Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa

Parasitology

Volumn 760, Issue , 2014, Pages

  Reid, Adam J ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

antigenic variation; Apicomplexa; Babesia; Eimeria; gene families; host parasite interactions; immune evasion; Plasmodium; Theileria; Toxoplasma

Indexed keywords

ANTIGENIC VARIATION; APICOMPLEXA; ARTICLE; BABESIA BIGEMINA; BABESIA BOVIS; BABESIA DIVERGENS; BABESIA MICROTI; CRYPTOSPORIDIUM PARVUM; EIMERIA; GENE CONVERSION; GENE DUPLICATION; GENE EXPRESSION; GENE STRUCTURE; HOST PARASITE INTERACTION; IMMUNE SYSTEM; MULTIGENE FAMILY; NEOSPORA CANINUM; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM CYNOMOLGI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PLASMODIUM YOELII; PROTEIN DOMAIN; PROTEIN LOCALIZATION; THEILERIA ANNULATA; THEILERIA PARVA; TOXOPLASMA GONDII; EVOLUTION; GENETICS; GENOME; GENOMICS; HUMAN; IMMUNE EVASION; IMMUNOLOGY; PHYSIOLOGY;

PROTOZOAL PROTEIN;

ANTIGENIC VARIATION; APICOMPLEXA; BIOLOGICAL EVOLUTION; GENOME, PROTOZOAN; GENOMICS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNE EVASION; MULTIGENE FAMILY; PROTOZOAN PROTEINS;

EID: 84911370512     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014001528     Document Type: Article

References (106)

1. Abrahamsen, M. S., Templeton, T. J., Enomoto, S., Abrahante, J. E., Zhu, G., Lancto, C. A., Deng, M., Liu, C., Widmer, G., Tzipori, S., Buck, G. A., Xu, P., Bankier, A. T., Dear, P. H., Konfortov, B. A., Spriggs, H. F., Iyer, L., Anantharaman, V., Aravind, L. and Kapur, V. (2004). Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441-445
2. Al-Khedery, B. and Allred, D. R. (2006). Antigenic variation in Babesia bovis occurs through segmental gene conversion of the ves multigene family, within a bidirectional locus of active transcription. Molecular Microbiology 59, 402-414
3. Allred, D. R., Carlton, J. M., Satcher, R. L., Long, J. A., Brown, W. C., Patterson, P. E., O'Connor, R. M. and Stroup, S. E. (2000). The ves multigene family of B. bovis encodes components of rapid antigenic variation at the infected erythrocyte surface. Molecular Cell 5, 153-162
4. Arredondo, S. A., Cai, M., Takayama, Y., MacDonald, N. J., Anderson, D. E., Aravind, L., Clore, G. M. and Miller, L. H. (2012). Structure of the Plasmodium 6-cysteine s48/45 domain. Proceedings of the National Academy of Sciences of the United States of America 109, 6692-6697
5. Assefa, S. (2013). De Novo Assembly of the Var Multi-Gene Family in Clinical Samples of Plasmodium Falciparum. PhD thesis, University of Cambridge, UK.
6. Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Stoeckert, C. J., Jr., Treatman, C. and Wang, H. (2009). PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Research 37, D539-543
7. Barnwell, J.W., Howard, R. J., Coon, H. G. and Miller, L. H. (1983). Splenic requirement for antigenic variation and expression of the variant antigen on the erythrocyte membrane in cloned Plasmodium knowlesi malaria. Infection and Immunity 40, 985-994
8. Bayliss, C. D., Field, D. and Moxon, E. R. (2001). The simple sequence contingency loci of Haemophilus influenzae and Neisseria meningitidis. Journal of Clinical Investigation 107, 657-662
9. Bernabeu, M., Lopez, F. J., Ferrer, M., Martin-Jaular, L., Razaname, A., Corradin, G., Maier, A. G., Del Portillo, H. A. and Fernandez-Becerra, C. (2012). Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor. Cellular Microbiology 14, 386-400
10. Blythe, J. E., Yam, X. Y., Kuss, C., Bozdech, Z., Holder, A. A., Marsh, K., Langhorne, J. and Preiser, P. R. (2008). Plasmodium Falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites. Infection and Immunity 76, 3329-3336
11. Bohne, W., Heesemann, J. and Gross, U. (1993). Induction of bradyzoite-specific Toxoplasma gondii antigens in gamma interferon-treated mouse macrophages. Infection and Immunity 61, 1141-1145
12. Borst, P. (1991). Molecular genetics of antigenic variation. Immunology Today 12, A29-33
13. Boulter, N. and Hall, R. (1999). Immunity and vaccine development in the bovine theilerioses. Advances in Parasitology 44, 41-97
14. Bozdech, Z., Llinas, M., Pulliam, B. L., Wong, E. D., Zhu, J. and DeRisi, J. L. (2003). The transcriptome of the intraerythrocytic developmental cycle of Plasmodium Falciparum. PLoS Biology 1, E5
15. Brannan, L. R., Turner, C. M. and Phillips, R. S. (1994). Malaria parasites undergo antigenic variation at high rates in vivo. Proceedings of the Royal Society B: Biological Sciences 256, 71-75
16. Brayton, K. A., Lau, A. O., Herndon, D. R., Hannick, L., Kappmeyer, L. S., Berens, S. J., Bidwell, S. L., Brown, W. C., Crabtree, J., Fadrosh, D., Feldblum, T., Forberger, H. A., Haas, B. J., Howell, J. M., Khouri, H., Koo, H., Mann, D. J., Norimine, J., Paulsen, I. T., Radune, D., Ren, Q., Smith, R. K., Jr., Suarez, C. E., White, O., Wortman, J. R., Knowles, D. P., Jr., McElwain, T. F. and Nene, V. M. (2007). Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathogens 3, 1401-1413
17. Brugat, T., Cunningham, D., Sodenkamp, J., Coomes, S., Wilson, M., Spence, P. J., Jarra, W., Thompson, J., Scudamore, C. and Langhorne, J. (2014). Sequestration and histopathology in Plasmodium chabaudi malaria are influenced by the immune response in an organ-specific manner. Cellular Microbiology 16, 687-700
18. Bultrini, E., Brick, K., Mukherjee, S., Zhang, Y., Silvestrini, F., Alano, P. and Pizzi, E. (2009). Revisiting the Plasmodium Falciparum RIFIN family: from comparative genomics to 3D-model prediction. BMC Genomics 10, 445.
19. Carlton, J. M., Angiuoli, S. V., Suh, B. B., Kooij, T.W., Pertea, M., Silva, J. C., Ermolaeva, M. D., Allen, J. E., Selengut, J. D., Koo, H. L., Peterson, J. D., Pop, M., Kosack, D. S., Shumway, M. F., Bidwell, S. L., Shallom, S. J., van Aken, S. E., Riedmuller, S. B., Feldblyum, T. V., Cho, J. K., Quackenbush, J., Sedegah, M., Shoaibi, A., Cummings, L. M., Florens, L., Yates, J. R., Raine, J. D., Sinden, R. E., Harris, M. A., Cunningham, D. A. et al. (2002). Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419, 512-519
