Francisella and Antibodies

. 2021 Oct 12 ; 9 (10) : . [epub] 20211012

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34683457

Grantová podpora
VJ01030003 Ministry of Interior of the Czech Republic

Odkazy

PubMed 34683457
PubMed Central PMC8538966
DOI 10.3390/microorganisms9102136
PII: microorganisms9102136
Knihovny.cz E-zdroje

Immune responses to intracellular pathogens depend largely upon the activation of T helper type 1-dependent mechanisms. The contribution of B cells to establishing protective immunity has long been underestimated. Francisella tularensis, including a number of subspecies, provides a suitable model for the study of immune responses against intracellular bacterial pathogens. We previously demonstrated that Francisella infects B cells and activates B-cell subtypes to produce a number of cytokines and express the activation markers. Recently, we documented the early production of natural antibodies as a consequence of Francisella infection in mice. Here, we summarize current knowledge on the innate and acquired humoral immune responses initiated by Francisella infection and their relationships with the immune defense systems.

Zobrazit více v PubMed

Elkins K.L., Cowley S.C., Bosio C.M. Innate and adaptive immunity to Francisella. Ann. N. Y. Acad. Sci. 2007;1105:284–324. doi: 10.1196/annals.1409.014. PubMed DOI

Meunier E., Wallet P., Dreier R.F., Costanzo S., Anton L., Rühl S., Dussurgey S., Dick M., Kistner A., Rigard M., et al. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat. Immunol. 2015;16:476–484. doi: 10.1038/ni.3119. PubMed DOI PMC

Wallet P., Lagrange B., Henry T. Francisella Inflammasomes: Integrated Responses to a Cytosolic Stealth Bacterium. Curr. Top. Microbiol. Immunol. 2016;397:229–256. PubMed

Krocova Z., Macela A., Kubelkova K. Innate Immune Recognition: Implications for the Interaction of Francisella tularensis with the Host Immune System. Front. Cell Infect. Microbiol. 2017;7:446. doi: 10.3389/fcimb.2017.00446. PubMed DOI PMC

Lagrange B., Benaoudia S., Wallet P., Magnotti F., Provost A., Michal F., Martin A., Di Lorenzo F., Py B., Molinaro A., et al. Human caspase-4 detects tetra-acylated LPS and cytosolic Francisella and functions differently from murine caspase-11. Nat. Commun. 2018;9:242. doi: 10.1038/s41467-017-02682-y. PubMed DOI PMC

Kubelkova K., Macela A. Innate Immune Recognition: An Issue More Complex than Expected [Internet] Front. Cell Infect. Microbiol. 2019;9:241. doi: 10.3389/fcimb.2019.00241. PubMed DOI PMC

Kinkead L.C., Allen L.-A.H. Multifaceted effects of Francisella tularensis on human neutrophil function and lifespan. Immunol. Rev. 2016;273:266–281. doi: 10.1111/imr.12445. PubMed DOI PMC

Kinkead L.C., Fayram D.C., Allen L.H. Francisella novicida inhibits spontaneous apoptosis and extends human neutrophil lifespan. J. Leukoc. Biol. 2017;102:815–828. doi: 10.1189/jlb.4MA0117-014R. PubMed DOI PMC

Pulavendran S., Prasanthi M., Ramachandran A., Grant R., Snider T.A., Chow V.T.K., Malayer J.R., Teluguakula N. Production of Neutrophil Extracellular Traps Contributes to the Pathogenesis of Francisella tularemia. Front. Immunol. 2020;11:679. doi: 10.3389/fimmu.2020.00679. PubMed DOI PMC

Fink A., Hassan M.A., Okan N.A., Sheffer M., Camejo A., Saeij J.P., Kasper D.L. Early Interactions of Murine Macrophages with Francisella tularensis Map to Mouse Chromosome 19. mBio. 2016;7:e02243. doi: 10.1128/mBio.02243-15. PubMed DOI PMC

Steiner D.J., Furuya Y., Jordan M.B., Metzger D.W. Protective Role for Macrophages in Respiratory Francisella tularensis Infection. Infect. Immun. 2017;85:e00064-17. doi: 10.1128/IAI.00064-17. PubMed DOI PMC

Steiner D.J., Furuya Y., Metzger D.W. Detrimental Influence of Alveolar Macrophages on Protective Humoral Immunity during Francisella tularensis SchuS4 Pulmonary Infection. Infect. Immun. 2018;86:e00787-17. doi: 10.1128/IAI.00787-17. PubMed DOI PMC

Bradford M.K., Elkins K.I. Immune lymphocytes halt replication of Francisella tularensis LVS within the cytoplasm of infected macrophages. Sci. Rep. 2020;10:12023. doi: 10.1038/s41598-020-68798-2. PubMed DOI PMC

Fabrik I., Härtlova A., Rehulka P., Stulik J. Serving the new masters—Dendritic cells as hosts for stealth intracellular bacteria. Cell. Microbiol. 2013;15:1473–1483. doi: 10.1111/cmi.12160. PubMed DOI

Fabrik I., Link M., Putzova D., Plzakova L., Lubovska Z., Philimonenko V., Pavkova I., Rehulka P., Krocova Z., Hozak P., et al. The early dendritic cell signaling induced by virulent Francisella tularensis strain occurs in phases and involves the activation of extracellular signal-regulated kinases (ERKs) and p38 in the later stage. Mol. Cell. Proteom. MCP. 2018;17:81–94. doi: 10.1074/mcp.RA117.000160. PubMed DOI PMC

Nelson N.L.J., Zajd C.M., Lennartz M.R., Gosselin E.J. Fcγ receptors and toll-like receptor 9 synergize to drive immune complex-induced dendritic cell maturation. Cell. Immunol. 2019;345:103962. doi: 10.1016/j.cellimm.2019.103962. PubMed DOI PMC

De Pascalis R., Rossi A.P., Mittereder L., Takeda K., Akue A., Kurtz S.L., Elkins K.L. Production of IFN-γ by splenic dendritic cells during innate immune responses against Francisella tularensis LVS depends on MyD88, but not TLR2, TLR4, or TLR9. PLoS ONE. 2020;15:e0237034. doi: 10.1371/journal.pone.0237034. PubMed DOI PMC

