Babesiosis Vaccines: Lessons Learned, Challenges Ahead, and Future Glimpses

Suarez, 2011, Emerging perspectives in the research of bovine babesiosis and anaplasmosis, Vet. Parasitol., 180, 109, 10.1016/j.vetpar.2011.05.032 Krause, 2019, Human babesiosis, Int. J. Parasitol., 49, 165, 10.1016/j.ijpara.2018.11.007 Suarez, 2019, Unravelling the cellular and molecular pathogenesis of bovine babesiosis: is the sky the limit?, Int. J. Parasitol., 49, 183, 10.1016/j.ijpara.2018.11.002 Jiang, 2015, Epidemiological, clinical, and laboratory characteristics of 48 cases of Babesia venatorum infection in China: a descriptive study, Lancet Infect. Dis., 15, 196, 10.1016/S1473-3099(14)71046-1 Ord, 2015, Human babesiosis: pathogens, prevalence, diagnosis, and treatment, Curr. Clin. Microbiol. Rep., 2, 173, 10.1007/s40588-015-0025-z Cooke, 2005, Cellular adhesive phenomena in apicomplexan parasites of red blood cells, Vet. Parasitol., 132, 273, 10.1016/j.vetpar.2005.07.002 Solano-Gallego, 2016, A review of canine babesiosis: the European perspective, Parasit. Vectors, 9, 336, 10.1186/s13071-016-1596-0 Uilenberg, 2006, Babesia – a historical overview, Vet. Parasitol., 138, 3, 10.1016/j.vetpar.2006.01.035 Brown, 2006, Prospects for recombinant vaccines against Babesia bovis and related parasites, Parasite Immunol., 28, 315, 10.1111/j.1365-3024.2006.00849.x Goff, 2010, The bovine spleen: interactions among splenic cell populations in the innate immunologic control of hemoparasitic infections, Vet. Immunol. Immunopathol., 138, 1, 10.1016/j.vetimm.2010.07.006 Hein, 1991, Prominence of gamma delta T cells in the ruminant immune system, Immunol. Today, 12, 30, 10.1016/0167-5699(91)90109-7 Deroost, 2018, Gamma/delta T cells and their role in protection against malaria, Front. Immunol., 9, 2973, 10.3389/fimmu.2018.02973 Hajdusek, 2013, Interaction of the tick immune system with transmitted pathogens, Front. Cell. Infect. Microbiol., 3, 26, 10.3389/fcimb.2013.00026 Schetters, 1995, Vaccines against babesiosis using soluble parasite antigens, Parasitol. Today, 11, 456, 10.1016/0169-4758(95)80059-X Timms, 1989, Development of babesial vaccines, Trans. R. Soc. Trop. Med. Hyg., 83, 73, 10.1016/0035-9203(89)90608-1 Mahoney, 1967, Bovine babesiosis: the immunization of cattle with killed Babesia argentina, Exp. Parasitol., 20, 125, 10.1016/0014-4894(67)90030-6 Mahoney, 1976, Babesia argentina: immunization of cattle with a killed antigen against infection with a heterologous strain, Vet. Parasitol., 2, 273, 10.1016/0304-4017(76)90085-6 Sibinovic, 1967, Immunogenic properties of babesial serum antigens, J. Parasitol., 53, 1121, 10.2307/3276666 Montenegro-James, 1995, Development of conventional subunit vaccines for anaplasmosis and babesiosis, Vet. Parasitol., 57, 255, 10.1016/0304-4017(94)03124-F Smith, 1981, Bovine babesiosis: protection of cattle with culture-derived soluble Babesia bovis antigen, Science, 212, 335, 10.1126/science.7209532 Montenegro-James, 1989, Immunoprophylactic control of bovine babesiosis: role of exoantigens of Babesia, Trans. R. Soc. Trop. Med. Hyg., 83, 85, 10.1016/0035-9203(89)90610-X Moreau, 1989, Vaccination against canine babesiosis: an overview of field observations, Trans. R. Soc. Trop. Med. Hyg., 83, 95, 10.1016/0035-9203(89)90611-1 Valentin, 1993, Cellular and humoral immune responses induced in cattle by vaccination with Babesia