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. 2007 Mar 26;152(7):1259. doi: 10.1007/s00705-007-0959-4

Full-length genome sequence and genetic relationship of two paramyxoviruses isolated from bat and pigs in the Americas

L-F Wang 1, E Hansson 1, M Yu 1, K B Chua 2, N Mathe 1, G Crameri 1, B K Rima 3, J Moreno-López 4, B T Eaton 1
PMCID: PMC7086891  PMID: 17385069

Summary

Mapuera virus (MPRV) was isolated from a fruit bat in Brazil in 1979, but its host range and disease-causing potential are unknown. Porcine rubulavirus (PoRV) was identified as the aetiological agent of disease outbreaks in pigs in Mexico during early 1980s, but the origin of PoRV remains elusive. In this study, the completed genome sequence of MPRV was determined, and the complete genome sequence of PoRV was assembled from previously published protein-coding genes and the non-coding genome regions determined from this study. Comparison of sequence and genome organization indicated that PoRV is more closely related to MPRV than to any other members of the genus Rubulavirus. In the P gene coding region of both viruses, there is an ORF located at the 5′ end of the P gene overlapping with the P protein coding region, similar to the C protein ORF present in most viruses of the subfamily Paramyxovirinae, but absent in other known rubulaviruses. Based on these findings, we hypothesise that PoRV may also originate from bats, and spillover events from bats to pigs, either directly or via an intermediate host, were responsible for the sporadic disease outbreaks observed in Mexico.

Keywords: Newcastle Disease Virus, Emerg Infect, Nipah Virus, Hendra Virus, Length Genome Sequence

