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Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain

Year 2018, Volume: 65 Issue: 3, 239 - 246, 01.09.2018
https://doi.org/10.1501/Vetfak_0000002852

Abstract

This study was performed to molecular characterization and expression of AMA-1 protein molecules of in vivo and in vitro cultivated and passaged isolates from “Babesia bigemina Kayseri/Turkey” strain, and also to determine the possible polymorphisms of these molecules due to the attenuation of the isolates. For this aim, target gene was completely amplified by PCR after isolation of genomic DNA and total RNA from the in vivo and in vitro cultivated isolates which were obtained from Babesia bigemina Kayseri/Turkey strain. The isolates were cloned into suitable vectors after PCR analysis. The cloned isolates were sequenced and the obtained sequences were deposited in GenBank with accession numbers KP000032-33. Multiple and pairwise alignments of the sequences were performed and phylogenies were investigated. The obtained recombinant plasmids were transformed into E. coli BL21 (DE3) cells and expressed after induction with IPTG. The target proteins were analyzed by using SDS-PAGE and Western Blot techniques. Nucleotide sequences of Kayseri/Turkey IV1 and Kayseri/Turkey IT2 isolates showed 99.7% identity to each other and a difference (0.2%) was also determined in amino acid sequences of these two isolates due to a mutation in 103rd nucleotide. According to results of SDS-PAGE and Western Blot analyses, the BbigAMA-1 isolates were expressed with a molecular mass of 72 kDa in different IPTG concentration levels and time periods. In conclusion, attenuation-related polymorphic sites that indicate the mutational differences between AMA-1 nucleotide and amino acid sequences from in vivo and in vitro isolates of Babesia bigemina Kayseri/Turkey strain were revealed with this study

