Dynamics of Theileria orientalis genotype population in cattle in a year-round grazing system

Tatsunori Masatani; Shunpei Yoshihara; Atsuko Matsubara; Takafumi Gotoh; Hideyuki Takahashi; Tetsuya Tanaka; Masako Andoh; Yasuyuki Endo; Tomohide Matsuo

doi:10.1515/ap-2016-0056

Article

Dynamics of Theileria orientalis genotype population in cattle in a year-round grazing system

Tatsunori Masatani , Shunpei Yoshihara , Atsuko Matsubara , Takafumi Gotoh , Hideyuki Takahashi , Tetsuya Tanaka , Masako Andoh , Yasuyuki Endo and Tomohide Matsuo

Published/Copyright: March 30, 2016

Published by

Become an author with De Gruyter Brill

Author Information

From the journal Acta Parasitologica Volume 61 Issue 2

Abstract

Theirelia orientalis is a tick-borne haemoprotozoan parasite, and infection with this parasite is one of the most important diseases for grazing cattle. Co-infection of cattle with different genotypes of T. orientalis often occurs. In this study, we investigated the temporal dynamics of genotypes in cattle in a year-round grazing system in Japan. Genotype-specific PCR assays to determine major piroplasm surface protein (MPSP) genotypes (types 1 to 5) of T. orientalis were performed by using time-course blood samples collected from grazing cattle and ticks in a pasture. All 20 cattle investigated in this study were infected with T. orientalis. By using genotype-specific PCR, we detected the combination of genotypes of T. orientalis (types 1 to 5) from each cattle. These multiple genotypes of T. orientalis were also confirmed in ticks. Notably, each genotype of T. orientalis in cattle was temporally detected from cattle and more variable genotypes were found in summer. The observed temporal dynamics of the MPSP genotypes of T. orientalis in cattle could be explained by host immunity against the parasites or genetic recombination of parasite in ticks.

Key words: Cattle; MPSP; PCR; Theileria orientalis; Tick

Tatsunori Masatani and Shunpei Yoshihara contributed equally to this work and should be consider as first co-authors

Acknowledgements

We thank Mrs. T. Etoh, Y. Shiotsuka, and R. Fujino, Kuju Agricultural Research Center of Kyushu University, for help in collecting samples. This study was partially supported by a Grant-in-Aid for Scientific Research (KAKENHI) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (23292173 and 15H05264).

References

Beugnet F. and Chardonnet L. 1995. Tick resistance to pyrethroids in New Caledonia. Veterinary Parasitology, 56, 325–338. DOI: 10.1016/0304-4017(94)00686-710.1016/0304-4017(94)00686-7Search in Google Scholar

Beugnet F., Costa R, Chardonnet L. 1994. Adaptation of strategies of tick control to the problem of drug resistance: Boophilus microplus in New Caledonia. Revue De Medicine Veterinaire, 145, 931–940Search in Google Scholar

Bruce D. and Mazhowl W. 1992. Synthetic pyrethroid resistance in Boophilus decoloratus: a case report. Zimbabwe Veterinary Journal, 26, 127–131Search in Google Scholar

Eamens G.J., Bailey G., Gonsalves J.R., Jenkins C. 2013a. Distribution and temporal prevalence of Theileria orientalis major piroplasm surface protein types in eastern Australian cattle herds. Australian Veterinary Journal, 91, 332–340. DOI: 10.1111/avj.1207810.1111/avj.12078Search in Google Scholar

Eamens G.J., Bailey G., Jenkins C., Gonsalves J.R. 2013b. Significance of Theileria orientalis types in individual affected beef herds in New South Wales based on clinical, smear and PCR findings. Veterinary Parasitology, 196, 96–105. DOI: 10.1016/j.vetpar.2012.12.05910.1016/j.vetpar.2012.12.059Search in Google Scholar

