{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,4]],"date-time":"2026-03-04T10:47:22Z","timestamp":1772621242345,"version":"3.50.1"},"reference-count":69,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,6,4]],"date-time":"2021-06-04T00:00:00Z","timestamp":1622764800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Fonds voor Wetenschappelijk Onderzoek \u2013 Vlaanderen","award":["G013518N"],"award-info":[{"award-number":["G013518N"]}]},{"DOI":"10.13039\/501100004385","name":"Universiteit Gent","doi-asserted-by":"publisher","award":["BOF.STG.2018.0009.01 \/ 01N01518\/UGent-BOF 'Startkrediet'"],"award-info":[{"award-number":["BOF.STG.2018.0009.01 \/ 01N01518\/UGent-BOF 'Startkrediet'"]}],"id":[{"id":"10.13039\/501100004385","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004418","name":"Vrije Universiteit Brussel","doi-asserted-by":"publisher","award":["SRP63"],"award-info":[{"award-number":["SRP63"]}],"id":[{"id":"10.13039\/501100004418","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Ghent University Global Campus RC5 research center","award":["core funding"],"award-info":[{"award-number":["core funding"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vaccines"],"abstract":"<jats:p>Salivarian trypanosomes are extracellular parasites causing anthroponotic and zoonotic infections. Anti-parasite vaccination is considered the only sustainable method for global trypanosomosis control. Unfortunately, no single field applicable vaccine solution has been successful so far. The active destruction of the host\u2019s adaptive immune system by trypanosomes is believed to contribute to this problem. Here, we show that Trypanosome brucei brucei infection results in the lasting obliteration of immunological memory, including vaccine-induced memory against non-related pathogens. Using the well-established DTPa vaccine model in combination with a T. b. brucei infection and a diminazene diaceturate anti-parasite treatment scheme, our results demonstrate that while the latter ensured full recovery from the T. b. brucei infection, it failed to restore an efficacious anti-B. pertussis vaccine recall response. The DTPa vaccine failure coincided with a shift in the IgG1\/IgG2a anti-B. pertussis antibody ratio in favor of IgG2a, and a striking impact on all of the spleen immune cell populations. Interestingly, an increased plasma IFN\u03b3 level in DTPa-vaccinated trypanosome-infected mice coincided with a temporary antibody-independent improvement in early-stage trypanosomosis control. In conclusion, our results are the first to show that trypanosome-inflicted immune damage is not restored by successful anti-parasite treatment.<\/jats:p>","DOI":"10.3390\/vaccines9060603","type":"journal-article","created":{"date-parts":[[2021,6,7]],"date-time":"2021-06-07T01:56:40Z","timestamp":1623031000000},"page":"603","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["African Trypanosomosis Obliterates DTPa Vaccine-Induced Functional Memory So That Post-Treatment Bordetella pertussis Challenge Fails to Trigger a Protective Recall Response"],"prefix":"10.3390","volume":"9","author":[{"given":"Magdalena","family":"Radwanska","sequence":"first","affiliation":[{"name":"Department of Biomedical Molecular Biology, Ghent University, Technologiepark Zwijnaarde 71, 9000 Ghent, Belgium"},{"name":"Laboratory for Biomedical Research, Department of Molecular Biotechnology, Environment Technology and Food Technology, Ghent University Global Campus, Songdomunhwa-Ro 119-5, Yeonsu-Gu, Incheon 406-840, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1642-4700","authenticated-orcid":false,"given":"Hang Thi Thu","family":"Nguyen","sequence":"additional","affiliation":[{"name":"Laboratory for Biomedical Research, Department of Molecular Biotechnology, Environment Technology and Food Technology, Ghent University Global Campus, Songdomunhwa-Ro 119-5, Yeonsu-Gu, Incheon 406-840, Korea"},{"name":"Department of Biochemistry and Microbiology, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium"},{"name":"Laboratory of Cellular and Molecular Immunology, Department of Bioengineering Sciences, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stefan","family":"Magez","sequence":"additional","affiliation":[{"name":"Laboratory for Biomedical Research, Department of Molecular Biotechnology, Environment Technology and Food Technology, Ghent University Global Campus, Songdomunhwa-Ro 119-5, Yeonsu-Gu, Incheon 406-840, Korea"},{"name":"Department of Biochemistry and Microbiology, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium"},{"name":"Laboratory of Cellular and Molecular Immunology, Department of Bioengineering Sciences, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1016\/j.chom.2016.05.002","article-title":"Trypanosoma brucei Parasites Occupy and Functionally Adapt to the Adipose Tissue in Mice","volume":"19","author":"Trindade","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_2","first-page":"257","article-title":"Epidemiology