Molecular Comparisons of Full Length Metapneumovirus (MPV) Genomes, Including Newly Determined French AMPV-C and –D Isolates, Further Supports Possible Subclassification within the MPV Genus
Four avian metapneumovirus (AMPV) subgroups (A–D) have been reported previously based on genetic and antigenic differences. However, until now full length sequences of the only known isolates of European subgroup C and subgroup D viruses (duck and turkey origin, respectively) have been unavailable. These full length sequences were determined and compared with other full length AMPV and human metapneumoviruses (HMPV) sequences reported previously, using phylogenetics, comparisons of nucleic and amino acid sequences and study of codon usage bias. Results confirmed that subgroup C viruses were more closely related to HMPV than they were to the other AMPV subgroups in the study. This was consistent with previous findings using partial genome sequences. Closer relationships between AMPV-A, B and D were also evident throughout the majority of results. Three metapneumovirus “clusters” HMPV, AMPV-C and AMPV-A, B and D were further supported by codon bias and phylogenetics. The data presented here together with those of previous studies describing antigenic relationships also between AMPV-A, B and D and between AMPV-C and HMPV may call for a subclassification of metapneumoviruses similar to that used for avian paramyxoviruses, grouping AMPV-A, B and D as type I metapneumoviruses and AMPV-C and HMPV as type II.
References
[1]
Buys SB, Du Prees JH (1980) A preliminary report on the isolation of a virus causing sinusitis in turkeys in South Africa and attempts to attenuate the virus. Turkeys 28: 36.
[2]
Giraud P, Bennejean G, Guittet M, Toquin D (1986) Turkey rhinotracheitis in France: preliminary investigations on a ciliostatic virus. Vet Rec 119: 606–607.
[3]
McDougall JS, Cook JK (1986) Turkey rhinotracheitis: preliminary investigations. Vet Rec 118: 206–207. doi: 10.1136/vr.118.8.206
[4]
Wilding GP, Baxter-Jones C, Grant M (1986) Ciliostatic agent found in rhinotracheitis. Vet Rec 118: 735. doi: 10.1136/vr.118.26.735-b
[5]
Wyeth PJ, Gough RE, Chettle N, Eddy R (1986) Preliminary observations on a virus associated with turkey rhinotracheitis. Vet Rec 119: 139. doi: 10.1136/vr.119.6.139-a
[6]
Cook JK (2000) Avian pneumovirus infections of turkeys and chickens. Vet J 160: 118–125. doi: 10.1053/tvjl.2000.0486
[7]
van den Hoogen BG, de Jong JC, Groen J, Kuiken T, de Groot R, et al. (2001) A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med 7: 719–724. doi: 10.1038/89098
[8]
de Graaf M, Osterhaus AD, Fouchier RA, Holmes EC (2008) Evolutionary dynamics of human and avian metapneumoviruses. J Gen Virol 89: 2933–2942. doi: 10.1099/vir.0.2008/006957-0
[9]
Crowe JE Jr (2004) Human metapneumovirus as a major cause of human respiratory tract disease. Pediatr Infect Dis J 23: S215–221. doi: 10.1097/01.inf.0000144668.81573.6d
[10]
Falsey AR, Erdman D, Anderson LJ, Walsh EE (2003) Human metapneumovirus infections in young and elderly adults. J Infect Dis 187: 785–790. doi: 10.1086/367901
[11]
Williams JV, Wang CK, Yang CF, Tollefson SJ, House FS, et al. (2006) The role of human metapneumovirus in upper respiratory tract infections in children: a 20-year experience. J Infect Dis 193: 387–395. doi: 10.1086/499274
Ling R, Easton AJ, Pringle CR (1992) Sequence analysis of the 22K, SH and G genes of turkey rhinotracheitis virus and their intergenic regions reveals a gene order different from that of other pneumoviruses. J Gen Virol 73 (Pt 7): 1709–1715. doi: 10.1099/0022-1317-73-7-1709
[14]
Randhawa JS, Marriott AC, Pringle CR, Easton AJ (1997) Rescue of synthetic minireplicons establishes the absence of the NS1 and NS2 genes from avian pneumovirus. J Virol 71: 9849–9854.
