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Evaluation of the immunodiagnostic potential of a recombinant surface protein domain from Acanthamoeba castellanii

Published online by Cambridge University Press:  19 July 2016

ALEMAO G. CARPINTEYRO SÁNCHEZ ,
VERIDIANA GOMES VIRGINIO ,
VINICIUS JOSÉ MASCHIO ,
HENRIQUE BUNSELMEYER FERREIRA  and
MARILISE BRITTES ROTT
ALEMAO G. CARPINTEYRO SÁNCHEZ
Affiliation:
Programa de Pós-graduação em Microbiologia Agrícola e do Ambiente, Instituto de Ciencias Básicas e da Saúde, UFRGS, Porto Alegre, RS, Brazil
VERIDIANA GOMES VIRGINIO
Affiliation:
Laboratório de Genômica Estrutural e Funcional, Centro de Biotecnologia, UFRGS, Porto Alegre, RS, Brazil
VINICIUS JOSÉ MASCHIO
Affiliation:
Programa de Pós-graduação em Microbiologia Agrícola e do Ambiente, Instituto de Ciencias Básicas e da Saúde, UFRGS, Porto Alegre, RS, Brazil
HENRIQUE BUNSELMEYER FERREIRA
Affiliation:
Laboratório de Genômica Estrutural e Funcional, Centro de Biotecnologia, UFRGS, Porto Alegre, RS, Brazil Departamento de Biologia Molecular e Biotecnologia, Instituto de Biociências, UFRGS, Porto Alegre, RS, Brazil
MARILISE BRITTES ROTT*
Affiliation:
Programa de Pós-graduação em Microbiologia Agrícola e do Ambiente, Instituto de Ciencias Básicas e da Saúde, UFRGS, Porto Alegre, RS, Brazil Departamento de Parasitologia, Instituto de Ciências Basicas da Saúde, UFRGS, Porto Alegre, RS, Brazil
*
*Corresponding author: Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, RS, Porto Alegre, Brazil. E-mail: marilise.rott@ufrgs.br
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Summary

Acanthamoeba spp. are free-living protists widely distributed in environment, able to cause keratitis, encephalitis and skin lesions in humans and animals. Acanthamoeba spp. exist in two forms: an infective trophozoite and a dormant cyst. Several factors contribute to the pathogenesis of Acanthamoeba spp. The parasite adhesion to the host cell is the primary step for infection and is mediated by a mannose binding-protein, expressed in the surface and considered the main pathogenicity factor in Acanthamoeba spp. So far, there was no evidence of another surface protein of Acanthamoeba spp. relevant for host invasion or infection by these organisms. The aims of this study were to identify and characterize an Acanthamoeba castellanii surface protein and to evaluate its diagnostic potential. In silico predictions of surface proteins allowed to identify the A. castellanii calreticulin as a possible surface antigen. The coding sequence of a predicted extracellular domain of A. castellanii calreticulin was cloned by in vivo homologous recombination and the recombinant polypeptide (AcCRT29–130) was produced. Its immunodiagnostic potential was assessed in a recombinant antigen-based ELISA with sera from experimentally infected rats that developed keratitis and encephalitis, and sera from patients with encephalitis. The AcCRT29–130 was significantly more recognized by sera from encephalitis infected rats in comparison with the non-infected controls. Human sera from encephalitis patients, however presented no significant response. These results showed the AcCRT29–130 potential for A. castellanii infection immunodiagnosis in animals, with further studies being required for assessment of its use for human infections.

Keywords

Acanthamoeba castellaniicalreticulinrecombinant proteinimmunodiagnosticELISA
Type
Research Article
Information
Parasitology , Volume 143 , Issue 12 , October 2016 , pp. 1656 - 1664
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Copyright
Copyright © Cambridge University Press 2016 

