Ferritin-Like Proteins: A Conserved Core for a Myriad of Enzyme Complexes.
Aldehyde deformylating oxygenase
Cryo-electron microscopy
Ferritin-like superfamily
Methane monooxygenase
Ribonucleotide reductase
Serial femtosecond crystallography
X-ray crystallography
X-ray free electron laser
Journal
Sub-cellular biochemistry
ISSN: 0306-0225
Titre abrégé: Subcell Biochem
Pays: United States
ID NLM: 0316571
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
23
9
2022
pubmed:
24
9
2022
medline:
28
9
2022
Statut:
ppublish
Résumé
Ferritin-like proteins share a common fold, a four α-helix bundle core, often coordinating a pair of metal ions. Although conserved, the ferritin fold permits a diverse set of reactions, and is central in a multitude of macromolecular enzyme complexes. Here, we emphasize this diversity through three members of the ferritin-like superfamily: the soluble methane monooxygenase, the class I ribonucleotide reductase and the aldehyde deformylating oxygenase. They all rely on dinuclear metal cofactors to catalyze different challenging oxygen-dependent reactions through the formation of multi-protein complexes. Recent studies using cryo-electron microscopy, serial femtosecond crystallography at an X-ray free electron laser source, or single-crystal X-ray diffraction, have reported the structures of the active protein complexes, and revealed unprecedented insights into the molecular mechanisms of these three enzymes.
Identifiants
pubmed: 36151375
doi: 10.1007/978-3-031-00793-4_4
doi:
Substances chimiques
Aldehydes
0
Ions
0
Multienzyme Complexes
0
Ferritins
9007-73-2
Oxygenases
EC 1.13.-
Ribonucleotide Reductases
EC 1.17.4.-
Oxygen
S88TT14065
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
109-153Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Aberg A, Nordlund P, Eklund H (1993) Unusual clustering of carboxyl side chains in the core of iron-free ribonucleotide reductase. Nature 361(6409):276–278. https://doi.org/10.1038/361276a0
doi: 10.1038/361276a0
pubmed: 8423856
Acheson JF, Bailey LJ, Elsen NL, Fox BG (2014) Structural basis for biomolecular recognition in overlapping binding sites in a diiron enzyme system. Nat Commun 5:5009. https://doi.org/10.1038/ncomms6009
doi: 10.1038/ncomms6009
pubmed: 25248368
Ambundo EA, Friesner RA, Lippard SJ (2002) Reactions of methane monooxygenase intermediate Q with derivitized methanes. J Am Chem Soc 124(30):8770–8771
pubmed: 12137510
Andersson CS, Högbom M (2009) A mycobacterium tuberculosis ligand-binding Mn/Fe protein reveals a new cofactor in a remodeled R2-protein scaffold. Proc Natl Acad Sci 106(14):5633–5638. https://doi.org/10.1073/pnas.0812971106
doi: 10.1073/pnas.0812971106
pubmed: 19321420
pmcid: 2667070
Ando N, Brignole EJ, Zimanyi CM, Funk MA, Yokoyama K, Asturias FJ, Stubbe J, Drennan CL (2011) Structural interconversions modulate activity of Escherichia coli ribonucleotide reductase. Proc Natl Acad Sci U S A 108(52):21046–21051. https://doi.org/10.1073/pnas.1112715108
doi: 10.1073/pnas.1112715108
pubmed: 22160671
pmcid: 3248520
Andrews SC (2010) The Ferritin-like superfamily: evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim Biophys Acta 1800(8):691–705. https://doi.org/10.1016/j.bbagen.2010.05.010
doi: 10.1016/j.bbagen.2010.05.010
pubmed: 20553812
Argirević T, Riplinger C, Stubbe J, Neese F, Bennati M (2012) ENDOR spectroscopy and DFT calculations: evidence for the hydrogen-bond network within α2 in the PCET of E. coli ribonucleotide reductase. J Am Chem Soc 134(42):17661–17670. https://doi.org/10.1021/ja3071682
doi: 10.1021/ja3071682
pubmed: 23072506
pmcid: 4516058
Atkin CL, Thelander L, Reichard P, Lang G (1973) Iron and free radical in ribonucleotide reductase. Exchange of iron and Mössbauer spectroscopy of the protein B2 subunit of the Escherichia coli enzyme. J Biol Chem 248(21):7464–7472
pubmed: 4355582
Aukema KG, Makris TM, Stoian SA, Richman JE, Münck E, Lipscomb JD, Wackett LP (2013) Cyanobacterial aldehyde deformylase oxygenation of aldehydes yields n-1 aldehydes and alcohols in addition to alkanes. ACS Catal 3(10):2228–2238. https://doi.org/10.1021/cs400484m
doi: 10.1021/cs400484m
pubmed: 24490119
pmcid: 3903409
Aye Y, Li M, Long MJC, Weiss RS (2015) Ribonucleotide reductase and cancer: biological mechanisms and targeted therapies. Oncogene 34(16):2011–2021. https://doi.org/10.1038/onc.2014.155
doi: 10.1038/onc.2014.155
pubmed: 24909171
Bailey LJ, McCoy JG, Phillips GN, Fox BG (2008) Structural consequences of effector protein complex formation in a diiron hydroxylase. Proc Natl Acad Sci U S A 105(49):19194–19198. https://doi.org/10.1073/pnas.0807948105
doi: 10.1073/pnas.0807948105
pubmed: 19033467
pmcid: 2614738
Banerjee R, Lipscomb JD (2021) Small-molecule tunnels in metalloenzymes viewed as extensions of the active site. Acc Chem Res 54(9):2185–2195. https://doi.org/10.1021/acs.accounts.1c00058
doi: 10.1021/acs.accounts.1c00058
pubmed: 33886257
pmcid: 8130187
Banerjee R, Meier KK, Münck E, Lipscomb JD (2013) Intermediate P* from soluble methane monooxygenase contains a diferrous cluster. Biochemistry 52(25):4331–4342
pubmed: 23718184
Banerjee R, Proshlyakov Y, Lipscomb JD, Proshlyakov DA (2015) Structure of the key species in the enzymatic oxidation of methane to methanol. Nature 518(7539):431–434. https://doi.org/10.1038/nature14160
doi: 10.1038/nature14160
pubmed: 25607364
pmcid: 4429310
Banerjee R, Jones JC, Lipscomb JD (2019) Soluble methane monooxygenase. Ann Rev. Biochemist 88:409–431. https://doi.org/10.1146/annurev-biochem-013118-111529
doi: 10.1146/annurev-biochem-013118-111529
Bao L, Li J-J, Jia C, Li M, Lu X (2016) Structure-oriented substrate specificity engineering of aldehyde-deformylating oxygenase towards aldehydes carbon chain length. Biotechnol Biofuels 9(1):185. https://doi.org/10.1186/s13068-016-0596-9
doi: 10.1186/s13068-016-0596-9
pubmed: 27588038
pmcid: 5007808
Barynin VV, Whittaker MM, Antonyuk SV, Lamzin VS, Harrison PM, Artymiuk PJ, Whittaker JW (2001) Crystal structure of manganese catalase from Lactobacillus plantarum. Structure 9(8):725–738. https://doi.org/10.1016/s0969-2126(01)00628-1
doi: 10.1016/s0969-2126(01)00628-1
pubmed: 11587647
Basri RS, Rahman RNZRA, Kamarudin NHA, Ali MSM (2020) Cyanobacterial aldehyde deformylating oxygenase: structure, function, and potential in biofuels production. Int J Biol Macromol 164:3155–3162. https://doi.org/10.1016/j.ijbiomac.2020.08.162
doi: 10.1016/j.ijbiomac.2020.08.162
pubmed: 32841666
Berggren G, Duraffourg N, Sahlin M, Sjöberg B-M (2014) Semiquinone-induced maturation of Bacillus anthracis ribonucleotide reductase by a superoxide intermediate. J Biol Chem 289(46):31940–31949. https://doi.org/10.1074/jbc.M114.592535
doi: 10.1074/jbc.M114.592535
pubmed: 25262022
pmcid: 4231672