[15]
Govindarajan D, Samal SK (2004) Sequence analysis of the large polymerase (L) protein of the US strain of avian metapneumovirus indicates a close resemblance to that of the human metapneumovirus. Virus Res 105: 59–66. doi: 10.1016/j.virusres.2004.04.014
[16]
Govindarajan D, Samal SK (2005) Analysis of the complete genome sequence of avian metapneumovirus subgroup C indicates that it possesses the longest genome among metapneumoviruses. Virus Genes 30: 331–333. doi: 10.1007/s11262-005-6775-6
[17]
Govindarajan D, Yunus AS, Samal SK (2004) Complete sequence of the G glycoprotein gene of avian metapneumovirus subgroup C and identification of a divergent domain in the predicted protein. J Gen Virol 85: 3671–3675. doi: 10.1099/vir.0.80400-0
[18]
Toquin D, de Boisseson C, Beven V, Senne DA, Eterradossi N (2003) Subgroup C avian metapneumovirus (MPV) and the recently isolated human MPV exhibit a common organization but have extensive sequence divergence in their putative SH and G genes. J Gen Virol 84: 2169–2178. doi: 10.1099/vir.0.19043-0
[19]
Yunus AS, Govindarajan D, Huang Z, Samal SK (2003) Deduced amino acid sequence of the small hydrophobic protein of US avian pneumovirus has greater identity with that of human metapneumovirus than those of non-US avian pneumoviruses. Virus Res 93: 91–97. doi: 10.1016/s0168-1702(03)00074-1
[20]
Toquin D, Bayon-Auboyer MH, Eterradossi N, Jestin V (1999) Isolation of a pneumovirus from a Muscovy duck. Vet Rec: 23, 145, 680.
[21]
Bennett RS, Nezworski J, Velayudhan BT, Nagaraja KV, Zeman DH, et al. (2004) Evidence of avian pneumovirus spread beyond Minnesota among wild and domestic birds in central North America. Avian Dis 48: 902–908. doi: 10.1637/7208-051804r
[22]
Cook JK, Huggins MB, Orbell SJ, Senne DA (1999) Preliminary antigenic characterization of an avian pneumovirus isolated from commercial turkeys in Colorado, USA. Avian Pathology 28: 607–617. doi: 10.1080/03079459994407
[23]
Shin HJ, Njenga MK, McComb B, Halvorson DA, Nagaraja KV (2000) Avian pneumovirus (APV) RNA from wild and sentinel birds in the United States has genetic homology with RNA from APV isolates from domestic turkeys. J Clin Microbiol 38: 4282–4284.
[24]
Toquin D, Guionie O, Jestin V, Zwingelstein F, Allee C, et al. (2006) European and American subgroup C isolates of avian metapneumovirus belong to different genetic lineages. Virus Genes 32: 97–103. doi: 10.1007/s11262-005-5850-3
[25]
Turpin EA, Stallknecht DE, Slemons RD, Zsak L, Swayne DE (2008) Evidence of avian metapneumovirus subtype C infection of wild birds in Georgia, South Carolina, Arkansas and Ohio, USA. Avian Pathol 37: 343–351. doi: 10.1080/03079450802068566
[26]
Wei L, Zhu S, Yan X, Wang J, Zhang C, et al. (2013) Avian metapneumovirus subgroup C infection in chickens, China. Emerg Infect Dis 19: 1092–1094. doi: 10.3201/eid1907.121126
[27]
Catelli E, Cecchinato M, Savage CE, Jones RC, Naylor CJ (2006) Demonstration of loss of attenuation and extended field persistence of a live avian metapneumovirus vaccine. Vaccine 24: 6476–6482. doi: 10.1016/j.vaccine.2006.06.076
[28]
Lupini C, Cecchinato M, Ricchizzi E, Naylor CJ, Catelli E (2011) A turkey rhinotracheitis outbreak caused by the environmental spread of a vaccine-derived avian metapneumovirus. Avian Pathol 40: 525–530. doi: 10.1080/03079457.2011.607428
