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Crystal structure of a novel Plasmodium falciparum 1-Cys peroxiredoxin.

Sarma GN, Nickel C, Rahlfs S, Fischer M, Becker K, Karplus PA
J Mol Biol 346 1021-34 (2005)
Cited: 59 times
EuropePMC logo PMID: 15701514

Abstract

Plasmodium falciparum, the causative agent of malaria, is sensitive to oxidative stress and therefore the family of antioxidant enzymes, peroxiredoxins (Prxs) represent a target for antimalarial drug design. We present here the 1.8 A resolution crystal structure of P.falciparum antioxidant protein, PfAOP, a Prx that in terms of sequence groups with mammalian PrxV. The structure is compared to all 11 known Prx structures to gain maximal insight into its properties. We describe the common Prx fold and show that the dimeric PfAOP can be mechanistically categorized as a 1-Cys Prx. In the active site the peroxidatic Cys is over-oxidized to cysteine sulfonic acid, making this the first Prx structure seen in that state. Now with structures of Prxs in Cys-sulfenic, -sulfinic and -sulfonic acid oxidation states known, the structural steps involved in peroxide binding and over-oxidation are suggested. We also describe that PfAOP has an alpha-aneurism (a one residue insertion), a feature that appears characteristic of the PrxV-like group. In terms of crystallographic methodology, we enhance the information content of the model by identifying bound water sites based on peak electron densities, and we use that information to infer that the oxidized active site has suboptimal interactions that may influence catalysis. The dimerization interface of PfAOP is representative of an interface that is widespread among Prxs, and has sequence-dependent variation in geometry. The interface differences and the structural features (like the alpha-aneurism) may be used as markers to better classify Prxs and study their evolution.

Reviews - 1xiy mentioned but not cited (3)

  1. Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Hall A, Nelson K, Poole LB, Karplus PA. Antioxid Redox Signal 15 795-815 (2011)
  2. Peroxiredoxins in parasites. Gretes MC, Poole LB, Karplus PA. Antioxid Redox Signal 17 608-633 (2012)
  3. Cysteine Oxidation in Proteins: Structure, Biophysics, and Simulation. Garrido Ruiz D, Sandoval-Perez A, Rangarajan AV, Gunderson EL, Jacobson MP. Biochemistry 61 2165-2176 (2022)

Articles - 1xiy mentioned but not cited (5)

  1. Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization. Hall A, Parsonage D, Poole LB, Karplus PA. J Mol Biol 402 194-209 (2010)
  2. Analysis of the peroxiredoxin family: using active-site structure and sequence information for global classification and residue analysis. Nelson KJ, Knutson ST, Soito L, Klomsiri C, Poole LB, Fetrow JS. Proteins 79 947-964 (2011)
  3. Inverse docking based screening and identification of protein targets for Cassiarin alkaloids against Plasmodium falciparum. Negi A, Bhandari N, Shyamlal BRK, Chaudhary S. Saudi Pharm J 26 546-567 (2018)
  4. Crystal structures from the Plasmodium peroxiredoxins: new insights into oligomerization and product binding. Qiu W, Dong A, Pizarro JC, Botchkarsev A, Min J, Wernimont AK, Hills T, Hui R, Artz JD. BMC Struct Biol 12 2 (2012)
  5. Characterization of the glutathione-dependent reduction of the peroxiredoxin 5 homolog PfAOP from Plasmodium falciparum. Schumann R, Lang L, Deponte M. Protein Sci 31 e4290 (2022)


Reviews citing this publication (11)

