Evidence of Mycobacterium avium subsp. paratuberculosis binding to albumin: technical and biological implications.

Albumin binding ability BSA Mycobacteria Paratuberculosis

Journal

Veterinary research communications
ISSN: 1573-7446
Titre abrégé: Vet Res Commun
Pays: Switzerland
ID NLM: 8100520

Informations de publication

Date de publication:
01 Sep 2023
Historique:
received: 12 05 2023
accepted: 01 08 2023
medline: 1 9 2023
pubmed: 1 9 2023
entrez: 1 9 2023
Statut: aheadofprint

Résumé

Albumin binding ability is a well-characterized feature of many bacteria. To the best of our knowledge, there are no previous reports about this ability among mycobacteria, even when bovine serum albumin (BSA) is a common component of supplements used for the enrichment of synthetic media for mycobacterial growth in vitro and also of buffers used in laboratory techniques. In this work we explored the albumin binding ability of Mycobacterium avium subsp. paratuberculosis (MAP), a pathogenic bacterium causing a known and relevant ruminant disease worldwide, by immunizing rabbits with MAP (grown in media containing or not BSA) or BSA and conducting ELISA and immunoblot experiments with the obtained sera. As a result, we found that MAP can bind BSA when cultured in a conventional BSA-containing medium and when incubated for a short time in the presence of the protein. We also evaluated the host specificity of MAP interaction with albumin and found a preference for the protein of bovine origin when compared with its horse and rabbit homologs. Considerations about its technical and biological implications are discussed.

Identifiants

pubmed: 37656341
doi: 10.1007/s11259-023-10192-0
pii: 10.1007/s11259-023-10192-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT 2017-1145
Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT-2018-03595
Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT-2018-03595
Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT 2017-1145
Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT-2018-03595
Organisme : Agencia Nacional de Promoción Científica y Técnica
ID : BID PICT-2018-03595
Organisme : Secretaría de Ciencia y Técnica Universidad de Buenos Aires
ID : UBACyT 20020170100327BA
Organisme : Secretaría de Ciencia y Técnica Universidad de Buenos Aires
ID : UBACyT 20020170100327BA
Organisme : Secretaría de Ciencia y Técnica Universidad de Buenos Aires
ID : UBACyT 20020170100327BA
Organisme : Secretaría de Ciencia y Técnica Universidad de Buenos Aires
ID : UBACyT 20020170100327BA
Organisme : Secretaria de Ciencia y Tecnica, Universidad de Buenos Aires
ID : 20020190200158BA
Organisme : Secretaria de Ciencia y Tecnica, Universidad de Buenos Aires
ID : 20020190200158BA