Krocova Z., Härtlova A., Souckova D., Zivna L., Kroca M., Rudolf E., Macela A., Stulik J. Interaction of B cells with intracellular pathogen Francisella tularensis. Microb. Pathog. 2008;45:79–85. doi: 10.1016/j.micpath.2008.01.010. PubMed DOI

Plzakova L., Kubelkova K., Krocova Z., Zarybnicka L., Sinkorova Z., Macela A. B cell subsets are activated and produce cytokines during early phases of Francisella tularensis LVS infection. Microb. Pathog. 2014;75:49–58. doi: 10.1016/j.micpath.2014.08.009. PubMed DOI

Plzakova L., Krocova Z., Kubelkova K., Macela A. Entry of Francisella tularensis into Murine B Cells: The Role of B Cell Receptors and Complement Receptors. PLoS ONE. 2015;10:e0132571. doi: 10.1371/journal.pone.0132571. PubMed DOI PMC

García-Gil A., Lopez-Bailon L.U., Ortiz-Navarrete V. Beyond the antibody: B cells as a target for bacterial infection. J. Leukoc. Biol. 2019;105:905–913. doi: 10.1002/JLB.MR0618-225R. PubMed DOI

Kelava. I., Marecic V., Fucak P., Ivek E., Kolaric D., Ozanic M., Mihelcic M., Santic M. Optimisation of External Factors for the Growth of Francisella novicida within Dictyostelium discoideum. BioMed Res. Int. 2020;2020:6826983. doi: 10.1155/2020/6826983. PubMed DOI PMC

Zellner B., Huntley J.F. Ticks and Tularemia: Do We Know What We Don’t Know? Front. Cell. Infect. Microbiol. 2019;9:146. doi: 10.3389/fcimb.2019.00146. PubMed DOI PMC

Abdellahoum Z., Maurin M., Bitam I. Tularemia as a Mosquito-Borne Disease. Microorganisms. 2020;9:26. doi: 10.3390/microorganisms9010026. PubMed DOI PMC

Lewisch E., Menanteau-Ledouble S., Tichy A., El-Matbouli M. Susceptibility of common carp and sunfish to a strain of Francisella noatunensis subsp. orientalis in a challenge experiment. Dis. Aquat. Organ. 2016;121:161–166. doi: 10.3354/dao03044. PubMed DOI

Mörner T. The ecology of tularaemia. Rev. Sci. Tech. Int. Off. Epizoot. 1992;11:1123–1130. doi: 10.20506/rst.11.4.657. PubMed DOI

Hopla C.E. The ecology of tularemia. Adv. Vet. Sci. Comp. Med. 1974;18:25–53. PubMed

Mörner T., Mattsson R. Experimental infection of five species of raptors and of hooded crows with Francisella tularensis biovar palaearctica. J. Wildl. Dis. 1988;24:15–21. doi: 10.7589/0090-3558-24.1.15. PubMed DOI

McKeever S., Schubert J.H., Moody M.D., Gorman G.W., Chapman J.F. Natural occurrence of tularemia in marsupials, carnivores, lagomorphs, and large rodents in southwestern Georgia and northwestern Florida. J. Infect. Dis. 1958;103:120–126. doi: 10.1093/infdis/103.2.120. PubMed DOI

Mätz-Rensing K., Floto A., Schrod A., Becker T., Finke E.J., Seibold E., Splettstoesser W.D., Kaup F.J. Epizootic of tularemia in an outdoor housed group of cynomolgus monkeys (Macaca fascicularis) Vet. Pathol. 2007;44:327–334. PubMed

Yeni D.K., Büyük F., Ashraf A., Shah M.S.U.D. Tularemia: A re-emerging tick-borne infectious disease. Folia Microbiol. 2021;66:1–14. doi: 10.1007/s12223-020-00827-z. PubMed DOI PMC

Cowley S.C., Elkins K.L. Immunity to francisella. Front. Microbiol. 2011;2:26. doi: 10.3389/fmicb.2011.00026. PubMed DOI PMC

Bártová E., Kučerová H.L., Žákovská A., Budíková M., Nejezchlebová H. Coxiella burnetii and Francisella tularensis in wild small mammals from the Czech Republic. Ticks Tick Borne Dis. 2020;11:101350. doi: 10.1016/j.ttbdis.2019.101350. PubMed DOI

Hestvik G., Uhlhorn H., Koene M., Åkerström S., Malmsten A., Dahl F., Åhlén P.-A., Dalin A.-M., Gavier-Widén D. Francisella tularensis in Swedish predators and scavengers. Epidemiol. Infect. 2019;147:e293. doi: 10.1017/S0950268819001808. PubMed DOI PMC

Al Dahouk S., Nöckler K., Tomaso H., Splettstoesser W.D., Jungersen G., Riber U., Petry T., Hoffmann D., Scholz H.C., Hensel A., et al. Seroprevalence of brucellosis, tularemia, and yersiniosis in wild boars (Sus scrofa) from north-eastern Germany. J. Vet. Med. B Infect. Dis. Vet. Public Health. 2005;52:444–455. doi: 10.1111/j.1439-0450.2005.00898.x. PubMed DOI

Jacob D., Barduhn A., Tappe D., Rauch J., Heuner K., Hierhammer D., Vom Berge K., Riehm J.M., Hanczaruk M., Böhm S., et al. Outbreak of Tularemia in a Group of Hunters in Germany in 2018-Kinetics of Antibody and Cytokine Responses. Microorganisms. 2020;8:1645. doi: 10.3390/microorganisms8111645. PubMed DOI PMC

Otto P., Chaignat V., Klimpel D., Diller R., Melzer F., Müller W., Tomaso H. Serological investigation of wild boars (Sus scrofa) and red foxes (Vulpes vulpes) as indicator animals for circulation of Francisella tularensis in Germany. Vector Borne Zoonotic Dis. 2014;14:46–51. doi: 10.1089/vbz.2013.1321. PubMed DOI PMC

