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Molecular cloning, characterization and antigenicity of Babesia sp. BQ1 (Lintan) (Babesia cf. motasi) apical membrane antigen-1 (AMA-1)

Published online by Cambridge University Press:  12 December 2016

QINGLI NIU Open the ORCID record for QINGLI NIU [Opens in a new window] ,
ZHIJIE LIU ,
JIFEI YANG ,
GUIQUAN GUAN ,
YUPING PAN ,
JIANXUN LUO  and
HONG YIN
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
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
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
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
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: [email protected], [email protected]; [email protected]
*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: [email protected], [email protected]; [email protected]
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Summary

Apical membrane antigen-1 (AMA-1) has been described as a potential vaccine candidate in apicomplexan parasites. Here we characterize the ama-1 gene. The full-length ama-1 gene of Babesia sp. BQ1 (Lintan) (BLTAMA-1) is 1785 bp, which contains an open reading frame (ORF) encoding a 65-kDa protein of 594 amino acid residues; by definition, the 5′ UTR precedes the first methionine of the ORF. Phylogenetic analysis based on AMA-1 amino acid sequences clearly separated Piroplasmida from other Apicomplexa parasites. The Babesia sp. BQ1 (Lintan) AMA-1 sequence is most closely associated with that of B. ovata and B. bigemina, with high bootstrap value. A recombinant protein encoding a conserved region and containing ectodomains I and II of BLTAMA-1 was constructed. BLTrAMA-1-DI/DII proteins were tested for reactivity with sera from sheep infected by Babesia sp. BQ1 (Lintan). In Western-blot analysis, native Babesia sp. BQ1 (Lintan) AMA-1 proteins were recognized by antibodies raised in rabbits against BLTrAMA-1 in vitro. The results of this study are discussed in terms of gene characterization, taxonomy and antigenicity.