[29]
Naylor CJ, Brown PA, Edworthy N, Ling R, Jones RC, et al. (2004) Development of a reverse-genetics system for Avian pneumovirus demonstrates that the small hydrophobic (SH) and attachment (G) genes are not essential for virus viability. J Gen Virol 85: 3219–3227. doi: 10.1099/vir.0.80229-0
[30]
Sugiyama M, Ito H, Hata Y, Ono E, Ito T (2010) Complete nucleotide sequences of avian metapneumovirus subtype B genome. Virus Genes 41: 389–395. doi: 10.1007/s11262-010-0518-z
[31]
Lwamba HC, Alvarez R, Wise MG, Yu Q, Halvorson D, et al. (2005) Comparison of the full-length genome sequence of avian metapneumovirus subtype C with other paramyxoviruses. Virus Res 107: 83–92. doi: 10.1016/j.virusres.2004.07.002
[32]
Bennett RS, LaRue R, Shaw D, Yu Q, Nagaraja KV, et al. (2005) A wild goose metapneumovirus containing a large attachment glycoprotein is avirulent but immunoprotective in domestic turkeys. J Virol 79: 14834–14842. doi: 10.1128/jvi.79.23.14834-14842.2005
[33]
Lee E, Song MS, Shin JY, Lee YM, Kim CJ, et al. (2007) Genetic characterization of avian metapneumovirus subtype C isolated from pheasants in a live bird market. Virus Res 128: 18–25. doi: 10.1016/j.virusres.2007.03.029
[34]
Brown PA, Briand FX, Guionie O, Lemaitre E, Courtillon C, et al. (2013) An alternative method to determine the 5′ extremities of non-segmented, negative sense RNA viral genomes using positive replication intermediate 3′ tailing: Application to two members of the Paramyxoviridae family. J Virol Methods 193: 121–127. doi: 10.1016/j.jviromet.2013.05.007
[35]
Bayon-Auboyer MH, Arnauld C, Toquin D, Eterradossi N (2000) Nucleotide sequences of the F, L and G protein genes of two non-A/non-B avian pneumoviruses (APV) reveal a novel APV subgroup. J Gen Virol 81: 2723–2733.
[36]
Bayon-Auboyer MH, Jestin V, Toquin D, Cherbonnel M, Eterradossi N (1999) Comparison of F-, G- and N-based RT-PCR protocols with conventional virological procedures for the detection and typing of turkey rhinotracheitis virus. Arch Virol 144: 1091–1109. doi: 10.1007/s007050050572
[37]
Toquin D, Guionie O, Allee C, Morin Y, Le CoQ L, et al.. (2006) Compared suceptibility of SPF ducklings and SPF turkeys to the infection by avian metapneumoviruses belonging to the four subgroups. In: Heffels-Redman U, Kaleta, E. F, editor; University of Giessen Rauischholzhausen, Germany. VVB Laufersweiler Verlag. pp. 70–76.
[38]
Reed LJ, Meunch H (1938) A simple method of estimating fifty percent end points. American journal of hygiene 27: 493–497.
[39]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. doi: 10.1093/molbev/msr121
[40]
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. doi: 10.1016/s0022-2836(05)80360-2
[41]
Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87: 23–29. doi: 10.1016/0378-1119(90)90491-9
[42]
Zhang Z, Dai W, Dai D (2013) Synonymous codon usage in TTSuV2: analysis and comparison with TTSuV1. PLoS One 8: e81469. doi: 10.1371/journal.pone.0081469
[43]
Zhong Q, Xu W, Wu Y, Xu H (2012) Patterns of synonymous codon usage on human metapneumovirus and its influencing factors. J Biomed Biotechnol 2012: 460837. doi: 10.1155/2012/460837
[44]
Calain P, Roux L (1993) The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67: 4822–4830.