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Bannantine JP, Radosevich TJ, Stabel JR, Sreevatsan S, Kapur V, Paustian ML (2007) Development and characterization of monoclonal antibodies and aptamers against major antigens of Mycobacterium avium subsp. paratuberculosis. Clin Vaccine Immunol 14(5):518–526. https://doi.org/10.1128/CVI.00022-07
doi: 10.1128/CVI.00022-07 pubmed: 17344350 pmcid: 1865628
Bannantine JP, Wadhwa A, Stabel JR, Eda S (2019) Characterization of ethanol extracted cell Wall Components of Mycobacterium avium subsp. Paratuberculosis Vet Sci 6(4):88. https://doi.org/10.3390/vetsci6040088
doi: 10.3390/vetsci6040088 pubmed: 31683552
Berry A, Wu CW, Venturino AJ, Talaat AM (2018) Biomarkers for early stages of Johne’s Disease infection and immunization in goats. Front Microbiol 9:2284. https://doi.org/10.3389/fmicb.2018.02284
doi: 10.3389/fmicb.2018.02284 pubmed: 30323794 pmcid: 6172484
Björck L, Kastern W, Lindahl G, Widebäck K (1987) Streptococcal protein G, expressed by streptococci or by Escherichia coli, has separate binding sites for human albumin and IgG. Mol Immunol 24(10):1113–1122. https://doi.org/10.1016/0161-5890(87)90080-0
doi: 10.1016/0161-5890(87)90080-0 pubmed: 3316991
Dane H, Koidis A, Stewart LD, Grant IR (2022) Optimization of the composition of a solid culture medium for Mycobacterium avium subsp. paratuberculosis using factorial design and response surface methodology. J Appl Microbiol 132(6):4252–4265. https://doi.org/10.1111/jam.15517
doi: 10.1111/jam.15517 pubmed: 35261128 pmcid: 9320839
De Château M, Holst E, Björck L (1996) Protein PAB, an albumin-binding bacterial surface protein promoting growth and virulence. J Biol Chem 271(28):16725–16733. https://doi.org/10.1074/jbc.271.43.26609
doi: 10.1074/jbc.271.43.26609
Duarte JJ (2021) Utilidad y caracterización de anticuerpos monoclonales contra Mycobacterium avium subsp. paratuberculosis. Tesis inédita de Maestría en Biotecnología, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Argentina,
Egesten A, Frick IM, Mörgelin M, Olin AI, Björck L (2011) Binding of albumin promotes bacterial survival at the epithelial surface. J Biol Chem 286(4):2469–2476. https://doi.org/10.1074/jbc.M110.148171
doi: 10.1074/jbc.M110.148171 pubmed: 21098039
Escalante J, Nishimura B, Tuttobene MR, Subils T, Pimentel C, Georgeos N, Sieira R, Bonomo RA, Tolmasky ME, Ramirez MS (2022) Human serum albumin (HSA) regulates the expression of histone-like nucleoid structure protein (H-NS) in Acinetobacter baumannii. Sci Rep 12(1):14644. https://doi.org/10.1038/s41598-022-19012-y
doi: 10.1038/s41598-022-19012-y pubmed: 36030268 pmcid: 9420150
Hall-Stoodley L, Watts G, Crowther JE, Balagopal A, Torrelles JB, Robison-Cox J, Bargatze RF, Harmsen AG, Crouch EC, Schlesinger LS (2006) Mycobacterium tuberculosis binding to human surfactant proteins A and D, fibronectin, and small airway epithelial cells under shear conditions. Infect Immun 74(6):3587–3596. https://doi.org/10.1128/IAI.01644-05
doi: 10.1128/IAI.01644-05 pubmed: 16714591 pmcid: 1479241
Harlow E, Lane D (1988) Storing and purifying antibodies. Antibodies, a Laboratory Manual, 1st edn. Cold Spring Harbor Laboratory /CSHL Press), New York, USA, pp 298–299
Lejon S, Frick IM, Björck L, Wikström M, Svensson S (2004) Crystal structure and biological implications of a bacterial albumin binding module in complex with human serum albumin. J Biol Chem 279(41):42924–42928. https://doi.org/10.1074/jbc.M406957200
doi: 10.1074/jbc.M406957200 pubmed: 15269208
Lieske B, Jantz A, Finke B (2005) An improved analytical approach for the determination of bovine serum albumin in milk. Le Lait 85(3). https://doi.org/10.1051/lait:2005018
Lynn M, Wilson AR, Solotorovsky M (1979) Role of bovine serum albumin in the nutrition of Mycobacterium tuberculosis. Appl Environ Microbiol 38(5):806–810. https://doi.org/10.1128/aem.38.5.806-810.1979
doi: 10.1128/aem.38.5.806-810.1979 pubmed: 120697 pmcid: 243590
Majorek KA, Porebski PJ, Dayal A, Zimmerman MD, Jablonska K, Stewart AJ, Chruszcz M, Minor W (2012) Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Mol Immunol 46(8–9):1595–1604. https://doi.org/10.1016/j.molimm.2012.05.011