Gürcan S., Otkun M.T., Otkun M., Arikan O.K., Ozer B. An outbreak of tularemia in Western Black Sea region of Turkey. Yonsei Med. J. 2004;45:17–22. doi: 10.3349/ymj.2004.45.1.17. PubMed DOI

Gürcan S., Eskiocak M., Varol G., Uzun C., Tatman-Otkun M., Sakru N., Karadenizli A., Karagöl C., Otkun M. Tularemia re-emerging in European part of Turkey after 60 years. Jpn. J. Infect. Dis. 2006;59:391–393. PubMed

Hemati M., Khalili M., Rohani M., Sadeghi B., Esmaeili S., Ghasemi A., Mahmoudi A., Gyuranecz M., Mostafavi E. A serological and molecular study on Francisella tularensis in rodents from Hamadan province, Western Iran. Comp. Immunol. Microbiol. Infect. Dis. 2020;68:101379. doi: 10.1016/j.cimid.2019.101379. PubMed DOI

Hotta A., Tanabayashi K., Yamamoto Y., Fujita O., Uda A., Mizoguchi T., Yamada A. Seroprevalence of tularemia in wild bears and hares in Japan. Zoonoses Public Health. 2012;59:89–95. doi: 10.1111/j.1863-2378.2011.01422.x. PubMed DOI

Sharma N., Hotta A., Yamamoto Y., Uda A., Fujita O., Mizoguchi T., Shindo J., Park C.-H., Kudo N., Hatai H., et al. Serosurveillance for Francisella tularensis among wild animals in Japan using a newly developed competitive enzyme-linked immunosorbent assay. Vector Borne Zoonotic Dis. 2014;14:234–239. doi: 10.1089/vbz.2013.1349. PubMed DOI PMC

Gromov A.I., Timofeeva N.S., Trukhmanov M.M., Veide A.A., Golovina T.I., Dobroliubova R.P., Lazarev O.P., Merzliakov A.P., Rafailov M.G., Timofeeva A.A., et al. [On the establishment of a natural focus of tularemia on Sakhalin] Zh. Mikrobiol. Epidemiol. Immunobiol. 1969;46:125–127. PubMed

Egorov I.E., Mironchuk Y.V., Maramovich A.S., Chesnokova M.V., Botvinkin A.D., Makeev S.M., Ochirov I.D., Vershinin E.A., Tugutov L.D., Cherniavskiĭ V.F., et al. [Zoonotic infections in the central and southern ulusy of the Republic of Sakha] Zh. Mikrobiol. Epidemiol. Immunobiol. 1997;2:38–43. PubMed

Podobedova Y.S., Demidova T.N., Kormilitsyna M.I., Meshcheriakova I.S. [Natural foci of tularemia on the Wrangel island] Med. Parazitol. 2006;4:32–34. PubMed

Dobrokhotov B.P., Mnatsakanian A.G., Meshcheriakova I.S., Rudnev M.M. [Exploration of natural foci of tularemia and plague in Armenia using the serological examination of bird droppings and excrements of predatory mammals] Zh. Mikrobiol. Epidemiol. Immunobiol. 1978;2:111–115. PubMed

Ditchfield J., Meads E.B., Julian R.J. Tularemia of muskrats in Eastern Ontario. Can. J. Public Health. 1960;51:474–478. PubMed

Hoff G.l., Yuill T.M., Iversen J.O., Hanson R.P. Selected microbial agents in snowshoe hares and other vertebrates of Alberta. J. Wildl. Dis. 1970;6:472–478. doi: 10.7589/0090-3558-6.4.472. PubMed DOI

Akerman M.B., Embil J.A. Antibodies to Francisella tularensis in the snowshoe hare (Lepus americanus struthopus) populations of Nova Scotia and Prince Edward Island and in the moose (Alces alces americana Clinton) population of Nova Scotia. Can. J. Microbiol. 1982;28:403–405. doi: 10.1139/m82-061. PubMed DOI

Wobeser G., Campbell G.D., Dallaire A., McBurney S. Tularemia, plague, yersiniosis, and Tyzzer’s disease in wild rodents and lagomorphs in Canada: A review. Can. Vet. J. Rev. Vét. Can. 2009;50:1251–1256. PubMed PMC

Gabriele-Rivet V., Ogden N., Massé A., Antonation K., Corbett C., Dibernardo A., Lindsay L.R., Leighton P.A., Arsenault J. Eco-epizootiologic study of Francisella tularensis, the agent of tularemia, in Québec wildlife. J. Wildl. Dis. 2016;52:217–229. doi: 10.7589/2015-04-096. PubMed DOI

Kwit N.A., Middaugh N.A., VinHatton E.S., Melman S.D., Onischuk L., Aragon A.S., Nelson C.A., Mead P.S., Ettestad P.J. Francisella tularensis infection in dogs: 88 cases (2014–2016) J. Am. Vet. Med. Assoc. 2020;256:220–225. doi: 10.2460/javma.256.2.220. PubMed DOI

Petersen J.M., Schriefer M.E., Carter L.G., Zhou Y., Sealy T., Bawiec D., Yockey B., Urich S., Zeidner N.S., Avashia S., et al. Laboratory analysis of tularemia in wild-trapped, commercially traded prairie dogs, Texas, 2002. Emerg. Infect. Dis. 2004;10:419–425. doi: 10.3201/eid1003.030504. PubMed DOI PMC

Hansen C.M., Vogler A.J., Keim P., Wagner D.M., Hueffer K. Tularemia in Alaska, 1938–2010. Acta Vet. Scand. 2011;53:61. doi: 10.1186/1751-0147-53-61. PubMed DOI PMC

Beest J.T., Cushing A., McClean M., Hsu W., Bildfell R. Disease Surveillance of California Ground Squirrels (Spermophilus beecheyi) in a Drive-through Zoo in Oregon, USA. J. Wildl. Dis. 2017;53:667–670. doi: 10.7589/2016-05-119. PubMed DOI

Berrada Z.L., Goethert H.K., Telford S.R. Raccoons and skunks as sentinels for enzootic tularemia. Emerg. Infect. Dis. 2006;12:1019–1021. PubMed PMC