Pham QN, Biacchesi S, Skiadopoulos MH, Murphy BR, Collins PL, et al. (2005) Chimeric recombinant human metapneumoviruses with the nucleoprotein or phosphoprotein open reading frame replaced by that of avian metapneumovirus exhibit improved growth in vitro and attenuation in vivo. J Virol 79: 15114–15122. doi: 10.1128/jvi.79.24.15114-15122.2005
[49]
de Graaf M, Herfst S, Schrauwen EJ, Choi Y, van den Hoogen BG, et al. (2008) Specificity and functional interaction of the polymerase complex proteins of human and avian metapneumoviruses. J Gen Virol 89: 975–983. doi: 10.1099/vir.0.83537-0
[50]
van den Hoogen BG, Bestebroer TM, Osterhaus AD, Fouchier RA (2002) Analysis of the genomic sequence of a human metapneumovirus. Virology 295: 119–132. doi: 10.1006/viro.2001.1355
[51]
Ling R, Davis PJ, Yu Q, Wood CM, Pringle CR, et al. (1995) Sequence and in vitro expression of the phosphoprotein gene of avian pneumovirus. Virus Res 36: 247–257. doi: 10.1016/0168-1702(95)00008-e
[52]
Leyrat C, Renner M, Harlos K, Grimes JM (2013) Solution and crystallographic structures of the central region of the phosphoprotein from human metapneumovirus. PLoS One 8: e80371. doi: 10.1371/journal.pone.0080371
[53]
Loo LH, Jumat MR, Fu Y, Ayi TC, Wong PS, et al. (2013) Evidence for the interaction of the human metapneumovirus G and F proteins during virus-like particle formation. Virol J 10: 294. doi: 10.1186/1743-422x-10-294
[54]
Takimoto T, Portner A (2004) Molecular mechanism of paramyxovirus budding. Virus Res 106: 133–145. doi: 10.1016/j.virusres.2004.08.010
[55]
Easton AJ, Chambers P (1997) Nucleotide sequence of the genes encoding the matrix and small hydrophobic proteins of pneumonia virus of mice. Virus Res 48: 27–33. doi: 10.1016/s0168-1702(96)01430-x
[56]
Lamb RA, Paterson RG, Jardetzky TS (2006) Paramyxovirus membrane fusion: lessons from the F and HN atomic structures. Virology 344: 30–37. doi: 10.1016/j.virol.2005.09.007
[57]
de Graaf M, Schrauwen EJ, Herfst S, van Amerongen G, Osterhaus AD, et al.. (2009) Fusion protein is the main determinant of metapneumovirus host tropism. J Gen Virol.
[58]
Schlender J, Zimmer G, Herrler G, Conzelmann KK (2003) Respiratory syncytial virus (RSV) fusion protein subunit F2, not attachment protein G, determines the specificity of RSV infection. J Virol 77: 4609–4616. doi: 10.1128/jvi.77.8.4609-4616.2003
[59]
Molloy SS, Bresnahan PA, Leppla SH, Klimpel KR, Thomas G (1992) Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J Biol Chem 267: 16396–16402.
[60]
Naylor CJ, Britton P, Cavanagh D (1998) The ectodomains but not the transmembrane domains of the fusion proteins of subtypes A and B avian pneumovirus are conserved to a similar extent as those of human respiratory syncytial virus. J Gen Virol 79: 1393–1398.
[61]
Herfst S, Mas V, Ver LS, Wierda RJ, Osterhaus AD, et al. (2008) Low-pH-induced membrane fusion mediated by human metapneumovirus F protein is a rare, strain-dependent phenomenon. J Virol 82: 8891–8895. doi: 10.1128/jvi.00472-08
[62]
Mas V, Herfst S, Osterhaus AD, Fouchier RA, Melero JA (2011) Residues of the human metapneumovirus fusion (F) protein critical for its strain-related fusion phenotype: implications for the virus replication cycle. J Virol 85: 12650–12661. doi: 10.1128/jvi.05485-11
[63]
Naylor CJ, Lupini C, Brown PA (2010) Charged amino acids in the AMPV fusion protein have more influence on induced protection than deletion of the SH or G genes. Vaccine 28: 6800–6807. doi: 10.1016/j.vaccine.2010.07.015
[64]
Wei Y, Zhang Y, Cai H, Mirza AM, Iorio RM, et al.. (2014) Roles of the putative integrin-binding motif of the human metapneumovirus fusion (F) protein in cell-cell fusion, viral infectivity, and pathogenesis. J Virol.