Bergmann U, Kern J, Schoenlein RW, Wernet P, Yachandra VK, Yano J (2021) Using X-ray free-electron lasers for spectroscopy of molecular catalysts and metalloenzymes. Nat Rev Phys 3(4):264–282. https://doi.org/10.1038/s42254-021-00289-3
doi: 10.1038/s42254-021-00289-3
pubmed: 34212130
pmcid: 8245202
Blaesi EJ, Palowitch GM, Hu K, Kim AJ, Rose HR, Alapati R, Lougee MG, Kim HJ, Taguchi AT, Tan KO, Laremore TN, Griffin RG, Krebs C, Matthews ML, Silakov A, Bollinger JM, Allen BD, Boal AK (2018) Metal-free class Ie ribonucleotide reductase from pathogens initiates catalysis with a tyrosine-derived dihydroxyphenylalanine radical. Proc Natl Acad Sci U S A 115(40):10022–10027. https://doi.org/10.1073/pnas.1811993115
doi: 10.1073/pnas.1811993115
pubmed: 30224458
pmcid: 6176560
Boal AK, Cotruvo JA, Stubbe J, Rosenzweig AC (2010) Structural basis for activation of class Ib ribonucleotide reductase. Science 329(5998):1526–1530. https://doi.org/10.1126/science.1190187
doi: 10.1126/science.1190187
pubmed: 20688982
pmcid: 3020666
Boal AK, Cotruvo JA, Stubbe J, Rosenzweig AC (2012) The dimanganese(II) site of Bacillus subtilis class Ib ribonucleotide reductase. Biochemistry 51(18):3861–3871. https://doi.org/10.1021/bi201925t
doi: 10.1021/bi201925t
pubmed: 22443445
Bou-Abdallah F (2010) The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta 1800(8):719–731. https://doi.org/10.1016/j.bbagen.2010.03.021
doi: 10.1016/j.bbagen.2010.03.021
pubmed: 20382203
Brazeau BJ, Lipscomb JD (2000) Kinetics and activation thermodynamics of methane monooxygenase compound Q formation and reaction with substrates. Biochemistry 39(44):13503–13515
pubmed: 11063587
Brazeau BJ, Lipscomb JD (2003) Key amino acid residues in the regulation of soluble methane monooxygenase catalysis by component B. Biochemistry 42(19):5618–5631
pubmed: 12741818
Brazeau BJ, Wallar BJ, Lipscomb JD (2001) Unmasking of deuterium kinetic isotope effects on the methane monooxygenase compound Q reaction by site-directed mutagenesis of component B. J Am Chem Soc 123(42):10421–10422
pubmed: 11604007
Buer BC, Paul B, Das D, Stuckey JA, Marsh ENG (2014) Insights into substrate and metal binding from the crystal structure of cyanobacterial aldehyde deformylating oxygenase with substrate bound. ACS Chem Biol 9(11):2584–2593. https://doi.org/10.1021/cb500343j
doi: 10.1021/cb500343j
pubmed: 25222710
pmcid: 4245163
Castillo RG, Banerjee R, Allpress CJ, Rohde GT, Bill E, Que L Jr, Lipscomb JD, DeBeer S (2017) High-energy-resolution fluorescence-detected X-ray absorption of the Q intermediate of soluble methane monooxygenase. J Am Chem Soc 139:18024–18033. https://doi.org/10.1021/jacs.7b09560
doi: 10.1021/jacs.7b09560
pubmed: 29136468
pmcid: 5729100
Chang SL, Wallar BJ, Lipscomb JD, Mayo KH (2001) Residues in Methylosinus trichosporium OB3b methane monooxygenase component B involved in molecular interactions with reduced- and oxidized-hydroxylase component: a role for the N-terminus. Biochemistry 40(32):9539–9551
pubmed: 11583153
Chang M, Shimba K, Hayashi Y, Arai M (2020) Electrostatic interactions at the interface of two enzymes are essential for two-step alkane biosynthesis in cyanobacteria. Biosci Biotechnol Biochem 84(2):228–237. https://doi.org/10.1080/09168451.2019.1677142
doi: 10.1080/09168451.2019.1677142
pubmed: 31601165
Chapman HN (2019) X-Ray free-electron lasers for the structure and dynamics of macromolecules. Annu Rev Biochem 88(1):35–58. https://doi.org/10.1146/annurev-biochem-013118-110744
doi: 10.1146/annurev-biochem-013118-110744
pubmed: 30601681
Chatwood LL, Mueller J, Gross JD, Wagner G, Lippard SJ (2004) NMR structure of the flavin domain from soluble methane monooxygenase reductase from Methylococcus capsulatus (Bath). Biochemistry 43(38):11983–11991
pubmed: 15379538
Cheng Y (2018) Single-particle cryo-EM-How did it get here and where will it go. Science 361(6405):876–880. https://doi.org/10.1126/science.aat4346
doi: 10.1126/science.aat4346
pubmed: 30166484
pmcid: 6460916
Chino M, Maglio O, Nastri F, Pavone V, DeGrado WF, Lombardi A (2015) Artificial Diiron enzymes with a de novo designed four-helix bundle structure: artificial diiron enzymes with a four-helix bundle structure. Eur J Inorg Chem 2015(21):3371–3390. https://doi.org/10.1002/ejic.201500470
doi: 10.1002/ejic.201500470
pubmed: 27630532
pmcid: 5019575
Choi YS, Zhang H, Brunzelle JS, Nair SK, Zhao H (2008) In vitro reconstitution and crystal structure of p-aminobenzoate N-oxygenase (Aur F) involved in aureothin biosynthesis. Proc Natl Acad Sci U S A 105(19):6858–6863. https://doi.org/10.1073/pnas.0712073105
doi: 10.1073/pnas.0712073105
pubmed: 18458342
pmcid: 2383931
Climent I, Sjöberg BM, Huang CY (1992) Site-directed mutagenesis and deletion of the carboxyl terminus of Escherichia coli ribonucleotide reductase protein R2. Effects on catalytic activity and subunit interaction. Biochemistry 31(20):4801–4807. https://doi.org/10.1021/bi00135a009
doi: 10.1021/bi00135a009
pubmed: 1591241
Clomburg JM, Crumbley AM, Gonzalez R (2017) Industrial biomanufacturing: The future of chemical production. Science 355(6320):aag0804. https://doi.org/10.1126/science.aag0804
doi: 10.1126/science.aag0804
pubmed: 28059717
Conrado RJ, Gonzalez R (2014) Envisioning the bioconversion of methane to liquid fuels. Science 343(6171):621–623. https://doi.org/10.1126/science.1246929
doi: 10.1126/science.1246929
pubmed: 24503844
Cooley RB, Arp DJ, Karplus PA (2010) Evolutionary origin of a secondary structure: π-helices as cryptic but widespread insertional variations of α-helices that enhance protein functionality. J Mol Biol 404(2):232–246. https://doi.org/10.1016/j.jmb.2010.09.034
doi: 10.1016/j.jmb.2010.09.034
pubmed: 20888342
pmcid: 2981643
Cotruvo JA Jr, Stubbe J (2012) Metallation and mismetallation of iron and manganese proteins in vitro and in vivo: the class I ribonucleotide reductases as a case study. Metallomics 4(10):1020. https://doi.org/10.1039/c2mt20142a
doi: 10.1039/c2mt20142a
pubmed: 22991063
Cotruvo JA, Stubbe J (2010) An active dimanganese(III)-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Biochemistry 49(6):1297–1309. https://doi.org/10.1021/bi902106n
doi: 10.1021/bi902106n
pubmed: 20070127
Cotruvo JA, Stich TA, Britt RD, Stubbe J (2013) Mechanism of assembly of the dimanganese-tyrosyl radical cofactor of class Ib ribonucleotide reductase: enzymatic generation of superoxide is required for tyrosine oxidation via a Mn(III)Mn(IV) intermediate. J Am Chem Soc 135(10):4027–4039. https://doi.org/10.1021/ja312457t
doi: 10.1021/ja312457t
pubmed: 23402532
pmcid: 3739481
Cox N, Ogata H, Stolle P, Reijerse E, Auling G, Lubitz W (2010) A tyrosyl-dimanganese coupled spin system is the native metalloradical cofactor of the R2F subunit of the ribonucleotide reductase of Corynebacterium ammoniagenes. J Am Chem Soc 132(32):11197–11213. https://doi.org/10.1021/ja1036995
