Variant analysis of the sporozoite surface antigen gene reveals that asymptomatic cattle from wildlife-livestock interface areas in northern Tanzania harbour buffalo-derived T. parva.
Alleles
Animals
Animals, Wild
/ parasitology
Antigens, Surface
/ genetics
Buffaloes
/ parasitology
Cattle
Genotype
Host Specificity
Kenya
Livestock
/ parasitology
Polymorphism, Genetic
/ genetics
Sporozoites
/ genetics
Tanzania
Theileria parva
/ classification
Theileriasis
/ parasitology
Vaccination
/ veterinary
Antigen diversity
Cape Buffalo
Live vaccine
Theileria parva
Tp2
p67
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
17
06
2020
accepted:
23
09
2020
pubmed:
4
10
2020
medline:
17
12
2020
entrez:
3
10
2020
Statut:
ppublish
Résumé
Buffalo-derived Theileria parva can 'break through' the immunity induced by the infection and treatment vaccination method (ITM) in cattle. However, no such 'breakthroughs' have been reported in northern Tanzania where there has been long and widespread ITM use in pastoralist cattle, and the Cape buffalo (Syncerus caffer) is also present. We studied the exposure of vaccinated and unvaccinated cattle in northern Tanzania to buffalo-derived T. parva using p67 gene polymorphisms and compared this to its distribution in vaccinated cattle exposed to buffalo-derived T. parva in central Kenya, where vaccine 'breakthroughs' have been reported. Additionally, we analysed the CD8+ T cell target antigen Tp2 for positive selection. Our results showed that 10% of the p67 sequences from Tanzanian cattle (n = 39) had a buffalo type p67 (allele 4), an allele that is rare among East African isolates studied so far. The percentage of buffalo-derived p67 alleles observed in Kenyan cattle comprised 19% of the parasites (n = 36), with two different p67 alleles (2 and 3) of presumptive buffalo origin. The Tp2 protein was generally conserved with only three Tp2 variants from Tanzania (n = 33) and five from Kenya (n = 40). Two Tanzanian Tp2 variants and two Kenyan Tp2 variants were identical to variants present in the trivalent Muguga vaccine. Tp2 evolutionary analysis did not show evidence for positive selection within previously mapped epitope coding sites. The p67 data indicates that some ITM-vaccinated cattle are protected against disease induced by a buffalo-derived T. parva challenge in northern Tanzania and suggests that the parasite genotype may represent one factor explaining this.
Identifiants
pubmed: 33009946
doi: 10.1007/s00436-020-06902-1
pii: 10.1007/s00436-020-06902-1
pmc: PMC7578158
doi:
Substances chimiques
Antigens, Surface
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3817-3828Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : CL166/4-2
Références
Akoolo L, Pellé R, Saya R, Awino E, Nyanjui J, Taracha ELN, Kanyari P, Mwangi DM, Graham SP (2008) Evaluation of the recognition of Theileria parva vaccine candidate antigens by cytotoxic T lymphocytes from Zebu cattle. Vet Immunol Immunopathol 121(3-4):216–221. https://doi.org/10.1016/j.vetimm.2007.09.012
doi: 10.1016/j.vetimm.2007.09.012
pubmed: 17983665
Amzati GS, Djikeng A, Odongo DO, Nimpaye H, Sibeko KP, Muhigwa JBB, Madder M, Kirschvink N, Marcotty T (2019) Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa. Parasit Vectors 12(1):588. https://doi.org/10.1186/s13071-019-3848-2
doi: 10.1186/s13071-019-3848-2
pubmed: 31842995
pmcid: 6915983
Bishop R, Nene V, Staeyert J, Rowlands J, Nyanjui J, Osaso J, Morzaria S, Musoke A (2003) Immunity to East Coast fever in cattle induced by a polypeptide fragment of the major surface coat protein of Theileria parva sporozoites. Vaccine 21(11-12):1205–1212. https://doi.org/10.1016/s0264-410x(02)00621-7
doi: 10.1016/s0264-410x(02)00621-7
pubmed: 12559799
