Advertisement

Genomics and Genetic Manipulation of Protozoan Parasites Affecting Farm Animals

  • Carlos E. Suarez
  • Heba F. Alzan
  • Brian M. Cooke
Chapter

Abstract

In this chapter we present a brief but state-of-the-art account of the genomics and current gene manipulation methods that can be used to improve our understanding of the genetics and the biology of an arbitrary group of 17 protozoan parasites responsible for diseases that affect animals worldwide, including babesiosis, toxoplasmosis, theileriosis, cryptosporidiosis, eimeriosis, trypanosomiasis, and trichomoniasis. Complete genomes are available for all parasites discussed, except for Besnoitia, an apicomplexan parasite responsible for dermatitis and other disorders with high infection rates, but low mortality. Dramatic differences in genome sizes are evident among the group of parasites under study, consistent with the distinct dependency of parasitic lifestyle for each organism. In addition, linear regression analysis correlating the ratios of the number of genes per genome and genome size among all the selected protozoan parasites suggests a strong association between these two parameters, in alignment with the notion that smaller protozoan genomes are generally more compact than larger genomes. A brief description of the methods for genome manipulations, including transient and stable transfections and gene editing methods, is provided. These methods, required to understand gene function and for improving control measures, have been successfully developed so far in most parasites selected. Rapid progress of genomic and gene manipulation techniques will likely result in the constant emergence of novel integrated methods for the interrogation and modification of genomes, leading to our better understanding of parasite lifestyle and, ultimately, to the rational design of improved methods for the control of animal infectious diseases.

Keywords

Transfection Gene editing Genomics Apicomplexan Protozoans 

References

  1. Aarthi S, Raj GD, Raman M, Blake D, Subramaniam C, Tomley F. Expressed sequence tags from Eimeria brunetti—preliminary analysis and functional annotation. Parasitol Res. 2011;108(4):1059–62.PubMedCrossRefGoogle Scholar
  2. AbouLaila M, Yokoyama N, Igarashi I. RNA interference (rnai) for some genes from Babesia bovis. RJAB. 2016;2:81–92. ISSN.2356:9433.Google Scholar
  3. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004;304(5669):441–5.Google Scholar
  4. Adamson R, Lyons K, Sharrard M, Kinnaird J, Swan D, Graham S, et al. Transient transfection of Theileria annulata. Mol Biochem Parasitol. 2001;114(1):53–61.PubMedCrossRefGoogle Scholar
  5. Agüero F, Abdellah KB, Tekiel V, Sánchez DO, González A. Generation and analysis of expressed sequence tags from Trypanosoma cruzi trypomastigote and amastigote cDNA libraries. Mol Biochem Parasitol. 2004;136(2):221–5.PubMedCrossRefGoogle Scholar
  6. Al-Khedery B, Allred DR. Antigenic variation in Babesia bovis occurs through segmental gene conversion of the ves multigene family, within a bidirectional locus of active transcription. Mol Microbiol. 2006;59(2):402–14.PubMedCrossRefGoogle Scholar
  7. Archer SK, Inchaustegui D, Queiroz R, Clayton C. The cell cycle regulated transcriptome of Trypanosoma brucei. PLoS One. 2011;6(3):e18425.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arjmand M, Madrakian A, Khalili G, Najafi A, Zamani Z, Akbari Z. Metabolomics-based study of logarithmic and stationary phases of promastigotes in Leishmania major by 1H NMR spectroscopy. Iran Biomed J. 2016;20(2):77.PubMedPubMedCentralGoogle Scholar
  9. Asada M, Tanaka M, Goto Y, Yokoyama N, Inoue N, Kawazu S-i. Stable expression of green fluorescent protein and targeted disruption of thioredoxin peroxidase-1 gene in Babesia bovis with the WR99210/dhfr selection system. Mol Biochem Parasitol. 2012a;181(2):162–70.PubMedCrossRefGoogle Scholar
  10. Asada M, Goto Y, Yahata K, Yokoyama N, Kawai S, Inoue N, et al. Gliding motility of Babesia bovis merozoites visualized by time-lapse video microscopy. PLoS One. 2012b;7(4):e35227.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Asada M, Yahata K, Hakimi H, Yokoyama N, Igarashi I, Kaneko O, et al. Transfection of Babesia bovis by double selection with WR99210 and blasticidin-S and its application for functional analysis of thioredoxin peroxidase-1. PLoS One. 2015;10(5):e0125993.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Atwood J, Weatherly D, Minning T, Bundy B, Cavola C, Opperdoes F, et al. The Trypanosoma cruzi proteome. Science. 2005;309(5733):473–6.PubMedCrossRefGoogle Scholar