divergens culture-derived exoantigens correlate with protection, Infect. Immun., 61, 734, 10.1128/IAI.61.2.734-741.1993 Zhao, 2002, Culture-derived Babesia orientalis exoantigens used as a vaccine against buffalo babesiosis, Parasitol. Res., 88, S38, 10.1007/s00436-001-0569-0 Timms, 1983, Babesia bovis: comparison of culture-derived parasites, non-living antigen and conventional vaccine in the protection of cattle against heterologous challenge, Aust. Vet. J., 60, 75, 10.1111/j.1751-0813.1983.tb05874.x Cockburn, 2018, Malaria prevention: from immunological concepts to effective vaccines and protective antibodies, Nat. Immunol., 19, 1199, 10.1038/s41590-018-0228-6 Fish, 2008, Vaccination of cattle against B. bovis infection with live attenuated parasites and non-viable immunogens, Vaccine, 26, G29, 10.1016/j.vaccine.2008.09.070 Schetters, 2005, Vaccination against canine babesiosis, Trends Parasitol., 21, 179, 10.1016/j.pt.2005.02.006 Moreau, 1984, Antibabesial vaccination using antigens from cell culture fluids: industrial requirements, 129 Schetters, 1995, Strain variation limits protective activity of vaccines based on soluble Babesia canis antigens, Parasite Immunol., 17, 215, 10.1111/j.1365-3024.1995.tb00891.x Schetters, 2001, Vaccination of dogs against heterologous Babesia canis infection using antigens from culture supernatants, Vet. Parasitol., 100, 75, 10.1016/S0304-4017(01)00485-X Delbecq, 2006, Hydrophobic moeties in recombinant proteins are crucial to generate efficient saponin-based vaccine against apicomplexan Babesia divergens, Vaccine, 24, 613, 10.1016/j.vaccine.2005.08.073 Hadj-Kaddour, 2007, Recombinant protein Bd37 protected gerbils against heterologous challenges with isolates of Babesia divergens polymorphic for the bd37 gene, Parasitology, 134, 187, 10.1017/S0031182006001399 Moubri, 2018, Discovery of a recombinant Babesia canis supernatant antigen that protects dogs against virulent challenge infection, Vet. Parasitol., 249, 21, 10.1016/j.vetpar.2017.11.002 Di Pasquale, 2015, Vaccine adjuvants: from 1920 to 2015 and beyond, Vaccines (Basel), 3, 320, 10.3390/vaccines3020320 de la Fuente, 2015, Tick vaccines: current status and future directions, Expert Rev. Vaccines, 14, 1367, 10.1586/14760584.2015.1076339 Schetters, 2016, Cattle tick vaccine researchers join forces in CATVAC, Parasit. Vectors, 9, 105, 10.1186/s13071-016-1386-8 Hussein, 2015, Targeted silencing of the Aquaporin 2 gene of Rhipicephalus (Boophilus) microplus reduces tick fitness, Parasit. Vectors, 8, 618, 10.1186/s13071-015-1226-2 Rodriguez-Mallon, 2016, Developing anti-tick vaccines, Meth. Mol. Biol., 1404, 243, 10.1007/978-1-4939-3389-1_17 Cornillot, 2012, Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti, Nucleic Acids Res., 40, 9102, 10.1093/nar/gks700 Cuesta, 2014, High-Quality draft genome sequence of Babesia divergens, the etiological agent of cattle and human babesiosis, Genome Announc., 2, e01194-14, 10.1128/genomeA.01194-14 Eichenberger, 2017, Genome-wide analysis of gene expression and protein secretion of Babesia canis during virulent infection identifies potential pathogenicity factors, Sci. Rep., 7, 3357, 10.1038/s41598-017-03445-x Gohil, 2013, Bioinformatic prediction of the exportome of Babesia bovis and identification of novel proteins in parasite-infected red blood cells, Int. J. Parasitol., 43, 409, 10.1016/j.ijpara.2013.01.002 