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References

Aguillón, J. C., Harris, R., Molina, M. C., Colombo, A., Cortés, C., Hermosilla, T., Carreño, P., Orn, A. and Ferreira, A. (1997). Recognition of an immunogenetically selected Trypanosoma cruzi antigen by seropositive chagasic human sera. Acta Tropica 63, 159–166.Google Scholar
Aljanabi, S. M. and Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692–4693.Google Scholar
Atassi, M. Z. (1975). Antigenic structure of myoglobin: the complete immunochemical anatomy of a protein and conclusions relating to antigenic structures of proteins. Immunochemistry 12, 423–438.Google Scholar
Atassi, M. Z. (1978). Precise determination of the entire antigenic structure of lysozyme: molecular features of protein antigenic structures and potential of “surface-simulation” synthesis – a powerful new concept for protein binding sites. Immunochemistry 15, 909–936.Google Scholar
Baig, A. M. (2015). Pathogenesis of amoebic encephalitis: are the amoebae being credited to an ‘inside job’ done by the host immune response? Acta Tropica 148, 72–76.Google Scholar
Bouheraoua, N., Gaujoux, T., Goldschmidt, P., Chaumeil, C., Laroche, L. and Borderie, V. M. (2013). Prognostic factors associated with the need for surgical treatments in Acanthamoeba keratitis. Cornea 32, 130–136.Google Scholar
Capilla, J., Maffei, C. M., Clemons, K. V., Sobel, R. A. and Stevens, D. A. (2006). Experimental systemic infection with Cryptococcus neoformans var. grubii and Cryptococcus gattii in normal and immunodeficient mice. Medical Mycology 44, 601–610.Google Scholar
Clarke, D. W. and Niederkorn, J. Y. (2006). The pathophysiology of Acanthamoeba keratitis. Trends in Parasitology 22, 175–180.Google Scholar
Clarke, M., Lohan, A. J., Liu, B., Lagkouvardos, I., Roy, S., Zafar, N., Bertelli, C., Schilde, C., Kianianmomeni, A., Bürglin, T. R., Frech, C., Turcotte, B., Kopec, K. O., Synnott, J. M., Choo, C., Paponov, I., Finkler, A., Heng Tan, C. S., Hutchins, A. P., Weinmeier, T., Rattei, T., Chu, J. S., Gimenez, G., Irimia, M., Rigden, D. J., Fitzpatrick, D. A., Lorenzo-Morales, J., Bateman, A., Chiu, C. H., Tang, P. et al. (2013). Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biology 14, R11.Google Scholar
Coppolino, M. G. and Dedhar, S. (1998). Calreticulin. International Journal of Biochemistry & Cell Biology 30, 553–558.Google Scholar
Corsaro, D., Walochnik, J., Köhsler, M. and Rott, M. B. (2015). Acanthamoeba misidentification and multiple labels: redefining genotypes T16, T19, and T20 and proposal for Acanthamoeba micheli sp. nov. (genotype T19). Parasitology Research 114, 2481–2490.Google Scholar
Ferreira, V., Molina, M. C., Valck, C., Rojas, A., Aguilar, L., Ramírez, G., Schwaeble, W. and Ferreira, A. (2004). Role of calreticulin from parasites in its interaction with vertebrate hosts. Molecular Immunology 40, 1279–1291.Google Scholar
Garate, M., Alizadeh, H., Neelam, S., Niederkorn, J. Y. and Panjwani, N. (2006). Oral immunization with Acanthamoeba castellanii mannose-binding protein ameliorates amoebic keratitis. Infection and Immunity 74, 7032–7034.Google Scholar
Girard-Misguich, F., Sachse, M., Santi-Rocca, J. and Guillén, N. (2008). The endoplasmic reticulum chaperone calreticulin is recruited to the uropod during capping of surface receptors in Entamoeba histolytica . Molecular and Biochemical Parasitology 157, 236–240.Google Scholar
González, E., Rico, G., Mendoza, G., Ramos, F., García, G., Morán, P., Valadez, A., Melendro, E. I. and Ximénez, C. (2002). Calreticulin-like molecule in trophozoites of Entamoeba histolytica HM1:IMSS (Swissprot: accession P83003). American Journal of Tropical Medicine and Hygiene 67, 636–639.Google Scholar
González, E., de Leon, M. E. C., Meza, I., Ocadiz-Delgado, R., Gariglio, P., Silva-Olivares, A., Galindo-Gómez, S., Shibayama, M., Morán, P., Valadez, A., Limón, A., Rojas, L., Hernández, E. G., Cerritos, R. and Ximenez, C. (2011). Entamoeba histolytica calreticulin: an endoplasmic reticulum protein expressed by trophozoites into experimentally induced amoebic liver abscesses. Parasitology Research 108, 439–449.Google Scholar