Fujisaki K., Kawazu S., Kamio T. 1994. The taxonomy of the bovine Theileria spp. Parasitology Today, 10, 31–33. DOI: 10.1016/ 0169-4758(94)90355-710.1016/0169-4758(94)90355-7Search in Google Scholar

Hammer J.F., Emery D., Bogema D.R., Jenkins C. 2015. Detection of Theileria orientalis genotypes in Haemaphysalis longicornis ticks from southern Australia. Parasites and Vectors, 8, 229. DOI: 10.1186/s13071-015-0839-910.1186/s13071-015-0839-9Search in Google Scholar

Islam M.K., Jabbar A., Campbell B.E., Cantacessi C., Gasser R.B. 2011. Bovine theileriosis – an emerging problem in southeastern Australia? Infection, Genetics and Evolution, 11, 2095–2097. DOI: 10.1016/j.meegid.2011.08.01210.1016/j.meegid.2011.08.012Search in Google Scholar

Iwasaki T., Kakuda T., Sako Y., Sugimoto C., Onuma M. 1998. Differentiation and quantification of Theileria sergenti piroplasm types using type-specific monoclonal antibodies. Journal of Veterinary Medical Science, 60, 665–669. DOI: 10.1292/ jvms.60.66510.1292/jvms.60.665Search in Google Scholar

Jenkins C., Micallef M., Alex S.M., Collins D., Djordjevic S.P., Bogema D.R. 2015. Temporal dynamics and subpopulation analysis of Theileria orientalis genotypes in cattle. Infection, Genetics and Evolution, 32, 199–207. DOI: 10.1016/j.meegid. 2015.03.01710.1016/j.meegid.2015.03.017Search in Google Scholar

Kamio T., Ito Y., Fujisaki K., Minami T. 1990. Infection rates of Theileria sergenti in Haemaphysalis longicornis ticks collected from the field in Japan. Japanese Journal of Veterinary Science, 52, 43–48. DOI: 10.1292/jvms1939.52.4310.1292/jvms1939.52.43Search in Google Scholar

Kawazu S., Sugimoto C., Kamio T., Fujisaki K. 1992. Analysis of the genes encoding immunodominant piroplasm surface proteins to Theileria sergenti and Theileria buffeli by nucleotide sequencing and polymerase chain reaction. Molecular and Biochemical Parasitology, 56, 169–175. DOI: 10.1016/01666851(92)90164-F10.1016/0166-6851(92)90164-FSearch in Google Scholar

Kim J.Y., Yokoyama N., Kumar S., Inoue N., Yamaguchi T., Sentoku S., Fujisaki K., Sugimoto C. 2004. Molecular epidemiological survey of benign Theileria parasites of cattle in Japan: Detection of a new type of major piroplasm surface protein gene. Journal of Veterinary Medical Science, 66, 251–256. DOI: 10.1292/jvms.66.25110.1292/jvms.66.251Search in Google Scholar

Kubota S., Sugimoto C., Onuma M. 1995. A genetic analysis of mixed population in Theileria sergenti stocks and isolates using allele-specific polymerase chain reaction. Journal of Veterinary Medical Science, 57, 279–282. DOI: 10.1292/ jvms.57.27910.1292/jvms.57.279Search in Google Scholar

Kubota S., Sugimoto C., Onuma, M. 1996. Population dynamics of Theileria sergenti in persistently infected cattle and vector ticks analyzed by a polymerase chain reaction. Parasitology, 112, 437–442. DOI: 10.1017/S003118200007689710.1017/S0031182000076897Search in Google Scholar

MacHugh N.D., Burrells A.C., Morrison W.I. 2008. Demonstration of strain-specific CD8 T cell responses to Theileria annulata. Parasite Immunology, 30, 385–393. DOI: 10.1111/j.13653024.2008.01038.x10.1111/j.1365-3024.2008.01038.xSearch in Google Scholar