  13. Barrett MP, Bakker BM, Breitling R. Metabolomic systems biology of trypanosomes. Parasitology. 2010;137(09):1285–90.PubMedCrossRefGoogle Scholar
  14. Bellofatto V, Cross GA. Expression of a bacterial gene in a trypanosomatid protozoan. Science. 1989;244(4909):1167–70.PubMedCrossRefGoogle Scholar
  15. Benchimol M, de Almeida LGP, Vasconcelos AT, et al. Draft genome sequence of Tritrichomonas foetus strain K. Genome Announc. 2017;5(16):e00195-17.  https://doi.org/10.1128/genomeA.00195-17.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bishop R, Shah T, Pelle R, Hoyle D, Pearson T, Haines L, et al. Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Res. 2005;33(17):5503–11.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Blake DP. Eimeria genomics: where are we now and where are we going? Vet Parasitol. 2015;212(1):68–74.PubMedCrossRefGoogle Scholar
  18. Bouzid M, Hunter PR, Chalmers RM, Tyler KM. Cryptosporidium pathogenicity and virulence. Clin Microbiol Rev. 2013;26(1):115–34.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Braun L, Cannella D, Ortet P, Barakat M, Sautel CF, Kieffer S, et al. A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog. 2010;6(5):e1000920.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bruno S, Duschak VG, Ledesma B, Ferella M, Andersson B, Guarnera EA, et al. Identification and characterization of serine proteinase inhibitors from Neospora caninum. Mol Biochem Parasitol. 2004;136(1):101–7.PubMedCrossRefGoogle Scholar
  21. Cantacessi C, Dantas-Torres F, Nolan MJ, Otranto D. The past, present, and future of Leishmania genomics and transcriptomics. Trends Parasitol. 2015;31(3):100–8.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science. 2007;315(5809):207–12.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Caumo KS, Monteiro KM, Ott TR, Maschio VJ, Wagner G, Ferreira HB, et al. Proteomic profiling of the infective trophozoite stage of Acanthamoeba polyphaga. Acta Trop. 2014;140:166–72.PubMedCrossRefGoogle Scholar
  24. Cerqueira GC, DaRocha WD, Campos PC, Zouain CS, Teixeira SM. Analysis of expressed sequence tags from Trypanosoma cruzi amastigotes. Mem Inst Oswaldo Cruz. 2005;100(4):385–9.PubMedCrossRefGoogle Scholar
  25. Cleary MD, Singh U, Blader IJ, Brewer JL, Boothroyd JC. Toxoplasma gondii asexual development: identification of developmentally regulated genes and distinct patterns of gene expression. Eukaryot Cell. 2002;1(3):329–40.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Creek DJ, Nijagal B, Kim D-H, Rojas F, Matthews KR, Barrett MP. Metabolomics guides rational development of a simplified cell culture medium for drug screening against Trypanosoma brucei. Antimicrob Agents Chemother. 2013;57(6):2768–79.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Creek DJ, Mazet M, Achcar F, Anderson J, Kim D-H, Kamour R, et al. Probing the metabolic network in bloodstream-form Trypanosoma brucei using untargeted metabolomics with stable isotope labelled glucose. PLoS Pathog. 2015;11(3):e1004689.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cruz A, Beverley SM. Gene replacement in parasitic protozoa. Nature. 1990;348(6297):171.PubMedCrossRefGoogle Scholar
  29. Cui Y, Yu L. Application of the CRISPR/Cas9 gene editing technique to research on functional genomes of parasites. Parasitol Int. 2016;65(6):641–4.PubMedCrossRefGoogle Scholar
  30. De Goeyse I, Jansen F, Madder M, Hayashida K, Berkvens D, Dobbelaere D, et al. Transfection of live, tick derived sporozoites of the protozoan Apicomplexan parasite Theileria parva. Vet Parasitol. 2015;208(3):238–41.PubMedCrossRefGoogle Scholar
  31. de Jesus JB, Mesquita-Rodrigues C, Cuervo P. Proteomics advances in the study of Leishmania parasites and leishmaniasis. Proteins and proteomics of Leishmania and Trypanosoma. Berlin: Springer; 2014. p. 323–49.CrossRefGoogle Scholar
  32. de Koning-Ward TF, Janse CJ, Waters AP. The development of genetic tools for dissecting the biology of malaria parasites. Annu Rev Microbiol. 2000;54(1):157–85.PubMedCrossRefGoogle Scholar
  33. de Miguel N, Lustig G, Twu O, Chattopadhyay A, Wohlschlegel JA, Johnson PJ. Proteome analysis of the surface of Trichomonas vaginalis reveals novel proteins and strain-dependent differential expression. Mol Cell Proteomics. 2010;9(7):1554–66.PubMedPubMedCentralCrossRefGoogle Scholar
  34. de Vries E, Corton C, Harris B, Cornelissen AW, Berriman M. Expressed sequence tag (EST) analysis of the erythrocytic stages of Babesia bovis. Vet Parasitol. 2006;138(1):61–74.PubMedCrossRefGoogle Scholar