Feldman K.A., Stiles-Enos D., Julian K., Matyas B.T., Telford S.R., III, Chu M.C., Petersen L.R., Hayes E.B. Tularemia on Martha’s Vineyard: Seroprevalence and occupational risk. Emerg. Infect. Dis. 2003;9:350–354. doi: 10.3201/eid0903.020462. PubMed DOI PMC

Siret V., Barataud D., Prat M., Vaillant V., Ansart S., Le Coustumier A., Vaissaire J., Raffi F., Garré M., Capek I. An outbreak of airborne tularaemia in France, August 2004. Eurosurveillance. 2006;11:3–4. doi: 10.2807/esm.11.02.00598-en. PubMed DOI

Leblebicioglu. H., Esen S., Turan D., Tanyeri Y., Karadenizli A., Ziyagil F., Goral G. Outbreak of tularemia: A case-control study and environmental investigation in Turkey. Int. J. Infect. Dis. 2008;12:265–269. doi: 10.1016/j.ijid.2007.06.013. PubMed DOI

Grunow R., Kalaveshi A., Kühn A., Mulliqi-Osmani G., Ramadani N. Surveillance of tularaemia in Kosovo, 2001 to 2010. Eurosurveillance. 2012;17:20217. doi: 10.2807/ese.17.28.20217-en. PubMed DOI

Raghavan R.K., Harrington J., Anderson G.A., Hutchinson J.M., Debey B.M. Environmental, climatic, and residential neighborhood determinants of feline tularemia. Vector Borne Zoonotic Dis. 2013;13:449–456. doi: 10.1089/vbz.2012.1234. PubMed DOI

Akhvlediani. N., Burjanadze I., Baliashvili D., Tushishvili T., Broladze M., Navdarashvili A., Dolbadze S., Chitadze N., Topuridze M., Imnadze P., et al. Tularemia transmission to humans: A multifaceted surveillance approach. Epidemiol. Infect. 2018;146:2139–2145. doi: 10.1017/S0950268818002492. PubMed DOI PMC

Maurin M. Francisella tularensis, Tularemia and Serological Diagnosis. Front. Cell. Infect. Microbiol. 2020;10:512090. doi: 10.3389/fcimb.2020.512090. PubMed DOI PMC

Viljanen M.K., Nurmi T., Salminen A. Enzyme-linked immunosorbent assay (ELISA) with bacterial sonicate antigen for IgM, IgA, and IgG antibodies to Francisella tularensis: Comparison with bacterial agglutination test and ELISA with lipopolysaccharide antigen. J. Infect. Dis. 1983;148:715–720. doi: 10.1093/infdis/148.4.715. PubMed DOI

Koskela P., Salminen A. Humoral immunity against Francisella tularensis after natural infection. J. Clin. Microbiol. 1985;22:973–979. doi: 10.1128/jcm.22.6.973-979.1985. PubMed DOI PMC

Rastawicki W., Rokosz-Chudziak N., Wolaniuk N. [Serum immunoglobulin IgG subclass distribution of antibody responses to Francisella tularensis in patients with tularemia] Med. Dosw. Mikrobiol. 2014;66:11–15. PubMed

Koskela P., Herva E. Cell-mediated and humoral immunity induced by a live Francisella tularensis vaccine. Infect. Immun. 1982;36:983–989. doi: 10.1128/iai.36.3.983-989.1982. PubMed DOI PMC

Ericsson M., Sandström G., Sjöstedt A., Tärnvik A. Persistence of cell-mediated immunity and decline of humoral immunity to the intracellular bacterium Francisella tularensis 25 years after natural infection. J. Infect. Dis. 1994;170:110–114. doi: 10.1093/infdis/170.1.110. PubMed DOI

Sandström G., Tärnvik A., Wolf-Watz H., Löfgren S. Antigen from Francisella tularensis: Nonidentity between determinants participating in cell-mediated and humoral reactions. Infect. Immun. 1984;45:101–106. doi: 10.1128/iai.45.1.101-106.1984. PubMed DOI PMC

Okan N.A., Kasper D.L. The atypical lipopolysaccharide of Francisella. Carbohydr. Res. 2013;378:79–83. doi: 10.1016/j.carres.2013.06.015. PubMed DOI PMC

Jones B.D., Faron M., Rasmussen J.A., Fletcher J.R. Uncovering the components of the Francisella tularensis virulence stealth strategy. Front. Cell. Infect. Microbiol. 2014;4:32. doi: 10.3389/fcimb.2014.00032. PubMed DOI PMC

Rahhal R.M., Vanden Bush T.J., McLendon M.K., Apicella M.A., Bishop G.A. Differential effects of Francisella tularensis lipopolysaccharide on B lymphocytes. J. Leukoc. Biol. 2007;82:813–820. doi: 10.1189/jlb.1206765. PubMed DOI

Fulton K.M., Zhao X., Petit M.D., Kilmury S.L., Wolfraim L.A., House R.V., Sjostedt A., Twine S.M. Immunoproteomic analysis of the human antibody response to natural tularemia infection with Type A or Type B strains or LVS vaccination. Int. J. Med. Microbiol. IJMM. 2011;301:591–601. doi: 10.1016/j.ijmm.2011.07.002. PubMed DOI PMC

Gaur R., Alam S.I., Kamboj D.V. Immunoproteomic Analysis of Antibody Response of Rabbit Host Against Heat-Killed Francisella tularensis Live Vaccine Strain. Curr. Microbiol. 2017;74:499–507. doi: 10.1007/s00284-017-1217-y. PubMed DOI

Saslaw S., Eigelsbach H.T., Wilson H.E., Prior J.A., Carhart S. Tularemia vaccine study. I. Intracutaneous challenge. Arch. Intern. Med. 1961;107:689–701. doi: 10.1001/archinte.1961.03620050055006. PubMed DOI

Saslaw S., Carhart S. Studies with tularemia vaccines in volunteers. III. Serologic aspects following intracutaneous or respiratory challenge in both vaccinated and nonvaccinated volunteers. Am. J. Med. Sci. 1961;241:689–699. doi: 10.1097/00000441-196106000-00001. PubMed DOI

