Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-05T23:24:43.820Z Has data issue: false hasContentIssue false

Isolation and characterization of a potentially virulent species Entamoeba nuttalli from captive Japanese macaques

Published online by Cambridge University Press:  27 July 2009

H. TACHIBANA*
Affiliation:
Department of Infectious Diseases, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan
T. YANAGI
Affiliation:
Animal Research Center for Tropical Infections, Nagasaki University, Nagasaki 852-8523, Japan
A. AKATSUKA
Affiliation:
Teaching and Research Support Center, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan
S. KOBAYASHI
Affiliation:
Department of Tropical Medicine and Parasitology, Keio University School of Medicine, Shinjuku-ku, Tokyo 160-8582, Japan
H. KANBARA
Affiliation:
Department of Protozoology, Institute of Tropical Medicine, Nagasaki University, Nagasaki 852-8523, Japan
V. TSUTSUMI
Affiliation:
Department of Infectomic and Molecular Pathogenesis, Center for Research and Advanced Studies, National Polytechnic Institute, Mexico City 07360, Mexico Research Center for Innovative Cancer Therapy, Kurume University School of Medicine, Kurume 830-0011, Japan
*
*Corresponding author: Department of Infectious Diseases, Tokai University School of Medicine, Isehara, Kanagawa 259-1193, Japan. Tel: +81 463 93 1121. Fax: +81 463 95 5450. E-mail: [email protected]

Summary

We have recently proposed revival of the name Entamoeba nuttalliCastellani, 1908 for a virulent amoeba (P19-061405 strain) isolated from a rhesus monkey (Macaca mulatta) and located phylogenetically between E. histolytica and E. dispar. In this study, E. nuttalli was isolated from feces of captive Japanese macaques (M. fuscata) in an open-air corral in Japan. The sequence of the 18S rRNA gene in the isolates differed from the P19-061405 strain in 2 nucleotide positions, but was identical to the EHMfas1 strain isolated previously from a cynomolgus monkey (M. fascicularis). One of the E. nuttalli isolates from Japanese macaques, named the NASA6 strain, was axenized and cloned. In isoenzyme analysis, the mobilities of hexokinase and phosphate glucose isomerase in the NASA6 strain were identical to those in the P19-061405 and EHMfas1 strains, but the mobility of phosphoglucomutase was different. These results were supported by gene analyses of these enzymes. Inoculation of NASA6 strain trophozoites into the liver of hamsters led to formation of an amoebic liver abscess. The liver lesions were characterized by extensive necrosis associated with inflammatory reactions. These results demonstrate that the NASA6 strain is potentially virulent and that E. nuttalli should be recognized as a common parasite in macaques.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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