References

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  • Beghetto E, Nielsen HV, Del Porto P ve ark. (2005): A combination of antigenic regions of Toxoplasma gondii microneme proteins induces protective immunity against oral infection with parasite cysts. J Infect Dis, 191, 637-645.
  • Biller L, Schmidt H, Krause E ve ark. (2009): Comparison of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. Proteomics, 9, 4107-20.
  • Bock R, Jackson L, De Vos A ve ark. (2004): Babesiosis of cattle. Parasitology, 129, 247-269.
  • Brands SJ (2015): Taxon: species Babesia bigemina. Systema naturae 2000. The Taxonomicon. Available at http://taxonomicon.taxonomy.nl/TaxonTree.aspx?id=1353 &src=0. (Accessed 15 Şubat 2017).
  • Chesne-Seck ML, Pizarro J, Vulliez-Le Normand B ve ark. (2005): Structural comparison of apical membrane antigen 1 orthologues and paralogues in apicomplexan parasites. Mol Biochem Parasitol, 144, 55-67.
  • De Vos AJ, Bock RE (2000): Vaccination against bovine babesiosis. Ann N Y Acad Sci, 916, 540-545.
  • De Waal DT, Combrink MP (2006): Live vaccines against bovine babesiosis. Vet Parasitol, 138, 88-96.
  • Drew DR, Hodder AN, Wilson DW ve ark. (2012): Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. Plos One, 7, e51023.
  • Ellis RD, Sagara I, Doumbo O ve ark. (2010): Blood stage vaccines for Plasmodium falciparum: Current status and the way forward. Hum Vaccin, 6, 627-634.
  • Elsify A, Sivakumar T, Nayel M ve ark. (2015): An epidemiological survey of bovine Babesia and Theileria parasites in cattle, buffaloes, and sheep in Egypt. Parasitol Int, 64, 79-85.
  • Filatov DA (2009): Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics, 25, 3189-90.
  • Gaffar FR, Yatsuda AP, Franssen FJ ve ark. (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. Infect Immun, 72, 2947-55.
  • Gunasekera AM, Wickramarachchi T, Neafsey DE ve ark. (2007): Genetic diversity and selection at the Plasmodium vivax apical membrane antigen-1 (PvAMA-1) locus in a Sri Lankan population. Mol Biol Evol, 24, 939- 947.
  • He L, Fan L, Hu J ve ark. (2015): Characterisation of a Babesia orientalis apical membrane antigen, and comparison apicomplexans. Ticks Tick Borne Dis, 6, 290-296. among selected
  • Hehl AB, Lekutis C, Grigg ME ve ark. (2000): Toxoplasma gondii homologue of plasmodium apical membrane antigen 1 is involved in invasion of host cells. Infect Immun, 68, 7078-86.
  • Huelsenbeck JP, Ronquist F (2001): MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754- 755.
  • İnci A, Yazar S, Tunçbilek AS ve ark. (2013): Vectors and vector-borne diseases in Turkey. Vet J Ankara Univ, 60, 281-296.
  • İnci A, Yıldırım A, Duzlu O ve ark. (2016): Tick-borne diseases in Turkey: A review based on one health perspective. PLoS Neglect Trop D, 10, e0005021. 20. Karaer Z, Nalbantoglu S (2005): Protozoon hastalıklarında tedavi. 1-19. In: A Burgu, Z Karaer (Eds), Parazit Hastalıklarında Tedavi. Türkiye Parazitoloji Derneği Yayınları, İzmir.
  • Kaya S, Pirinçci İ (2007): Protozoonları etkileyen ilaçlar. 562-565. In: S Kaya (Ed), Veteriner Farmakoloji. Medisan Yayın Serisi, Ankara.
  • Kearse M, Moir R, Wilson A (2012): Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-49.
  • Kumar S, Stecher G, Tamura K (2016): MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 33, 1870-74.
  • Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
  • Liu M, Vakharia VN (2004): VP1 protein of infectious bursal disease virus modulates the virulence in vivo. Virology, 330, 62-73.
  • Moitra P, Zheng H, Anantharaman V ve ark. (2015): Expression, purification, and biological characterization of Babesia microti apical membrane antigen 1. Infect Immun, 83, 3890-01.
  • Montero E, Rodriguez M, Oksov Y ve ark. (2009): Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell. Infect Immun, 77, 4783-93.
  • Moreau E, Bonsergent C, Al Dybiat I ve ark. (2015): Babesia divergens apical membrane antigen-1 (BdAMA-1): A poorly polymorphic protein that induces a weak and late immune response. Exp Parasitol, 155, 40-45.
  • Ochirkhuu N, Konnai S, Mingala CN ve ark. (2015): Molecular epidemiological survey and genetic analysis of vector-borne infections of cattle in Luzon Island, the Philippines. Vet Parasitol, 212, 161-167.
  • ORF Finder (2015): Open reading frame finder. Available at http://www.ncbi.nlm.nih.gov/projects/gorf/ (Accessed 08 April 2015).
  • Posada D (2008): jModelTest: Phylogenetic model averaging. Mol Biol Evol, 25, 1253-56.
  • Ramsey KH, Sigar IM, Schripsema JH ve ark. (2009): Strain and virulence diversity in the mouse pathogen Chlamydia muridarum. Infect Immun, 77, 3284-93.
  • Remarque EJ, Faber BW, Kocken CH ve ark. (2008): Apical membrane antigen 1: A malaria vaccine candidate in review. Trends Parasitol, 24, 74-84.
  • Remarque EJ, Roestenberg M, Younis S ve ark. (2012): Humoral immune responses to a single allele PfAMA1 vaccine in healthy malaria-naive adults. Plos One, 7, e38898.
  • Rice P, Longden I, Bleasby A (2000): EMBOSS: The European molecular biology open software suite. Trends Genet, 16, 276-277.
  • Rodrigues MHC, Rodrigues KM, Oliveira TR ve ark. (2005): Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Int J Parasitol, 35, 185-192.
  • Salama AA, Terkawi MA, Kawai S ve ark. (2013): Specific antibody to a conserved region of Babesia apical membrane antigen-1 inhibited the invasion of B. bovis into the erythrocyte. Exp Parasitol, 135, 623-628.
  • Sambrook J, Russell DW (2001): Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
  • Sevinc F, Xuan X (2015): Major tick-borne parasitic diseases of animals: A frame of references in Turkey. Eurasian J Vet Sci, 31, 132-142.
  • Sivakumar T, Lan DT, Long PT ve ark. (2013): PCR detection and genetic diversity of bovine hemoprotozoan parasites in Vietnam. J Vet Med Sci, 75, 1455-62.
  • Sivakumar T, Tattiyapong M, Fukushi S ve ark. (2014): Genetic characterization of Babesia and Theileria parasites in water buffaloes in Sri Lanka. Vet Parasitol, 200, 24-30.
  • Takala SL, Coulibaly D, Thera M ve ark. (2009): Extreme polymorphism in a vaccine antigen and risk of clinical malaria: Implications for vaccine development. Sci Transl Med, 1, 2ra5.
  • Terkawi MA, Thekisoe OM, Katsande C ve ark. (2011): Serological survey of Babesia bovis and Babesia bigemina in cattle in South Africa. Vet Parasitol, 182, 337-342.
  • Tonukari NJ (2010): Theileria parva apical membrane antigen-1 (AMA-1) shares conserved sequences with apicomplexan homologs. Int J Biotech Mol Biol Res, 1, 36- 41.
  • Torina A, Agnone A, Sireci G (2010): Characterization of the apical membrane antigen-1 in Italian strains of Babesia bigemina. Transbound Emerg Dis, 57, 52-56.
  • Torina A, Caracappa S (2007): Babesiosis in Italy: An overview. Parasitologia, 49, 23-28.
  • Torina A, Cordaro A, Blanda V ve ark. (2016): A promising new ELISA diagnostic test for cattle babesiosis based on Babesia bigemina apical membrane antigen-1. Vet Ital, 52, 63-69.
  • Tyler JS, Treeck M, Boothroyd JC (2011): Focus on the ringleader: The role of AMA1 in apicomplexan invasion and replication. Trends Parasitol, 27, 410-420.
  • Uilenberg G (2006): Babesia-A historical overview. Vet Parasitol, 138, 3-10.
  • Xu L, Bao L, Zhou J ve ark. (2011): Genomic polymorphism of the pandemic A (H1N1) influenza viruses correlates pathogenicity in vitro and in vivo. Plos One, 6, e20698.
  • Ybanez AP, Sivakumar T, Ybanez RH ve ark. (2013): Molecular survey of bovine vector-borne pathogens in Cebu, Philippines. Vet Parasitol, 196, 13-20.
  • Zhang H, Compaore MK, Lee EG ve ark. (2007): Apical membrane antigen 1 is a cross-reactive antigen between Neospora caninum and Toxoplasma gondii, and the anti- NcAMA1 antibody inhibits host cell invasion by both parasites. Mol Biochem Parasitol, 151, 205-212.
  • Zhou J, Yang J, Zhang G ve ark. (2006): Babesia gibsoni: An apical membrane antigen-1 homologue and its antibody response in the infected dogs. Exp Parasitol, 114, 329-333. Geliş tarihi: 16.02.2017 / Kabul tarihi: 15.06.2017 Address for correspondence: Dr. Arif ÇİLOĞLU Erciyes Üniversitesi, Veteriner Fakültesi, Parazitoloji Anabilim Dalı, 38039, Kayseri, Türkiye. e-mail: arifciloglu@gmail.com

