Production, purification, and quality assessment of borrelial proteins CspZ from Borrelia burgdorferi and FhbA from Borrelia hermsii.
CspZ
Factor H
Factor-H like 1
FhbA
Protein quality control
Surface plasmon resonance
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
23 Jul 2024
23 Jul 2024
Historique:
received:
25
03
2024
accepted:
21
05
2024
revised:
14
05
2024
medline:
23
7
2024
pubmed:
23
7
2024
entrez:
23
7
2024
Statut:
epublish
Résumé
Borrelia, spirochetes transmitted by ticks, are the etiological agents of numerous multisystemic diseases, such as Lyme borreliosis (LB) and tick-borne relapsing fever (TBRF). This study focuses on two surface proteins from two Borrelia subspecies involved in these diseases: CspZ, expressed by Borrelia burgdorferi sensu stricto (also named BbCRASP-2 for complement regulator-acquiring surface protein 2), and the factor H binding A (FhbA), expressed by Borrelia hermsii. Numerous subspecies of Borrelia, including these latter, are able to evade the immune defenses of a variety of potential vertebrate hosts in a number of ways. In this context, previous data suggested that both surface proteins play a role in the immune evasion of both Borrelia subspecies by interacting with key regulators of the alternative pathway of the human complement system, factor H (FH) and FH-like protein 1 (FHL-1). The recombinant proteins, CspZ and FhbA, were expressed in Escherichia coli and purified by one-step metal-affinity chromatography, with yields of 15 and 20 mg or pure protein for 1 L of cultured bacteria, respectively. The purity was evaluated by SDS-PAGE and HPLC and is close to about 95%. The mass of CspZ and FhbA was checked by mass spectrometry (MS). Proper folding of CspZ and FhbA was confirmed by circular dichroism (CD), and their biological activity, namely their interaction with purified FH from human serum (recombinant FH
Identifiants
pubmed: 39042328
doi: 10.1007/s00253-024-13195-2
pii: 10.1007/s00253-024-13195-2
doi:
Substances chimiques
Bacterial Proteins
0
Recombinant Proteins
0
Complement Factor H
80295-65-4
Complement C3b Inactivator Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
425Subventions
Organisme : Ministère de l'Enseignement Supérieur et de la Recherche
ID : Ministère de l'Enseignement Supérieur et de la Recherche
Organisme : Sorbonne Université
ID : Investissements d'Avenir
Organisme : Lyme Support endowments
ID : Lyme Support endowments
Informations de copyright
© 2024. The Author(s).
Références
Adinolfi M, Dobson NC, Bradwell AR (1981) Synthesis of two components of human complement, β1 h and C3bINA, during fetal life. Acta Paediatr 70:705–710. https://doi.org/10.1111/j.1651-2227.1981.tb05772.x
doi: 10.1111/j.1651-2227.1981.tb05772.x
Anderson C, Brissette CA (2021) The brilliance of Borrelia: mechanisms of host immune evasion by Lyme disease-causing Spirochetes. Pathogens 10:281. https://doi.org/10.3390/pathogens10030281
doi: 10.3390/pathogens10030281
pubmed: 33801255
pmcid: 8001052
Barbosa AS, Isaac L (2020) Strategies used by Leptospira spirochetes to evade the host complement system. FEBS Lett 594:2633–2644. https://doi.org/10.1002/1873-3468.13768
doi: 10.1002/1873-3468.13768
pubmed: 32153015
Ben-Bassat A, Bauer K, Chang SY, Myambo K, Boosman A, Chang S (1987) Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J Bacteriol 169:751–757. https://doi.org/10.1128/jb.169.2.751-757.1987
doi: 10.1128/jb.169.2.751-757.1987
pubmed: 3027045
pmcid: 211843
Berrow N, de Marco A, Lebendiker M, Garcia-Alai M, Knauer SH, Lopez-Mendez B, Matagne A, Parret A, Remans K, Uebel S, Raynal B (2021) Quality control of purified proteins to improve data quality and reproducibility: results from a large-scale survey. Eur Biophys J 50:453–460. https://doi.org/10.1007/s00249-021-01528-2
doi: 10.1007/s00249-021-01528-2
pubmed: 33881595
