Toxoplasma gondii sexual cross in a single naturally infected feline host: Generation of highly mouse-virulent and avirulent clones, genotypically different from clonal types I, II and III

Veterinary Research

Volumn 43, Issue 1, 2012, Pages

  Herrmann, Daland C ^a   Bärwald, Andrea ^a   Maksimov, Aline ^a   Pantchev, Nikola ^b   Vrhovec, Majda G ^b   Conraths, Franz J ^a   Schares, Gereon ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b IDEXX LABORATORIES   (Germany)

Author keywords

Cats; Genotype; PCR RFLP; Toxoplasma gondii; Virulence

Indexed keywords

FELIDAE; MUS; TOXOPLASMA GONDII;

ANIMAL; ANIMAL DISEASE; ARTICLE; BAGG ALBINO MOUSE; CAT; CAT DISEASE; CLASSIFICATION; FECES; GENETICS; GENOTYPE; GERMANY; ISOLATION AND PURIFICATION; MOUSE; PARASITOLOGY; PATHOGENICITY; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE;

ANIMALS; CAT DISEASES; CATS; FECES; GENOTYPE; GERMANY; MICE; MICE, INBRED BALB C; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; VIRULENCE;

EID: 84866383124     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/1297-9716-43-39     Document Type: Article

References (58)

