Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T23:23:24.690Z Has data issue: false hasContentIssue false
  • English
  • Français

A new thrombospondin-related anonymous protein homologue in Neospora caninum (NcMIC2-like1)

Published online by Cambridge University Press:  30 September 2010

L. M. PEREIRA ,
J. A. CANDIDO-SILVA ,
E. DE VRIES  and
A. P. YATSUDA
L. M. PEREIRA
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av do Café, sn/n, 14040-903, Ribeirão Preto, SP, Brazil
J. A. CANDIDO-SILVA
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av do Café, sn/n, 14040-903, Ribeirão Preto, SP, Brazil
E. DE VRIES
Affiliation:
Division of Parasitology and Tropical Veterinary Medicine, Department of Infectious Diseases and Immunology, Utrecht University, P.O. Box 80165, 3508 TD, Utrecht, The Netherlands
A. P. YATSUDA*
Affiliation:
Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av do Café, sn/n, 14040-903, Ribeirão Preto, SP, Brazil
*
*Corresponding author: Departamento de Análises Clínicas, Bromatológicas e Toxicológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, 14040-903, Brazil. Tel: +55 16 3602 4724. Fax: 1636024725. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Neospora caninum is an Apicomplexan protozoan that has the dog as a definitive host and cattle (among other animals) as intermediate hosts. It causes encephalopathy in dogs and abortion in cows, with significant loss in worldwide livestock. As any Apicomplexan, the parasite invades the cells using proteins contained in the phylum-specific organelles, like the micronemes, rhoptries and dense granules. The aim of this study was the characterization of a homologue (denominated NcMIC2-like1) of N. caninum thrombospondin-related anonymous protein (NcMIC2), a micronemal protein previously shown to be involved in the attachment and connection with the intracellular motor responsible for the active process of invasion. A polyclonal antiserum raised against the recombinant NcMIC2-like1 functional core (thrombospondin and integrin domains) recognized the native form of NcMIC2-like1, inhibited the in vitro invasion process and localized NcMIC2-like1 at the apical complex of the parasite by confocal immunofluorescence, indicating its micronemal localization. The new molecule, NcMIC2-like1, has features that differentiates it from NcMIC2 in a substantial way to be considered a homologue†.

Keywords

Neospora caninumApicomplexathrombospondin-related anonymous proteinmicronemeinvasion assayTRAPMIC2-like1MIC2
Type
Research Article
Information
Parasitology , Volume 138 , Issue 3 , March 2011 , pp. 287 - 297
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Achbarou, A., Mercereau-Puijalon, O., Autheman, J. M., Fortier, B., Camus, D. and Dubremetz, J. F. (1991). Characterization of microneme proteins of Toxoplasma gondii. Molecular and Biochemical Parasitology 47, 223–233. doi:10.1016/0166-6851(91)90182-6.CrossRefGoogle ScholarPubMed
Aurrecoechea, C., Brestelli, J., Brunk, B. P., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E. T., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Srinivasamoorthy, G., Stoeckert, C. J. Jr., Thibodeau, R., Treatman, C. and Wang, H. (2010). EuPathDB: a portal to eukaryotic pathogen databases. Nucleic Acids Research 38, 415–419. doi:10.1093/nar/gkp941CrossRefGoogle ScholarPubMed
Barragan, A., Brossier, F. and Sibley, L. D. (2005). Transepithelial migration of Toxoplasma gondii involves an interaction of intracellular adhesion molecule 1 (ICAM-I) with parasite adhesion MIC 2. Cellular Microbiology 7, 561–568. doi:10.1111/j.1462-5822.2005.00486.xCrossRefGoogle Scholar
Baum, J., Gilberger, T. W., Frischknecht, F. and Meissner, M. (2008). Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends in Parasitology 24, 557–563. doi:10.1016/j.pt.2008.08.006CrossRefGoogle ScholarPubMed
