Skip to main content Accessibility help
×
Home
Hostname: page-component-55597f9d44-qcsxw Total loading time: 0.263 Render date: 2022-08-15T14:03:42.127Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Article contents

High throughput sequencing of the Angiostrongylus cantonensis genome: a parasite spreading worldwide

Published online by Cambridge University Press:  17 July 2013

ALESSANDRA L. MORASSUTTI*
Affiliation:
Laboratório de Biologia Parasitária da Faculdade de Biociências e Laboratório de Parasitologia Molecular do Instituto de Pesquisas Biomédicas da Pontifícia Universidade do Rio Grande do Sul (PUCRS), Av Ipiranga 6690, 90690-900 Porto Alegre RS, Brasil
ANDREY PERELYGIN
Affiliation:
Division of Parasitic Diseases & Malaria, Center for Global Health, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA, 30329, USA
MARCOS O. DE CARVALHO
Affiliation:
Programa de Pós-Graduação em Genética e Biologia Molecular, Universidade Federal do Rio Grande do Sul, Porto Alegre RS, Brasil
LEANDRO NASCIMENTO LEMOS
Affiliation:
Universidade Federal do Pampa – Campus São Gabriel, Av. Antônio Trilha, 1847 – São Gabriel – RS – CEP: 97300-000
PAULO MARCOS PINTO
Affiliation:
Universidade Federal do Pampa – Campus São Gabriel, Av. Antônio Trilha, 1847 – São Gabriel – RS – CEP: 97300-000
MIKE FRACE
Affiliation:
Division of Parasitic Diseases & Malaria, Center for Global Health, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA, 30329, USA
PATRICIA P. WILKINS
Affiliation:
Division of Parasitic Diseases & Malaria, Center for Global Health, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA, 30329, USA
CARLOS GRAEFF-TEIXEIRA
Affiliation:
Laboratório de Biologia Parasitária da Faculdade de Biociências e Laboratório de Parasitologia Molecular do Instituto de Pesquisas Biomédicas da Pontifícia Universidade do Rio Grande do Sul (PUCRS), Av Ipiranga 6690, 90690-900 Porto Alegre RS, Brasil
ALEXANDRE J. DA SILVA
Affiliation:
Division of Parasitic Diseases & Malaria, Center for Global Health, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, GA, 30329, USA
*
*Corresponding author. Instituto de Pesquisas Biomédicas da PUCRS, Avenida Ipiranga 6690, 2 andar, Sala 20, CEP: 90690-900 Porto Alegre RS, Brazil. E-mail: almorassutti@gmail.com

