Comparative genomics of the apicomplexan parasites Toxoplasma gondii and neospora caninum: Coccidia differing in host range and transmission strategy

PLoS Pathogens

Volumn 8, Issue 3, 2012, Pages

  Reid, Adam James ^a   Vermont, Sarah J ^b   Cotton, James A ^a   Harris, David ^a   Hill Cawthorne, Grant A ^c   Könen Waisman, Stephanie ^d   Latham, Sophia M ^b   Mourier, Tobias ^e   Norton, Rebecca ^b   Quail, Michael A ^a   Sanders, Mandy ^a   Shanmugam, Dhanasekaran ^f   Sohal, Amandeep ^a   Wasmuth, James D ^g,h   Brunk, Brian ^f   Grigg, Michael E ^h   Howard, Jonathan C ^d   Parkinson, John ^g   Roos, David S ^f   Trees, Alexander J ^b   Berriman, Matthew ^a   Pain, Arnab ^a,c   Wastling, Jonathan M ^b   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g HOSPITAL FOR SICK CHILDREN   (Canada)

^h NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ANTIGEN;

ARTICLE; CONSERVATION GENETICS; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOME; NEOSPORA CANINUM; NONHUMAN; PARASITE VIRULENCE; PHOSPHORYLATION; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TOXOPLASMA GONDII; ANIMAL; COCCIDIOSIS; COMPARATIVE GENOMIC HYBRIDIZATION; COMPARATIVE STUDY; DISEASE TRANSMISSION; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; HOST PARASITE INTERACTION; NEOSPORA; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; TOXOPLASMA; TOXOPLASMOSIS; VERTICAL TRANSMISSION; VIRULENCE; ZOONOSIS;

APICOMPLEXA; BOS; CANIS FAMILIARIS; COCCIDIA; NEOSPORA; NEOSPORA CANINUM; PROTOZOA; RODENTIA; TOXOPLASMA; TOXOPLASMA GONDII; VERTEBRATA;

ANIMALS; COCCIDIOSIS; COMPARATIVE GENOMIC HYBRIDIZATION; GENE EXPRESSION REGULATION; GENOMICS; HOST-PARASITE INTERACTIONS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; NEOSPORA; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE; ZOONOSES;

EID: 84861207409     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002567     Document Type: Article

References (94)

1. Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, et al. (2001) Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol 154: 357-365.
2. Mandell GL, Douglas RGJ, Bennet JE, (2010) Principles and practice of infectious diseases Philadelphia Churchill Livingstone.
3. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, et al. (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445: 324-327.
4. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, et al. (2006) A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314: 1776-1780.
5. Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC, (2001) Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294: 161-165.
6. Su C, Evans D, Cole RH, Kissinger JC, Ajioka JW, et al. (2003) Recent expansion of Toxoplasma through enhanced oral transmission. Science 299: 414-416.
7. Dubey JP, Carpenter JL, Speer CA, Topper MJ, Uggla A, (1988) Newly recognized fatal protozoan disease of dogs. J Am Vet Med Assoc 192: 1269-1285.
8. Dubey JP, Barr BC, Barta JR, Bjerkas I, Bjorkman C, et al. (2002) Redescription of Neospora caninum and its differentiation from related coccidia. Int J Parasitol 32: 929-946.
9. McAllister MM, Dubey JP, Lindsay DS, Jolley WR, Wills RA, et al. (1998) Dogs are definitive hosts of Neospora caninum. Int J Parasitol 28: 1473-1478.
10. McCann CM, Vyse AJ, Salmon RL, Thomas D, Williams DJ, et al. (2008) Lack of serologic evidence of Neospora caninum in humans, England. Emerg Infect Dis 14: 978-980.
11. Dubey JP, Schares G, Ortega-Mora LM, (2007) Epidemiology and control of neosporosis and Neospora caninum. Clin Microbiol Rev 20: 323-367.
12. Davison HC, Otter A, Trees AJ, (1999) Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. Int J Parasitol 29: 1683-1689.
13. Trees AJ, Davison HC, Innes EA, Wastling JM, (1999) Towards evaluating the economic impact of bovine neosporosis. Int J Parasitol 29: 1195-1200.
14. Carruthers VB, Sibley LD, (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73: 114-123.
15. Jung C, Lee CY, Grigg ME, (2004) The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol 34: 285-296.
16. Keeley A, Soldati D, (2004) The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol 14: 528-532.
17. Morisaki JH, Heuser JE, Sibley LD, (1995) Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J Cell Sci 108 (Pt 6): 2457-2464.
18. Dobrowolski JM, Sibley LD, (1996) Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
19. Alexander DL, Mital J, Ward GE, Bradley P, Boothroyd JC, (2005) Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog 1: e17.
20. Sinai AP, Joiner KA, (2001) The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 154: 95-108.
21. Ong YC, Reese ML, Boothroyd JC, (2010) Toxoplasma rhoptry protein 16 (ROP16) subverts host function by direct tyrosine phosphorylation of STAT6. J Biol Chem 285: 28731-28740.
22. El Hajj H, Lebrun M, Arold ST, Vial H, Labesse G, et al. (2007) ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog 3: e14.
23. Steinfeldt T, Konen-Waisman S, Tong L, Pawlowski N, Lamkemeyer T, et al. (2010) Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. PLoS Biol 8: e1000576.
24. Fentress SJ, Behnke MS, Dunay IR, Mashayekhi M, Rommereim LM, et al. (2010) Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe 8: 484-495.
25. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, et al. (2008) ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Res 36: D553-556.
26. DeBarry JD, Kissinger JC, (2011) Jumbled genomes: missing Apicomplexan synteny. Mol Biol Evol 28: 2855-2871.
27. Bahl A, Davis PH, Behnke M, Dzierszinski F, Jagalur M, et al. (2010) A novel multifunctional oligonucleotide microarray for Toxoplasma gondii. BMC Genomics 11: 603.
28. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-215.
29. Ellis J, Luton K, Baverstock PR, Brindley PJ, Nimmo KA, et al. (1994) The phylogeny of Neospora caninum. Mol Biochem Parasitol 64: 303-311.
30. Ricklefs RE, Outlaw DC, (2010) A molecular clock for malaria parasites. Science 329: 226-229.
31. Hedges SB, Dudley J, Kumar S, (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22: 2971-2972.
32. Kim SK, Boothroyd JC, (2005) Stage-specific expression of surface antigens by Toxoplasma gondii as a mechanism to facilitate parasite persistence. J Immunol 174: 8038-8048.
33. Boothroyd JC, (2009) Expansion of host range as a driving force in the evolution of Toxoplasma. Mem Inst Oswaldo Cruz 104: 179-184.
34. Howe DK, Crawford AC, Lindsay D, Sibley LD, (1998) The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii. Infect Immun 66: 5322-5328.
