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Product bound structures of the soluble methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath): protein motion in the alpha-subunit.

Sazinsky MH, Lippard SJ
J Am Chem Soc 127 5814-25 (2005)
Related entries: 1xu3, 1xu5, 1xvb, 1xvc, 1xvd, 1xvf, 1xvg

Cited: 40 times
EuropePMC logo PMID: 15839679

Abstract

The soluble methane monooxygenase hydroxylase (MMOH) alpha-subunit contains a series of cavities that delineate the route of substrate entrance to and product egress from the buried carboxylate-bridged diiron center. The presence of discrete cavities is a major structural difference between MMOH, which can hydroxylate methane, and toluene/o-xylene monooxygenase hydroxylase (ToMOH), which cannot. To understand better the functions of the cavities and to investigate how an enzyme designed for methane hydroxylation can also accommodate larger substrates such as octane, methylcubane, and trans-1-methyl-2-phenylcyclopropane, MMOH crystals were soaked with an assortment of different alcohols and their X-ray structures were solved to 1.8-2.4 A resolution. The product analogues localize to cavities 1-3 and delineate a path of product exit and/or substrate entrance from the active site to the surface of the protein. The binding of the alcohols to a position bridging the two iron atoms in cavity 1 extends and validates previous crystallographic, spectroscopic, and computational work indicating this site to be where substrates are hydroxylated and products form. The presence of these alcohols induces perturbations in the amino acid side-chain gates linking pairs of cavities, allowing for the formation of a channel similar to one observed in ToMOH. Upon binding of 6-bromohexan-1-ol, the pi helix formed by residues 202-211 in helix E of the alpha-subunit is extended through residue 216, changing the orientations of several amino acid residues in the active site cavity. This remarkable secondary structure rearrangement in the four-helix bundle has several mechanistic implications for substrate accommodation and the function of the effector protein, MMOB.

Reviews - 1xve mentioned but not cited (1)

  1. Enzymatic oxidation of methane. Sirajuddin S, Rosenzweig AC. Biochemistry 54 2283-2294 (2015)

Articles - 1xve mentioned but not cited (1)

  1. Insights into the different dioxygen activation pathways of methane and toluene monooxygenase hydroxylases. Bochevarov AD, Li J, Song WJ, Friesner RA, Lippard SJ. J Am Chem Soc 133 7384-7397 (2011)


