Effects of zinc on particulate methane monooxygenase activity and structure

Journal of Biological Chemistry

Volumn 289, Issue 31, 2014, Pages 21782-21794

  Sirajuddin, Sarah ^a   Barupala, Dulmini ^b   Helling, Stefan ^c   Marcus, Katrin ^c   Stemmler, Timothy L ^b   Rosenzweig, Amy C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; METHANE; ZINC;

ACTIVITY ASSAYS; MEMBRANE-BOUND; MEMBRANE-BOUND METALLOENZYME; METAL BINDING; METHANE MONOOXYGENASE; METHANOTROPHIC BACTERIA; RESPIRATORY COMPLEX; ZINC BINDING;

COPPER;

COPPER; COPPER ION; IRON; METAL; METHANE MONOOXYGENASE; ZINC; ZINC ION; OXYGENASE;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; LIGAND BINDING; METHYLOCOCCUS CAPSULATUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTON TRANSPORT; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PROTEIN CONFORMATION; X RAY ABSORPTION SPECTROSCOPY;

CRYSTALLIZATION; METHYLOCOCCUS CAPSULATUS; OXYGENASES; PROTEIN CONFORMATION; X-RAY ABSORPTION SPECTROSCOPY; ZINC;

EID: 84905366330     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.581363     Document Type: Article

References (65)

