Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-20T07:41:27.302Z Has data issue: false hasContentIssue false

Characterization of acid phosphatases from marine scuticociliate parasites and their activation by host's factors

Published online by Cambridge University Press:  18 April 2011

I. SALINAS*
Affiliation:
National Institute of Water and Atmospheric Research Ltd, Private Bag 14-901, Kilbirnie, Wellington 6241, New Zealand
E. W. MAAS
Affiliation:
National Institute of Water and Atmospheric Research Ltd, Private Bag 14-901, Kilbirnie, Wellington 6241, New Zealand
P. MUÑOZ
Affiliation:
Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Murcia, Murcia, Spain
*
*Corresponding author: National Institute of Water and Atmospheric Research Ltd, Private Bag 14-901, Kilbirnie, Wellington 6241, New Zealand. Tel: +64 4 3860 535. Fax: +64 4 3860 574. E-mail: [email protected]

Summary

Scuticociliates are histophagous marine parasites that cause mortality in fish. Acid phosphatases (AcPs) are considered virulence factors and they are used by different parasites to dephosphorylate host molecules. The aim of this work was to characterize the AcPs from 3 scuticociliate species, Uronema marinum, Miamiensis avidus and Parauronema virginianum, which parasitize marine finfish species. We identified AcP activity (pH 5·2) with differential cellular distribution in the 3 parasite species. Native gel electrophoresis of ciliate lysates revealed the presence of 1 high molecular weight AcP activity band in M. avidus (tartrate-sensitive), several low molecular weight AcPs in U. marinum and 1 low molecular weight band only in P. virginianum (tartrate-resistant). Scuticociliate AcP was inhibited by specific inhibitors of tyrosine protein phosphatases. AcP decreased upon starvation but rapid reactivation occurred following exposure to skin mucus. Groper (Polyprion oxygeneios) peripheral blood leucocytes (PBLs) and, to a lesser extent, red blood cells, also increased AcP activity. Protein tyrosine phosphatase PTP1b was primarily detected in the plasma membrane of M. avidus and ingestion of groper PBLs upregulated its expression. M. avidus recovered from experimentally infected groper had greater levels of PTP1b expression than the injected suspension. The present results highlight the importance of PTPs in histophagous parasites and their interaction with fish host's factors.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

