Heme-based globin-coupled oxygen sensors: linking oxygen binding to functional regulation of diguanylate cyclase, histidine kinase, and methyl-accepting chemotaxis
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
23928310
PubMed Central
PMC3784688
DOI
10.1074/jbc.r113.473249
PII: S0021-9258(20)48898-2
Knihovny.cz E-zdroje
- Klíčová slova
- Chemotaxis, Cyclic GMP (cGMP), Heme, Hemoglobin, Histidine Kinases, Myoglobin, Oxygen Binding,
- MeSH
- Azotobacter vinelandii enzymologie MeSH
- Bordetella pertussis enzymologie MeSH
- chemotaxe MeSH
- Escherichia coli enzymologie MeSH
- globiny chemie MeSH
- hem chemie MeSH
- hemoglobiny chemie MeSH
- histidinkinasa MeSH
- katalytická doména MeSH
- katalýza MeSH
- kyslík chemie MeSH
- lyasy štěpící vazby P-O chemie MeSH
- molekulární evoluce MeSH
- molekulární sekvence - údaje MeSH
- myoglobin chemie MeSH
- proteinkinasy chemie MeSH
- proteiny z Escherichia coli chemie MeSH
- regulace genové exprese enzymů * MeSH
- sekvence aminokyselin MeSH
- sekvenční homologie aminokyselin MeSH
- vazba proteinů MeSH
- vazebná místa MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- diguanylate cyclase MeSH Prohlížeč
- globiny MeSH
- hem MeSH
- hemoglobiny MeSH
- histidinkinasa MeSH
- kyslík MeSH
- lyasy štěpící vazby P-O MeSH
- myoglobin MeSH
- proteinkinasy MeSH
- proteiny z Escherichia coli MeSH
An emerging class of novel heme-based oxygen sensors containing a globin fold binds and senses environmental O2 via a heme iron complex. Structure-function relationships of oxygen sensors containing a heme-bound globin fold are different from those containing heme-bound PAS and GAF folds. It is thus worth reconsidering from an evolutionary perspective how heme-bound proteins with a globin fold similar to that of hemoglobin and myoglobin could act as O2 sensors. Here, we summarize the molecular mechanisms of heme-based oxygen sensors containing a globin fold in an effort to shed light on the O2-sensing properties and O2-stimulated catalytic enhancement observed for these proteins.
Zobrazit více v PubMed
Voet D., Voet J. G. (2011) Hemoglobin: protein function in microcosm. in Biochemistry, 4th Ed., pp. 323–358, John Wiley & Sons, New York
Antonini E., Brunori M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, North-Holland Publishing Co., Amsterdam
Gardner P. R., Gardner A. M., Brashear W. T., Suzuki T., Hvitved A. N., Setchell K. D. R., Olson J. S. (2006) Hemoglobins deoxygenate nitric oxide with high fidelity. J. Inorg. Biochem. 100, 542–550 PubMed
Yukl E. T., de Vries S., Moënne-Loccoz P. (2009) The millisecond intermediate in the reaction of nitric oxide with oxymyoglobin is an iron(III)-nitrato complex, not a peroxynitrite. J. Am. Chem. Soc. 131, 7234–7235 PubMed PMC
Springer B. A., Sligar S. G., Olson J. S., Phillips G. N., Jr. (1994) Mechanisms of ligand recognition in myoglobin. Chem. Rev. 94, 699–714
Shikama K. (1998) The molecular mechanism of autoxidation for myoglobin and hemoglobin: a venerable puzzle. Chem. Rev. 98, 1357–1374 PubMed
Igarashi J., Kitanishi K., Shimizu T. (2011) Emerging roles of heme as a signal and a gas-sensing site: heme-sensing and gas-sensing proteins. in Handbook of Porphyrin Science (Kadish K. M., Smith K. M., Guilard R., eds) Vol. 15, pp. 399–460, World Scientific Publishing, Hackensack, NJ