Babesia bigemina Kayseri/Türkiye suşunun in vivo ve in vitro izolatlarında apikal membran antijen-1 proteininin moleküler karakterizasyonu ve ekspresyonu

Year 2018, Volume: 65 Issue: 3, 239 - 246, 01.09.2018
https://doi.org/10.1501/Vetfak_0000002852

Abstract

Bu çalışma, “Babesia bigemina Kayseri/Türkiye” suşundan in vivo ve in vitro kültivasyon yapılarak ve pasajlanarak elde edilmiş olan izolatların AMA-1 proteinlerinin moleküler karakterizasyonu ve ekspresyonu ile söz konusu proteinin attenüasyona bağlı polimorfizm gösterip göstermediğini ortaya koymak amacıyla yapılmıştır. Bu amaçla, Babesia bigemina Kayseri/Türkiye suşuna ait, in vivo ve in vitro izolatlardan genomik DNA ve total RNA izolasyonu sonrasında hedef gen, PCR ile bütün olarak amplifiye edilmiş ve pürifiye amplikonlar uygun vektörlere klonlanmıştır. Klonlama sonrasında rekombinant plazmidler, sekanslanarak izolatlara ait nükleotid dizilimleri GenBank’a kaydedilmiştir . Nükleotid ve amino asit sekansların çoklu ve ikili hizalama analizleri yapılmış ve izolatların filogenileri araştırılmıştır. Elde edilen rekombinant plazmidler, E. coli BL21 (DE3) hücrelerine transforme edilerek IPTG ile indüklenmiş ve ekspresyonları sağlanmıştır. Ekspresyon ürünlerinde hedef proteinler SDS-PAGE ve Western Blot teknikleri ile analiz edilmiştir. Kayseri/Turkey IV1 ve Kayseri/Turkey IT2 izolatları nükleotid dizilimlerinin kendi aralarında %99.7 identiklik gösterdiği ve 103. nükleotiddeki mutasyona bağlı olarak amino asit diziliminde farklılık (%0.2) oluştuğu belirlenmiştir. SDSPAGE ve Western Blot analizleri sonucu söz konusu iki izolata ait AMA-1 proteinlerinin 72 kDa moleküler ağırlıklarla farklı IPTG konsantrasyon düzeyleri ve zaman aralıklarında eksprese oldukları belirlenmiştir. Sonuç olarak bu çalışma ile Babesia bigemina Kayseri/Türkiye suşunun in vivo ve in vitro pasajlarından elde edilmiş iki izolata ait AMA-1 nükleotid ve amino asit dizilimleri arasında mutasyonel farklılıkları gösteren attenüasyona bağlı polimorfik alanlar olduğu ortaya konulmuştur

