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Genetic analysis of foot-and-mouth disease virus serotype A of Indian origin and detection of positive selection and recombination in leader protease- and capsid-coding regions

S B Nagendrakumar1,M Madhanmohan1,P N Rangarajan2,V A Srinivasan1,✉
1Research and Development Centre, Indian Immunologicals Limited, Gachibowli, Hyderabad, 500 032 India
2Department of Biochemistry, Indian Institute of Sciences, Bangalore, 560 080 India
✉

Corresponding author.

Received 2008 Jul 14; Accepted 2008 Oct 16; Issue date 2009.

© Indian Academy of Sciences 2009

This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

PMCID: PMC7090849  PMID:19430121

Abstract

The leader protease (Lpro) and capsid-coding sequences (P1) constitute approximately 3 kb of the foot-and-mouth disease virus (FMDV). We studied the phylogenetic relationship of 46 FMDV serotype A isolates of Indian origin collected during the period 1968–2005 and also eight vaccine strains using the neighbour-joining tree and Bayesian tree methods. The viruses were categorized under three major groups — Asian, Euro-South American and European. The Indian isolates formed a distinct genetic group among the Asian isolates. The Indian isolates were further classified into different genetic subgroups (<5% divergence). Post-1995 isolates were divided into two subgroups while a few isolates which originated in the year 2005 from Andhra Pradesh formed a separate group. These isolates were closely related to the isolates of the 1970s. The FMDV isolates seem to undergo reverse mutation or convergent evolution wherein sequences identical to the ancestors are present in the isolates in circulation. The eight vaccine strains included in the study were not related to each other and belonged to different genetic groups. Recombination was detected in the Lpro region in one isolate (A IND 20/82) and in the VP1 coding 1D region in another isolate (A RAJ 21/96). Positive selection was identified at aa positions 23 in the Lpro (P<0.05; 0.046*) and at aa 171 in the capsid protein VP1 (P<0.01; 0.003**).

Keywords: Foot-and-mouth disease virus, phylogeny, Picornaviridae, positive selection, recombination