Antunes, 2019, Transcriptome and proteome response of Rhipicephalus annulatus tick vector to Babesia bigemina infection, Front. Physiol., 10, 318, 10.3389/fphys.2019.00318 Cornillot, 2016, A targeted immunomic approach identifies diagnostic antigens in the human pathogen Babesia microti, Transfusion, 56, 2085, 10.1111/trf.13640 Magni, 2019, Analysis of the Babesia microti proteome in infected red blood cells by a combination of nanotechnology and mass spectrometry, Int. J. Parasitol., 49, 139, 10.1016/j.ijpara.2018.08.004 Silva, 2016, Genome-wide diversity and gene expression profiling of Babesia microti isolates identify polymorphic genes that mediate host–pathogen interactions, Sci. Rep., 6, 35284, 10.1038/srep35284 McWilliam, 2013, Local immune responses of the Chinese water buffalo, Bubalus bubalis, against Schistosoma japonicum larvae: crucial insights for vaccine design, PLoS Negl. Trop. Dis., 7, 10.1371/journal.pntd.0002460 Norimine, 2003, Infect. Immun., 71, 5021, 10.1128/IAI.71.9.5021-5032.2003 Flaxman, 2018, Methods for measuring T-Cell memory to vaccination: from mouse to man, Vaccines, 6, 43, 10.3390/vaccines6030043 Coakley, 2015, Exosomes and other extracellular vesicles: the new communicators in parasite infections, Trends Parasitol., 31, 477, 10.1016/j.pt.2015.06.009 Zhang, 2018, Exosomes in pathogen infections: a bridge to deliver molecules and link functions, Front. Immunol., 9, 90, 10.3389/fimmu.2018.00090 Marcilla, 2014, Extracellular vesicles in parasitic diseases, J. Extracell. Vesicles, 3, 25040, 10.3402/jev.v3.25040 Martin-Jaular, 2016, Spleen-dependent immune protection elicited by CpG adjuvanted reticulocyte-derived exosomes from malaria infection is associated with changes in T cell subsets’ distribution, Front. Cell Dev. Biol., 4, 131, 10.3389/fcell.2016.00131 Martin-Jaular, 2011, Exosomes from Plasmodium yoelii-infected reticulocytes protect mice from lethal infections, PLoS One, 6, 10.1371/journal.pone.0026588 Jalovecka, 2019, Babesia life cycle – when phylogeny meets biology, Trends Parasitol., 35, 356, 10.1016/j.pt.2019.01.007 Goncalves, 2016, Transmission-blocking strategies: the roadmap from laboratory bench to the community, Malar. J., 15, 95, 10.1186/s12936-016-1163-3 Alzan, 2019, Transgenic Babesia bovis lacking 6-Cys sexual-stage genes as the foundation for non-transmissible live vaccines against bovine babesiosis, Ticks Tick Borne Dis., 10, 722, 10.1016/j.ttbdis.2019.01.006 Hussein, 2017, The Babesia bovis hap2 gene is not required for blood stage replication, but expressed upon in vitro sexual stage induction, PLoS Negl. Trop. Dis., 11, 10.1371/journal.pntd.0005965 Bastos, 2013, Differential expression of three members of the multidomain adhesion CCp family in Babesia bigemina, Babesia bovis and Theileria equi, PLoS One, 8, 10.1371/journal.pone.0067765 Malkin, 2005, Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria, Vaccine, 23, 3131, 10.1016/j.vaccine.2004.12.019 Wu, 2008, Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51, PLoS One, 3, 10.1371/journal.pone.0002636 de Waal, 2006, Live vaccines against bovine babesiosis, Vet. Parasitol., 138, 88, 10.1016/j.vetpar.2006.01.042 Callow, 1997, Development of effective living vaccines against bovine babesiosis – the longest field trial?, Int. J. Parasitol., 27, 747, 10.1016/S0020-7519(97)00034-9 Florin-Christensen, 2014, Vaccines