References

  • Altschul SF, Gish W, Miller W ve ark. (1990): Basic local alignment search tool. J Mol Biol, 215, 403-410.
  • Beghetto E, Nielsen HV, Del Porto P ve ark. (2005): A combination of antigenic regions of Toxoplasma gondii microneme proteins induces protective immunity against oral infection with parasite cysts. J Infect Dis, 191, 637-645.
  • Biller L, Schmidt H, Krause E ve ark. (2009): Comparison of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. Proteomics, 9, 4107-20.
  • Bock R, Jackson L, De Vos A ve ark. (2004): Babesiosis of cattle. Parasitology, 129, 247-269.
  • Brands SJ (2015): Taxon: species Babesia bigemina. Systema naturae 2000. The Taxonomicon. Available at http://taxonomicon.taxonomy.nl/TaxonTree.aspx?id=1353 &src=0. (Accessed 15 Şubat 2017).
  • Chesne-Seck ML, Pizarro J, Vulliez-Le Normand B ve ark. (2005): Structural comparison of apical membrane antigen 1 orthologues and paralogues in apicomplexan parasites. Mol Biochem Parasitol, 144, 55-67.
  • De Vos AJ, Bock RE (2000): Vaccination against bovine babesiosis. Ann N Y Acad Sci, 916, 540-545.
  • De Waal DT, Combrink MP (2006): Live vaccines against bovine babesiosis. Vet Parasitol, 138, 88-96.
  • Drew DR, Hodder AN, Wilson DW ve ark. (2012): Defining the antigenic diversity of Plasmodium falciparum apical membrane antigen 1 and the requirements for a multi-allele vaccine against malaria. Plos One, 7, e51023.
  • Ellis RD, Sagara I, Doumbo O ve ark. (2010): Blood stage vaccines for Plasmodium falciparum: Current status and the way forward. Hum Vaccin, 6, 627-634.
  • Elsify A, Sivakumar T, Nayel M ve ark. (2015): An epidemiological survey of bovine Babesia and Theileria parasites in cattle, buffaloes, and sheep in Egypt. Parasitol Int, 64, 79-85.
  • Filatov DA (2009): Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics, 25, 3189-90.
  • Gaffar FR, Yatsuda AP, Franssen FJ ve ark. (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. Infect Immun, 72, 2947-55.
  • Gunasekera AM, Wickramarachchi T, Neafsey DE ve ark. (2007): Genetic diversity and selection at the Plasmodium vivax apical membrane antigen-1 (PvAMA-1) locus in a Sri Lankan population. Mol Biol Evol, 24, 939- 947.
  • He L, Fan L, Hu J ve ark. (2015): Characterisation of a Babesia orientalis apical membrane antigen, and comparison apicomplexans. Ticks Tick Borne Dis, 6, 290-296. among selected
  • Hehl AB, Lekutis C, Grigg ME ve ark. (2000): Toxoplasma gondii homologue of plasmodium apical membrane antigen 1 is involved in invasion of host cells. Infect Immun, 68, 7078-86.
  • Huelsenbeck JP, Ronquist F (2001): MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754- 755.
  • İnci A, Yazar S, Tunçbilek AS ve ark. (2013): Vectors and vector-borne diseases in Turkey. Vet J Ankara Univ, 60, 281-296.
  • İnci A, Yıldırım A, Duzlu O ve ark. (2016): Tick-borne diseases in Turkey: A review based on one health perspective. PLoS Neglect Trop D, 10, e0005021. 20. Karaer Z, Nalbantoglu S (2005): Protozoon hastalıklarında tedavi. 1-19. In: A Burgu, Z Karaer (Eds), Parazit Hastalıklarında Tedavi. Türkiye Parazitoloji Derneği Yayınları, İzmir.
  • Kaya S, Pirinçci İ (2007): Protozoonları etkileyen ilaçlar. 562-565. In: S Kaya (Ed), Veteriner Farmakoloji. Medisan Yayın Serisi, Ankara.
  • Kearse M, Moir R, Wilson A (2012): Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-49.
  • Kumar S, Stecher G, Tamura K (2016): MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 33, 1870-74.
  • Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
  • Liu M, Vakharia VN (2004): VP1 protein of infectious bursal disease virus modulates the virulence in vivo. Virology, 330, 62-73.
  • Moitra P, Zheng H, Anantharaman V ve ark. (2015): Expression, purification, and biological characterization of Babesia microti apical membrane antigen 1. Infect Immun, 83, 3890-01.
  • Montero E, Rodriguez M, Oksov Y ve ark. (2009): Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell. Infect Immun, 77, 4783-93.
  • Moreau E, Bonsergent C, Al Dybiat I ve ark. (2015): Babesia divergens apical membrane antigen-1 (BdAMA-1): A poorly polymorphic protein that induces a weak and late immune response. Exp Parasitol, 155, 40-45.