Abbreviations used

BHK-21

baby hamster kidney cell line

BTy

bovine thyroid

CTE

C-terminal extension

FMD

foot-and-mouth disease

FMDV

foot-and-mouth disease virus

GARD

genetic analysis for recombination detection

Lpro

leader protease

MCMC

Markov Chain Monte Carlo

NJ

neighbour-joining

ORF

open reading frame

P1

capsid-coding sequence

PCR

polymerase chain reaction

RT-PCR

reverse transcriptase-polymerase chain reaction

SLAC

single likelihood ancestor counting

UTR

untranslated region

UV

ultraviolet

VMMS

virus maintenance medium with (1%) serum

References

  1. Aggarwal N., Barnett P. V. Antigenic sites of foot-and-mouth disease virus (FMDV): an analysis of the specificities of anti-FMDV antibodies after vaccination of naturally susceptible host species. J. Gen. Virol. 2002;83:775–782. doi: 10.1099/0022-1317-83-4-775. [DOI] [PubMed] [Google Scholar]
  2. Araujo J. P., Jr, Montassier H. J., Pinto A. A. Extensive antigenic and genetic variation among foot-and-mouth disease type A viruses isolated from the 1994 and 1995 foci in Sao Paulo Brazil. Vet. Microbiol. 2002;84:15–27. doi: 10.1016/S0378-1135(01)00451-5. [DOI] [PubMed] [Google Scholar]
  3. Arrowsmith A. E. Variation among strains of type A foot-and-mouth disease virus in the Eastern Mediterranean region. J. Hyg. (London) 1975;75:387–97. doi: 10.1017/S0022172400024451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Armstrong R. M., Samuel A. R., Carpenter W. C., Kant R., Knowles N. J. A comparative study of serological and biochemical methods for strain differentiation of foot-and-mouth disease type A viruses. Vet. Microbiol. 1994;39:285–298. doi: 10.1016/0378-1135(94)90165-1. [DOI] [PubMed] [Google Scholar]
  5. Azad H. M., Srinivasan V. A., Crowther J. R. Serological study of type A Indian foot-and-mouth disease virus isolates. Acta Virol. 1995;39:193–196. [PubMed] [Google Scholar]
  6. Baxt B., Vakharia V., Moore D. M., Franke A. J., Morgan D. O. Analysis of neutralizing antigenic sites on the surface of type A12 foot-and-mouth disease virus. J. Virol. 1989;63:2143–2151. doi: 10.1128/jvi.63.5.2143-2151.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Belwal L. M., Palanisamy R., Nagaiah K., Kalanidhi A. P., Jagannatha M., Ramanna B. C., Srinivasan V. A. Serological study of foot and mouth disease virus type A in India. Rev. Sci. Tech. Off. Int. Epiz. 1986;5:723–730. doi: 10.20506/rst.5.3.264. [DOI] [PubMed] [Google Scholar]
  8. Belwal L. M., Kalanidhi A. P., Nagaiah K., Ramanna B. C., Srinivasan V. A. Immuno-serological studies on a foot and mouth disease virus type A strain involved in breakdown of vaccine immunity. Rev. Sci. Tech. Off. Int. Epiz. 1987;6:115–126. doi: 10.20506/rst.6.1.283. [DOI] [PubMed] [Google Scholar]
  9. Bolwell C., Brown A. L., Barnett P. V., Campbell R. O., Clarke B. E., Parry N. R., Ouldridge E. J., Brown F., Rowlands D. J. Host cell selection of antigenic variants of foot-and-mouth disease virus. J. Gen. Virol. 1989;70:45–57. doi: 10.1099/0022-1317-70-1-45. [DOI] [PubMed] [Google Scholar]
  10. Cammack N., Phillips A., Dunn G., Patel V., Minor P. D. Intertypic genomic rearrangements of poliovirus strains in vaccines. Virology. 1988;167:507–514. doi: 10.1016/S0042-6822(88)90113-4. [DOI] [PubMed] [Google Scholar]
  11. Carrillo C., Tulman E. R., Delhon G., Lu Z., Carreno A., Vagnozzi A., Kutish G. F., Rock D. L. Comparative genomics of foot-and-mouth disease virus. J. Virol. 2005;79:6487–6504. doi: 10.1128/JVI.79.10.6487-6504.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheung A., Whitehead P., Weiss S., Kupper H. Nucleotide sequence of the VP1 gene of the foot-and-mouth disease virus strain A Venesclau. Gene. 1984;30:241–245. doi: 10.1016/0378-1119(84)90127-6. [DOI] [PubMed] [Google Scholar]
  13. Freshney R. I. Culture of animal cells: a manual of basic technique. New Jersey: John Wiley; 2004. Primary culture; pp. 158–169. [Google Scholar]
  14. Furione M., Guillot S., Otelea D., Balanant J., Candrea A., Crainic R. Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology. 1993;196:199–208. doi: 10.1006/viro.1993.1468. [DOI] [PubMed] [Google Scholar]
  15. Gorbalenya A. E., Koonin E. V., Lai M. M. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-alpha- and coronaviruses. FEBS Lett. 1991;288:201–205. doi: 10.1016/0014-5793(91)81034-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grubman M. J., Baxt B. Foot-and-mouth disease. Clin. Microbiol. Rev. 2004;17:465–493. doi: 10.1128/CMR.17.2.465-493.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Guarné A., Hampoelz B., Glaser W., Carpena X., Tormo J., Fita I., Skern T. Structural and biochemical features distinguish the foot-and-mouth disease virus leader proteinase from other papain-like enzymes. J. Mol. Biol. 2000;302:1227–1240. doi: 10.1006/jmbi.2000.4115. [DOI] [PubMed] [Google Scholar]