Havlasová J., Hernychová L., Halada P., Pellantová V., Krejsek J., Stulík J., Macela A., Jungblut P.R., Larsson P., Forsman M. Mapping of immunoreactive antigens of Francisella tularensis live vaccine strain. Proteomics. 2002;2:857–867. doi: 10.1002/1615-9861(200207)2:7<857::AID-PROT857>3.0.CO;2-L. PubMed DOI

Twine S.M., Petit M.D., Shen H., Mykytczuk N.C., Kelly J.F., Conlan J.W. Immunoproteomic analysis of the murine antibody response to successful and failed immunization with live anti-Francisella vaccines. Biochem. Biophys. Res. Commun. 2006;346:999–1008. doi: 10.1016/j.bbrc.2006.06.008. PubMed DOI

Havlasová J., Hernychová L., Brychta M., Hubálek M., Lenco J., Larsson P., Lundqvist M., Forsman M., Kročová Z., Stulík J., et al. Proteomic analysis of anti-Francisella tularensis LVS antibody response in murine model of tularemia. Proteomics. 2005;5:2090–2103. doi: 10.1002/pmic.200401123. PubMed DOI

Pasetti M.F., Cuberos L., Horn T.L., Shearer J.D., Matthews S.J., House R.V., Sztein M.B. An improved Francisella tularensis live vaccine strain (LVS) is well tolerated and highly immunogenic when administered to rabbits in escalating doses using various immunization routes. Vaccine. 2008;26:1773–1785. doi: 10.1016/j.vaccine.2008.01.005. PubMed DOI PMC

Nutter J.E. Effect of vaccine, route, and schedule on antibody response of rabbits to Pasteurella tularensis. Appl. Microbiol. 1969;17:355–359. doi: 10.1128/am.17.3.355-359.1969. PubMed DOI PMC

Tulis J.J., Eigelsbach H.T., Kerpsack R.W. Host-parasite relationship in monkeys administered live tularemia vaccine. Am. J. Pathol. 1970;58:329–336. PubMed PMC

Stinson E., Smith L.P., Cole K.S., Barry E.M., Reed D.S. Respiratory and oral vaccination improves protection conferred by the live vaccine strain against pneumonic tularemia in the rabbit model. Pathog. Dis. 2016;74:ftw079. doi: 10.1093/femspd/ftw079. PubMed DOI PMC

Sunagar R., Kumar S., Namjoshi P., Rosa S.J., Hazlett K.R.O., Gosselin E.J. Evaluation of an outbred mouse model for Francisella tularensis vaccine development and testing. PLoS ONE. 2018;13:e0207587. doi: 10.1371/journal.pone.0207587. PubMed DOI PMC

Mara-Koosham G., Hutt J.A., Lyons C.R., Wu T.H. Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains. Infect. Immun. 2011;79:1770–1778. doi: 10.1128/IAI.00605-10. PubMed DOI PMC

Avrameas S. Natural autoantibodies: From “horror autotoxicus” to “gnothi seauton”. Immunol. Today. 1991;12:154–159. PubMed

Coutinho A., Kazatchkine M.D., Avrameas S. Natural autoantibodies. Curr. Opin. Immunol. 1995;7:812–818. doi: 10.1016/0952-7915(95)80053-0. PubMed DOI

Ménoret A., Chandawarkar R.Y., Srivastava P.K. Natural autoantibodies against heat-shock proteins hsp70 and gp96: Implications for immunotherapy using heat-shock proteins. Immunology. 2000;101:364–370. doi: 10.1046/j.1365-2567.2000.00127.x. PubMed DOI PMC

Dragon-Durey M.A., Blanc C., Marinozzi M.C., van Schaarenburg R.A., Trouw L.A. Autoantibodies against complement components and functional consequences. Mol. Immunol. 2013;56:213–221. doi: 10.1016/j.molimm.2013.05.009. PubMed DOI

Sauerborn M., van de Vosse E., Delawi D., van Dissel J.T., Brinks V., Schellekens H. Natural antibodies against bone morphogenic proteins and interferons in healthy donors and in patients with infections linked to type-1 cytokine responses. J. Interferon Cytokine Res. 2011;31:661–669. doi: 10.1089/jir.2010.0075. PubMed DOI

Huflejt M.E., Vuskovic M., Vasiliu D., Xu H., Obukhova P., Shilova N., Tuzikov A., Galanina O., Arun B., Lu K., et al. Anti-carbohydrate antibodies of normal sera: Findings, surprises and challenges. Mol. Immunol. 2009;46:3037–3049. doi: 10.1016/j.molimm.2009.06.010. PubMed DOI

Shilova N., Huflejt M.E., Vuskovic M., Obukhova P., Navakouski M., Khasbiullina N., Pazynina G., Galanina O., Bazhenov A., Bovin N. Natural Antibodies Against Sialoglycans. Top. Curr. Chem. 2015;366:169–181. PubMed

Prieto J.M.B., Felippe M.J.B. Development, phenotype, and function of non-conventional B cells. Comp. Immunol. Microbiol. Infect. Dis. 2017;54:38–44. doi: 10.1016/j.cimid.2017.08.002. PubMed DOI

Smith F.L., Baumgarth N. B-1 cell responses to infections. Curr. Opin. Immunol. 2019;57:23–31. doi: 10.1016/j.coi.2018.12.001. PubMed DOI PMC

Yang Y., Tung J.W., Ghosn E.E., Herzenberg L.A., Herzenberg L.A. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc. Natl. Acad. Sci. USA. 2007;104:4542–4546. doi: 10.1073/pnas.0700001104. PubMed DOI PMC

Yang Y., Ghosn E.E., Cole L.E., Obukhanych T.V., Sadate-Ngatchou P., Vogel S.N., Herzenberg L.A., Herzenberg L.A. Antigen-specific antibody responses in B-1a and their relationship to natural immunity. Proc. Natl. Acad. Sci. USA. 2012;109:5382–5387. doi: 10.1073/pnas.1121631109. PubMed DOI PMC