  1. Peroxiredoxin 5: structure, mechanism, and function of the mammalian atypical 2-Cys peroxiredoxin. Knoops B, Goemaere J, Van der Eecken V, Declercq JP. Antioxid Redox Signal 15 817-829 (2011)
  2. A primer on peroxiredoxin biochemistry. Karplus PA. Free Radic Biol Med 80 183-190 (2015)
  3. Thioredoxin networks in the malarial parasite Plasmodium falciparum. Nickel C, Rahlfs S, Deponte M, Koncarevic S, Becker K. Antioxid Redox Signal 8 1227-1239 (2006)
  4. The thiol-based redox networks of pathogens: unexploited targets in the search for new drugs. Jaeger T, Flohé L. Biofactors 27 109-120 (2006)
  5. Peroxiredoxins in malaria parasites: parasitologic aspects. Kawazu S, Komaki-Yasuda K, Oku H, Kano S. Parasitol Int 57 1-7 (2008)
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  7. Oxidative stress in malaria and artemisinin combination therapy: Pros and Cons. Kavishe RA, Koenderink JB, Alifrangis M. FEBS J 284 2579-2591 (2017)
  8. Overview of peroxiredoxins in oxidant defense and redox regulation. Poole LB, Hall A, Nelson KJ. Curr Protoc Toxicol Chapter 7 Unit7.9 (2011)
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  11. The Architecture of Thiol Antioxidant Systems among Invertebrate Parasites. Guevara-Flores A, Martínez-González JJ, Rendón JL, Del Arenal IP. Molecules 22 E259 (2017)

Articles citing this publication (40)

