Genetic analysis of Canine adenovirus type 2 strains circulating in Turkey from past to present

Yıl 2021, Cilt: 32 Sayı: 2, 111 - 117, 30.12.2021

Fahriye Saraç , Veli Gülyaz , Mustafa Hasöksüz , Serdar Uzar , İrem Gülaçtı , Esra Satır , Pelin Tuncer-göktuna , Eray Atıl

https://doi.org/10.35864/evmd.1002786

Öz

Canine adenoviruses (CAV) can infect both domestic and wild canid. Canine Adenovirus Type-1 (CAV-1) and Canine Adenovirus Type-2 (CAV-2) are the cause of infectious canine hepatitis and infectious canine laryngotracheitis, respectively. The epidemiology of the virus is not clear enough in the most territory. For this purpose, data on the virus in Turkey, which is a bridge between continents, were examined. Comparing the sequence data of strains circulated in the field over a ten-year period revealed a genetic heterogeneity. To make this comparision total of 32 fecal samples collected from shelter dogs with diarrhea in 2011 was used. Firstly, virus isolation was performed in MDCK cells and cytopathogenic effects were observed in 4/32 samples. Secondly, the supernatant of four isolates were found positive for the E3 gene of CAV-2 by PCR. Strains were placed on a different branch from other Turkish isolates under the same subgroup in the phylogenetic tree. According to partial E3 gene analysis, seven amino acid substitutions were detected between the strains. Due to Shannon entropy value and ConSurf analysis, all of them were indicated as important antigenic sites. This study pointed out the possible genetic heterogeneity among CAV-2 in Turkey.

Anahtar Kelimeler

Canine adenovirus type 2, molecular characterization, virus isolation

Destekleyen Kurum

Ministry of Agriculture and Forestry General Directorate of Food and Control

Geçmişten günümüze Türkiye’de dolaşımda olan Canine adenovirus tip 2 suşlarının genetik incelemesi

Öz

Canine adenoviruslar (CAV) hem evcil hem de vahşi yaşamda köpek ve tilkilerde enfeksiyona neden olabilmektedir. Canine Adenovirus Tip-1 (CAV-1) infectious canine hepatitis (ICH) enfeksiyonuna ve Canine Adenovirus Tip-2 (CAV-2) infectious canine laryngotracheitis enfeksiyonuna neden olmaktadır. Virusun epidemiyolojisi çoğu bölgede yeterince net değildir. Bu amaçla Türkiye'de on yıllık süre zarfında dolaşımda olan suşlar moleküler düzeyde incelendi ve genetik bir heterojenlik olduğu görüldü. Bu incelemeyi yapabilmek için 2011 yılında ishalli barınak köpeklerinden toplanan 32 adet dışkı örneği kullanıldı. İlk olarak, MDCK hücre hattında virus izolasyonu yapıldı ve 4/32 örnekte sitopatojenik etkiler (CPE) gözlendi. İkinci olarak, CPE pozitif dört izolat CAV-2'nin E3 geni yönünden PCR ile pozitif bulundu. Sekans işlemi sonucu elde edilen diziler filogenetik ağaçta aynı alt grup altındaki diğer Türk izolatlarından farklı bir dal üzerine yerleşti. Kısmi E3 gen analizine göre, suşlar arasında yedi amino asitte değişim tespit edildi. Shannon entropi değeri ve ConSurf analizine göre tüm amino asit değişikliklerinin önemli antijenik bölgelerde meydana geldiği belirlendi. Bu çalışma, Türkiye CAV-2 suşları arasındaki olası genetik heterojeniteye dikkat çekmektedir.

