Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-11T08:42:49.324Z Has data issue: false hasContentIssue false

Expression of sheep pathogen Babesia sp. Xinjiang rhoptry-associated protein 1 and evaluation of its diagnostic potential by enzyme-linked immunosorbent assay

Published online by Cambridge University Press:  17 October 2016

QINGLI NIU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
ZHIJIE LIU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
JIFEI YANG
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
PEIFA YU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
YUPING PAN
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
BINTAO ZHAI
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
JIANXUN LUO
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
GUIQUAN GUAN*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China
HONG YIN*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, People's Republic of China
*
*Corresponding authors. State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China. E-mail: guanguiquan@caas.cn; yinhong@caas.cn
*Corresponding authors. State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Xujiaping 1, Lanzhou, Gansu 730046, People's Republic of China. E-mail: guanguiquan@caas.cn; yinhong@caas.cn

Summary

Ovine babesiosis is one of the most important tick-borne haemoparasitic diseases of small ruminants. The ovine parasite Babesia sp. Xinjiang is widespread in China. In this study, recombinant full-length XJrRAP-1aα2 (rhoptry-associated protein 1aα2) and C-terminal XJrRAP-1aα2 CT of Babesia sp. Xinjiang were expressed and used to evaluate their diagnostic potential for Babesia sp. Xinjiang infections by indirect enzyme-linked immunosorbent assay (ELISA). Purified XJrRAP-1aα2 was tested for reactivity with sera from animals experimentally infected with Babesia sp. Xinjiang and other haemoparasites using Western blotting and ELISA. The results showed no cross-reactivities between XJrRAP-1aα2 CT and sera from animals infected by other pathogens. High level of antibodies against RAP-1a usually lasted 10 weeks post-infection (wpi). A total of 3690 serum samples from small ruminants in 23 provinces located in 59 different regions of China were tested by ELISA. The results indicated that the average positive rate was 30·43%, and the infections were found in all of the investigated provinces. This is the first report on the expression and potential use of a recombinant XJrRAP-1aα2 CT antigen for the development of serological assays for the diagnosis of ovine babesiosis, caused by Babesia sp. Xinjiang.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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