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  2. Evolutionary origin of a secondary structure: π-helices as cryptic but widespread insertional variations of α-helices that enhance protein functionality. Cooley RB, Arp DJ, Karplus PA. J Mol Biol 404 232-246 (2010)
  3. Structural basis for activation of class Ib ribonucleotide reductase. Boal AK, Cotruvo JA, Stubbe J, Rosenzweig AC. Science 329 1526-1530 (2010)
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  5. Characterization of the arene-oxidizing intermediate in ToMOH as a diiron(III) species. Murray LJ, Naik SG, Ortillo DO, García-Serres R, Lee JK, Huynh BH, Lippard SJ. J Am Chem Soc 129 14500-14510 (2007)
  6. X-ray structure of a hydroxylase-regulatory protein complex from a hydrocarbon-oxidizing multicomponent monooxygenase, Pseudomonas sp. OX1 phenol hydroxylase. Sazinsky MH, Dunten PW, McCormick MS, DiDonato A, Lippard SJ. Biochemistry 45 15392-15404 (2006)
  7. Determining macromolecular assembly structures by molecular docking and fitting into an electron density map. Lasker K, Sali A, Wolfson HJ. Proteins 78 3205-3211 (2010)
  8. Coupling Oxygen Consumption with Hydrocarbon Oxidation in Bacterial Multicomponent Monooxygenases. Wang W, Liang AD, Lippard SJ. Acc Chem Res 48 2632-2639 (2015)
  9. X-ray crystal structures of manganese(II)-reconstituted and native toluene/o-xylene monooxygenase hydroxylase reveal rotamer shifts in conserved residues and an enhanced view of the protein interior. McCormick MS, Sazinsky MH, Condon KL, Lippard SJ. J Am Chem Soc 128 15108-15110 (2006)
  10. Analysis of substrate access to active sites in bacterial multicomponent monooxygenase hydroxylases: X-ray crystal structure of xenon-pressurized phenol hydroxylase from Pseudomonas sp. OX1. McCormick MS, Lippard SJ. Biochemistry 50 11058-11069 (2011)
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  13. Identification of the binding region of the [2Fe-2S] ferredoxin in stearoyl-acyl carrier protein desaturase: insight into the catalytic complex and mechanism of action. Sobrado P, Lyle KS, Kaul SP, Turco MM, Arabshahi I, Marwah A, Fox BG. Biochemistry 45 4848-4858 (2006)
  14. Site-directed amino acid substitutions in the hydroxylase alpha subunit of butane monooxygenase from Pseudomonas butanovora: Implications for substrates knocking at the gate. Halsey KH, Sayavedra-Soto LA, Bottomley PJ, Arp DJ. J Bacteriol 188 4962-4969 (2006)
  15. Dissecting π-helices: sequence, structure and function. Kumar P, Bansal M. FEBS J 282 4415-4432 (2015)
  16. MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase. Kim H, An S, Park YR, Jang H, Yoo H, Park SH, Lee SJ, Cho US. Sci Adv 5 eaax0059 (2019)
  17. Structural Studies of the Methylosinus trichosporium OB3b Soluble Methane Monooxygenase Hydroxylase and Regulatory Component Complex Reveal a Transient Substrate Tunnel. Jones JC, Banerjee R, Shi K, Aihara H, Lipscomb JD. Biochemistry 59 2946-2961 (2020)
  18. Systematic Perturbations of Binuclear Non-heme Iron Sites: Structure and Dioxygen Reactivity of de Novo Due Ferri Proteins. Snyder RA, Betzu J, Butch SE, Reig AJ, DeGrado WF, Solomon EI. Biochemistry 54 4637-4651 (2015)
  19. Reactions of the diiron(IV) intermediate Q in soluble methane monooxygenase with fluoromethanes. Beauvais LG, Lippard SJ. Biochem Biophys Res Commun 338 262-266 (2005)
  20. Structure-Spectroscopy Correlations for Intermediate Q of Soluble Methane Monooxygenase: Insights from QM/MM Calculations. Schulz CE, Castillo RG, Pantazis DA, DeBeer S, Neese F. J Am Chem Soc 143 6560-6577 (2021)
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  22. Alanine 101 and alanine 110 of the alpha subunit of Pseudomonas stutzeri OX1 toluene-o-xylene monooxygenase influence the regiospecific oxidation of aromatics. Vardar G, Tao Y, Lee J, Wood TK. Biotechnol Bioeng 92 652-658 (2005)
  23. Crystal structures of substrate-free and nitrosyl cytochrome P450cin: implications for O(2) activation. Madrona Y, Tripathi S, Li H, Poulos TL. Biochemistry 51 6623-6631 (2012)
  24. Deciphering the origin of million-fold reactivity observed for the open core diiron [HO-FeIII-O-FeIV[double bond, length as m-dash]O]2+ species towards C-H bond activation: role of spin-states, spin-coupling, and spin-cooperation. Ansari M, Senthilnathan D, Rajaraman G. Chem Sci 11 10669-10687 (2020)
  25. Syntrophic Interactions Within a Butane-Oxidizing Bacterial Consortium Isolated from Puguang Gas Field in China. Zhang Y, Deng CP, Shen B, Yang JS, Wang ET, Yuan HL. Microb Ecol 72 538-548 (2016)
  26. Mechanistic investigation of cyclohexane oxidation by a non-heme iron complex: evidence of product inhibition by UV/vis stopped-flow studies. Gregor LC, Rowe GT, Rybak-Akimova E, Caradonna JP. Dalton Trans 41 777-782 (2012)
  27. Batch Production of High-Quality Graphene Grids for Cryo-EM: Cryo-EM Structure of Methylococcus capsulatus Soluble Methane Monooxygenase Hydroxylase. Ahn E, Kim B, Park S, Erwin AL, Sung SH, Hovden R, Mosalaganti S, Cho US. ACS Nano 17 6011-6022 (2023)
  28. Electron Transfer to Hydroxylase through Component Interactions in Soluble Methane Monooxygenase. Lee C, Hwang Y, Kang HG, Lee SJ. J Microbiol Biotechnol 32 287-293 (2022)


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