Structural analysis of Borrelia burgdorferi periplasmic lipoprotein BB0365 involved in Lyme disease infection.


Journal

FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157

Informations de publication

Date de publication:
01 2020
Historique:
received: 28 05 2019
revised: 15 07 2019
accepted: 28 08 2019
pubmed: 6 9 2019
medline: 24 7 2020
entrez: 6 9 2019
Statut: ppublish

Résumé

The periplasmic lipoprotein BB0365 of the Lyme disease agent Borrelia burgdorferi is expressed throughout mammalian infection and is essential for all phases of Lyme disease infection; its function, however, remains unknown. In the current study, our structural analysis of BB0365 revealed the same structural fold as that found in the NqrC and RnfG subunits of the NADH:quinone and ferredoxin:NAD

Identifiants

pubmed: 31486526
doi: 10.1002/1873-3468.13594
doi:

Substances chimiques

BB0365 protein, Borrelia burgdorferi 0
Bacterial Proteins 0
Lipoproteins 0
Sodium-Potassium-Exchanging ATPase EC 7.2.2.13
Zinc J41CSQ7QDS

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

317-326

Informations de copyright

© 2019 Federation of European Biochemical Societies.

Références

Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E and Davis JP (1982) Lyme disease-a tick-borne spirochetosis? Science 216, 1317-1319.
Rudenko N, Golovchenko M, Grubhoffer L and Oliver JH Jr (2011) Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick Borne Dis 2, 123-128.
Pritt BS, Respicio-Kingry LB, Sloan LM, Schriefer ME, Replogle AJ, Bjork J, Liu G, Kingry LC, Mead PS, Neitzel DF et al. (2016) Borrelia mayonii sp. nov., a member of the Borrelia burgdorferi sensu lato complex, detected in patients and ticks in the upper midwestern United States. Int J Syst Evol Microbiol 66, 4878-4880.
Haake DA (2000) Spirochaetal lipoproteins and pathogenesis. Microbiology 146 (Pt 7), 1491-1504.
Casjens S, Palmer N, van VR, Huang WM, Stevenson B, Rosa P, Lathigra R, Sutton G, Peterson J, Dodson RJ et al. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35, 490-516.
Gilmore RD Jr, Howison RR, Dietrich G, Patton TG, Clifton DR and Carroll JA (2010) The bba64 gene of Borrelia burgdorferi, the Lyme disease agent, is critical for mammalian infection via tick bite transmission. Proc Natl Acad Sci USA 107, 7515-7520.
Kraiczy P (2016) Hide and seek: how Lyme disease spirochetes overcome complement attack. Front Immunol 7, 385.
Kumar M, Kaur S, Kariu T, Yang X, Bossis I, Anderson JF and Pal U (2011) Borrelia burgdorferi BBA52 is a potential target for transmission blocking Lyme disease vaccine. Vaccine 29, 9012-9019.
Bestor A, Rego RO, Tilly K and Rosa PA (2012) Competitive advantage of Borrelia burgdorferi with outer surface protein BBA03 during tick-mediated infection of the mammalian host. Infect Immun 80, 3501-3511.
Zhang L, Zhang Y, Adusumilli S, Liu L, Narasimhan S, Dai J, Zhao YO and Fikrig E (2011) Molecular interactions that enable movement of the Lyme disease agent from the tick gut into the hemolymph. PLoS Pathog 7, e1002079.
Revel AT, Blevins JS, Almazan C, Neil L, Kocan KM, de la Fuente J, Hagman KE and Norgard MV (2005) bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc Natl Acad Sci USA 102, 6972-6977.
Yang X, Qin J, Promnares K, Kariu T, Anderson JF and Pal U (2013) Novel microbial virulence factor triggers murine lyme arthritis. J Infect Dis 207, 907-918.
Zhang X, Yang X, Kumar M and Pal U (2009) BB0323 function is essential for Borrelia burgdorferi virulence and persistence through tick-rodent transmission cycle. J Infect Dis 200, 1318-1330.