1. Semrau, J. D., Dispirito, A. A., and Yoon, S. (2010) Methanotrophs and copper. FEMS Microbiol. Lett. 34, 496-531
2. Conrado, R. J., and Gonzalez, R. (2014) Envisioning the bioconversion of methane to liquid fuels. Science 343, 621-623
3. Culpepper, M. A., and Rosenzweig, A. C. (2012) Architecture and active site of particulate methane monooxygenase. Crit. Rev. Biochem. Mol. Biol. 47, 483-492
4. Tinberg, C. E., and Lippard, S. J. (2011) Dioxygen activation in soluble methane monooxygenase. Acc. Chem. Res. 44, 280-288
5. Murrell, J. C., McDonald, I. R., and Gilbert, B. (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol. 8, 221-225 (Pubitemid 30236242)
6. Rosenzweig, A. C., Frederick, C. A., Lippard, S. J., and Nordlund, P. (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366, 537-543 (Pubitemid 24035993)
7. Rosenzweig, A. C. (2008) The metal centres of particulate methane monooxygenase. Biochem. Soc. Trans. 36, 1134-1137
8. Lieberman, R. L., and Rosenzweig, A. C. (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434, 177-182 (Pubitemid 40388042)
9. Hakemian, A. S., Kondapalli, K. C., Telser, J., Hoffman, B. M., Stemmler, T. L., and Rosenzweig, A. C. (2008) The metal centers of particulate methane monooxygenase from Methylosinus trichosporium OB3b. Biochemistry 47, 6793-6801 (Pubitemid 351898934)
10. Smith, S. M., Rawat, S., Telser, J., Hoffman, B. M., Stemmler, T. L., and Rosenzweig, A. C. (2011) Crystal structure and characterization of particulate methane monooxygenase from Methylocystis species strain M. Biochemistry 50, 10231-10240
11. Balasubramanian, R., Smith, S. M., Rawat, S., Yatsunyk, L. A., Stemmler, T. L., and Rosenzweig, A. C. (2010) Oxidation of methane by a biological dicopper centre. Nature 465, 115-119
12. Culpepper, M. A., Cutsail, G. E., 3rd, Hoffman, B. M., and Rosenzweig, A. C. (2012) Evidence for oxygen binding at the active site of particulate methane monooxygenase. J. Am. Chem. Soc. 134, 7640-7643
13. Martinho, M., Choi, D. W., Dispirito, A. A., Antholine, W. E., Semrau, J. D., and Münck, E. (2007) Mössbauer studies of the membrane-associated methane monooxygenase from Methylococcus capsulatus Bath: evidence for a diiron center. J. Am. Chem. Soc. 129, 15783-15785
14. Hakemian, A. S., and Rosenzweig, A. C. (2007) The biochemistry of methane oxidation. Annu. Rev. Biochem. 76, 223-241
15. Chen, C. L., Chen, K. H., Ke, S. C., Yu, S. S., and Chan, S. I. (2004) Preparation and characterization of a (Cu, Zn)-pMMO from Methylococcus capsulatus (Bath). J. Inorg. Biochem. 98, 2125-2130 (Pubitemid 39488141)
16. Cook, S. A., and Shiemke, A. K. (1996) Evidence that copper is a required cofactor for the membrane-bound form of methane monooxygenase. J. Inorg. Biochem. 63, 273-284 (Pubitemid 26275203)
17. Takeguchi, M., Miyakawa, K., and Okura, I. (1999) The role of copper in particulate methane monooxygenase from Methylosinus trichosporium OB3b. J. Mol. Catal. A 137, 161-168
18. Smith, S. M., Balasubramanian, R., and Rosenzweig, A. C. (2011) Metal reconstitution of particulate methane monooxygenase and heterologous expression of the pmoB subunit. Methods Enzymol. 495, 195-210
19. Whittenbury, R., Phillips, K. C., and Wilkinson, J. F. (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J. Gen. Microbiol. 61, 205-218
20. Helling, S., Hüttemann, M., Kadenbach, B., Ramzan, R., Vogt, S., and Marcus, K. (2012) Discovering the phosphoproteome of the hydrophobic cytochrome c oxidase membrane protein complex. Methods Mol. Biol. 893, 345-358
21. Reidegeld, K. A., Eisenacher, M., Kohl, M., Chamrad, D., Körting, G., Blüggel, M., Meyer, H. E., and Stephan, C. (2008) An easy-to-use Decoy Database Builder software tool, implementing different decoy strategies for false discovery rate calculation in automated MS/MS protein ientifications. Proteomics 8, 1129-1137 (Pubitemid 351462918)
22. Voegtli, W.C., Sommerhalter, M., Saleh, L., Baldwin, J., Bollinger, J. M., Jr., and Rosenzweig, A. C. (2003) Variable coordination geometries at the diiron(II) active site of ribonucleotide reductase R2. J. Am. Chem. Soc. 125, 15822-15830 (Pubitemid 37553699)
23. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
24. Strong, M., Sawaya, M. R., Wang, S., Phillips, M., Cascio, D., and Eisenberg, D. (2006) Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 103, 8060-8065 (Pubitemid 43801052)
25. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
26. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
27. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
28. Adams, P. D., Afonine, P. V., Bunkczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
29. George, G., and Pickering, I. (1995) EXAFSPAK: a suite of computer programs for analysis of x-ray absorption spectra. SSRL, Stanford
30. Ankudinov, A. L., and Rehr, J. J. (1997) Relativistic calculations of spin-dependent X-ray absorption spectra. Phys. Rev. B 56, R1712-R1715
31. Lee, P. A., Citrin, P. H., Eisenberger, P., and Kincaid, B. M. (1981) Extended x-ray absorption fine structure- its strengths and limitations as a structural tool. Rev. Mod. Phys. 53, 769-806
32. Lieberman, R. L., Kondapalli, K. C., Shrestha, D. B., Hakemian, A. S., Smith, S. M., Telser, J., Kuzelka, J., Gupta, R., Borovik, A. S., Lippard, S. J., Hoffman, B. M., Rosenzweig, A. C., and Stemmler, T. L. (2006) Characterization of the particulate methane monooxygenase metal centers in multiple redox states by X-ray absorption spectroscopy. Inorg. Chem. 45, 8372-8381
33. Wang, B., Alam, S. L., Meyer, H. H., Payne, M., Stemmler, T. L., Davis, D. R., and Sundquist, W. I. (2003) Structure and ubiquitin interactions of the conserved zinc finger domain of Npl4. J. Biol. Chem. 278, 20225-20234 (Pubitemid 36799220)
34. Bencze, K. Z., Kondapalli, K. C., and Stemmler, T. L. (2007) in Applications of Physical Methods to Inorganic and Bioinorganic Chemistry: Handbook, Encyolopedia of Inorganic Chemistry (Scott, R. A., and Lukehart, C. M., eds) 2nd Ed., pp. 513-528, John Wiley & Sons, Ltd, Chichester, UK
