Genomic and biological characterization of Pigeon Paramyxovirus Type-1 isolated from Indian pigeons: First report on the six nucleotide insertion in the non-coding region of nucleoprotein gene


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Authors

  • V S AKHILA Department of Veterinary Microbiology, Madras Veterinary College, Chennai, Tamil Nadu
  • J JOHN KIRUBAHARAN Department of Veterinary Microbiology, Madras Veterinary College, Chennai, Tamil Nadu
  • RANJANI RAJASEKARAN Department of Veterinary Microbiology, Veterinary College and Research Institute, TANUVAS, Theni, Tamil Nadu
  • P SHILPA Veterinary Polyclinic, Kodugallur, Thrissur, Kerala
  • M VIDHYA Department of Veterinary Microbiology, Madras Veterinary College, Chennai, Tamil Nadu
  • S RAJALAKSHMI Department of Veterinary Microbiology, Madras Veterinary College, Chennai, Tamil Nadu

https://doi.org/10.56093/ijans.v93i6.132450

Keywords:

Avian Orthoavulavirus 1, FPCS analysis, Genotyping, Newcastle disease, Pathotype, Pigeon Paramyxovirus

Abstract

Genotypic analysis of Pigeon Paramyxovirus Type-1 (PPMV-1) virus, in corroboration with pathotyping, underpins the knowledge on the occurrence of PPMV-1 mediated Newcastle disease in poultry. In the present study, two PPMV-1 isolates, namely D167 and D168, obtained from feral pigeons of India in the year 2014 were analysed for their genotypic and pathotypic characteristics. Phylogenetic analysis of Fusion (F) gene grouped D167 and D168 under sub-genotypes VI.2.2.2. and VI.2.1.1.2.2. respectively. The separate positioning of these isolates within genotype VI is corroborated with the variation in restriction enzyme sites analysed through virtual restriction mapping. Analysis of FPCS region showed that both D167 and D168 possessed 112RRQKRF117 amino-acid pattern. Intra-cerebral pathogenicity index (ICPI) of D167 and D168 was 1.57 and 1.3, and mean death time (MDT) was 48 and 70 hrs respectively, designating D168 as a mesogenic pathotype, and D167 as a velogenic pathotype. Histopathological analysis of proventriculus, intestine, lungs and spleen of chickens infected with D167 and D168 isolates through intramuscular (I/M), subcutaneous (S/C) and oculo-nasal/oral (O/N) routes of inoculation showed similar severity of tissue damage. This study shows that PPMV-1 isolates belonging to two different sub-genotypes without a common ancestor, can occur together in a particular geographical region. It also shows that PPMV-1 gains virulence in chickens, which needs to be addressed in order to avoid emergence of PPMV-1 as new velogenic variant causing Newcastle disease in chickens.

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References

Afonso C L. 2021. Virulence during Newcastle disease viruses cross species adaptation. Viruses 13(1): 110. DOI: https://doi.org/10.3390/v13010110

Alexander D J and Swayne D E. 1998. Newcastle disease virus and other avian paramyxoviruses. A laboratory manual for the isolation and identification of avian pathogens, 4th ed, pp 156–163. (Eds) Swayne D E, Glisson J R, Jackwood M W, Pearson J E and Reed W M. The American Association of Avian Pathologists, Kennett Square, PA. https://doi.org/10.1002/9781119421481.ch3 DOI: https://doi.org/10.1002/9781119421481.ch3

Allan W H, Lancaster J E and Toth B. 1978. Newcastle disease vaccine, their production and use. FAO Animal production and health services. 10th edn. Food and Agricultural Organisation of the United Nations, Rome.

Awu A, Shao M Y, Liu M M, Hu Y X, Qin Z M, Tian F L and Zhang G Z. 2015. Characterization of two pigeon paramyxovirus type 1 isolates in China. Avian Pathology 44(3): pp. 204–11. https://doi.org/10.1080/03079457.2015.1025255 DOI: https://doi.org/10.1080/03079457.2015.1025255

Collins M S, Strong I and Alexander D J. 1994. Evaluation of the molecular basis of pathogenicity of the variant Newcastle disease viruses termed “pigeon PMV-1 viruses”. Archives of Virology 134(3): 403–11. https://doi.org/10.1007/bf01310577 DOI: https://doi.org/10.1007/BF01310577

Czeglédi A, Ujvári D, Somogyi E, Wehmann E, Werner O and Lomniczi B. 2006. Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications. Virus Research 120(1-2): 36–48. https://doi.org/10.1016/j.virusres.2005.11.009 DOI: https://doi.org/10.1016/j.virusres.2005.11.009