Hopp, T. P. and Woods, K. R. (1981). Prediction of protein antigenic determinants from amino acid sequences. Proceedings of the National Academy of Sciences of the United States of America 78, 3824–3828.Google Scholar
Karkowska-Kuleta, J. and Kozik, A. (2014). Moonlighting proteins as virulence factors of pathogenic fungi, parasitic protozoa and multicellular parasites. Molecular Oral Microbiology 29, 270–283.Google Scholar
Kennett, M. J., Hook, R. R., Franklin, C. L. and Riley, L. K. (1999). Acanthamoeba castellanii: characterization of an adhesin molecule. Experimental Parasitology 92, 161–169.Google Scholar
Khan, N. A. (2006). Acanthamoeba: biology and increasing importance in human health. FEMS Microbiology Reviews 30, 564–595.Google Scholar
Khan, N. A., Greenman, J., Topping, K. P., Hough, V. C., Temple, G. S. and Paget, T. A. (2000). Isolation of Acanthamoeba-specific antibodies from a bacteriophage display library. Journal of Clinical Microbiology 38, 2374–2377.Google Scholar
Kong, H. H. and Pollard, T. D. (2002). Intracellular localization and dynamics of myosin-II and myosin-IC in live Acanthamoeba by transient transfection of EGFP fusion proteins. Journal of Cell Science 115, 4993–5002.Google Scholar
Laughlin, R. C. and Temesvari, L. A. (2005). Cellular and molecular mechanisms that underlie Entamoeba histolytica pathogenesis: prospects for intervention. Expert Reviews in Molecular Medicine 7, 1–19.Google Scholar
Leher, H., Kinoshita, K., Alizadeh, H., Zaragoza, F. L., He, Y. and Niederkorn, J. (1998). Impact of oral immunization with Acanthamoeba antigens on parasite adhesion and corneal infection. Investigative Ophthalmology & Visual Science 39, 2337–2343.Google Scholar
Lorenzo-Morales, J., Martín-Navarro, C. M., López-Arencibia, A., Arnalich-Montiel, F., Piñero, J. E. and Valladares, B. (2013). Acanthamoeba keratitis: an emerging disease gathering importance worldwide? Trends in Parasitology 29, 181–187.Google Scholar
Lorenzo-Morales, J., Khan, N. A. and Walochnik, J. (2015). An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite 22, 10.Google Scholar
Marcelain, K., Colombo, A., Molina, M. C., Ferreira, L., Lorca, M., Aguillón, J. C. and Ferreira, A. (2000). Development of an immunoenzymatic assay for the detection of human antibodies against Trypanosoma cruzi calreticulin, an immunodominant antigen. Acta Tropica 75, 291–300.Google Scholar
Martínez, M. J., Vogel, M., Stoppel, J., Charlin, R., Squella, O., Srur, M., Traipe, L., Verdaguer, J. and Suárez, M. (1997). [Herpetic keratitis: clinical-virological correlation]. Revista Medica de Chile 125, 659–664.Google Scholar
Mendlovic, F. (2010). Calreticulin: a multifaceted protein. In Nature Education, Vol. 4 (ed. Conconi, M.). Universidad Autónoma de México, Universidad Anahuac, Medicina.Google Scholar
Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I. and Opas, M. (2009). Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochemical Journal 417, 651–666.Google Scholar
Na, B. K., Cho, J. H., Song, C. Y. and Kim, T. S. (2002). Degradation of immunoglobulins, protease inhibitors and interleukin-1 by a secretory proteinase of Acanthamoeba castellanii . Korean Journal of Parasitology 40, 93–99.Google Scholar
Novotný, J., Handschumacher, M., Haber, E., Bruccoleri, R. E., Carlson, W. B., Fanning, D. W., Smith, J. A. and Rose, G. D. (1986). Antigenic determinants in proteins coincide with surface regions accessible to large probes (antibody domains). Proceedings of the National Academy of Sciences of the United States of America 83, 226–230.Google Scholar
Parrish, J. R., Limjindaporn, T., Hines, J. A., Liu, J., Liu, G. and Finley, R. L. (2004). High-throughput cloning of Campylobacter jejuni ORfs by in vivo recombination in Escherichia coli. Journal of Proteome Research 3, 582–586.Google Scholar
Pollard, T. D. and Ostap, E. M. (1996). The chemical mechanism of myosin-I: implications for actin-based motility and the evolution of the myosin family of motor proteins. Cell Structure and Function 21, 351–356.CrossRefGoogle ScholarPubMed