Yang Y., Ghosn E.E., Cole L.E., Obukhanych T.V., Sadate-Ngatchou P., Vogel S.N., Herzenberg L.A., Herzenberg L.A. Antigen-specific memory in B-1a and its relationship to natural immunity. Proc. Natl. Acad. Sci. USA. 2012;109:5388–5393. doi: 10.1073/pnas.1121627109. PubMed DOI PMC

Kubelkova K., Hudcovic T., Kozakova H., Pejchal J., Macela A. Early infection-induced natural antibody response. Sci. Rep. 2021;11:1541. doi: 10.1038/s41598-021-81083-0. PubMed DOI PMC

Madar M., Bencurova E., Mlynarcik P., Almeida A.M., Soares R., Bhide K., Pulzova L., Kovac A., Coelho A.V., Bhide M. Exploitation of complement regulatory proteins by Borrelia and Francisella. Mol. Biosyst. 2015;11:1684–1695. doi: 10.1039/C5MB00027K. PubMed DOI

Cowley S.C., Gray C.J., Nano F.E. Isolation and characterization of Francisella novicida mutants defective in lipopolysaccharide biosynthesis. FEMS Microbiol. Lett. 2000;182:63–67. doi: 10.1111/j.1574-6968.2000.tb08874.x. PubMed DOI

Li J., Ryder C., Mandal M., Ahmed F., Azadi P., Snyder D.S., Pechous R.D., Zahrt T., Inzana T.J. Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS. Pt 9Microbiology. 2007;153:3141–3153. doi: 10.1099/mic.0.2007/006460-0. PubMed DOI

Thomas R.M., Titball R.W., Oyston P.C.F., Griffin K., Waters E., Hitchen P.G., Michell S.L., Grice I.D., Wilson J.C., Prior J.L. The Immunologically Distinct O Antigens from Francisella tularensis Subspecies tularensis and Francisella novicida Are both Virulence Determinants and Protective Antigens. Infect. Immun. 2007;75:371–378. doi: 10.1128/IAI.01241-06. PubMed DOI PMC

Mdluli K.E., Anthony L.S., Baron G.S., McDonald M.K., Myltseva S.V., Nano F.E. Serum-sensitive mutation of Francisella novicida: Association with an ABC transporter gene. Pt 12Microbiology. 1994;140:3309–3318. doi: 10.1099/13500872-140-12-3309. PubMed DOI

Ben Nasr A., Klimpel G.R. Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J. Leukoc. Biol. 2008;84:77–85. doi: 10.1189/jlb.0807526. PubMed DOI

Parente R., Clark S.J., Inforzato A., Day A.J. Complement factor H in host defense and immune evasion. Cell. Mol. Life Sci. 2017;74:1605–1624. doi: 10.1007/s00018-016-2418-4. PubMed DOI PMC

Kreizinger Z., Bhide M., Bencurova E., Dolinska S., Gyuranecz M. Complement sensitivity and factor H binding of European Francisella tularensis ssp. holarctica strains in selected animal species. Acta Vet. Hung. 2015;63:275–284. doi: 10.1556/004.2015.026. PubMed DOI

Clay C.D., Soni S., Gunn J.S., Schlesinger L.S. Evasion of complement-mediated lysis and complement C3 deposition are regulated by Francisella tularensis lipopolysaccharide O antigen. J. Immunol. 2008;181:5568–5578. doi: 10.4049/jimmunol.181.8.5568. PubMed DOI PMC

Janeway C.A., Jr., Travers P., Walport M., Shlomchik M.J. Immunobiology: The Immune System in Health and Disease. 5th ed. Garland Science; New York, NY, USA: 2020. The complement system and innate immunity.

Kubagawa H., Oka S., Kubagawa Y., Torii I., Takayama E., Kang D.-W., Gartland G.L., Bertoli L.F., Mori H., Takatsu H., et al. Identity of the elusive IgM Fc receptor (FcμR) in humans. J. Exp. Med. 2009;206:2779–2793. doi: 10.1084/jem.20091107. PubMed DOI PMC

Honjo K., Kubagawa Y., Jones D.M., Dizon B., Zhu Z., Ohno H., Izui S., Kearney J.F., Kubagawa H. Altered Ig levels and antibody responses in mice deficient for the Fc receptor for IgM (FcμR) Proc. Natl. Acad. Sci. USA. 2012;109:15882–15887. doi: 10.1073/pnas.1206567109. PubMed DOI PMC

Lang K.S., Lang P.A., Meryk A., Pandyra A.A., Boucher L.-M., Pozdeev V.I., Tusche M.W., Göthert J.R., Haight J., Wakeham A., et al. Involvement of Toso in activation of monocytes, macrophages, and granulocytes. Proc. Natl. Acad. Sci. USA. 2013;110:2593–2598. doi: 10.1073/pnas.1222264110. PubMed DOI PMC

Liu J., Zhu H., Qian J., Xiong E., Zhang L., Wang Y.-Q., Chu Y., Kubagawa H., Tsubata T., Wang J.-Y. Fcµ Receptor Promotes the Survival and Activation of Marginal Zone B Cells and Protects Mice against Bacterial Sepsis. Front. Immunol. 2018;9:160. doi: 10.3389/fimmu.2018.00160. PubMed DOI PMC

Liu J., Wang Y., Xiong E., Hong R., Lu Q., Ohno H., Wang J.Y. Role of the IgM Fc Receptor in Immunity and Tolerance. Front. Immunol. 2019;10:529. doi: 10.3389/fimmu.2019.00529. PubMed DOI PMC

Schwartz J.T., Barker J.H., Long M.E., Kaufman J., McCracken J., Allen L.-A. Natural IgM mediates complement-dependent uptake of Francisella tularensis by human neutrophils via complement receptors 1 and 3 in nonimmune serum. J. Immunol. 2012;189:3064–3077. doi: 10.4049/jimmunol.1200816. PubMed DOI PMC

Geier H., Celli J. Phagocytic receptors dictate phagosomal escape and intracellular proliferation of Francisella tularensis. Infect Immun. 2011;79:2204–2214. doi: 10.1128/IAI.01382-10. PubMed DOI PMC