  35. Dillon LA, Okrah K, Hughitt VK, Suresh R, Li Y, Fernandes MC, et al. Transcriptomic profiling of gene expression and RNA processing during Leishmania major differentiation. Nucleic Acids Res. 2015;43:6799–813.PubMedPubMedCentralCrossRefGoogle Scholar
  36. dos Santos ADCM, Kalume DE, Camargo R, Gómez-Mendoza DP, Correa JR, Charneau S, et al. Unveiling the Trypanosoma cruzi nuclear proteome. PLoS One. 2015;10(9):e0138667.CrossRefGoogle Scholar
  37. Drummelsmith J, Brochu V, Girard I, Messier N, Ouellette M. Proteome mapping of the protozoan parasite Leishmania and application to the study of drug targets and resistance mechanisms. Mol Cell Proteomics. 2003;2(3):146–55.PubMedCrossRefGoogle Scholar
  38. El-Sayed NM, Alarcon CM, Beck JC, Sheffield VC, Donelson JE. cDNA expressed sequence tags of Trypanosoma brucei rhodesiense provide new insights into the biology of the parasite. Mol Biochem Parasitol. 1995;73(1–2):75–90.PubMedCrossRefGoogle Scholar
  39. Elsheikha HM, Alkurashi M, Kong K, Zhu X-Q. Metabolic footprinting of extracellular metabolites of brain endothelium infected with Neospora caninum in vitro. BMC Res Notes. 2014;7(1):406.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gaji RY, Zhang D, Breathnach CC, Vaishnava S, Striepen B, Howe DK. Molecular genetic transfection of the coccidian parasite Sarcocystis neurona. Mol Biochem Parasitol. 2006;150(1):1–9.PubMedCrossRefGoogle Scholar
  41. Gawryluk RM, Chisholm KA, Pinto DM, Gray MW. Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. J Proteome. 2014;109:400–16.CrossRefGoogle Scholar
  42. Gentil LG, Lasakosvitsch F, Silveira JFD, Santos MRMD, Barbiéri CL. Analysis and chromosomal mapping of Leishmania (Leishmania) amazonensis amastigote expressed sequence tags. Mem Inst Oswaldo Cruz. 2007;102(6):707–11.PubMedCrossRefGoogle Scholar
  43. Goonewardene R, Daily J, Kaslow D, Sullivan TJ, Duffy P, Carter R, et al. Transfection of the malaria parasite and expression of firefly luciferase. Proc Natl Acad Sci. 1993;90(11):5234–6.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Gould SB, Woehle C, Kusdian G, Landan G, Tachezy J, Zimorski V, et al. Deep sequencing of Trichomonas vaginalis during the early infection of vaginal epithelial cells and amoeboid transition. Int J Parasitol. 2013;43(9):707–19.PubMedCrossRefGoogle Scholar
  45. Greif G, De Leon MP, Lamolle G, Rodriguez M, Piñeyro D, Tavares-Marques LM, et al. Transcriptome analysis of the bloodstream stage from the parasite Trypanosoma vivax. BMC Genomics. 2013;14(1):149.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hayashida K, Hara Y, Abe T, Yamasaki C, Toyoda A, Kosuge T, et al. Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation. MBio. 2012;3:e00204-212.  https://doi.org/10.1128/mBio.00204-12. PubMed: 22951932. 2012.CrossRefGoogle Scholar
  47. Howe D. Initiation of a Sarcocystis neurona expressed sequence tag (EST) sequencing project: a preliminary report. Vet Parasitol. 2001;95(2):233–9.PubMedCrossRefGoogle Scholar
  48. Howe DK, Gaji RY, Mroz-Barrett M, Gubbels M-J, Striepen B, Stamper S. Sarcocystis neurona merozoites express a family of immunogenic surface antigens that are orthologues of the Toxoplasma gondii surface antigens (SAGs) and SAG-related sequences. Infect Immun. 2005;73(2):1023–33.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Huang K-Y, Chien K-Y, Lin Y-C, Hsu W-M, Fong I-K, Huang P-J, et al. A proteome reference map of Trichomonas vaginalis. Parasitol Res. 2009;104(4):927.PubMedCrossRefGoogle Scholar
  50. Huang K-Y, Huang P-J, F-M K, Lin R, Alderete JF, Tang P. Comparative transcriptomic and proteomic analyses of Trichomonas vaginalis following adherence to fibronectin. Infect Immun. 2012;80(11):3900–11.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hublin JSN, Ryan U, Trengove R, Maker G. Metabolomic profiling of faecal extracts from Cryptosporidium parvum infection in experimental mouse models. PLoS One. 2013;8(10):e77803.CrossRefGoogle Scholar
  52. Huynh M-H, Carruthers VB. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell. 2009;8(4):530–9.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Jiang L-L, Huang B, Han H-Y, Zhao Q, Dong H, Chen Z. Comparison of the proteome of the sporutated oocysts of Eimeria tenella diclazuril sensitive strain with diclazuril resistant strain. Chin J Biotechnol. 2005;21(3):435–9.Google Scholar
  54. Johnson WC, Taus NS, Reif KE, Bohaliga GA, Kappmeyer LS, Ueti MW. Analysis of stage specific protein expression during Babesia bovis development within female Rhipicephalus microplus. J Proteome Res. 2017.  https://doi.org/10.1021/acs.jproteome.6b00947.