Castellani, A. (1908). Note on a liver abscess of amoebic origin in a monkey. Parasitology 1, 101102.CrossRefGoogle Scholar
Chu, J. H., Lin, Y. S. and Wu, H. Y. (2007). Evolution and dispersal of three closely related macaque species, Macaca mulatta, M. cyclopis, and M. fuscata, in the eastern Asia. Molecular Phylogenetics and Evolution 43, 418429.CrossRefGoogle Scholar
Clark, C. G. (1995). Axenic cultivation of Entamoeba dispar Brumpt 1925, Entamoeba insolita Geiman and Wichterman 1937 and Entamoeba ranarum Grassi 1879. Journal of Eukaryotic Microbiology 42, 590593.CrossRefGoogle ScholarPubMed
Diamond, L. S. (1968). Techniques of axenic cultivation of Entamoeba histolytica Schaudinn, 1903 and E. histolytica-like amebae. Journal of Parasitology 54, 10471056.CrossRefGoogle ScholarPubMed
Diamond, L. S. and Clark, C. G. (1993). A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. Journal of Eukaryotic Microbiology 40, 340344.Google Scholar
Diamond, L. S., Harlow, D. R. and Cunnick, C. C. (1978). A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 431432.Google Scholar
Espinosa-Cantellano, M., Gonzáles-Robles, A., Chávez, B., Castañón, G., Argüello, C., Lázaro-Haller, A. and Martínez-Palomo, A. (1998). Entamoeba dispar: ultrastructure, surface properties and cytopathic effect. Journal of Eukaryotic Microbiology 45, 265272.CrossRefGoogle ScholarPubMed
Ghosh, S., Frisardi, M., Ramirez-Avila, L., Descoteaux, S., Sturm-Ramirez, K., Newton-Sanchez, O. A., Santos-Preciado, J. I., Ganguly, C., Lohia, A., Reed, S. and Samuelson, J. (2000). Molecular epidemiology of Entamoeba spp.: evidence of a bottleneck (Demographic sweep) and transcontinental spread of diploid parasites. Journal of Clinical Microbiology 38, 38153821.Google Scholar
Hayasaka, K., Fujii, K. and Horai, S. (1996). Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA. Molecular Biology and Evolution 13, 10441053.Google Scholar
Hegner, R. and Schumaker, E. (1928). Some intestinal amoebae and flagellates from the chimpanzee, three-toed sloth, sheep and guinea-pig. Journal of Parasitology 15, 3137.CrossRefGoogle Scholar
Kobayashi, S., Imai, E., Haghighi, A., Khalifa, S. A., Tachibana, H. and Takeuchi, T. (2005). Axenic cultivation of Entamoeba dispar in newly designed yeast extract-iron-gluconic acid-dihydroxyacetone-serum medium. Journal of Parasitology 91, 14.CrossRefGoogle ScholarPubMed
López-Revilla, R. and Gómez-Domínguez, R. (1988). Trophozoite and nuclear size, DNA base composition, and nucleotide sequence homology of several Entamoeba strains in axenic culture. Parasitology Research 74, 424430.CrossRefGoogle ScholarPubMed
Martínez-Palomo, A. (1993). Parasitic amebas of the intestinal tract. In Parasitic Protozoa, 2nd Edn., (ed. Kreier, J. P. and Baker, J. R.), Vol. 3, pp. 65141. Academic Press, San Diego, USA.CrossRefGoogle Scholar
McLean, I. W. and Nakane, P. K. (1974). Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 10771083.Google Scholar
Muriuki, S. M., Murugu, R. K., Munene, E., Karere, G. M. and Chai, D. C. (1998). Some gastro-intestinal parasites of zoonotic (public health) importance commonly observed in old world non-human primates in Kenya. Acta Tropica 71, 7382.CrossRefGoogle ScholarPubMed
Neal, R. A. (1966). Experimental studies on Entamoeba with reference to speciation. Advances in Parasitology 4, 151.Google ScholarPubMed
Perez-Tamayo, R., Martinez, R. D., Montfort, I., Becker, I., Tello, E. and Perez-Montfort, R. (1991). Pathogenesis of acute experimental amebic liver abscess in hamsters. Journal of Parasitology 77, 982988.CrossRefGoogle ScholarPubMed
Rivera, W. L. and Kanbara, H. (1999). Detection of Entamoeba dispar DNA in macaque feces by polymerase chain reaction. Parasitology Research 85, 493495.Google Scholar
Robinson, G. L. (1968). The laboratory diagnosis of human parasitic amoebae. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 285294.CrossRefGoogle ScholarPubMed
Sargeaunt, P. G. (1988). Zymodemes of Entamoeba histolytica. In Amebiasis: Human Infection by Entamoeba histolytica (ed. Ravdin, J. I.), pp. 370387. John Wiley & Sons, New York, USA.Google Scholar
Smith, J. M. and Meerovitch, E. (1985). Primates as a source of Entamoeba histolytica, their zymodeme status and zoonotic potential. Journal of Parasitology 71, 751756.Google Scholar
Suzuki, J., Kobayashi, S., Murata, R., Yanagawa, Y. and Takeuchi, T. (2007). Profiles of a pathogenic Entamoeba histolytica-like variant with variations in the nucleotide sequence of the small subunit ribosomal RNA isolated from a primate (De Brazza's guenon). Journal of Zoo and Wildlife Medicine 38, 471474.CrossRefGoogle ScholarPubMed
Tachibana, H., Cheng, X. J., Kobayashi, S., Fujita, Y. and Udono, T. (2000). Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitology Research 86, 537541.CrossRefGoogle ScholarPubMed
Tachibana, H., Cheng, X. J., Kobayashi, S., Matsubayashi, N., Gotoh, S. and Matsubayashi, K. (2001). High prevalence of infection with Entamoeba dispar, but not E. histolytica, in captive macaques. Parasitology Research 87, 1417.Google Scholar
Tachibana, H., Yanagi, T., Pandey, K., Cheng, X. J., Kobayashi, S., Sherchand, J. B. and Kanbara, H. (2007). An Entamoeba sp. strain isolated from rhesus monkey is virulent but genetically different from Entamoeba histolytica. Molecular and Biochemical Parasitology 153, 107114.Google Scholar
Takano, J., Narita, T., Tachibana, H., Shimizu, T., Komatsubara, H., Terao, K. and Fujimoto, K. (2005). Entamoeba histolytica and Entamoeba dispar infections in cynomolgus monkeys imported into Japan for research. Parasitology Research 97, 255257.Google Scholar
Takano, J., Narita, T., Tachibana, H., Terao, K. and Fujimoto, K. (2007). Comparison of Entamoeba histolytica DNA isolated from a cynomolgus monkey with human isolates. Parasitology Research 101, 539546.Google Scholar
Takano, J., Tachibana, H., Kato, M., Narita, T., Yanagi, T., Yasutomi, Y. and Fujimoto, K. (2009). DNA characterization of simian Entamoeba histolytica-like strains to differentiate them from Entamoeba histolytica. Parasitology Research 105, (in the Press). doi:10.1017/S00436-009-1480-3Google Scholar
Tsutsumi, V., Mena-Lopez, R., Anaya-Velazquez, F. and Martinez-Palomo, A. (1984). Cellular bases of experimental amebic liver abscess formation. American Journal of Pathology 117, 8191.Google Scholar
Tsutsumi, V. and Martínez-Palomo, A. (1988). Inflammatory reaction in experimental hepatic amebiasis. An ultrastructural study. American Journal of Pathology 130, 112119.Google Scholar
Tsutsumi, V. and Shibayama, M. (2006). Experimental amebiasis: a selected review of some in vivo models. Archives of Medical Research 37, 210220.Google Scholar
Verweij, J. J., Polderman, A. M. and Clark, C. G. (2001). Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. Journal of Clinical Microbiology 39, 16441646.Google Scholar
Verweij, J. J., Vermeer, J., Brienen, E. A., Blotkamp, C., Laeijendecker, D., van Lieshout, L. and Polderman, A. M. (2003). Entamoeba histolytica infections in captive primates. Parasitology Research 90, 100103.Google Scholar
Wenyon, C. M. (1965). Protozoology: A Manual for Medical Men, Veterinarians and Zoologists. Hafner Publishing Company, New York, USA.Google Scholar
World Health Organization (1997). Amoebiasis. Weekly Epidemiological Record 72, 9799.Google Scholar