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BMC genomics2012; 13; 603; doi: 10.1186/1471-2164-13-603

Comparative genomic analysis and phylogenetic position of Theileria equi.

Abstract: Transmission of arthropod-borne apicomplexan parasites that cause disease and result in death or persistent infection represents a major challenge to global human and animal health. First described in 1901 as Piroplasma equi, this re-emergent apicomplexan parasite was renamed Babesia equi and subsequently Theileria equi, reflecting an uncertain taxonomy. Understanding mechanisms by which apicomplexan parasites evade immune or chemotherapeutic elimination is required for development of effective vaccines or chemotherapeutics. The continued risk of transmission of T. equi from clinically silent, persistently infected equids impedes the goal of returning the U. S. to non-endemic status. Therefore comparative genomic analysis of T. equi was undertaken to: 1) identify genes contributing to immune evasion and persistence in equid hosts, 2) identify genes involved in PBMC infection biology and 3) define the phylogenetic position of T. equi relative to sequenced apicomplexan parasites. Results: The known immunodominant proteins, EMA1, 2 and 3 were discovered to belong to a ten member gene family with a mean amino acid identity, in pairwise comparisons, of 39%. Importantly, the amino acid diversity of EMAs is distributed throughout the length of the proteins. Eight of the EMA genes were simultaneously transcribed. As the agents that cause bovine theileriosis infect and transform host cell PBMCs, we confirmed that T. equi infects equine PBMCs, however, there is no evidence of host cell transformation. Indeed, a number of genes identified as potential manipulators of the host cell phenotype are absent from the T. equi genome. Comparative genomic analysis of T. equi revealed the phylogenetic positioning relative to seven apicomplexan parasites using deduced amino acid sequences from 150 genes placed it as a sister taxon to Theileria spp. Conclusions: The EMA family does not fit the paradigm for classical antigenic variation, and we propose a novel model describing the role of the EMA family in persistence. T. equi has lost the putative genes for host cell transformation, or the genes were acquired by T. parva and T. annulata after divergence from T. equi. Our analysis identified 50 genes that will be useful for definitive phylogenetic classification of T. equi and closely related organisms.
Publication Date: 2012-11-09 PubMed ID: 23137308PubMed Central: PMC3505731DOI: 10.1186/1471-2164-13-603Google Scholar: Lookup
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  • Journal Article
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  • N.I.H.
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Summary

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The research article elaborates on a comparative genomic analysis and phylogenetic positioning of Theileria equi, an arthropod-carried parasite known to cause persistent diseases and deaths in humans and animals. Focused on better understanding the parasite’s evasive mechanisms against immune or chemotherapeutic measures, the study presents findings on its genetics, infection biology and phylogenetic relationship with other parasites in its group.

Study Objectives and Goals

  • The research had three major objectives: Firstly, the identification of genes in T. equi that contribute to the evasion of immune responses and sustaining persistent infections in host bodies was targeted.
  • Secondly, the study aimed at identifying genes implicated in the infection cycle within peripheral blood mononuclear cells (PBMCs).
  • Lastly, the researchers sought to compile a phylogenetic overview of Theileria equi, by positioning it relative to other similar parasites that have their genome sequences already determined.

Detailed Findings and Propositions

  • The research led to the finding that the immunodominant proteins -EMA1, 2, and 3 -belong to a ten-member gene family, with an average pairwise amino acid identity of 39%. These findings highlight the unique properties surrounding the EMA family that deviates from classical antigenic variation, prompting scientists to propose a new model for understanding the family’s role in maintaining infections.
  • Unlike bovine theileriosis-causing agents that infect and transform host cell PBMCs, T. equi was found to infect equine PBMCs without transformation. Several genes that are potential manipulators of host cell phenotype are also absent in the T. equi genome.
  • Phylogenetically, T. equi was concluded to be a sister taxon to Theileria species, based on comparisons using 150 deduced amino acid sequences.
  • The comparative genomic analysis points out the absence of genes for host cell transformation in T. equi. It suggests that these genes were either lost over time or acquired by T. parva and T. annulata post their evolution from T. equi. The study also identifies 50 genes useful for the definitive phylogenetic classification of Theileria equi and closely related organisms.

Cite This Article

APA
Kappmeyer LS, Thiagarajan M, Herndon DR, Ramsay JD, Caler E, Djikeng A, Gillespie JJ, Lau AO, Roalson EH, Silva JC, Silva MG, Suarez CE, Ueti MW, Nene VM, Mealey RH, Knowles DP, Brayton KA. (2012). Comparative genomic analysis and phylogenetic position of Theileria equi. BMC Genomics, 13, 603. https://doi.org/10.1186/1471-2164-13-603

Publication

ISSN: 1471-2164
NlmUniqueID: 100965258
Country: England
Language: English
Volume: 13
Pages: 603

Researcher Affiliations

Kappmeyer, Lowell S
  • Animal Disease Research Unit, Agricultural Research Service, USDA, Pullman, WA 99164-7030, USA.
Thiagarajan, Mathangi
    Herndon, David R
      Ramsay, Joshua D
        Caler, Elisabet
          Djikeng, Appolinaire
            Gillespie, Joseph J
              Lau, Audrey Ot
                Roalson, Eric H
                  Silva, Joana C
                    Silva, Marta G
                      Suarez, Carlos E
                        Ueti, Massaro W
                          Nene, Vishvanath M
                            Mealey, Robert H
                              Knowles, Donald P
                                Brayton, Kelly A

                                  MeSH Terms

                                  • Animals
                                  • Cattle
                                  • Chromosome Mapping
                                  • Chromosomes / genetics
                                  • Chromosomes / metabolism
                                  • Comparative Genomic Hybridization
                                  • Energy Metabolism / genetics
                                  • Genome, Protozoan
                                  • Leukocytes, Mononuclear / immunology
                                  • Leukocytes, Mononuclear / metabolism
                                  • Phospholipids / metabolism
                                  • Phylogeny
                                  • Protozoan Proteins / genetics
                                  • Theileria / classification
                                  • Theileria / genetics
                                  • Theileriasis / genetics
                                  • Theileriasis / metabolism
                                  • Theileriasis / parasitology

                                  Grant Funding

                                  • HHSN272200900040C / PHS HHS
                                  • R01AI017828 / NIAID NIH HHS
                                  • R01AI59118 / NIAID NIH HHS