20. Carlton, J. M., Adams, J. H., Silva, J. C., Bidwell, S. L., Lorenzi, H., Caler, E., Crabtree, J., Angiuoli, S. V., Merino, E. F., Amedeo, P., Cheng, Q., Coulson, R. M., Crabb, B. S., Del Portillo, H. A., Essien, K., Feldblyum, T. V., Fernandez-Becerra, C., Gilson, P. R., Gueye, A. H., Guo, X., Kang'a, S., Kooij, T.W., Korsinczky, M., Meyer, E. V., Nene, V., Paulsen, I., White, O., Ralph, S. A., Ren, Q., Sargeant, T. J. et al. (2008). Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455, 757-763
21. Carruthers, V. and Boothroyd, J. C. (2007). Pulling together: an integrated model of Toxoplasma cell invasion. Current Opinion in Microbiology 10, 83-89
22. Chatterjee, A., Banerjee, S., Steffen, M., O'Connor, R. M., Ward, H. D., Robbins, P.W. and Samuelson, J. (2010). Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryotic Cell 9, 84-96
23. Chen, Q., Fernandez, V., Sundstrom, A., Schlichtherle, M., Datta, S., Hagblom, P. and Wahlgren, M. (1998). Developmental selection of var gene expression in Plasmodium Falciparum. Nature 394, 392-395
24. Cheng, Q., Cloonan, N., Fischer, K., Thompson, J., Waine, G., Lanzer, M. and Saul, A. (1998). Stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Molecular and Biochemical Parasitology 97, 161-176
25. Cornillot, E., Hadj-Kaddour, K., Dassouli, A., Noel, B., Ranwez, V., Vacherie, B., Augagneur, Y., Bres, V., Duclos, A., Randazzo, S., Carcy, B., Debierre-Grockiego, F., Delbecq, S., Moubri-Menage, K., Shams-Eldin, H., Usmani-Brown, S., Bringaud, F., Wincker, P., Vivares, C. P., Schwarz, R. T., Schetters, T. P., Krause, P. J., Gorenflot, A., Berry, V., Barbe, V. and Ben Mamoun, C. (2012). Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Research 40, 9102-9114
26. Cunningham, D., Fonager, J., Jarra, W., Carret, C., Preiser, P. and Langhorne, J. (2009). Rapid changes in transcription profiles of the Plasmodium yoelii yir multigene family in clonal populations: lack of epigenetic memory' PLoS One 4, e4285.
27. Cunningham, D. A., Jarra, W., Koernig, S., Fonager, J., Fernandez-Reyes, D., Blythe, J. E., Waller, C., Preiser, P. R. and Langhorne, J. (2005). Host immunity modulates transcriptional changes in a multigene family (yir) of rodent malaria. Molecular Microbiology 58, 636-647
28. Deitsch, K.W., Calderwood, M. S. and Wellems, T. E. (2001). Malaria. Cooperative silencing elements in var genes. Nature 412, 875-876
29. del Portillo, H. A., Fernandez-Becerra, C., Bowman, S., Oliver, K., Preuss, M., Sanchez, C. P., Schneider, N. K., Villalobos, J. M., Rajandream, M. A., Harris, D., Pereira da Silva, L. H., Barrell, B. and Lanzer, M. (2001). A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 410, 839-842
30. Di Girolamo, F., Raggi, C., Birago, C., Pizzi, E., Lalle, M., Picci, L., Pace, T., Bachi, A., de Jong, J., Janse, C. J., Waters, A. P., Sargiacomo, M. and Ponzi, M. (2008). Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics 8, 2500-2513
31. Dobbelaere, D. A. and Kuenzi, P. (2004). The strategies of the Theileria parasite: a new twist in host-pathogen interactions Current Opinion in Immunology 16, 524-530
32. D'Ombrain, M. C., Voss, T. S., Maier, A. G., Pearce, J. A., Hansen, D. S., Cowman, A. F. and Schofield, L. (2007). Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host and Microbe 2, 130-138
33. Dzierszinski, F., Mortuaire, M., Cesbron-Delauw, M. F. and Tomavo, S. (2000). Targeted disruption of the glycosylphosphatidylinositol- anchored surface antigen SAG3 gene in Toxoplasma gondii decreases host cell adhesion and drastically reduces virulence in mice. Molecular Microbiology 37, 574-582