of human African trypanosomiasis","volume":"6","author":"Franco","year":"2014","journal-title":"Clin. Epidemiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/s41564-017-0085-3","article-title":"The structure of serum resistance-associated protein and its implications for human African trypanosomiasis","volume":"3","author":"Zoll","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1038\/nrmicro3298","article-title":"The molecular arms race between African trypanosomes and humans","volume":"12","author":"Pays","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"S108","DOI":"10.1017\/S0031182014000602","article-title":"A co-evolutionary arms race: Trypanosomes shaping the human genome, humans shaping the trypanosome genome","volume":"142","author":"Capewell","year":"2015","journal-title":"Parasitology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2253","DOI":"10.3389\/fimmu.2018.02253","article-title":"Salivarian Trypanosomosis: A Review of Parasites Involved, Their Global Distribution and Their Interaction with the Innate and Adaptive Mammalian Host Immune System","volume":"9","author":"Radwanska","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Truc, P., B\u00fcscher, P., Cuny, G., Gonzatti, M.I., Jannin, J., Joshi, P., Juyal, P., Lun, Z.R., Mattioli, R., and Pays, E. (2013). Atypical human infections by animal trypanosomes. PLoS Negl. Trop. Dis., 7.","DOI":"10.1371\/journal.pntd.0002256"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1093\/cid\/ciw052","article-title":"A Clinical and Epidemiological Investigation of the First Reported Human Infection with the Zoonotic Parasite Trypanosoma evansi in Southeast Asia","volume":"62","author":"Desquesnes","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2752","DOI":"10.1056\/NEJMoa063265","article-title":"Human Trypanosoma evansi infection linked to a lack of apolipoprotein L-I","volume":"355","author":"Vanhollebeke","year":"2006","journal-title":"N. Engl. J. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.ijpara.2008.07.004","article-title":"Development of a mathematical model for mechanical transmission of trypanosomes and other pathogens of cattle transmitted by tabanids","volume":"39","author":"Desquesnes","year":"2009","journal-title":"Int. J. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.exppara.2003.12.014","article-title":"Mechanical transmission of Trypanosoma congolense in cattle by the African tabanid Atylotus agrestis","volume":"105","author":"Desquesnes","year":"2003","journal-title":"Exp. Parasitol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.meegid.2018.05.033","article-title":"Tsetse fly evolution, genetics and the trypanosomiases\u2014A review","volume":"64","author":"Krafsur","year":"2018","journal-title":"Infect. Genet. Evol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"6201350","DOI":"10.1155\/2016\/6201350","article-title":"Tsetse Flies (Glossina) as Vectors of Human African Trypanosomiasis: A Review","volume":"2016","author":"Wamwiri","year":"2016","journal-title":"Biomed. Res. Int."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4225","DOI":"10.1093\/nar\/9.17.4225","article-title":"Analysis of the DNA and RNA changes associated with the expression of isotypic variant-specific antigens of trypanosomes","volume":"9","author":"Pays","year":"1981","journal-title":"Nucleic Acids Res."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Frenkel, D., Zhang, F., Guirnalda, P., Haynes, C., Bockstal, V., Radwanska, M., Magez, S., and Black, S.J. (2016). Trypanosoma brucei Co-opts NK Cells to Kill Splenic B2 B Cells. PLoS Pathog., 12.","DOI":"10.1371\/journal.ppat.1005733"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e1800181","DOI":"10.1002\/bies.201800181","article-title":"Evolution of Antigenic Variation in African Trypanosomes: Variant Surface Glycoprotein Expression, Structure, and Function","volume":"40","author":"Bangs","year":"2018","journal-title":"Bioessays"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"382","DOI":"10.3389\/fimmu.2020.00382","article-title":"Infections with Extracellular Trypanosomes Require Control by Efficient Innate Immune Mechanisms and Can Result in the Destruction of the Mammalian Humoral Immune System","volume":"11","author":"Magez","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Schwede, A., Macleod, O.J., MacGregor, P., and Carrington, M. (2015). How Does the VSG Coat of Bloodstream Form African Trypanosomes Interact with External Proteins?. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1005259"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.cell.2007.08.046","article-title":"Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes","volume":"131","author":"Engstler","year":"2007","journal-title":"Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.chom.2007.10.006","article-title":"Restless gossamers: Antibody clearance by hydrodynamic flow forces generated at the surface of motile trypanosome parasites","volume":"2","author":"Dean","year":"2007","journal-title":"Cell Host Microbe"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1042\/ETLS20170104","article-title":"Emerging challenges in understanding trypanosome antigenic variation","volume":"1","author":"McCulloch","year":"2017","journal-title":"Emerg. Top. Life Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1128\/IAI.00729-08","article-title":"T-cell responses to the trypanosome variant surface glycoprotein are not limited to hypervariable subregions","volume":"77","author":"Dagenais","year":"2009","journal-title":"Infect. Immun."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1128\/iai.52.1.223-229.1986","article-title":"Restriction of the alternative pathway of human complement by intact Trypanosoma brucei subsp. gambiense","volume":"52","author":"Devine","year":"1986","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1016\/j.micinf.2005.11.009","article-title":"CR3 (CD11b\/CD18) is the major macrophage receptor for IgM antibody-mediated phagocytosis of African trypanosomes: Diverse effect on subsequent synthesis of tumor necrosis factor alpha and nitric oxide","volume":"8","author":"Pan","year":"2006","journal-title":"Microbes Infect."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/0165-2427(93)90121-J","article-title":"Immune lysis of Trypanosoma congolense: Generation of a soluble covalent complex of variant surface glycoprotein and bovine complement component C3b","volume":"38","author":"Liu","year":"1993","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1128\/iai.27.3.832-836.1980","article-title":"Hemolytic complement and serum C3 levels in Zebu cattle infected with Trypanosoma congolense and Trypanosoma vivax and the effect of trypanocidal treatment","volume":"27","author":"Rurangirwa","year":"1980","journal-title":"Infect. Immun."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Bockstal, V., Guirnalda, P., Caljon, G., Goenka, R., Telfer, J.C., Frenkel, D., Radwanska, M., Magez, S., and Black, S.J. (2011). T. brucei infection reduces B lymphopoiesis in bone marrow and truncates compensatory splenic lymphopoiesis through transitional B-cell apoptosis. PLoS Pathog., 7.","DOI":"10.1371\/journal.ppat.1002089"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1111\/pim.12099","article-title":"Chronic Trypanosoma congolense infections in mice cause a sustained disruption of the B-cell homeostasis in the bone marrow and spleen","volume":"36","author":"Obishakin","year":"2014","journal-title":"Parasite Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Blom-Potar, M.C., Chamond, N., Cosson, A., Jouvion, G., Droin-Bergere, S., Huerre, M., and Minoprio, P. (2010). Trypanosoma vivax infections: Pushing ahead with mouse models for the study of Nagana. II. Immunobiological dysfunctions. PLoS Negl. Trop. Dis., 4.","DOI":"10.1371\/journal.pntd.0000793"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Radwanska, M., Guirnalda, P., De Trez, C., Ryffel, B., Black, S., and Magez, S. (2008). Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000078"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Magez, S., Schwegmann, A., Atkinson, R., Claes, F., Drennan, M., De Baetselier, P., and Brombacher, F. (2008). The role of B-cells and IgM antibodies in parasitemia, anemia, and VSG switching in Trypanosoma brucei-infected mice. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000122"},{"key":"ref_32","unstructured":"Magez, S., Bockstal, V., Brombacher, F., Black, S., and Radwanska, M. (2010, January 15\u201320). Parasite-induced B-cell Apoptosis Results in Loss of Specific Protective Anti-trypanosome Antibody Responses, and Abolishment of Vaccine Induced Protective Memory Responses. Proceedings of the XII International Congress of Parasitology (ICOPA), Melbourne, Australia."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0304-4017(02)00363-1","article-title":"The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever","volume":"111","author":"Holland","year":"2003","journal-title":"Vet. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"194176","DOI":"10.1155\/2013\/194176","article-title":"Trypanosoma evansi and surra: A review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects","volume":"2013","author":"Desquesnes","year":"2013","journal-title":"BioMed Res. Int."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1007\/s11250-009-9461-1","article-title":"Immune responses to haemorrhagic septicaemia (HS) vaccination in Trypanosoma evansi infected buffalo-calves","volume":"42","author":"Singla","year":"2010","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0021-9975(97)80067-9","article-title":"Effects of Trypanosoma evansi on the output of cells from a lymph node draining the site of Pasteurella haemolytica vaccine administration","volume":"117","author":"Onah","year":"1997","journal-title":"J. Comp. Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/S0304-4017(01)00534-9","article-title":"The influence of T. evansi infection on the immuno-responsiveness of experimentally infected water buffaloes","volume":"102","author":"Holland","year":"2001","journal-title":"Vet. Parasitol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Lejon, V., Mumba Ngoyi, D., Kestens, L., Boel, L., Barbe, B., Kande Betu, V., van Griensven, J., Bottieau, E., Muyembe Tamfum, J.J., and Jacobs, J. (2014). Gambiense human african trypanosomiasis and immunological memory: Effect on phenotypic lymphocyte profiles and humoral immunity. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1003947"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Dickie, E.A., Giordani, F., Gould, M.K., Maser, P., Burri, C., Mottram, J.C., Rao, S.P.S., and Barrett, M.P. (2020). New Drugs for Human African Trypanosomiasis: A Twenty First Century Success Story. Trop. Med. Infect. Dis., 5.","DOI":"10.3390\/tropicalmed5010029"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Roy Chowdhury, A., Bakshi, R., Wang, J., Yildirir, G., Liu, B., Pappas-Brown, V., Tolun, G., Griffith, J.D., Shapiro, T.A., and Jensen, R.E. (2010). The killing of African trypanosomes by ethidium bromide. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001226"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1046\/j.1365-3024.2000.00348.x","article-title":"Antibodies raised against the flagellar pocket fraction of Trypanosoma brucei preferentially recognize HSP60 in cDNA expression library","volume":"22","author":"Radwanska","year":"2000","journal-title":"Parasite Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1128\/IAI.68.2.848-860.2000","article-title":"Comparative analysis of antibody responses against HSP60, invariant surface glycoprotein 70, and variant surface glycoprotein reveals a complex antigen-specific pattern of immunoglobulin isotype switching during infection by Trypanosoma brucei","volume":"68","author":"Radwanska","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e12664","DOI":"10.1111\/pim.12664","article-title":"Trypanosoma brucei brucei causes a rapid and persistent influx of neutrophils in the spleen of infected mice","volume":"41","author":"Deleeuw","year":"2019","journal-title":"Parasite Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3521","DOI":"10.1128\/IAI.70.7.3521-3528.2002","article-title":"Immunogenicity and protective efficacy of neonatal vaccination against Bordetella pertussis in a murine model: Evidence for early control of pertussis","volume":"70","author":"Roduit","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4281","DOI":"10.1016\/j.vaccine.2014.06.019","article-title":"Heterologous prime-boost immunization with live attenuated B. pertussis BPZE1 followed by acellular pertussis vaccine in mice","volume":"32","author":"Feunou","year":"2014","journal-title":"Vaccine"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.pt.2017.11.008","article-title":"Do Cryptic Reservoirs Threaten Gambiense-Sleeping Sickness Elimination?","volume":"34","author":"Buscher","year":"2018","journal-title":"Trends Parasitol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2397","DOI":"10.1016\/S0140-6736(17)31510-6","article-title":"Human African trypanosomiasis","volume":"390","author":"Cecchi","year":"2017","journal-title":"Lancet"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/s13071-019-3311-4","article-title":"Systematic review and meta-analysis on the global distribution, host range, and prevalence of Trypanosoma evansi","volume":"12","author":"Aregawi","year":"2019","journal-title":"Parasite Vectors"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Hall, J.P., Wang, H., and Barry, J.D. (2013). Mosaic VSGs and the scale of Trypanosoma brucei antigenic variation. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003502"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1983","DOI":"10.4049\/jimmunol.131.4.1983","article-title":"Trypanosomal surface coat variant antigen causes polyclonal lymphocyte activation","volume":"131","author":"Diffley","year":"1983","journal-title":"J. Immunol."},{"key":"ref_51","first-page":"10","article-title":"Expression of the B cell repertoire and autoantibodies in human African trypanosomiasis","volume":"65","author":"Kazyumba","year":"1986","journal-title":"Clin. Exp. Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2836","DOI":"10.1128\/JCM.00456-10","article-title":"Low specificities of HIV diagnostic tests caused by T. brucei gambiense sleeping sickness","volume":"48","author":"Lejon","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"582","DOI":"10.3389\/fimmu.2017.00582","article-title":"African Trypanosomes Undermine Humoral Responses and Vaccine Development: Link with Inflammatory Responses?","volume":"8","author":"Stijlemans","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"5492","DOI":"10.4049\/jimmunol.151.10.5492","article-title":"Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins","volume":"151","author":"Schleifer","year":"1993","journal-title":"J. Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1849","DOI":"10.1086\/648374","article-title":"Identification of a parasitic immunomodulatory protein triggering the development of suppressive M1 macrophages during African trypanosomiasis","volume":"200","author":"Stijlemans","year":"2009","journal-title":"J. Infect. Dis."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2738","DOI":"10.3389\/fimmu.2019.02738","article-title":"Host Immune Responses and Immune Evasion Strategies in African Trypanosomiasis","volume":"10","author":"Onyilagha","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3449","DOI":"10.1016\/j.vaccine.2011.02.062","article-title":"Induction of Bordetella pertussis-specific immune memory by DTPa vaccines","volume":"29","author":"Morel","year":"2011","journal-title":"Vaccine"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"7396","DOI":"10.1038\/s41598-020-63998-2","article-title":"Intranasal immunization with outer membrane vesicle pertussis vaccine confers broad protection through mucosal IgA and Th17 responses","volume":"10","author":"Raeven","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.micinf.2004.01.004","article-title":"Alternative diphtheria, tetanus and whooping cough immunization schedule to evoke a Th2 tetanus and a Th1 pertussis immune response","volume":"6","author":"Lavigne","year":"2004","journal-title":"Microbes Infect."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/S1286-4579(02)01601-5","article-title":"Whole-cell Bordetella pertussis vaccine component modulates the mouse immune response to an unrelated soluble antigen","volume":"4","author":"Lavigne","year":"2002","journal-title":"Microbes Infect."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.3389\/fimmu.2017.01105","article-title":"Interferon Gamma in African Trypanosome Infections: Friends or Foes?","volume":"8","author":"Wu","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Cnops, J., De Trez, C., Stijlemans, B., Keirsse, J., Kauffmann, F., Barkhuizen, M., Keeton, R., Boon, L., Brombacher, F., and Magez, S. (2015). NK-, NKT- and CD8-Derived IFNgamma Drives Myeloid Cell Activation and Erythrophagocytosis, Resulting in Trypanosomosis-Associated Acute Anemia. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1004964"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1111\/pim.12208","article-title":"IFN-gamma mediates early B-cell loss in experimental African trypanosomosis","volume":"37","author":"Cnops","year":"2015","journal-title":"Parasite Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"6775","DOI":"10.4049\/jimmunol.161.12.6775","article-title":"Resistance to the African trypanosomes is IFN-gamma dependent","volume":"161","author":"Hertz","year":"1998","journal-title":"J. Immunol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1284","DOI":"10.1086\/592048","article-title":"Interleukin-12p70 deficiency increases survival and diminishes pathology in Trypanosoma congolense infection","volume":"198","author":"Barkhuizen","year":"2008","journal-title":"J. Infect. Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"2501","DOI":"10.4049\/jimmunol.175.4.2501","article-title":"The induction of a type 1 immune response following a Trypanosoma brucei infection is MyD88 dependent","volume":"175","author":"Drennan","year":"2005","journal-title":"J. Immunol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1083\/jcb.137.3.715","article-title":"Specific uptake of tumor necrosis factor-alpha is involved in growth control of Trypanosoma brucei","volume":"137","author":"Magez","year":"1997","journal-title":"J. Cell. Biol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1086\/319257","article-title":"Human macrophage tumor necrosis factor (TNF)-alpha production induced by Trypanosoma brucei gambiense and the role of TNF-alpha in parasite control","volume":"183","author":"Bouteille","year":"2001","journal-title":"J. Infect. Dis."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1111\/pim.12387","article-title":"Prospects for vaccination against pathogenic African trypanosomes","volume":"38","author":"Black","year":"2016","journal-title":"Parasite Immunol."}],"container-title":["Vaccines"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/6\/603\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:11:06Z","timestamp":1760163066000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/6\/603"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,4]]},"references-count":69,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["vaccines9060603"],"URL":"https:\/\/doi.org\/10.3390\/vaccines9060603","relation":{"has-preprint":[{"id-type":"doi","id":"10.20944\/preprints202104.0785.v1","asserted-by":"object"}]},"ISSN":["2076-393X"],"issn-type":[{"value":"2076-393X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,4]]}}}