Bishop RP, Hemmink JD, Morrison WI, Weir W, Toye PG, Sitt T, Spooner PR, Musoke AJ, Skilton RA, Odongo DO (2015) The African buffalo parasite Theileria sp. (buffalo) can infect and immortalize cattle leukocytes and encodes divergent orthologues of Theileria parva antigen genes. Int J Parasitol Parasites Wildl 4(3):333–342. https://doi.org/10.1016/j.ijppaw.2015.08.006
doi: 10.1016/j.ijppaw.2015.08.006
pubmed: 26543804
pmcid: 4589832
Bishop RP, Odongo D, Ahmed J, Mwamuye M, Fry LM, Knowles DP, Nanteza A, Lubega G, Gwakisa P, Clausen PH, Obara I (2020) A review of recent research on Theileria parva: implications for the infection and treatment vaccination method for control of East Coast fever. Transbound Emerg Dis 67(Suppl 1):56–67. https://doi.org/10.1111/tbed.13325
doi: 10.1111/tbed.13325
pubmed: 32174044
Cunningham MP, Brown CGD, Burridge MJ, Irvin AD, Kirimi IM, Purnell RE, Radley DE, Wagner GG (1974) Theileriosis: the exposure of immunized cattle in a Theileria lawrencei enzootic area. Trop Anim Health Prod 6(1):39–43. https://doi.org/10.1007/BF02380747
doi: 10.1007/BF02380747
pubmed: 4213497
Cunningham MP, Joyner LP, Brown CGD, Purnell RE, Bailey KP (1973) Infection of cattle with East Coast fever by inoculation of the infective stage of Theileria parva harvested from the tick vector Rhipicephalus appendiculatus. Bull epizoot Dis Afr 21:235–238
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109
doi: 10.1038/nmeth.2109
pubmed: 22847109
pmcid: 4594756
Di Giulio G, Lynen G, Morzaria S, Oura C, Bishop R (2009) Live immunization against East Coast fever--current status. Trends Parasitol 25(2):85–92. https://doi.org/10.1016/j.pt.2008.11.007
doi: 10.1016/j.pt.2008.11.007
pubmed: 19135416
Gao F, Chen C, Arab DA, Du Z, He Y, Ho SYW (2019) EasyCodeML: a visual tool for analysis of selection using CodeML. Ecol Evol 9(7):3891–3898. https://doi.org/10.1002/ece3.5015
doi: 10.1002/ece3.5015
pubmed: 31015974
pmcid: 6467853
George JE, Pound JM, Davey RB (2004) Chemical control of ticks on cattle and the resistance of these parasites to acaricides. Parasitology 129(Suppl):S353–S366. https://doi.org/10.1017/s0031182003004682
doi: 10.1017/s0031182003004682
pubmed: 15938518
Graham SP, Pelle R, Honda Y, Mwangi DM, Tonukari NJ, Yamage M, Glew EJ, de Villiers EP, Shah T, Bishop R, Abuya E, Awino E, Gachanja J, Luyai AE, Mbwika F, Muthiani AM, Ndegwa DM, Njahira M, Nyanjui JK, Onono FO, Osaso J, Saya RM, Wildmann C, Fraser CM, Maudlin I, Gardner MJ, Morzaria SP, Loosmore S, Gilbert SC, Audonnet JC, van der Bruggen P, Nene V, Taracha ELN (2006) Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 103(9):3286–3291. https://doi.org/10.1073/pnas.0511273103
doi: 10.1073/pnas.0511273103
pubmed: 16492763
pmcid: 1413922
Gwakisa P, Kindoro F, Mwega E, Kimera S, Obara I, Ahmed J, Clausen PH, Bishop R (2020) Monitoring vaccinated cattle for induction and longevity of persistent tick-transmissible infection: implications for wider deployment of live vaccination against East Coast fever in Tanzania. Transbound Emerg Dis 67(Suppl 1):79–87. https://doi.org/10.1111/tbed.13405
doi: 10.1111/tbed.13405
pubmed: 32174035
Hayashida K et al (2012) Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation. mBio 3(5):e00204-12. https://doi.org/10.1128/mBio.00204-12
Hemmink JD, Weir W, MacHugh ND, Graham SP, Patel E, Paxton E, Shiels B, Toye PG, Morrison WI, Pelle R (2016) Limited genetic and antigenic diversity within parasite isolates used in a live vaccine against Theileria parva. Int J Parasitol 46(8):495–506. https://doi.org/10.1016/j.ijpara.2016.02.007
doi: 10.1016/j.ijpara.2016.02.007
pubmed: 27080723
pmcid: 4935670
Henson S, Bishop RP, Morzaria S, Spooner PR, Pelle R, Poveda L, Ebeling M, Küng E, Certa U, Daubenberger CA, Qi W (2012) High-resolution genotyping and mapping of recombination and gene conversion in the protozoan Theileria parva using whole genome sequencing. BMC Genomics 13:503. https://doi.org/10.1186/1471-2164-13-503