Sasakura Y., Yoshimura-Suzuki T., Kurokawa H., Shimizu T. (2006) Structure-function relationships of EcDOS, a heme-regulated phosphodiesterase from Escherichia coli. Acc. Chem. Res. 39, 37–43 PubMed
Farhana A., Saini V., Kumar A., Lancaster J. R., Jr., Steyn A. J. C. (2012) Environmental heme-base sensor proteins: Implications for understanding bacterial pathogenesis. Antioxid. Redox Signal. 17, 1232–1245 PubMed PMC
Green J., Crack J. C., Thomson A. J., LeBrun N. E. (2009) Bacterial sensors of oxygen. Curr. Opin. Microbiol. 12, 145–151 PubMed
Gilles-Gonzalez M. A., Gonzalez G. (2005) Heme-based sensors: defining characteristics, recent developments, and regulatory hypotheses. J. Inorg. Biochem. 99, 1–22 PubMed
Aono S. (2012) Novel bacterial gas sensor proteins with transition metal-containing prosthetic groups as active sites. Antioxid. Redox Signal. 16, 678–686 PubMed
Uchida T., Kitagawa T. (2005) Mechanism for transduction of the ligand-binding signal in heme-based gas sensory proteins revealed by resonance Raman spectroscopy. Acc. Chem. Res. 38, 662–670 PubMed
Freitas T. A. K., Saito J. A., Hou S., Alam M. (2005) Globin-coupled sensors, protoglobins, and the last universal common ancestor. J. Inorg. Biochem. 99, 23–33 PubMed
Freitas T. A. K., Hou S., Alam M. (2003) The diversity of globin-coupled sensors. FEBS Lett. 552, 99–104 PubMed
Vinogradov S. N., Tinajero-Trejo M., Poole R. K., Hoogewijs D. (2013) Bacterial and archaeal globins–a revised perspective. Biochim. Biophys. Acta 1834, 1789–1800 PubMed
Wittenberg J. B., Bolognesi M., Wittenberg B. A., Guertin M. (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J. Biol. Chem. 277, 871–874 PubMed
Vinogradov S. N., Moens L. (2008) Diversity of globin function: enzymatic, transport, storage, and sensing. J. Biol. Chem. 283, 8773–8777 PubMed
Pesce A., Thijs L., Nardini M., Desmet F., Sisinni L., Gourlay L., Bolli A., Coletta M., Van Doorslaer S., Wan X., Alam M., Ascenzi P., Moens L., Bolognesi M., Dewilde S. (2009) HisE11 and HisF8 provide bis-histidyl heme hexa-coordination in the globin domain of Geobacter sulfurreducens globin-coupled sensor. J. Mol. Biol. 386, 246–260 PubMed
Hou S., Larsen R. W., Boudko D., Riley C. W., Karatan E., Zimmer M., Ordal G. W., Alam M. (2000) Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544 PubMed
Hou S., Freitas T., Larsen R. W., Piatibratov M., Sivozhelezov V., Yamamoto A., Meleshkevitch E. A., Zimmer M., Ordal G. W., Alam M. (2001) Globin-coupled sensors: a class of heme-containing sensors in Archaea and Bacteria. Proc. Natl. Acad. Sci. U.S.A. 98, 9353–9358 PubMed PMC
Zhang W., Phillips G. N., Jr. (2003) Structure of the oxygen sensor in Bacillus subtilis: signal transduction of chemotaxis by control of symmetry. Structure 11, 1097–1110 PubMed
Freitas T. A. K., Hou S., Dioum E. M., Saito J. A., Newhouse J., Gonzalez G., Gilles-Gonzalez M. A., Alam M. (2004) Ancestral hemeglobins in Archaea. Proc. Natl. Acad. Sci. U.S.A. 101, 6675–6680 PubMed PMC
Zhang W., Olson J. S., Phillips G. N., Jr. (2005) Biophysical and kinetic characterization of HemAT, an aerotaxis receptor from Bacillus subtilis. Biophys. J. 88, 2801–2814 PubMed PMC
Aono S., Kato T., Matsuki M., Nakajima H., Ohta T., Uchida T., Kitagawa T. (2002) Resonance Raman and ligand binding studies of the oxygen-sensing signal transducer protein HemAT from Bacillus subtilis. J. Biol. Chem. 277, 13528–13538 PubMed
