Proteome expression changes among virulent and attenuated Neospora caninum isolates

Journal of Proteomics

Volumn 75, Issue 8, 2012, Pages 2306-2318

  Regidor Cerrillo, Javier ^a   Álvarez García, Gema ^a   Pastor Fernández, Iván ^a   Marugán Hernández, Virginia ^a   Gómez Bautista, Mercedes ^a   Ortega Mora, Luis M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

DIGE; Intra specific diversity; MS; Neospora caninum; Tachyzoite proteome

Indexed keywords

PROTOZOAL PROTEIN;

ARTICLE; GEL ELECTROPHORESIS; IN VITRO STUDY; IN VIVO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEOSPORA CANINUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE ISOLATION; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ANIMALS; CELLS, CULTURED; CLUSTER ANALYSIS; COCCIDIOSIS; GENE EXPRESSION REGULATION; METABOLOME; MODELS, BIOLOGICAL; NEOSPORA; PROTEOME; PROTEOMICS; VALIDATION STUDIES AS TOPIC; VIRULENCE;

BOS; CANIS FAMILIARIS; NEOSPORA CANINUM;

EID: 84859268355     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.01.039     Document Type: Article

References (67)

1. Dubey J.P., Buxton D., Wouda W. Pathogenesis of bovine neosporosis. J Comp Pathol 2006, 134:267-289.
2. Dubey J.P., Schares G., Ortega-Mora L.M. Epidemiology and control of neosporosis and Neospora caninum. Clin Microbiol Rev 2007, 20:323-367.
3. Wapenaar W., Jenkins M.C., O'Handley R.M., Barkema H.W. Neospora caninum-like oocysts observed in feces of free-ranging red foxes (Vulpes vulpes) and coyotes (Canis latrans). J Parasitol 2006, 92:1270-1274.
4. Dubey J.P., Schares G. Diagnosis of bovine neosporosis. Vet Parasitol 2006, 140:1-34.
5. Atkinson R., Harper P.A., Ryce C., Morrison D.A., Ellis J.T. Comparison of the biological characteristics of two isolates of Neospora caninum. Parasitology 1999, 118(Pt 4):363-370.
6. Quinn H.E., Miller C.M., Ryce C., Windsor P.A., Ellis J.T. Characterization of an outbred pregnant mouse model of Neospora caninum infection. J Parasitol 2002, 88:691-696.
7. Miller C.M., Quinn H.E., Windsor P.A., Ellis J.T. Characterisation of the first Australian isolate of Neospora caninum from cattle. Aust Vet J 2002, 80:620-625.
8. Collantes-Fernandez E., Lopez-Perez I., Alvarez-Garcia G., Ortega-Mora L.M. Temporal distribution and parasite load kinetics in blood and tissues during Neospora caninum infection in mice. Infect Immun 2006, 74:2491-2494.
9. Rojo-Montejo S., Collantes-Fernandez E., Regidor-Cerrillo J., Alvarez-Garcia G., Marugan-Hernandez V., Pedraza-Diaz S., et al. Isolation and characterization of a bovine isolate of Neospora caninum with low virulence. Vet Parasitol 2009, 159:7-16.
10. Pereira Garcia-Melo D., Regidor-Cerrillo J., Collantes-Fernandez E., Aguado-Martinez A., Del Pozo I., Minguijon E., et al. Pathogenic characterization in mice of Neospora caninum isolates obtained from asymptomatic calves. Parasitology 2010, 137:1057-1068.
11. Regidor-Cerrillo J., Gomez-Bautista M., Del Pozo I., Jimenez-Ruiz E., Aduriz G., Ortega-Mora L.M. Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Vet Res 2010, 41:52.
12. Williams D.J., Guy C.S., McGarry J.W., Guy F., Tasker L., Smith R.F., et al. Neospora caninum-associated abortion in cattle: the time of experimentally-induced parasitaemia during gestation determines foetal survival. Parasitology 2000, 121(Pt 4):347-358.
13. Gibney E.H., Kipar A., Rosbottom A., Guy C.S., Smith R.F., Hetzel U., et al. The extent of parasite-associated necrosis in the placenta and foetal tissues of cattle following Neospora caninum infection in early and late gestation correlates with foetal death. Int J Parasitol 2008, 38:579-588.