Brangulis K, Petrovskis I, Kazaks A, Bogans J, Otikovs M, Jaudzems K, Ranka R, 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. https://doi.org/10.1111/febs.12808
doi: 10.1111/febs.12808
pubmed: 24702793
Brooimans RA, van der Ark AA, Buurman WA, van Es LA, Daha MR (1990) Differential regulation of complement factor H and C3 production in human umbilical vein endothelial cells by IFN-gamma and IL-1. J Immunol 144:3835–3840
doi: 10.4049/jimmunol.144.10.3835
pubmed: 2139673
Bykowski T, Woodman ME, Cooley AE, Brissette CA, Brade V, Wallich R, Kraiczy P, Stevenson B (2007) Coordinated expression of Borrelia burgdorferi complement regulator-acquiring surface proteins during the Lyme disease Spirochete’s mammal-tick infection cycle. Infect Immun 75:4227–4236. https://doi.org/10.1128/IAI.00604-07
doi: 10.1128/IAI.00604-07
pubmed: 17562769
pmcid: 1951152
Clark SJ, Schmidt CQ, White AM, Hakobyan S, Morgan BP, Bishop PN (2014) Identification of factor H–like protein 1 as the predominant complement regulator in Bruch’s membrane: implications for age-related macular degeneration. J Immunol 193:4962–4970. https://doi.org/10.4049/jimmunol.1401613
doi: 10.4049/jimmunol.1401613
pubmed: 25305316
de Marco A, Berrow N, Lebendiker M, Garcia-Alai M, Knauer SH, Lopez-Mendez B, Matagne A, Parret A, Remans K, Uebel S, Raynal B (2021) Quality control of protein reagents for the improvement of research data reproducibility. Nat Commun 12:2795. https://doi.org/10.1038/s41467-021-23167-z
doi: 10.1038/s41467-021-23167-z
pubmed: 33990604
pmcid: 8121922
Esparza-Gordillo J, Soria JM, Buil A, Almasy L, Blangero J, Fontcuberta J, Rodríguez de Córdoba S (2004) Genetic and environmental factors influencing the human factor H plasma levels. Immunogenet 56:77–82. https://doi.org/10.1007/s00251-004-0660-7
doi: 10.1007/s00251-004-0660-7
Faccini-Martínez ÁA, Silva-Ramos CR, Santodomingo AM, Ramírez-Hernández A, Costa FB, Labruna MB, Muñoz-Leal S (2022) Historical overview and update on relapsing fever group Borrelia in Latin America. Parasit Vectors 15:196. https://doi.org/10.1186/s13071-022-05289-5
doi: 10.1186/s13071-022-05289-5
pubmed: 35676728
pmcid: 9175325
Friese MA, Hellwage J, Jokiranta TS, Meri S, Müller-Quernheim HJ, Peter HH, Eibel H, Zipfel PF (2000) Different regulation of factor H and FHL-1/reconectin by inflammatory mediators and expression of the two proteins in rheumatoid arthritis (RA). Clin Exp Immunol 121:406–415. https://doi.org/10.1046/j.1365-2249.2000.01285.x
doi: 10.1046/j.1365-2249.2000.01285.x
pubmed: 10931160
pmcid: 1905714
Guérin M, Shawky M, Zedan A, Octave S, Avalle B, Maffucci I, Padiolleau-Lefèvre S (2023) Lyme borreliosis diagnosis: state of the art of improvements and innovations. BMC Microbiol 23:1–20. https://doi.org/10.1186/s12866-023-02935-5
doi: 10.1186/s12866-023-02935-5
Hartmann K, Corvey C, Skerka C, Kirschfink M, Karas M, Brade V, Miller JC, Stevenson B, Wallich R, Zipfel PF, Kraiczy P (2006) Functional characterization of BbCRASP-2, a distinct outer membrane protein of Borrelia burgdorferi that binds host complement regulators factor H and FHL-1. Mol Microbiol 61:1220–1236. https://doi.org/10.1111/j.1365-2958.2006.05318.x
doi: 10.1111/j.1365-2958.2006.05318.x
pubmed: 16925556
Hovis KM, McDowell JV, Griffin L, Marconi RT (2004) Identification and characterization of a linear-plasmid-encoded factor H-binding protein (FhbA) of the Relapsing Fever Spirochete Borrelia hermsii. J Bacteriol 186:2612–2618. https://doi.org/10.1128/JB.186.9.2612-2618.2004
doi: 10.1128/JB.186.9.2612-2618.2004
pubmed: 15090501
pmcid: 387808
Hovis KM, Jones JP, Sadlon T, Raval G, Gordon DL, Marconi RT (2006) Molecular analyses of the interaction of Borrelia hermsii FhbA with the complement regulatory proteins factor H and factor H-like protein 1. Infect Immun 74:2007–2014. https://doi.org/10.1128/IAI.74.4.2007-2014.2006
doi: 10.1128/IAI.74.4.2007-2014.2006