Ohta T., Yoshimura H., Yoshioka S., Aono S., Kitagawa T. (2004) Oxygen-sensing mechanism of HemAT from Bacillus subtillis: a resonance Raman spectroscopic study. J. Am. Chem. Soc. 126, 15000–15001 PubMed
El-Mashtoly S. F., Kubo M., Gu Y., Sawai H., Nakashima S., Ogura T., Aono S., Kitagawa T. (2012) Site-specific protein dynamics in communication pathway from sensor to signaling domain of oxygen sensor protein, HemAT-Bs. Time-resolved ultraviolet Resonance Raman study. J. Biol. Chem. 287, 19973–19984 PubMed PMC
Pinakoulaki E., Yoshimura H., Daskalakis V., Yoshioka S., Aono S., Varotsis C. (2006) Two ligand binding sites in the O2-sensing signal transducer HemAT: implication for ligand recognition/discrimination and signaling. Proc. Natl. Acad. Sci. U.S.A. 103, 14796–14801 PubMed PMC
Pinakoulaki E., Yoshimura H., Yoshioka S., Aono S., Varotsis C. (2006) Recognition and discrimination of gases by the oxygen-sensing signal transducer protein HemAT as revealed by FTIR. Biochemistry 45, 7763–7766 PubMed
Yoshimura H., Yoshioka S., Kobayashi K., Ohta T., Uchida T., Kubo M., Kitagawa T., Aono S. (2006) Specific hydrogen-bonding networks responsible for selective O2 sensing of the oxygen sensor protein HemAT from Bacillus subtilis. Biochemistry 45, 8301–8307 PubMed
Casino P., Rubio V., Marina A. (2010) The mechanism of signal transduction by two-component systems. Curr. Opin. Struct. Biol. 20, 763–771 PubMed
Kitanishi K., Kobayashi K., Kawamura Y., Ishigami I., Ogura T., Nakajima K., Igarashi J., Tanaka A., Shimizu T. (2010) Important roles of Tyr43 at the putative heme distal side in the oxygen recognition and stability of the Fe(II)-O2 complex of YddV, a globin-coupled heme-based oxygen sensor diguanylate cyclase. Biochemistry 49, 10381–10393 PubMed
Hengge R. (2009) Principles of c-diGMP signalling in bacteria. Nat. Rev. Microbiol. 7, 263–273 PubMed
Schirmer T., Jenal U. (2009) Structure and mechanistic determinants of c-diGMP signaling. Nat. Rev. Microbiol. 7, 724–735 PubMed
Thijs L., Vinck E., Bolli A., Trandafir F., Wan X., Hoogewijs D., Coletta M., Fago A., Weber R. E., Van Doorslaer S., Ascenzi P., Alam M., Moens L., Dewilde S. (2007) Characterization of a globin-coupled oxygen sensor with a gene-regulating function. J. Biol. Chem. 282, 37325–37340 PubMed
Wan X., Tuckerman J. R., Saito J. A., Freitas T. A. K., Newhouse J. S., Denery J. R., Galperin M. Y., Gonzalez G., Gilles-Gonzalez M. A., Alam M. (2009) Globins synthesize the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate in bacteria. J. Mol. Biol. 388, 262–270 PubMed PMC
Sawai H., Yoshioka S., Uchida T., Hyodo M., Hayakawa Y., Ishimori K., Aono S. (2010) Molecular oxygen regulates the enzymatic activity of a heme-containing diguanylate cyclase (HemDGC) for the synthesis of cyclic diGMP. Biochim. Biophys. Acta 1804, 166–172 PubMed
Tuckerman J. R., Gonzalez G., Sousa E. H. S., Wan X., Saito J. A., Alam M., Gilles-Gonzalez M. A. (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-diGMP control. Biochemistry 48, 9764–9774 PubMed
Nakajima K., Kitanishi K., Kobayashi K., Kobayashi N., Igarashi J., Shimizu T. (2012) Leu65 in the heme distal side is critical for the stability of the Fe(II)-O2 complex of YddV, a globin-coupled oxygen sensor diguanylate cyclase. J. Inorg. Biochem. 108, 163–170 PubMed