Bell, A. and Ranford-Cartwright, L. (2002). Real-time quantitative PCR in parasitology. Trends in Parasitology 18, 337–342. doi:10.1016/S1471-4922(02)02331-0CrossRefGoogle ScholarPubMed
Brossier, F. and Sibley, L. (2005). Toxoplasma gondii: microneme protein MIC 2. The International Journal of Biochemistry & Cell Biology 37, 2266–2272. doi:10.1016/j.biocel.2005.06.006CrossRefGoogle Scholar
Carruthers, V. B. and Sibley, L. D. (1999). Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii. Molecular Microbiology 31, 421–428. Doi:10.1046/j.1365-2958.1999.01174.xCrossRefGoogle ScholarPubMed
Cérède, O., Dubremetz, J. F., Soête, M., Deslée, D., Vial, H., Bout, D. and Lebrun, M. (2005). Synergistic role of micronemal proteins in Toxoplasma gondii virulence. Israel Journal of Experimental Medicine 201, 453–463. doi: 10.1084/jem.20041672.CrossRefGoogle ScholarPubMed
Cesbron-Delauw, M. F., Gendrin, C., Travier, L., Ruffiot, P. and Mercier, C. (2008). Apicomplexa in mammalian cells: trafficking to the parasitophorous vacuole. Traffic 9, 657–664. doi: 10.1111/j.1600-0854.2008.00728.xCrossRefGoogle Scholar
Collantes-Fernández, E., Zaballos, A., Alvarez-García, G. and Ortega-Mora, L. M. (2002). Quantitative detection of Neospora caninum in bovine aborted fetuses and experimentally infected mice by real-time PCR. Journal of Clinical Microbiology 40, 1194–1198. doi: 10.1128/JCM.40.4.1194-1198.2002CrossRefGoogle ScholarPubMed
Daher, W. and Soldati-Favre, D. (2009). Mechanisms controlling glideosome function in apicomplexans. Current Opinion in Microbiology 12, 408–414. doi:10.1016/j.mib.2009.06.008CrossRefGoogle ScholarPubMed
Dessens, J. T., Beetsma, A. L., Dimopoulos, G., Wengelnik, K., Crisanti, A., Kafatos, F. C. and Sinden, R. E. (1999). CTRP is essential for mosquito infection by malaria ookinetes. The EMBO Journal 18, 6221–6227. doi:10.1093/emboj/18.22.6221CrossRefGoogle ScholarPubMed
Di Cristina, M., Spaccapelo, R., Soldati, D., Bistoni, F. and Crisanti, A. (2000). Two conserved amino acid motifs mediate protein targeting to the micronemes of the Apicomplexan parasite Toxoplasma gondii. Molecular and Cellular Biology 10, 7332–7341. PMCID: PMC86287CrossRefGoogle Scholar
Dubey, J. P., Schares, G. and Ortega-Mora, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology Reviews 20, 323–367. doi:10.1128/CMR.00031-06CrossRefGoogle ScholarPubMed
Dubey, J. P., Hattel, A. L., Lindsay, D. S. and Topper, M. J. (1988). Neonatal N. caninum infection in dogs: isolation of the causative agent and experimental transmission. Journal of the American Veterinary Medical Association 193, 1259–1263.Google ScholarPubMed
El Hajj, H., Papoin, J., Cérède, O., Garcia-Réguet, N., Soête, M., Dubremetz, J. F. and Lebrun, M. (2008). Molecular signals in the trafficking of Toxoplasma gondii protein MIC3 to the micronemes. Eukaryotic Cell 7, 1119–1128. doi: 10.1128/EC.00413-07CrossRefGoogle Scholar
Friedrich, N., Santos, J. M., Liu, Y., Palma, A. S., Leon, E., Saouros, S., Kiso, M., Blackman, M. J., Matthews, S., Feizi, T. and Soldati-Favre, D. (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. The Journal of Biological Chemistry 285, 2064–2076. doi:10.1074/jbc.M109.060988CrossRefGoogle ScholarPubMed
Gaffar, F. R., Yatsuda, A. P., Franssen, F. F. and de Vries, E. (2004 a). A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin-related anonymous protein (TRAP) present in Plasmodium sporozoites. Molecular and Biochemical Parasitology 136, 25–34. doi:10.1016/j.molbiopara.2004.02.006CrossRefGoogle Scholar
Gaffar, F. R., Yatsuda, A. P., Franssen, F. F. and de Vries, E. (2004 b). Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infection and Immunity 72, 2947–2955. doi:10.1128/IAI.72.5.2947-2955.2004CrossRefGoogle ScholarPubMed
Ghalmi, F., China, B., Kaidi, R., Daube, G. and Losson, B. (2008). Detection of Neospora caninum in dog organs using real time PCR systems. Veterinary Parasitology 155, 161–167. doi:10.1016/j.vetpar.2008.04.007CrossRefGoogle ScholarPubMed