pubmed: 16552029
pmcid: 1418896
Johnson WC (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35:307–312
doi: 10.1002/(SICI)1097-0134(19990515)35:3<307::AID-PROT4>3.0.CO;2-3
pubmed: 10328265
Kogan K, Haapasalo K, Kotila T, Moore R, Lappalainen P, Goldman A, Meri T (2022) Mechanism of Borrelia immune evasion by FhbA-related proteins. PLoS Pathog 18:e1010338. https://doi.org/10.1371/journal.ppat.1010338
doi: 10.1371/journal.ppat.1010338
pubmed: 35303742
pmcid: 8967061
Kraiczy P, Hellwage J, Skerka C, Becker H, Kirschfink M, Simon MM, Brade V, Zipfel PF, Wallich R (2004) Complement resistance of Borrelia burgdorferi correlates with the expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to erp proteins. J Biol Chem 279:2421–2429. https://doi.org/10.1074/jbc.M308343200
doi: 10.1074/jbc.M308343200
pubmed: 14607842
Kraiczy P, Schreiber J, Skerka C, Haupt K, Brade V, Wallich R, Zipfel PF (2008a) Assessment of the regions within complement regulator-acquiring surface protein (CRASP)-2 of Borrelia burgdorferi required for interaction with host immune regulators FHL-1 and factor H. Int J Med Microbiol 298:268–271. https://doi.org/10.1016/j.ijmm.2007.12.008
doi: 10.1016/j.ijmm.2007.12.008
Kraiczy P, Seling A, Brissette CA, Rossmann E, Hunfeld K-P, Bykowski T, Burns LH, Troese MJ, Cooley AE, Miller JC, Brade V, Wallich R, Casjens S, Stevenson B (2008b) Borrelia burgdorferi complement regulator-acquiring surface protein 2 (CspZ) as a serological marker of human Lyme disease. Clin Vaccine Immunol 15:484–491. https://doi.org/10.1128/CVI.00415-07
doi: 10.1128/CVI.00415-07
pubmed: 18160620
Lin Y-P, Diuk-Wasser MA, Stevenson B, Kraiczy P (2020) Complement evasion contributes to Lyme borreliae–host associations. Trends Parasitol 36:634–645. https://doi.org/10.1016/j.pt.2020.04.011
doi: 10.1016/j.pt.2020.04.011
pubmed: 32456964
pmcid: 7292789
Marcinkiewicz AL, Dupuis IIAP, Zamba-Campero M, Nowak N, Kraiczy P, Ram S, Kramer LD, Lin Y-P (2019) Blood treatment of Lyme borreliae demonstrates the mechanism of CspZ-mediated complement evasion to promote systemic infection in vertebrate hosts. Cell Microbiol 21:e12998. https://doi.org/10.1111/cmi.12998
doi: 10.1111/cmi.12998
pubmed: 30571845
pmcid: 6336514
Marcinkiewicz AL, Lieknina I, Yang X, Lederman PL, Hart TM, Yates J, Chen W-H, Bottazzi ME, Mantis NJ, Kraiczy P, Pal U, Tars K, Lin Y-P (2020) The factor H-binding site of CspZ as a protective target against multistrain, tick-transmitted Lyme disease. Infect Immun 88:e00956–e00919. https://doi.org/10.1128/IAI.00956-19
doi: 10.1128/IAI.00956-19
pubmed: 32122944
pmcid: 7171238
Marcinkiewicz AL, Brangulis K, Dupuis AP, Hart TM, Zamba-Campero M, Nowak TA, Stout JL, Akopjana I, Kazaks A, Bogans J, Ciota AT, Kraiczy P, Kolokotronis S-O, Lin Y-P (2023) Structural evolution of an immune evasion determinant shapes pathogen host tropism. Proc Natl Acad Sci U S A 120:e2301549120. https://doi.org/10.1073/pnas.2301549120
doi: 10.1073/pnas.2301549120
pubmed: 37364114
pmcid: 10319004
Marty MT, Baldwin AJ, Marklund EG, Hochberg GKA, Benesch JLP, Robinson CV (2015) Bayesian deconvolution of mass and ion mobility spectra: from binary interactions to polydisperse ensembles. Anal Chem 87:4370–4376. https://doi.org/10.1021/acs.analchem.5b00140
doi: 10.1021/acs.analchem.5b00140
pubmed: 25799115
pmcid: 4594776
Meri T, Amdahl H, Lehtinen MJ, Hyvärinen S, McDowell JV, Bhattacharjee A, Meri S, Marconi R, Goldman A, Jokiranta TS (2013) Microbes bind complement inhibitor factor H via a common site. PLoS Pathog 9:e1003308. https://doi.org/10.1371/journal.ppat.1003308
doi: 10.1371/journal.ppat.1003308
pubmed: 23637600
pmcid: 3630169
Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT (2015a) Complement system part I – molecular mechanisms of activation and regulation. Front Immunol 6:262. https://doi.org/10.3389/fimmu.2015.00262