Gong W., Hao B., Chan M. K. (2000) New mechanistic insights from structural studies of the oxygen-sensing domain of Bradyrhizobium japonicum FixL. Biochemistry 39, 3955–3962 PubMed
Hao B., Isaza C., Arndt J., Soltis M., Chan M. K. (2002) Structure-based mechanism of O2 sensing and ligand discrimination by the FixL heme domain of Bradyrhizobium japonicum. Biochemistry 41, 12952–12958 PubMed
Kurokawa H., Lee D. S., Watanabe M., Sagami I., Mikami B., Raman C. S., Shimizu T. (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J. Biol. Chem. 279, 20186–20193 PubMed
Park H., Suquet C., Satterlee J. D., Kang C. (2004) 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 43, 2738–2746 PubMed
Kitanishi K., Kobayashi K., Uchida T., Ishimori K., Igarashi J., Shimizu T. (2011) Identification and functional and spectral characterization of a globin-coupled histidine kinase from Anaeromyxobacter sp. Fw109-5. J. Biol. Chem. 286, 35522–35534 PubMed PMC
Stranzl G. R., Santelli E., Bankston L. A., La Clair C., Bobkov A., Schwarzenbacher R., Godzik A., Perego M., Grynberg M., Liddington R. C. (2011) Structural insights into inhibition of Bacillus anthracis sporulation by a novel class of non-heme globin sensor domains. J. Biol. Chem. 286, 8448–8458 PubMed PMC
Murray J. W., Delumeau O., Lewis R. J. (2005) Structure of a nonheme globin in environmental stress signaling. Proc. Natl. Acad. Sci. U.S.A. 102, 17320–17325 PubMed PMC
Nardini M., Pesce A., Thijs L., Saito J. A., Dewilde S., Alam M., Ascenzi P., Coletta M., Ciaccio C., Moens L., Bolognesi M. (2008) Archaeal protoglobin structure indicates new ligand diffusion paths and modulation of haem-reactivity. EMBO Rep. 9, 157–163 PubMed PMC
Kumar A., Toledo J. C., Patel R. P., Lancaster J. R., Jr., Steyn A. J. C. (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. U.S.A. 104, 11568–11573 PubMed PMC
Sousa E. H. S., Tuckerman J. R., Gonzalez G., Gilles-Gonzalez M. A. (2007) DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci. 16, 1708–1719 PubMed PMC
Ioanoviciu A., Yukl E. T., Moënne-Loccoz P., Ortiz de Montellano P. R. (2007) DevS, a heme-containing two-component oxygen sensor of Mycobacterium tuberculosis. Biochemistry 46, 4250–4260 PubMed PMC
Yukl E. T., Ioanoviciu A., Nakano M. M., Ortiz de Montellano P. R., Moënne-Loccoz P. (2008) A distal tyrosine residue is required for ligand discrimination in DevS from Mycobacterium tuberculosis. Biochemistry 47, 12532–12539 PubMed PMC
Ioanoviciu A., Meharenna Y. T., Poulos T. L., Ortiz de Montellano P. R. (2009) DevS oxy complex stability identified this heme protein as a gas sensor in Mycobacterium tuberculosis dormancy. Biochemistry 48, 5839–5848 PubMed PMC
Cho H. Y., Cho H. J., Kim Y. M., Oh J. I., Kang B. S. (2009) Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. J. Biol. Chem. 284, 13057–13067 PubMed PMC
Vos M. H., Bouzhir-Sima L., Lambry J.-C., Luo H., Eaton-Rye J. J., Ioanoviciu A., Ortiz de Montellano P. R., Liebl U. (2012) Ultrafast ligand dynamics in the heme-based GAF sensor domains of the histidine kinases DosS and DosT from Mycobacterium tuberculosis. Biochemistry 51, 159–166 PubMed PMC