1. Dubey JP, Beattie CP, Toxoplasmosis of Animals and Man CRC Press, Boca Raton 1988
2. An outbreak of toxoplasmosis linked to cats. Stagno S, Dykes AC, Amos CS, Head RA, Juranek DD, Walls K, Pediatrics 1980 65 706 712 7189277
3. Outbreak of toxoplasmosis associated with municipal drinking water. Bowie WR, King AS, Werker DH, Isaac-Renton JL, Bell A, Eng SB, Marion SA, The BC Toxoplasma Investigation Team Lancet 1997 350 173 177
4. The history of Toxoplasma gondii-the first 100years. Dubey JP, J Eukaryot Microbiol 2008 55 467 475 10.1111/j.1550-7408.2008.00345.x 19120791
5. Toxoplasma gondii infection in humans and animals in the United States. Dubey JP, Jones JL, Int J Parasitol 2008 38 1257 1278 10.1016/j.ijpara.2008.03. 007 18508057
6. Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Demar M, Ajzenberg D, Maubon D, Djossou F, Panchoe D, Punwasi W, Valery N, Peneau C, Daigre JL, Aznar C, Cottrelle B, Terzan L, Darde ML, Carme B, Clin Infect Dis 2007 45 88 e95 10.1086/521246 17806043
7. Remington JS, Klein JO, Infectious diseases of the fetus and newborn infant Elsevier Saunders, London 2006
8. Toxoplasma gondii comprises three clonal lineages: Correlation of parasite genotype with human disease. Howe DK, Sibley LD, J Infect Dis 1995 172 1561 1566 10.1093/infdis/172.6.1561 7594717
9. Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Ajzenberg D, Banuls AL, Tibayrenc M, Darde ML, Int J Parasitol 2002 32 27 38 10.1016/S0020-7519(01) 00301-0 11796120
10. Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America. Khan A, Dubey JP, Su C, Ajioka JW, Rosenthal BM, Sibley LD, Int J Parasitol 2011 41 645 655 10.1016/j.ijpara.2011.01.005 21320505
11. Genotypic characterization of Toxoplasma gondii strains associated with human toxoplasmosis in Spain: direct analysis from clinical samples. Fuentes I, Rubio JM, Ramirez C, Alvar J, J Clin Microbiol 2001 39 1566 1570 10.1128/JCM.39.4.1566-1570.2001 11283088
12. Biologic and molecular characterization of Toxoplasma gondii isolates from pigs from Portugal. Sousa S, Ajzenberg D, Canada N, Freire L, Costa JM, Darde ML, Thulliez P, Dubey JP, Vet Parasitol 2006 135 133 136 10.1016/j.vetpar.2005.08.012 16188390
13. Molecular characterization of Toxoplasma gondii isolates from cats in Spain. Montoya A, Miro G, Mateo M, Ramirez C, Fuentes I, J Parasitol 2008 94 1044 1046 10.1645/GE-1403.1 18576763
14. Epidemiological and genetic characterization of Toxoplasma gondii in urban pigeons from the area of Lisbon (Portugal). Waap H, Vilares A, Rebelo E, Gomes S, Angelo H, Vet Parasitol 2008 157 306 309 10.1016/j.vetpar.2008.07.017 18722717
15. Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany. Herrmann DC, Pantchev N, Vrhovec MG, Barutzki D, Wilking H, Fröhlich A, Lüder CG, Conraths FJ, Schares G, Int J Parasitol 2010 40 285 292 10.1016/j.ijpara.2009.08.001 19695254
16. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Sibley LD, Boothroyd JC, Nature 1992 359 82 85 10.1038/359082a0 1355855
17. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD, Brooke-Powell ET, Ajioka JW, Boothroyd JC, Science 2006 314 1780 1783 10.1126/science.1133690 17170306
18. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, Tang K, Beatty WL, Hajj HE, Jerome M, Behnke MS, White M, Wootton JC, Sibley LD, Science 2006 314 1776 1780 10.1126/science.1133643 17170305
19. Phosphorylation of mouse immunity-related GTPase (IRG) resistance proteins is an evasion strategy for virulent Toxoplasma gondii. Steinfeldt T, Konen-Waisman S, Tong L, Pawlowski N, Lamkemeyer T, Sibley LD, Hunn JP, Howard JC, PLoS Biol 2010 8 1000576 10.1371/journal.pbio.1000576 21203588
20. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Fentress SJ, Behnke MS, Dunay IR, Mashayekhi M, Rommereim LM, Fox BA, Bzik DJ, Taylor GA, Turk BE, Lichti CF, Townsend RR, Qiu W, Hui R, Beatty WL, Sibley LD, Cell Host Microbe 2010 8 484 495 10.1016/j.chom.2010.11.005 21147463
21. ATF6beta is a host cellular target of the Toxoplasma gondii virulence factor ROP18. Yamamoto M, Ma JS, Mueller C, Kamiyama N, Saiga H, Kubo E, Kimura T, Okamoto T, Okuyama M, Kayama H, Nagamune K, Takashima S, Matsuura Y, Soldati-Favre D, Takeda K, J Exp Med 2011 208 1533 1546 10.1084/jem.20101660 21670204
22. Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Reese ML, Zeiner GM, Saeij JP, Boothroyd JC, Boyle JP, Proc Natl Acad Sci USA 2011 108 9625 9630 10.1073/pnas.1015980108 21436047
23. Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases. Behnke MS, Khan A, Wootton JC, Dubey JP, Tang K, Sibley LD, Proc Natl Acad Sci USA 2011 108 9631 9636 10.1073/pnas.1015338108 21586633
24. Globalization and the population structure of Toxoplasma gondii. Lehmann T, Marcet PL, Graham DH, Dahl ER, Dubey JP, Proc Natl Acad Sci USA 2006 103 11423 11428 10.1073/pnas.0601438103 16849431
25. Molecular and biological characterization of Toxoplasma gondii isolates from free-range chickens from Guyana, South America, identified several unique and common parasite genotypes. Dubey JP, Applewhaite L, Sundar N, Velmurugan GV, Bandini LA, Kwok OC, Hill R, Su C, Parasitology 2007 134 1559 1565 17572931
26. Genetic diversity of Toxoplasma gondii isolates from chickens from Brazil. Dubey JP, Velmurugan GV, Chockalingam A, Pena HF, de Oliveira LN, Leifer CA, Gennari SM, Bahia Oliveira LM, Su C, Vet Parasitol 2008 157 299 305 10.1016/j.vetpar.2008.07.036 18804329
27. Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Pena HF, Gennari SM, Dubey JP, Su C, Int J Parasitol 2008 38 561 569 10.1016/j.ijpara.2007.09.004 17963770
28. Recent transcontinental sweep of Toxoplasma gondii driven by a single monomorphic chromosome. Khan A, Fux B, Su C, Dubey JP, Darde ML, Ajioka JW, Rosenthal BM, Sibley LD, Proc Natl Acad Sci USA 2007 104 14872 14877 10.1073/pnas.0702356104 17804804
29. Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC, Science 2001 294 161 165 10.1126/science.1061888 11588262
30. Waterborne toxoplasmosis, Brazil, from field to gene. De Moura L, Bahia-Oliveira LM, Wada MY, Jones JL, Tuboi SH, Carmo EH, Ramalho WM, Camargo NJ, Trevisan R, Graca RM, da Silva AJ, Moura I, Dubey JP, Garrett DO, Emerg Infect Dis 2006 12 326 329 10.3201/eid1202.041115 16494765
31. Genetic Divergence of Toxoplasma gondii Strains Associated with Ocular Toxoplasmosis. Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, Belfort R, Ricardo WAV, Silveira C, Sibley LD, Brazil Emerging Infectious Diseases 2006 12 942 949 10.3201/eid1206.060025
32. Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Carme B, Demar M, Ajzenberg D, Darde ML, Emerg Infect Dis 2009 15 656 658 10.3201/eid1504.081306 19331765
33. Generation of a restriction fragment length polymorphism linkage map for Toxoplasma gondii. Sibley LD, LeBlanc AJ, Pfefferkorn ER, Boothroyd JC, Genetics 1992 132 1003 1015 1360931
34. Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii. Su C, Howe DK, Dubey JP, Ajioka JW, Sibley LD, Proc Natl Acad Sci USA 2002 99 10753 10758 10.1073/pnas.172117099 12149482
35. Toxoplasma gondii and sex: essential or optional extra? Ferguson DJ, Trends Parasitol 2002 18 355 359 12380023
36. Sexual recombination and clonal evolution of virulence in Toxoplasma. Grigg ME, Suzuki Y, MICROBES INFECT 2003 5 685 690 10.1016/S1286-4579(03)00088-1 12787745
37. Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Dubey JP, Zhu XQ, Sundar N, Zhang H, Kwok OC, Su C, Vet Parasitol 2007 145 352 356 10.1016/j.vetpar.2006.12.016 17267132
38. Seroprevalence and isolation of Toxoplasma gondii from free-range chickens in Ghana, Indonesia, Italy, Poland, and Vietnam. Dubey JP, Huong LT, Lawson BW, Subekti DT, Tassi P, Cabaj W, Sundar N, Velmurugan GV, Kwok OC, Su C, J Parasitol 2008 94 68 71 10.1645/GE-1362.1 18372623
39. Biologic and genetic comparison of Toxoplasma gondii isolates in free-range chickens from the northern Para state and the southern state Rio Grande do Sul, Brazil revealed highly diverse and distinct parasite populations. Dubey JP, Sundar N, Gennari SM, Minervino AH, Farias NA, Ruas JL, dos Santos TR, Cavalcante GT, Kwok OC, Su C, Vet Parasitol 2007 143 182 188 10.1016/j.vetpar.2006.08.024 16982151
40. Whole genome sequencing of a natural recombinantToxoplasma gondiistrain reveals chromosome sorting and local allelic variants. Lindström Bontell IL, Hall N, Ashelford KE, Dubey JP, Boyle JP, Lindh J, Smith JE, Genome Biol 2009 10 53 10.1186/gb-2009-10-5-r53 19457243
41. Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Schares G, Vrhovec MG, Pantchev N, Herrmann DC, Conraths FJ, Vet Parasitol 2008 152 34 45 10.1016/j.vetpar.2007.12.004 18226453
42. Identification of bovine Neospora parasites by PCR amplification and specific small-subunit rRNA sequence probe hybridization. Ho MSY, Barr BC, Marsh AE, Anderson ML, Rowe JD, Tarantal AF, Hendrickx AG, Sverlow K, Dubey JP, Conrad PA, J Clin Microbiol 1996 34 1203 1208 8727903
43. Identification of a 200- to 300-fold repetitive 529bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Homan WL, Vercammen M, De Braekeleer J, Verschueren H, Int J Parasitol 2000 30 69 75 10.1016/S0020-7519(99)00170-8 10675747
44. Comparison of two DNA targets for the diagnosis of Toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. Reischl U, Bretagne S, Kruger D, Ernault P, Costa JM, BMC Infect Dis 2003 3 7 10.1186/1471-2334-3-7 12729464
45. Selection at a single locus leads to widespread expansion of Toxoplasma gondii lineages that are virulent in mice. Khan A, Taylor S, Ajioka JW, Rosenthal BM, Sibley LD, PLoS Genet 2009 5 1000404 10.1371/journal.pgen.1000404 19266027
46. Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Su C, Zhang X, Dubey JP, Int J Parasitol 2006 36 841 848 10.1016/j.ijpara.2006.03.003 16643922
47. Toxoplasma Genome Database (Toxo Genetic Marker Table), http://www.toxomap.wustl.edu/Toxo-Genetic-Map-Table.html
48. Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in swine from Northeastern Brazil. Azevedo SS, Pena HF, Alves CJ, Guimaraes Filho AA, Oliveira RM, Maksimov P, Schares G, Gennari SM, Rev Bras Parasitol Vet 2010 19 80 84 10.4322/rbpv.01902002 20624342
49. Serological survey and risk factors for Toxoplasma gondii in domestic ducks and geese in Lower Saxony, Germany. Maksimov P, Buschtöns S, Herrmann DC, Conraths FJ, Görlich K, Tenter AM, Dubey JP, Nagel-Kohl U, Thoms B, Bötcher L, Kühne M, Schares G, Vet Parasitol 2011 182 140 149 10.1016/j.vetpar.2011.05.049 21719198
50. Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal Type II lineage. Prestrud KW, Asbakk K, Mork T, Fuglei E, Tryland M, Su C, Vet Parasitol 2008 158 121 128 10.1016/j.vetpar.2008.08.020 18922642
51. Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii. Wendte JM, Miller MA, Lambourn DM, Magargal SL, Jessup DA, Grigg ME, PLoS Genet 2010 6 1001261 10.1371/journal.pgen.1001261 21203443
52. Toxoplasma gondii in foxes and rodents from the German Federal States of Brandenburg and Saxony-Anhalt: Seroprevalence and genotypes. Herrmann DC, Maksimov P, Maksimov A, Sutor A, Schwarz S, Jaschke W, Schliephake A, Denzin N, Conraths FJ, Schares G, Vet Parasitol 2011 doi: 10.1016/j.vetpar.2011.10.030
53. Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Grigg ME, Sundar N, Int J Parasitol 2009 39 925 933 10.1016/j.ijpara.2009.02.005 19217909
54. Atypical Toxoplasma gondii strain from a free-living jaguar (Panthera onca) in French Guiana. Demar M, Ajzenberg D, Serrurier B, Darde ML, Carme B, Am J Trop Med Hyg 2008 78 195 197 18256411
55. Characterization of Toxoplasma gondii isolates in free-range chickens from Chile, South America. Dubey JP, Patitucci AN, Su C, Sundar N, Kwok OC, Shen SK, Vet Parasitol 2006 140 76 82 10.1016/j.vetpar.2006.03.023 16672177
56. Isolation and genetic characterization of Toxoplasma gondii from raccoons (Procyon lotor), cats (Felis domesticus), striped skunk (Mephitis mephitis), black bear (Ursus americanus), and cougar (Puma concolor) from Canada. Dubey JP, Quirk T, Pittt JA, Sundar N, Velmurugan GV, Kwok OC, Leclair D, Hill R, Su C, J Parasitol 2008 94 42 45 10.1645/GE-1349.1 18372620
57. ToxoDB: an integrated Toxoplasma gondii database resource. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, Gao X, Heiges M, Iodice J, Kissinger JC, Mackey A J, et al. Nucleic Acids Res 2007 November 14 km981v1
58. A conserved non-canonical motif in the pseudoactive site of the ROP5 pseudokinase domain mediates its effect on Toxoplasma virulence. Reese ML, Boothroyd JC, J Biol Chem 2011 286 29366 29375 10.1074/jbc.M111.253435 21708941