References

  1. Berg M, Bergvall AC, Svenda M, Sundqvist A, Moreno-López J, Linné T. Analysis of the fusion protein gene of the porcine rubulavirus LPMV: comparative analysis of paramyxovirus F proteins. Virus Genes. 1997;14:55–61. doi: 10.1023/A:1007987407250. [DOI] [PubMed] [Google Scholar]
  2. Berg M, Hjertner B, Moreno-López J, Linné T. The P gene of the porcine paramyxovirus LPMV encodes three possible polypeptides P, V and C: the P protein mRNA is edited. J Gen Virol. 1992;73:1195–1200. doi: 10.1099/0022-1317-73-5-1195. [DOI] [PubMed] [Google Scholar]
  3. Berg M, Sundqvist A, Moreno-López J, Linné T. Identification of the porcine paramyxovirus LPMV matrix protein gene: comparative sequence analysis with other paramyxoviruses. J Gen Virol. 1991;72:1045–1050. doi: 10.1099/0022-1317-72-5-1045. [DOI] [PubMed] [Google Scholar]
  4. Bowden TR, Boyle DB. Completion of the full-length genome sequence of Menangle virus: characterisation of the polymerase gene and genomic 5′ trailer region. Arch Virol. 2005;150:2125–2137. doi: 10.1007/s00705-005-0552-7. [DOI] [PubMed] [Google Scholar]
  5. Bowden TR, Westenberg M, Wang L-F, Eaton BT, Boyle DB. Molecular characterization of Menangle virus, a novel paramyxovirus which infects pigs, fruit bats, and humans. Virology. 2001;283:358–373. doi: 10.1006/viro.2001.0893. [DOI] [PubMed] [Google Scholar]
  6. Bossart KN, Wang LF, Eaton BT, Broder CC. Functional expression and membrane fusion tropism of the envelope glycoproteins of Hendra virus. Virology. 2001;10:121–135. doi: 10.1006/viro.2001.1158. [DOI] [PubMed] [Google Scholar]
  7. Chadha MS, Comer JA, Lowe L, Rota PA, Rollin PE, Bellini WJ, Ksiazek TG, Mishra A. Nipah virus-associated encephalitis outbreak, Siliguri, India. Emerg Infect Dis. 2006;12:235–240. doi: 10.3201/eid1202.051247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chant K, Chan R, Smith M, Dwyer DE, Kirkland P. Probable human infection with a newly described virus in the family Paramyxoviridae. Emerg Infect Dis. 1998;4:273–275. doi: 10.3201/eid0402.980215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chua KB, Bellini WJ, Rota PA, Harcourt BA, amin A, Lam SK, Ksiazek TR, Rollin PE, Zaki SR, Shieh WJ, Goldsmith CS, Gubler DJ, Roehrig JT, Eaton B, Gould AR, Olson J, Field H, Daniels P, Ling AE, Peters CJ, Anderson LJ, Mahy WJ. Nipah virus: a recently emergent deadly paramyxovirus. Science. 2000;288:1432–1435. doi: 10.1126/science.288.5470.1432. [DOI] [PubMed] [Google Scholar]
  10. Chua KB, Wang L-F, Lam SK, Crameri G, Yu M, Wise T, Boyle D, Hyatt AD, Eaton BT. Tioman virus, a novel paramyxovirus isolated from fruit bats in Malaysia. Virology. 2001;283:215–229. doi: 10.1006/viro.2000.0882. [DOI] [PubMed] [Google Scholar]
  11. Chua KB, Wang L-F, Lam SK, Eaton BT. Full length genome sequence of Tioman virus, a novel paramyxovirus in the genus Rubulavirus isolated from fruit bats in Malaysia. Arch Virol. 2002;147:1323–1348. doi: 10.1007/s00705-002-0815-5. [DOI] [PubMed] [Google Scholar]
  12. Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P. Nipah virus: impact, origins, and causes of emergence. Curr Infect Dis Rep. 2006;8:59–65. doi: 10.1007/s11908-006-0036-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Field HE, Breed AC, Shield J, Hedlefs RM, Pittard K, Pott B, Summers PM (2007) Epidemiological perspectives on Hendra virus infection in horses and flying foxes. Aust Vet J (in press) [DOI] [PubMed]
  14. Henderson GW, Laird C, Dermott E, Rima BK. Characterization of Mapuera virus: structure, proteins and nucleotide sequence of the gene encoding the nucleocapsid protein. J Gen Virol. 1995;76:2509–2518. doi: 10.1099/0022-1317-76-10-2509. [DOI] [PubMed] [Google Scholar]
  15. Hollinger FB, Pavri KM. Bat parainfluenza virus. Immunological, chemical, and physical properties. Am J Trop Med Hyg. 1971;20:131–138. [PubMed] [Google Scholar]
  16. Hosaka M, Nagahama M, Kim WS, Watanabe T, Hatsuzawa K, Ikemizu J, Murakami K, Nakayama K. Arg-X-Lys/Arg-Arg motif as a signal for precursor cleavage catalyzed by furin within the constitutive secretory pathway. J Biol Chem. 1991;266:12127–12130. [PubMed] [Google Scholar]