Wallich R, Simon MM, Hofmann H, Moter SE, Schaible UE and Kramer MD (1993) Molecular and immunological characterization of a novel polymorphic lipoprotein of Borrelia burgdorferi. Infect Immun 61, 4158-4166.
Lam TT, Nguyen TP, Fikrig E and Flavell RA (1994) A chromosomal Borrelia burgdorferi gene encodes a 22-kilodalton lipoprotein, P22, that is serologically recognized in Lyme disease. J Clin Microbiol 32, 876-883.
Yang X, Hegde S, Shroder DY, Smith AA, Promnares K, Neelakanta G, Anderson JF, Fikrig E and Pal U (2013) The lipoprotein La7 contributes to Borrelia burgdorferi persistence in ticks and their transmission to naive hosts. Microbes Infect 15, 729-737.
von Lackum K, Ollison KM, Bykowski T, Nowalk AJ, Hughes JL, Carroll JA, Zuckert WR and Stevenson B (2007) Regulated synthesis of the Borrelia burgdorferi inner-membrane lipoprotein IpLA7 (P22, P22-A) during the Lyme disease spirochaete's mammal-tick infectious cycle. Microbiology 153, 1361-1371.
Pal U, Dai J, Li X, Neelakanta G, Luo P, Kumar M, Wang P, Yang X, Anderson JF and Fikrig E (2008) A differential role for BB0365 in the persistence of Borrelia burgdorferi in mice and ticks. J Infect Dis 197, 148-155.
Brangulis K, Jaudzems K, Petrovskis I, Akopjana I, Kazaks A and Tars K (2015) Structural and functional analysis of BB0689 from Borrelia burgdorferi, a member of the bacterial CAP superfamily. J Struct Biol 192, 320-330.
Brangulis K, Petrovskis I, Kazaks A, Bogans J, Otikovs M, Jaudzems K, Ranka R and Tars K (2014) Structural characterization of CspZ, a complement regulator factor H and FHL-1 binding protein from Borrelia burgdorferi. FEBS J 281, 2613-2622.
Mueller U, Darowski N, Fuchs MR, Förster R, Hellmig M, Paithankar KS, Pühringer S, Steffien M, Zocher G and Weiss MS (2012) Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J Synchrotron Radiat 19, 442-449.
Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67, 235-242.
Evans PR (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr D Biol Crystallogr 67, 282-292.
Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66, 125-132.
Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64, 112-122.
Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62, 1002-1011.
Emsley P and Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
Murshudov GN, Vagin AA and Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255.
Brangulis K, Petrovskis I, Kazaks A, Tars K and Ranka R (2014) Crystal structure of the infectious phenotype-associated outer surface protein BBA66 from the Lyme disease agent Borrelia burgdorferi. Ticks Tick Borne Dis 5, 63-68.
McCall KA, Huang C and Fierke CA (2000) Function and mechanism of zinc metalloenzymes. J Nutr 130, 1437S-1446S.
Tamames B, Sousa SF, Tamames J, Fernandes PA and Ramos MJ (2007) Analysis of zinc-ligand bond lengths in metalloproteins: trends and patterns. Proteins 69, 466-475.
Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215, 403-410.
Holm L and Laakso LM (2016) Dali server update. Nucleic Acids Res 44, W351-W355.
Steuber J, Vohl G, Casutt MS, Vorburger T, Diederichs K and Fritz G (2014) Structure of the V. cholerae Na+-pumping NADH:quinone oxidoreductase. Nature 516, 62-67.
Biegel E, Schmidt S, Gonzalez JM and Muller V (2011) Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol Life Sci 68, 613-634.
Robert X and Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42, W320-W324.
Hase CC, Fedorova ND, Galperin MY and Dibrov PA (2001) Sodium ion cycle in bacterial pathogens: evidence from cross-genome comparisons. Microbiol Mol Biol Rev 65, 353-370, table of contents.