  55. Kepczynski M, Róg T. Functionalized lipids and surfactants for specific applications. Biochim Biophys Acta Biomembr. 2016;1858(10):2362–79.CrossRefGoogle Scholar
  56. Kim K, Weiss LM. Toxoplasma gondii: the model apicomplexan. Int J Parasitol Parasites. 2004;34(3):423–32.CrossRefGoogle Scholar
  57. Kim K, Soldati D, Boothroyd JC. Gene replacement in Toxoplasma gondii with chloramphenicol acetyltransferase as selectable marker. Science. 1993;262:911.PubMedCrossRefGoogle Scholar
  58. Kishima M, Dolan T, Njamunggeh R, Nkonge C, Spooner P. Humoral immune responses to Theileria parva in cattle as measured by two-dimensional western blotting. Parasitol Res. 1995;81(4):334–42.PubMedCrossRefGoogle Scholar
  59. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog. 2010;6(9):e1001090.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kolev NG, Tschudi C, Ullu E. RNA interference in protozoan parasites: achievements and challenges. Eukaryot Cell. 2011;10(9):1156–63.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kong H-H, Hwang M-Y, Kim H-K, Chung D-I. Expressed sequence tags (ESTs) analysis of Acanthamoeba healyi. Korean J Parasitol. 2001;39(2):151–60.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kovarova J. Unravelling metabolism of Leishmania by metabolomics: University of Glasgow; 2016.Google Scholar
  63. Kumar A, Misra P, Sisodia B, Shasany AK, Sundar S, Dube A. Mass spectrometry-based proteomic analysis of Leishmania donovani soluble proteins in Indian clinical isolate. Pathog Dis. 2014;70(1):84–7.PubMedCrossRefGoogle Scholar
  64. Laban A, Wirth DF. Transfection of Leishmania enriettii and expression of chloramphenicol acetyltransferase gene. Proc Natl Acad Sci. 1989;86(23):9119–23.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lal K, Bromley E, Oakes R, Prieto JH, Sanderson SJ, Kurian D, et al. Proteomic comparison of four Eimeria tenella life-cycle stages: Unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite. Proteomics. 2009;9(19):4566–76.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lander ES. The heroes of CRISPR. Cell. 2016;164(1):18–28.PubMedCrossRefGoogle Scholar
  67. Lau AO. An overview of the Babesia, Plasmodium and Theileria genomes: a comparative perspective. Mol Biochem Parasitol. 2009;164(1):1–8.PubMedCrossRefGoogle Scholar
  68. Lau AO, Tibbals DL, McElwain TF. Babesia bovis: the development of an expression oligonucleotide microarray. Exp Parasitol. 2007;117(1):93–8.PubMedCrossRefGoogle Scholar
  69. Laughery JM, Lau AO, White SN, Howell JM, Suarez CE. Babesia bovis: transcriptional analysis of rRNA gene unit expression. Exp Parasitol. 2009;123(1):45–50.PubMedCrossRefGoogle Scholar
  70. Lee MG-S, Van der Ploeg LH. Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei. Science. 1990;250(4987):1583–8.PubMedCrossRefGoogle Scholar
  71. Lee EG, Kim JH, Shin YS, Shin GW, Suh MD, Kim DY, et al. Establishment of a two-dimensional electrophoresis map for Neospora caninum tachyzoites by proteomics. Proteomics. 2003;3(12):2339–50.PubMedCrossRefGoogle Scholar
  72. Lee E-G, Kim J-H, Shin Y-S, Shin G-W, Kim Y-H, Kim G-S, et al. Two-dimensional gel electrophoresis and immunoblot analysis of Neospora caninum tachyzoites. J Vet Sci. 2004;5(2):139–46.PubMedGoogle Scholar
  73. Lee E-G, Kim J-H, Shin Y-S, Shin G-W, Kim Y-R, Palaksha K, et al. Application of proteomics for comparison of proteome of Neospora caninum and Toxoplasma gondii tachyzoites. J Chromatogr B. 2005;815(1):305–14.CrossRefGoogle Scholar
  74. Levick MP, Blackwell JM, Connor V, Coulson RM, Miles A, Smith HE, et al. An expressed sequence tag analysis of a full-length, spliced-leader cDNA library from Leishmania major promastigotes. Mol Biochem Parasitol. 1996;76(1–2):345–8.PubMedCrossRefGoogle Scholar
  75. Li L, Brunk BP, Kissinger JC, Pape D, Tang K, Cole RH, et al. Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 2003;13(3):443–54.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Li Y, Shah-Simpson S, Okrah K, Belew AT, Choi J, Caradonna KL, et al. Transcriptome remodeling in Trypanosoma cruzi and human cells during intracellular infection. PLoS Pathog. 2016;12(4):e1005511.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lv Z, Wu Z, Zhang L, Ji P, Cai Y, Luo S, et al. Genome mining offers a new starting point for parasitology research. Parasitol Res. 2015;114(2):399–409.PubMedCrossRefGoogle Scholar