35. Lieberman, R. L., Shrestha, D. B., Doan, P. E., Hoffman, B. M., Stemmler, T. L., and Rosenzweig, A. C. (2003) Purified particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a dimer with both mononuclear copper and a copper-containing cluster. Proc. Natl. Acad. Sci. U.S.A. 100, 3820-3825 (Pubitemid 36418114)
36. 2+ with extremely high affinity. J. Am. Chem. Soc. 134, 7773-7779
37. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems, pp.465-473, John Wiley & Sons, Inc., New York
38. Wang, S., Lee, M. H., Hausinger, R. P., Clark, P. A., Wilcox, D. E., and Scott, R. A. (1994) Structure of the dinuclear active site of urease. X-ray absorption spectroscopic study of native and 2-mercaptoethanol-inhibited bacterial and plant enzymes. Inorg. Chem. 33, 1589-1593
39. Allen, F. H. (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr. Sect. B Struct. Sci. 58, 380-388
40. Stemmler, T. L., Sossong, T. M., Jr., Goldstein, J. I., Ash, D. E., Elgren, T. E., Kurtz, D. M., Jr., and Penner-Hahn, J. E. (1997) EXAFS comparison of the dimanganese core structures of manganese catalase, arginase and manga-nese- substituted ribonucleotide reductase and hemerythrin. Biochemistry 36, 9847-9858 (Pubitemid 27364696)
41. Reiter, N. J., Osterman, A., Torres-Larios, A., Swinger, K. K., Pan, T., and Mondragón, A. (2010) Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature 468, 784-789
42. McLellan, J. S., Yang, Y., Graham, B. S., and Kwong, P. D. (2011) Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J. Virol. 85, 7788-7796
43. Brohawn, S. G., del Mármol, J., and MacKinnon, R. (2012) Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K+ Ion Channel. Science 335, 436-441
44. Yamashita, S., Takeshita, D., and Tomita, K. (2014) Translocation and rotation of tRNA during template-independent RNA polymerization by tRNA nucleotidyltransferase. Structure 22, 315-325
45. 3 cytochrome oxidase provides insights into proton pumping. Science 329, 327-330
46. Törnroth-Horsefield, S., Gourdon, P., Horsefield, R., Brive, L., Yamamoto, N., Mori, H., Snijder, A., and Neutze, R. (2007) Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 15, 1663-1673 (Pubitemid 350213410)
47. Bowman, J. P., Skerratt, J. H., Nichols, P. D., and Sly, L. I. (1991) Phospholipid fatty acid and lipopolysaccharide fatty acid signature lipids in methane utilizing bacteria. FEMS Microbiol. Lett. 85, 15-22
48. Fang, J., Barcelona, M. J., and Semrau, J. D. (2000) Characterization of methanotrophic bacteria on the basis of intact phospholipid profiles. FEMS Microbiol. Lett. 189, 67-72 (Pubitemid 30456248)
49. o site. Biochemistry 50, 4263-4272
50. Faxén, K., Salomonsson, L., Adelroth, P., and Brzezinski, P. (2006) Inhibition of proton pumping by zinc ions during specific reaction steps in cytochrome c oxidase. Biochim. Biophys. Acta 1757, 388-394 (Pubitemid 43993872)
51. Kuznetsova, S. S., Azarkina, N. V., Vygodina, T. V., Siletsky, S. A., and Konstantinov, A. A. (2005) Zinc ions as cytochrome c oxidase inhibitors: Two sites of action. Biochemistry 70, 128-136 (Pubitemid 40512318)
52. Mills, D. A., Schmidt, B., Hiser, C., Westley, E., and Ferguson-Miller, S. (2002) Membrane potential-controlled inhibition of cytochrome c oxidase by zinc. J. Biol. Chem. 277, 14894-14901 (Pubitemid 34952563)
53. 2+-binding site at the P-side of the membrane. FEBS Lett. 582, 4158-4162
54. Muramoto, K., Hirata, K., Shinzawa-Itoh, K., Yoko-o, S., Yamashita, E., Aoyama, H., Tsukihara, T., and Yoshikawa, S. (2007) A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. U.S.A. 104, 7881-7886 (Pubitemid 47185845)
55. Qin, L., Mills, D. A., Hiser, C., Murphree, A., Garavito, R. M., Ferguson-Miller, S., and Hosler, J. (2007) Crystallographic location and mutational analysis of Zn and Cd inhibitory sites and role of lipidic carboxylates in rescuing proton path mutants in cytochrome c oxidase. Biochemistry 46, 6239-6248 (Pubitemid 46842867)
56. 2+ in bacterial reaction centers. Proc. Natl. Acad. Sci. U.S.A. 97, 1542-1547
57. Paddock, M. L., Graige, M. S., Feher, G., and Okamura, M. Y. (1999) Identification of the proton pathway in bacterial reaction centers: Inhibition of proton transfer by binding of Zn2+ or Cd2+. Proc. Natl. Acad. Sci. U.S.A. 96, 6183-6188 (Pubitemid 29256640)
58. Utschig, L. M., Ohigashi, Y., Thurnauer, M. C., and Tiede, D. M. (1998) A new metal-binding site in photosynthetic bacterial reaction centers that modulates QA to QB electron transfer. Biochemistry 37, 8278-8281 (Pubitemid 28275446)
59. 1 complex. Biochim. Biophys. Acta 1459, 440-448
60. 1 complexes. Biophys. J. 93, 2934-2951
61. Shiemke, A. K., Cook, S. A., Miley, T., and Singleton, P. (1995) Detergent solubilization of membrane-bound methane monooxygenase requires plastoquinol analogs as electron donors. Arch. Biochem. Biophys. 321, 421-428
62. Choi, D. W., Kunz, R. C., Boyd, E. S., Semrau, J. D., Antholine, W. E., Han, J. I., Zahn, J. A., Boyd, J. M., de la Mora, A. M., and DiSpirito, A. A. (2003) The membrane-associated methane monooxygenase pMMO and pMMO-NADH:quinone oxidoreductase complex from Methylococcus capsulatus Bath. J. Bacteriol. 185, 5755-5764 (Pubitemid 37176487)
63. Cook, S. A., and Shiemke, A. K. (2002) Evidence that a type-2 NADH: quinone oxidoreductase mediates electron transfer to particulate methane monooxygenase in Methylococcus capsulatus. Arch. Biochem. Biophys. 398, 32-40 (Pubitemid 34848322)
64. Shiemke, A. K., Arp, D. J., and Sayavedra-Soto, L. A. (2004) Inhibition of membrane-bound methane monooxygenase and ammonia monooxygenase by diphenyliodonium: implications for electron transfer. J. Bacteriol. 186, 928-937 (Pubitemid 38209452)
65. Palsdottir, H., and Hunte, C. (2004) Lipids in membrane protein structures. Biochim. Biophys. Acta 1666, 2-18