward cyclic diGMP. The Journal of Biological Chemistry 2007, 282:21301-21307.
157. Taylor B.L., Rebbapragada A., Johnson M.S. The FAD-PAS domain as a sensor for behavioral responses in Escherichia coli. Antioxidants & Redox Signaling 2001, 3:867-879.
158. Thijs L., Vinck E., Bolli A., Trandafir F., Wan X., Hoogewijs D., et al. Characterization of a globin-coupled oxygen sensor with a gene-regulating function. The Journal of Biological Chemistry 2007, 282:37325-37340.
159. Tomita T., Gonzalez G., Chang A.L., Ikeda-Saito M., Gilles-Gonzalez M.A. A comparative resonance Raman analysis of heme-binding PAS domains: Heme iron coordination structures of the BjFixL, AxPDEA1, EcDos, and MtDos proteins. Biochemistry 2002, 41:4819-4826.
160. Tuckerman J.R., Gonzalez G., Dioum E.M., Gilles-Gonzalez M.A. Ligand and oxidation-state specific regulation of the heme-based oxygen sensor FixL from Sinorhizobium meliloti. Biochemistry 2002, 41:6170-6177.
161. Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.A. Complexation precedes phosphorylation for two-component regulatory system FixL/FixJ of Sinorhizobium meliloti. Journal of Molecular Biology 2001, 308:449-455.
162. Tuckerman J.R., Gonzalez G., Sousa E.H., Wan X., Saito J.A., Alam M., et al. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 2009, 48:9764-9774.
163. Uchida T., Sagami I., Shimizu T., Ishimori K., Kitagawa T. Effects of the bHLH domain on axial coordination of heme in the PAS-A domain of neuronal PAS domain protein 2 (NPAS2): Conversion from His119/Cys170 coordination to His119/His171 coordination. Journal of Inorganic Biochemistry 2012, 108:188-195.
164. Uchida T., Sato E., Sato A., Sagami I., Shimizu T., Kitagawa T. CO-dependent activity-controlling mechanism of heme-containing CO-sensor protein, neuronal PAS domain protein 2. The Journal of Biological Chemistry 2005, 280:21358-21368.
165. van Wilderen L.J., Key J.M., Van Stokkum I.H., van Grondelle R., Groot M.L. Dynamics of carbon monoxide photodissociation in Bradyrhizobium japonicum FixL probed by picosecond midinfrared spectroscopy. The Journal of Physical Chemistry. B 2009, 113:3292-3297.
166. Voordouw G. Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. Journal of Bacteriology 2002, 184:5903-5911.
167. Wan X., Tuckerman J.R., Saito J.A., Freitas T.A., Newhouse J.S., Denery J.R., et al. Globins synthesize the second messenger bis-(3'-5')-cyclic diguanosine monophosphate in bacteria. Journal of Molecular Biology 2009, 388:262-270.
168. Watts K.J., Taylor B.L., Johnson M.S. PAS/poly-HAMP signaling in Aer-2, a soluble haem-based sensor. Molecular Microbiology 2011, 79:686-699.
169. Williams P.A., Fülöp V., Garman E.F., Saunders N.F., Ferguson S.J., Hajdu J. Haem-ligand switching during catalysis in crystals of a nitrogen-cycle enzyme. Nature 1997, 389:406-412.
170. Winkler W.C., Gonzalez G., Wittenberg J.B., Hille R., Dakappagari N., Jacob A., et al. Nonsteric factors dominate binding of nitric oxide, azide, imidazole, cyanide, and fluoride to the rhizobial heme-based oxygen sensor FixL. Chemistry & Biology 1996, 3:841-850.
171. Yamada S., Sugimoto H., Kobayashi M., Ohno A., Nakamura H., Shiro Y. Structure of PAS-linked histidine kinase and the response regulator complex. Structure 2009, 17:1333-1344.
172. 1H NMR spectroscopic studies. The Journal of Biological Chemistry 2001, 276:11473-11476.
173. Yeh S.R., Couture M., Ouellet Y., Guertin M., Rousseau D.L. A cooperative oxygen binding hemoglobin from Mycobacterium tuberculosis. Stabilization of heme ligands by a distal tyrosine residue. The Journal of Biological Chemistry 2000, 275:1679-1684.
174. Yoshioka S., Kobayashi K., Yoshimura H., Uchida T., Kitagawa T., Aono S. Biophysical properties of a c-type heme in chemotaxis signal transducer protein DcrA. Biochemistry 2005, 44:15406-15413.
175. Yukl E.T., Ioanoviciu A., Nakano M.M., Ortiz de Montellano P.R., Moënne-Loccoz P. A distal tyrosine residue is required for ligand discrimination in DevS from Mycobacterium tuberculosis. Biochemistry 2008, 47:12532-12539.
176. Yukl E.T., Ioanoviciu A., Ortiz de Montellano P.R., Moënne-Loccoz P. Interdomain interactions within the two-component heme-based sensor DevS from Mycobacterium tuberculosis. Biochemistry 2007, 46:9728-9736.
177. Yukl E.T., Ioanoviciu A., Sivaramakrishnan S., Nakano M.M., Ortiz de Montellano P.R., Moënne-Loccoz P. Nitric oxide dioxygenation reaction in DevS and the initial response to nitric oxide in Mycobacterium tuberculosis. Biochemistry 2011, 50:1023-1028.