  78. Ma D, Liu F. Genome editing and its applications in model organisms. Genomics Proteomics Bioinformatics. 2015;13(6):336–44.PubMedCrossRefGoogle Scholar
  79. Manger ID, Hehl A, Parmley S, Sibley LD, Marra M, Hillier L, et al. Expressed sequence tag analysis of the bradyzoite stage of Toxoplasma gondii: identification of developmentally regulated genes. Infect Immun. 1998;66(4):1632–7.PubMedPubMedCentralGoogle Scholar
  80. Mauzy MJ, Enomoto S, Lancto CA, Abrahamsen MS, Rutherford MS. The Cryptosporidium parvum transcriptome during in vitro development. PLoS One. 2012;7(3):e31715.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Meissner M, Agop-Nersesian C, Sullivan WJ. Molecular tools for analysis of gene function in parasitic microorganisms. Appl Microbiol Biotechnol. 2007;75(5):963–75.PubMedCrossRefGoogle Scholar
  82. Menezes JPBD, Almeida TFD, Petersen ALOA, Guedes CES, Mota M, Lima JGB, et al. Proteomic analysis reveals differentially expressed proteins in macrophages infected with Leishmania amazonensis or Leishmania major. Microb Infect. 2013;15(8):579–91.CrossRefGoogle Scholar
  83. Mesplet M, Palmer GH, Pedroni MJ, Echaide I, Florin-Christensen M, Schnittger L, et al. Genome-wide analysis of peptidase content and expression in a virulent and attenuated Babesia bovis strain pair. Mol Biochem Parasitol. 2011;179(2):111–3.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Min W, Lillehoj HS, Ashwell CM, Van Tassell CP, Dalloul RA, Matukumalli LK, et al. Expressed sequence tag analysis of Eimeria-stimulated intestinal intraepithelial lymphocytes in chickens. Mol Biotechnol. 2005;30(2):143–9.PubMedCrossRefGoogle Scholar
  85. Miska K, Fetterer R, Rosenberg G. Analysis of transcripts from intracellular stages of Eimeria acervulina using expressed sequence tags. J Parasitol. 2008;94(2):462–6.PubMedCrossRefGoogle Scholar
  86. Mogollon CM, van Pul FJ, Imai T, Ramesar J, Chevalley-Maurel S, de Roo GM, et al. Rapid generation of marker-free P. falciparum fluorescent reporter lines using modified CRISPR/Cas9 constructs and selection protocol. PLoS One. 2016;11(12):e0168362.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nene V, Lee D, Kang’a S, Skilton R, Shah T, de Villiers E, et al. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem Mol Biol. 2004;34(10):1117–28.PubMedCrossRefGoogle Scholar
  88. Ng JSY, Ryan U, Trengove RD, Maker GL. Development of an untargeted metabolomics method for the analysis of human faecal samples using Cryptosporidium-infected samples. Mol Biochem Parasitol. 2012;185(2):145–50.PubMedCrossRefGoogle Scholar
  89. Ngô HM, Yang M, Joiner KA. Are rhoptries in Apicomplexan parasites secretory granules or secretory lysosomal granules? Mol Microbiol. 2004;52(6):1531–41.PubMedCrossRefGoogle Scholar
  90. Oakes RD, Kurian D, Bromley E, Ward C, Lal K, Blake DP, et al. The rhoptry proteome of Eimeria tenella sporozoites. Int J Parasitol. 2013;43(2):181–8.PubMedCrossRefGoogle Scholar
  91. Oura C, Tait A, Shiels B. Theileria annulata: identification, by differential mRNA display, of modulated host and parasite gene expression in cell lines that are competent or attenuated for differentiation to the merozoite. Exp Parasitol. 2001;98(1):10–9.PubMedCrossRefGoogle Scholar
  92. Oura CA, McKellar S, Swan DG, Okan E, Shiels BR. Infection of bovine cells by the protozoan parasite Theileria annulata modulates expression of the ISGylation system. Cell Microbiol. 2006;8(2):276–88.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Oyhenart J, Breccia JD. Evidence for repeated gene duplications in Tritrichomonas foetus supported by EST analysis and comparison with the Trichomonas vaginalis genome. Vet Parasitol. 2014;206(3–4):267–76.PubMedCrossRefGoogle Scholar
  94. Paba J, Santana JM, Teixeira AR, Fontes W, Sousa MV, Ricart CA. Proteomic analysis of the human pathogen Trypanosoma cruzi. Proteomics. 2004;4(4):1052–9.PubMedCrossRefGoogle Scholar