14. Rojo-Montejo S., Collantes-Fernandez E., Blanco-Murcia J., Rodriguez-Bertos A., Risco-Castillo V., Ortega-Mora L.M. Experimental infection with a low virulence isolate of Neospora caninum at 70 days gestation in cattle did not result in foetopathy. Vet Res 2009, 40:49.
15. Regidor-Cerrillo J., Gomez-Bautista M., Sodupe I., Aduriz G., Alvarez-Garcia G., Del Pozo I., et al. In vitro invasion efficiency and intracellular proliferation rate comprise virulence-related phenotypic traits of Neospora caninum. Vet Res 2011, 42:41.
16. Regidor-Cerrillo J., Pedraza-Diaz S., Gomez-Bautista M., Ortega-Mora L.M. Multilocus microsatellite analysis reveals extensive genetic diversity in Neospora caninum. J Parasitol 2006, 92:517-524.
17. Beck H.P., Blake D., Darde M.L., Felger I., Pedraza-Diaz S., Regidor-Cerrillo J., et al. Molecular approaches to diversity of populations of apicomplexan parasites. Int J Parasitol 2009, 39:175-189.
18. Taylor S., Barragan A., Su C., Fux B., Fentress S.J., Tang K., et al. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 2006, 314:1776-1780.
19. Saeij J.P., Boyle J.P., Coller S., Taylor S., Sibley L.D., Brooke-Powell E.T., et al. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 2006, 314:1780-1783.
20. El Hajj H., Lebrun M., Arold S.T., Vial H., Labesse G., Dubremetz J.F. ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog 2007, 3:e14.
21. Reese M.L., Zeiner G.M., Saeij J.P., Boothroyd J.C., Boyle J.P. Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Proc Natl Acad Sci U S A 2011, 108:9625-9630.
22. Behnke M.S., Khan A., Wootton J.C., Dubey J.P., Tang K., Sibley L.D. Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases. Proc Natl Acad Sci U S A 2011, 108:9631-9636.
23. Marugan-Hernandez V., Alvarez-Garcia G., Risco-Castillo V., Regidor-Cerrillo J., Ortega-Mora L.M. Identification of Neospora caninum proteins regulated during the differentiation process from tachyzoite to bradyzoite stage by DIGE. Proteomics 2010, 10:1740-1750.
24. Lee E.G., Kim J.H., Shin Y.S., Shin G.W., Kim Y.R., Palaksha K.J., et al. Application of proteomics for comparison of proteome of Neospora caninum and Toxoplasma gondii tachyzoites. J Chromatogr B Analyt Technol Biomed Life Sci 2005, 815:305-314.
25. Shin Y.S., Shin G.W., Kim Y.R., Lee E.Y., Yang H.H., Palaksha K.J., et al. Comparison of proteome and antigenic proteome between two Neospora caninum isolates. Vet Parasitol 2005, 134:41-52.
26. Barber J.S., Holmdahl O.J., Owen M.R., Guy F., Uggla A., Trees A.J. Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper and Uggla). Parasitology 1995, 111(Pt 5):563-568.
27. Regidor-Cerrillo J., Gomez-Bautista M., Pereira-Bueno J., Aduriz G., Navarro-Lozano V., Risco-Castillo V., et al. Isolation and genetic characterization of Neospora caninum from asymptomatic calves in Spain. Parasitology 2008, 135:1651-1659.
28. Alban A., David S.O., Bjorkesten L., Andersson C., Sloge E., Lewis S., et al. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 2003, 3:36-44.
29. Fodor I.K., Nelson D.O., Alegria-Hartman M., Robbins K., Langlois R.G., Turteltaub K.W., et al. Statistical challenges in the analysis of two-dimensional difference gel electrophoresis experiments using DeCyder. Bioinformatics 2005, 21:3733-3740.
30. Sechi S., Chait B.T. Modification of cysteine residues by alkylation. A tool in peptide mapping and protein identification. Anal Chem 1998, 70:5150-5158.