Aguirre-García, M. M. and Okhuysen, P. C. (2007). Cryptosporidium parvum: identification and characterization of an acid phosphatase. Parasitology Research 101, 8589.CrossRefGoogle ScholarPubMed
Aguirre-García, M. M., Escalona-Montaño, A. R., Bakalara, N., Pérez-Torres, A., Gutiérrez-Kobeh, L. and Becker, I. (2006). Leishmania major: detection of membrane-bound protein tyrosine phosphatase. Parasitology 132, 641649.Google Scholar
Anderson, S. A., Hulston, D. A., Mcveagh, S. M., Webb, V. L. and Smith, P. J. (2009). In vitro culture and cryopreservation of Uronema marinum isolated from farmed New Zealand groper (Polyprion oxygeneios). Journal of Microbiological Methods 79, 6266.Google Scholar
Azad, I. S., Al-Marzouk, A., James, C. M., Almatar, S. and Al-Gharabally, H. (2007). Scuticociliatosis-associated mortalities and histopathology of natural infection in cultured silver pomfret (Pampus argenteus Euphrasen) in Kuwait. Aquaculture 262, 202210.Google Scholar
Baca, O. G., Roman, M. J., Glew, R. H., Christner, R. T. F., Buhler, J. E., Adam, S. and Aragon, A. S. (1993). Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infection and Immunity 61, 42324239.Google Scholar
Bakalara, N., Santarelli, X., Davis, C. and Baltz, T. (2000). Purification, cloning, and characterization of an acidic ectoprotein phosphatase differentially expressed in the infectious bloodstream form of Trypanosoma brucei. Journal of Biological Chemistry 275, 88638871.Google Scholar
Bliska, J. B. and Black, D. S. (1995). Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase. Infection and Immunity 63, 681685.Google Scholar
Braun, M., Waheed, A. and Von Figura, K. (1989). Lysosomal acid phosphatase is transported to lysosomes via the cell surface. EMBO Journal 8, 36333640.Google Scholar
Cosentino-Gomes, D., Russo-Abrahão, T., Fonseca-De-Souza, A. L., Rodrigues-Ferreira, C. R., Galina, A. and Meyer-Fernandes, J. R. (2009). Modulation of Trypanosoma rangeli ecto-phosphatase activity by hydrogen peroxide. Free Radical Biology and Medicine 47, 152158.CrossRefGoogle ScholarPubMed
Escalona-Montaño, A. R., Pardavé-Alejandre, D., Cervantes-Sarabia, R., García-López, P., Gutiérrez-Quiroz, M., Gutiérrez-Kobeh, L., Becker-Fauser, I. and Aguirre-García, M. M. (2010). Leishmania mexicana promastigotes secrete a protein tyrosine phosphatase. Parasitology Research 107, 309315.CrossRefGoogle ScholarPubMed
Furuya, T., Zhong, L., Meyer-Fernandes, J. R., Lu, H-G., Moreno, Snj and Docampo, R. (1998). Ecto-protein tyrosine phosphatase activity in Trypanosoma cruzi infective stages. Molecular and Biochemical Parasitology 92, 339348.CrossRefGoogle ScholarPubMed
Ghosh, D. and Chakraborty, P. (2002). Involvement of protein tyrosine kinases and phosphatases in uptake and intracellular replication of virulent and avirulent Leishmania donovani promastigotes in mouse macrophage cells. Bioscience Reports 22, 395406.CrossRefGoogle ScholarPubMed
Gomori, G. (1952). Microscopic Histochemistry: Principles and Practice. University of Chicago Press, Chicago, IL, USA.Google Scholar
Guan, K. L. and Dixon, J. E. (1990). Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249, 553556.CrossRefGoogle ScholarPubMed
Hamid, N., Gustavsson, A., Andersson, K., Mcgee, K., Persson, C., Rudd, C. E. and Fallman, M. (1999). YopH dephosphorylates Cas and Fyn-binding protein in macrophages. Microbial Pathogenesis 27, 231242.CrossRefGoogle ScholarPubMed
Harikrishnan, R., Balasundaram, C. and Heo, M. S. (2010). Scuticociliatosis and its recent prophylactic measures in aquaculture with special reference to South Korea Taxonomy, diversity and diagnosis of scuticociliatosis: Part I Control strategies of scuticociliatosis: Part II. Fish & Shellfish Immunology 29, 1531.Google Scholar
Iglesias, R., Parama, A., Alvarez, M. F., Leiro, J., Fernandez, J. and Sanmartin, M. L. (2001). Philasterides dicentrarchi (Ciliophora, Scuticociliatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Diseases of Aquatic Organisms 46, 4755.Google Scholar
Jee, B. Y., Kim, Y. C. and Park, M. S. (2001). Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms 47, 4955.CrossRefGoogle ScholarPubMed