[65]
Dolganiuc V, McGinnes L, Luna EJ, Morrison TG (2003) Role of the cytoplasmic domain of the Newcastle disease virus fusion protein in association with lipid rafts. J Virol 77: 12968–12979. doi: 10.1128/jvi.77.24.12968-12979.2003
[66]
Brown PA, Bonci M, Ricchizzi E, Jones RC, Naylor CJ (2009) Identification of two regions within the subtype A avian metapneumovirus fusion protein (amino acids 211–310 and 336–479) recognized by neutralizing antibodies. Virus Res 146: 13–18. doi: 10.1016/j.virusres.2009.08.009
[67]
Lounsbach GR, Bourgeois C, West WH, Robinson JW, Carter MJ, et al. (1993) Binding of neutralizing monoclonal antibodies to regions of the fusion protein of respiratory syncytial virus expressed in Escherichia coli. J Gen Virol 74 (Pt 12): 2559–2565. doi: 10.1099/0022-1317-74-12-2559
[68]
Ulbrandt ND, Ji H, Patel NK, Barnes AS, Wilson S, et al. (2008) Identification of antibody neutralization epitopes on the fusion protein of human metapneumovirus. J Gen Virol 89: 3113–3118. doi: 10.1099/vir.0.2008/005199-0
[69]
Werle B, Bourgeois C, Alexandre A, Massonneau V, Pothier P (1998) Immune response to baculovirus expressed protein fragment amino acids 190–289 of respiratory syncytial virus (RSV) fusion protein. Vaccine 16: 1127–1130. doi: 10.1016/s0264-410x(98)80109-6
[70]
Toquin D, Bayon-Auboyer MH, Senne DA, Eterradossi N (2000) Lack of antigenic relationship between French and recent North American non-A/non-B turkey rhinotracheitis viruses. Avian Dis 44: 977–982. doi: 10.2307/1593075
[71]
Clubbe J, Naylor CJ (2011) Avian metapneumovirus M2:2 protein inhibits replication in Vero cells: modification facilitates live vaccine development. Vaccine 29: 9493–9498. doi: 10.1016/j.vaccine.2011.10.024
[72]
Govindarajan D, Buchholz UJ, Samal SK (2006) Recovery of avian metapneumovirus subgroup C from cDNA: cross-recognition of avian and human metapneumovirus support proteins. J Virol 80: 5790–5797. doi: 10.1128/jvi.00138-06
[73]
Esperante SA, Noval MG, Altieri TA, de Oliveira GA, Silva JL, et al. (2013) Fine modulation of the respiratory syncytial virus M2-1 protein quaternary structure by reversible zinc removal from its Cys(3)-His(1) motif. Biochemistry 52: 6779–6789. doi: 10.1021/bi401029q
[74]
Tanner SJ, Ariza A, Richard CA, Kyle HF, Dods RL, et al. (2014) Crystal structure of the essential transcription antiterminator M2-1 protein of human respiratory syncytial virus and implications of its phosphorylation. Proc Natl Acad Sci U S A 111: 1580–1585. doi: 10.1073/pnas.1317262111
[75]
Ren J, Wang Q, Kolli D, Prusak DJ, Tseng CT, et al. (2012) Human metapneumovirus M2-2 protein inhibits innate cellular signaling by targeting MAVS. J Virol 86: 13049–13061. doi: 10.1128/jvi.01248-12
[76]
Deng Q, Weng Y, Lu W, Demers A, Song M, et al. (2011) Topology and cellular localization of the small hydrophobic protein of avian metapneumovirus. Virus Res 160: 102–107. doi: 10.1016/j.virusres.2011.05.020
[77]
de Graaf M, Herfst S, Aarbiou J, Burgers PC, Zaaraoui-Boutahar F, et al. (2013) Small hydrophobic protein of human metapneumovirus does not affect virus replication and host gene expression in vitro. PLoS One 8: e58572. doi: 10.1371/journal.pone.0058572
[78]
Karron RA, Buonagurio DA, Georgiu AF, Whitehead SS, Adamus JE, et al. (1997) Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc Natl Acad Sci U S A 94: 13961–13966. doi: 10.1073/pnas.94.25.13961
[79]