  95. Panigrahi AK, Ogata Y, Zíková A, Anupama A, Dalley RA, Acestor N, et al. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics. 2009;9(2):434–50.PubMedPubMedCentralCrossRefGoogle Scholar
  96. Pedroni MJ, Sondgeroth KS, Gallego-Lopez GM, Echaide I, Lau AO. Comparative transcriptome analysis of geographically distinct virulent and attenuated Babesia bovis strains reveals similar gene expression changes through attenuation. BMC Genomics. 2013;14(1):763.PubMedPubMedCentralCrossRefGoogle Scholar
  97. Peng Z, Omaruddin R, Bateman E. Stable transfection of Acanthamoeba castellanii. Biochim Biophys Acta. 2005;1743(1):93–100.PubMedCrossRefGoogle Scholar
  98. Peng D, Kurup SP, Yao PY, Minning TA, Tarleton RL. CRISPR-Cas9-mediated single-gene and gene family disruption in Trypanosoma cruzi. MBio. 2015;6(1):e02097–14.Google Scholar
  99. Qin M, Liu XY, Tang XM, Suo JX, Tao GR, Suo X. Transfection of Eimeria mitis with yellow fluorescent protein as reporter and the endogenous development of the transgenic parasite. PLoS One. 2014;9(12):e114188.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Rachinsky A, Guerrero FD, Scoles GA. Proteomic profiling of Rhipicephalus (Boophilus) microplus midgut responses to infection with Babesia bovis. Vet Parasitol. 2008;152(3):294–313.PubMedCrossRefGoogle Scholar
  101. Radke JR, Behnke MS, Mackey AJ, Radke JB, Roos DS, White MW. The transcriptome of Toxoplasma gondii. BMC Biol. 2005;3(1):26.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Könen-Waisman S, et al. Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Pathog. 2012;8(3):e1002567.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Savadye D. Establishment of an expressed sequence-tag database, mapping of theileria parva schizont cDNAs and molecular characterisation of a parasite-specific protein: University of Zimbabwe; 1999.Google Scholar
  104. Saxena A, Lahav T, Holland N, Aggarwal G, Anupama A, Huang Y, et al. Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Mol Biochem Parasitol. 2007;152(1):53–65.PubMedCrossRefGoogle Scholar
  105. Scheltema RA, Decuypere S, T'kindt R, Dujardin J-C, Coombs GH, Breitling R. The potential of metabolomics for Leishmania research in the post-genomics era. Parasitology. 2010;137(09):1291–302.PubMedCrossRefGoogle Scholar
  106. Schwarz RS, Fetterer RH, Rosenberg GH, Miska KB. Coccidian merozoite transcriptome analysis from Eimeria maxima in comparison to Eimeria tenella and Eimeria acervulina. J Parasitol. 2010;96(1):49–57.PubMedCrossRefGoogle Scholar
  107. Shen B, Brown KM, Lee TD, Sibley LD. Efficient gene disruption in diverse strains of Toxoplasma gondii using CRISPR/CAS9. MBio. 2014;5(3):e01114-14.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Shin Y-S, Shin G-W, Kim Y-R, Lee E-Y, Yang H-H, Palaksha K, et al. Comparison of proteome and antigenic proteome between two Neospora caninum isolates. Vet Parasitol. 2005;134(1):41–52.PubMedCrossRefGoogle Scholar
  109. Shompole S, McElwain TF, Jasmer DP, Hines SA, Katende J, Musoke AJ, et al. Identification of Babesia bigemina infected erythrocyte surface antigens containing epitopes conserved among strains. Parasite Immunol. 1994;16(3):119–27.PubMedCrossRefGoogle Scholar
  110. Siddiki A. Sporozoite proteome analysis of Cryptosporidium parvum by one-dimensional SDS-PAGE and liquid chromatography tandem mass spectrometry. J Vet Sci. 2013;14(2):107–14.PubMedPubMedCentralCrossRefGoogle Scholar
  111. Siddiki A, Wastling JM. Charting the proteome of Cryptosporidium parvum sporozoites using sequence similarity-based BLAST searching. J Vet Sci. 2009;10(3):203–10.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sidik SM, Huet D, Ganesan SM, Huynh MH, Wang T, Nasamu AS, Thiru P, Saeij JP, Carruthers VB, Niles JC, Lourido S. A genome-wide CRISPR screen in Toxoplasma identifies essential Apicomplexan genes. Cell. 2016;166(6):1423–1435.e12.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Silva MG, Graça T, Suarez CE, Knowles DP. Repertoire of Theileria equi immunodominant antigens bound by equine antibody. Mol Biochem Parasitol. 2013;188(2):109–15.PubMedCrossRefGoogle Scholar