Ahmed, J., Yin, H., Schnittger, L. and Jongejan, F. (2002). Ticks and tick-borne diseases in Asia with special emphasis on China. Parasitology Research 88, S51S55.CrossRefGoogle Scholar
Besteiro, S., Dubremetz, J. F. and Lebrun, M. (2011). The moving junction of apicomplexan parasites: a key structure for invasion. Cellular Microbiology 13, 797805.Google Scholar
Bhoora, R., Quan, M., Zweygarth, E., Guthrie, A. J., Prinsloo, S. A. and Collins, N. E. (2010). Sequence heterogeneity in the gene encoding the rhoptry-associated protein-1 (RAP-1) of Babesia caballi isolates from South Africa. Veterinary Parasitology 169, 279288.Google Scholar
Boonchit, S., Xuan, X., Yokoyama, N., Goff, W. L., Wagner, G. and Igarashi, I. (2002). Evaluation of an enzyme-linked immunosorbent assay with recombinant rhoptry-associated protein 1 antigen against Babesia bovis for the detection of specific antibodies in cattle. Journal of Clinical Microbiology 40, 37713775.Google Scholar
Boonchit, S., Alhassan, A., Chan, B., Xuan, X., Yokoyama, N., Ooshiro, M., Goff, W. L., Waghela, S. D., Wagner, G. and Igarashi, I. (2006). Expression of C-terminal truncated and full length Babesia bigemina rhoptry-associated protein 1 and their potential use in enzyme linked immunosorbent assay. Veterinary Parasitology 137, 2835.Google Scholar
Böse, R., Jorgensen, W. K., Dalgliesh, R. J., Friedhoff, K. T. and de Vos, A. J. (1995). Current state and future trends in the diagnosis of babesiosis. Veterinary Parasitology 57, 6174.Google Scholar
Dalrymple, B. P., Casu, R. E., Peters, J. M., Dimmock, C. M., Gale, K. R., Boese, R. and Wright, I. G. (1993). Characterization of a family of multi-copy genes encoding rhoptry protein homologues in Babesia bovis, B. ovis and B. canis . Molecular and Biochemical Parasitology 57, 181192.Google Scholar
Duzgun, A., Wright, I. G., Waltisbuhl, D. J., Gale, K. R., Goodger, B. V., Dargie, J. D., Alabay, M. and Cerci, H. (1991). An ELISA for the diagnosis of Babesia ovis infection utilizing a synthetic, Babesia bovis-derived antigen. Veterinary Parasitology 39, 225231.Google Scholar
Guan, G., Yin, H., Luo, J., Lu, W., Zhang, Q., Ma, M., Yuan, G., Lu, B., Wang, Y. and Muhe, T. (2001). Isolation of a large ovine Babesia sp. in Xinjiang, China. Chinese Journal of Veterinary Science and Technology 31, 3536.Google Scholar
Guan, G., Ma, M., Moreau, E., Liu, J., Lu, B., Bai, Q., Luo, J., Jorgensen, W., Chauvin, A. and Yin, H. (2009). A new ovine Babesia species transmitted by Hyalomma anatolicum anatolicum . Experimental Parasitology 122, 261267.Google Scholar
Guan, G., Ma, M., Liu, A., Du, P., Ren, Q., Li, Y., Wang, J., Liu, Z., Yin, H. and Luo, J. (2012 a). Continuous in vitro cultivation of a recently identified Babesia that infects small ruminants in China. Veterinary Parasitology 187, 371378.Google Scholar
Guan, G., Ma, M., Liu, A., Ren, Q., Wang, J., Yang, J., Li, A., Liu, Z., Du, P., Li, Y., Liu, Q., Zhu, H., Yin, H. and Luo, J. (2012 b). A recently identified ovine Babesia in China: serology and sero-epidemiology. Parasitology International 61, 532537.CrossRefGoogle Scholar
Guan, G., Moreau, E., Liu, J., Ma, M., Rogniaux, H., Liu, A., Niu, Q., Li, Y., Ren, Q., Luo, J., Chauvin, A. and Yin, H. (2012 c). BQP35 is a novel member of the intrinsically unstructured protein (IUP) family which is a potential antigen for the sero-diagnosis of Babesia sp. BQ1 (Lintan) infection. Veterinary Parasitology 187, 421430.Google Scholar
Guan, G., Liu, J., Liu, A., Li, Y., Niu, Q., Gao, J., Chauvin, A., Yin, H. and Moreau, E. (2015). A member of the HSP90 family from ovine Babesia in China: molecular characterization, phylogenetic analysis and antigenicity. Parasitology 142, 13871397.Google Scholar
Hötzel, I., Suarez, C. E., McElwain, T. F. and Palmer, G. H. (1997). Genetic variation in the dimorphic regions of RAP-1 genes and rap-1 loci of Babesia bigemina . Molecular and Biochemical Parasitology 90, 479489.Google Scholar
Huang, X., Xuan, X., Yokoyama, N., Xu, L., Suzuki, H., Sugimoto, C., Nagasawa, H., Fujisaki, K. and Igarashi, I. (2003). High-level expression and purification of a truncated merozoite antigen-2 of Babesia equi in Escherichia coli and its potential for immunodiagnosis. Journal of Clinical Microbiology 41, 11471151.Google Scholar
Jouglin, M., Fernández-de-Mera, I. G., de la Cotte, N., Ruiz-Fons, F., Gortázar, C., Moreau, E., Bastian, S., de la Fuente, J. and Malandrin, L. (2014). Isolation and characterization of Babesia pecorum sp. nov. from farmed red deer (Cervus elaphus). Veterinary Research 45, 78.Google ScholarPubMed
Liu, A., Yin, H., Guan, G., Schnittger, L., Liu, Z., Ma, M., Dang, Z., Liu, J., Ren, Q., Bai, Q., Ahmed, J. and Luo, J. (2007). At least two genetically distinct large Babesia species infective to sheep and goats in China. Veterinary Parasitology 147, 246251.Google Scholar
Luo, J. and Yin, H. (1997). Theileriosis of sheep and goats in China. Tropical Animal Health and Production 29, 8S10S.Google Scholar
Malandrin, L., Jouglin, M., Moreau, E. and Chauvin, A. (2009). Individual heterogeneity in erythrocyte susceptibility to Babesia divergens is a critical factor for the outcome of experimental spleen-intact sheep infections. Veterinary Research 40, 25.Google Scholar