Anahtar Kelimeler

Canine adenovirus tip 2, moleküler karakterizasyon, virus izolasyonu

Kaynakça

• Abdelmagid OY, Larson L, Payne L, Tubbs A, Wasmoen T, Schultz R R. (2004) Evaluation of the efficacy and duration of immunity of a canine combination vaccine against virulent parvovirus, infectious canine hepatitis virus, and distemper virus experimental challenges. Vet Ther. 5, :173-186.
• Andrukonis A, Brown KM, Hall NJ, Protopopova A. (2021) Intake vaccinations reduced signs of canine respiratory disease during an outbreak at an animal shelter. Front Vet Sci. 8, :627580. https://doi.org/10.3389/fvets.2021.627580
• Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. (2010) ConSurf 2010: Calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38 (Web Server issue): W529–-W533. https://doi.org/10.1093/nar/gkq399
• Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T, Ben-Tal N. (2016) ConSurf 2016: An improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44 (W1): W344-–W350. https://doi.org/10.1093/nar/gkw408
• Balboni A, Verin R, Morandi F, Poli A, Prosperi S, Battilani M. (2013) Molecular epidemiology of canine adenovirus type 1 and type 2 in free-ranging red foxes (Vulpes vulpes) in Italy. Vet Mic. 162, :551-–557. https://doi.org/10.1016/j.vetmic.2012.11.015
• Balboni A, Mollace C, Giunti M, Dondi F, Prosperi S, Battilani M. (2014) Investigation of presence of canine adenovirus (CAV) in owned dogs in Northern Italy. Res Vet Sci. 97, :631-636. https://doi.org/10.1016/j.rvsc.2014.10.010
• Barthold SW, Lairmore MD, Bowen RA, Parrish CR, Hedrick RP, Saif LJ, Knowles DP, Swayne DE. (2011) Adenoviridae. In: Maclachlan NJ, Dubovi EJ. (Eeds). Fenner’s Veterinary Virology, 4Fourth edition. Academic Press, United States, pp. 203-212.
• Benetka V, Weissenbock H, Kudielka I, Pallan C, Rothmuller G, Mostl K. (2006) Canineadenovirus type 2 infection in four puppies with neurological signs. Vet Rec. 158, :91–-94. https://doi.org/10.1136/vr.158.3.91
• Bulut O, Yapici O, Avci O, Simsek A, Atli K, Dik I, Yavru S, Hasırcıoglu S, Kale M, Mamak N. (2013) The serological and virological investigation of canine adenovirus infection on the dogs. Scientific World Journal. 587024. https://doi.org/10.1155/2013/587024
• Buonavoglia C, Martella V. (2007) Canine respiratory viruses. Veterinary Research. 38, : 355-373. https://doi.org/ 10.1051/vetres:2006058
• Can Şahna K, Aslan Ö. (2015) Köpek idrar ve plazma örneklerinde canine adenovirus (CAV) antijeninin ELISA ile araştırılması. Harran Univ Vet Fak Dergsi. 4, :45--47 (in Turkish with an abstract in English)
• Celniker G, Nimrod G, Ashkenazy H, Glaser F, Martz E, Mayrose I, Pupko T, Ben-Tal N. (2013) ConSurf: Using evolutionary data to raise testable hypotheses about protein function. Isr J Chem. 53, :199-206. https://doi.org/10.1002/ijch.201200096
• Chander, V., Sharma, G.K., Bhatt, M, Nandi S, Mahajan S, Singh M, Mahendran K, Karikalan M, Pawde AM, Gupta V, Singh KP, Rajak KK, Gupta VK, Singh RK. (2021) Isolation and genetic characterization of canine adenovirus type 2 from a domestic dog showing neurological symptoms. Braz J Microbiol. https://doi.org/10.1007/s42770-021-00540-0
• Chaturvedi U, Tiwari AK, Ratta B, Ravindra PV, Rajawat YS, Palia SK, Rai A. (2008) Detection of canine adenoviral infections in urine and faeces by the polymerase chain reaction. J Virol Methods. 149, :260–263. https://doi.org/10.1016/j.jviromet.2008.01.024
• Cunha RDS, Silva Junior CL, Costa CA, de Aguiar HM, Junqueira Júnior DG. (2020) Comparison of immunity against canine distemper, adenovirus and parvovirus after vaccination with two multivalent canine vaccines. Vet Med Sci. 6, :330-334. https://doi.org/10.1002/vms3.274
• Damián M, Morales E, Salas G, Trigo FJ. (2005) Immunohistochemical detection of antigens of distemper, adenovirus and parainfluenza viruses in domestic dogs with pneumonia. J Comp Pathol. 133, :289-93. https://doi.org/10.1016/j.jcpa.2005.05.005
• Day MJ, Carey S, Clercx C, Kohnx B, MarsilIo F, Thiry E, Freyburger L, Schulz B, Walker DJ. (2020) Aetiology of canine infectious respiratory disease complex and prevalence of its pathogens in Europe. J Comp Pathol. 176:, 86-108. https://doi.org/10.1016/j.jcpa.2020.02.005
• Ditchfield J, Macpherson LW, Zbitnew A. (1962) Association of a canine adenovirus (Toronto A 26/61) with an outbreak of laryngotracheitis ("Kennel Cough"): A Preliminary Report. Can Vet J. 3, :238-247.
• Erles K, Dubovi EJ, Brooks HV, Brownli J. (2004) Longitudinal study of viruses associated with canine ınfectious respiratory disease. J Clin Microbiol. 42, :4524–-4529. https://doi.org/10.1128/JCM.42.10.4524-4529.2004