Dai Y, Cheng X, Liu M, Shen X, Li J, Yu S, Zou J and Ding C. 2014. Experimental infection of duck origin virulent Newcastle disease virus strain in ducks. BMC Veterinary Research 10(1): 1–9. https://doi.org/10.1186/1746-6148-10-164 DOI: https://doi.org/10.1186/1746-6148-10-164

Dey S, Chellappa M M, Gaikwad S, Kataria J M and Vakharia V N. 2014. Genotype characterization of commonly used Newcastle disease virus vaccine strains of India. PLoS One 9(6): e98869. https://doi.org/10.1371/journal. pone.0098869 DOI: https://doi.org/10.1371/journal.pone.0098869

Dimitrov K M, Abolnik C, Afonso C L, Albina E, Bahl J, Berg M, Briand F X, Brown I H, Choi K S, Chvala I and Diel D G. 2019. Updated unified phylogenetic classification system and revised nomenclature for Newcastle disease virus. Infection, Genetics and Evolution 74: 103917. https://doi. org/10.1016/j.meegid.2019.103917 DOI: https://doi.org/10.1016/j.meegid.2019.103917

Dortmans J C, Fuller C M, Aldous E W, Rottier P J and Peeters B P. 2010. Two genetically closely related pigeon paramyxovirus type 1 (PPMV-1) variants with identical velogenic fusion protein cleavage sites but with strongly contrasting virulence. Veterinary Microbiology 143(2-4): 139–44. https://doi.org/10.1016/j.vetmic.2009.11.021 DOI: https://doi.org/10.1016/j.vetmic.2009.11.021

El-Morshidy Y, Abdo W, Elmahallawy E K, Abd EL-Dayem G A, El-Sawak A, El-Habashi N, Mosad S M, Lokman M S, Albrakati A and Abou Asa S. 2021. Pathogenesis of velogenic genotype VII. 1.1 Newcastle Disease Virus isolated from chicken in Egypt via different inoculation routes: Molecular, histopathological, and immunohistochemical study. Animals (Basel) 11(12): 3567. https://doi.org/10.3390/ani11123567 DOI: https://doi.org/10.3390/ani11123567

Ganar K, Das M, Raut A A, Mishra A and Kumar S. 2017. Emergence of a deviating genotype VI pigeon paramyxovirus type-1 isolated from India. Archives of Virology 162(7): 2169– 74. https://doi.org/10.1007/s00705-017-3340-2 DOI: https://doi.org/10.1007/s00705-017-3340-2

Hall T A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series 41: 95–8.

Huang Y, Wan H Q, Liu H Q, Wu Y T and Liu X F. 2004. Genomic sequence of an isolate of Newcastle disease virus isolated from an outbreak in geese: a novel six nucleotide insertion in the non-coding region of the nucleoprotein gene. Archives of Virology 149(7): 1445–57. https://doi.org/10.1007/s00705- 004-0297-8 DOI: https://doi.org/10.1007/s00705-004-0297-8

Kaleta E F, Alexander D J and Russell P H. 1985. The first isolation of the avian PMV-1 virus responsible for the current panzootic in pigeons? Avian Pathology 14: 553–57. https://doi.org/10.1080/03079458508436258 DOI: https://doi.org/10.1080/03079458508436258

Khan T A, Rue C A, Rehmani S F, Ahmed A, Wasilenko J L, Miller P J and Afonso C L. 2010. Phylogenetic and biological characterization of Newcastle disease virus isolates from Pakistan. Journal of Clinical Microbiology 48(5): 1892–94. https://doi.org/10.1128/JCM.00148-10 DOI: https://doi.org/10.1128/JCM.00148-10

Kommers G D, King D J, Seal B S and Brown C C. 2003. Virulence of six heterogeneous-origin Newcastle disease virus isolates before and after sequential passages in domestic chickens. Avian Pathology 32(1): 81–93. https://doi.org/10.1080/0307945021000070750 DOI: https://doi.org/10.1080/0307945021000070750

Kumanan K, Meenu R, Sridhar R, Muralimanohar B and Nainar A M. 2002. A report on Ranikhet disease in emus (Dromaius novaehollandiae). Indian Veterinary Journal 79(7): 741–42.

Lamb R A and Parks T S. 2007. Structural basis of viral invasion: Lessons from paramyxovirus. Current Opinion in Structural Biology 17: 427–36. https://doi.org/10.1016/j.sbi.2007.08.016 DOI: https://doi.org/10.1016/j.sbi.2007.08.016

Mangat A P, Singh G and Gill B S. 1988. An outbreak of paramyxovirus encephalomyelitis in racing pigeons in India. Veterinar Records 123(19): 496. https://doi.org/10.1136/vr.123.19.496 DOI: https://doi.org/10.1136/vr.123.19.496

Meulemans G, Berg T V, Decaesstecker M and Boschmans M. 2002. Evolution of pigeon Newcastle disease virus strains. Avian Pathology 31(5): 515–19. https://doi.org/10.1080/0307945021000005897 DOI: https://doi.org/10.1080/0307945021000005897

Millar N S and Emmerson P T. 1988. Molecular cloning and nucleotide sequencing of Newcastle disease virus. Newcastle Disease, pp. 79-97. (Ed) Alexander D J. Kluwer Academic Publishers Springer, Boston. https://doi.org/10.1007/978-1-4613-1759-3_5 DOI: https://doi.org/10.1007/978-1-4613-1759-3_5

Miller P J, Dimitrov K M, Williams-Coplin D, Peterson M P, Pantin-Jackwood M J, Swayne D E, Suarez D L and Afonso C L. 2015. International biological engagement programs facilitate Newcastle disease epidemiological studies. Front Public Health 3: 235. https://doi.org/10.3389/fpubh.2015.00235 DOI: https://doi.org/10.3389/fpubh.2015.00235

Munir M, Abbas M, Khan M T, Zohari S and Berg M. 2010. Genomic and biological characterization of a velogenic Newcastle disease virus isolated from a healthy backyard poultry flock in 2010. Virology Journal 9(1): 46. https://doi. org/10.1186/1743-422x-9-46 DOI: https://doi.org/10.1186/1743-422X-9-46

Naveen K A and Singh S D. 2004. Studies on characterization and pathogenicity of Newcastle disease virus isolated from pigeons in India. Indian Journal of Veterinary Pathology 24: 150–58.

Naveen K A, Singh S D, Kataria J M, Barathidasan and Dhama K. 2013. Detection and differentiation of pigeon paramyxovirus serotype-1 (PPMV-1) isolates by RT-PCR and restriction enzyme analysis. Tropical Animal Health and Production 45(5): 1231–36. https://doi.org/10.1007/s11250-013-0352-0 DOI: https://doi.org/10.1007/s11250-013-0352-0

Office International des Epizooties. 2012. Newcastle disease. Chapter 2.3.14. OIE terrestrial manual 2012: manual of diagnostic tests and vaccines for terrestrial animals. pp. 576 – 589. World Organization for Animal Health, Paris.

Phillips R J, Samson A C and Emmerson P T. 1998. Nucleotide sequence of the 5′-terminus of Newcastle disease virus and assembly of the complete genomic sequence: agreement with the “rule of six”. Archives of Virology 143(10): 1993–2002. https://doi.org/10.1007/s007050050435 DOI: https://doi.org/10.1007/s007050050435

Pushpa R N, Kirubaharan J J and Koteeswaran A. 2009. Phylogenetic analysis of the Nucleoprotein gene of Newcastle disease vaccine viruses in India. International Journal of Poultry Science 8(12): 1137–50. http://dx.doi.org/10.3923/ ijps.2009.1137.1150 DOI: https://doi.org/10.3923/ijps.2009.1137.1150

Qin Z M, Tan L T, Xu H Y, Ma B C, Wang Y L, Yuan X Y and Liu W J. 2008. Pathotypical characterization and molecular epidemiology of Newcastle disease virus isolates from different hosts in China from 1996 to 2005. Journal of Clinical Microbiology 46(2): 601–11. https://doi.org/10.1128/jcm.01356-07 DOI: https://doi.org/10.1128/JCM.01356-07

Qiu X, Meng C, Zhan Y, Yu S, Li S, Ren T, Yuan W, Xu S, Sun Y, Tan L and Song C. 2017. Phylogenetic, antigenic and biological characterization of pigeon paramyxovirus type 1 circulating in China. Virology Journal 14(1): 1–3. https://doi.org/10.1186/s12985-017-0857-7 DOI: https://doi.org/10.1186/s12985-017-0857-7

Saif Y M, Fadly A M, Glisson J R and McDougald L R. 2008. Newcastle disease, other avian paramyxoviruses, and pneumovirus infections. Diseases of Poultry, 12th edition, pp. 75 – 93. (Eds) Swayne D E. Blackwell Publishing Professional, Ames, Iowa, USA. https://doi.org/10.20506/rst.19.2.1231 DOI: https://doi.org/10.20506/rst.19.2.1231