Podust L. M., Ioanoviciu A., Ortiz de Montellano P. R. (2008) 2.3 Å x-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis. Biochemistry 47, 12523–12531 PubMed PMC
Gilles-Gonzalez M. A., Ditta G. S., Helinski D. R. (1991) A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350, 170–172 PubMed
Gong W., Hao B., Mansy S. S., Gonzalez G., Gilles-Gonzalez M. A., Chan M. K. (1998) Structure of a biological oxygen sensor: a new mechanism for heme-driven signal transduction. Proc. Natl. Acad. Sci. U.S.A. 95, 15177–15182 PubMed PMC
Gilles-Gonzalez M. A., Caceres A. I., Sousa E. H. S., Tomchick D. R., Brautigam C., Gonzalez C., Machius M. (2006) A proximal arginine R206 participates in switching of the Bradyrhizobium japonicum FixL oxygen sensor. J. Mol. Biol. 360, 80–89 PubMed
Miyatake H., Mukai M., Park S. Y., Adachi S., Tamura K., Nakamura H., Nakamura K., Tsuchiya T., Iizuka T., Shiro Y. (2000) Sensory mechanism of oxygen sensor FixL from Rhizobium meliloti: crystallographic, mutagenesis and resonance Raman spectroscopic studies. J. Mol. Biol. 301, 415–431 PubMed
Yamada S., Sugimoto H., Kobayashi M., Ohno A., Nakamura H., Shiro S. (2009) Structure of PAS-linked histidine kinase and the response regulator complex. Structure 17, 1333–1344 PubMed
Nakamura H., Kumita H., Imai K., Iizuka T., Shiro Y. (2004) ADP reduces the oxygen-binding affinity of a sensory histidine kinase, FixL: the possibility of an enhanced reciprocating kinase reaction. Proc. Natl. Acad. Sci. U.S.A. 101, 2742–2746 PubMed PMC
Nuernberger P., Lee K. F., Bonvalet A., Bouzhir-Sima L., Lambry J.-C., Liebl U., Joffre M., Vos M. H. (2011) Strong ligand-protein interactions revealed by ultrafast infrared spectroscopy of CO in the heme pocket of the oxygen sensor FixL. J. Am. Chem. Soc. 133, 17110–17113 PubMed
Gonzalez G., Gilles-Gonzalez M. A., Rybak-Akimova E. V., Buchalova M., Busch D. H. (1998) Mechanisms of autooxidation of the oxygen sensor FixL and Aplysia myoglobin: implication for oxygen-binding heme proteins. Biochemistry 37, 10188–10194 PubMed
Delgado-Nixon V. M., Gonzalez G., Gilles-Gonzalez M. A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39, 2685–2691 PubMed
Sasakura Y., Hirata S., Sugiyama S., Suzuki S., Taguchi S., Watanabe M., Matsui T., Sagami I., Shimizu T. (2002) Characterization of a direct oxygen sensor heme protein from Escherichia coli. Kinetics of the heme redox states and mutations at the heme-binding site on catalysis and structure. J. Biol. Chem. 277, 23821–23827 PubMed
Taguchi S., Matsui T., Igarashi J., Sasakura Y., Araki Y., Ito O., Sugiyama S., Sagami I., Shimizu T. (2004) Binding of oxygen and carbon monoxide to a heme-regulated phosphodiesterase from Escherichia coli. Kinetics and infrared spectra of the full-length wild-type enzyme, isolated PAS domain, and Met-95 mutants. J. Biol. Chem. 279, 3340–3347 PubMed
Tanaka A., Takahashi H., Shimizu T. (2007) Critical role of the heme axial ligand, Met95, in locking catalysis of the phosphodiesterase from Escherichia coli (Ec DOS) toward cyclic diGMP. J. Biol. Chem. 282, 21301–21307 PubMed
Ishitsuka Y., Araki Y., Tanaka A., Igarashi J., Ito O., Shimizu T. (2008) Arg97 at the heme distal side of the isolated heme-bound PAS domain of a heme-based oxygen sensor from Escherichia coli (Ec DOS) plays critical roles in autoxidation and binding to gases, particularly O2. Biochemistry 47, 8874–8884 PubMed