Kitamura D., Roes J., Kühn R., Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 1991;350:423–426. doi: 10.1038/350423a0. PubMed DOI

Elkins K.L., MacIntyre A.T., Rhinehart-Jones T.R. Nonspecific early protective immunity in Francisella and Listeria infections can be dependent on lymphocytes. Infect. Immun. 1998;66:3467–3469. doi: 10.1128/IAI.66.7.3467-3469.1998. PubMed DOI PMC

Crane D.D., Scott D.P., Bosio C.M. Generation of a convalescent model of virulent Francisella tularensis infection for assessment of host requirements for survival of tularemia. PLoS ONE. 2012;7:e33349. doi: 10.1371/journal.pone.0033349. PubMed DOI PMC

Ding Z., Bergman A., Rutemark C., Ouchida R., Ohno H., Wang J.-Y., Heyman B. Complement-Activating IgM Enhances the Humoral but Not the T Cell Immune Response in Mice. PLoS ONE. 2013;8:e81299. doi: 10.1371/journal.pone.0081299. PubMed DOI PMC

Sörman A., Zhang L., Ding Z., Heyman B. How antibodies use complement to regulate antibody responses. Mol. Immunol. 2014;61:79–88. doi: 10.1016/j.molimm.2014.06.010. PubMed DOI

Zivna L., Krocova Z., Härtlova A., Kubelkova K., Zakova J., Rudolf E., Hrstka R., Macela A., Stulík J. Activation of B cell apoptotic pathways in the course of Francisella tularensis infection. Microb. Pathog. 2010;49:226–236. doi: 10.1016/j.micpath.2010.06.003. PubMed DOI

Li Z., Woo C.J., Iglesias-Ussel M.D., Ronai D., Scharff M.D. The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 2004;18:1–11. doi: 10.1101/gad.1161904. PubMed DOI

Bournazos S., Wang T.T., Dahan R., Maamary J., Ravetch J.V. Signaling by Antibodies: Recent Progress. Annu. Rev. Immunol. 2017;35:285–311. doi: 10.1146/annurev-immunol-051116-052433. PubMed DOI PMC

Pincetic A., Bournazos S., DiLillo D.J., Maamary J., Wang T.T., Dahan R., Fiebiger B.M., Ravetch J.V. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat. Immunol. 2014;15:707–716. doi: 10.1038/ni.2939. PubMed DOI PMC

Wang T.T., Ravetch J.V. Functional diversification of IgGs through Fc glycosylation. J. Clin. Investig. 2019;129:3492–3498. doi: 10.1172/JCI130029. PubMed DOI PMC

Lu L.L., Suscovich T.J., Fortune S.M., Alter G. Beyond binding: Antibody effector functions in infectious diseases. Nat. Rev. Immunol. 2018;18:46–61. doi: 10.1038/nri.2017.106. PubMed DOI PMC

Cole L.E., Yang Y., Elkins K.L., Fernandez E.T., Qureshi N., Shlomchik M.J., Herzenberg L.A., Herzenberg L.A., Vogel S.N. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. USA. 2009;106:4343–4348. doi: 10.1073/pnas.0813411106. PubMed DOI PMC

Furuya Y., Kirimanjeswara G.S., Roberts S., Metzger D.W. Increased susceptibility of IgA-deficient mice to pulmonary Francisella tularensis live vaccine strain infection. Infect. Immun. 2013;81:3434–3441. doi: 10.1128/IAI.00408-13. PubMed DOI PMC

Conlan W.J., Shen H., Kuolee R., Zhao X., Chen W. Aerosol-, but not intradermal-immunization with the live vaccine strain of Francisella tularensis protects mice against subsequent aerosol challenge with a highly virulent type A strain of the pathogen by an alphabeta T cell-and interferon gamma- dependent mechanism. Vaccine. 2005;23:2477–2485. PubMed

Wu T.H., Hutt J.A., Garrison K.A., Berliba L.S., Zhou Y., Lyons C.R. Intranasal vaccination induces protective immunity against intranasal infection with virulent Francisella tularensis biovar A. Infect. Immun. 2005;73:2644–2654. doi: 10.1128/IAI.73.5.2644-2654.2005. PubMed DOI PMC

Furuya Y., Kirimanjeswara G.S., Roberts S., Racine R., Wilson-Welder J., Sanfilippo A.M., Salmon S.I., Metzger D.W. Defective anti-polysaccharide IgG vaccine responses in IgA deficient mice. Vaccine. 2017;35:4997–5005. doi: 10.1016/j.vaccine.2017.07.071. PubMed DOI PMC

Rawool D.B., Bitsaktsis C., Li Y., Gosselin D.R., Lin Y., Kurkure N.V., Metzger D.W., Gosselinet E.J. Utilization of Fc receptors as a mucosal vaccine strategy against an intracellular bacterium, Francisella tularensis. J. Immunol. 2008;180:5548–5557. doi: 10.4049/jimmunol.180.8.5548. PubMed DOI PMC

Iglesias B.V., Bitsaktsis C., Pham G., Drake J.R., Hazlett K.R.O., Porter K., Gosselin E.J. Multiple mechanisms mediate enhanced immunity generated by mAb-inactivated F. tularensis immunogen. Immunol. Cell Biol. 2013;91:139–148. doi: 10.1038/icb.2012.66. PubMed DOI PMC

Kirimanjeswara G.S., Golden J.M., Bakshi C.S., Metzger D.W. Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J. Immunol. 2007;179:532–539. doi: 10.4049/jimmunol.179.1.532. PubMed DOI

Bermudez L.E., Kolonoski P., Young L.S. Natural killer cell activity and macrophage-dependent inhibition of growth or killing of Mycobacterium avium complex in a mouse model. J. Leukoc. Biol. 1990;47:135–141. doi: 10.1002/jlb.47.2.135. PubMed DOI

Galdiero F., Romano Carratelli C., Nuzzo I., Folgore A. Cytotoxic antibody dependent cells in mice experimentally infected with Brucella abortus. Microbiologica. 1985;8:217–224. PubMed