Summary

Angiostrongylus cantonensis is a parasitic nematode of rodents and a leading aetiological agent of eosinophilic meningitis in humans. Definitive diagnosis is difficult, often relying on immunodiagnostic methods which utilize crude antigens. New immunodiagnostic methods based on recombinant proteins are being developed, and ideally these methods would be made available worldwide. Identification of diagnostic targets, as well as studies on the biology of the parasite, are limited by a lack of molecular information on Angiostrongylus spp. available in databases. In this study we present data collected from DNA random high-throughput sequencing together with proteomic analyses and a cDNA walking methodology to identify and obtain the nucleotide or amino acid sequences of unknown immunoreactive proteins. 28 080 putative ORFs were obtained, of which 3371 had homology to other deposited protein sequences. Using the A. cantonensis genomic sequences, 156 putative ORFs, matching peptide sequences obtained from previous proteomic studies, were considered novel, with no homology to existing sequences. Full-length coding sequences of eight antigenic target proteins were obtained. In this study we generated not only the complete nucleotide sequences of the antigenic protein targets but also a large amount of genomic data which may help facilitate future genomic, proteomic, transcriptomic or metabolomic studies on Angiostrongylus.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Archer, C. E., Appleton, C. C., Mukaratirwa, S. and Hope, K. J. (2011). The rat lung-worm Angiostrongylus cantonensis: a first report in South Africa. South African Medical Journal 101, 174175.CrossRefGoogle ScholarPubMed
Caldeira, R. L., Mendonça, C. L., Goveia, C. O., Lenzi, H. L., Graeff-Teixeira, C., Lima, W. S., Mota, E. M., Pecora, I. L., Medeiros, A. M. and Carvalho, O. S. (2007). First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Memorias do Instituto Oswaldo Cruz 102, 887889.CrossRefGoogle Scholar
Diaz, J. H. (2008). Helminthic eosinophilic meningitis: emerging zoonotic diseases in the South. Journal of the Louisiana State Medical Society 160, 333342.Google ScholarPubMed
Foster, J. M., Kumar, S., Ford, L., Johnston, K. L., Ben, R., Graeff-Teixeira, C. and Taylor, M. J. (2008). Absence of Wolbachia endobacteria in the non-filariid nematodes Angiostrongylus cantonensis and A. costaricensis. Parasites and Vectors 1, 31.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C., da Silva, A. C. and Yoshimura, K. (2009). Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322348.CrossRefGoogle ScholarPubMed
Greub, G., Kebbi-Beghdadi, C., Bertelli, C., Collyn, F., Riederer, B. M., Yersin, C., Croxatto, A. and Raoult, D. (2009). High throughput sequencing and proteomics to identify immunogenic proteins of a new pathogen: the dirty genome approach. PLoS ONE 4, e8423.CrossRefGoogle ScholarPubMed
Hao, L., Wu, K., Chen, X. G. and Wang, Q. (2007). Cloning, prokaryotic expression and immunoreactivity evaluation of Angiostrongylus cantonensis galectin. Nan Fang Yi Ke Da Xue Xue Bao 27, 584587.Google ScholarPubMed
Hewitson, J. P., Harcus, Y. M., Curwen, R. S., Dowle, A. A., Atmadja, A. K., Ashton, P. D., Wilson, A. and Maizels, R. M. (2008). The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Molecular and Biochemical Parasitology 160, 821.CrossRefGoogle ScholarPubMed
Hwang, J. S., Takaku, Y., Momose, T., Adamczyk, P., Özbek, S., Ikeo, K., Khalturin, K., Hemmrich, G., Bosch, T. C., Holstein, T. W. et al. (2010). Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra. Proceedings of the National Academy of Sciences USA 107, 1853918544.CrossRefGoogle ScholarPubMed
Ideo, H., Fukushima, K., Gengyo-Ando, K., Mitani, S., Dejima, K., Nomura, K. and Yamashita, K. (2009). A Caenorhabditis elegans glycolipid-binding galectin functions in host defense against bacterial infection. Journal of Biological Chemistry 284, 2649326501.CrossRefGoogle ScholarPubMed
Kiel, M., Josh, P., Jones, A., Windon, R., Hunt, P. and Kongsuwan, K. (2007). Identification of immuno-reactive proteins from a sheep gastrointestinal nematode, Trichostrongylus colubriformis, using two-dimensional electrophoresis and mass spectrometry. International Journal of Parasitology 37, 14191429.CrossRefGoogle ScholarPubMed
Klion, A. D. and Donelson, J. E. (1944). OvGalBP, a filarial antigen with homology to vertebrate galactoside-binding proteins. Molecular and Biochemical Parasitology 65, 305315.CrossRefGoogle Scholar
Knight, R., Maxwell, P., Birmingham, A., Carnes, J., Caporaso, J. G., Easton, B. C., Eaton, M., Hamady, M., Lindsay, H., Liu, Z. et al. (2007). PyCogent: a toolkit for making sense from sequence. Genome Biology 8, R171.CrossRefGoogle ScholarPubMed