against bovine babesiosis: where we are now and possible roads ahead, Parasitology, 141, 1563, 10.1017/S0031182014000961 Wright, 1983, Babesia bovis: isolation of a protective antigen by using monoclonal antibodies, Infect. Immun., 41, 244, 10.1128/IAI.41.1.244-250.1983 Wright, 1992, The development of a recombinant Babesia vaccine, Vet. Parasitol., 44, 3, 10.1016/0304-4017(92)90138-Y Hope, 2005, Potential for recombinant Babesia bovis antigens to protect against a highly virulent isolate, Parasite Immunol., 27, 439, 10.1111/j.1365-3024.2005.00795.x Mosqueda, 2002, Babesia bovis merozoite surface antigen 2 proteins are expressed on the merozoite and sporozoite surface, and specific antibodies inhibit attachment and invasion of erythrocytes, Infect. Immun., 70, 6448, 10.1128/IAI.70.11.6448-6455.2002 Antonio Alvarez, 2010, Immunization of Bos taurus steers with Babesia bovis recombinant antigens MSA-1, MSA-2c and 12D3, Transbound. Emerg. Dis., 57, 87, 10.1111/j.1865-1682.2010.01117.x Leroith, 2005, Sequence variation and immunologic cross-reactivity among Babesia bovis merozoite surface antigen 1 proteins from vaccine strains and vaccine breakthrough isolates, Infect. Immun., 73, 5388, 10.1128/IAI.73.9.5388-5394.2005 Goff, 1988, Identification of Babesia bovis merozoite surface antigens by using immune bovine sera and monoclonal antibodies, Infect. Immun., 56, 2363, 10.1128/IAI.56.9.2363-2368.1988 Suarez, 1993, Immunogenic B-cell epitopes of Babesia bovis rhoptry-associated protein 1 are distinct from sequences conserved between species, Infect. Immun., 61, 3511, 10.1128/IAI.61.8.3511-3517.1993 Commins, 1985, Proteinases in the lysate of bovine erythrocytes infected with Babesia bovis: initial vaccination studies, Int. J. Parasitol., 15, 491, 10.1016/0020-7519(85)90042-6 McElwain, 1991, Molecular characterization and immunogenicity of neutralization-sensitive Babesia bigemina merozoite surface proteins, Mol. Biochem. Parasitol., 47, 213, 10.1016/0166-6851(91)90181-5 Suarez, 2011, A novel neutralization sensitive and subdominant RAP-1-related antigen (RRA) is expressed by Babesia bovis merozoites, Parasitology, 138, 809, 10.1017/S0031182011000321 Rosano, 2014, Recombinant protein expression in Escherichia coli: advances and challenges, Front. Microbiol., 5, 172, 10.3389/fmicb.2014.00172 Li, 2002, Role of disulfide bonds in regulating antigen processing and epitope selection, J. Immunol., 169, 2444, 10.4049/jimmunol.169.5.2444 Hensmann, 2004, Disulfide bonds in merozoite surface protein 1 of the malaria parasite impede efficient antigen processing and affect the in vivo antibody response, Eur. J. Immunol., 34, 639, 10.1002/eji.200324514 Bushkin, 2010, Suggestive evidence for Darwinian Selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii, Eukaryot. Cell, 9, 228, 10.1128/EC.00197-09 Goddard-Borger, 2018, Implications of Plasmodium glycosylation on vaccine efficacy and design, Future Microbiol, 13, 609, 10.2217/fmb-2017-0284 Mahla, 2013, Sweeten PAMPs: role of sugar complexed PAMPs in innate immunity and vaccine biology, Front. Immunol., 4, 248, 10.3389/fimmu.2013.00248 Marciani, 2018, Elucidating the mechanisms of action of saponin-derived adjuvants, Trends Pharmacol. Sci., 39, 573, 10.1016/j.tips.2018.03.005 den Brok, 2016, Saponin-based adjuvants induce cross-presentation in dendritic cells by intracellular lipid body