1zj9 › Citations

Siroheme- and [Fe4-S4]-dependent NirA from Mycobacterium tuberculosis is a sulfite reductase with a covalent Cys-Tyr bond in the active site.

Schnell R, Sandalova T, Hellman U, Lindqvist Y, Schneider G
J Biol Chem 280 27319-28 (2005)
Cited: 58 times
EuropePMC logo PMID: 15917234

Abstract

The nirA gene of Mycobacterium tuberculosis is up-regulated in the persistent state of the bacteria, suggesting that it is a potential target for the development of antituberculosis agents particularly active against the pathogen in its dormant phase. This gene encodes a ferredoxin-dependent sulfite reductase, and the structure of the enzyme has been determined using x-ray crystallography. The enzyme is a monomer comprising 555 amino acids and contains a [Fe4-S4] cluster and a siroheme cofactor. The molecule is built up of three domains with an alpha/beta fold. The first domain consists of two ferredoxin-like subdomains, related by a pseudo-2-fold symmetry axis passing through the whole molecule. The other two domains, which provide much of the binding interactions with the cofactors, have a common fold that is unique to the sulfite/nitrite reductase family. The domains form a trilobal structure, with the cofactors and the active site located at the interface of all three domains in the center of the molecule. NirA contains an unusual covalent bond between the side chains of Tyr69 and Cys161 in the active site, in close proximity to the siroheme cofactor. Removal of this covalent bond by site-directed mutagenesis impairs catalytic activity, suggesting that it is important for the enzymatic reaction. These residues are part of a sequence fingerprint, able to distinguish between ferredoxin-dependent sulfite and nitrite reductases. Comparison of NirA with the structure of the truncated NADPH-dependent sulfite reductase from Escherichia coli suggests a binding site for the external electron donor ferredoxin close to the [Fe4-S4] cluster.

Articles - 1zj9 mentioned but not cited (3)

  1. Comparative Genome and Network Centrality Analysis to Identify Drug Targets of Mycobacterium tuberculosis H37Rv. Melak T, Gakkhar S. Biomed Res Int 2015 212061 (2015)
  2. Maximum flow approach to prioritize potential drug targets of Mycobacterium tuberculosis H37Rv from protein-protein interaction network. Melak T, Gakkhar S. Clin Transl Med 4 61 (2015)
  3. Isolation, expression, and biochemical characterization: nitrite reductase from Bacillus cereus LJ01. Huang YY, Liang MH, Zhao S, Chen SM, Liu JS, Liu DM, Lu YZ. RSC Adv 10 37871-37882 (2020)


Reviews citing this publication (6)

  1. Drug targets in mycobacterial sulfur metabolism. Bhave DP, Muse WB, Carroll KS. Infect Disord Drug Targets 7 140-158 (2007)
  2. Thiol dioxygenases: unique families of cupin proteins. Stipanuk MH, Simmons CR, Karplus PA, Dominy JE. Amino Acids 41 91-102 (2011)
  3. Structure and function of atypically coordinated enzymatic mononuclear non-heme-Fe(II) centers. Buongiorno D, Straganz GD. Coord Chem Rev 257 541-563 (2013)
  4. Understanding and applying tyrosine biochemical diversity. Jones LH, Narayanan A, Hett EC. Mol Biosyst 10 952-969 (2014)
  5. New targets and inhibitors of mycobacterial sulfur metabolism. Paritala H, Carroll KS. Infect Disord Drug Targets 13 85-115 (2013)
  6. Molecular understanding of heteronuclear active sites in heme-copper oxidases, nitric oxide reductases, and sulfite reductases through biomimetic modelling. Reed CJ, Lam QN, Mirts EN, Lu Y. Chem Soc Rev 50 2486-2539 (2021)

Articles citing this publication (49)