                                  References

                                  This article includes 81 references
                                  1. Schwint ON, Knowles DP, Ueti MW, Kappmeyer LS, Scoles GA. Transmission of Babesia caballi by Dermacentor nitens (Acari: Ixodidae) is restricted to one generation in the absence of alimentary reinfection on a susceptible equine host.. J Med Entomol 2008 Nov;45(6):1152-5.
                                  2. Ueti MW, Palmer GH, Scoles GA, Kappmeyer LS, Knowles DP. Persistently infected horses are reservoirs for intrastadial tick-borne transmission of the apicomplexan parasite Babesia equi.. Infect Immun 2008 Aug;76(8):3525-9.
                                    doi: 10.1128/IAI.00251-08pmc: PMC2493223pubmed: 18490466google scholar: lookup
                                  3. MAURER FD. Equine piroplasmosis--another emerging disease.. J Am Vet Med Assoc 1962 Sep 15;141:699-702.
                                    pubmed: 14471543
                                  4. Short MA, Clark CK, Harvey JW, Wenzlow N, Hawkins IK, Allred DR, Knowles DP, Corn JL, Grause JF, Hennager SG, Kitchen DL, Traub-Dargatz JL. Outbreak of equine piroplasmosis in Florida.. J Am Vet Med Assoc 2012 Mar 1;240(5):588-95.
                                    doi: 10.2460/javma.240.5.588pubmed: 22332629google scholar: lookup
                                  5. Scoles GA, Hutcheson HJ, Schlater JL, Hennager SG, Pelzel AM, Knowles DP. Equine piroplasmosis associated with Amblyomma cajennense Ticks, Texas, USA.. Emerg Infect Dis 2011 Oct;17(10):1903-5.
                                    doi: 10.3201/eid1710.101182pmc: PMC3310643pubmed: 22000367google scholar: lookup
                                  6. Traub-Dargatz JL, Short MA, Pelzel AM, Norman TE, Knowles DP. Panel on equine piroplasmosis. American Association of Equine Practitioners Dec. 4, 2010 2010.
                                  7. ProMed-mail. Equine piroplasmosis - USA (11): multi-state. ProMed-mail 2009;3:2009–20091203.4128.
                                  8. Mehlhorn H, Schein E. Redescription of Babesia equi Laveran, 1901 as Theileria equi Mehlhorn, Schein 1998.. Parasitol Res 1998 Jun;84(6):467-75.
                                    doi: 10.1007/s004360050431pubmed: 9660136google scholar: lookup
                                  9. Allsopp MT, Cavalier-Smith T, De Waal DT, Allsopp BA. Phylogeny and evolution of the piroplasms.. Parasitology 1994 Feb;108 ( Pt 2):147-52.
                                    pubmed: 8159459doi: 10.1017/s0031182000068232google scholar: lookup
                                  10. Allsopp MT, Allsopp BA. Molecular sequence evidence for the reclassification of some Babesia species.. Ann N Y Acad Sci 2006 Oct;1081:509-17.
                                    doi: 10.1196/annals.1373.076pubmed: 17135560google scholar: lookup
                                  11. Musoke AJ, Nene V. Development of recombinant antigen vaccines for the control of theileriosis.. Parassitologia 1990 Apr;32(1):73-85.
                                    pubmed: 2149448
                                  12. Morrison WI. Progress towards understanding the immunobiology of Theileria parasites.. Parasitology 2009 Oct;136(12):1415-26.
                                    doi: 10.1017/S0031182009990916pubmed: 19691866google scholar: lookup
                                  13. Schein E, Rehbein G, Voigt WP, Zweygarth E. Babesia equi (Laveran 1901) 1. Development in horses and in lymphocyte culture.. Tropenmed Parasitol 1981 Dec;32(4):223-7.
                                    pubmed: 7345686
                                  14. Knowles DP Jr, Kappmeyer LS, Perryman LE. Specific immune responses are required to control parasitemia in Babesia equi infection.. Infect Immun 1994 May;62(5):1909-13.
                                  15. Schein E. Equine babesiosis. Babesiosis of domestic animals and man pp. 197–208.
                                  16. Ueti MW, Palmer GH, Kappmeyer LS, Statdfield M, Scoles GA, Knowles DP. Ability of the vector tick Boophilus microplus to acquire and transmit Babesia equi following feeding on chronically infected horses with low-level parasitemia.. J Clin Microbiol 2005 Aug;43(8):3755-9.
                                  17. Allred DR, Carlton JM, Satcher RL, Long JA, Brown WC, Patterson PE, O'Connor RM, Stroup SE. The ves multigene family of B. bovis encodes components of rapid antigenic variation at the infected erythrocyte surface.. Mol Cell 2000 Jan;5(1):153-62.
                                    doi: 10.1016/S1097-2765(00)80411-6pubmed: 10678177google scholar: lookup
                                  18. Le Scanf C, Fandeur T, Morales-Betoulle ME, Mercereau-Puijalon O. Plasmodium falciparum: altered expressions of erythrocyte membrane-associated antigens during antigenic variation.. Exp Parasitol 1997 Feb;85(2):135-48.
                                    doi: 10.1006/expr.1996.4121pubmed: 9030664google scholar: lookup
                                  19. Hajduk SL. Antigenic variation during the developmental cycle of Trypanosoma brucei.. J Protozool 1984 Feb;31(1):41-7.
                                    pubmed: 6204043
                                  20. Lau AO, McElwain TF, Brayton KA, Knowles DP, Roalson EH. Babesia bovis: a comprehensive phylogenetic analysis of plastid-encoded genes supports green algal origin of apicoplasts.. Exp Parasitol 2009 Nov;123(3):236-43.
                                    doi: 10.1016/j.exppara.2009.07.007pubmed: 19646439google scholar: lookup
                                  21. Waller RF, McFadden GI. The apicoplast: a review of the derived plastid of apicomplexan parasites.. Curr Issues Mol Biol 2005 Jan;7(1):57-79.
                                    pubmed: 15580780
                                  22. Oborník M, Janouskovec J, Chrudimský T, Lukes J. Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again.. Int J Parasitol 2009 Jan;39(1):1-12.
                                    doi: 10.1016/j.ijpara.2008.07.010pubmed: 18822291google scholar: lookup
                                  23. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum.. Science 2003 Jan 31;299(5607):705-8.