doi: 10.3389/fimmu.2015.00262
pubmed: 26082779
pmcid: 4451739
Merle NS, Noe R, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina LT (2015b) Complement system part II: role in immunity. Front Immunol 6:257. https://doi.org/10.3389/fimmu.2015.00257
doi: 10.3389/fimmu.2015.00257
pubmed: 26074922
pmcid: 4443744
Parente R, Clark SJ, Inforzato A, Day AJ (2017) Complement factor H in host defense and immune evasion. Cell Mol Life Sci 74:1605–1624. https://doi.org/10.1007/s00018-016-2418-4
doi: 10.1007/s00018-016-2418-4
pubmed: 27942748
Provencher SW, Glöckner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochem 20:33–37. https://doi.org/10.1021/bi00504a006
doi: 10.1021/bi00504a006
Rogers EA, Marconi RT (2007) Delineation of species-specific binding properties of the CspZ protein (BBH06) of Lyme disease spirochetes: evidence for new contributions to the pathogenesis of Borrelia spp. Infect Immun 75:5272–5281. https://doi.org/10.1128/IAI.00850-07
doi: 10.1128/IAI.00850-07
pubmed: 17846117
pmcid: 2168308
Schwaeble W, Zwirner J, Schulz TF, Linke RP, Dierich MP, Weiss EH (1987) Human complement factor H: expression of an additional truncated gene product of 43 kDa in human liver. Eur J Immunol 17:1485–1489. https://doi.org/10.1002/eji.1830171015
doi: 10.1002/eji.1830171015
pubmed: 2445583
Sreerama N, Woody RW (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209:32–44. https://doi.org/10.1006/abio.1993.1079
doi: 10.1006/abio.1993.1079
pubmed: 8465960
Sreerama N, Woody RW (2000) Estimation of protein secondary structure from Circular dichroism Spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252–260. https://doi.org/10.1006/abio.2000.4880
doi: 10.1006/abio.2000.4880
pubmed: 11112271
Sreerama N, Venyaminov SY, Woody RW (1999) Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci 8:370–380. https://doi.org/10.1110/ps.8.2.370
doi: 10.1110/ps.8.2.370
pubmed: 10048330
pmcid: 2144265
Trevisan G, Cinco M, Trevisini S, di Meo N, Chersi K, Ruscio M, Forgione P, Bonin S (2021a) Borreliae part 1: Borrelia Lyme group and Echidna-Reptile group. Biology 10:1036. https://doi.org/10.3390/biology10101036
doi: 10.3390/biology10101036
pubmed: 34681134
pmcid: 8533607
Trevisan G, Cinco M, Trevisini S, di Meo N, Ruscio M, Forgione P, Bonin S (2021b) Borreliae part 2: Borrelia relapsing fever group and unclassified Borrelia. Biology 10:1117. https://doi.org/10.3390/biology10111117
doi: 10.3390/biology10111117
pubmed: 34827110
pmcid: 8615063
Trouw LA, Daha MR (2011) Role of complement in innate immunity and host defense. Immunol Lett 138:35–37. https://doi.org/10.1016/j.imlet.2011.02.014
doi: 10.1016/j.imlet.2011.02.014
pubmed: 21333684
Valand N, Brunt E, Gazioglu O, Yesilkaya H, Mitchell D, Horley N, Arroo R, Kishore U, Wallis R, Venkatraman Girija U (2022) Inactivation of the complement lectin pathway by Candida tropicalis secreted aspartyl protease-1. Immunobiology 227:152263. https://doi.org/10.1016/j.imbio.2022.152263
doi: 10.1016/j.imbio.2022.152263
pubmed: 36063565
van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal Biochem 191:110–118. https://doi.org/10.1016/0003-2697(90)90396-q
doi: 10.1016/0003-2697(90)90396-q
pubmed: 2077933
Venyaminov SY, Yang JT (1996) Determination of protein secondary structure. In: Fasman GD (ed) Circular dichroism and the conformational analysis of biomolecules. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-2508-7_3
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552. https://doi.org/10.1385/1-59259-584-7:531
doi: 10.1385/1-59259-584-7:531
pubmed: 10027275
Wingfield PT (2017) N-Terminal Methionine Processing. Curr Protoc Protein Sci 88
Zipfel PF, Skerka C (1999) FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function. Immunol Today 20:135–140. https://doi.org/10.1016/S0167-5699(98)01432-7
doi: 10.1016/S0167-5699(98)01432-7
pubmed: 10203705