Mandal, M., Banerjee, P. S., Kumar, S., Garg, R., Ram, H. and Raina, O. K. (2016). Development of recombinant BgP12 based enzyme linked immunosorbent assays for serodiagnosis of Babesia gibsoni infection in dogs. Veterinary Immunology and Immunopathology 169, 2733.Google Scholar
McElwain, T. F., Perryman, L. E., Davis, W. C. and McGuire, T. C. (1987). Antibodies define multiple proteins with epitopes exposed on the surface of live Babesia bigemina merozoites. Journal of Immunology 138, 22982304.Google Scholar
Mendes, T. A., Lobo, F. P., Rodrígues, T. S., Rodrígues-Luiz, G. F., daRocha, W. D., Fujiwara, R. T., Teixeira, S. M. and Bartholomeu, D. C. (2013). Repeat-enriched proteins are related to host cell invasion and immune evasion in parasitic protozoa. Molecular Biology and Evolution 30, 951963.Google Scholar
Moitra, P., Zheng, H., Anantharaman, V., Banerjee, R., Takeda, K., Kozakai, Y., Lepore, T., Krause, P. J., Aravind, L. and Kumar, S. (2015). Expression, purification, and biological characterization of Babesia microti apical membrane antigen 1. Infection and Immunity 83, 38903901.Google Scholar
Niu, Q., Luo, J., Guan, G., Liu, Z., Ma, M., Liu, A., Gao, J., Ren, Q., Li, Y., Qiu, J. and Yin, H. (2009). Differentiation of two ovine Babesia based on the ribosomal DNA internal transcribed spacer (ITS) sequences. Experimental Parasitology 121, 6468.Google Scholar
Niu, Q., Bonsergent, C., Guan, G., Yin, H. and Malandrin, L. (2013). Sequence and organization of the rhoptry-associated-protein-1 (rap-1) locus for the sheep hemoprotozoan Babesia sp. BQ1 Lintan (B. motasi phylogenetic group). Veterinary Parasitology 198, 2438.Google Scholar
Niu, Q., Valentin, C., Bonsergent, C. and Malandrin, L. (2014). Strong conservation of rhoptry-associated-protein-1 (RAP-1) locus organization and sequence among Babesia isolates infecting sheep from China (Babesia motasi-like phylogenetic group). Infection Genetics and Evolution 28, 2132.Google Scholar
Niu, Q., Marchand, J., Yang, C., Bonsergent, C., Guan, G., Yin, H. and Malandrin, L. (2015). Rhoptry-associated protein (rap-1) genes in the sheep pathogen Babesia sp. Xinjiang: multiple transcribed copies differing by 3′ end repeated sequences. Veterinary Parasitology 211, 158169.Google Scholar
Ooka, H., Terkawi, M. A., Cao, S., Aboge, G., Goo, Y. K., Luo, Y., Li, Y., Nishikawa, Y., Igarashi, I. and Xuan, X. (2012). Molecular and immunological characterization of a novel 32-kDa secreted protein of Babesia microti . Journal of Parasitology 98, 10451048.Google Scholar
Oosthuizen, M. C., Allsopp, B. A., Troskie, M., Collins, N. E. and Penzhorn, B. L. (2009). Identification of novel Babesia and Theileria species in South African giraffe (Giraffa camelopardalis, Linnaeus, 1758) and roan antelope (Hippotragus equinus, Desmarest 1804). Veterinary Parasitology 163, 3946.Google Scholar
Rodriguez, M., Alhassan, A., Ord, R. L., Cursino-Santos, J. R., Singh, M., Gray, J. and Lobo, C. A. (2014). Identification and characterization of the RouenBd1987 Babesia divergens rhopty-associated protein 1. PLoS ONE 9, e107727.Google Scholar
Sevinc, F., Cao, S., Zhou, M., Sevinc, M., Ceylan, O. and Xuan, X. (2015 a). A new immunoreactive recombinant protein designated as rBoSA2 from Babesia ovis: its molecular characterization, subcellular localization and antibody recognition by infected sheep. Veterinary Parasitology 214, 213218.Google Scholar
Sevinc, F., Cao, S., Xuan, X., Sevinc, M. and Ceylan, O. (2015 b). Identification and expression of Babesia ovis secreted antigen 1 and evaluation of its diagnostic potential in an enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 53, 15311536.Google Scholar
Suarez, C. E., Palmer, G. H., Jasmer, D. P., Hines, S. A., Perryman, L. E. and McElwain, T. F. (1991). Characterization of the gene encoding a 60-kilodalton Babesia bovis merozoite protein with conserved and surface exposed epitopes. Molecular and Biochemical Parasitology 46, 4552.Google Scholar
Terkawi, M. A., Amornthep, A., Ooka, H., Aboge, G., Jia, H., Goo, Y. K., Nelson, B., Yamagishi, J., Nishikawa, Y., Igarashi, I., Kawazu, S. I., Fujisakik, K. and Xuan, X. (2009). Molecular characterizations of three distinct Babesia gibsoni rhoptry-associated protein-1s (RAP-1s). Parasitology 136, 11471160.Google Scholar
Terkawi, M. A., Huyen, N. X., Shinuo, C., Inpankaew, T., Maklon, K., Aboulaila, M., Ueno, A., Goo, Y. K., Yokoyama, N., Jittapalapong, S., Xuan, X. and Igarashi, I. (2011). Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Veterinary Parasitology 178, 201207.Google Scholar
Uilenberg, G. (2006). Babesia – a historical overview. Veterinary Parasitology 138, 310.Google Scholar
Vannier, E. and Krause, P. J. (2009). Update on babesiosis. Interdisciplinary Perspectives on Infectious Diseases 2009, 984568.Google Scholar
Yokoyama, N., Okamura, M. and Igarashi, I. (2006). Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Veterinary Parasitology 138, 2232.Google Scholar
Yu, Q., He, L., Zhang, W. J., Cheng, J. X., Hu, J. F., Miao, X. Y., Huang, Y., Fan, L. Z., Khan, M. K., Zhou, Y. Q., Hu, M. and Zhao, J. L. (2014). Molecular cloning and characterization of Babesia orientalis rhoptry-associated protein 1. Veterinary Parasitology 205, 499505.Google Scholar
Zhou, J. L., Jia, H. L., Nishikawa, Y., Fujisaki, K. and Xuan, X. X. (2007). Babesia gibsoni rhoptry associated protein 1 and its potential use as a diagnostic antigen. Veterinary Parasitology 145, 1620.Google Scholar