34. Fass, D. (2012). Disulfide bonding in protein biophysics. Annual Review of Biophysics 41, 63-79
35. Fentress, S. J., Behnke, M. S., Dunay, I. R., Mashayekhi, M., Rommereim, L. M., Fox, B. A., Bzik, D. J., Taylor, G. A., Turk, B. E., Lichti, C. F., Townsend, R. R., Qiu, W., Hui, R., Beatty, W. L. and Sibley, L.D. (2010). Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host and Microbe 8, 484-495
36. Fernandez-Becerra, C., Pein, O., de Oliveira, T. R., Yamamoto, M. M., Cassola, A. C., Rocha, C., Soares, I. S., de Braganca Pereira, C. A. and del Portillo, H. A. (2005). Variant proteins of Plasmodium vivax are not clonally expressed in natural infections. Molecular Microbiology 58, 648-658
37. Figueiredo, L. M., Pirrit, L. A. and Scherf, A. (2000). Genomic organisation and chromatin structure of Plasmodium falciparum chromosome ends. Molecular and Biochemical Parasitology 106, 169-174
38. Freitas-Junior, L. H., Bottius, E., Pirrit, L. A., Deitsch, K.W., Scheidig, C., Guinet, F., Nehrbass, U., Wellems, T. E. and Scherf, A. (2000). Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407, 1018-1022
39. Freitas-Junior, L. H., Hernandez-Rivas, R., Ralph, S. A., Montiel- Condado, D., Ruvalcaba-Salazar, O. K., Rojas-Meza, A. P., Mancio- Silva, L., Leal-Silvestre, R. J., Gontijo, A. M., Shorte, S. and Scherf, A. (2005). Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121, 25-36
40. Gajria, B., Bahl, A., Brestelli, J., Dommer, J., Fischer, S., Gao, X., Heiges, M., Iodice, J., Kissinger, J. C., Mackey, A. J., Pinney, D. F., Roos, D. S., Stoeckert, C. J., Jr., Wang, H. and Brunk, B. P. (2008). ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Research 36, D553-556
41. Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M.W., Vaidya, A. B., Martin, D. M. et al. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511
42. Gardner, M. J., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B. (2005). Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134-137
43. Guizetti, J. and Scherf, A. (2013). Silence, activate, poise and switch! Mechanisms of antigenic variation in Plasmodium falciparum. Cellular Microbiology 15, 718-726
44. Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T.W., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D., Churcher, C., Quail, M. A., Ormond, D., Doggett, J., Trueman, H. E., Mendoza, J., Bidwell, S. L., Rajandream, M. A., Carucci, D. J., Yates, J. R., 3rd, Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M., Waters, A. P. and Sinden, R. E. (2005). A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82-86
45. Hiller, N. L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C. and Haldar, K. (2004). A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306, 1934-1937
46. Homer, M. J., Bruinsma, E. S., Lodes, M. J., Moro, M. H., Telford, S., 3rd, Krause, P. J., Reynolds, L. D., Mohamath, R., Benson, D. R., Houghton, R. L., Reed, S. G. and Persing, D. H. (2000). A polymorphic multigene family encoding an immunodominant protein from Babesia microti. Journal of Clinical Microbiology 38, 362-368
47. Howard, R. J., Barnwell, J.W. and Kao, V. (1983). Antigenic variation of Plasmodium knowlesi malaria: identification of the variant antigen on infected erythrocytes. Proceedings of the National Academy of Sciences of the United States of America 80, 4129-4133
48. Howe, D. K., Crawford, A. C., Lindsay,D. and Sibley, L. D. (1998). The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii. Infection and Immunity 66, 5322-5328