doi: 10.1016/j.molimm.2012.05.011
Mitra A, Ko YH, Cingolani G, Niederweis M (2019) Heme and hemoglobin utilization by Mycobacterium tuberculosis. Nat Commun 10(1):4260. https://doi.org/10.1038/s41467-019-12109-5
doi: 10.1038/s41467-019-12109-5 pubmed: 31534126 pmcid: 6751184
Pekmezovic M, Kaune AK, Austermeier S, Hitzler SUJ, Mogavero S, Hovhannisyan H, Gabaldón T, Gresnigt MS, Hube B (2021) Human albumin enhances the pathogenic potential of Candida glabrata on vaginal epithelial cells. PLoS Pathog 17(10):e1010037. https://doi.org/10.1371/journal.ppat.1010037
doi: 10.1371/journal.ppat.1010037 pubmed: 34710198 pmcid: 8577789
Peng Q, Zhang S, Yang Q, Zhang T, Wei XQ, Jiang L, Zhang CL, Chen QM, Zhang ZR, Lin YF (2013) Preformed albumin corona, a protective coating for nanoparticles based drug delivery system. Biomaterials 34(33):8521–8530. https://doi.org/10.1016/j.biomaterials.2013.07.102
doi: 10.1016/j.biomaterials.2013.07.102 pubmed: 23932500
Quinn B, Rodman N, Jara E, Fernandez JS, Martinez J, Traglia GM, Montaña S, Cantera V, Place K, Bonomo RA, Iriarte A, Ramírez MS (2018) Human serum albumin alters specific genes that can play a role in survival and persistence in Acinetobacter baumannii. Sci Rep 8(1):1–16. https://doi.org/10.1038/s41598-018-33072-z
doi: 10.1038/s41598-018-33072-z
Rakhra K, Abraham W, Wang C, Moynihan KD, Li N, Donahue N, Baldeon AD, Irvine DJ (2021) Exploiting albumin as a mucosal vaccine chaperone for robust generation of lung-resident memory T cells. Sci Immunol 6(57):eabd8003. https://doi.org/10.1126/sciimmunol.abd8003
doi: 10.1126/sciimmunol.abd8003 pubmed: 33741657 pmcid: 8279396
Sani M, Houben EN, Geurtsen J, Pierson J, de Punder K, van Zon M, Wever B, Piersma SR, Jiménez CR, Daffé M, Appelmelk BJ, Bitter W, van der Wel N, Peters PJ (2010) Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog 6(3):e1000794. https://doi.org/10.1371/journal.ppat.1000794
doi: 10.1371/journal.ppat.1000794 pubmed: 20221442 pmcid: 2832766
Sankar S, Yamaguchim M, Kawabata S, Ponnuraj K (2020) Streptococcus pneumoniae Surface Adhesin PfbA exhibits host specificity by binding to human serum albumin but not bovine, rabbit and porcine serum albumins. Protein J 39(1):1–9. https://doi.org/10.1007/s10930-019-09875-y
doi: 10.1007/s10930-019-09875-y pubmed: 31741170
Stempler A, Jolly A, Colavecchia SB, Soba M, Fontanals A, Mundo SL (2009) Development and evaluation of a monoclonal antibody against Mycobacterium avium subsp. paratuberculosis. Vet Immunol Immunopathol 128(1):335–336
doi: 10.1016/j.vetimm.2008.10.266
Thiele L, Diederichs JE, Reszka R, Merkle HP, Walter E (2003) Competitive adsorption of serum proteins at microparticles affects phagocytosis by dendritic cells. Biomaterials 24(8):1409–1418. https://doi.org/10.1016/s0142-9612(02)00525-2
doi: 10.1016/s0142-9612(02)00525-2 pubmed: 12527282

Auteurs

Ana Jolly (A)

Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Cátedra de Inmunología, (0054) 11-5287-2155, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina. ajolly@fvet.uba.ar.

María Laura Barnech (ML)

Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Cátedra de Inmunología, (0054) 11-5287-2155, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.

Juan José Duarte (JJ)

Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Cátedra de Inmunología, (0054) 11-5287-2155, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.

Jorge Suhevic (J)

Escuela de Educación Técnico Profesional de nivel medio en Producción Agropecuaria y Agroalimentaria, Universidad de Buenos Aires, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.

Ana María Jar (AM)

Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Cátedra de Inmunología, (0054) 11-5287-2155, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.

Silvia Leonor Mundo (SL)

Facultad de Ciencias Veterinarias, Universidad de Buenos Aires, Cátedra de Inmunología, (0054) 11-5287-2155, Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.
Universidad de Buenos Aires - CONICET, Instituto de Investigaciones en Producción Animal (INPA), Av. Chorroarín 280, Ciudad Autónoma de Buenos Aires C1427CWO, Buenos Aires, Argentina.

Classifications MeSH