  • Ochirkhuu N, Konnai S, Mingala CN ve ark. (2015): Molecular epidemiological survey and genetic analysis of vector-borne infections of cattle in Luzon Island, the Philippines. Vet Parasitol, 212, 161-167.
  • ORF Finder (2015): Open reading frame finder. Available at http://www.ncbi.nlm.nih.gov/projects/gorf/ (Accessed 08 April 2015).
  • Posada D (2008): jModelTest: Phylogenetic model averaging. Mol Biol Evol, 25, 1253-56.
  • Ramsey KH, Sigar IM, Schripsema JH ve ark. (2009): Strain and virulence diversity in the mouse pathogen Chlamydia muridarum. Infect Immun, 77, 3284-93.
  • Remarque EJ, Faber BW, Kocken CH ve ark. (2008): Apical membrane antigen 1: A malaria vaccine candidate in review. Trends Parasitol, 24, 74-84.
  • Remarque EJ, Roestenberg M, Younis S ve ark. (2012): Humoral immune responses to a single allele PfAMA1 vaccine in healthy malaria-naive adults. Plos One, 7, e38898.
  • Rice P, Longden I, Bleasby A (2000): EMBOSS: The European molecular biology open software suite. Trends Genet, 16, 276-277.
  • Rodrigues MHC, Rodrigues KM, Oliveira TR ve ark. (2005): Antibody response of naturally infected individuals to recombinant Plasmodium vivax apical membrane antigen-1. Int J Parasitol, 35, 185-192.
  • Salama AA, Terkawi MA, Kawai S ve ark. (2013): Specific antibody to a conserved region of Babesia apical membrane antigen-1 inhibited the invasion of B. bovis into the erythrocyte. Exp Parasitol, 135, 623-628.
  • Sambrook J, Russell DW (2001): Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
  • Sevinc F, Xuan X (2015): Major tick-borne parasitic diseases of animals: A frame of references in Turkey. Eurasian J Vet Sci, 31, 132-142.
  • Sivakumar T, Lan DT, Long PT ve ark. (2013): PCR detection and genetic diversity of bovine hemoprotozoan parasites in Vietnam. J Vet Med Sci, 75, 1455-62.
  • Sivakumar T, Tattiyapong M, Fukushi S ve ark. (2014): Genetic characterization of Babesia and Theileria parasites in water buffaloes in Sri Lanka. Vet Parasitol, 200, 24-30.
  • Takala SL, Coulibaly D, Thera M ve ark. (2009): Extreme polymorphism in a vaccine antigen and risk of clinical malaria: Implications for vaccine development. Sci Transl Med, 1, 2ra5.
  • Terkawi MA, Thekisoe OM, Katsande C ve ark. (2011): Serological survey of Babesia bovis and Babesia bigemina in cattle in South Africa. Vet Parasitol, 182, 337-342.
  • Tonukari NJ (2010): Theileria parva apical membrane antigen-1 (AMA-1) shares conserved sequences with apicomplexan homologs. Int J Biotech Mol Biol Res, 1, 36- 41.
  • Torina A, Agnone A, Sireci G (2010): Characterization of the apical membrane antigen-1 in Italian strains of Babesia bigemina. Transbound Emerg Dis, 57, 52-56.
  • Torina A, Caracappa S (2007): Babesiosis in Italy: An overview. Parasitologia, 49, 23-28.
  • Torina A, Cordaro A, Blanda V ve ark. (2016): A promising new ELISA diagnostic test for cattle babesiosis based on Babesia bigemina apical membrane antigen-1. Vet Ital, 52, 63-69.
  • Tyler JS, Treeck M, Boothroyd JC (2011): Focus on the ringleader: The role of AMA1 in apicomplexan invasion and replication. Trends Parasitol, 27, 410-420.
  • Uilenberg G (2006): Babesia-A historical overview. Vet Parasitol, 138, 3-10.
  • Xu L, Bao L, Zhou J ve ark. (2011): Genomic polymorphism of the pandemic A (H1N1) influenza viruses correlates pathogenicity in vitro and in vivo. Plos One, 6, e20698.
  • Ybanez AP, Sivakumar T, Ybanez RH ve ark. (2013): Molecular survey of bovine vector-borne pathogens in Cebu, Philippines. Vet Parasitol, 196, 13-20.
  • Zhang H, Compaore MK, Lee EG ve ark. (2007): Apical membrane antigen 1 is a cross-reactive antigen between Neospora caninum and Toxoplasma gondii, and the anti- NcAMA1 antibody inhibits host cell invasion by both parasites. Mol Biochem Parasitol, 151, 205-212.
  • Zhou J, Yang J, Zhang G ve ark. (2006): Babesia gibsoni: An apical membrane antigen-1 homologue and its antibody response in the infected dogs. Exp Parasitol, 114, 329-333. Geliş tarihi: 16.02.2017 / Kabul tarihi: 15.06.2017 Address for correspondence: Dr. Arif ÇİLOĞLU Erciyes Üniversitesi, Veteriner Fakültesi, Parazitoloji Anabilim Dalı, 38039, Kayseri, Türkiye. e-mail: arifciloglu@gmail.com
There are 52 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Other ID JA59UT85AP
Journal Section Research Article
Authors