Lv, S., Zhang, Y., Zhang, L., Liu, Q., Liu, H. X., Hu, L., Wei, F. R., Steinmann, P., Graeff-Teixeira, C., Zhou, X. N. and Utzinger, J. (2012). The complete mitochondrial genome of the rodent intra-arterial nematodes Angiostrongylus cantonensis and Angiostrongylus costaricensis. Parasitology Research 111, 115123.CrossRefGoogle ScholarPubMed
Ma, Z. Q., Dasari, S., Chambers, M. C., Litton, M. D., Sobecki, S. M., Zimmerman, L. J., Halvey, P. J., Schilling, B., Drake, P. M., Gibson, B. W. and Tabb, D. L. (2009). IDPicker 2·0: improved protein assembly with high discrimination peptide identification filtering. Journal of Proteome Research 8, 38723881.CrossRefGoogle ScholarPubMed
Maldonado, A. Jr., Simões, R. O., Oliveira, A. P., Motta, E. M., Fernandez, M. A., Pereira, Z. M., Monteiro, S. S., Torres, E. J. and Thiengo, S. C. (2010). First report of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Achatina fulica (Mollusca: Gastropoda) from Southeast and South Brazil. Memorias do Instituto Oswaldo Cruz 105, 938941.CrossRefGoogle ScholarPubMed
Morassutti, A. L., Levert, K., Pinto, P. M., da Silva, A. J., Wilkins, P. and Graeff-Teixeira, C. (2012 a). Characterization of Angiostrongylus cantonensis excretory-secretory proteins as potential diagnostic targets. Experimental Parasitology 130, 2631.CrossRefGoogle ScholarPubMed
Morassutti, A. L., Levert, K., Perelygin, A., da Silva, A. J., Wilkins, P. and Graeff-Teixeira, C. (2012 b). The 31-kDa antigen of Angiostrongylus cantonensis comprises distinct antigenic glycoproteins. Vector Borne and Zoonotic Diseases 12, 961968.CrossRefGoogle ScholarPubMed
Nemoto-Sasaki, Y., Hayama, K., Ohya, H., Arata, Y., Kaneko, M. K., Saitou, N., Hirabayashi, J. and Kasai, K. (2008). Caenorhabditis elegans galectins LEC-1-LEC-11: structural features and sugar-binding properties. Biochimica et Biophysica Acta 1780, 11311142.CrossRefGoogle ScholarPubMed
Pincay, T., García, L., Narváez, E., Decker, O., Martini, L. and Moreira, J. M. (2009). Angiostrongyliasis due to Parastrongylus (Angiostrongylus) cantonensis in Ecuador. First report in South America. Tropical Medicine and International Health 14, 37.Google Scholar
Rebello, K. M., Barros, J. S., Mota, E. M., Carvalho, P. C., Perales, J., Lenzi, H. L. and Neves-Ferreira, A. G. (2011). Comprehensive proteomic profiling of adult Angiostrongylus costaricensis, a human parasitic nematode. Journal of Proteomics 74, 15451559.CrossRefGoogle ScholarPubMed
Schechtman, D., Winnen, R., Tarrab-Hazdai, R., Ram, D., Shinder, V., Grevelding, C. G., Kunz, W. and Arnon, R. (2001). Expression and immunolocalization of the 14-3-3 protein of Schistosoma mansoni. Parasitology 123, 573582.CrossRefGoogle ScholarPubMed
Siles-Lucas, M., Merli, M. and Gottstein, B. (2008). 14-3-3 proteins in Echinococcus: their role and potential as protective antigens. Experimental Parasitology 119, 516523.CrossRefGoogle ScholarPubMed
Stanke, M., Diekhans, M., Baertsch, R. and Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24, 637644.CrossRefGoogle ScholarPubMed
Tabb, D. L., Fernando, C. G. and Chambers, M. C. (2007). MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. Journal of Proteome Research 6, 654661.CrossRefGoogle ScholarPubMed
Wang, Q. P., Lai, D. H., Zhu, X. Q., Chen, X. G. and Lun, Z. R. (2008). Human angiostrongyliasis. Lancet Infectious Diseases 8, 621630.CrossRefGoogle ScholarPubMed
Wang, Y., Cheng, Z., Lu, X. and Tang, C. (2009). Echinococcus multilocularis: proteomic analysis of the protoscoleces by two-dimensional electrophoresis and mass spectrometry. Experimental Parasitology 123, 162167.CrossRefGoogle ScholarPubMed
Winham, S. J. and Motsinger-Reif, A. A. (2011). An R package implementation of multifactor dimensionality reduction. BioData Mining 4, 24.CrossRefGoogle Scholar
Supplementary material: File

Morassutti Supplementary Material

Appendix

Download Morassutti Supplementary Material(File)
File 813 KB
Supplementary material: File

Morassutti Supplementary Material

Appendix

Download Morassutti Supplementary Material(File)
File 592 KB
10
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

High throughput sequencing of the Angiostrongylus cantonensis genome: a parasite spreading worldwide
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

High throughput sequencing of the Angiostrongylus cantonensis genome: a parasite spreading worldwide
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

High throughput sequencing of the Angiostrongylus cantonensis genome: a parasite spreading worldwide
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *