Intra and inter species genetic variability of transferrin receptor gene regions in Trypanosoma evansi isolates of different livestock and geographical regions of India

Souti Prasad Sarkhel; S.K. Gupta; Jyoti Kaushik; Jarnail Singh; Vijesh Kumar Saini; Sanjay Kumar; Rajender Kumar

doi:10.1515/ap-2017-0016

Article

Intra and inter species genetic variability of transferrin receptor gene regions in Trypanosoma evansi isolates of different livestock and geographical regions of India

Souti Prasad Sarkhel , S.K. Gupta , Jyoti Kaushik , Jarnail Singh , Vijesh Kumar Saini , Sanjay Kumar and Rajender Kumar

Published/Copyright: December 28, 2016

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From the journal Acta Parasitologica Volume 62 Issue 1

Abstract

Trypanosoma evansi, the aetiological agent of Surra affects a wide range of livestock and wild animals in India. In the present study, we studied intra- and inter species genetic variability in the transferrin receptor encoding gene regions (ESAG6/7 gene region) of T. evansi isolates by cloning, sequencing and phylogenetic study collected from camel, cattle, donkeys and ponies from North-Western and Central India. The nucleotide sequence variation of ESAG6/7 gene region between Indian T. evansi isolates was up to 17.7% and amino acid sequence variation was up to 31%. Twenty nine clones from six T. evansi isolates from geographical regions of India were included into Clade 1, 5, 6, 7 and 9 consisting of ESAG6 variants reported among T. evansi isolates from South-east Asia and South America. The cladogram indicated a relation between the host species and the genetic variability in the hyper-variable region of ESAG6 gene. Analysis of the Indian ESAG6 variants and their respective Clade positions presented a host specific distribution indicating homogenous parasite population in their respective animal hosts.

Keywords: Trypanosoma evansi; Surra; transferrin receptor encoding gene; ESAG; genetic variability; India

Conflict of Interest Statement: All authors disclose that they have no financial and personal relationships with other people or organization that could inappropriately influence their work, including employment, consultancies, stock ownership, honoraria, paid expert testimony, patent applications/registration, and grants or other funding.
Ethics
All authors certify that the animal experimentations carried out in the present work after approval of Institute Animal Ethic Committee and as per guidelines set by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Animal Welfare Division, Government of India.

Acknowledgements

The work was performed at ICAR-National Research Centre on Equines, Hisar, India. The financial support for this study provided by Indian Council of Agricultural Research, New Delhi under National Fellow project is gratefully acknowledged.

References

Alarcon C., Pedram M., Donelson J. 1999. Leaky transcription of variant surface glycoprotein gene expression sites in blood-stream African trypanosomes. Journal of Biological Chemistry, 274, 16884–1689310.1074/jbc.274.24.16884Search in Google Scholar

Amer S., Ryu O., Tada C., Fukuda Y., Inoue N., Nakai Y.2011. Molecular identification and phylogenetic analysis of Trypanosoma evansi from dromedary camels ( Camelus dromedarius) in Egypt, a pilot study. Acta Tropica, 117, 39–4610.1016/j.actatropica.2010.09.010Search in Google Scholar

Ansorge I., Steverding D., Melville S., Hartmann C., Clayton C. 1999. Transcription of ‘inactive’ expression sites in African trypanosomes leads to expression of multiple transferrin receptor RNAs in bloodstream forms. Molecular and Biochemical Parasitology, 101, 81–9410.1016/S0166-6851(99)00060-2Search in Google Scholar

Bitter W., Gerrits H., Kieft R., Borst P. 1998. The role of transferrinreceptor variation in host range of Trypanosoma brucei. Nature, 391, 499–50210.1038/35166Search in Google Scholar

Borst P. 1991. Transferrin receptor, antigenic variation and the prospect of a trypanosome vaccine. Trends in Genetics, 7, 307–30910.1016/0168-9525(91)90406-GSearch in Google Scholar

Borst P., Bitter W., Blundell P., Cross M., McCulloch R., Rudenko G., Taylor M.C., Van Leeuwen F. 1997. The expression sites for variant surface glycoproteins of Trypanosoma brucei. In: (Eds Hide G., Mottram J. C., Coombs G. H. and Holmes P. H.) Trypanosomiasis and Leishmaniasis: Biology and Control. Oxford: British Society for Parasitology: CAB International, 1997, 109–131Search in Google Scholar

El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., et al. 2005. Comparative genomics of trypanosomatid parasitic protozoa. Science, 309, 404–40910.1126/science.1112181Search in Google Scholar

Gerrits H., Mussmann R., Bitter W., Kieft R., Borst P. 2002. The physiological significance of transferrin receptor variations in Trypanosoma brucei. Molecular and Biochemical Parasitol ogy, 119, 237–24710.1016/S0166-6851(01)00417-0Search in Google Scholar

Hertz-Fowler C., Figueiredo L.M., Quail M.A., Becker M., Jackson A., Bason N., et al. 2008. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS One, 3, e352710.1371/journal.pone.0003527Search in Google Scholar PubMed PubMed Central

Isobe T., Holmes E.C., Rudenko, G. 2003. The transferrin receptor genes of Trypanosoma equiperdum are less diverse in their transferrin binding site than those of the broad-host range Trypanosoma brucei. Journal of Molecular Evolution, 56, 377–38610.1007/s00239-002-2408-zSearch in Google Scholar PubMed

Kabiri M., Steverding, D. 2001. Trypanosoma evansi: demonstration of a transferrin receptor derived from expression site-associated genes 6 and 7. Journal of Parasitology, 87, 1189–119110.2307/3285262Search in Google Scholar