                                    doi: 10.1126/science.1078599pubmed: 12560551google scholar: lookup
                                  24. Cilingir G, Broschat SL, Lau AO. ApicoAP: the first computational model for identifying apicoplast-targeted proteins in multiple species of Apicomplexa.. PLoS One 2012;7(5):e36598.
                                  25. Hikosaka K, Watanabe Y, Tsuji N, Kita K, Kishine H, Arisue N, Palacpac NM, Kawazu S, Sawai H, Horii T, Igarashi I, Tanabe K. Divergence of the mitochondrial genome structure in the apicomplexan parasites, Babesia and Theileria.. Mol Biol Evol 2010 May;27(5):1107-16.
                                    doi: 10.1093/molbev/msp320pubmed: 20034997google scholar: lookup
                                  26. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum.. Nature 2002 Oct 3;419(6906):498-511.
                                    doi: 10.1038/nature01097pmc: PMC3836256pubmed: 12368864google scholar: lookup
                                  27. Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, Weir W, Kerhornou A, Aslett M, Bishop R, Bouchier C, Cochet M, Coulson RM, Cronin A, de Villiers EP, Fraser A, Fosker N, Gardner M, Goble A, Griffiths-Jones S, Harris DE, Katzer F, Larke N, Lord A, Maser P, McKellar S, Mooney P, Morton F, Nene V, O'Neil S, Price C, Quail MA, Rabbinowitsch E, Rawlings ND, Rutter S, Saunders D, Seeger K, Shah T, Squares R, Squares S, Tivey A, Walker AR, Woodward J, Dobbelaere DA, Langsley G, Rajandream MA, McKeever D, Shiels B, Tait A, Barrell B, Hall N. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva.. Science 2005 Jul 1;309(5731):131-3.
                                    doi: 10.1126/science.1110418pubmed: 15994557google scholar: lookup
                                  28. Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, Hall N, Ren Q, Paulsen IT, Pain A, Berriman M, Wilson RJ, Sato S, Ralph SA, Mann DJ, Xiong Z, Shallom SJ, Weidman J, Jiang L, Lynn J, Weaver B, Shoaibi A, Domingo AR, Wasawo D, Crabtree J, Wortman JR, Haas B, Angiuoli SV, Creasy TH, Lu C, Suh B, Silva JC, Utterback TR, Feldblyum TV, Pertea M, Allen J, Nierman WC, Taracha EL, Salzberg SL, White OR, Fitzhugh HA, Morzaria S, Venter JC, Fraser CM, Nene V. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes.. Science 2005 Jul 1;309(5731):134-7.
                                    doi: 10.1126/science.1110439pubmed: 15994558google scholar: lookup
                                  29. Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa.. PLoS Pathog 2007 Oct 19;3(10):1401-13.
                                  30. Nagai A, Yokoyama N, Matsuo T, Bork S, Hirata H, Xuan X, Zhu Y, Claveria FG, Fujisaki K, Igarashi I. Growth-inhibitory effects of artesunate, pyrimethamine, and pamaquine against Babesia equi and Babesia caballi in in vitro cultures.. Antimicrob Agents Chemother 2003 Feb;47(2):800-3.
                                  31. Gaffar FR, Wilschut K, Franssen FF, de Vries E. An amino acid substitution in the Babesia bovis dihydrofolate reductase-thymidylate synthase gene is correlated to cross-resistance against pyrimethamine and WR99210.. Mol Biochem Parasitol 2004 Feb;133(2):209-19.
                                  32. Florin-Christensen J, Suarez CE, Florin-Christensen M, Hines SA, McElwain TF, Palmer GH. Phosphatidylcholine formation is the predominant lipid biosynthetic event in the hemoparasite Babesia bovis.. Mol Biochem Parasitol 2000 Feb 25;106(1):147-56.
                                    doi: 10.1016/S0166-6851(99)00209-1pubmed: 10743618google scholar: lookup
                                  33. Florin-Christensen J, Suarez CE, Florin-Christensen M, Wainszelbaum M, Brown WC, McElwain TF, Palmer GH. A unique phospholipid organization in bovine erythrocyte membranes.. Proc Natl Acad Sci U S A 2001 Jul 3;98(14):7736-41.
                                    doi: 10.1073/pnas.131580998pmc: PMC35411pubmed: 11427712google scholar: lookup
                                  34. Knowles DP, Kappmeyer LS, Perryman LE. Genetic and biochemical analysis of erythrocyte-stage surface antigens belonging to a family of highly conserved proteins of Babesia equi and Theileria species.. Mol Biochem Parasitol 1997 Dec 1;90(1):69-79.
                                    doi: 10.1016/S0166-6851(97)00150-3pubmed: 9497033google scholar: lookup
                                  35. Koenderink JB, Kavishe RA, Rijpma SR, Russel FG. The ABCs of multidrug resistance in malaria.. Trends Parasitol 2010 Sep;26(9):440-6.
                                    doi: 10.1016/j.pt.2010.05.002pubmed: 20541973google scholar: lookup
                                  36. Pao SS, Paulsen IT, Saier MH Jr. Major facilitator superfamily.. Microbiol Mol Biol Rev 1998 Mar;62(1):1-34.
                                    pmc: PMC98904pubmed: 9529885doi: 10.1128/mmbr.62.1.1-34.1998google scholar: lookup
                                  37. DeBarry JD, Kissinger JC. Jumbled genomes: missing Apicomplexan synteny.. Mol Biol Evol 2011 Oct;28(10):2855-71.
                                    doi: 10.1093/molbev/msr103pmc: PMC3176833pubmed: 21504890google scholar: lookup
                                  38. Bishop R, Musoke A, Morzaria S, Sohanpal B, Gobright E. Concerted evolution at a multicopy locus in the protozoan parasite Theileria parva: extreme divergence of potential protein-coding sequences.. Mol Cell Biol 1997 Mar;17(3):1666-73.
                                    pmc: PMC231891pubmed: 9032293doi: 10.1128/mcb.17.3.1666google scholar: lookup
                                  39. Knowles DP Jr, Perryman LE, Kappmeyer LS, Hennager SG. Detection of equine antibody to Babesia equi merozoite proteins by a monoclonal antibody-based competitive inhibition enzyme-linked immunosorbent assay.. J Clin Microbiol 1991 Sep;29(9):2056-8.
                                  40. Ikadai H, Ishida H, Sasaki M, Taniguchi K, Miyata N, Koda M, Igarashi I, Oyamada T. Molecular cloning and partial characterization of Babesia equi EMA-3.. Mol Biochem Parasitol 2006 Dec;150(2):371-3.
                                  41. Kumar S, Yokoyama N, Kim JY, Huang X, Inoue N, Xuan X, Igarashi I, Sugimoto C. Expression of Babesia equi EMA-1 and EMA-2 during merozoite developmental stages in erythrocyte and their interaction with erythrocytic membrane skeleton.. Mol Biochem Parasitol 2004 Feb;133(2):221-7.