  18. Guarné A., Tormo J., Kirchweger R., Pfistermueller D., Fita I., Skern T. Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBOS J. 1998;17:7469–7479. doi: 10.1093/emboj/17.24.7469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hamblin C., Armstrong R. M., Hedger R. S. A rapid enzyme-linked immunosorbent assay for the detection of foot-and-mouth disease virus in epithelial tissues. Vet. Microbiol. 1984;9:443–435. doi: 10.1016/0378-1135(84)90064-6. [DOI] [PubMed] [Google Scholar]
  20. Huelsenbeck J. P., Ronquist F. Mr.Bayes: Bayesian inference of phylogeny. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. [DOI] [PubMed] [Google Scholar]
  21. Jangra R. K., Tosh C., Sanyal A., Hemadri D., Bandyopadhyay S. K. Antigenic and genetic analyses of foot-and-mouth disease virus type A isolates for selection of candidate vaccine strain reveals emergence of a variant virus that is responsible for most recent outbreaks in India. Virus Res. 2005;112:52–59. doi: 10.1016/j.virusres.2005.03.021. [DOI] [PubMed] [Google Scholar]
  22. King A. M. Q., McCahon Q., Slade D., Newman J. W. I. Biochemical evidence of recombination within the unsegmented RNA genome of Aphthovirus. J. Virol. 1982;41:66–77. doi: 10.1128/jvi.41.1.66-77.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. King A. M. Q., Underwood B. O., McCahon D., Newman J. W. I., Brown F. Biochemical identification of viruses causing the 1981 outbreaks of foot-and-mouth disease in the UK. Nature (London) 1981;293:479–480. doi: 10.1038/293479a0. [DOI] [PubMed] [Google Scholar]
  24. Klein J., Parlak U., Ozyoruk F., Christensen L. S. The molecular epidemiology of foot-and-mouth disease virus serotypes A and O from 1998 to 2004 in Turkey. BMC Vet. Res. 2006;4:35. doi: 10.1186/1746-6148-2-35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Knowles N. J., Samuel A. R. Polymerase chain reaction amplification and cycle sequencing of the 1D (VP1) gene of foot-and-mouth disease virus. Report on Session of Research Group’s Standing Technical Committee of European Commission for the Control of FMD. Austria: FAO; 1995. pp. 45–53. [Google Scholar]
  26. Kumar S., Tamura K., Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinfo. 2004;5:150–163. doi: 10.1093/bib/5.2.150. [DOI] [PubMed] [Google Scholar]
  27. Lole K. S., Bollinger R. C., Paranjape R. S., Gadkari D., Kulkarni S. S., Novak N. G., Ingersoll R., Sheppard H. W., Ray S. C. Fulllength human immunodeficiency virus type 1 genomes from subtype C-infected sero converters in India with evidence of inter subtype recombination. J. Virol. 1999;73:152–160. doi: 10.1128/jvi.73.1.152-160.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mittal M., Tosh C., Hemadri D., Sanyal A., Bandyopadhyay S. K. Phylogeny genome evolution and antigenic variability among endemic foot-and-mouth disease virus type A isolates from India. Arch. Virol. 2005;150:911–928. doi: 10.1007/s00705-004-0469-6. [DOI] [PubMed] [Google Scholar]
  29. Mohapatra J. K., Sanyal A., Hemadri D., Tosh C., Sabarinath G. P., Venkataramanan R. Sequence and phylogenetic analysis of the L and VP1 genes of foot-and-mouth disease virus serotype Asia1. Virus Res. 2002;87:107–118. doi: 10.1016/S0168-1702(02)00006-0. [DOI] [PubMed] [Google Scholar]
  30. Mohapatra J. K., Hemadri D., Rao T. V., Sreenivasa B. P., Subramaniam S., Sanyal A., Periyasamy T. R., Singh N. K., Pattnaik B., Venkataramanan R. Assessment of suitability of two serotype A candidate vaccine strains for inclusion in FMD vaccine in India. Vet. Microbiol. 2008;131:65–72. doi: 10.1016/j.vetmic.2008.02.020. [DOI] [PubMed] [Google Scholar]
  31. Nagendrakumar S. B., Mythili T., Maroudam V., Madhanmohan M., Thiagarajan D., Srinivasan V. A. Comparison of different methods of routine typing of Indian isolates of foot-and-mouth disease virus. Acta Virol. 2006;50:279–280. [PubMed] [Google Scholar]
  32. Page R. D. M. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 1996;12:357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  33. Pond S. L., Frost S. D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005;21:2531–2533. doi: 10.1093/bioinformatics/bti320. [DOI] [PubMed] [Google Scholar]