  17. Hsu VP, Hossain MJ, Parashar UD, Ali MM, Ksiazek TG, Kuzmin I, Niezgoda M, Rupprecht C, Bresee J, Breiman RF. Nipah virus encephalitis reemergence, Bangladesh. Emerg Infect Dis. 2004;10:2082–2087. doi: 10.3201/eid1012.040701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jack PJM, Boyle DB, Eaton BT, Wang L-F. The complete genome sequence of J virus reveals a unique genome structure in the family Paramyxoviridae. J Virol. 2005;79:10690–10700. doi: 10.1128/JVI.79.16.10690-10700.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Karabatsos N. International Catalogue of Arboviruses. 3. San Antonio, Texas: American Society of Tropical Medicine and Hygiene; 1985. [Google Scholar]
  20. Kolakofsky D, Pelet T, Garcin D, Hausmann S, Curran J, Roux L. Paramyxovirus RNA synthesis and the requirement for hexamer genome length: the rule of six revisited. J Virol. 1998;72:891–899. doi: 10.1128/jvi.72.2.891-899.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kumar S, Tamura K, Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 2004;5:150–163. doi: 10.1093/bib/5.2.150. [DOI] [PubMed] [Google Scholar]
  22. Lamb RA, Collins PL, Kolakofsky D, Melero JA, Nagai Y, Oldstone MBA, Pringle CR, Rima BK (2005) Family Paramyxoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy: 8th Report of the International Comittee on Taxonomy of Viruses. Elsevier Acedemic Press, San Diego, pp 655–668
  23. Lamb RA, Kolakofsky D (2001) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Lippincott Williams & Wilkins, Philadelphia, pp 305–1340
  24. Langedijk JP, Daus FJ, van Oirschot JT. Sequence and structure alignment of Paramyxoviridae attachment proteins and discovery of enzymatic activity for a morbillivirus hemagglutinin. J Virol. 1997;71:6155–6167. doi: 10.1128/jvi.71.8.6155-6167.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA. 2005;102:14040–14045. doi: 10.1073/pnas.0506735102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Delicat A, Paweska JT, Gonzalez JP, Swanepoel R. Fruit bats as reservoirs of Ebola virus. Nature. 2005;438:575–576. doi: 10.1038/438575a. [DOI] [PubMed] [Google Scholar]
  27. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang L-F. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  28. Linné T, Berg M, Bergvall AC, Hjertner B, Moreno-López J. The molecular biology of the porcine paramyxovirus LPMV. Vet Microbiol. 1992;33:263–273. doi: 10.1016/0378-1135(92)90054-W. [DOI] [PubMed] [Google Scholar]
  29. Miller PJ, Boyle DB, Eaton BT, Wang L-F. Full-length genome sequence of Mossman virus, a novel paramyxovirus isolated from rodents in Australia. Virology. 2003;317:330–344. doi: 10.1016/j.virol.2003.08.013. [DOI] [PubMed] [Google Scholar]
  30. Mirza AM, Deng R, Iorio RM. Site-directed mutagenesis of a conserved hexapeptide in the paramyxovirus hemagglutinin-neuraminidase glycoprotein: effects on antigenic structure and function. J Virol. 1994;68:5093–5099. doi: 10.1128/jvi.68.8.5093-5099.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Moreno-López J, Correa-Giron P, Martinez A, Ericsson A. Characterization of a paramyxovirus isolated from the brain of a piglet in Mexico. Arch Virol. 1986;91:221–231. doi: 10.1007/BF01314282. [DOI] [PubMed] [Google Scholar]
  32. Murray K, Selleck P, Hooper P, Hyatt A, Gould A, Gleeson L, Westbury H, Hiley L, Selvey L, Rodwell B, Ketterer P. A morbillivirus that caused fatal disease in horses and humans. Science. 1995;268:94–97. doi: 10.1126/science.7701348. [DOI] [PubMed] [Google Scholar]
  33. Pavri KM, Singh KR, Hollinger FB. Isolation of a new parainfluenza virus from a frugivorous bat, Rousettus leschenaulti, collected at Poona, India. Am J Trop Med Hyg. 1971;20:125–130. doi: 10.4269/ajtmh.1971.20.125. [DOI] [PubMed] [Google Scholar]
  34. Philbey AW, Kirkland PD, Ross AD, Davis RJ, Gleeson AB, Love RJ, Daniels PW, Gould AR, Hyatt AD. An apparently new virus (family Paramyxoviridae) infectious for pigs, humans, and fruit bats. Emerg Infect Dis. 1998;4:269–271. doi: 10.3201/eid0402.980214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Poch O, Blumberg BM, Bougueleret L, Tordo N. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol. 1990;71:1153–1162. doi: 10.1099/0022-1317-71-5-1153. [DOI] [PubMed] [Google Scholar]