Heckmann, D., Laufer, B., Marinelli, L., Limongelli, V., Novellino, E., Zahn, G., Stragies, R. and Kressler, H. (2009). Breaking the dogma of the metal-coordinating carboxylate group in integrin ligands: introducing hydroxamic acids to the MIDAS to tune potency and selectivity. Angewandte Chemie 48, 4436–4440. doi: 10.1002/anie.200900206CrossRefGoogle Scholar
Hemphill, A., Vonlaufen, N. and Naguleswaran, A. (2006). Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum. Parasitology 133, 261–278. doi:10.1017/S0031182006000485CrossRefGoogle ScholarPubMed
Hoff, E. F., Cook, S. H., Sherman, G. D., Harper, J. M., Fergunson, D. J., Dubremetz, J. F. and Carruthers, V. B. (2001). Toxoplasma gondii: molecular cloning and characterization of a novel 18-kDa secretory antigen, TgMIC10. Experimental Parasitology 97, 77–88. doi:10.1006/expr.2000.4585CrossRefGoogle ScholarPubMed
Howe, D. K., Mercier, C., Messina, M. and Sibley, L. D. (1997). Expression of Toxoplasma gondii genes in the closely-related apicomplexan parasite Neospora caninum. Molecular and Biochemical Parasitology 86, 29–36. doi:10.1016/S0166-6851(96)02838-1CrossRefGoogle ScholarPubMed
Huynh, M. H., Opitz, C., Kwok, L. Y., Tomley, F. M., Carruthers, V. B., Soldati, D. (2004). Trans-genera reconstitution and complementation of an adhesion complex in Toxoplasma gondii. Cellular Microbiology 6, 771–782. doi:10.1111/j.1462-5822.2004.00403.xCrossRefGoogle ScholarPubMed
Jongert, E., Verhelst, D., Abady, M., Petersen, E. and Gargano, N. (2008). Protective Th1 immune responses against chronic toxoplasmosis induced by a protein-protein vaccine combination but not by its DNA-protein counterpart. Vaccine 26, 5289–5295. doi:10.1016/j.vaccine.2008.07.032CrossRefGoogle Scholar
Jonhson, M. S., Lu, N., Denessiouk, K., Heino, J. and Gullberg, D. (2009). Integrins during evolution: Evolutionary trees and model organisms. Biochimica et Biophysica Acta 1788, 779–789. doi:10.1016/j.bbamem.2008.12.013CrossRefGoogle Scholar
Kawasaki, P. M., Kano, F. S., Vidotto, O. and Vidotto, M. C. (2007). Cloning, sequencing, expression, and antigenic characterization of rMSP4 from Anaplasma marginale isolated from Paraná State, Brazil. Genetics and Molecular Research: GMR 6, 15–22. PMID: 17278086.Google ScholarPubMed
Kawase, O., Nishikawa, Y., Bannai, H., Igarashi, M., Matsuo, T. and Xuan, X. (2010). Characterization of a novel thrombospondin-related protein in Toxoplasma gondii. Parasitology International 59, 211–216. doi:10.1016/j.parint.2010.02.001CrossRefGoogle ScholarPubMed
Keller, N., Naguleswaran, A., Cannas, A., Vonlaufen, N., Bienz, M., Bjorkman, C., Bohne, W. and Hemphill, A. (2002). Identification of a N. caninum microneme protein (NcMIC1) which interacts with sulfated host cell surface glycosaminoglycans. Infection and Immunity 70, 3187–3198. doi:10.1128/IAI.70.6.3187-3198.2002CrossRefGoogle Scholar
Lovett, J. L., Howe, D. K. and Sibley, L. D. (2000). Molecular characterization of a thrombospondin-related anonymous protein homologue in Neospora caninum. Molecular and Biochemical Parasitology 15, 33–43. doi:10.1016/S0166-6851(99)00228-5CrossRefGoogle Scholar
Menard, R. (2000). The journey of the malaria sporozoite through its hosts: two parasite proteins lead the way. Microbes and Infection 2, 633–642. doi:10.1016/S1286-4579(00)00362-2CrossRefGoogle ScholarPubMed
Morahan, B. J., Wang, L. and Coopel, R. L. (2008). No TRAP, no invasion. Trends in Parasitology 25, 77–84. doi:10.1016/j.pt.2008.11.004CrossRefGoogle ScholarPubMed
Naguleswaran, A., Müller, N. and Hemphill, A. (2003). N. caninum and Toxoplasma gondii: a novel adhesion/invasion assay reveals distinct differences in tachyzoite-host cell interactions. Experimental Parasitology 104, 149–158. doi:10.1016/S0014-4894(03)00137-1CrossRefGoogle ScholarPubMed