doi: 10.1021/ja1036995
pubmed: 20698687
Crépin L, Barthe M, Leray F, Guillouet SE (2018) Alka(e)ne synthesis in Cupriavidus necator boosted by the expression of endogenous and heterologous ferredoxin–ferredoxin reductase systems. Biotechnol Bioeng 115(10):2576–2584. https://doi.org/10.1002/bit.26805
doi: 10.1002/bit.26805
pubmed: 30063082
Crichton RR, Declercq J-P (2010) X-ray structures of ferritins and related proteins. Biochim Biophys Acta 1800(8):706–718. https://doi.org/10.1016/j.bbagen.2010.03.019
doi: 10.1016/j.bbagen.2010.03.019
pubmed: 20363295
Cutsail GE, Banerjee R, Zhou A, Que L, Lipscomb JD, DeBeer S (2018) High-resolution extended X-ray absorption fine structure analysis provides evidence for a longer Fe···Fe distance in the Q intermediate of methane monooxygenase. J Am Chem Soc 140(48):16807–16820. https://doi.org/10.1021/jacs.8b10313
doi: 10.1021/jacs.8b10313
pubmed: 30398343
pmcid: 6470014
Das D, Ellington B, Paul B, Marsh ENG (2014) Mechanistic insights from reaction of α-oxiranyl-aldehydes with cyanobacterial aldehyde deformylating oxygenase. ACS Chem Biol 9(2):570–577. https://doi.org/10.1021/cb400772q
doi: 10.1021/cb400772q
pubmed: 24313866
Dassama LMK, Krebs C, Bollinger JM, Rosenzweig AC, Boal AK (2013) Structural basis for assembly of the Mn(IV)/Fe(III) cofactor in the class Ic ribonucleotide reductase from Chlamydia trachomatis. Biochemistry 52(37):6424–6436. https://doi.org/10.1021/bi400819x
doi: 10.1021/bi400819x
pubmed: 23924396
Divakaran A, Kirberger SE, Pomerantz WCK (2019) SAR by (protein-observed) 19F NMR. Acc Chem Res 52(12):3407–3418. https://doi.org/10.1021/acs.accounts.9b00377
doi: 10.1021/acs.accounts.9b00377
pubmed: 31718149
pmcid: 8117411
Doan PE, Shanmugam M, Stubbe J, Hoffman BM (2015) Composition and Structure of the Inorganic Core of Relaxed Intermediate X (Y122F) of Escherichia coli Ribonucleotide Reductase. J Am Chem Soc 137(49):15558–15566. https://doi.org/10.1021/jacs.5b10763
doi: 10.1021/jacs.5b10763
pubmed: 26636616
pmcid: 4732524
Ehrenberg A, Reichard P (1972) Electron spin resonance of the iron-containing protein B2 from ribonucleotide reductase. J Biol Chem 247(11):3485–3488
pubmed: 4337857
Elango NA, Radhakrishnan R, Froland WA, Wallar BJ, Earhart CA, Lipscomb JD, Ohlendorf DH (1997) Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b: structure methane monooxygenase hydroxylase. Protein Sci 6(3):556–568. https://doi.org/10.1002/pro.5560060305
doi: 10.1002/pro.5560060305
pubmed: 9070438
pmcid: 2143674
Eriksson M, Uhlin U, Ramaswamy S, Ekberg M, Regnström K, Sjöberg BM, Eklund H (1997) Binding of allosteric effectors to ribonucleotide reductase protein R1: reduction of active-site cysteines promotes substrate binding. Structure 5(8):1077–1092. https://doi.org/10.1016/s0969-2126(97)00259-1
doi: 10.1016/s0969-2126(97)00259-1
pubmed: 9309223
Eriksson M, Jordan A, Eklund H (1998) Structure of Salmonella typhimurium nrdF ribonucleotide reductase in its oxidized and reduced forms. Biochemistry 37(38):13359–13369. https://doi.org/10.1021/bi981380s
doi: 10.1021/bi981380s
pubmed: 9748343
Fox BG (2021) Diiron enzyme structure and catalysis. In: Comprehensive coordination chemistry III. Elsevier, pp 455–499
Fox BG, Froland WA, Dege JE, Lipscomb JD (1989) Methane monooxygenase from Methylosinus trichosporium OB3b. Purification and properties of a three-component system with high specific activity from a type II methanotroph. J Biol Chem 264(17):10023–10033
pubmed: 2542319
Fox BG, Liu Y, Dege JE, Lipscomb JD (1991) Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. Identification of sites of component interaction. J Biol Chem 266(1):540–550
pubmed: 1845980
Froland WA, Andersson KK, Lee S-K, Liu Y, Lipscomb JD (1992) Methane monooxygenase component B and reductase alter the regioselectivity of the hydroxylase component-catalyzed reactions. A novel role for protein-protein interactions in an oxygenase mechanism. J Biol Chem 267(25):17588–17597
pubmed: 1325441
Fuller FD, Gul S, Chatterjee R, Burgie ES, Young ID, Lebrette H, Srinivas V, Brewster AS, Michels-Clark T, Clinger JA, Andi B, Ibrahim M, Pastor E, de Lichtenberg C, Hussein R, Pollock CJ, Zhang M, Stan CA, Kroll T, Fransson T, Weninger C, Kubin M, Aller P, Lassalle L, Bräuer P, Miller MD, Amin M, Koroidov S, Roessler CG, Allaire M, Sierra RG, Docker PT, Glownia JM, Nelson S, Koglin JE, Zhu D, Chollet M, Song S, Lemke H, Liang M, Sokaras D, Alonso-Mori R, Zouni A, Messinger J, Bergmann U, Boal AK, Bollinger JM, Krebs C, Högbom M, Phillips GN, Vierstra RD, Sauter NK, Orville AM, Kern J, Yachandra VK, Yano J (2017) Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nat Methods 14(4):443–449. https://doi.org/10.1038/nmeth.4195
doi: 10.1038/nmeth.4195
pubmed: 28250468
pmcid: 5376230
Gallagher SC, Callaghan AJ, Zhao J, Dalton H, Trewhella J (1999) Global conformational changes control the reactivity of methane monooxygenase. Biochemistry 38(21):6752–6760
pubmed: 10346895
Gao Y, Zhang H, Fan M, Jia C, Shi L, Pan X, Cao P, Zhao X, Chang W, Li M (2020) Structural insights into catalytic mechanism and product delivery of cyanobacterial acyl-acyl carrier protein reductase. Nat Commun 11(1):1525. https://doi.org/10.1038/s41467-020-15268-y
doi: 10.1038/s41467-020-15268-y
pubmed: 32251275
pmcid: 7089970
Gassner GT, Lippard SJ (1999) Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath). Biochemistry 38(39):12768–12785
pubmed: 10504247
Ge J, Yu G, Ator MA, Stubbe J (2003) Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42(34):10071–10083. https://doi.org/10.1021/bi034374r
doi: 10.1021/bi034374r
pubmed: 12939135
Gräslund A, Sahlin M, Sjöberg BM (1985) The tyrosyl free radical in ribonucleotide reductase. Environ Health Perspect 64:139–149. https://doi.org/10.1289/ehp.64-1568609
doi: 10.1289/ehp.64-1568609
pubmed: 3007085
pmcid: 1568609
Grāve K, Lambert W, Berggren G, Griese JJ, Bennett MD, Logan DT, Högbom M (2019) Redox-induced structural changes in the di-iron and di-manganese forms of Bacillus anthracis ribonucleotide reductase subunit NrdF suggest a mechanism for gating of radical access. J Biol Inorg Chem 24(6):849–861. https://doi.org/10.1007/s00775-019-01703-z
doi: 10.1007/s00775-019-01703-z
pubmed: 31410573
pmcid: 6754363
Grāve K, Griese JJ, Berggren G, Bennett MD, Högbom M (2020) The Bacillus anthracis class Ib ribonucleotide reductase subunit NrdF intrinsically selects manganese over iron. J Biol Inorg Chem 25(4):571–582. https://doi.org/10.1007/s00775-020-01782-3
doi: 10.1007/s00775-020-01782-3
pubmed: 32296998
pmcid: 7239806
Green J, Dalton H (1985) Protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). A novel regulatory protein of enzyme activity. J Biol Chem 260(29):15795–15801
pubmed: 3934164