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  2. Compartmentation of redox metabolism in malaria parasites. Kehr S, Sturm N, Rahlfs S, Przyborski JM, Becker K. PLoS Pathog 6 e1001242 (2010)
  3. 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)
  4. Novel roles of peroxiredoxins in inflammation, cancer and innate immunity. Ishii T, Warabi E, Yanagawa T. J Clin Biochem Nutr 50 91-105 (2012)
  5. The malarial parasite Plasmodium falciparum imports the human protein peroxiredoxin 2 for peroxide detoxification. Koncarevic S, Rohrbach P, Deponte M, Krohne G, Prieto JH, Yates J, Rahlfs S, Becker K. Proc Natl Acad Sci U S A 106 13323-13328 (2009)
  6. Bovine mitochondrial peroxiredoxin III forms a two-ring catenane. Cao Z, Roszak AW, Gourlay LJ, Lindsay JG, Isaacs NW. Structure 13 1661-1664 (2005)
  7. Crystallographic and mutational studies of Mycobacterium tuberculosis recA mini-inteins suggest a pivotal role for a highly conserved aspartate residue. Van Roey P, Pereira B, Li Z, Hiraga K, Belfort M, Derbyshire V. J Mol Biol 367 162-173 (2007)
  8. Structural and biochemical characterization of a mitochondrial peroxiredoxin from Plasmodium falciparum. Boucher IW, McMillan PJ, Gabrielsen M, Akerman SE, Brannigan JA, Schnick C, Brzozowski AM, Wilkinson AJ, Müller S. Mol Microbiol 61 948-959 (2006)
  9. Conformational and oligomeric effects on the cysteine pK(a) of tryparedoxin peroxidase. Yuan Y, Knaggs M, Poole L, Fetrow J, Salsbury F. J Biomol Struct Dyn 28 51-70 (2010)
  10. The sensitive balance between the fully folded and locally unfolded conformations of a model peroxiredoxin. Perkins A, Nelson KJ, Williams JR, Parsonage D, Poole LB, Karplus PA. Biochemistry 52 8708-8721 (2013)
  11. A genome-wide chromatin-associated nuclear peroxiredoxin from the malaria parasite Plasmodium falciparum. Richard D, Bartfai R, Volz J, Ralph SA, Muller S, Stunnenberg HG, Cowman AF. J Biol Chem 286 11746-11755 (2011)
  12. Functional and structural characterization of a thiol peroxidase from Mycobacterium tuberculosis. Rho BS, Hung LW, Holton JM, Vigil D, Kim SI, Park MS, Terwilliger TC, Pédelacq JD. J Mol Biol 361 850-863 (2006)
  13. Structural changes common to catalysis in the Tpx peroxiredoxin subfamily. Hall A, Sankaran B, Poole LB, Karplus PA. J Mol Biol 393 867-881 (2009)
  14. Crystal structure of an archaeal peroxiredoxin from the aerobic hyperthermophilic crenarchaeon Aeropyrum pernix K1. Mizohata E, Sakai H, Fusatomi E, Terada T, Murayama K, Shirouzu M, Yokoyama S. J Mol Biol 354 317-329 (2005)
  15. Identification of dynamic structural motifs involved in peptidoglycan glycosyltransfer. Lovering AL, De Castro L, Strynadka NC. J Mol Biol 383 167-177 (2008)
  16. Oxidation of archaeal peroxiredoxin involves a hypervalent sulfur intermediate. Nakamura T, Yamamoto T, Abe M, Matsumura H, Hagihara Y, Goto T, Yamaguchi T, Inoue T. Proc Natl Acad Sci U S A 105 6238-6242 (2008)
  17. Involvement of a 1-Cys peroxiredoxin in bacterial virulence. Kaihami GH, Almeida JR, Santos SS, Netto LE, Almeida SR, Baldini RL. PLoS Pathog 10 e1004442 (2014)
  18. How pH modulates the dimer-decamer interconversion of 2-Cys peroxiredoxins from the Prx1 subfamily. Morais MA, Giuseppe PO, Souza TA, Alegria TG, Oliveira MA, Netto LE, Murakami MT. J Biol Chem 290 8582-8590 (2015)
  19. Plasmodium falciparum 2-Cys peroxiredoxin reacts with plasmoredoxin and peroxynitrite. Nickel C, Trujillo M, Rahlfs S, Deponte M, Radi R, Becker K. Biol Chem 386 1129-1136 (2005)
  20. An indel in transmembrane helix 2 helps to trace the molecular evolution of class A G-protein-coupled receptors. Devillé J, Rey J, Chabbert M. J Mol Evol 68 475-489 (2009)
  21. Insights into the alkyl peroxide reduction pathway of Xanthomonas campestris bacterioferritin comigratory protein from the trapped intermediate-ligand complex structures. Liao SJ, Yang CY, Chin KH, Wang AH, Chou SH. J Mol Biol 390 951-966 (2009)
  22. Mapping the active site helix-to-strand conversion of CxxxxC peroxiredoxin Q enzymes. Perkins A, Gretes MC, Nelson KJ, Poole LB, Karplus PA. Biochemistry 51 7638-7650 (2012)