Ling R, Sinkovic S, Toquin D, Guionie O, Eterradossi N, et al. (2008) Deletion of the SH gene from avian metapneumovirus has a greater impact on virus production and immunogenicity in turkeys than deletion of the G gene or M2-2 open reading frame. J Gen Virol 89: 525–533. doi: 10.1099/vir.0.83309-0
[80]
Biacchesi S, Pham QN, Skiadopoulos MH, Murphy BR, Collins PL, et al. (2005) Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J Virol 79: 12608–12613. doi: 10.1128/jvi.79.19.12608-12613.2005
[81]
Cox RG, Livesay SB, Johnson M, Ohi MD, Williams JV (2012) The human metapneumovirus fusion protein mediates entry via an interaction with RGD-binding integrins. J Virol 86: 12148–12160. doi: 10.1128/jvi.01133-12
[82]
Bao X, Kolli D, Ren J, Liu T, Garofalo RP, et al. (2013) Human metapneumovirus glycoprotein G disrupts mitochondrial signaling in airway epithelial cells. PLoS One 8: e62568. doi: 10.1371/journal.pone.0062568
[83]
Bao X, Liu T, Shan Y, Li K, Garofalo RP, et al. (2008) Human metapneumovirus glycoprotein G inhibits innate immune responses. PLoS Pathog 4: e1000077. doi: 10.1371/journal.ppat.1000077
[84]
Kolli D, Bao X, Liu T, Hong C, Wang T, et al. (2011) Human metapneumovirus glycoprotein G inhibits TLR4-dependent signaling in monocyte-derived dendritic cells. J Immunol 187: 47–54. doi: 10.4049/jimmunol.1002589
[85]
Chockalingam AK, Chander Y, Halvorson DA, Goyal SM (2010) Stability of the glycoprotein gene of avian metapneumovirus (Canada goose isolate 15a/01) after serial passages in cell cultures. Avian Dis 54: 915–918. doi: 10.1637/9016-081909-resnote.1
[86]
Kong BW, Foster LK, Foster DN (2008) Species-specific deletion of the viral attachment glycoprotein of avian metapneumovirus. Virus Res 132: 114–121. doi: 10.1016/j.virusres.2007.11.006
[87]
Velayudhan BT, Yu Q, Estevez CN, Nagaraja KV, Halvorson DA (2008) Glycoprotein gene truncation in avian metapneumovirus subtype C isolates from the United States. Virus Genes 37: 266–272. doi: 10.1007/s11262-008-0220-6
[88]
Poch O, Blumberg BM, Bougueleret L, Tordo N (1990) Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 71 (Pt 5): 1153–1162. doi: 10.1099/0022-1317-71-5-1153
[89]
Svenda M, Berg M, Moreno-Lopez J, Linne T (1997) Analysis of the large (L) protein gene of the porcine rubulavirus LPMV: identification of possible functional domains. Virus Res 48: 57–70. doi: 10.1016/s0168-1702(96)01426-8
[90]
Li J, Ling R, Randhawa JS, Shaw K, Davis PJ, et al. (1996) Sequence of the nucleocapsid protein gene of subgroup A and B avian pneumoviruses. Virus Res 41: 185–191. doi: 10.1016/0168-1702(96)01288-9
[91]
Yu Q, Davis PJ, Brown TD, Cavanagh D (1992) Sequence and in vitro expression of the M2 gene of turkey rhinotracheitis pneumovirus. J Gen Virol 73 (Pt 6): 1355–1363. doi: 10.1099/0022-1317-73-6-1355
[92]
Yu Q, Davis PJ, Li J, Cavanagh D (1992) Cloning and sequencing of the matrix protein (M) gene of turkey rhinotracheitis virus reveal a gene order different from that of respiratory syncytial virus. Virology 186: 426–434. doi: 10.1016/0042-6822(92)90007-c
[93]
Alvarez R, Jones LP, Seal BS, Kapczynski DR, Tripp RA (2004) Serological cross-reactivity of members of the Metapneumovirus genus. Virus Res 105: 67–73. doi: 10.1016/j.virusres.2004.09.003
[94]
de Almeida RS, Hammoumi S, Gil P, Briand FX, Molia S, et al. (2013) New avian paramyxoviruses type I strains identified in Africa provide new outcomes for phylogeny reconstruction and genotype classification. PLoS One 8: e76413. doi: 10.1371/journal.pone.0076413
[95]
Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, et al. (2012) Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12: 1770–1779. doi: 10.1016/j.meegid.2012.07.012