31. Asai T., Howe D.K., Nakajima K., Nozaki T., Takeuchi T., Sibley L.D. Neospora caninum: tachyzoites express a potent type-I nucleoside triphosphate hydrolase. Exp Parasitol 1998, 90:277-285.
32. Dobrowolski J.M., Carruthers V.B., Sibley L.D. Participation of myosin in gliding motility and host cell invasion by Toxoplasma gondii. Mol Microbiol 1997, 26:163-173.
33. Alvarez-Garcia G., Pitarch A., Zaballos A., Fernandez-Garcia A., Gil C., Gomez-Bautista M., et al. The NcGRA7 gene encodes the immunodominant 17 kDa antigen of Neospora caninum. Parasitology 2007, 134:41-50.
34. Marouga R., David S., Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 2005, 382:669-678.
35. Carruthers V., Boothroyd J.C. Pulling together: an integrated model of Toxoplasma cell invasion. Curr Opin Microbiol 2007, 10:83-89.
36. Daher W., Soldati-Favre D. Mechanisms controlling glideosome function in apicomplexans. Curr Opin Microbiol 2009, 12:408-414.
37. Gilk S.D., Gaskins E., Ward G.E., Beckers C.J. GAP45 phosphorylation controls assembly of the Toxoplasma myosin XIV complex. Eukaryot Cell 2009, 8:190-196.
38. Sahoo N., Beatty W., Heuser J., Sept D., Sibley L.D. Unusual kinetic and structural properties control rapid assembly and turnover of actin in the parasite Toxoplasma gondii. Mol Biol Cell 2006, 17:895-906.
39. Agop-Nersesian C., Naissant B., Ben Rached F., Rauch M., Kretzschmar A., Thiberge S., et al. Rab11A-controlled assembly of the inner membrane complex is required for completion of apicomplexan cytokinesis. PLoS Pathog 2009, 5:e1000270.
40. Heaslip A.T., Leung J.M., Carey K.L., Catti F., Warshaw D.M., Westwood N.J., et al. A small-molecule inhibitor of T. gondii motility induces the posttranslational modification of myosin light chain-1 and inhibits myosin motor activity. PLoS Pathog 2010, 6:e1000720.
41. Mehta S., Sibley L.D. Actin depolymerizing factor controls actin turnover and gliding motility in Toxoplasma gondii. Mol Biol Cell 2011, 22:1290-1299.
42. Keller N., Naguleswaran A., Cannas A., Vonlaufen N., Bienz M., Bjorkman C., et al. Identification of a Neospora caninum microneme protein (NcMIC1) which interacts with sulfated host cell surface glycosaminoglycans. Infect Immun 2002, 70:3187-3198.
43. Cerede O., Dubremetz J.F., Soete M., Deslee D., Vial H., Bout D., et al. Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 2005, 201:453-463.
44. Boothroyd J.C., Dubremetz J.F. Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol 2008, 6:79-88.
45. Qiu W., Wernimont A., Tang K., Taylor S., Lunin V., Schapira M., et al. Novel structural and regulatory features of rhoptry secretory kinases in Toxoplasma gondii. EMBO J 2009, 28:969-979.
46. Marugan-Hernandez V., Alvarez-Garcia G., Tomley F., Hemphill A., Regidor-Cerrillo J., Ortega-Mora L.M. Identification of novel rhoptry proteins in Neospora caninum by LC/MS-MS analysis of subcellular fractions. J Proteomics 2011, 74:629-642.
47. Reichmann G., Dlugonska H., Fischer H.G. Characterization of TgROP9 (p36), a novel rhoptry protein of Toxoplasma gondii tachyzoites identified by T cell clone. Mol Biochem Parasitol 2002, 119:43-54.
48. Phelps E.D., Sweeney K.R., Blader I.J. Toxoplasma gondii rhoptry discharge correlates with activation of the early growth response 2 host cell transcription factor. Infect Immun 2008, 76:4703-4712.
49. Mercier C., Adjogble K.D., Daubener W., Delauw M.F. Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites?. Int J Parasitol 2005, 35:829-849.