49. Huang, Y., Xiao, Y. P. and Allred, D. R. (2013). Unusual chromatin structure associated with monoparalogous transcription of the Babesia bovis ves multigene family. International Journal for Parasitology 43, 163-172
50. Jackson, A. P., Otto, T. D., Darby, A., Ramaprasad, A., Xia, D., Echaide, I. E., Farber, M., Gahlot, S., Gamble, J., Gupta, D., Gupta, Y., Jackson, L., Malandrin, L., Malas, T. B., Moussa, E., Nair, M., Reid, A. J., Sanders, M., Sharma, J., Tracey, A., Quail, M. A., Weir, W., Wastling, J. M., Hall, N., Willadsen, P., Lingelbach, K., Shiels, B., Tait, A., Berriman, M., Allred, D. R. et al. (2014). The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction Nucleic Acids Research 42, 7113-7131
51. Janssen, C. S., Phillips, R. S., Turner, C. M. and Barrett, M. P. (2004). Plasmodium interspersed repeats: the major multigene superfamily of malaria parasites. Nucleic Acids Research 32, 5712-5720
52. Jiang, L., Mu, J., Zhang, Q., Ni, T., Srinivasan, P., Rayavara, K., Yang, W., Turner, L., Lavstsen, T., Theander, T. G., Peng, W., Wei, G., Jing, Q., Wakabayashi, Y., Bansal, A., Luo, Y., Ribeiro, J. M., Scherf, A., Aravind, L., Zhu, J., Zhao, K. and Miller, L. H. (2013). PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499, 223-227
53. Jung, C., Lee, C. Y. and Grigg, M. E. (2004). The SRS superfamily of Toxoplasma surface proteins. International Journal for Parasitology 34, 285-296
54. Kaviratne, M., Khan, S. M., Jarra, W. and Preiser, P. R. (2002). Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryotic Cell 1, 926-935
55. Khattab, A. and Klinkert, M. Q. (2006). Maurer's clefts-restricted localization, orientation and export of a Plasmodium falciparum RIFIN. Traffic 7, 1654-1665
56. Kim, S. K. and Boothroyd, J. C. (2005). Stage-specific expression of surface antigens by Toxoplasma gondii as a mechanism to facilitate parasite persistence. Journal of immunology 174, 8038-8048
57. Kyes, S., Horrocks, P. and Newbold, C. (2001). Antigenic variation at the infected red cell surface in malaria. Annual Review of Microbiology 55, 673-707
58. Kyes, S., Christodoulou, Z., Pinches, R., Kriek, N., Horrocks, P. and Newbold, C. (2007). Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. Molecular Microbiology 63, 1237-1247
59. Kyes, S. A., Rowe, J. A., Kriek, N. and Newbold, C. I. (1999). Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proceedings of the National Academy of Sciences of the United States of America 96, 9333-9338
60. Lavstsen, T., Salanti, A., Jensen, A. T., Arnot, D. E. and Theander, T. G. (2003). Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malaria Journal 2, 27.
61. Lawton, J., Brugat, T., Yan, Y. X., Reid, A. J., Bohme, U., Otto, T. D., Pain, A., Jackson, A., Berriman, M., Cunningham, D., Preiser, P. and Langhorne, J. (2012). Characterization and gene expression analysis of the cir multi-gene family of Plasmodium chabaudi chabaudi (AS). BMC Genomics 13, 125
62. Lekutis, C., Ferguson, D. J., Grigg, M. E., Camps, M. and Boothroyd, J. C. (2001). Surface antigens of Toxoplasma gondii: variations on a theme. International Journal for Parasitology 31, 1285-1292
63. Logan-Klumpler, F. J., De Silva, N., Boehme, U., Rogers, M. B., Velarde, G., McQuillan, J. A., Carver, T., Aslett, M., Olsen, C., Subramanian, S., Phan, I., Farris, C., Mitra, S., Ramasamy, G., Wang, H., Tivey, A., Jackson, A., Houston, R., Parkhill, J., Holden, M., Harb, O. S., Brunk, B. P., Myler, P. J., Roos, D., Carrington, M., Smith, D. F., Hertz-Fowler, C. and Berriman, M. (2012). GeneDB - an annotation database for pathogens Nucleic Acids Research 40, D98-D108