  1. TubercuList--10 years after. Lew JM, Kapopoulou A, Jones LM, Cole ST. Tuberculosis (Edinb) 91 1-7 (2011)
  2. The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration. Oliveira TF, Vonrhein C, Matias PM, Venceslau SS, Pereira IA, Archer M. J Biol Chem 283 34141-34149 (2008)
  3. Anaerobic growth of Corynebacterium glutamicum using nitrate as a terminal electron acceptor. Nishimura T, Vertès AA, Shinoda Y, Inui M, Yukawa H. Appl Microbiol Biotechnol 75 889-897 (2007)
  4. Synthesis of amino acid cofactor in cysteine dioxygenase is regulated by substrate and represents a novel post-translational regulation of activity. Dominy JE, Hwang J, Guo S, Hirschberger LL, Zhang S, Stipanuk MH. J Biol Chem 283 12188-12201 (2008)
  5. Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga Cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sulfite reductase-like enzyme. Imamura S, Terashita M, Ohnuma M, Maruyama S, Minoda A, Weber AP, Inouye T, Sekine Y, Fujita Y, Omata T, Tanaka K. Plant Cell Physiol 51 707-717 (2010)
  6. High-resolution structural analysis of a novel octaheme cytochrome c nitrite reductase from the haloalkaliphilic bacterium Thioalkalivibrio nitratireducens. Polyakov KM, Boyko KM, Tikhonova TV, Slutsky A, Antipov AN, Zvyagilskaya RA, Popov AN, Bourenkov GP, Lamzin VS, Popov VO. J Mol Biol 389 846-862 (2009)
  7. Comparative analyses of nonpathogenic, opportunistic, and totally pathogenic mycobacteria reveal genomic and biochemical variabilities and highlight the survival attributes of Mycobacterium tuberculosis. Rahman SA, Singh Y, Kohli S, Ahmad J, Ehtesham NZ, Tyagi AK, Hasnain SE. mBio 5 e02020 (2014)
  8. A designed heme-[4Fe-4S] metalloenzyme catalyzes sulfite reduction like the native enzyme. Mirts EN, Petrik ID, Hosseinzadeh P, Nilges MJ, Lu Y. Science 361 1098-1101 (2018)
  9. Perturbation of cytochrome c maturation reveals adaptability of the respiratory chain in Mycobacterium tuberculosis. Small JL, Park SW, Kana BD, Ioerger TR, Sacchettini JC, Ehrt S. mBio 4 e00475-13 (2013)
  10. Structure of the dissimilatory sulfite reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus. Schiffer A, Parey K, Warkentin E, Diederichs K, Huber H, Stetter KO, Kroneck PM, Ermler U. J Mol Biol 379 1063-1074 (2008)
  11. The alternative route to heme in the methanogenic archaeon Methanosarcina barkeri. Kühner M, Haufschildt K, Neumann A, Storbeck S, Streif J, Layer G. Archaea 2014 327637 (2014)
  12. Cross-link formation of the cysteine 228-tyrosine 272 catalytic cofactor of galactose oxidase does not require dioxygen. Rogers MS, Hurtado-Guerrero R, Firbank SJ, Halcrow MA, Dooley DM, Phillips SE, Knowles PF, McPherson MJ. Biochemistry 47 10428-10439 (2008)
  13. Spectroscopic and computational characterization of the NO adduct of substrate-bound Fe(II) cysteine dioxygenase: insights into the mechanism of O2 activation. Blaesi EJ, Gardner JD, Fox BG, Brunold TC. Biochemistry 52 6040-6051 (2013)
  14. Cleavage of a carbon-fluorine bond by an engineered cysteine dioxygenase. Li J, Griffith WP, Davis I, Shin I, Wang J, Li F, Wang Y, Wherritt DJ, Liu A. Nat Chem Biol 14 853-860 (2018)
  15. Sulfite reduction in mycobacteria. Pinto R, Harrison JS, Hsu T, Jacobs WR, Leyh TS. J Bacteriol 189 6714-6722 (2007)
  16. Spectroscopic and computational investigation of iron(III) cysteine dioxygenase: implications for the nature of the putative superoxo-Fe(III) intermediate. Blaesi EJ, Fox BG, Brunold TC. Biochemistry 53 5759-5770 (2014)