Barquera B, Hellwig P, Zhou W, Morgan JE, Häse CC, Gosink KK, Nilges M, Bruesehoff PJ, Roth A, Lancaster CR et al. (2002) Purification and characterization of the recombinant Na(+)-translocating NADH:quinone oxidoreductase from Vibrio cholerae. Biochemistry 41, 3781-3789.
Zhou W, Bertsova YV, Feng B, Tsatsos P, Verkhovskaya ML, Gennis RB, Bogachev AV and Barquera B (1999) Sequencing and preliminary characterization of the Na+-translocating NADH:ubiquinone oxidoreductase from Vibrio harveyi. Biochemistry 38, 16246-16252.
Steuber J, Halang P, Vorburger T, Steffen W, Vohl G and Fritz G (2014) Central role of the Na(+)-translocating NADH:quinone oxidoreductase (Na(+)-NQR) in sodium bioenergetics of Vibrio cholerae. Biol Chem 395, 1389-1399.
Skulachev VP (1991) Chemiosmotic systems in bioenergetics: H(+)-cycles and Na(+)-cycles. Biosci Rep 11, 387-441; discussion 441-4.
Liu J, Lin T, Botkin DJ, McCrum E, Winkler H and Norris SJ (2009) Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J Bacteriol 191, 5026-5036.
Radolf JD, Deka RK, Anand A, Smajs D, Norgard MV and Yang XF (2016) Treponema pallidum, the syphilis spirochete: making a living as a stealth pathogen. Nat Rev Microbiol 14, 744-759.
Deka RK, Brautigam CA, Liu WZ, Tomchick DR and Norgard MV (2015) Evidence for posttranslational protein flavinylation in the syphilis spirochete Treponema pallidum: structural and biochemical insights from the catalytic core of a periplasmic flavin-trafficking protein. MBio 6, e00519-15.
Fraser CM, Norris SJ, Weinstock GM, White O, Sutton GG, Dodson R, Gwinn M, Hickey EK, Clayton R, Ketchum KA et al. (1998) Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281, 375-388.
Deka RK, Brautigam CA, Liu WZ, Tomchick DR and Norgard MV (2013) The TP0796 lipoprotein of Treponema pallidum is a bimetal-dependent FAD pyrophosphatase with a potential role in flavin homeostasis. J Biol Chem 288, 11106-11121.
Welte C and Deppenmeier U (2014) Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim Biophys Acta 1837, 1130-1147.
Mayer F and Muller V (2014) Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 38, 449-472.
Hayashi M, Nakayama Y and Unemoto T (2001) Recent progress in the Na(+)-translocating NADH-quinone reductase from the marine Vibrio alginolyticus. Biochim Biophys Acta 1505, 37-44.
Vallee BL and Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29, 5647-5659.
Posey JE and Gherardini FC (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288, 1651-1653.
Pal U, Li X, Wang T, Montgomery RR, Ramamoorthi N, Desilva AM, Bao F, Yang X, Pypaert M, Pradhan D et al. (2004) TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119, 457-468.
Poland GA (2011) Vaccines against Lyme disease: what happened and what lessons can we learn? Clin Infect Dis 52 (Suppl 3), s253-s258.

Auteurs

Kalvis Brangulis (K)

Latvian Biomedical Research and Study Centre, Riga, Latvia.

Inara Akopjana (I)

Latvian Biomedical Research and Study Centre, Riga, Latvia.

Ivars Petrovskis (I)

Latvian Biomedical Research and Study Centre, Riga, Latvia.

Andris Kazaks (A)

Latvian Biomedical Research and Study Centre, Riga, Latvia.

Atis Jekabsons (A)

Latvian Institute of Organic Synthesis, Riga, Latvia.

Kristaps Jaudzems (K)

Latvian Institute of Organic Synthesis, Riga, Latvia.
Faculty of Chemistry, University of Latvia, Riga, Latvia.

Arturs Viksna (A)

Faculty of Chemistry, University of Latvia, Riga, Latvia.

Maris Bertins (M)

Faculty of Chemistry, University of Latvia, Riga, Latvia.

Kaspars Tars (K)

Latvian Biomedical Research and Study Centre, Riga, Latvia.
Faculty of Biology, University of Latvia, Riga, Latvia.

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