64. Lopez-Rubio, J. J., Gontijo, A. M., Nunes, M. C., Issar, N., Hernandez Rivas, R. and Scherf, A. (2007). 5' flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Molecular Microbiology 66, 1296-1305
65. Marti, M., Good, R. T., Rug, M., Knuepfer, E. and Cowman, A. F. (2004). Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306, 1930-1933
66. Niang, M., Yan Yam, X. and Preiser, P. R. (2009). The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte. PLoS pathogens 5, e1000307
67. Nunes, M. C., Goldring, J. P., Doerig, C. and Scherf, A. (2007). A novel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell. Molecular Microbiology 63, 391-403
68. Nunes, M. C., Okada, M., Scheidig-Benatar, C., Cooke, B. M. and Scherf, A. (2010). Plasmodium falciparum FIKK kinase members target distinct components of the erythrocyte membrane. PLoS One 5, e11747
69. O'Connor, R. M. and Allred, D. R. (2000). Selection of Babesia bovisinfected erythrocytes for adhesion to endothelial cells coselects for altered variant erythrocyte surface antigen isoforms. Journal of Immunology 164, 2037-2045
70. O'Connor, R. M., Lane, T. J., Stroup, S. E. and Allred, D. R. (1997). Characterization of a variant erythrocyte surface antigen (VESA1) expressed by Babesia bovis during antigenic variation. Molecular and Biochemical Parasitology 89, 259-270
71. Otto, T. D., Boehme, U., Jackson, A. P., Hunt, M., Franke-Fayard, B., Hoeijmakers, W. A. M., Religa, A. A., Robertson, L., Sanders, M., Ogun, S. A., Cunningham, D., Erhart, A., Billker, O., Khan, S. M., Stunnenberg, H. G., Langhorne, J., Holder, A. A., Waters, A. P., Newbold, C. I., Pain, A., Berriman, M. and Janse, C. J. A comprehensive evaluation of rodent malaria parasite genomes and gene-expression. under review
72. Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R. M., Cronin, A., de Villiers, E. P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D. E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C. et al. (2005). Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309, 131-133
73. Pain, A., Bohme, U., Berry, A. E., Mungall, K., Finn, R. D., Jackson, A. P., Mourier, T., Mistry, J., Pasini, E. M., Aslett, M. A., Balasubrammaniam, S., Borgwardt, K., Brooks, K., Carret, C., Carver, T. J., Cherevach, I., Chillingworth, T., Clark, T. G., Galinski, M. R., Hall, N., Harper, D., Harris, D., Hauser, H., Ivens, A., Janssen, C. S., Keane, T., Larke, N., Lapp, S., Marti, M., Moule, S. et al. (2008). The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455, 799-803
74. Pei, X., Guo, X., Coppel, R., Bhattacharjee, S., Haldar, K., Gratzer, W., Mohandas, N. and An, X. (2007). The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110, 1036-1042
75. Petter, M., Haeggstrom, M., Khattab, A., Fernandez, V., Klinkert, M. Q. and Wahlgren, M. (2007). Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns. Molecular and Biochemical Parasitology 156, 51-61
76. Phillips, R. S., Brannan, L. R., Balmer, P. and Neuville, P. (1997). Antigenic variation during malaria infection - the contribution from the murine parasite Plasmodium chabaudi Parasite Immunology 19, 427-434
77. Pollard, A. M., Onatolu, K. N., Hiller, L., Haldar, K. and Knoll, L. J. (2008). Highly polymorphic family of glycosylphosphatidylinositolanchored surface antigens with evidence of developmental regulation in Toxoplasma gondii. Infection and Immunity 76, 103-110