MacHugh N.D., Weir W., Burrells A., Lizundia R., Graham S.P., Taracha E.L., Shiels B.R., Langsley G., Morrison W.I. 2011. Extensive polymorphism and evidence of immune selection in a highly dominant antigen recognized by bovine CD8 T cells specific for Theileria annulata. Infection and Immunity, 79, 2059–2069. DOI: 10.1128/IAI.01285-1010.1128/IAI.01285-10Search in Google Scholar

McFadden A.M., Rawdon T.G., Meyer J., Makin J., Clough R.R., Tham K., Mullner P., Geysen D. 2011. An outbreak of haemolytic anaemia associated with infection of Theileria orientalis in native cattle. New Zealand Veterinary Journal, 59, 79–85. DOI: 10.1080/00480169.2011.55285710.1080/00480169.2011.552857Search in Google Scholar

McFadden A., Pulford D., Lawrence K., Frazer J., van Andel M., Donald J., Bingham P. 2013. Epidemiology of Theileria orientalis in cattle in New Zealand. Proceedings of the Society of Dairy Cattle Veterinarians of the NZVA Annual Conference (2013), 207–217Search in Google Scholar

Matsuba T., Kubota H., Tanaka M., Hattori M., Murata M., Sugimoto C., Onuma M. 1993. Analysis of mixed parasite populations of Theileria sergenti using cDNA probes encoding a major piroplasm surface protein. Parasitology, 107, 369–377. DOI: 10.1017/S003118200006771810.1017/S0031182000067718Search in Google Scholar

Nkhoma S.C., Nair S., Cheeseman I.H., Rohr-Allegrini C., Singlam S., Nosten F., Anderson T.J. 2012. Close kinship within multiple-genotype malaria parasite infections. Proceedings of the Royal Society B, DOI:10.1098/rspb.2012.011310.1098/rspb.2012.0113Search in Google Scholar

Onuma M., Kakuda T., Sugimoto C. 1998. Theileria parasite infection in East Asia and control of the diseases. Comparative Immunology, Microbiology and Infectious Diseases, 21, 165–177. DOI: 10.1016/S0147-9571(98)00008-310.1016/S0147-9571(98)00008-3Search in Google Scholar

Ota N., Mizuno D., Kuboki N., Igarashi I., Nakamura Y., Yamashina H., Hanzaike T., Fujii K., Onoe S., Hata H., Kondo S., Mat-sui S., Koga M., Matsumoto K., Inokuma H., Yokoyama N. 2009. Epidemiological survey of Theileria orientalis infection in grazing cattle in the eastern part of Hokkaido, Japan. Journal of Veterinary Medical Science, 71, 937–944. DOI: 10.1292/jvms.71.93710.1292/jvms.71.937Search in Google Scholar PubMed

Portugal S., Carret C., Recker M., Armitage A.E., Gonçalves L.A., Epiphanio S., Sullivan D., Roy C., Newbold C.I., Drakesmith H., Mota M.M. 2011. Host-mediated regulation of superinfection in malaria. Nature Medicine, 17, 732–737. DOI: 10.1038/nm.236810.1038/nm.2368Search in Google Scholar

Preston P.M., Hall F.R., Glass E.J., Campbell J.D., Darghouth M.A., Ahmed J.S., Shiels B.R., Spooner R.L., Jongejan F., Brown C.G. 1999. Innate and adaptive immune responses co-operate to protect cattle against Theileria annulata. Parasitol Today, 15, 268–274. DOI: 10.1016/S0169-4758(99)01466-010.1016/S0169-4758(99)01466-0Search in Google Scholar

Sako Y., Asada M., Kubota S., Sugimoto C., Onuma M. 1999. Molecular cloning and characterization of 23-kDa piroplasm surface proteins of Theileria sergenti and Theileria buffeli. International Journal for Parasitology, 29, 593–599. DOI: 10.1016/S0020-7519(99)00004-110.1016/S0020-7519(99)00004-1Search in Google Scholar