Green J, Dalton H (1986) Steady-state kinetic-analysis of soluble methane mono-oxygenase from Methylococcus-capsulatus (Bath). Biochem J 236(1):155–162
pubmed: 3098230
pmcid: 1146800
Green J, Dalton H (1989) Substrate specificity of soluble methane monooxygenase. Mechanistic implications. J Biol Chem 264(30):17698–17703
pubmed: 2808342
Greene BL, Taguchi AT, Stubbe J, Nocera DG (2017) Conformationally dynamic radical transfer within ribonucleotide reductase. J Am Chem Soc 139(46):16657–16665. https://doi.org/10.1021/jacs.7b08192
doi: 10.1021/jacs.7b08192
pubmed: 29037038
pmcid: 5702266
Greene BL, Kang G, Cui C, Bennati M, Nocera DG, Drennan CL, Stubbe J (2020) Ribonucleotide reductases: structure, chemistry, and metabolism suggest new therapeutic targets. Annu Rev Biochem 89(1):45–75. https://doi.org/10.1146/annurev-biochem-013118-111843
doi: 10.1146/annurev-biochem-013118-111843
pubmed: 32569524
pmcid: 7316142
Griese JJ, Roos K, Cox N, Shafaat HS, Branca RMM, Lehtio J, Graslund A, Lubitz W, Siegbahn PEM, Högbom M (2013) Direct observation of structurally encoded metal discrimination and ether bond formation in a heterodinuclear metalloprotein. Proc Natl Acad Sci U S A 110(43):17189–17194. https://doi.org/10.1073/pnas.1304368110
doi: 10.1073/pnas.1304368110
pubmed: 24101498
pmcid: 3808653
Guy JE, Whittle E, Moche M, Lengqvist J, Lindqvist Y, Shanklin J (2011) Remote control of regioselectivity in acyl-acyl carrier protein-desaturases. Proc Natl Acad Sci U S A 108(40):16594–16599. https://doi.org/10.1073/pnas.1110221108
doi: 10.1073/pnas.1110221108
pubmed: 21930947
pmcid: 3189045
Hammerstad M, Hersleth H-P, Tomter AB, Røhr AK, Andersson KK (2014) Crystal structure of Bacillus cereus class Ib ribonucleotide reductase di-iron NrdF in complex with NrdI. ACS Chem Biol 9(2):526–537. https://doi.org/10.1021/cb400757h
doi: 10.1021/cb400757h
pubmed: 24295378
Hayashi Y, Yasugi F, Arai M (2015) Role of cysteine residues in the structure, stability, and alkane producing activity of cyanobacterial aldehyde deformylating oxygenase. PLoS One 10(4):e0122217. https://doi.org/10.1371/journal.pone.0122217
doi: 10.1371/journal.pone.0122217
pubmed: 25837679
pmcid: 4383598
Hendrich MP, Münck E, Fox BG, Lipscomb JD (1990) Integer-spin EPR studies of the fully reduced methane monooxygenase hydroxylase component. J Am Chem Soc 112:5861–5865
Högbom M, Galander M, Andersson M, Kolberg M, Hofbauer W, Lassmann G, Nordlund P, Lendzian F (2003) Displacement of the tyrosyl radical cofactor in ribonucleotide reductase obtained by single-crystal high-field EPR and 1.4-Å x-ray data. Proc Natl Acad Sci U S A 100(6):3209–3214. https://doi.org/10.1073/pnas.0536684100
doi: 10.1073/pnas.0536684100
pubmed: 12624184
pmcid: 404301
Högbom M, Stenmark P, Voevodskaya N, McClarty G, Gräslund A, Nordlund P (2004) The radical site in chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305(5681):245–248. https://doi.org/10.1126/science.1098419
doi: 10.1126/science.1098419
pubmed: 15247479
Högbom M, Sjöberg B-M, Berggren G (2020) Radical enzymes. In: eLS. Wiley, pp 375–393
Jacobs AB, Banerjee R, Deweese DE, Braun A, Babicz JT Jr, Gee LB, Sutherlin KD, Bottger LH, Yoda Y, Saito M, Kitao S, Kobayashi Y, Seto M, Tamasaku K, Lipscomb JD, Park K, Solomon EI (2021) Nuclear resonance vibrational spectroscopic definition of the Fe(IV)2 intermediate Q in methane monooxygenase and its reactivity. J Am Chem Soc 143(39):16007–16029. https://doi.org/10.1021/jacs.1c05436
doi: 10.1021/jacs.1c05436
pubmed: 34570980
pmcid: 8631202
Jasniewski AJ, Que L (2018) Dioxygen activation by nonheme diiron enzymes: diverse dioxygen adducts, high-valent intermediates, and related model complexes. Chem Rev 118(5):2554–2592. https://doi.org/10.1021/acs.chemrev.7b00457
doi: 10.1021/acs.chemrev.7b00457
pubmed: 29400961
pmcid: 5920527
Jia C, Li M, Li J, Zhang J, Zhang H, Cao P, Pan X, Lu X, Chang W (2015) Structural insights into the catalytic mechanism of aldehyde-deformylating oxygenases. Protein Cell 6(1):55–67. https://doi.org/10.1007/s13238-014-0108-2
doi: 10.1007/s13238-014-0108-2
pubmed: 25482408
Jiang W, Yun D, Saleh L, Barr EW, Xing G, Hoffart LM, Maslak M-A, Krebs C, Bollinger JM (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science 316(5828):1188–1191. https://doi.org/10.1126/science.1141179
doi: 10.1126/science.1141179
pubmed: 17525338
Johansson R, Torrents E, Lundin D, Sprenger J, Sahlin M, Sjöberg B-M, Logan DT (2010) High-resolution crystal structures of the flavoprotein NrdI in oxidized and reduced states--an unusual flavodoxin. Structural biology. FEBS J 277(20):4265–4277. https://doi.org/10.1111/j.1742-4658.2010.07815.x
doi: 10.1111/j.1742-4658.2010.07815.x
pubmed: 20831589
Jones JC, Banerjee R, Shi K, Aihara H, Lipscomb JD (2020) Structural studies of the Methylosinus trichosporium OB3b soluble methane monooxygenase hydroxylase and regulatory component complex reveal a transient substrate tunnel. Biochemistry 59(32):2946–2961. https://doi.org/10.1021/acs.biochem.0c00459
doi: 10.1021/acs.biochem.0c00459
pubmed: 32692178
Jones JC, Banerjee R, Shi K, Semonis MM, Aihara H, Pomerantz WCK, Lipscomb JD (2021) Soluble methane monooxygenase component interactions monitored by 19F NMR. Biochemistry 60(25):1995–2010. https://doi.org/10.1021/acs.biochem.1c00293
doi: 10.1021/acs.biochem.1c00293
pubmed: 34100595
Kang G, Taguchi AT, Stubbe J, Drennan CL (2020) Structure of a trapped radical transfer pathway within a ribonucleotide reductase holocomplex. Science 368(6489):424–427. https://doi.org/10.1126/science.aba6794
doi: 10.1126/science.aba6794
pubmed: 32217749
pmcid: 7774503
Khara B, Menon N, Levy C, Mansell D, Das D, Marsh ENG, Leys D, Scrutton NS (2013) Production of propane and other short-chain alkanes by structure-based engineering of ligand specificity in aldehyde-deformylating oxygenase. Chembiochem 14(10):1204–1208. https://doi.org/10.1002/cbic.201300307
doi: 10.1002/cbic.201300307
pubmed: 23757044
pmcid: 4159587
Kim H, An S, Park YR, Jang H, Yoo H, Park SH, Lee SJ, Cho US (2019) MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase. Sci Adv 5(10):eaax0059. https://doi.org/10.1126/sciadv.aax0059
doi: 10.1126/sciadv.aax0059
pubmed: 31616787
pmcid: 6774732
Klähn S, Baumgartner D, Pfreundt U, Voigt K, Schön V, Steglich C, Hess WR (2014) Alkane biosynthesis genes in cyanobacteria and their transcriptional organization. Front Bioeng Biotechnol 2:24. https://doi.org/10.3389/fbioe.2014.00024
doi: 10.3389/fbioe.2014.00024
pubmed: 25022427
pmcid: 4094844
Klinman JP, Kohen A (2013) Hydrogen tunneling links protein dynamics to enzyme catalysis. Annu Rev Biochem 82:471–496. https://doi.org/10.1146/annurev-biochem-051710-133623
doi: 10.1146/annurev-biochem-051710-133623
pubmed: 23746260
pmcid: 4066974