  23. Characterization of the Vibrio vulnificus 1-Cys peroxiredoxin Prx3 and regulation of its expression by the Fe-S cluster regulator IscR in response to oxidative stress and iron starvation. Lim JG, Bang YJ, Choi SH. J Biol Chem 289 36263-36274 (2014)
  24. In vivo parameters influencing 2-Cys Prx oligomerization: The role of enzyme sulfinylation. Noichri Y, Palais G, Ruby V, D'Autreaux B, Delaunay-Moisan A, Nyström T, Molin M, Toledano MB. Redox Biol 6 326-333 (2015)
  25. Insights into the catalytic mechanism of the Bcp family: functional and structural analysis of Bcp1 from Sulfolobus solfataricus. D'Ambrosio K, Limauro D, Pedone E, Galdi I, Pedone C, Bartolucci S, De Simone G. Proteins 76 995-1006 (2009)
  26. Plasmodium falciparum antioxidant protein as a model enzyme for a special class of glutaredoxin/glutathione-dependent peroxiredoxins. Djuika CF, Fiedler S, Schnölzer M, Sanchez C, Lanzer M, Deponte M. Biochim Biophys Acta 1830 4073-4090 (2013)
  27. Exploring the catalytic mechanism of the first dimeric Bcp: Functional, structural and docking analyses of Bcp4 from Sulfolobus solfataricus. Limauro D, D'Ambrosio K, Langella E, De Simone G, Galdi I, Pedone C, Pedone E, Bartolucci S. Biochimie 92 1435-1444 (2010)
  28. Crystal structure of thioredoxin peroxidase from aerobic hyperthermophilic archaeon Aeropyrum pernix K1. Nakamura T, Yamamoto T, Inoue T, Matsumura H, Kobayashi A, Hagihara Y, Uegaki K, Ataka M, Kai Y, Ishikawa K. Proteins 62 822-826 (2006)
  29. Structural and electrostatic asymmetry at the active site in typical and atypical peroxiredoxin dimers. Salsbury FR, Yuan Y, Knaggs MH, Poole LB, Fetrow JS. J Phys Chem B 116 6832-6843 (2012)
  30. Structural changes upon peroxynitrite-mediated nitration of peroxiredoxin 2; nitrated Prx2 resembles its disulfide-oxidized form. Randall L, Manta B, Nelson KJ, Santos J, Poole LB, Denicola A. Arch Biochem Biophys 590 101-108 (2016)
  31. Crystal structure of the C107S/C112S mutant of yeast nuclear 2-Cys peroxiredoxin. Choi J, Choi S, Chon JK, Choi J, Cha MK, Kim IH, Shin W. Proteins 61 1146-1149 (2005)
  32. Observed octameric assembly of a Plasmodium yoelii peroxiredoxin can be explained by the replacement of native "ball-and-socket" interacting residues by an affinity tag. Gretes MC, Karplus PA. Protein Sci 22 1445-1452 (2013)
  33. Plasmodium falciparum antioxidant protein reveals a novel mechanism for balancing turnover and inactivation of peroxiredoxins. Staudacher V, Djuika CF, Koduka J, Schlossarek S, Kopp J, Büchler M, Lanzer M, Deponte M. Free Radic Biol Med 85 228-236 (2015)
  34. A Novel Thioredoxin-Dependent Peroxiredoxin (TPx-Q) Plays an Important Role in Defense Against Oxidative Stress and Is a Possible Drug Target in Babesia microti. Zhang H, Wang Z, Huang J, Cao J, Zhou Y, Zhou J. Front Vet Sci 7 76 (2020)
  35. Effect of thioredoxin peroxidase-1 gene disruption on the liver stages of the rodent malaria parasite Plasmodium berghei. Usui M, Masuda-Suganuma H, Fukumoto S, Angeles JM, Hakimi H, Inoue N, Kawazu S. Parasitol Int 64 290-294 (2015)
  36. Structure of TSA2 reveals novel features of the active-site loop of peroxiredoxins. Nielsen MH, Kidmose RT, Jenner LB. Acta Crystallogr D Struct Biol 72 158-167 (2016)
  37. The Human Pathogen Paracoccidioides brasiliensis Has a Unique 1-Cys Peroxiredoxin That Localizes Both Intracellularly and at the Cell Surface. Longo LVG, Breyer CA, Novaes GM, Gegembauer G, Leitão NP, Octaviano CE, Toyama MH, de Oliveira MA, Puccia R. Front Cell Infect Microbiol 10 394 (2020)
  38. Crystallization and preliminary X-ray analysis of a truncated mutant of yeast nuclear thiol peroxidase, a novel atypical 2-Cys peroxiredoxin. Choi J, Choi S, Choi J, Cha MK, Kim IH, Shin W. Acta Crystallogr Sect F Struct Biol Cryst Commun 61 659-662 (2005)
  39. In silico insights into the dimer structure and deiodinase activity of type III iodothyronine deiodinase from bioinformatics, molecular dynamics simulations, and QM/MM calculations. Marsan ES, Dreab A, Bayse CA. J Biomol Struct Dyn 41 4819-4829 (2023)
  40. In vivo observation of peroxiredoxins oligomerization dynamics. Zeida A, Manta B, Trujillo M. Proc Natl Acad Sci U S A 117 18918-18920 (2020)


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