Jung, S. J., Kitamura, S., Song, J. Y. and Oh, M. J. (2007). Miamiensis avidus (Ciliophora: Scuticociliatida) causes systemic infection of olive flounder Paralichthys olivaceus and is a senior synonym of Philasterides dicentrarchi. Diseases of Aquatic Organisms 18, 227234.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680685.CrossRefGoogle ScholarPubMed
Leibowitz, P., Ofir, M., Golan-Goldhirsh, R. and Zilberg, A. D. (2009). Cysteine proteases and acid phosphatases contribute to Tetrahymena spp. pathogenicity in guppies, Poecilia reticulate. Veterinary Parasitology 166, 2126.Google Scholar
Lonsdale-Eccles, J. D. and Grab, D. J. (2002). Trypanosome hydrolases blood stream barrier. Trends in Parasitology 18, 1719.Google Scholar
Marzouk, A. and Azad, I. S. (2007). Growth kinetics, protease activity and histophagous capability of Uronema sp. infesting cultured silver pomfret Pampus argenteus in Kuwait. Diseases of Aquatic Organisms 76, 4956.CrossRefGoogle ScholarPubMed
Matthews, R. A. (2005). Ichthyophthirius multifiliis Fouquet and Ichthyophthiriosis in freshwater teleosts. Advances in Parasitology 59, 159241.Google Scholar
Mohapatra, N. P., Balagopal, A., Shilpa, S., Schlesinger, L. S. and Gunn, J. S. (2007). AcpA is a Francisella acid phosphatase that affects intramacrophage survival and virulence. Infection and Immunity 75, 390396.Google Scholar
Müller, I. B., Knöckel, J., Eschbach, M. L., Bergmann, B., Walter, R. D. and Wrenger, C. (2010). Secretion of an acid phosphatase provides a possible mechanism to acquire host nutrients by Plasmodium falciparum. Cellular Microbiology 12, 677691.Google Scholar
Olivier, M., Romero-Gallo, B. J., Matte, C., Blanchette, J., Posner, B. I., Tremblay, M. J. and Faure, R. (1998). Modulation of interferon-γ induced macrophage activation by phosphotyrosine phosphatase inhibition. Journal of Biological Chemistry 273, 1394413949.Google Scholar
Parama, A., Castro, R., Arranz, J. A., Sanmartin, M. L., Lamas, J. and Leiro, J. (2007). Scuticociliate cysteine proteinases modulate turbot leucocyte functions. Fish & Shellfish Immunology 23, 945956.CrossRefGoogle ScholarPubMed
Paramá, A., Iglesias, R., Alvarez, M. F., Leiro, J., Ubeira, F. M. and Sanmartín, M. L. (2004). Cysteine proteinase activities in the fish pathogen Philasterides dicentrarchi (Ciliophora: Scuticociliatida). Parasitology 128, 541548.CrossRefGoogle ScholarPubMed
Saha, A. K., Das, S., Robert, H., Glew, R. H. and Gottlieb, M. (1985). Resistance of Leishmanial Phosphatases to Inactivation by Oxygen Metabolites. Journal of Clinical Microbiology 22, 329332.Google Scholar
Seaman, G. R. (1961). Acid phosphatase activity associated with phagotrophy in the ciliate, Tetrahymena. Journal of Biophysical and Biochemical Cytology 9, 243245.Google Scholar
Shenberg, S. (2003). Histopathology of the ciliate Tetrahymena corlissi infection in guppy Poecilia reticulata. M.Sc. thesis, The Hebrew University of Jerusalem, Jerusalem, Israel.Google Scholar
Shephard, K. L. (1994). Functions for fish mucus. Reviews in Fish Biology and Fisheries 4, 401429.CrossRefGoogle Scholar
Smith, P. J., Mcveagh, S. M., Hulston, D., Anderson, S. A. and Gublin, Y. (2009). DNA identification of ciliates associated with disease outbreaks in a New Zealand marine fish hatchery. Diseases of Aquatic Organisms 86, 163167.CrossRefGoogle Scholar
Song, J. Y., Sasaki, K., Okada, T., Sakashita, M., Kawakami, H., Matsuoka, S., Kang, H. S., Nakayama, K., Jung, S. J., Oh, M. J. and Kitamura, S. I. (2009). Antigenic differences of the scuticociliate Miamiensis avidus from Japan. Journal of Fish Diseases 32, 10271034.Google Scholar
Szöor, B., Wilson, J., Mcelhinney, H., Tabernero, L. and Matthews, K. R. (2006). Protein tyrosine phosphatase TbPTP1: a molecular switch controlling life cycle differentiation in trypanosomes. Journal of Cell Biology 175, 293303.Google Scholar
Tiedtke, A. and Görtz, H. D. (1983). Acid phosphatase associated with discharging secretory vesicles (mucocysts) of Tetrahymena thermophila. European Journal of Cell Biology 30, 254257.Google ScholarPubMed
Volety, A. K. and Chu, F. L. E. (1997). Acid phosphatase activity in Perkinsus marinus, the protistan parasite of the American oyster, Crassostrea virginica. Journal of Parasitology 83, 10931098.Google Scholar