Kopp DA, Gassner GT, Blazyk JL, Lippard SJ (2001) Electron-transfer reactions of the reductase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Biochemistry 40(49):14932–14941
pubmed: 11732913
Kudo H, Nawa R, Hayashi Y, Arai M (2016) Comparison of aldehyde-producing activities of cyanobacterial acyl-(acyl carrier protein) reductases. Biotechnol Biofuels 9:234. https://doi.org/10.1186/s13068-016-0644-5
doi: 10.1186/s13068-016-0644-5
pubmed: 27822307
pmcid: 5090900
Kudo H, Hayashi Y, Arai M (2019a) Identification of non-conserved residues essential for improving the hydrocarbon-producing activity of cyanobacterial aldehyde-deformylating oxygenase. Biotechnol Biofuels 12:89. https://doi.org/10.1186/s13068-019-1409-8
doi: 10.1186/s13068-019-1409-8
pubmed: 31015863
pmcid: 6469105
Kudo H, Hayashi Y, Arai M (2019b) Improving hydrocarbon production by engineering cyanobacterial acyl-(acyl carrier protein) reductase. Biotechnol Biofuels 12:291. https://doi.org/10.1186/s13068-019-1623-4
doi: 10.1186/s13068-019-1623-4
pubmed: 31890019
pmcid: 6916063
Lee SK, Lipscomb JD (1999) Oxygen activation catalyzed by methane monooxygenase hydroxylase component: proton delivery during the O-O bond cleavage steps. Biochemistry 38(14):4423–4432. https://doi.org/10.1021/bi982712w
doi: 10.1021/bi982712w
pubmed: 10194363
Lee SK, Fox BG, Froland WA, Lipscomb JD, Münck E (1993a) A transient intermediate of the methane monooxygenase catalytic cycle containing a FeIVFeIV cluster. J Am Chem Soc 115:6450–6451
Lee SK, Nesheim JC, Lipscomb JD (1993b) Transient intermediates of the methane monooxygenase catalytic cycle. J Biol Chem 268(29):21569–21577
pubmed: 8408008
Lee SJ, McCormick MS, Lippard SJ, Cho U-S (2013) Control of substrate access to the active site in methane monooxygenase. Nature 494(7437):380–384. https://doi.org/10.1038/nature11880
doi: 10.1038/nature11880
pubmed: 23395959
pmcid: 3596810
Li N, Nørgaard H, Warui DM, Booker SJ, Krebs C, Bollinger JM (2011) Conversion of fatty aldehydes to alka(e)nes and formate by a cyanobacterial aldehyde decarbonylase: cryptic redox by an unusual dimetal oxygenase. J Am Chem Soc 133(16):6158–6161. https://doi.org/10.1021/ja2013517
doi: 10.1021/ja2013517
pubmed: 21462983
pmcid: 3113487
Li N, Chang W-C, Warui DM, Booker SJ, Krebs C, Bollinger JM (2012) Evidence for only oxygenative cleavage of aldehydes to alk(a/e)nes and formate by cyanobacterial aldehyde decarbonylases. Biochemistry 51(40):7908–7916. https://doi.org/10.1021/bi300912n
doi: 10.1021/bi300912n
pubmed: 22947199
Lin F, Das D, Lin XN, Marsh ENG (2013) Aldehyde-forming fatty acyl-CoA reductase from cyanobacteria: expression, purification and characterization of the recombinant enzyme. FEBS J 280(19):4773–4781. https://doi.org/10.1111/febs.12443
doi: 10.1111/febs.12443
pubmed: 23895371
Lin Q, Parker MJ, Taguchi AT, Ravichandran K, Kim A, Kang G, Shao J, Drennan CL, Stubbe J (2017) Glutamate 52-β at the α/β subunit interface of Escherichia coli class Ia ribonucleotide reductase is essential for conformational gating of radical transfer. J Biol Chem 292(22):9229–9239. https://doi.org/10.1074/jbc.M117.783092
doi: 10.1074/jbc.M117.783092
pubmed: 28377505
pmcid: 5454104
Lindqvist Y, Huang W, Schneider G, Shanklin J (1996) Crystal structure of delta9 stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J 15(16):4081–4092
pubmed: 8861937
pmcid: 452130
Liu KE, Valentine AM, Wang DL, Huynh BH, Edmondson DE, Salifoglou A, Lippard SJ (1995a) Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 117(41):10174–10185
Liu Y, Nesheim JC, Lee S-K, Lipscomb JD (1995b) Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component. J Biol Chem 270(42):24662–246625
pubmed: 7559577
Liu Y, Nesheim JC, Paulsen KE, Stankovich MT, Lipscomb JD (1997) Roles of the methane monooxygenase reductase component in the regulation of catalysis. Biochemistry 36(17):5223–5233
pubmed: 9136884
Livada J, Martinie RJ, Dassama LMK, Krebs C, Bollinger JM, Silakov A (2015) direct measurement of the radical translocation distance in the class I ribonucleotide reductase from Chlamydia trachomatis. J Phys Chem B 119(43):13777–13784. https://doi.org/10.1021/acs.jpcb.5b04067
doi: 10.1021/acs.jpcb.5b04067
pubmed: 26087051
pmcid: 5840866
Logan DT (2011) Closing the circle on ribonucleotide reductases. Nat Struct Mol Biol 18(3):251–253. https://doi.org/10.1038/nsmb0311-251
doi: 10.1038/nsmb0311-251
pubmed: 21372851
Lundin D, Poole AM, Sjöberg B-M, Högbom M (2012) Use of structural phylogenetic networks for classification of the ferritin-like superfamily. J Biol Chem 287(24):20565–20575. https://doi.org/10.1074/jbc.M112.367458
doi: 10.1074/jbc.M112.367458
pubmed: 22535960
pmcid: 3370241
Lundin D, Berggren G, Logan D, Sjöberg B-M (2015) The origin and evolution of ribonucleotide reduction. Life 5(1):604–636. https://doi.org/10.3390/life5010604
doi: 10.3390/life5010604
pubmed: 25734234
pmcid: 4390871
Machado IMP, Atsumi S (2012) Cyanobacterial biofuel production. J Biotechnol 162(1):50–56. https://doi.org/10.1016/j.jbiotec.2012.03.005
doi: 10.1016/j.jbiotec.2012.03.005
pubmed: 22446641
Mak WS, Wang X, Arenas R, Cui Y, Bertolani S, Deng WQ, Tagkopoulos I, Wilson DK, Siegel JB (2020) Discovery, design, and structural characterization of alkane-producing enzymes across the ferritin-like superfamily. Biochemistry 59(40):3834–3843. https://doi.org/10.1021/acs.biochem.0c00665
doi: 10.1021/acs.biochem.0c00665
pubmed: 32935984
Makhlynets O, Boal AK, Rhodes DV, Kitten T, Rosenzweig AC, Stubbe J (2014) Streptococcus sanguinis class Ib ribonucleotide reductase: high activity with both iron and manganese cofactors and structural insights. J Biol Chem 289(9):6259–6272. https://doi.org/10.1074/jbc.M113.533554
doi: 10.1074/jbc.M113.533554
pubmed: 24381172
McCormick MS, Lippard SJ (2011) 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. Biochemistry 50(51):11058–11069. https://doi.org/10.1021/bi201248b
doi: 10.1021/bi201248b
pubmed: 22136180
McHugh JP, Rodríguez-Quinoñes F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 278(32):29478–29486. https://doi.org/10.1074/jbc.M303381200
doi: 10.1074/jbc.M303381200
pubmed: 12746439
McNeil BWJ, Thompson NR (2010) X-ray free-electron lasers. Nat Photonics 4:814–821. https://doi.org/10.1038/nphoton.2010.239
doi: 10.1038/nphoton.2010.239
Merkx M, Lippard SJ (2002) Why orfY? Characterization of MMOD, a long overlooked component of the soluble methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 277(8):5858–5865
pubmed: 11709550
Minnihan EC, Ando N, Brignole EJ, Olshansky L, Chittuluru J, Asturias FJ, Drennan CL, Nocera DG, Stubbe J (2013a) Generation of a stable, aminotyrosyl radical-induced α2β2 complex of Escherichia coli class Ia ribonucleotide reductase. Proc Natl Acad Sci U S A 110(10):3835–3840. https://doi.org/10.1073/pnas.1220691110
doi: 10.1073/pnas.1220691110