                                  42. Skilton RA, Musoke AJ, Wells CW, Yagi Y, Nene V, Spooner PR, Gachanja J, Osaso J, Bishop RP, Morzaria SP. A 32 kDa surface antigen of Theileria parva: characterization and immunization studies.. Parasitology 2000 Jun;120 ( Pt 6):553-64.
                                    pubmed: 10874718doi: 10.1017/s0031182099005934google scholar: lookup
                                  43. Gubbels MJ, Katzer F, Hide G, Jongejan F, Shiels BR. Generation of a mosaic pattern of diversity in the major merozoite-piroplasm surface antigen of Theileria annulata.. Mol Biochem Parasitol 2000 Sep;110(1):23-32.
                                    doi: 10.1016/S0166-6851(00)00253-Xpubmed: 10989142google scholar: lookup
                                  44. Cunha CW, Kappmeyer LS, McGuire TC, Dellagostin OA, Knowles DP. Conformational dependence and conservation of an immunodominant epitope within the babesia equi erythrocyte-stage surface protein equi merozoite antigen 1.. Clin Diagn Lab Immunol 2002 Nov;9(6):1301-6.
                                  45. Allred DR, Cinque RM, Lane TJ, Ahrens KP. Antigenic variation of parasite-derived antigens on the surface of Babesia bovis-infected erythrocytes.. Infect Immun 1994 Jan;62(1):91-8.
                                    pmc: PMC186072pubmed: 8262654doi: 10.1128/iai.62.1.91-98.1994google scholar: lookup
                                  46. Shiels B, Langsley G, Weir W, Pain A, McKellar S, Dobbelaere D. Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes.. Int J Parasitol 2006 Jan;36(1):9-21.
                                    doi: 10.1016/j.ijpara.2005.09.002pubmed: 16221473google scholar: lookup
                                  47. Wright IG, Casu R, Commins MA, Dalrymple BP, Gale KR, Goodger BV, Riddles PW, Waltisbuhl DJ, Abetz I, Berrie DA. The development of a recombinant Babesia vaccine.. Vet Parasitol 1992 Sep;44(1-2):3-13.
                                    pubmed: 1441189doi: 10.1016/0304-4017(92)90138-ygoogle scholar: lookup
                                  48. Gaffar FR, Yatsuda AP, Franssen FF, de Vries E. Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1.. Infect Immun 2004 May;72(5):2947-55.
                                  49. Kocken CH, Withers-Martinez C, Dubbeld MA, van der Wel A, Hackett F, Valderrama A, Blackman MJ, Thomas AW. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion.. Infect Immun 2002 Aug;70(8):4471-6.
                                  50. Anders RF, Crewther PE, Edwards S, Margetts M, Matthew ML, Pollock B, Pye D. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi.. Vaccine 1998 Jan-Feb;16(2-3):240-7.
                                    pubmed: 9607037doi: 10.1016/s0264-410x(97)88331-4google scholar: lookup
                                  51. Kocken CH, Dubbeld MA, Van Der Wel A, Pronk JT, Waters AP, Langermans JA, Thomas AW. High-level expression of Plasmodium vivax apical membrane antigen 1 (AMA-1) in Pichia pastoris: strong immunogenicity in Macaca mulatta immunized with P. vivax AMA-1 and adjuvant SBAS2.. Infect Immun 1999 Jan;67(1):43-9.
                                    pmc: PMC96275pubmed: 9864194doi: 10.1128/iai.67.1.43-49.1999google scholar: lookup
                                  52. Healer J, Murphy V, Hodder AN, Masciantonio R, Gemmill AW, Anders RF, Cowman AF, Batchelor A. Allelic polymorphisms in apical membrane antigen-1 are responsible for evasion of antibody-mediated inhibition in Plasmodium falciparum.. Mol Microbiol 2004 Apr;52(1):159-68.
                                  53. Gaffar FR, Yatsuda AP, Franssen FF, de Vries E. A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin-related anonymous protein (TRAP) present in Plasmodium sporozoites.. Mol Biochem Parasitol 2004 Jul;136(1):25-34.
                                  54. Dolo A, Modiano D, Doumbo O, Bosman A, Sidibé T, Keita MM, Naitza S, Robson KJ, Crisanti A. Thrombospondin related adhesive protein (TRAP), a potential malaria vaccine candidate.. Parassitologia 1999 Sep;41(1-3):425-8.
                                    pubmed: 10697897
                                  55. Blagborough AM, Sinden RE. Plasmodium berghei HAP2 induces strong malaria transmission-blocking immunity in vivo and in vitro.. Vaccine 2009 Aug 20;27(38):5187-94.
                                    doi: 10.1016/j.vaccine.2009.06.069pubmed: 19596419google scholar: lookup
                                  56. Ferguson DJ, Sahoo N, Pinches RA, Bumstead JM, Tomley FM, Gubbels MJ. MORN1 has a conserved role in asexual and sexual development across the apicomplexa.. Eukaryot Cell 2008 Apr;7(4):698-711.
                                    doi: 10.1128/EC.00021-08pmc: PMC2292627pubmed: 18310354google scholar: lookup
                                  57. Jani D, Nagarkatti R, Beatty W, Angel R, Slebodnick C, Andersen J, Kumar S, Rathore D. HDP-a novel heme detoxification protein from the malaria parasite.. PLoS Pathog 2008 Apr 25;4(4):e1000053.
                                  58. Musoke A, Rowlands J, Nene V, Nyanjui J, Katende J, Spooner P, Mwaura S, Odongo D, Nkonge C, Mbogo S, Bishop R, Morzaria S. Subunit vaccine based on the p67 major surface protein of Theileria parva sporozoites reduces severity of infection derived from field tick challenge.. Vaccine 2005 Apr 27;23(23):3084-95.
                                    doi: 10.1016/j.vaccine.2004.09.039pubmed: 15811656google scholar: lookup
                                  59. Freeman JM, Kappmeyer LS, Ueti MW, McElwain TF, Baszler TV, Echaide I, Nene VM, Knowles DP. A Babesia bovis gene syntenic to Theileria parva p67 is expressed in blood and tick stage parasites.. Vet Parasitol 2010 Oct 29;173(3-4):211-8.
                                    doi: 10.1016/j.vetpar.2010.06.024pubmed: 20638797google scholar: lookup
                                  60. Graham SP, Pellé 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 EL. Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes.. Proc Natl Acad Sci U S A 2006 Feb 28;103(9):3286-91.
                                    doi: 10.1073/pnas.0511273103pmc: PMC1413922pubmed: 16492763google scholar: lookup