Arif Çiloğlu

Abdullah İnci

Alparslan Yıldırım

Zuhal Önder

Önder Düzlü

Publication Date September 1, 2018
Published in Issue Year 2018Volume: 65 Issue: 3

Cite

APA Çiloğlu, A., İnci, A., Yıldırım, A., Önder, Z., et al. (2018). Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 65(3), 239-246. https://doi.org/10.1501/Vetfak_0000002852
AMA Çiloğlu A, İnci A, Yıldırım A, Önder Z, Düzlü Ö. Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain. Ankara Univ Vet Fak Derg. September 2018;65(3):239-246. doi:10.1501/Vetfak_0000002852
Chicago Çiloğlu, Arif, Abdullah İnci, Alparslan Yıldırım, Zuhal Önder, and Önder Düzlü. “Molecular Characterization and Expression of the Apical Membrane Antigen-1 from in Vivo and in Vitroisolates of Babesia Bigemina Kayseri/Turkey Strain”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65, no. 3 (September 2018): 239-46. https://doi.org/10.1501/Vetfak_0000002852.
EndNote Çiloğlu A, İnci A, Yıldırım A, Önder Z, Düzlü Ö (September 1, 2018) Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65 3 239–246.
IEEE A. Çiloğlu, A. İnci, A. Yıldırım, Z. Önder, and Ö. Düzlü, “Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain”, Ankara Univ Vet Fak Derg, vol. 65, no. 3, pp. 239–246, 2018, doi: 10.1501/Vetfak_0000002852.
ISNAD Çiloğlu, Arif et al. “Molecular Characterization and Expression of the Apical Membrane Antigen-1 from in Vivo and in Vitroisolates of Babesia Bigemina Kayseri/Turkey Strain”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 65/3 (September 2018), 239-246. https://doi.org/10.1501/Vetfak_0000002852.
JAMA Çiloğlu A, İnci A, Yıldırım A, Önder Z, Düzlü Ö. Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain. Ankara Univ Vet Fak Derg. 2018;65:239–246.
MLA Çiloğlu, Arif et al. “Molecular Characterization and Expression of the Apical Membrane Antigen-1 from in Vivo and in Vitroisolates of Babesia Bigemina Kayseri/Turkey Strain”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 65, no. 3, 2018, pp. 239-46, doi:10.1501/Vetfak_0000002852.
Vancouver Çiloğlu A, İnci A, Yıldırım A, Önder Z, Düzlü Ö. Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitroisolates of Babesia bigemina Kayseri/Turkey strain. Ankara Univ Vet Fak Derg. 2018;65(3):239-46.