pubmed: 23431160
pmcid: 3593893
Minnihan EC, Nocera DG, Stubbe J (2013b) Reversible, long-range radical transfer in E. coli class Ia ribonucleotide reductase. Acc Chem Res 46(11):2524–2535. https://doi.org/10.1021/ar4000407
doi: 10.1021/ar4000407
pubmed: 23730940
Miret-Casals L, Baelo A, Julián E, Astola J, Lobo-Ruiz A, Albericio F, Torrents E (2018) Hydroxylamine derivatives as a new paradigm in the search of antibacterial agents. ACS Omega 3(12):17057–17069. https://doi.org/10.1021/acsomega.8b01384
doi: 10.1021/acsomega.8b01384
pubmed: 31458325
pmcid: 6643834
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49(D1):D412–D419. https://doi.org/10.1093/nar/gkaa913
doi: 10.1093/nar/gkaa913
pubmed: 33125078
Mitić N, Schwartz JK, Brazeau BJ, Lipscomb JD, Solomon EI (2008) CD and MCD studies of the effects of component B variant binding on the biferrous active site of methane monooxygenase. Biochemistry 47(32):8386–8397. https://doi.org/10.1021/bi800818w
doi: 10.1021/bi800818w
pubmed: 18627173
Monje-Casas F, Jurado J, Prieto-Alamo MJ, Holmgren A, Pueyo C (2001) Expression analysis of the nrdHIEF operon from Escherichia coli. Conditions that trigger the transcript level in vivo. J Biol Chem 276(21):18031–18037. https://doi.org/10.1074/jbc.M011728200
doi: 10.1074/jbc.M011728200
pubmed: 11278973
Muller J, Lugovskoy AA, Wagner G, Lippard SJ (2002) NMR structure of the [2Fe-2S] ferredoxin domain from soluble methane monooxygenase reductase and interaction with its hydroxylase. Biochemistry 41(1):42–51
pubmed: 11772001
Murzin AG, Chothia C (1992) Protein architecture: new superfamilies. Curr Opin Struct Biol 2(6):895–903. https://doi.org/10.1016/0959-440X(92)90116-O
doi: 10.1016/0959-440X(92)90116-O
Nastri F, Chino M, Maglio O, Bhagi-Damodaran A, Lu Y, Lombardi A (2016) Design and engineering of artificial oxygen-activating metalloenzymes. Chem Soc Rev 45(18):5020–5054. https://doi.org/10.1039/C5CS00923E
doi: 10.1039/C5CS00923E
pubmed: 27341693
pmcid: 5021598
Nesheim JC, Lipscomb JD (1996) Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C-H bond cleavage in a reaction cycle intermediate. Biochemistry 35(31):10240–10247. https://doi.org/10.1021/bi960596w
doi: 10.1021/bi960596w
pubmed: 8756490
Nick TU, Lee W, Kossmann S, Neese F, Stubbe J, Bennati M (2015) Hydrogen bond network between amino acid radical intermediates on the proton-coupled electron transfer pathway of E. coli α2 ribonucleotide reductase. J Am Chem Soc 137(1):289–298. https://doi.org/10.1021/ja510513z
doi: 10.1021/ja510513z
pubmed: 25516424
Nick TU, Ravichandran KR, Stubbe J, Kasanmascheff M, Bennati M (2017) Spectroscopic evidence for a H bond network at Y356 located at the subunit interface of active E. coli ribonucleotide reductase. Biochemistry 56(28):3647–3656. https://doi.org/10.1021/acs.biochem.7b00462
doi: 10.1021/acs.biochem.7b00462
pubmed: 28640584
Nordlund P, Eklund H (1995) Di-iron—carboxylate proteins. Curr Opin Struct Biol 5(6):758–766. https://doi.org/10.1016/0959-440X(95)80008-5
doi: 10.1016/0959-440X(95)80008-5
pubmed: 8749363
Nordlund P, Reichard P (2006) Ribonucleotide reductases. Annu Rev Biochem 75(1):681–706. https://doi.org/10.1146/annurev.biochem.75.103004.142443
doi: 10.1146/annurev.biochem.75.103004.142443
pubmed: 16756507
Nordlund P, Sjöberg BM, Eklund H (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345(6276):593–598. https://doi.org/10.1038/345593a0
doi: 10.1038/345593a0
pubmed: 2190093
Offenbacher AR, Vassiliev IR, Seyedsayamdost MR, Stubbe J, Barry BA (2009) Redox-linked structural changes in ribonucleotide reductase. J Am Chem Soc 131(22):7496–7497. https://doi.org/10.1021/ja901908j
doi: 10.1021/ja901908j
pubmed: 19489635
pmcid: 2917099
Onderko EL, Silakov A, Yosca TH, Green MT (2017) Characterization of a selenocysteine-ligated P450 compound I reveals direct link between electron donation and reactivity. Nat Chem 9(7):623–628. https://doi.org/10.1038/nchem.2781
doi: 10.1038/nchem.2781
pubmed: 28644466
Pandelia ME, Li N, Nørgaard H, Warui DM, Rajakovich LJ, Chang W-C, Booker SJ, Krebs C, Bollinger JM (2013) Substrate-triggered addition of dioxygen to the diferrous cofactor of aldehyde-deformylating oxygenase to form a diferric-peroxide intermediate. J Am Chem Soc 135(42):15801–15812. https://doi.org/10.1021/ja405047b
doi: 10.1021/ja405047b
pubmed: 23987523
Park AK, Kim I-S, Jeon BW, Roh SJ, Ryu M-Y, Baek H-R, Jo S-W, Kim Y-S, Park H, Lee JH, Yoon H-S, Kim H-W (2016) Crystal structures of aldehyde deformylating oxygenase from Limnothrix sp. KNUA012 and Oscillatoria sp. KNUA011. Biochem Biophys Res Commun 477(3):395–400. https://doi.org/10.1016/j.bbrc.2016.06.090
doi: 10.1016/j.bbrc.2016.06.090
pubmed: 27329814
Pilkington SJ, Dalton H (1990) Soluble methane monooxygenase from Methylococcus capsulatus (Bath). Methods Enzym 188:181–190
Plays M, Müller S, Rodriguez R (2021) Chemistry and biology of ferritin. Metallomics 13(5):mfab021. https://doi.org/10.1093/mtomcs/mfab021
doi: 10.1093/mtomcs/mfab021
pubmed: 33881539
Poulos TL (2014) Heme enzyme structure and function. Chem Rev 114:3919–3962
pubmed: 24400737
pmcid: 3981943
Pozzi C, Di Pisa F, Lalli D, Rosa C, Theil E, Turano P, Mangani S (2015) Time-lapse anomalous X-ray diffraction shows how Fe
doi: 10.1107/S1399004715002333
pubmed: 25849404
pmcid: 4388269
Rahmana Z, Sung BH, Yi J-Y, Bui LM, Lee JH, Kim SC (2014) Enhanced production of n-alkanes in Escherichia coli by spatial organization of biosynthetic pathway enzymes. J Biotechnol 192(Pt A):187–191. https://doi.org/10.1016/j.jbiotec.2014.10.014
doi: 10.1016/j.jbiotec.2014.10.014
pubmed: 25456061
Rajakovich LJ, Nørgaard H, Warui DM, Chang W, Li N, Booker SJ, Krebs C, Bollinger JM, Pandelia M-E (2015) Rapid reduction of the diferric-peroxyhemiacetal intermediate in aldehyde-deformylating oxygenase by a cyanobacterial ferredoxin: evidence for a free-radical mechanism. J Am Chem Soc 137(36):11695–11709. https://doi.org/10.1021/jacs.5b06345
doi: 10.1021/jacs.5b06345
pubmed: 26284355
Rajakovich LJ, Zhang B, McBride MJ, Boal AK, Krebs C, Martin Bollinger J (2020) Emerging structural and functional diversity in proteins with dioxygen-reactive dinuclear transition metal cofactors. In: Comprehensive natural products III. Elsevier, pp 215–250
Ravichandran KR, Minnihan EC, Wei Y, Nocera DG, Stubbe J (2015) Reverse electron transfer completes the catalytic cycle in a 2,3,5-trifluorotyrosine-substituted ribonucleotide reductase. J Am Chem Soc 137(45):14387–14395. https://doi.org/10.1021/jacs.5b09189
doi: 10.1021/jacs.5b09189
pubmed: 26492582
pmcid: 4678968
Ravichandran K, Minnihan EC, Lin Q, Yokoyama K, Taguchi AT, Shao J, Nocera DG, Stubbe J (2017) Glutamate 350 plays an essential role in conformational gating of long-range radical transport in Escherichia coli Class Ia ribonucleotide reductase. Biochemistry 56(6):856–868. https://doi.org/10.1021/acs.biochem.6b01145