  17. Structural insights into dissimilatory sulfite reductases: structure of desulforubidin from desulfomicrobium norvegicum. Oliveira TF, Franklin E, Afonso JP, Khan AR, Oldham NJ, Pereira IA, Archer M. Front Microbiol 2 71 (2011)
  18. Probing the Cys-Tyr Cofactor Biogenesis in Cysteine Dioxygenase by the Genetic Incorporation of Fluorotyrosine. Li J, Koto T, Davis I, Liu A. Biochemistry 58 2218-2227 (2019)
  19. Probing the function of the Tyr-Cys cross-link in metalloenzymes by the genetic incorporation of 3-methylthiotyrosine. Zhou Q, Hu M, Zhang W, Jiang L, Perrett S, Zhou J, Wang J. Angew Chem Int Ed Engl 52 1203-1207 (2013)
  20. The electronic structure of the Cys-Tyr(*) free radical in galactose oxidase determined by EPR spectroscopy. Lee YK, Whittaker MM, Whittaker JW. Biochemistry 47 6637-6649 (2008)
  21. Identification and functional analysis of a nitrate assimilation operon nasACKBDEF from Amycolatopsis mediterranei U32. Shao Z, Gao J, Ding X, Wang J, Chiao J, Zhao G. Arch Microbiol 193 463-477 (2011)
  22. Structural and mutational studies of an electron transfer complex of maize sulfite reductase and ferredoxin. Kim JY, Nakayama M, Toyota H, Kurisu G, Hase T. J Biochem 160 101-109 (2016)
  23. Atomic resolution modeling of the ferredoxin:[FeFe] hydrogenase complex from Chlamydomonas reinhardtii. Chang CH, King PW, Ghirardi ML, Kim K. Biophys J 93 3034-3045 (2007)
  24. Shifting redox states of the iron center partitions CDO between crosslink formation or cysteine oxidation. Njeri CW, Ellis HR. Arch Biochem Biophys 558 61-69 (2014)
  25. Spectroscopic Investigation of Cysteamine Dioxygenase. Fernandez RL, Dillon SL, Stipanuk MH, Fox BG, Brunold TC. Biochemistry 59 2450-2458 (2020)
  26. The C-terminal of CysM from Mycobacterium tuberculosis protects the aminoacrylate intermediate and is involved in sulfur donor selectivity. Agren D, Schnell R, Schneider G. FEBS Lett 583 330-336 (2009)
  27. Mycobacterium tuberculosis H2S Functions as a Sink to Modulate Central Metabolism, Bioenergetics, and Drug Susceptibility. Kunota TTR, Rahman MA, Truebody BE, Mackenzie JS, Saini V, Lamprecht DA, Adamson JH, Sevalkar RR, Lancaster JR, Berney M, Glasgow JN, Steyn AJC. Antioxidants (Basel) 10 1285 (2021)
  28. A novel variant of ferredoxin-dependent sulfite reductase having preferred substrate specificity for nitrite in the unicellular red alga Cyanidioschyzon merolae. Sekine K, Sakakibara Y, Hase T, Sato N. Biochem J 423 91-98 (2009)
  29. Identifying proteins that can form tyrosine-cysteine crosslinks. Martinie RJ, Godakumbura PI, Porter EG, Divakaran A, Burkhart BJ, Wertz JT, Benson DE. Metallomics 4 1037-42, 1008 (2012)
  30. Purification, crystallization and preliminary crystallographic analysis of a dissimilatory DsrAB sulfite reductase in complex with DsrC. Oliveira TF, Vonrhein C, Matias PM, Venceslau SS, Pereira IA, Archer M. J Struct Biol 164 236-239 (2008)
  31. The Nonphysiological Reductant Sodium Dithionite and [FeFe] Hydrogenase: Influence on the Enzyme Mechanism. Martini MA, Rüdiger O, Breuer N, Nöring B, DeBeer S, Rodríguez-Maciá P, Birrell JA. J Am Chem Soc 143 18159-18171 (2021)
  32. RNA‑seq analyses of antibiotic resistance mechanisms in Serratia marcescens. Li Z, Xu M, Wei H, Wang L, Deng M. Mol Med Rep 20 745-754 (2019)
  33. The crystal structure of siroheme decarboxylase in complex with iron-uroporphyrin III reveals two essential histidine residues. Haufschildt K, Schmelz S, Kriegler TM, Neumann A, Streif J, Arai H, Heinz DW, Layer G. J Mol Biol 426 3272-3286 (2014)