Taylor D.W. Schistosome vaccines. Experientia. 1991;47:152–157. doi: 10.1007/BF01945416. PubMed DOI

Tagliabue A., Boraschi D., Villa L., Keren D.F., Lowell G.H., Rappuoli R., Nencioni L. IgA-dependent cell-mediated activity against enteropathogenic bacteria: Distribution, specificity, and characterization of the effector cells. J. Immunol. 1984;133:988–992. PubMed

Sanapala S., Yu J.J., Murthy A.K., Li W., Guentzel M.N., Chambers J.P., Klose K.E., Arulanandamet B.P. Perforin- and granzyme-mediated cytotoxic effector functions are essential for protection against Francisella tularensis following vaccination by the defined F. tularensis subsp. novicida ΔfopC vaccine strain. Infect. Immun. 2012;80:2177–2185. doi: 10.1128/IAI.00036-12. PubMed DOI PMC

Francis E., Felton L. Antitularemic serum. Public Health Rep. 1942;57:44–50. doi: 10.2307/4583978. DOI

Foshay L., Ruchman I., Nicholes P.S. Antitularense serum: Correlation between protective capacity for white rats and precipitable antibody content. J. Clin. Investig. 1947;26:756–760. doi: 10.1172/JCI101858. PubMed DOI PMC

Foshay L. Tularemia. Annu. Rev. Microbiol. 1950;4:313–330. doi: 10.1146/annurev.mi.04.100150.001525. PubMed DOI

Tärnvik A. Nature of protective immunity to Francisella tularensis. Rev. Infect. Dis. 1989;11:440–451. doi: 10.1093/clinids/11.3.440. PubMed DOI

Lu Z., Roche M.I., Hui J.H., Unal B., Felgner P.L., Gulati S., Madico G., Sharon J. Generation and characterization of hybridoma antibodies for immunotherapy of tularemia. Immunol. Lett. 2007;112:92–103. doi: 10.1016/j.imlet.2007.07.006. PubMed DOI PMC

Rhinehart-Jones T.R., Fortier A.H., Elkins K.L. Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect. Immun. 1994;62:3129–3137. doi: 10.1128/iai.62.8.3129-3137.1994. PubMed DOI PMC

Culkin S.J., Rhinehart-Jones T., Elkins K.L. A novel role for B cells in early protective immunity to an intracellular pathogen, Francisella tularensis strain LVS. J. Immunol. 1997;158:3277–3284. PubMed

Fulop M., Mastroeni P., Green M., Titball R.W. Role of antibody to lipopolysaccharide in protection against low-and high-virulence strains of Francisella tularensis. Vaccine. 2001;19:4465–4472. doi: 10.1016/S0264-410X(01)00189-X. PubMed DOI

Stenmark S., Lindgren H., Tärnvik A., Sjöstedt A. Specific antibodies contribute to the host protection against strains of Francisella tularensis subspecies holarctica. Microb. Pathog. 2003;35:73–80. doi: 10.1016/S0882-4010(03)00095-0. PubMed DOI

Stenmark S., Sjöstedt A. Transfer of specific antibodies results in increased expression of TNF-alpha and IL12 and recruitment of neutrophils to the site of a cutaneous Francisella tularensis infection. Pt 6J. Med. Microbiol. 2004;53:501–504. doi: 10.1099/jmm.0.05352-0. PubMed DOI

Kirimanjeswara G.S., Olmos S., Bakshi C.S., Metzger D.W. Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis. Immunol. Rev. 2008;225:244–255. doi: 10.1111/j.1600-065X.2008.00689.x. PubMed DOI PMC

Kubelkova K., Krocova Z., Balonova L., Pejchal J., Stulik J., Macela A. Specific antibodies protect gamma-irradiated mice against Francisella tularensis infection. Microb. Pathog. 2012;53:259–268. doi: 10.1016/j.micpath.2012.07.006. PubMed DOI

Kubelkova K., Benuchova M., Kozakova H., Sinkora M., Krocova Z., Pejchal J., Macela A. Gnotobiotic mouse model’s contribution to understanding host-pathogen interactions. Cell. Mol. Life Sci. 2016;73:3961–3969. doi: 10.1007/s00018-016-2341-8. PubMed DOI PMC

Chou A.Y., Kennett N.J., Melillo A.A., Elkins K.L. Murine survival of infection with Francisella novicida and protection against secondary challenge is critically dependent on B lymphocytes. Microbes Infect. 2017;19:91–100. doi: 10.1016/j.micinf.2016.12.001. PubMed DOI

Sebastian S., Pinkham J.T., Lynch J.G., Ross R.A., Reinap B., Blalock L.T., Conlan J.W., Kasper D.L. Cellular and humoral immunity are synergistic in protection against types A and B Francisella tularensis. Vaccine. 2009;27:597–605. doi: 10.1016/j.vaccine.2008.10.079. PubMed DOI PMC

Del Barrio L., Sahoo M., Lantier L., Reynolds J.M., Ceballos-Olvera I., Re F. Production of anti-LPS IgM by B1a B cells depends on IL-1β and is protective against lung infection with Francisella tularensis LVS. PLoS Pathog. 2015;11:e1004706. doi: 10.1371/journal.ppat.1004706. PubMed DOI PMC

Lu Z., Rynkiewicz M.J., Madico G., Li S., Yang C.Y., Perkins H.M., Sompuram S.R., Kodela V., Liu T., Morris T., et al. B-cell epitopes in GroEL of Francisella tularensis. PLoS ONE. 2014;9:e99847. doi: 10.1371/journal.pone.0099847. PubMed DOI PMC

Holland-Tummillo K.M., Shoudy L.E., Steiner D., Kumar S., Rosa S.J., Namjoshi P., Singh A., Sellati T.J., Gosselin E.J., Hazlett K.R. Autotransporter-Mediated Display of Complement Receptor Ligands by Gram-Negative Bacteria Increases Antibody Responses and Limits Disease Severity. Pathogens. 2020;9:375. doi: 10.3390/pathogens9050375. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...