Shimizu S., Nojiri K., Matsunaga N., Yamane I., Minami T. 2000. Reduction in tick numbers (Haemaphysalis longicornis), mortality and incidence of Theileria sergenti infection in field-grazed calves treated with flumethrin pour-on. Veterinary Parasitology, 92, 129–138. DOI: 10.1016/S0304-4017(00) 00278-810.1016/S0304-4017(00)00278-8Search in Google Scholar

Shimizu S., Yoshiura N., Mizumoto T., Kongou, Y. 1992. Theileria sergenti infection in dairy cattle. Journal of Veterinary Medical Science, 54, 375–377. DOI: 10.1292/jvms.54.37510.1292/jvms.54.375Search in Google Scholar

Sivakumar, T., Hayashida, K., Sugimoto, C. and Yokoyama, N. 2014. Evolution and genetic diversity of Theileria. Infection, Genetics and Evolution, 27, 250–263. DOI: 10.1016/j.meegid. 2014.07.01310.1016/j.meegid.2014.07.013Search in Google Scholar

Tanaka M., Onoe S., Matsuba T., Katayama S., Yamanaka M., Yonemichi H., Hiramatsu K., Baek B.K., Sugimoto C., Onuma M. 1993. Detection of Theileria sergenti infection in cattle by polymerase chain reaction amplification of parasite-specific DNA. Journal of Clinical Microbiology, 31, 2565–256910.1128/jcm.31.10.2565-2569.1993Search in Google Scholar

Yamane I., Koiwai M., Tsutsui T., Hamaoka T. 2001. A survey of Theileria sergenti infection, daily weight gain and conception proportions in 85 herds of grazing heifers in Japan. Veterinary Parasitology, 99, 189–198. DOI: 10.1016/S0304-4017(01) 00458-710.1016/S0304-4017(01)00458-7Search in Google Scholar

Yokoyama N., Ueno A., Mizuno D., Kuboki N., Khukhuu A., Igarashi I., Miyahara T., Shiraishi T., Kudo R., Oshiro M., Zakimi S., Sugimoto C., Matsumoto K., Inokuma H. 2011. Genotypic diversity of Theileria orientalis detected from cattle grazing in Kumamoto and Okinawa prefectures of Japan. Journal of Veterinary Medical Science, 73, 305–312. DOI: 10.1292/jvms.10-026310.1292/jvms.10-0263Search in Google Scholar PubMed

Yokoyama N., Sivakumar T., Ota N., Igarashi I., Nakamura Y., Yamashina H., Matsui S., Fukumoto N., Hata H., Kondo S., Oshiro M., Zakimi S., Kuroda Y., Kojima N., Matsumoto K., Inokuma H. 2012. Genetic diversity of Theileria orientalis in tick vectors detected in Hokkaido and Okinawa, Japan. Infection, Genetics and Evolution, 12, 1669–1675. DOI: 10.1016/j.meegid.2012.07.00710.1016/j.meegid.2012.07.007Search in Google Scholar PubMed

Zakimi S., Kim J.Y., Oshiro M., Hayashida K., Fujisaki K., Sugimoto C. 2006. Genetic diversity of benign Theileria parasites of cattle in Okinawa prefecture. Journal of Veterinary Medical Science, 68, 1335–1338. DOI: 10.1292/jvms.68.133510.1292/jvms.68.1335Search in Google Scholar PubMed

Zhuang W., Sugimoto C., Matsuba T., Niinuma S., Murata M., Onuma M. 1994. Analysis of antigenic and genetic diversities of Theileria sergenti piroplasm surface proteins. Journal of Veterinary Medical Science, 56, 469–473. DOI: 10.1292/jvms.56.46910.1292/jvms.56.469Search in Google Scholar PubMed

Received: 2015-7-6

Revised: 2015-11-27

Accepted: 2016-1-19

Published Online: 2016-3-30

Published in Print: 2016-6-1

You are currently not able to access this content.

Articles in the same Issue

https://doi.org/10.1515/ap-2016-0056

Keywords for this article

Cattle; MPSP; PCR; Theileria orientalis; Tick