Keywords

Babesia sp. BQ1 (Lintan)AMA-1characterizationexpression
Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 641 - 649
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Bock, R., de Vos, A. J., Kingston, T. G., Shiels, I. A. and Dalgliesh, R. J. (1992). Investigations of breakdowns in protection provided by living Babesia bovis vaccine. Veterinary Parasitology 43, 45–56.Google Scholar
Callow, L. L., Mellors, L. T. and McGregor, W. (1979). Reduction in virulence of Babesia bovis due to rapid passage in splenectomized cattle. International Journal for Parasitology 9, 333–338.Google Scholar
Collins, W. E., Pye, D., Crewter, P. E., Vandeberg, K. L., Galland, G. G., Sulzer, A. J., Kemp, D. J., Edwards, S. J., Coppel, R. L., Sullivan, J. S., Morris, C. L. and Anders, R. F. (1994). Protective immunity induced in squirrel monkeys with recombinant apical membrane antigen-1 of Plasmodium fragile . American Journal of Tropical Medicine and Hygiene 51, 711–719.CrossRefGoogle ScholarPubMed
Gaffar, F. R., Yatsuda, A. P., Franssen, F. F. and de Vries, E. (2004). Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infection and Immunity 72, 2947–2955.Google Scholar
Gohil, S., Herrmann, S., Günther, S. and Cooke, B. M. (2013). Bovine babesiosis in the 21st century: advances in biology and functional genomics. International Journal for Parasitology 43, 125–132.Google Scholar
Guan, G. Q., Yin, H., Luo, J. X., Lu, W. S., Zhang, Q. C., Gao, Y. L. and Lu, B. Y. (2002). Transmission of Babesia sp. to sheep with field-collected Haemaphysalis qinghaiensis . Parasitology Research 88, S22–S24.CrossRefGoogle ScholarPubMed
Guan, G., Moreau, E., Liu, J., Hao, X., Ma, M., Luo, J., Chauvin, A. and Yin, H. (2010 a). Babesia sp. BQ1 (Lintan): molecular evidence of experimental transmission to sheep by Haemaphysalis qinghaiensis and Haemaphysalis longicornis . Parasitology International 59, 265–267.Google Scholar
Guan, G., Chauvin, A., Rogniaux, H., Luo, J., Yin, H. and Moreau, E. (2010 b). Merozoite proteins from Babesia sp. BQ1 (Lintan) as potential antigens for serodiagnosis by ELISA. Parasitology 137, 927–938.Google Scholar
He, L., Fan, L. Z., Hu, J. F., Miao, X. Y., Huang, Y., Zhou, Y. Q., Hu, M. and Zhao, J. L. (2015). Characterisation of a Babesia orientalis apical membrane antigen, and comparison of its orthologues among selected apicomplexans. Ticks and Tick-borne Diseases 6, 290–296.Google Scholar
Healer, J., Crawford, S., Ralph, S., McFadden, G. and Cowman, A. F. (2002). Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infection and Immunity 70, 5751–5758.Google Scholar
Hodder, A. N., Crewther, P. E., Matthew, M. L., Reid, G. E., Moritz, R. L., Simpson, R. J. and Anders, R. F. (1996). The disulfide bond structure of Plasmodium apical membrane antigen-1. Journal of Biological Chemistry 271, 29446–29452.CrossRefGoogle ScholarPubMed
Kumar, S., Stecher, G. and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasetes. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Lack, J. B., Reichard, M. V. and Van Den Bussche, R. A. (2012). Phylogeny and evolution of the Piroplasmida as inferred from 18S rRNA sequences. International Journal for Parasitology 42, 353–363.Google Scholar
Lal, A. A., Hughes, M. A., Oliveira, D. A., Nelson, C., Bloland, P. B., Oloo, A. J., Hawley, W. E., Hightower, A. W., Nahlen, B. L. and Udhayakumar, V. (1996). Identification of T-cell determinants in natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in an adult population exposed to malaria. Infection and Immunity 64, 1054–1059.Google Scholar
Lobo, C. A., Rodríguez, M. and Cursino-Santos, J. R. (2012). Babesia and red cell invasion. Current Opinion in Hematology 19, 170–175.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, 3890–3901.Google Scholar
Montero, E., Rodríguez, M., Oksov, Y. and Lobo, C. A. (2009). Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell. Infection and Immunity 77, 4783–4793.CrossRefGoogle ScholarPubMed
Moreau, E., Bonsergent, C., Al Dybiat, I., Gonzalez, L. M., Lobo, C. A., Montero, E. and Malandrin, L. (2015). Babesia divergens apical membrane antigen-1 (BdAMA-1): a poorly polymorphic protein that induces a weak and late immune response. Experimental Parasitology 155, 40–45.CrossRefGoogle ScholarPubMed
Nakajima, R., Tsuji, M., Oda, K., Zamoto-Niikura, A., Wei, Q., Kawabuchi-Kurata, T., Nishida, A. and Ishihara, C. (2009). Babesia microti-group parasites compared phylogenetically by complete sequencing of the CCTeta gene in 36 isolates. Journal of Veterinary Medical Science 71, 55–68.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, 24–38.Google Scholar
Pipano, E. (1995). Live vaccine against hemoparasitic disease in livestock. Veterinary Parasitology 57, 213–231.Google Scholar
Pizarro, J. C., Vulliez-Le Normand, B., Chesne-Seck, M. L., Collins, C. R., Withers-Martinez, C., Hackett, F., Blackman, M. J., Faber, B. W., Remarque, E. J., Kocken, C. H., Thomas, A. W. and Bentley, G. A. (2005). Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science 308, 408–411.Google Scholar
Salama, A. A., Terkawi, M. A., Kawai, S., Aboulaila, M., Nayel, M., Mousa, A., Zaghawa, A., Yokoyama, N. and Igarashi, I. (2013). Specific antibody to a conserved region of Babesia apical membrane antigen-1 inhibited the invasion of B. bovis into the erythrocyte. Experimental Parasitology 135, 623–628.Google Scholar
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection Genetics and Evolution 12, 1788–1809.Google Scholar
Torina, A., Agnone, A., Sireci, G., Mosqueda, J. J., Blanda, V., Albanese, I., La Farina, M., Cerrone, A., Cusumano, F. and Caracappa, S. (2010). Characterization of the apical membrane antigen-1 in Italian strains of Babesia bigemina . Transboundary and Emerging Diseases 57, 52–56.Google Scholar
Tonkin, M. L., Crawford, J., Lebrun, M. L. and Boulanger, M. J. (2013). Babesia divergens and Neospora caninum apical membrane antigen 1 structures reveal selectivity and plasticity in apicomplexan parasite host cell invasion. Protein Science 22, 114–127.CrossRefGoogle ScholarPubMed
Wang, J. M., Ma, M. L., Liu, A. H., Ren, Q. Y., Li, A. Y., Liu, Z. J., Li, Y. Q., Yin, H., Luo, J. X. and Guan, G. Q. (2013). A sero-epidemiological survey of Chinese Babesia motasi for small ruminants in China. Parasitology Research 112, 2387–2391.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, 22–32.Google Scholar
Zhou, J. L., Yang, J., Zhang, G. H., Nishikawa, Y., Fujisaki, K. and Xuan, X. N. (2006). Babesia gibsoni: an apical membrane antigen-1 homologue and its antibody response in the infected dogs. Experimental Parasitology 114, 329–333.Google Scholar