  114. Silva JC, Cornillot E, McCracken C, Usmani-Brown S, Dwivedi A, Ifeonu OO, et al. Genome-wide diversity and gene expression profiling of Babesia microti isolates identify polymorphic genes that mediate host-pathogen interactions. Sci Rep. 2016a;6:35284.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Silva MG, Knowles DP, Suarez CE. Identification of interchangeable cross-species function of elongation factor-1 alpha promoters in Babesia bigemina and Babesia bovis. Parasit Vectors. 2016b;9(1):576.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Singh S, Dubey VK. Quantitative proteome analysis of Leishmania donovani under Spermidine starvation. PLoS One. 2016;11(4):e0154262.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Smolarz B, Wilczyński J, Nowakowska D. DNA repair mechanisms and Toxoplasma gondii infection. Arch Microbiol. 2014;196(1):1–8.PubMedCrossRefGoogle Scholar
  118. Snelling WJ, Lin Q, Moore JE, Millar BC, Tosini F, Pozio E, et al. Proteomics analysis and protein expression during sporozoite excystation of Cryptosporidium parvum (Coccidia, Apicomplexa). Mol Cell Proteomics. 2007;6(2):346–55.PubMedCrossRefGoogle Scholar
  119. Soldati D, Boothroyd JC. Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science. 1993;260:349.PubMedCrossRefGoogle Scholar
  120. Strong WB, Nelson RG. Preliminary profile of the Cryptosporidium parvum genome: an expressed sequence tag and genome survey sequence analysis. Mol Biochem Parasitol. 2000;107(1):1–32.PubMedCrossRefGoogle Scholar
  121. Suarez CE, McElwain TF. Transient transfection of purified Babesia bovis merozoites. Exp Parasitol. 2008;118(4):498–504.PubMedCrossRefGoogle Scholar
  122. Suarez CE, McElwain TF. Stable expression of a GFP-BSD fusion protein in Babesia bovis merozoites. Int J Parasitol. 2009;39(3):289–97.PubMedCrossRefGoogle Scholar
  123. Suarez CE, McElwain TF. Transfection systems for Babesia bovis: a review of methods for the transient and stable expression of exogenous genes. Vet Parasitol. 2010;167(2):205–15.PubMedCrossRefGoogle Scholar
  124. Suarez CE, Palmer GH, Florin-Christensen M, Hines SA, Hötzel I, McElwain TF. Organization, transcription, and expression of rhoptry associated protein genes in the Babesia bigemina rap-1 locus. Mol Biochem Parasitol. 2003;127(2):101–12.PubMedCrossRefGoogle Scholar
  125. Suarez CE, Palmer GH, LeRoith T, Florin-Christensen M, Crabb B, McElwain TF. Intergenic regions in the rhoptry associated protein-1 (rap-1) locus promote exogenous gene expression in Babesia bovis. Int J Parasitol Parasites. 2004;34(10):1177–84.CrossRefGoogle Scholar
  126. Suarez CE, Norimine J, Lacy P, McElwain TF. Characterization and gene expression of Babesia bovis elongation factor-1α. Int J Parasitol Parasites. 2006;36(8):965–73.CrossRefGoogle Scholar
  127. Suarez C, Lacy P, Laughery J, Gonzalez MG, McElwain T. Optimization of Babesia bovis transfection methods. Parassitologia. 2007;49:67.PubMedGoogle Scholar
  128. Suarez CE, Johnson WC, Herndon DR, Laughery JM, Davis WC. Integration of a transfected gene into the genome of Babesia bovis occurs by legitimate homologous recombination mechanisms. Mol Biochem Parasitol. 2015;202(2):23–8.PubMedCrossRefGoogle Scholar
  129. Sugimoto C, Conrad PA, Mutharia L, Dolan T, Brown W, Goddeeris B, et al. Phenotypic characterization of Theileria parva schizonts by two-dimensional gel electrophoresis. Parasitol Res. 1989a;76(1):1–7.PubMedCrossRefGoogle Scholar
  130. Sugimoto C, Mutharia LM, Conrad PA, Dolan TT, Brown WC, Goddeeris BM, et al. Protein changes in bovine lymphoblastoid cells induced by infection with the intracellular parasite Theileria parva. Mol Biochem Parasitol. 1989b;37(2):159–69.PubMedCrossRefGoogle Scholar
  131. Sugimoto C, Mutharia L, Brown W, Pearson T, Dolan T, Conrad PA. Analysis of Theileria parva immunodominant schizont surface antigen by two-dimensional polyacrylamide gel electrophoresis and immunoblotting. Parasitol Res. 1992;78(1):82–5.PubMedCrossRefGoogle Scholar
  132. Sundberg L-R, Pulkkinen K. Genome size evolution in macroparasites. Int J Parasitol. 2015;45(5):285–8.PubMedCrossRefGoogle Scholar