                                  61. Criado-Fornelio A, Martinez-Marcos A, Buling-Saraña A, Barba-Carretero JC. Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe. Part II. Phylogenetic analysis and evolutionary history.. Vet Parasitol 2003 Jun 11;114(3):173-94.
                                    doi: 10.1016/S0304-4017(03)00141-9pubmed: 12788253google scholar: lookup
                                  62. Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA. Babesia: a world emerging.. Infect Genet Evol 2012 Dec;12(8):1788-809.
                                    doi: 10.1016/j.meegid.2012.07.004pubmed: 22871652google scholar: lookup
                                  63. Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies.. Nucleic Acids Res 2003 Oct 1;31(19):5654-66.
                                    doi: 10.1093/nar/gkg770pmc: PMC206470pubmed: 14500829google scholar: lookup
                                  64. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.. Nucleic Acids Res 1997 Mar 1;25(5):955-64.
                                    pmc: PMC146525pubmed: 9023104doi: 10.1093/nar/25.5.955google scholar: lookup
                                  65. Allen JE, Majoros WH, Pertea M, Salzberg SL. JIGSAW, GeneZilla, and GlimmerHMM: puzzling out the features of human genes in the ENCODE regions.. Genome Biol 2006;7 Suppl 1(Suppl 1):S9.1-13.
                                    doi: 10.1186/gb-2006-7-s1-s1pmc: PMC1810558pubmed: 16925843google scholar: lookup
                                  66. Cawley SE, Wirth AI, Speed TP. Phat--a gene finding program for Plasmodium falciparum.. Mol Biochem Parasitol 2001 Dec;118(2):167-74.
                                    doi: 10.1016/S0166-6851(01)00363-2pubmed: 11738707google scholar: lookup
                                  67. Korf I. Gene finding in novel genomes.. BMC Bioinformatics 2004 May 14;5:59.
                                    doi: 10.1186/1471-2105-5-59pmc: PMC421630pubmed: 15144565google scholar: lookup
                                  68. Huang X, Adams MD, Zhou H, Kerlavage AR. A tool for analyzing and annotating genomic sequences.. Genomics 1997 Nov 15;46(1):37-45.
                                    doi: 10.1006/geno.1997.4984pubmed: 9403056google scholar: lookup
                                  69. Liang C, Liu L, Ji G. WebGMAP: a web service for mapping and aligning cDNA sequences to genomes.. Nucleic Acids Res 2009 Jul;37(Web Server issue):W77-83.
                                    pmc: PMC2703992pubmed: 19465381doi: 10.1093/nar/gkp389google scholar: lookup
                                  70. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments.. Genome Biol 2008 Jan 11;9(1):R7.
                                    doi: 10.1186/gb-2008-9-1-r7pmc: PMC2395244pubmed: 18190707google scholar: lookup
                                  71. Haas BJ, Wortman JR, Ronning CM, Hannick LI, Smith RK Jr, Maiti R, Chan AP, Yu C, Farzad M, Wu D, White O, Town CD. Complete reannotation of the Arabidopsis genome: methods, tools, protocols and the final release.. BMC Biol 2005 Mar 22;3:7.
                                    doi: 10.1186/1741-7007-3-7pmc: PMC1082884pubmed: 15784138google scholar: lookup
                                  72. Claudel-Renard C, Chevalet C, Faraut T, Kahn D. Enzyme-specific profiles for genome annotation: PRIAM.. Nucleic Acids Res 2003 Nov 15;31(22):6633-9.
                                    doi: 10.1093/nar/gkg847pmc: PMC275543pubmed: 14602924google scholar: lookup
                                  73. Karp PD, Paley S, Romero P. The Pathway Tools software.. Bioinformatics 2002;18 Suppl 1:S225-32.
                                  74. Ren Q, Chen K, Paulsen IT. TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels.. Nucleic Acids Res 2007 Jan;35(Database issue):D274-9.
                                    pmc: PMC1747178pubmed: 17135193doi: 10.1093/nar/gkl925google scholar: lookup
                                  75. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families.. Nucleic Acids Res 2002 Apr 1;30(7):1575-84.
                                    doi: 10.1093/nar/30.7.1575pmc: PMC101833pubmed: 11917018google scholar: lookup
                                  76. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX.. Curr Protoc Bioinformatics 2002 Aug;Chapter 2:Unit 2.3.
                                    pubmed: 18792934doi: 10.1002/0471250953.bi0203s00google scholar: lookup
                                  77. Wilgenbusch JC, Swofford D. Inferring evolutionary trees with PAUP*.. Curr Protoc Bioinformatics 2003 Feb;Chapter 6:Unit 6.4.
                                    pubmed: 18428704doi: 10.1002/0471250953.bi0604s00google scholar: lookup
                                  78. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models.. Bioinformatics 2003 Aug 12;19(12):1572-4.
                                    doi: 10.1093/bioinformatics/btg180pubmed: 12912839google scholar: lookup
                                  79. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers.. Syst Biol 2008 Oct;57(5):758-71.
                                    doi: 10.1080/10635150802429642pubmed: 18853362google scholar: lookup
                                  80. Hayashida K, Hara Y, Abe T, Yamasaki C, Toyoda A, Kosuge T, Suzuki Y, Sato Y, Kawashima S, Katayama T, Wakaguri H, Inoue N, Homma K, Tada-Umezaki M, Yagi Y, Fujii Y, Habara T, Kanehisa M, Watanabe H, Ito K, Gojobori T, Sugawara H, Imanishi T, Weir W, Gardner M, Pain A, Shiels B, Hattori M, Nene V, Sugimoto C. Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation.. mBio 2012;3(5):e00204-12.
                                    pmc: PMC3445966pubmed: 22951932doi: 10.1128/mbio.00204-12google scholar: lookup
                                  81. Cornillot E, Hadj-Kaddour K, Dassouli A, Noel B, Ranwez V, Vacherie B, Augagneur Y, Brès V, Duclos A, Randazzo S, Carcy B, Debierre-Grockiego F, Delbecq S, Moubri-Ménage K, Shams-Eldin H, Usmani-Brown S, Bringaud F, Wincker P, Vivarès CP, Schwarz RT, Schetters TP, Krause PJ, Gorenflot A, Berry V, Barbe V, Ben Mamoun C. Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti.. Nucleic Acids Res 2012 Oct;40(18):9102-14.
                                    doi: 10.1093/nar/gks700pmc: PMC3467087pubmed: 22833609google scholar: lookup