50. Nam H.W. GRA proteins of Toxoplasma gondii: maintenance of host-parasite interactions across the parasitophorous vacuolar membrane. Korean J Parasitol 2009, 47(Suppl.):S29-S37.
51. Bermudes D., Peck K.R., Afifi M.A., Beckers C.J., Joiner K.A. Tandemly repeated genes encode nucleoside triphosphate hydrolase isoforms secreted into the parasitophorous vacuole of Toxoplasma gondii. J Biol Chem 1994, 269:29252-29260.
52. Asai T., Miura S., Sibley L.D., Okabayashi H., Takeuchi T. Biochemical and molecular characterization of nucleoside triphosphate hydrolase isozymes from the parasitic protozoan Toxoplasma gondii. J Biol Chem 1995, 270:11391-11397.
53. Nakaar V., Samuel B.U., Ngo E.O., Joiner K.A. Targeted reduction of nucleoside triphosphate hydrolase by antisense RNA inhibits Toxoplasma gondii proliferation. J Biol Chem 1999, 274:5083-5087.
54. Asai T., Takeuchi T., Diffenderfer J., Sibley L.D. Identification of small-molecule inhibitors of nucleoside triphosphate hydrolase in Toxoplasma gondii. Antimicrob Agents Chemother 2002, 46:2393-2399.
55. Silverman J.A., Qi H., Riehl A., Beckers C., Nakaar V., Joiner K.A. Induced activation of the Toxoplasma gondii nucleoside triphosphate hydrolase leads to depletion of host cell ATP levels and rapid exit of intracellular parasites from infected cells. J Biol Chem 1998, 273:12352-12359.
56. Esposito M., Moores S., Naguleswaran A., Muller J., Hemphill A. Induction of tachyzoite egress from cells infected with the protozoan Neospora caninum by nitro- and bromo-thiazolides, a class of broad-spectrum anti-parasitic drugs. Int J Parasitol 2007, 37:1143-1152.
57. Pinheiro A.M., Costa S.L., Freire S.M., Ribeiro C.S., Tardy M., El-Bacha R.S., et al. Neospora caninum: early immune response of rat mixed glial cultures after tachyzoites infection. Exp Parasitol 2010, 124:442-447.
58. Rostovtseva T.K., Bezrukov S.M. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J Bioenerg Biomembr 2008, 40:163-170.
59. Peixoto P.M., Ryu S.Y., Kinnally K.W. Mitochondrial ion channels as therapeutic targets. FEBS Lett 2010, 584:2142-2152.
60. Park S.G., Ewalt K.L., Kim S. Functional expansion of aminoacyl-tRNA synthetases and their interacting factors: new perspectives on housekeepers. Trends Biochem Sci 2005, 30:569-574.
61. Bour T., Akaddar A., Lorber B., Blais S., Balg C., Candolfi E., et al. Plasmodial aspartyl-tRNA synthetases and peculiarities in Plasmodium falciparum. J Biol Chem 2009, 284:18893-18903.
62. Nischik N., Schade B., Dytnerska K., Dlugonska H., Reichmann G., Fischer H.G. Attenuation of mouse-virulent Toxoplasma gondii parasites is associated with a decrease in interleukin-12-inducing tachyzoite activity and reduced expression of actin, catalase and excretory proteins. Microbes Infect 2001, 3:689-699.
63. Choi S.H., Kim T.Y., Park S.G., Cha G.H., Shin D.W., Chai J.Y., et al. Proteomic analysis of Toxoplasma gondii KI-1 tachyzoites. Korean J Parasitol 2010, 48:195-201.
64. Howe D.K., Sibley L.D. Comparison of the major antigens of Neospora caninum and Toxoplasma gondii. Int J Parasitol 1999, 29:1489-1496.
65. Jung C., Lee C.Y.F., Grigg M.E. The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol 2004, 34:285-296.
66. Reese M.L., Boothroyd J.C. A helical membrane-domain targets the Toxoplasma ROP2 family to the parasitophorous vacuole. Traffic 2009, 10:1458-1470.
67. Alaeddine F., Keller N., Leepin A., Hemphill A. Reduced infection and protection from clinical signs of cerebral neosporosis in C57BL/6 mice vaccinated with recombinant microneme antigen NcMIC1. J Parasitol 2005, 91:657-665.