doi: 10.1021/acs.biochem.6b01145
pubmed: 28103007
Reece SY, Seyedsayamdost MR (2017) Long-range proton-coupled electron transfer in the Escherichia coli class Ia ribonucleotide reductase. Essays Biochem 61(2):281–292. https://doi.org/10.1042/EBC20160072
doi: 10.1042/EBC20160072
pubmed: 28487404
Reece SY, Hodgkiss JM, Stubbe J, Nocera DG (2006) Proton-coupled electron transfer: the mechanistic underpinning for radical transport and catalysis in biology. Philos Trans R Soc Lond Ser B Biol Sci 361(1472):1351–1364. https://doi.org/10.1098/rstb.2006.1874
doi: 10.1098/rstb.2006.1874
Roca I, Torrents E, Sahlin M, Gibert I, Sjöberg B-M (2008) NrdI essentiality for class Ib ribonucleotide reduction in Streptococcus pyogenes. J Bacteriol 190(14):4849–4858. https://doi.org/10.1128/JB.00185-08
doi: 10.1128/JB.00185-08
pubmed: 18502861
pmcid: 2447006
Røhr AK, Hersleth H-P, Andersson KK (2010) Tracking flavin conformations in protein crystal structures with Raman spectroscopy and QM/MM calculations. Angew Chem Int Ed Engl 49(13):2324–2327. https://doi.org/10.1002/anie.200907143
doi: 10.1002/anie.200907143
pubmed: 20187055
Rose HR, Ghosh MK, Maggiolo AO, Pollock CJ, Blaesi EJ, Hajj V, Wei Y, Rajakovich LJ, Chang W-C, Han Y, Hajj M, Krebs C, Silakov A, Pandelia M-E, Bollinger JM, Boal AK (2018) Structural basis for superoxide activation of Flavobacterium johnsoniae Class I ribonucleotide reductase and for radical initiation by its dimanganese cofactor. Biochemistry 57(18):2679–2693. https://doi.org/10.1021/acs.biochem.8b00247
doi: 10.1021/acs.biochem.8b00247
pubmed: 29609464
Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366(6455):537–543
pubmed: 8255292
Rosenzweig AC, Nordlund P, Takahara PM, Frederick CA, Lippard SJ (1995) Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states. Chem Biol 2(6):409–418
pubmed: 9432288
Rozman Grinberg I, Lundin D, Hasan M, Crona M, Jonna VR, Loderer C, Sahlin M, Markova N, Borovok I, Berggren G, Hofer A, Logan DT, Sjöberg B-M (2018) Novel ATP-cone-driven allosteric regulation of ribonucleotide reductase via the radical-generating subunit. eLife 7:e31529. https://doi.org/10.7554/eLife.31529
doi: 10.7554/eLife.31529
pubmed: 29388911
pmcid: 5794259
Rozman Grinberg I, Berglund S, Hasan M, Lundin D, Ho FM, Magnuson A, Logan DT, Sjöberg B-M, Berggren G (2019) Class Id ribonucleotide reductase utilizes a Mn2(IV,III) cofactor and undergoes large conformational changes on metal loading. J Biol Inorg Chem 24(6):863–877. https://doi.org/10.1007/s00775-019-01697-8
doi: 10.1007/s00775-019-01697-8
pubmed: 31414238
pmcid: 6754362
Ruskoski TB, Boal AK (2021) The periodic table of ribonucleotide reductases. J Biol Chem 297(4):101137. https://doi.org/10.1016/j.jbc.2021.101137
doi: 10.1016/j.jbc.2021.101137
pubmed: 34461093
pmcid: 8463856
Sazinsky MH, Merkx M, Cadieux E, Tang S, Lippard SJ (2004) Preparation and X-ray structures of metal-free, dicobalt and dimanganese forms of soluble methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath). Biochemistry 43(51):16263–16276. https://doi.org/10.1021/bi048140z
doi: 10.1021/bi048140z
pubmed: 15610020
Sazinsky MH, Dunten PW, McCormick MS, DiDonato A, Lippard SJ (2006) X-ray structure of a hydroxylase-regulatory protein complex from a hydrocarbon-oxidizing multicomponent monooxygenase, Pseudomonas sp. OX1 phenol hydroxylase. Biochemistry 45(51):15392–15404. https://doi.org/10.1021/bi0618969
doi: 10.1021/bi0618969
pubmed: 17176061
Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329(5991):559–562. https://doi.org/10.1126/science.1187936
doi: 10.1126/science.1187936
pubmed: 20671186
Schwartz JK, Wei P, Mitchell KH, Fox BG, Solomon EI (2008) Geometric and electronic structure studies of the binuclear nonheme ferrous active site of toluene-4-monooxygenase: parallels with methane monooxygenase and insight into the role of the effector proteins in O2 activation. J Am Chem Soc 130(22):7098–7109
pubmed: 18479085
Seyedsayamdost MR, Stubbe J (2006) Site-specific replacement of Y356 with 3,4-dihydroxyphenylalanine in the beta2 subunit of E. coli ribonucleotide reductase. J Am Chem Soc 128(8):2522–2523. https://doi.org/10.1021/ja057776q
doi: 10.1021/ja057776q
pubmed: 16492021
Seyedsayamdost MR, Chan CTY, Mugnaini V, Stubbe J, Bennati M (2007) PELDOR spectroscopy with DOPA-beta2 and NH2Y-alpha2s: distance measurements between residues involved in the radical propagation pathway of E. coli ribonucleotide reductase. J Am Chem Soc 129(51):15748–15749. https://doi.org/10.1021/ja076459b
doi: 10.1021/ja076459b
pubmed: 18047343
Sharma A, Shakeel T, Gupta M, Rajacharya GH, Yazdani SS (2021) Biophysical and structural studies reveal marginal stability of a crucial hydrocarbon biosynthetic enzyme acyl ACP reductase. Sci Rep 11(1):12045. https://doi.org/10.1038/s41598-021-91232-0
doi: 10.1038/s41598-021-91232-0
pubmed: 34103559
pmcid: 8187606
Shu L, Nesheim JC, Kauffmann K, Münck E, Lipscomb JD, Que L Jr (1997) An FeIV2O2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 275(5299):515–518
pubmed: 8999792
Singh JS, Singh DP (2017) Methanotrophs: an emerging bioremediation tool with unique broad spectrum methane monooxygenase (MMO) enzyme. In: Agro-environmental sustainability, pp 1–18
Sjöberg BM, Reichard P, Gräslund A, Ehrenberg A (1978) The tyrosine free radical in ribonucleotide reductase from Escherichia coli. J Biol Chem 253(19):6863–6865
pubmed: 211133
Srinivas V, Lebrette H, Lundin D, Kutin Y, Sahlin M, Lerche M, Eirich J, Branca RMM, Cox N, Sjöberg B-M, Högbom M (2018) Metal-free ribonucleotide reduction powered by a DOPA radical in Mycoplasma pathogens. Nature 563(7731):416–420. https://doi.org/10.1038/s41586-018-0653-6
doi: 10.1038/s41586-018-0653-6
pubmed: 30429545
pmcid: 6317698
Srinivas V, Banerjee R, Lebrette H, Jones JC, Aurelius O, Kim I-S, Pham CC, Gul S, Sutherlin KD, Bhowmick A, John J, Bozkurt E, Fransson T, Aller P, Butryn A, Bogacz I, Simon P, Keable S, Britz A, Tono K, Kim KS, Park S-Y, Lee SJ, Park J, Alonso-Mori R, Fuller FD, Batyuk A, Brewster AS, Bergmann U, Sauter NK, Orville AM, Yachandra VK, Yano J, Lipscomb JD, Kern J, Högbom M (2020) High-resolution XFEL structure of the soluble methane monooxygenase hydroxylase complex with its regulatory component at ambient temperature in two oxidation states. J Am Chem Soc 142(33):14249–14266. https://doi.org/10.1021/jacs.0c05613
doi: 10.1021/jacs.0c05613
pubmed: 32683863
pmcid: 7457426
Stillman TJ, Hempstead PD, Artymiuk PJ, Andrews SC, Hudson AJ, Treffry A, Guest JR, Harrison PM (2001) The high-resolution X-ray crystallographic structure of the ferritin (EcFtnA) of Escherichia coli; comparison with human H ferritin (HuHF) and the structures of the Fe(3+) and Zn(2+) derivatives. J Mol Biol 307(2):587–603. https://doi.org/10.1006/jmbi.2001.4475
doi: 10.1006/jmbi.2001.4475
pubmed: 11254384
Theil EC (2011) Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry. Curr Opin Chem Biol 15(2):304–311. https://doi.org/10.1016/j.cbpa.2011.01.004
doi: 10.1016/j.cbpa.2011.01.004
pubmed: 21296609
pmcid: 3074017
Theil EC (2012) Ferritin protein nanocages-the story. Nanotechnol Percept 8(1):7–16. https://doi.org/10.4024/n03th12a.ntp.08.01
doi: 10.4024/n03th12a.ntp.08.01
pubmed: 24198751
pmcid: 3816979
Thomas WC, Brooks FP, Burnim AA, Bacik J-P, Stubbe J, Kaelber JT, Chen JZ, Ando N (2019) Convergent allostery in ribonucleotide reductase. Nat Commun 10(1):2653. https://doi.org/10.1038/s41467-019-10568-4
doi: 10.1038/s41467-019-10568-4
pubmed: 31201319
pmcid: 6572854
Tinberg CE, Lippard SJ (2011) Dioxygen activation in soluble methane monooxygenase. Acc Chem Res 44(4):280–288
pubmed: 21391602
pmcid: 3079780
Tomter AB, Zoppellaro G, Andersen NH, Hersleth H-P, Hammerstad M, Røhr ÅK, Sandvik GK, Strand KR, Nilsson GE, Bell CB, Barra A-L, Blasco E, Le Pape L, Solomon EI, Andersson KK (2013) Ribonucleotide reductase class I with different radical generating clusters. Coord Chem Rev 257(1):3–26. https://doi.org/10.1016/j.ccr.2012.05.021
doi: 10.1016/j.ccr.2012.05.021
Torrents E (2014) Ribonucleotide reductases: essential enzymes for bacterial life. Front Cell Infect Microbiol 4. https://doi.org/10.3389/fcimb.2014.00052
Trehoux A, Mahy J-P, Avenier F (2016) A growing family of O2 activating dinuclear iron enzymes with key catalytic diiron(III)-peroxo intermediates: Biological systems and chemical models. Coord Chem Rev 322:142–158. https://doi.org/10.1016/j.ccr.2016.05.014
doi: 10.1016/j.ccr.2016.05.014
Uhlin U, Eklund H (1994) Structure of ribonucleotide reductase protein R1. Nature 370(6490):533–539. https://doi.org/10.1038/370533a0
doi: 10.1038/370533a0
pubmed: 8052308
Uppsten M, Färnegårdh M, Domkin V, Uhlin U (2006) The first holocomplex structure of ribonucleotide reductase gives new insight into its mechanism of action. J Mol Biol 359(2):365–377. https://doi.org/10.1016/j.jmb.2006.03.035
doi: 10.1016/j.jmb.2006.03.035
pubmed: 16631785
Wallar BJ, Lipscomb JD (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters. Chem Rev 96(7):2625–2657
pubmed: 11848839
Wallar BJ, Lipscomb JD (2001) Methane monooxygenase component B mutants alter the kinetics of steps throughout the catalytic cycle. Biochemistry 40(7):2220–2233
pubmed: 11329291
Wang W, Lippard SJ (2014) Diiron oxidation state control of substrate access to the active site of soluble methane monooxygenase mediated by the regulatory component. J Am Chem Soc 136(6):2244–2247. https://doi.org/10.1021/ja412351b
doi: 10.1021/ja412351b
pubmed: 24476336
pmcid: 3954536
Wang Q, Huang X, Zhang J, Lu X, Li S, Li J-J (2014a) Engineering self-sufficient aldehyde deformylating oxygenases fused to alternative electron transfer systems for efficient conversion of aldehydes into alkanes. Chem Commun Camb Engl 50(33):4299–4301. https://doi.org/10.1039/c4cc00591k
doi: 10.1039/c4cc00591k
Wang W, Iacob RE, Luoh RP, Engen JR, Lippard SJ (2014b) Electron transfer control in soluble methane monooxygenase. J Am Chem Soc 136(27):9754–9762. https://doi.org/10.1021/ja504688z
doi: 10.1021/ja504688z
pubmed: 24937475
pmcid: 4105053
Wang W, Liang AD, Lippard SJ (2015) Coupling oxygen consumption with hydrocarbon oxidation in bacterial multicomponent monooxygenases. Acc Chem Res 48(9):2632–2639. https://doi.org/10.1021/acs.accounts.5b00312
doi: 10.1021/acs.accounts.5b00312
pubmed: 26293615
pmcid: 4624108
Wang C, Zhao C, Hu L, Chen H (2016) Calculated mechanism of cyanobacterial aldehyde-deformylating oxygenase: asymmetric aldehyde activation by a symmetric diiron cofactor. J Phys Chem Lett 7(21):4427–4432. https://doi.org/10.1021/acs.jpclett.6b02061
doi: 10.1021/acs.jpclett.6b02061
pubmed: 27775357
Wang Q, Bao L, Jia C, Li M, Li J-J, Lu X (2017a) Identification of residues important for the activity of aldehyde-deformylating oxygenase through investigation into the structure-activity relationship. BMC Biotechnol 17(1):31. https://doi.org/10.1186/s12896-017-0351-8
doi: 10.1186/s12896-017-0351-8
pubmed: 28302170
pmcid: 5356278
Wang VC-C, Maji S, Chen PP-Y, Lee HK, Yu SS-F, Chan SI (2017b) Alkane oxidation: methane monooxygenases, related enzymes, and their biomimetics. Chem Rev 117(13):8574–8621. https://doi.org/10.1021/acs.chemrev.6b00624
doi: 10.1021/acs.chemrev.6b00624
pubmed: 28206744
Wang W, Zhang Y, Zhao G, Wang H (2021) Ferritin with atypical ferroxidase centers takes B-channels as the pathway for Fe
doi: 10.1021/acs.inorgchem.1c00265
pubmed: 33852289
Warui DM, Li N, Nørgaard H, Krebs C, Bollinger JM, Booker SJ (2011) Detection of formate, rather than carbon monoxide, as the stoichiometric coproduct in conversion of fatty aldehydes to alkanes by a cyanobacterial aldehyde decarbonylase. J Am Chem Soc 133(10):3316–3319. https://doi.org/10.1021/ja111607x
doi: 10.1021/ja111607x
pubmed: 21341652
pmcid: 3069495
Warui DM, Pandelia M-E, Rajakovich LJ, Krebs C, Bollinger JM, Booker SJ (2015) Efficient delivery of long-chain fatty aldehydes from the Nostoc punctiforme Acyl–Acyl carrier protein reductase to its cognate aldehyde-deformylating oxygenase. Biochemistry 54(4):1006–1015. https://doi.org/10.1021/bi500847u
doi: 10.1021/bi500847u
pubmed: 25496470
Yokoyama K, Uhlin U, Stubbe J (2010) A hot oxidant, 3-NO2Y122 radical, unmasks conformational gating in ribonucleotide reductase. J Am Chem Soc 132(43):15368–15379. https://doi.org/10.1021/ja1069344
doi: 10.1021/ja1069344
pubmed: 20929229
pmcid: 3005585
Yu F, Cangelosi VM, Zastrow ML, Tegoni M, Plegaria JS, Tebo AG, Mocny CS, Ruckthong L, Qayyum H, Pecoraro VL (2014) Protein design: toward functional metalloenzymes. Chem Rev 114(7):3495–3578. https://doi.org/10.1021/cr400458x
doi: 10.1021/cr400458x
pubmed: 24661096
pmcid: 4300145
Zhang J, Wallar BJ, Popescu CV, Renner DB, Thomas DD, Lipscomb JD (2006) Methane monooxygenase hydroxylase and B component interactions. Biochemistry 45(9):2913–2926
pubmed: 16503646
Zhang J, Lu X, Li J-J (2013) Conversion of fatty aldehydes into alk (a/e)nes by in vitroreconstituted cyanobacterial aldehyde-deformylating oxygenase with the cognate electron transfer system. Biotechnol Biofuels 6(1):86. https://doi.org/10.1186/1754-6834-6-86
doi: 10.1186/1754-6834-6-86
pubmed: 23759169
pmcid: 3691600
Zheng H, Lipscomb JD (2006) Regulation of methane monooxygenase catalysis based on size exclusion and quantum tunneling. Biochemistry 45(6):1685–1692
pubmed: 16460015
Zhou YJ, Kerkhoven EJ, Nielsen J (2018) Barriers and opportunities in bio-based production of hydrocarbons. Nat Energy 3(11):925–935. https://doi.org/10.1038/s41560-018-0197-x
doi: 10.1038/s41560-018-0197-x