Kumar J., Chaudhury A., Bera B.C., Kumar Ritesh, Kumar R., Tatu U., Yadav S.C. 2015. Production and preliminary evaluation of Trypanosoma evansi HSP70 for antibody detection in equids. Acta Parasitologica, 60, 727–734.10.1515/ap-2015-0104Search in Google Scholar

Kumar R., Kumar S., Khurana S.K., Yadav S.C. 2013. Development of an antibody-ELISA for seroprevalence of Trypanosoma evansi in equids of North and North-western regions of India. Veterinary Parasitology, 196, 251–25710.1016/j.vetpar.2013.04.018Search in Google Scholar

Lanham S.M., Godfrey, D.G. 1970. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Experimental Parasitology, 28, 521–53410.1016/0014-4894(70)90120-7Search in Google Scholar

Ligtenberg M.J., Bitter W., Kieft R., Steverding D., Janssen H., Calafat J. and Borst P. 1994. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO Journal, 13, 2565–257310.1002/j.1460-2075.1994.tb06546.xSearch in Google Scholar

Liu A.Y.C., Michels P.A.M., Bernards A., Borst P. 1985. Trypanosome variant surface glycoprotein genes expressed early in infection. Journal of Molecular Biology, 182, 383–39610.1016/0022-2836(85)90198-6Search in Google Scholar

Mekata H., Konnai S., Witola W.H., Inoue N., Onuma, M., Ohashi, K. 2009. Molecular detection of trypanosomes in cattle in South America and genetic diversity of Trypanosoma evansi based on expression-site-associated gene 6. Infection Genetics and Evolution, 9, 1301–130510.1016/j.meegid.2009.07.009Search in Google Scholar

Narnaware S.D., Ghorui S.K., Kumar S., Patil N.V. 2016. Vertical transmission of Trypanosoma evansi in dromedary camels and studies on fetal pathology, diagnosis and treatment. Acta Parasitologica, 61, 329–33610.1515/ap-2016-0043Search in Google Scholar

Pathak K.M.L., Chhabra, M.B. 2011. Trypanosomosis of livestock in India: A review of two decades. Indian Journal of Animal Sciences, 81, 653–660Search in Google Scholar

Salmon D., Geuskens M., Hanocq F., Hanocq-Quertier J., Nolan D., Ruben L., Pays E. 1994. A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in Trypanosoma brucei. Cell, 78, 75–8610.1016/0092-8674(94)90574-6Search in Google Scholar

Salmon D., Hanocq-Quertier J., Paturiaux-Hanocq F., Pays A., Tebai P., Nolan D.P., Michel A., Pays, E. 1997. Characterisation of the ligand-binding site of the transferrin receptor in Trypanosoma brucei demonstrates a structural relationship with the N-terminal domain of the variant surface glycoprotein. EMBO Journal, 16, 7272–727810.1093/emboj/16.24.7272Search in Google Scholar

Steverding D. 2003. The significance of transferrin receptor variation in Trypanosoma brucei. Trends in Parasitology, 19, 125–12710.1016/S1471-4922(03)00006-0Search in Google Scholar

Steverding D., Overath, P. 1996. Trypanosoma brucei with an active metacyclic variant surface gene expression site expresses a transferrin receptor derived from esag 6 and esag 7. Molecular and Biochemical Parasitology, 78, 285–28810.1016/S0166-6851(96)02624-2Search in Google Scholar

Steverding D., Stierhof Y.D., Fuch H., Tauber R., Overath P. 1995. Transferrin-binding complex is the receptor for transferrin uptake in Trypanosoma brucei. Journal of Cellular Biology, 131, 1173–118210.1083/jcb.131.5.1173Search in Google Scholar

Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–273910.1093/molbev/msr121Search in Google Scholar

Witola W.H., Sarataphan N., Inoue N., Ohashi K., Onuma, M. 2005.Genetic variability in ESAG6 genes among Trypanosoma evansi isolates and in comparison to other Trypanozoon members. Acta Tropica, 93, 63–7310.1016/j.actatropica.2004.09.006Search in Google Scholar

Xong H.V., Vanhamme L., Chamekh M., Chimfwembe C.E., Van Den Abbeele J., Pays A., et al. 1998. A VSG expression site-associated gene confers resistance to human serum in Try-panosoma rhodesiense. Cell, 95, 839–84610.1016/S0092-8674(00)81706-7Search in Google Scholar

Young R., Taylor J.E., Kurioka A., Becker M., Louis E.J., Rudenko G. 2008. Isolation and analysis of the genetic diversity of repertoires of VSG expression site containing telomeres from Trypanosoma brucei gambiense, T. b. brucei and T. equiperdum. BMC Genomics, 9, 38510.1186/1471-2164-9-385Search in Google Scholar PubMed PubMed Central

Zomerdijk J.C., Ouellette M., ten Asbroek A.L., Kieft R., Bommer A.M., Clayton C.E., Borst P. 1990. The promoter for a variant surface glycoprotein gene expression site in Trypanosoma brucei. EMBO Journal, 9, 2791–280110.1002/j.1460-2075.1990.tb07467.xSearch in Google Scholar PubMed PubMed Central

Received: 2016-6-10

Revised: 2016-9-22

Accepted: 2016-10-14

Published Online: 2016-12-28

Published in Print: 2017-3-1

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https://doi.org/10.1515/ap-2017-0016

Keywords for this article

Trypanosoma evansi; Surra; transferrin receptor encoding gene; ESAG; genetic variability; India