Naguleswaran, A., Cannas, A., Keller, N., Vonlaufen, N., Björkman, C. and Hemphill, A. (2002). Vero cell surface proteoglycan interaction with the microneme protein NcMIC(3) mediates adhesion of N. caninum tachyzoites to host cells unlike that in Toxoplasma gondii. International Journal for Parasitology 32, 695–704. doi:10.1016/S0020-7519(02)00014-0CrossRefGoogle Scholar
Naguleswaran, A., Cannas, A., Keller, N., Vonlaufen, N., Schares, G., Conraths, F. J., Bjorkman, C. and Hemphill, A. (2001). N. caninum microneme protein NcMIC3: secretion, subcellular localization, and functional involvement in host cell interaction. Infection and Immunity 69, 6483–6494. doi:10.1128/IAI.69.10.6483-6494.2001CrossRefGoogle ScholarPubMed
Putignani, L., Possenti, A., Cherchi, S., Pozio, E., Crisanti, A. and Spano, F. (2008). The thrombospondin-related protein CpMIC1 (CpTSP8) belongs to the repertoire of micronemal proteins of Cryptosporidium parvum. Molecular and Biochemical Parasitology 157, 98–101. doi:10.1016/j.molbiopara.2007.09.004CrossRefGoogle Scholar
Ravindran, S. and Boothroyd, J. C. (2008). Secretion of proteins into host cells by Apicomplexan parasites. Traffic 9, 647–656. doi:10.1111/j.1600-0854.2008.00723.xCrossRefGoogle ScholarPubMed
Robson, K. J., Naitza, S., Barker, G., Sinden, R. E. and Crisanti, A. (1997). Cloning and expression of the thrombospondin related adhesive protein gene of Plasmodium berghei. Molecular and Biochemical Parasitology 84, 1–12. doi:10.1016/S0166-6851(96)02774-0CrossRefGoogle ScholarPubMed
Soldati, D., Dubremetz, J. F. and Lebrun, M. (2001). Microneme proteins: structural and functional requirements to promote adhesion and invasion by the Apicomplexan parasite Toxoplasma gondii. International Journal for Parasitology 31, 1293–1302. doi:10.1016/S0020-7519(01)00257-0CrossRefGoogle ScholarPubMed
Sonda, S., Fuchs, N., Gottstein, B. and Hemphill, A. (2000). Molecular characterization of a novel microneme antigen in Neospora caninum. Molecular and Biochemical Parasitology 108, 39–51. doi:10.1016/S0166-6851(00)00200-0CrossRefGoogle ScholarPubMed
Starnes, G. L., Jewett, T. J., Carruthers, V. B. and Sibley, L. D. (2006). Two separate, conserved acidic amino acid domains within the Toxoplasma gondii MIC 2 cytoplasmic tail are required for parasite survival. The Journal of Biological Chemistry 286, 45–54. doi: 10.1074/jbc.M606523200Google Scholar
Sultan, A. A., Thathy, V., Frevert, U., Robson, K. J., Crisanti, A., Nussenzweig, V., Nussenzweig, R. S. and Menard, R. (1997). TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90, 511–522. doi:10.1016/S0092-8674(00)80511-5CrossRefGoogle ScholarPubMed
Tomley, F. M., Billington, K. J., Bumstead, J. M., Clark, J. D. and Monaghan, P. (2001). EtMIC4: a microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factor-like repeats and thrombospondin type-I repeats. International Journal for Parasitology 31, 1303–1310. doi:10.1016/S0020-7519(01)00255-7CrossRefGoogle ScholarPubMed
Wan, K. L., Carruthers, V. B., Sibley, L. D. and Ajioka, J. W. (1997). Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC 2. Molecular and Biochemical Parasitology 84, 203–214. doi:10.1016/S0166-6851(96)02796-XCrossRefGoogle Scholar
Wetzel, D. M., Chen, L. A., Ruiz, F. A., Moreno, S. N. and Sibley, L. D. (2004). Calcium-mediated protein secretion potentiates motility in Toxoplasma gondii. Journal of Cell Science 117, 5739–5748. doi:10.1242/jcs.01495CrossRefGoogle ScholarPubMed
Zhang, H., Compaore, M. K., Lee, E. G., Liao, M., Zhang, G., Sugimoto, C., Fujisaki, K., Nishikawa, Y. and Xuan, X. (2006). Apical membrane antigen 1 is a cross-reactive antigen between Neospora caninum and Toxoplasma gondii, and the anti-NcAMA1 antibody inhibits host cell invasion by both parasites. Molecular and Biochemical Parasitology 151, 205–212. doi:10.1016/j.molbiopara.2006.11.005CrossRefGoogle ScholarPubMed