35. Pollard AM, Onatolu KN, Hiller L, Haldar K, Knoll LJ, (2008) Highly polymorphic family of glycosylphosphatidylinositol-anchored surface antigens with evidence of developmental regulation in Toxoplasma gondii. Infect Immun 76: 103-110.
36. Khan A, Taylor S, Ajioka JW, Rosenthal BM, Sibley LD, (2009) Selection at a single locus leads to widespread expansion of Toxoplasma gondii lineages that are virulent in mice. PLoS Genet 5: e1000404.
37. Khaminets A, Hunn JP, Konen-Waisman S, Zhao YO, Preukschat D, et al. (2010) Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol 12: 939-961.
38. Butcher BA, Fox BA, Rommereim LM, Kim SG, Maurer KJ, et al. (2011) Toxoplasma gondii Rhoptry Kinase ROP16 Activates STAT3 and STAT6 Resulting in Cytokine Inhibition and Arginase-1-Dependent Growth Control. PLoS Pathog 7: e1002236.
39. Yamamoto M, Standley DM, Takashima S, Saiga H, Okuyama M, et al. (2009) A single polymorphic amino acid on Toxoplasma gondii kinase ROP16 determines the direct and strain-specific activation of Stat3. J Exp Med 206: 2747-2760.
40. Reese ML, Zeiner GM, Saeij JP, Boothroyd JC, Boyle JP, (2011) Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Proc Natl Acad Sci U S A.
41. Dunn JD, Ravindran S, Kim SK, Boothroyd JC, (2008) The Toxoplasma gondii dense granule protein GRA7 is phosphorylated upon invasion and forms an unexpected association with the rhoptry proteins ROP2 and ROP4. Infect Immun 76: 5853-5861.
42. Shaw MK, Roos DS, Tilney LG, (2002) Cysteine and serine protease inhibitors block intracellular development and disrupt the secretory pathway of Toxoplasma gondii. Microbes Infect 4: 119-132.
43. Bradley PJ, Hsieh CL, Boothroyd JC, (2002) Unprocessed Toxoplasma ROP1 is effectively targeted and secreted into the nascent parasitophorous vacuole. Mol Biochem Parasitol 125: 189-193.
44. Naguleswaran A, Muller N, Hemphill A, (2003) Neospora caninum and Toxoplasma gondii: a novel adhesion/invasion assay reveals distinct differences in tachyzoite-host cell interactions. Exp Parasitol 104: 149-158.
45. Painter HJ, Campbell TL, Llinas M, (2011) The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol Biochem Parasitol 176: 1-7.
46. Yuda M, Iwanaga S, Shigenobu S, Kato T, Kaneko I, (2010) Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol Microbiol 75: 854-863.
47. Altschul SF, Wootton JC, Zaslavsky E, Yu YK, (2010) The construction and use of log-odds substitution scores for multiple sequence alignment. PLoS Comput Biol 6: e1000852.
48. De Silva EK, Gehrke AR, Olszewski K, Leon I, Chahal JS, et al. (2008) Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci U S A 105: 8393-8398.
49. Behnke MS, Wootton JC, Lehmann MM, Radke JB, Lucas O, et al. (2010) Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii. PLoS One 5: e12354.
50. Wasmuth J, Daub J, Peregrin-Alvarez JM, Finney CA, Parkinson J, (2009) The origins of apicomplexan sequence innovation. Genome Res 19: 1202-1213.
51. Ewald PW, (1993) Evolution of Infectious Disease New York Oxford University Press.
52. Stewart AD, Logsdon JM Jr, Kelley SE, (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59: 730-739.
53. Hunn JP, (2007) Evolution and Cellular Resistance Mechanisms of the Immunity-Related GTPases [PhD thesis] Koln Universitat zu Koln.
54. Barber JS, Holmdahl OJ, Owen MR, Guy F, Uggla A, et al. (1995) Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper and Uggla). Parasitology 111 (Pt 5): 563-568.
55. Cohen AM, Rumpel K, Coombs GH, Wastling JM, (2002) Characterisation of global protein expression by two-dimensional electrophoresis and mass spectrometry: proteomics of Toxoplasma gondii. Int J Parasitol 32: 39-51.
56. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, et al. (2002) ARACHNE: a whole-genome shotgun assembler. Genome Res 12: 177-189.
57. Delcher AL, Phillippy A, Carlton J, Salzberg SL, (2002) Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30: 2478-2483.
58. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, et al. (2009) Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat Methods 6: 291-295.
59. Ning Z, Cox AJ, Mullikin JC, (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11: 1725-1729.
60. Korf I, (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.
61. Stanke M, Schoffmann O, Morgenstern B, Waack S, (2006) Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7: 62.
62. Pertea M, Lin X, Salzberg SL, (2001) GeneSplicer: a new computational method for splice site prediction. Nucleic Acids Res 29: 1185-1190.