                                  Citations

                                  This article has been cited 43 times.
                                  1. Wang BH, Du LF, Zhang MZ, Xia LY, Li C, Lin ZT, Wang N, Gao WY, Ye RZ, Liu JY, Han XY, Shi WQ, Shi XY, Jiang JF, Jia N, Cui XM, Zhao L, Cao WC. Genomic Characterization of Theileria luwenshuni Strain Cheeloo.. Microbiol Spectr 2023 Aug 17;11(4):e0030123.
                                    doi: 10.1128/spectrum.00301-23pubmed: 37260375google scholar: lookup
                                  2. Grimsley M, Hicks J, Zeineldin M, Murphy G, Sigafoose T. Complete Genome Sequence of Theileria equi NVSL354.. Microbiol Resour Announc 2023 Feb 16;12(2):e0080922.
                                    doi: 10.1128/mra.00809-22pubmed: 36688717google scholar: lookup
                                  3. Rizk MA, Baghdadi HB, El-Sayed SAE, Eltaysh R, Igarashi I. Repurposing of the Malaria Box for Babesia microti in mice identifies novel active scaffolds against piroplasmosis.. Parasit Vectors 2022 Sep 19;15(1):329.
                                    doi: 10.1186/s13071-022-05430-4pubmed: 36123705google scholar: lookup
                                  4. Yam J, Bogema DR, Micallef ML, Djordjevic SP, Jenkins C. Complete Genomes of Theileria orientalis Chitose and Buffeli Genotypes Reveal within Species Translocations and Differences in ABC Transporter Content.. Pathogens 2022 Jul 15;11(7).
                                    doi: 10.3390/pathogens11070801pubmed: 35890045google scholar: lookup
                                  5. Salinas-Estrella E, Ueti MW, Lobanov VA, Castillo-Payró E, Lizcano-Mata A, Badilla C, Martínez-Ibáñez F, Mosqueda J. Serological and molecular detection of Babesia caballi and Theileria equi in Mexico: A prospective study.. PLoS One 2022;17(3):e0264998.
                                    doi: 10.1371/journal.pone.0264998pubmed: 35259206google scholar: lookup
                                  6. Schnittger L, Ganzinelli S, Bhoora R, Omondi D, Nijhof AM, Florin-Christensen M. The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: species compilation, molecular phylogeny, and evolutionary insights.. Parasitol Res 2022 May;121(5):1207-1245.
                                    doi: 10.1007/s00436-022-07424-8pubmed: 35098377google scholar: lookup
                                  7. Bastos RG, Thekkiniath J, Ben Mamoun C, Fuller L, Molestina RE, Florin-Christensen M, Schnittger L, Alzan HF, Suarez CE. Babesia microti Immunoreactive Rhoptry-Associated Protein-1 Paralogs Are Ancestral Members of the Piroplasmid-Confined RAP-1 Family.. Pathogens 2021 Oct 26;10(11).
                                    doi: 10.3390/pathogens10111384pubmed: 34832541google scholar: lookup
                                  8. Berná L, Rego N, Francia ME. The Elusive Mitochondrial Genomes of Apicomplexa: Where Are We Now?. Front Microbiol 2021;12:751775.
                                    doi: 10.3389/fmicb.2021.751775pubmed: 34721355google scholar: lookup
                                  9. Onzere CK, Fry LM, Bishop RP, Silva MG, Bastos RG, Knowles DP, Suarez CE. Theileria equi claudin like apicomplexan microneme protein contains neutralization-sensitive epitopes and interacts with components of the equine erythrocyte membrane skeleton.. Sci Rep 2021 Apr 29;11(1):9301.
                                    doi: 10.1038/s41598-021-88902-4pubmed: 33927329google scholar: lookup
                                  10. Tuvshintulga B, Nugraha AB, Mizutani T, Liu M, Ishizaki T, Sivakumar T, Xuan X, Yokoyama N, Igarashi I. Development of a stable transgenic Theileria equi parasite expressing an enhanced green fluorescent protein/blasticidin S deaminase.. Sci Rep 2021 Apr 27;11(1):9107.
                                    doi: 10.1038/s41598-021-88594-wpubmed: 33907262google scholar: lookup
                                  11. Nardini R, Bartolomé Del Pino LE, Cersini A, Manna G, Viola MR, Antognetti V, Autorino GL, Scicluna MT. Comparison of PCR-based methods for the detection of Babesia caballi and Theileria equi in field samples collected in Central Italy.. Parasitol Res 2021 Jun;120(6):2157-2164.
                                    doi: 10.1007/s00436-021-07153-4pubmed: 33855619google scholar: lookup
                                  12. Florin-Christensen M, Rodriguez AE, Suárez CE, Ueti MW, Delgado FO, Echaide I, Schnittger L. N-Glycosylation in Piroplasmids: Diversity within Simplicity.. Pathogens 2021 Jan 8;10(1).
                                    doi: 10.3390/pathogens10010050pubmed: 33429911google scholar: lookup
                                  13. Farhat S, Le P, Kayal E, Noel B, Bigeard E, Corre E, Maumus F, Florent I, Alberti A, Aury JM, Barbeyron T, Cai R, Da Silva C, Istace B, Labadie K, Marie D, Mercier J, Rukwavu T, Szymczak J, Tonon T, Alves-de-Souza C, Rouzé P, Van de Peer Y, Wincker P, Rombauts S, Porcel BM, Guillou L. Rapid protein evolution, organellar reductions, and invasive intronic elements in the marine aerobic parasite dinoflagellate Amoebophrya spp.. BMC Biol 2021 Jan 6;19(1):1.
                                    doi: 10.1186/s12915-020-00927-9pubmed: 33407428google scholar: lookup
                                  14. Tirosh-Levy S, Gottlieb Y, Fry LM, Knowles DP, Steinman A. Twenty Years of Equine Piroplasmosis Research: Global Distribution, Molecular Diagnosis, and Phylogeny.. Pathogens 2020 Nov 8;9(11).