Kobayashi K., Tanaka A., Takahashi H., Igarashi J., Ishitsuka Y., Yokota N., Shimizu T. (2010) Catalysis and oxygen binding of Ec DOS: a haem-based oxygen-sensor enzyme from Escherichia coli. J. Biochem. 148, 693–703 PubMed
Yamashita T., Bouzhir-Sima L., Lambry J.-C., Liebl U., Vos M. H. (2008) Ligand dynamics and early signaling events in the heme domain of the sensor protein Dos from Escherichia coli. J. Biol. Chem. 283, 2344–2352 PubMed
Lechauve C., Bouzhir-Sima L., Yamashita T., Marden M. C., Vos M. H., Liebl U., Kiger L. (2009) Heme ligand binding properties and intradimer interactions in the full-length sensor protein Dos from Escherichia coli and its isolated heme domain. J. Biol. Chem. 284, 36146–36159 PubMed PMC
Shimizu T. (2013) The heme-based oxygen-sensor phosphodiesterase Ec DOS (DosP): structure-function relationships. Biosensors 3, 211–237 PubMed PMC
Yang J., Kloek A. P., Goldberg D. E., Mathews F. S. (1995) The structure of Ascaris hemoglobin domain I at 2.2 Å resolution: molecular features of oxygen avidity. Proc. Natl. Acad. Sci. U.S.A. 92, 4224–4228 PubMed PMC
Dunham C. M., Dioum E. M., Tuckerman J. R., Gonzalez G., Scott W. G., Gilles-Gonzalez M. A. (2003) A distal arginine in oxygen-sensing heme-PAS domain is essential to ligand binding, signal transduction, and structure. Biochemistry 42, 7701–7708 PubMed
Derbyshire E. R., Winter M. B., Ibrahim M., Deng S., Spiro T. G., Marletta M. A. (2011) Probing domain interactions in soluble guanylate cyclase. Biochemistry 50, 4281–4290 PubMed PMC
Derbyshire E. R., Marletta M. A. (2012) Structure and regulation of soluble guanylate cyclase. Annu. Rev. Biochem. 81, 533–559 PubMed
Yazawa S., Tsuchiya H., Hori H., Makino R. (2006) Functional characterization of two nucleotide-binding sites in soluble guanylate cyclase. J. Biol. Chem. 281, 21763–21770 PubMed
Makino R., Park S. Y., Obayashi E., Iizuka T., Hori H., Shiro Y. (2011) Oxygen binding and redox properties of the heme in soluble guanylate cyclase: implications for the mechanism of ligand discrimination. J. Biol. Chem. 286, 15678–15687 PubMed PMC
Mujoo K., Sharin V. G., Bryan N. S., Krumenacker J. S., Sloan C., Parveen S., Nikonoff L. E., Kots A. Y., Murad F. (2008) Role of nitric oxide signaling components in differentiation of embryonic stem cells into myocardial cells. Proc. Natl. Acad. Sci. U.S.A. 105, 18924–18929 PubMed PMC
Winter M. B., Herzik M. A., Jr., Kuriyan J., Marletta M. A. (2011) Tunnels modulate ligand flux in a heme nitric oxide/oxygen binding (H-NOX) domain. Proc. Natl. Acad. Sci. U.S.A. 108, E881–E889 PubMed PMC
Plate L., Marletta M. A. (2012) Nitric oxide modulates bacterial biofilm formation through a multicomponent cyclic-diGMP signaling network. Mol. Cell 46, 449–460 PubMed PMC
Liu N., Xu Y., Hossain S., Huang N., Coursolle D., Gralnick J. A., Boon E. M. (2012) Nitric oxide regulation of cyclic diGMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry 51, 2087–2099 PubMed
Muralidharan S., Boon E. M. (2012) Heme flattering is sufficient for signal transduction in the H-NOX family. J. Am. Chem. Soc. 134, 2044–2046 PubMed
Roberts G. P., Youn H., Kerby R. L. (2004) CO-sensing mechanism. Microbiol. Mol. Biol. Rev. 68, 453–473 PubMed PMC