formation, Nat. Commun., 7, 13324, 10.1038/ncomms13324 Garcia, 2016, An updated review of ISCOMSTM and ISCOMATRIXTM vaccines, Curr. Pharm. Des., 22, 6294, 10.2174/1381612822666160915161302 Morelli, 2012, ISCOMATRIX: a novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases, J. Med. Microbiol., 61, 935, 10.1099/jmm.0.040857-0 Mahoney, 1981, Bovine babesiosis: the immunization of cattle with fractions of erythrocytes infected with Babesia bovis (syn B. argentina), Vet. Immunol. Immunopathol., 2, 145, 10.1016/0165-2427(81)90046-5 Goodger, 1984, Babesia bovis: vaccination of cattle against heterologous challenge with fractions of lysate from infected erythrocytes, Z. Parasitenkd., 70, 321, 10.1007/BF00927818 Goodger, 1985, Babesia bovis: successful vaccination against homologous challenge in splenectomised calves using a fraction of haemagglutinating antigen, Int. J. Parasitol., 15, 175, 10.1016/0020-7519(85)90084-0 Timms, 1984, Immune responses of cattle following vaccination with living and non-living Babesia bovis antigens, Vet. Parasitol., 16, 243, 10.1016/0304-4017(84)90042-6 Montenegro-James, 1985, Heterologous strain immunity in bovine babesiosis using a culture-derived soluble Babesia bovis immunogen, Vet. Parasitol., 18, 321, 10.1016/0304-4017(85)90067-6 Montenegro-James, 1987, Bovine babesiosis: induction of protective immunity with culture-derived Babesia bovis and Babesia bigemina immunogens, Parasitol. Res., 74, 142, 10.1007/BF00536025 Montenegro-James, 1992, Immunization of cattle with an inactivated polyvalent vaccine against anaplasmosis and babesiosis, Ann. N. Y. Acad. Sci., 653, 112, 10.1111/j.1749-6632.1992.tb19634.x Patarroyo, 1995, Exoantigens of an attenuated strain of Babesia bovis used as a vaccine against bovine babesiosis, Vet. Parasitol., 59, 189, 10.1016/0304-4017(94)00756-3 Schetters, 1997, Vaccination of dogs against Babesia canis infection, Vet. Parasitol., 73, 35, 10.1016/S0304-4017(97)00044-7 Wright, 1985, Protective vaccination against virulent Babesia bovis with a low-molecular-weight antigen, Infect. Immun., 48, 109, 10.1128/IAI.48.1.109-113.1985 Waltisbuhl, 1987, Babesia bovis: vaccination studies with three groups of high molecular weight antigens from lysate of infected erythrocytes, Parasitol. Res., 73, 319, 10.1007/BF00531085 Goodger, 1992, Babesia bovis: analysis of and preliminary vaccination studies with a defined infected erythrocyte membrane binding antigen, Int. J. Parasitol., 22, 533, 10.1016/0020-7519(92)90156-F Timms, 1988, Failure of a recombinant Babesia bovis antigen to protect cattle against heterologous strain challenge, Res. Vet. Sci., 45, 267, 10.1016/S0034-5288(18)30947-0 Hines, 1995, Immunization of cattle with recombinant Babesia bovis merozoite surface antigen-1, Infect. Immun., 63, 349, 10.1128/IAI.63.1.349-352.1995 East, 1997, Vaccination against Babesia bovis: T cells from protected and unprotected animals show different cytokine profiles, Int. J. Parasitol., 27, 1537, 10.1016/S0020-7519(97)00141-0 Munkhjargal, 2016, Identification and characterization of profilin antigen among Babesia species as a common vaccine candidate against babesiosis, Exp. Parasitol., 166, 29, 10.1016/j.exppara.2016.03.024 Man, 2017, Evaluation of a major surface antigen of Babesia microti merozoites as a vaccine candidate against Babesia infection, Front. Microbiol., 8, 2545, 10.3389/fmicb.2017.02545