78. Ralph, S. A., Bischoff, E., Mattei, D., Sismeiro, O., Dillies, M. A., Guigon, G., Coppee, J. Y., David, P. H. and Scherf, A. (2005). Transcriptome analysis of antigenic variation in Plasmodium falciparum - var silencing is not dependent on antisense RNA Genome Biology 6, R93
79. Reese, M. L., Zeiner, G. M., Saeij, J. P., Boothroyd, J. C. and Boyle, J. P. (2011). Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Proceedings of the National Academy of Sciences of the United States of America 108, 9625-9630
80. Reid, A. J., Vermont, S. J., Cotton, J. A., Harris, D., Hill- Cawthorne, G. A., Konen-Waisman, S., Latham, S. M., Mourier, T., Norton, R., Quail, M. A., Sanders, M., Shanmugam, D., Sohal, A., Wasmuth, J. D., Brunk, B., Grigg, M. E., Howard, J. C., Parkinson, J., Roos, D. S., Trees, A. J., Berriman, M., Pain, A. and Wastling, J. M. (2012). Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: Coccidia differing in host range and transmission strategy. PLoS Pathogens 8, e1002567
81. Reid, A. J., Blake, D. P., Ansari, H. R., Billington, K., Browne, H. P., Bryant, J. M., Dunn, M., Hung, S. S., Kawahara, F., Miranda- Saavedra, D., Malas, T., Mourier, T., Naghra, H., Nair, M., Otto, T. D., Rawlings, N. D., Rivailler, P., Sanchez-Flores, A., Sanders, M., Subramanian, C., Tay, Y. L., Woo, Y., Wu, X., Barrell, B., Dear, P. H., Doerig, C., Gruber, A., Ivens, A. C., Parkinson, J., Rajandream, M. A., Shirley, M.W., Wan, K. L., Berriman, M., Tomley, F.M. and Pain, A. (2014). Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Res. doi: 10.1101/gr.168955.113
82. Rowe, J. A., Moulds, J. M., Newbold, C. I. and Miller, L. H. (1997). P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388, 292-295
83. Rowe, J. A., Kyes, S. A., Rogerson, S. J., Babiker, H. A. and Raza, A. (2002). Identification of a conserved Plasmodium falciparum var gene implicated in malaria in pregnancy. Journal of Infectious Diseases 185, 1207-1211
84. Saeij, J. P., Coller, S., Boyle, J. P., Jerome, M. E., White, M.W. and Boothroyd, J. C. (2007). Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445, 324-327
85. Salanti, A., Dahlback, M., Turner, L., Nielsen, M. A., Barfod, L., Magistrado, P., Jensen, A. T., Lavstsen, T., Ofori, M. F., Marsh, K., Hviid, L. and Theander, T. G. (2004). Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. The Journal of Experimental Medicine 200, 1197-1203
86. Salcedo-Amaya, A. M., van Driel, M. A., Alako, B. T., Trelle, M. B., van den Elzen, A. M., Cohen, A. M., Janssen-Megens, E. M., van de Vegte-Bolmer, M., Selzer, R. R., Iniguez, A. L., Green, R. D., Sauerwein, R.W., Jensen, O.N. and Stunnenberg, H. G. (2009). Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proceedings of the National Academy of Sciences of the United States of America 106, 9655-9660
87. Sargeant, T. J., Marti, M., Caler, E., Carlton, J. M., Simpson, K., Speed, T. P. and Cowman, A. F. (2006). Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biology 7, R12
88. Scherf, A., Hernandez-Rivas, R., Buffet, P., Bottius, E., Benatar, C., Pouvelle, B., Gysin, J. and Lanzer, M. (1998). Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. The EMBO Journal 17, 5418-5426
89. Scherf, A., Lopez-Rubio, J. J. and Riviere, L. (2008). Antigenic variation in Plasmodium falciparum. Annual Review of Microbiology 62, 445-470
90. Schmuckli-Maurer, J., Casanova, C., Schmied, S., Affentranger, S., Parvanova, I., Kang'a, S., Nene, V., Katzer, F., McKeever, D., Muller, J., Bishop, R., Pain, A. and Dobbelaere, D. A. (2009). Expression analysis of the Theileria parva subtelomere-encoded variable secreted protein gene family. PLoS One 4, e4839.