Sarika N, Kirubaharan J J, Vidhya M, Shilpa P and Rajasekaran R. 2022. Emergence of XIII. 2.2 genotype of Avian Avulavirus-1 with unique FPCS site in India. Indian Journal of Animal Sciences 92(7): 814–18. https://doi.org/10.56093/ijans. v92i7.105529 DOI: https://doi.org/10.56093/ijans.v92i7.105529

Seal B S, King D J and Meinersmann R J. 2000. Molecular evolution of the Newcastle disease virus matrix protein gene and phylogenetic relationships among the paramyxoviridae. Virus Research 66(1): 1–11. https://doi.org/10.1016/s0168-1702(99)00119-7 DOI: https://doi.org/10.1016/S0168-1702(99)00119-7

Senthilkumar N, Kataria J M, Dhama K and Toroghi R. 2003. Sequence analysis of the cleavage site-encoding region of the fusion protein gene of Newcastle disease viruses obtained from pigeon, guinea fowl and quail. Indian Journal of Comparative Microbiology Immunology and Infectious Diseases 24(2): 191.

Shan S, Bruce K, Stevens V, Wong F Y, Wang J, Johnson D, Middleton D, O’Riley K, McCullough S, Williams D T and Bergfeld J. 2021. In vitro and in vivo characterization of a pigeon Paramyxovirus type 1 isolated from domestic pigeons in Victoria, Australia 2011. Viruses 13(3): 429. https://doi.org/10.3390/v13030429 DOI: https://doi.org/10.3390/v13030429

Tamura K and Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–26. https://doi.org/10.1093/oxfordjournals.molbev.a040023 DOI: https://doi.org/10.1093/oxfordjournals.molbev.a040023

Tamura K, Stecher G and Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution, 38: pp. 3022–27. https://doi.org/10.1093/molbev/msab120 DOI: https://doi.org/10.1093/molbev/msab120

Tirumurugaan K G, Kapgate S, Vinupriya M K, Vijayarani K, Kumanan K and Elankumaran S. 2011. Genotypic and pathotypic characterization of Newcastle disease viruses from India. PloS One 6(12): e28414. https://doi.org/10.1371/journal.pone.0028414 DOI: https://doi.org/10.1371/journal.pone.0028414

Ujvari D, Wehmann E, Kaleta E F, Werner O, Savic V, Nagy E, Czifra G and Lomniczi B. 2003. Phylogenetic analysis reveals extensive evolution of avian paramyxovirus type 1 strains of pigeons (Columba livia) and suggests multiple species transmission. Virus Research 96: 63–73. https://doi. org/10.1016/s0168-1702(03)00173-4 DOI: https://doi.org/10.1016/S0168-1702(03)00173-4

Uthrakumar A, Vijayarani K, Kumanan K and Thiagarajan V. 2013. Molecular characterization of thermostable Newcastle disease virus isolated from pigeon. Indian Journal of Virology 241: 42–47. https://doi.org/10.1007/s13337-012-0120-1 DOI: https://doi.org/10.1007/s13337-012-0120-1

Wang J, Liu H, Liu W, Zheng D, Zhao Y, Li Y, Wang Y, Ge S, Lv Y, Zuo Y and Yu S. 2015. Genomic characterizations of six pigeon paramyxovirus type 1 viruses isolated from live bird markets in China during 2011 to 2013. PLoS One 10(4): e0124261. https://doi.org/10.1371/journal.pone.0124261 DOI: https://doi.org/10.1371/journal.pone.0124261

Wang X, Gong Z, Zhao L, Wang J, Sun G, Liu Y, Tao P, Zhang H, Li S, Jiang F and Hu Y. 2013. Complete genome sequences of Newcastle disease virus strains isolated from three different poultry species in China. Genome Announcements 1(4): e00198-12. https://doi.org/10.1128/genomeA.00198-12 DOI: https://doi.org/10.1128/genomeA.00198-12

Submitted

2023-01-19

Published

2023-07-12

How to Cite

AKHILA, V. S., KIRUBAHARAN, J. J., RAJASEKARAN, R., SHILPA, P., VIDHYA, M., & RAJALAKSHMI, S. (2023). Genomic and biological characterization of Pigeon Paramyxovirus Type-1 isolated from Indian pigeons: First report on the six nucleotide insertion in the non-coding region of nucleoprotein gene. The Indian Journal of Animal Sciences, 93(6), 549–555. https://doi.org/10.56093/ijans.v93i6.132450
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