63. Majoros WH, Pertea M, Salzberg SL, (2004) TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20: 2878-2879.
64. Korf I, Flicek P, Duan D, Brent MR, (2001) Integrating genomic homology into gene structure prediction. Bioinformatics 17 (Suppl 1): S140-148.
65. Allen JE, Salzberg SL, (2005) JIGSAW: integration of multiple sources of evidence for gene prediction. Bioinformatics 21: 3596-3603.
66. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, et al. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9: R7.
67. Quackenbush J, Cho J, Lee D, Liang F, Holt I, et al. (2001) The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res 29: 159-164.
68. Carver T, Berriman M, Tivey A, Patel C, Bohme U, et al. (2008) Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24: 2672-2676.
69. Li L, Stoeckert CJ Jr, Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
70. Bradley PJ, Ward C, Cheng SJ, Alexander DL, Coller S, et al. (2005) Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J Biol Chem 280: 34245-34258.
71. Boothroyd JC, Dubremetz JF, (2008) Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol 6: 79-88.
72. Dowse T, Soldati D, (2004) Host cell invasion by the apicomplexans: the significance of microneme protein proteolysis. Curr Opin Microbiol 7: 388-396.
73. Friedrich N, Santos JM, Liu Y, Palma AS, Leon E, et al. (2010) Members of a novel protein family containing microneme adhesive repeat domains act as sialic acid-binding lectins during host cell invasion by apicomplexan parasites. J Biol Chem 285: 2064-2076.
74. Sohn CS, Cheng TT, Drummond ML, Peng ED, Vermont SJ, et al. (2011) Identification of novel proteins in Neospora caninum using an organelle purification and monoclonal antibody approach. PLoS One 6: e18383.
75. Michelin A, Bittame A, Bordat Y, Travier L, Mercier C, et al. (2009) GRA12, a Toxoplasma dense granule protein associated with the intravacuolar membranous nanotubular network. Int J Parasitol 39: 299-306.
76. Lebrun M, Carruthers VB, Cesbron-Delauw MF, (2007) Toxoplasma Secretory Proteins and Their Roles in Cell Invasion. In: Weiss LM, Kim K, editors. London Academic Press.
77. Altschul SF, Wootton JC, Zaslavsky E, Yu YK, (2010) The construction and use of log-odds substitution scores for multiple sequence alignment. PLoS Comput Biol 6: e1000852.
78. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
79. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
80. Felsenstein J, (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368-376.
81. Swofford DL, (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Sunderland, Massachusetts Sinauer Associates.
82. Tavare S, (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM, editors. Some mathematical questions in biology- DNA sequence analysis Providence, RI. Amer. Math. Soc. pp. 57-86.
83. Yang Z, (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39: 306-314.
84. Hasegawa M, Kishino H, Yano T, (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160-174.
85. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
86. Neafsey DE, Hartl DL, Berriman M, (2005) Evolution of noncoding and silent coding sites in the Plasmodium falciparum and Plasmodium reichenowi genomes. Mol Biol Evol 22: 1621-1626.
87. Eizirik E, Murphy W, (2009) Carnivores (Carnivora). In: Hedges SB, Kumar S, editors. The Timetree of Life Oxford Oxford UniversityPress pp. 504-507.
88. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
89. Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC, (2008) Inactive and active states of the interferon-inducible resistance GTPase, Irga6, in vivo. J Biol Chem 283: 32143-32151.
90. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, et al. (2005) Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog 1: e24.
91. Martens S, Sabel K, Lange R, Uthaiah R, Wolf E, et al. (2004) Mechanisms regulating the positioning of mouse p47 resistance GTPases LRG-47 and IIGP1 on cellular membranes: retargeting to plasma membrane induced by phagocytosis. J Immunol 173: 2594-2606.
92. Jones AR, Siepen JA, Hubbard SJ, Paton NW, (2009) Improving sensitivity in proteome studies by analysis of false discovery rates for multiple search engines. Proteomics 9: 1220-1229.
93. Camon EB, Barrell DG, Dimmer EC, Lee V, Magrane M, et al. (2005) An evaluation of GO annotation retrieval for BioCreAtIvE and GOA. BMC Bioinformatics 6 (Suppl 1): S17.
94. Hertz-Fowler C, Peacock CS, Wood V, Aslett M, Kerhornou A, et al. (2004) GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 32: D339-343.