91. Schneider, A. G. and Mercereau-Puijalon, O. (2005). A new Apicomplexa-specific protein kinase family: multiple members in Plasmodium falciparum, all with an export signature. BMC Genomics 6, 30
92. Shiels, B. R., McKellar, S., Katzer, F., Lyons, K., Kinnaird, J., Ward, C., Wastling, J. M. and Swan, D. (2004). A Theileria annulata DNA binding protein localized to the host cell nucleus alters the phenotype of a bovine macrophage cell line. Eukaryotic cell 3, 495-505
93. Singh, I., Theodos, C. and Tzipori, S. (2005). Recombinant proteins of Cryptosporidium parvum induce proliferation of mesenteric lymph node cells in infected mice. Infection and Immunity 73, 5245-5248
94. Sondgeroth, K. S., McElwain, T. F., Allen, A. J., Chen, A. V. and Lau, A. O. (2013). Loss of neurovirulence is associated with reduction of cerebral capillary sequestration during acute Babesia bovis infection. Parasites and Vectors 6, 181.
95. Spence, P. J., Jarra, W., Levy, P., Reid, A. J., Chappell, L., Brugat, T., Sanders, M., Berriman, M. and Langhorne, J. (2013). Vector transmission regulates immune control of Plasmodium virulence. Nature 498, 228-231
96. Tabares, E., Ferguson, D., Clark, J., Soon, P. E., Wan, K. L. and Tomley, F. (2004). Eimeria tenella sporozoites and merozoites differentially express glycosylphosphatidylinositol-anchored variant surface proteins. Molecular and Biochemical Parasitology 135, 123-132
97. Tachibana, S., Sullivan, S. A., Kawai, S., Nakamura, S., Kim, H. R., Goto, N., Arisue, N., Palacpac, N. M., Honma, H., Yagi, M., Tougan, T., Katakai, Y., Kaneko, O., Mita, T., Kita, K., Yasutomi, Y., Sutton, P. L., Shakhbatyan, R., Horii, T., Yasunaga, T., Barnwell, J.W., Escalante, A. A., Carlton, J.M. and Tanabe, K. (2012). Plasmodium cynomolgi genome sequences provide insight into Plasmodium vivax and the monkey malaria clade. Nature Genetics 44, 1051-1055
98. Talevich, E. and Kannan, N. (2013). Structural and evolutionary adaptation of rhoptry kinases and pseudokinases, a family of coccidian virulence factors. BMC Evolutionary Biology 13, 117.
99. Taylor, S., Barragan, A., Su, C., Fux, B., Fentress, S. J., Tang, K., Beatty, W. L., Hajj, H. E., Jerome, M., Behnke, M. S., White, M., Wootton, J. C. and Sibley, L. D. (2006). A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314, 1776-1780
100. Tolia, N. H., Enemark, E. J., Sim, B. K. and Joshua-Tor, L. (2005). Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122, 183-193
101. Tomavo, S. (1996). The major surface proteins of Toxoplasma gondii: structures and functions. Current Topics in Microbiology and Immunology 219, 45-54
102. Tomavo, S. (2001). The differential expression of multiple isoenzyme forms during stage conversion of Toxoplasma gondii: an adaptive developmental strategy. International Journal for Parasitology 31, 1023-1031
103. Voss, T. S., Healer, J., Marty, A. J., Duffy, M. F., Thompson, J. K., Beeson, J. G., Reeder, J. C., Crabb, B. S. and Cowman, A. F. (2006). A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439, 1004-1008
104. Wasmuth, J. D., Pszenny, V., Haile, S., Jansen, E. M., Gast, A. T., Sher, A., Boyle, J. P., Boulanger, M. J., Parkinson, J. and Grigg, M. E. (2012). Integrated bioinformatic and targeted deletion analyses of the SRS gene superfamily identify SRS29C as a negative regulator of Toxoplasma virulence. MBio 3, e00321-12
105. Weir, W., Karagenc, T., Baird, M., Tait, A. and Shiels, B. R. (2010). Evolution and diversity of secretome genes in the apicomplexan parasite Theileria annulata. BMC Genomics 11, 42.
106. Zhang, Q., Huang, Y., Zhang, Y., Fang, X., Claes, A., Duchateau, M., Namane, A., Lopez-Rubio, J. J., Pan, W. and Scherf, A. (2011). A critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites. Cell Host and Microbe 10, 451-463