                                    doi: 10.3390/pathogens9110926pubmed: 33171698google scholar: lookup
                                  15. Palmateer NC, Tretina K, Orvis J, Ifeonu OO, Crabtree J, Drabék E, Pelle R, Awino E, Gotia HT, Munro JB, Tallon L, Morrison WI, Daubenberger CA, Nene V, Knowles DP, Bishop RP, Silva JC. Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.. PLoS Negl Trop Dis 2020 Oct;14(10):e0008781.
                                    doi: 10.1371/journal.pntd.0008781pubmed: 33119590google scholar: lookup
                                  16. Zhao S, Wang H, Zhang S, Xie S, Li H, Zhang X, Jia L. First report of genetic diversity and risk factor analysis of equine piroplasm infection in equids in Jilin, China.. Parasit Vectors 2020 Sep 9;13(1):459.
                                    doi: 10.1186/s13071-020-04338-1pubmed: 32907616google scholar: lookup
                                  17. Kumar S, Gupta S, Mohmad A, Fular A, Parthasarathi BC, Chaubey AK. Molecular tools-advances, opportunities and prospects for the control of parasites of veterinary importance.. Int J Trop Insect Sci 2021;41(1):33-42.
                                    doi: 10.1007/s42690-020-00213-9pubmed: 32837530google scholar: lookup
                                  18. O'Connor RM, Nepveux V FJ, Abenoja J, Bowden G, Reis P, Beaushaw J, Bone Relat RM, Driskell I, Gimenez F, Riggs MW, Schaefer DA, Schmidt EW, Lin Z, Distel DL, Clardy J, Ramadhar TR, Allred DR, Fritz HM, Rathod P, Chery L, White J. A symbiotic bacterium of shipworms produces a compound with broad spectrum anti-apicomplexan activity.. PLoS Pathog 2020 May;16(5):e1008600.
                                    doi: 10.1371/journal.ppat.1008600pubmed: 32453775google scholar: lookup
                                  19. Tirosh-Levy S, Steinman A, Levy H, Katz Y, Shtilman M, Gottlieb Y. Parasite load and genotype are associated with clinical outcome of piroplasm-infected equines in Israel.. Parasit Vectors 2020 May 20;13(1):267.
                                    doi: 10.1186/s13071-020-04133-ypubmed: 32434550google scholar: lookup
                                  20. Bishop RP, Kappmeyer LS, Onzere CK, Odongo DO, Githaka N, Sears KP, Knowles DP, Fry LM. Equid infective Theileria cluster in distinct 18S rRNA gene clades comprising multiple taxa with unusually broad mammalian host ranges.. Parasit Vectors 2020 May 19;13(1):261.
                                    doi: 10.1186/s13071-020-04131-0pubmed: 32430015google scholar: lookup
                                  21. Bohaliga GAR, Johnson WC, Taus NS, Hussein HE, Bastos RG, Suarez CE, O'Connor R, Ueti MW. Identification of a putative methyltransferase gene of Babesia bigemina as a novel molecular biomarker uniquely expressed in parasite tick stages.. Parasit Vectors 2018 Aug 24;11(1):480.
                                    doi: 10.1186/s13071-018-3052-9pubmed: 30143025google scholar: lookup
                                  22. Jalovecka M, Hajdusek O, Sojka D, Kopacek P, Malandrin L. The Complexity of Piroplasms Life Cycles.. Front Cell Infect Microbiol 2018;8:248.
                                    doi: 10.3389/fcimb.2018.00248pubmed: 30083518google scholar: lookup
                                  23. Bogema DR, Micallef ML, Liu M, Padula MP, Djordjevic SP, Darling AE, Jenkins C. Analysis of Theileria orientalis draft genome sequences reveals potential species-level divergence of the Ikeda, Chitose and Buffeli genotypes.. BMC Genomics 2018 Apr 27;19(1):298.
                                    doi: 10.1186/s12864-018-4701-2pubmed: 29703152google scholar: lookup
                                  24. Ascencio ME, Florin-Christensen M, Mamoun CB, Weir W, Shiels B, Schnittger L. Cysteine Proteinase C1A Paralog Profiles Correspond with Phylogenetic Lineages of Pathogenic Piroplasmids.. Vet Sci 2018 Apr 17;5(2).
                                    doi: 10.3390/vetsci5020041pubmed: 29673170google scholar: lookup
                                  25. Lobanov VA, Peckle M, Massard CL, Brad Scandrett W, Gajadhar AA. Development and validation of a duplex real-time PCR assay for the diagnosis of equine piroplasmosis.. Parasit Vectors 2018 Mar 2;11(1):125.
                                    doi: 10.1186/s13071-018-2751-6pubmed: 29499748google scholar: lookup
                                  26. Gimenez F, Hines SA, Evanoff R, Ojo KK, Van Voorhis WC, Maly DJ, Vidadala RSR, Mealey RH. In vitro growth inhibition of Theileria equi by bumped kinase inhibitors.. Vet Parasitol 2018 Feb 15;251:90-94.
                                    doi: 10.1016/j.vetpar.2017.12.024pubmed: 29426483google scholar: lookup
                                  27. Hussein HE, Bastos RG, Schneider DA, Johnson WC, Adham FK, Davis WC, Laughery JM, Herndon DR, Alzan HF, Ueti MW, Suarez CE. The Babesia bovis hap2 gene is not required for blood stage replication, but expressed upon in vitro sexual stage induction.. PLoS Negl Trop Dis 2017 Oct;11(10):e0005965.
                                    doi: 10.1371/journal.pntd.0005965pubmed: 28985216google scholar: lookup
                                  28. Schreeg ME, Marr HS, Tarigo JL, Cohn LA, Bird DM, Scholl EH, Levy MG, Wiegmann BM, Birkenheuer AJ. Mitochondrial Genome Sequences and Structures Aid in the Resolution of Piroplasmida phylogeny.. PLoS One 2016;11(11):e0165702.