  34. Roberts P. J., Belsham G. J. Identification of critical amino acids within the foot-and-mouth disease virus leader protein a cysteine protease. Virology. 1995;213:140–146. doi: 10.1006/viro.1995.1554. [DOI] [PubMed] [Google Scholar]
  35. Sabarinath G. P. Comparison of nucleotide sequence of structural protein encoding (P1) region of foot-and-mouth disease virus serotype O isolates. Izatnagar, India: Indian Veterinary Research Institute; 2001. [Google Scholar]
  36. Saiz J. C., Gonzalez M. J., Borca M. V., Sobrino F., Moore D. M. Identification of neutralizing antigenic sites on VP1 and VP2 of type A5 foot-and-mouth disease virus defined by neutralization-resistant variants. J. Virol. 1991;65:2518–2524. doi: 10.1128/jvi.65.5.2518-2524.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Samuel A. R., Knowles N. J. Foot-and-mouth disease type O viruses exhibit genetically and geographically distinct evolutionary lineages (topotypes) J. Gen. Virol. 2001;82:609–621. doi: 10.1099/0022-1317-82-3-609. [DOI] [PubMed] [Google Scholar]
  38. Santti J., Hyypia T., Kinnunen L., Salminen M. Evidence of recombination among enteroviruses. J. Virol. 1996;73:8741–8749. doi: 10.1128/jvi.73.10.8741-8749.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sobrino F., Sa’iz M., Jiménez-Clavero M. A., Nún∼ez J. I., Rosas M. F., Baranowski E., Ley V. Foot-and-mouth disease virus: a long known virus but a current threat. Vet. Res. 2001;32:1–30. doi: 10.1051/vetres:2001106. [DOI] [PubMed] [Google Scholar]
  40. Suzuki Y., Gojobori T. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 1999;16:1315–1328. doi: 10.1093/oxfordjournals.molbev.a026042. [DOI] [PubMed] [Google Scholar]
  41. Thomas A. A., Woortmeijer R. J., Puijk W., Barteling S. J. Antigenic sites on foot-and-mouth disease virus type A10. J. Virol. 1988;62:2782–2789. doi: 10.1128/jvi.62.8.2782-2789.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W 18x: improving the sensitivity of progressive multiple sequence alignment through sequence weighting positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tosh C., Hemadri D., Sanyal A., Bandyopadhyay S. K. Genetic and antigenic analysis of two recently circulating genotypes of type A foot-and-mouth disease virus in India: evidence for positive selection in the capsid-encoding genes. Arch. Virol. 2003;148:853–869. doi: 10.1007/s00705-002-0968-2. [DOI] [PubMed] [Google Scholar]
  44. Tosh C., Sanyal A., Hemadri D., Venkataramanan R. Phylogenetic analysis of serotype A foot-and-mouth disease virus isolated in India between 1977 and 2000. Arch. Virol. 2002;147:493–513. doi: 10.1007/s007050200002. [DOI] [PubMed] [Google Scholar]
  45. Tosh C., Hemadri D., Sanyal A. Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. J. Gen. Virol. 2002;83:2455–2460. doi: 10.1099/0022-1317-83-10-2455. [DOI] [PubMed] [Google Scholar]
  46. Tosh C., Mittal M., Sanyal A., Hemadri D., Bandyopadhyay S. K. Molecular phylogeny of leader proteinase gene of type A of foot-and-mouth disease virus from India. Arch. Virol. 2004;149:523–536. doi: 10.1007/s00705-003-0224-4. [DOI] [PubMed] [Google Scholar]
  47. Vangrysperre W., de Clercq K. Rapid and sensitive polymerase chain reaction based detection and typing of foot-and-mouth disease virus in clinical samples and cell culture isolates combined with a simultaneous differentiation with other genomically and/or symptomatically related viruses. Arch. Virol. 1996;141:331–344. doi: 10.1007/BF01718403. [DOI] [PubMed] [Google Scholar]
  48. Vosloo W., Knowles N. J., Thomson G. R. Genetic relationships between southern African SAT-2 isolates of foot-and-mouth disease virus. Epidemiol. Infect. 1992;109:547–558. doi: 10.1017/S0950268800050536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Weddell G. N., Yansura D. G., Dowbenko D. J., Hoatlin M. E., Grubman M. J., Moore D. M., Kleid D. G. Sequence variation in the gene for the immunogenic capsid protein VP1 of foot-and-mouth disease virus type A. Proc. Natl. Acad. Sci. USA. 1985;82:2618–2622. doi: 10.1073/pnas.82.9.2618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wilson V., Taylor P., Desselberger U. Crossover regions in foot-and-mouth disease virus (FMDV) recombinants correspond to regions of high local secondary structure. Arch. Virol. 1988;102:131–139. doi: 10.1007/BF01315570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. WRL-FMD Network Report 2006 Annual OIE/FAO FMD Reference Laboratory Network Report;http://www.wrlfmdorg/fmd_network/FMD%20Network%20Report%202006pdf

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