  34. NirA Is an Alternative Nitrite Reductase from Pseudomonas aeruginosa with Potential as an Antivirulence Target. Fenn S, Dubern JF, Cigana C, De Simone M, Lazenby J, Juhas M, Schwager S, Bianconi I, Döring G, Elmsley J, Eberl L, Williams P, Bragonzi A, Cámara M. mBio 12 e00207-21 (2021)
  35. Covalent modifications of the catalytic tyrosine in octahaem cytochrome c nitrite reductase and their effect on the enzyme activity. Trofimov AA, Polyakov KM, Tikhonova TV, Tikhonov AV, Safonova TN, Boyko KM, Dorovatovskii PV, Popov VO. Acta Crystallogr D Biol Crystallogr 68 144-153 (2012)
  36. Ironing out the distribution of [2Fe-2S] motifs in ferrochelatases. Weerth RS, Medlock AE, Dailey HA. J Biol Chem 297 101017 (2021)
  37. Kinetics and mechanism of oxidation of super-reduced cobalamin and cobinamide species by thiosulfate, sulfite and dithionite. Dereven'kov IA, Salnikov DS, Makarov SV, Boss GR, Koifman OI. Dalton Trans 42 15307-15316 (2013)
  38. Structure-function relationship of assimilatory nitrite reductases from the leaf and root of tobacco based on high-resolution structures. Nakano S, Takahashi M, Sakamoto A, Morikawa H, Katayanagi K. Protein Sci 21 383-395 (2012)
  39. The reductive reaction mechanism of tobacco nitrite reductase derived from a combination of crystal structures and ultraviolet-visible microspectroscopy. Nakano S, Takahashi M, Sakamoto A, Morikawa H, Katayanagi K. Proteins 80 2035-2045 (2012)
  40. The twists and turns of enzyme function. White RH. J Bacteriol 192 2023-2025 (2010)
  41. A Single DNA Point Mutation Leads to the Formation of a Cysteine-Tyrosine Crosslink in the Cysteine Dioxygenase from Bacillus subtilis. Schultz RL, Sabat G, Fox BG, Brunold TC. Biochemistry 62 1964-1975 (2023)
  42. X-ray crystal structure of a mutant assimilatory nitrite reductase that shows sulfite reductase-like activity. Nakano S, Takahashi M, Sakamoto A, Morikawa H, Katayanagi K. Chem Biodivers 9 1989-1999 (2012)
  43. Spectroscopic analysis of the mammalian enzyme cysteine dioxygenase. Miller JR, Brunold TC. Methods Enzymol 682 101-135 (2023)
  44. A novel mechanism for dissimilatory nitrate reduction to ammonium in Acididesulfobacillus acetoxydans. Egas RA, Kurth JM, Boeren S, Sousa DZ, Welte CU, Sánchez-Andrea I. mSystems 9 e0096723 (2024)
  45. Divergent downstream biosynthetic pathways are supported by L-cysteine synthases of Mycobacterium tuberculosis. Khan MZ, Hunt DM, Singha B, Kapoor Y, Singh NK, Prasad DVS, Dharmarajan S, Sowpati DT, de Carvalho LPS, Nandicoori VK. Elife 12 RP91970 (2024)
  46. Fusion/fission protein family identification in Archaea. Padalko A, Nair G, Sousa FL. mSystems 9 e0094823 (2024)
  47. In Vivo Toxicity Evaluation of Sugar Adulterated Heterotrigona itama Honey Using Zebrafish Model. Fakhlaei R, Selamat J, Razis AFA, Sukor R, Ahmad S, Amani Babadi A, Khatib A. Molecules 26 6222 (2021)
  48. Kinetic and Spectroscopic Investigation of the Y157F and C93G/Y157F Variants of Cysteine Dioxygenase: Dissecting the Roles of the Second-Sphere Residues C93 and Y157. Miller JR, Schnorrenberg EC, Aschenbrener C, Fox BG, Brunold TC. Biochemistry 63 1684-1696 (2024)
  49. Nutrient removal efficacy and microbial dynamics in constructed wetlands using Fe(III)-mineral substrates for low carbon-nitrogen ratio sewage treatment. Li Y, Zhang M, Li L, Gao W, Huang F, Lai G, Jia L, Liu R. Bioprocess Biosyst Eng 47 1707-1722 (2024)


Quick links