doi: 10.1186/1471-2164-13-503
pubmed: 22998600
pmcid: 3575351
Irvin AD, Mwamachi DM (1983) Clinical and diagnostic features of East Coast fever (Theileria parva) infection of cattle. Vet Rec 113(9):192–198. https://doi.org/10.1136/vr.113.9.192
doi: 10.1136/vr.113.9.192
pubmed: 6415893
Jura WGZ, Losos GJ (1980) A comparative study of the diseases in cattle caused by Theileria lawrencei and Theileria parva. 1. Clinical signs and parasitological observations. Vet Parasitol 7(4):275–286
doi: 10.1016/0304-4017(80)90047-3
Katzer F, Lizundia R, Ngugi D, Blake D, McKeever D (2011) Construction of a genetic map for Theileria parva: identification of hotspots of recombination. Int J Parasitol 41(6):669–675. https://doi.org/10.1016/j.ijpara.2011.01.001
doi: 10.1016/j.ijpara.2011.01.001
pubmed: 21310160
pmcid: 3084458
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
doi: 10.1093/molbev/msy096
pubmed: 5967553
pmcid: 5967553
Matovelo JA, et al. (2003) Induction of acquired immunity in pastoral zebu cattle against East Coast fever after natural infection by early diagnosis and early treatment Int J Appl Res Vet Med 1(2)
Mbizeni S, Potgieter FT, Troskie C, Mans BJ, Penzhorn BL, Latif AA (2013) Field and laboratory studies on Corridor disease (Theileria parva infection) in cattle population at the livestock/game interface of uPhongolo-Mkuze area, South Africa. Ticks Tick Borne Dis 4(3):227–234. https://doi.org/10.1016/j.ttbdis.2012.11.005
doi: 10.1016/j.ttbdis.2012.11.005
pubmed: 23333107
McKeever DJ et al (1994) Adoptive transfer of immunity to Theileria parva in the CD8+ fraction of responding efferent lymph. Proc Natl Acad Sci U S A 91(5):1959–1963. https://doi.org/10.1073/pnas.91.5.1959
doi: 10.1073/pnas.91.5.1959
pubmed: 8127915
pmcid: 43284
Morrison WI, Connelley T, Hemmink JD, MacHugh ND (2015) Understanding the basis of parasite strain-restricted immunity to Theileria parva. Annu Rev Anim Biosci 3:397–418. https://doi.org/10.1146/annurev-animal-022513-114152
doi: 10.1146/annurev-animal-022513-114152
pubmed: 25422856
Morrison WI, Goddeeris BM, Brown WC, Baldwin CL, Teale AJ (1989) Theileria parva in cattle: characterization of infected lymphocytes and the immune responses they provoke. Vet Immunol Immunopathol 20(3):213–237. https://doi.org/10.1016/0165-2427(89)90003-2
doi: 10.1016/0165-2427(89)90003-2
pubmed: 2497579
Mukhebi AW, Perry BD, Kruska R (1992) Estimated economics of theileriosis control in Africa. Prev Vet Med 12(1-2):73–85
doi: 10.1016/0167-5877(92)90070-V
Mukolwe L, Odongo D, Byaruhanga C, Snyman L, Sibeko-Matjila K (2020) Analysis of p67 allelic sequences reveals a subtype of allele type 1 unique to buffalo-derived Theileria parva parasites from southern Africa. PLoS One 15(6):e0231434
doi: 10.1371/journal.pone.0231434
Musoke A, Morzaria S, Nkonge C, Jones E, Nene V (1992) A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proc Natl Acad Sci U S A 89(2):514–518. https://doi.org/10.1073/pnas.89.2.514
doi: 10.1073/pnas.89.2.514
pubmed: 1731322
pmcid: 48269
Musoke A, Rowlands J, Nene V, Nyanjui J, Katende J, Spooner P, Mwaura S, Odongo D, Nkonge C, Mbogo S, Bishop R, Morzaria S (2005) Subunit vaccine based on the p67 major surface protein of Theileria parva sporozoites reduces severity of infection derived from field tick challenge. Vaccine 23(23):3084–3095. https://doi.org/10.1016/j.vaccine.2004.09.039
doi: 10.1016/j.vaccine.2004.09.039
pubmed: 15811656
Nene V, Gobright E, Bishop R, Morzaria S, Musoke A (1999) Linear peptide specificity of bovine antibody responses to p67 of Theileria parva and sequence diversity of sporozoite-neutralizing epitopes: implications for a vaccine. Infect Immun 67(3):1261–1266
doi: 10.1128/IAI.67.3.1261-1266.1999
Nene V, Musoke A, Gobright E, Morzaria S (1996) Conservation of the sporozoite p67 vaccine antigen in cattle-derived Theileria parva stocks with different cross-immunity profiles. Infect Immun 64(6):2056–2061