• Gooding LR, Ranheim TS, Tollefson AE, Aquino L, Duerksen-Hughes P, Horton TM, Wold WMS. (1991) The 10,400 and 14,500 dalton proteins encoded by region E3 of adenoviruses function together to protect many but not all cell lines against lysis by tumor necrosis factor. J Virol. 65, :4114-4123. https://doi.org/10.1128/JVI.65.8.4114-4123.1991
• Gür S, Acar A. (2009) A retrospective investigation of canine adenovirus (CAV) infection in adult dogs in Turkey. J S Afr Vet Assoc. 80, :84-–86. https://doi.org/10.4102/jsava.v80i2.176
• Hamelin C, Jouvenne P, Assaf R. (1985) Association of a type-2 canine adenovirus with an outbreak of diarrhoeal disease among a large dog congregation J Diarrhoeal Dis Res. 3, :84-–87.
• Hamir AN, Raju N, Rupprecht CE. (1992) Experimental oral administration of canine adenovirus (type 2) to raccoons (Procyon lotori). (1992) Vet Pathol. 29, :509-513. https://doi.org/10.1177/030098589202900604
• Hu RL, Huang G, Qiu W, Zhong ZH, Xia XZ, Yin Z. (2001) Detection and differentiation of CAV-1 and CAV-2 by polymerase chain reaction. Vet Res Commun. 25, :77–84. https://doi.org/10.1023/a:1006417203856
• Kärber G. (1931) Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Archiv f Experiment Pathol U Pharmakol. 162:, 480–-483. https://doi.org/10.1007/BF01863914
• Kim SH, Huh JH, Bae SY, Kim JS, Yoon SY, Lim CS, Cho Y, Kim YK, Lee KN, Lee CK. (2006) Epidemiology of Respiratory Viral Infection in 2004-2006. The Korean J Lab Med. 26, :351-357. https://doi.org/10.3343/kjlm.2006.26.5.351
• Kvist S, Ostberg L, Persson H, Philipson L, Peterson PA. (1978) Molecular association between transplantation antigens and cell surface antigens in adenovirus-transformed cell line. Proc Natl Acad Sci U S A. 75, :5674-5678. https://doi.org/10.1073/pnas.75.11.5674
• Macartney L, Cavanagh HM, Spibey N. (1988) Isolation of canine adenovirus-2 from the faeces of dogs with enteric disease and its unambiguous typing by restriction endonuclease mapping. Res Vet Sci. 44,: 9-–14.
• Mochizuki M, Yachi A, Ohshima T, Ohuchi A, Ishida T. (2008) Etiologic study of upper respiratory infections of household dogs. J Vet Med Sci. 70, :563–569. https://doi.org/10.1292/jvms.70.563
• Mohammadi A, Masoudian M, Nemati Y. (2011) Evaluation of PCR techniques for detection and differentiation of canine adenoviruses in faecal samples in Shiraz, Iran. Iran Bulg J Vet Med. 14, :247−251.
• Parthiban M, Kumanan K, Sunder K, Senthil Kumar S, Kathiresan D. (2009) Molecular detection of canine adenovirus using polymerase chain reaction and sequencing. TNJVAS. 5, :140-142.
• Posuwan N, Payungporn S, Thontiravong A, Kitikoon P, Amonsin A, Poovorawan Y. (2010) Prevalence of respiratory viruses isolated from dogs in Thailand during 2008-2009. Asian Biomed. 4, :563-569. https://doi.org/10.2478/abm-2010-0071
• Raja P, Sachin V, Parthiban M, Janaki PA. (2021). Molecular characterization of canine adenovirus type 2 in dogs from India. Virus Dis. 32, :369–-374. https://doi.org/10.1007/s13337-021-00690-7
• Shannon CE. (1948) The mathematical theory of communication. Bell Syst Tech J. 27, :379-–423 & and 623–-656. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
• Spearman C. (1908) The method of “right and wrong cases” (constant stimuli) without Gauss’s formula. Br J Psychol. 2, :227-–242. https://doi.org/10.1111/j.2044-8295.1908.tb00176.x
• Timurkan MO, Aydin H, Alkan F. (2018) Detection and molecular characterization of canine adenovirus Type-2 (CAV-2) in dogs with respiratory tract symptoms in shelters in Turkey. Veterinarski Arhiv. 88, :467-479. https://doi.org/doi: 10.24099/vet.arhiv.0052
• Universidad Complutense de Madrid, Protein Variability Server [(online]). Access address: Website http://imed.med.ucm.es/PVS/ Date of access: Accessed 18 April 2021.
• Yang DK, Kim HH, Yoo JY, Ji M, Han BH, Oh S, Hyun BH. (2020) Immunogenicity of a new, inactivated canine adenovirus Type-2 vaccine for dogs. Clin Exp Vaccine Res. 9, :40-47. https://doi.org/10.7774/cevr.2020.9.1.40
• Yıldırım Y, Kırmızıgül AH, Gökçe E. (2009) Seroprevalence of canine adenovirus (CAV) infection in Kars dogs in Turkey. YYU Vet Fak Derg. 20, :37–39.
• Yoon SS, Byun JW, Park YI, Kim MJ, Bae YC, Song JY. (2010) Comparison of the Diagnostic Methods on the Canine Adenovirus Type-2 Infection. Basic Appl Pathol. 3, :52-56. https://doi.org/10.1111/j.1755-9294.2010.01073.x
• Zhang XL, Bellett AJ, Hla RT, Braithwaite AW, Müllbacher A. (1991) Adenovirus type 5 E3 gene products interfere with the expression of the cytolytic T cell immunodominant E1a antigen. Virology. 180, :199-206. https://doi.org/10.1016/0042-6822(91)90024-6