  133. Ten Asbroek AL, Ouellette M, Borst P. Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature. 1990;348:174–5.PubMedCrossRefGoogle Scholar
  134. Urbaniak MD, Guther MLS, Ferguson MA. Comparative SILAC proteomic analysis of Trypanosoma brucei bloodstream and procyclic lifecycle stages. PLoS One. 2012;7(5):e36619.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Van Dijk M, Waters A, Janse C. Stable transfection of malaria parasite blood stages. Science. 1995;268(5215):1358.PubMedCrossRefGoogle Scholar
  136. Veras PST, Bezerra de Menezes JP. Using proteomics to understand how Leishmania parasites survive inside the host and establish infection. Int J Mol Sci. 2016;17(8):1270.PubMedCentralCrossRefGoogle Scholar
  137. Verdun RE, Di Paolo N, Urmenyi TP, Rondinelli E, Frasch AC, Sanchez DO. Gene discovery through expressed sequence tag sequencing in Trypanosoma cruzi. Infect Immun. 1998;66(11):5393–8.PubMedPubMedCentralGoogle Scholar
  138. Vichido R, Falcon A, Ramos JA, Alvarez A, Figueroa JV, Norimine J, et al. Expression analysis of heat shock protein 20 and Rhoptry-associated protein 1a in sexual stages and Kinetes of Babesia bigemina. Ann N Y Acad Sci. 2008;1149(1):136–40.PubMedCrossRefGoogle Scholar
  139. Vinayak S, Pawlowic MC, Sateriale A, Brooks CF, Studstill CJ, Bar-Peled Y, et al. Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature. 2015;523(7561):477–80.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Westrop GD, Williams RA, Wang L, Zhang T, Watson DG, Silva AM, et al. Metabolomic analyses of Leishmania reveal multiple species differences and large differences in amino acid metabolism. PLoS One. 2015;10(9):e0136891.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Witschi M, Xia D, Sanderson S, Baumgartner M, Wastling J, Dobbelaere D. Proteomic analysis of the Theileria annulata schizont. Int J Parasitol Parasites. 2013;43(2):173–80.CrossRefGoogle Scholar
  142. Woehle C, Kusdian G, Radine C, Graur D, Landan G, Gould SB. The parasite Trichomonas vaginalis expresses thousands of pseudogenes and long non-coding RNAs independently from functional neighbouring genes. BMC Genomics. 2014;15(1):906.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Wright AV, Nuñez JK, Doudna JA. Biology and applications of CRISPR systems: harnessing nature’s toolbox for genome engineering. Cell. 2016;164(1):29–44.PubMedCrossRefGoogle Scholar
  144. Xia D, Sanderson SJ, Jones AR, Prieto JH, Yates JR, Bromley E, et al. The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol. 2008;9(7):R116.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, et al. The genome of Cryptosporidium hominis. Nature. 2004;431(7012):1107–12.PubMedCrossRefGoogle Scholar
  146. Zhang W-W, Matlashewski G. CRISPR-Cas9-mediated genome editing in Leishmania donovani. MBio. 2015;6(4):e00861-15.PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zhang H, Guo F, Zhou H, Zhu G. Transcriptome analysis reveals unique metabolic features in the Cryptosporidium parvum Oocysts associated with environmental survival and stresses. BMC Genomics. 2012;13(1):647.PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zhou C-X, Zhou D-H, Elsheikha HM, Liu G-X, Suo X, Zhu X-Q. Global metabolomic profiling of mice brains following experimental infection with the cyst-forming Toxoplasma gondii. PLoS One. 2015;10(10):e0139635.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhou C-X, Zhou D-H, Elsheikha HM, Zhao Y, Suo X, Zhu X-Q. Metabolomic profiling of mice serum during toxoplasmosis progression using liquid chromatography-mass spectrometry. Sci Rep. 2016;6:19557.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Carlos E. Suarez
    • 1
    • 2
  • Heba F. Alzan
    • 1
    • 3
  • Brian M. Cooke
    • 4
  1. 1.Department of Veterinary Microbiology and PathologyWashington State UniversityPullmanUSA
  2. 2.Animal Disease Research UnitARS-USDAPullmanUSA
  3. 3.Parasitology and Animal Diseases DepartmentNational Research CenterCairoEgypt
  4. 4.Department of MicrobiologyMonash UniversityClaytonAustralia

Personalised recommendations