Youn H., Kerby R. L., Roberts G. P. (2004) Changing the ligand specificity of CooA, a highly specific heme-based CO sensor. J. Biol. Chem. 279, 45744–45752 PubMed
Benabbas A., Karunakaran V., Youn H., Poulos T. L., Champion P. M. (2012) Effect of DNA binding on geminate CO recombination kinetics in the CO-sensing transcriptional factor, CooA. J. Biol. Chem. 287, 21729–21740 PubMed PMC
Lee A. J., Clark R. W., Youn H., Ponter S., Burstyn J. N. (2009) Guanidine hydrochloride-induced unfolding of the three heme coordination states of the CO-sensing transcription factor, CooA. Biochemistry 48, 6585–6597 PubMed PMC
Clark R. W., Youn H., Lee A. J., Roberts G. P., Burstyn J. N. (2007) DNA binding by an imidazole-sensing CooA variant is dependent on the heme redox state. J. Biol. Inorg. Chem. 12, 139–146 PubMed
Kubo M., Inagaki S., Yoshioka S., Uchida T., Mizutani Y., Aono S., Kitagawa T. (2006) Evidence for displacements of the C-helix by CO ligation and DNA binding to CooA revealed by UV resonance Raman spectroscopy. J. Biol. Chem. 281, 11271–11278 PubMed
Ibrahim M., Kerby R. L., Puranik M., Wasbotten I. H., Youn H., Roberts G. P., Spiro T. G. (2006) Heme displacement mechanism of CooA activation: mutational and Raman spectroscopic evidence. J. Biol. Chem. 281, 29165–29173 PubMed PMC
Komori H., Inagaki S., Yoshioka S., Aono S., Higuchi Y. (2007) Crystal structure of CO-sensing transcription activator CooA bound to exogenous ligand imidazole. J. Mol. Biol. 367, 864–871 PubMed
Tsai A. L., Berka V., Martin E., Olson J. S. (2012) A “sliding scale rule” for selectivity among NO, CO, and O2 by heme protein sensors. Biochemistry 51, 172–186 PubMed PMC
Tsai A. L., Martin E., Berka V., Olson J. S. (2012) How do heme-protein sensors exclude oxygen? Lessons learned from cytochrome c′, Nostoc puntiforme heme nitric oxide/oxygen-binding domain, and soluble guanylyl cyclase. Antioxid. Redox Signal. 17, 1246–1263 PubMed PMC
Tanaka A., Shimizu T. (2008) Ligand binding to the Fe(III)-protoporphyrin IX complex of phosphodiesterase from Escherichia coli (Ec DOS) markedly enhances catalysis of cyclic diGMP: roles of Met95, Arg97, and Phe113 of the putative heme distal side in catalytic regulation and ligand binding. Biochemistry 47, 13438–13446 PubMed
Chang A. L., Tuckerman J. R., Gonzalez G., Mayer R., Weinhouse H., Volman G., Amikam D., Benziman M., Gilles-Gonzalez M. A. (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40, 3420–3426 PubMed
Watts K. J., Taylor B. L., Johnson M. S. (2011) PAS/poly-HAMP signalling in Aer-2, a soluble haem-based sensor. Mol. Microbiol. 79, 686–699 PubMed PMC
Sawai H., Sugimoto H., Shiro Y., Ishikawa H., Mizutani Y., Aono S. (2012) Structural basis for oxygen sensing and signal transduction of the heme-based sensor protein Aer2 from Pseudomonas aeruginosa. Chem. Commun. 48, 6523–6525 PubMed
Vojtěchovský J., Chu K., Berendzen J., Sweet R. M., Schlichting I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77, 2153–2174 PubMed PMC
Pesce A., Nardini M., Dewilde S., Capece L., Martí M. A., Congia S., Salter M. D., Blouin G. C., Estrin D. A., Ascenzi P., Moens L., Bolognesi M., Olson J. S. (2011) Ligand migration in the apolar tunnel of Cerebratulus lacteus mini-hemoglobin. J. Biol. Chem. 286, 5347–5358 PubMed PMC
Hydrogen/Deuterium Exchange Mass Spectrometry of Heme-Based Oxygen Sensor Proteins