                                    doi: 10.1371/journal.pone.0165702pubmed: 27832128google scholar: lookup
                                  29. Alzan HF, Knowles DP, Suarez CE. Comparative Bioinformatics Analysis of Transcription Factor Genes Indicates Conservation of Key Regulatory Domains among Babesia bovis, Babesia microti, and Theileria equi.. PLoS Negl Trop Dis 2016 Nov;10(11):e0004983.
                                    doi: 10.1371/journal.pntd.0004983pubmed: 27832060google scholar: lookup
                                  30. Isaza JP, Alzate JF. Genome microsatellite diversity within the Apicomplexa phylum.. Mol Genet Genomics 2016 Dec;291(6):2117-2129.
                                    doi: 10.1007/s00438-016-1244-6pubmed: 27590734google scholar: lookup
                                  31. Tretina K, Pelle R, Silva JC. Cis regulatory motifs and antisense transcriptional control in the apicomplexan Theileria parva.. BMC Genomics 2016 Feb 20;17:128.
                                    doi: 10.1186/s12864-016-2444-5pubmed: 26896950google scholar: lookup
                                  32. Pedroni MJ, Vidadala RS, Choi R, Keyloun KR, Reid MC, Murphy RC, Barrett LK, Van Voorhis WC, Maly DJ, Ojo KK, Lau AO. Bumped kinase inhibitor prohibits egression in Babesia bovis.. Vet Parasitol 2016 Jan 15;215:22-8.
                                    doi: 10.1016/j.vetpar.2015.10.023pubmed: 26790733google scholar: lookup
                                  33. Jiménez D, Romero-Zuñiga JJ, Dolz G. Serosurveillance of infectious agents in equines of the Central Valley of Costa Rica.. Open Vet J 2014;4(2):107-12.
                                    pubmed: 26623349
                                  34. Baneth G, Florin-Christensen M, Cardoso L, Schnittger L. Reclassification of Theileria annae as Babesia vulpes sp. nov.. Parasit Vectors 2015 Apr 8;8:207.
                                    doi: 10.1186/s13071-015-0830-5pubmed: 25890372google scholar: lookup
                                  35. Mans BJ, Pienaar R, Latif AA. A review of Theileria diagnostics and epidemiology.. Int J Parasitol Parasites Wildl 2015 Apr;4(1):104-18.
                                    doi: 10.1016/j.ijppaw.2014.12.006pubmed: 25830110google scholar: lookup
                                  36. Bosch SS, Kronenberger T, Meissner KA, Zimbres FM, Stegehake D, Izui NM, Schettert I, Liebau E, Wrenger C. Oxidative stress control by apicomplexan parasites.. Biomed Res Int 2015;2015:351289.
                                    doi: 10.1155/2015/351289pubmed: 25722976google scholar: lookup
                                  37. Hines SA, Ramsay JD, Kappmeyer LS, Lau AO, Ojo KK, Van Voorhis WC, Knowles DP, Mealey RH. Theileria equi isolates vary in susceptibility to imidocarb dipropionate but demonstrate uniform in vitro susceptibility to a bumped kinase inhibitor.. Parasit Vectors 2015 Jan 20;8:33.
                                    doi: 10.1186/s13071-014-0611-6pubmed: 25600252google scholar: lookup
                                  38. Guidi E, Pradier S, Lebert I, Leblond A. Piroplasmosis in an endemic area: analysis of the risk factors and their implications in the control of Theileriosis and Babesiosis in horses.. Parasitol Res 2015 Jan;114(1):71-83.
                                    doi: 10.1007/s00436-014-4161-9pubmed: 25280516google scholar: lookup
                                  39. Tian ZC, Liu GY, Yin H, Luo JX, Guan GQ, Luo J, Xie JR, Shen H, Tian MY, Zheng JF, Yuan XS, Wang FF. RPS8--a new informative DNA marker for phylogeny of Babesia and Theileria parasites in China.. PLoS One 2013;8(11):e79860.
                                    doi: 10.1371/journal.pone.0079860pubmed: 24244571google scholar: lookup
                                  40. Ramsay JD, Ueti MW, Johnson WC, Scoles GA, Knowles DP, Mealey RH. Lymphocytes and macrophages are infected by Theileria equi, but T cells and B cells are not required to establish infection in vivo.. PLoS One 2013;8(10):e76996.
                                    doi: 10.1371/journal.pone.0076996pubmed: 24116194google scholar: lookup
                                  41. Cornillot E, Dassouli A, Garg A, Pachikara N, Randazzo S, Depoix D, Carcy B, Delbecq S, Frutos R, Silva JC, Sutton R, Krause PJ, Mamoun CB. Whole genome mapping and re-organization of the nuclear and mitochondrial genomes of Babesia microti isolates.. PLoS One 2013;8(9):e72657.
                                    doi: 10.1371/journal.pone.0072657pubmed: 24023759google scholar: lookup
                                  42. Bastos RG, Suarez CE, Laughery JM, Johnson WC, Ueti MW, Knowles DP. Differential expression of three members of the multidomain adhesion CCp family in Babesia bigemina, Babesia bovis and Theileria equi.. PLoS One 2013;8(7):e67765.
                                    doi: 10.1371/journal.pone.0067765pubmed: 23844089google scholar: lookup
                                  43. Hall CM, Busch JD, Scoles GA, Palma-Cagle KA, Ueti MW, Kappmeyer LS, Wagner DM. Genetic characterization of Theileria equi infecting horses in North America: evidence for a limited source of U.S. introductions.. Parasit Vectors 2013 Feb 11;6:35.
                                    doi: 10.1186/1756-3305-6-35pubmed: 23399005google scholar: lookup