Ricciardi, A. and Ndao, M. (2015). Diagnosis of parasitic infections: what's going on? Journal of Biomolecular Screening 20, 6–21.Google Scholar
Rokeach, L. A., Zimmerman, P. A. and Unnasch, T. R. (1994). Epitopes of the Onchocerca volvulus RAL1 antigen, a member of the calreticulin family of proteins, recognized by sera from patients with onchocerciasis. Infection and Immunity 62, 3696–3704.Google Scholar
Schumacher, D. J., Tien, R. D. and Lane, K. (1995). Neuroimaging findings in rare amebic infections of the central nervous system. AJNR American Journal of Neuroradiology 16, 930–935.Google ScholarPubMed
Schuster, F. L. (2002). Cultivation of pathogenic and opportunistic free-living amebas. Clinical Microbiology Reviews 15, 342–354.Google Scholar
Shirwadkar, C. G., Samant, R., Sankhe, M., Deshpande, R., Yagi, S., Schuster, F. L., Sriram, R. and Visvesvara, G. S. (2006). Acanthamoeba encephalitis in patient with systemic lupus, India. Emerging Infectious Diseases 12, 984–986.Google Scholar
Siqueira, F. M., Thompson, C. E., Virginio, V. G., Gonchoroski, T., Reolon, L., Almeida, L. G., da Fonsêca, M. M., de Souza, R., Prosdocimi, F., Schrank, I. S., Ferreira, H. B., de Vasconcelos, A. T. and Zaha, A. (2013). New insights on the biology of swine respiratory tract mycoplasmas from a comparative genome analysis. BMC Genomics 14, 175.CrossRefGoogle ScholarPubMed
Smith, D. B. and Johnson, K. S. (1988). Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31–40.Google Scholar
Soto-Arredondo, K. J., Flores-Villavicencio, L. L., Serrano-Luna, J. J., Shibayama, M. and Sabanero-López, M. (2014). Biochemical and cellular mechanisms regulating Acanthamoeba castellanii adherence to host cells. Parasitology 141, 531–541.Google Scholar
Suchitra, S. and Joshi, P. (2005). Characterization of Haemonchus contortus calreticulin suggests its role in feeding and immune evasion by the parasite. Biochimica et Biophysica Acta 1722, 293–303.Google Scholar
Szentmáry, N., Goebels, S., Matoula, P., Schirra, F. and Seitz, B. (2012). Acanthamoeba keratitis – a rare and often late diagnosed disease. Klin Monbl Augenheilkd 229, 521–528.Google Scholar
Thornton, J. M., Edwards, M. S., Taylor, W. R. and Barlow, D. J. (1986). Location of ‘continuous’ antigenic determinants in the protruding regions of proteins. EMBO Journal 5, 409–413.Google Scholar
Vaithilingam, A., Teixeira, J. E., Miller, P. J., Heron, B. T. and Huston, C. D. (2012). Entamoeba histolytica cell surface calreticulin binds human c1q and functions in amebic phagocytosis of host cells. Infection and Immunity 80, 2008–2018.CrossRefGoogle ScholarPubMed
Virginio, V. G., Hernández, A., Rott, M. B., Monteiro, K. M., Zandonai, A. F., Nieto, A., Zaha, A. and Ferreira, H. B. (2003). A set of recombinant antigens from Echinococcus granulosus with potential for use in the immunodiagnosis of human cystic hydatid disease. Clinical & Experimental Immunology 132, 309–315.Google Scholar
Virginio, V. G., Gonchoroski, T., Paes, J. A., Schuck, D. C., Zaha, A. and Ferreira, H. B. (2014). Immune responses elicited by Mycoplasma hyopneumoniae recombinant antigens and DNA constructs with potential for use in vaccination against porcine enzootic pneumonia. Vaccine 32, 5832–5838.Google Scholar
Visvesvara, G. S. (2013). Infections with free-living amebae. Handbook of Clinical Neurology 114, 153–168.Google Scholar
Visvesvara, G. S., Moura, H. and Schuster, F. L. (2007). Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea . FEMS Immunology and Medical Microbiology 50, 1–26.Google Scholar
Ximénez, C., González, E., Nieves, M. E., Silva-Olivares, A., Shibayama, M., Galindo-Gómez, S., Escobar-Herrera, J., García de León, M. E. C., Morán, P., Valadez, A., Rojas, L., Hernández, E. G., Partida, O. and Cerritos, R. (2014). Entamoeba histolytica and E. dispar Calreticulin: inhibition of classical complement pathway and differences in the level of expression in amoebic liver abscess. Biomed Research International 2014, 127453.Google Scholar
Yang, Z., Cao, Z. and Panjwani, N. (1997). Pathogenesis of Acanthamoeba keratitis: carbohydrate-mediated host-parasite interactions. Infection and Immunity 65, 439–445.Google Scholar