doi: 10.1128/IAI.64.6.2056-2061.1996
Norval RA, Lawrence JA, Young AS, Perry BD, Dolan TT, Scott J (1991) Theileria parva: influence of vector, parasite and host relationships on the epidemiology of theileriosis in southern Africa. Parasitology 102(Pt 3):347–356. https://doi.org/10.1017/s0031182000064295
doi: 10.1017/s0031182000064295
pubmed: 1907728
Nsubuga-Mutaka R (1999) ECF Immunisation in Uganda. In: Morzaria S, Williamson S (eds) Live vaccines for Theileria parva: deployment in Eastern, Central and Southern Africa. ILRI (International Livestock Research Institute), Nairobi, pp 26–29
Obara I, Ulrike S, Musoke T, Spooner PR, Jabbar A, Odongo D, Kemp S, Silva JC, Bishop RP (2015) Molecular evolution of a central region containing B cell epitopes in the gene encoding the p67 sporozoite antigen within a field population of Theileria parva. Parasitol Res 114(5):1729–1737. https://doi.org/10.1007/s00436-015-4358-6
doi: 10.1007/s00436-015-4358-6
pubmed: 25673078
pmcid: 4412645
Oura CA, Tait A, Asiimwe B, Lubega GW, Weir W (2011) Haemoparasite prevalence and Theileria parva strain diversity in Cape buffalo (Syncerus caffer) in Uganda. Vet Parasitol 175(3-4):212–219. https://doi.org/10.1016/j.vetpar.2010.10.032
doi: 10.1016/j.vetpar.2010.10.032
pubmed: 21074945
Pelle R, Graham SP, Njahira MN, Osaso J, Saya RM, Odongo DO, Toye PG, Spooner PR, Musoke AJ, Mwangi DM, Taracha ELN, Morrison WI, Weir W, Silva JC, Bishop RP (2011) Two Theileria parva CD8 T cell antigen genes are more variable in buffalo than cattle parasites, but differ in pattern of sequence diversity. PLoS One 6(4):e19015. https://doi.org/10.1371/journal.pone.0019015
doi: 10.1371/journal.pone.0019015
pubmed: 21559495
pmcid: 3084734
Radley DE et al (1975) East coast fever: 3. Chemoprophylactic immunization of cattle using oxytetracycline and a combination of theilerial strains. Vet Parasitol 1(1):51–60
doi: 10.1016/0304-4017(75)90007-2
Radley DE, Young AS, Grootenhuis JG, Cunningham MP, Dolan TT, Morzaria SP (1979) Further studies on the immunization of cattle against Theileria lawrencei by infection and chemoprophylaxis. Vet Parasitol 5(2-3):117–128
doi: 10.1016/0304-4017(79)90003-7
Sibeko KP, Geysen D, Oosthuizen MC, Matthee CA, Troskie M, Potgieter FT, Coetzer JAW, Collins NE (2010) Four p67 alleles identified in South African Theileria parva field samples. Vet Parasitol 167(2-4):244–254. https://doi.org/10.1016/j.vetpar.2009.09.026
doi: 10.1016/j.vetpar.2009.09.026
pubmed: 19836893
Sitt T, Henson S, Morrison WI, Toye P (2019) Similar levels of diversity in the gene encoding the p67 sporozoite surface protein of Theileria parva are observed in blood samples from buffalo and cattle naturally infected from buffalo. Vet Parasitol 269:21–27. https://doi.org/10.1016/j.vetpar.2019.04.006
doi: 10.1016/j.vetpar.2019.04.006
pubmed: 31079824
Sitt T, Poole EJ, Ndambuki G, Mwaura S, Njoroge T, Omondi GP, Mutinda M, Mathenge J, Prettejohn G, Morrison WI, Toye P (2015) Exposure of vaccinated and naive cattle to natural challenge from buffalo-derived Theileria parva. Int J Parasitol Parasites Wildl 4(2):244–251. https://doi.org/10.1016/j.ijppaw.2015.04.006
doi: 10.1016/j.ijppaw.2015.04.006
pubmed: 26005635
pmcid: 4437466
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
Thumbi SM et al (2013) Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology 140(14):1789–1798. https://doi.org/10.1017/S0031182013001261
doi: 10.1017/S0031182013001261
pubmed: 24001119
pmcid: 3829697
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591. https://doi.org/10.1093/molbev/msm088
doi: 10.1093/molbev/msm088
pubmed: 17483113
Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22(4):1107–1118. https://doi.org/10.1093/molbev/msi097
doi: 10.1093/molbev/msi097
pubmed: 15689528