  36. Reynes JM, Counor D, Ong S, Faure C, Seng V, Molia S, Walston J, Georges-Courbot MC, Deubel V, Sarthou JL. Nipah virus in Lyle’s flying foxes, Cambodia. Emerg Infect Dis. 2005;11(10):1042–1047. doi: 10.3201/eid1107.041350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Salas-Rojas M, Sánchez-Hernández C, Romero-Almaraz MDL, Schnell GD, Schmid RK, Aguilar-Setién A. Prevalence of rabies and LPM paramyxovirus antibody in non-hematophagous bats captured in the Central Pacific coast of Mexico. Trans R Soc Trop Med Hyg. 2004;98:577–584. doi: 10.1016/j.trstmh.2003.10.019. [DOI] [PubMed] [Google Scholar]
  38. Sendow I, Field HE, Curran J, Darminto, Morrissy C, Meehan G, Buick T, Daniels P. Henipavirus in Pteropus vampyrus bats, Indonesia. Emerg Infect Dis. 2006;12:711–712. doi: 10.3201/eid1204.051181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stephano HA, Gay GM, Ramírez TC. Encephalomyelitis, reproductive failure and corneal opacity (blue eye) in pigs, associated with a paramyxovirus infection. Vet Rec. 1998;122:6–10. doi: 10.1136/vr.122.1.6. [DOI] [PubMed] [Google Scholar]
  40. Sundqvist A, Berg M, Hernandez-Jauregui P, Linné T, Moreno-López J. The structural proteins of a porcine paramyxovirus (LPMV) J Gen Virol. 1990;71:609–613. doi: 10.1099/0022-1317-71-3-609. [DOI] [PubMed] [Google Scholar]
  41. Sundqvist A, Berg M, Moreno-López J, Linné T. The haemagglutinin-neuraminidase glycoprotein of the porcine paramyxovirus LPMV: comparison with other paramyxoviruses revealed the closest relationship to simian virus 5 and mumps virus. Arch Virol. 1992;122:331–340. doi: 10.1007/BF01317194. [DOI] [PubMed] [Google Scholar]
  42. Svenda M, Berg M, Moreno-López J, Linné T. Analysis of the large (L) protein gene of the porcine rubulavirus LPMV: identification of possible functional domains. Virus Res. 1997;48:57–70. doi: 10.1016/S0168-1702(96)01426-8. [DOI] [PubMed] [Google Scholar]
  43. Tillett D, Burns BP, Neilan BA. Optimized rapid amplification of cDNA (RACE) for mapping bacterial mRNA transcripts. Biotechniques. 2000;28:448–456. doi: 10.2144/00283st01. [DOI] [PubMed] [Google Scholar]
  44. Tsao K-L, DeBarbieri B, Michel H, Waugh DS. A versatile plasmid expression vector for the production of biotinylated proteins by site-specific, enzymatic modification in Escherichia coli. Gene. 1996;169:59–64. doi: 10.1016/0378-1119(95)00762-8. [DOI] [PubMed] [Google Scholar]
  45. Wacharapluesadee S, Lumlertdacha B, Boongird K, Wanghongsa S, Chanhome L, Rollin P, Stockton P, Rupprecht CE, Ksiazek TG, Hemachudha T. Bat Nipah virus, Thailand. Emerg Infect Dis. 2005;11:1949–1951. doi: 10.3201/eid1112.050613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wang L-F, Chua KB, Yu M, Eaton BT. Genome diversity of emerging paramyxoviruses. Curr Genom. 2003;4:263–273. doi: 10.2174/1389202033490385. [DOI] [Google Scholar]
  47. Wang L-F, Eaton BT. Emerging paramyxoviruses. Infect Dis Rev. 2001;3:52–69. [Google Scholar]
  48. Wang L-F, Michalski WP, Yu M, Pritchard LI, Crameri G, Shiell B, Eaton BT. A novel P/V/C gene in a new member of the Paramyxoviridae family, which causes lethal infection in humans, horses, and other animals. J Virol. 1998;72:1482–1490. doi: 10.1128/jvi.72.2.1482-1490.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wang L-F, Yu M, White JR, Eaton BT. BTag: a novel six-residue epitope tag for surveillance and purification of recombinant proteins. Gene. 1996;169:53–58. doi: 10.1016/0378-1119(95)00795-4. [DOI] [PubMed] [Google Scholar]
  50. Zeller HG, Karabatsos N, Calisher CH, Digoutte JP, Murphy FA, Shope RE. Electron microscopy and antigenic studies of uncharacterized viruses. I. Evidence suggesting the placement of viruses in families Arenaviridae, Paramyxoviridae, or Poxviridae. Arch Virol. 1989;108:191–209. doi: 10.1007/BF01310934. [DOI] [PubMed] [Google Scholar]

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