UNLABELLED: The J subgroup of avian leukosis virus (ALV-J) infects domestic chickens, jungle fowl, and turkeys. This virus enters the host cell through a receptor encoded by the tvj locus and identified as Na+/H+ exchanger 1. The resistance to avian leukosis virus subgroup J in a great majority of galliform species has been explained by deletions or substitutions of the critical tryptophan 38 in the first extracellular loop of Na+/H+ exchanger 1. Because there are concerns of transspecies virus transmission, we studied natural polymorphisms and susceptibility/resistance in wild galliforms and found the presence of tryptophan 38 in four species of New World quails. The embryo fibroblasts of New World quails are susceptible to infection with avian leukosis virus subgroup J, and the cloned Na+/H+ exchanger 1 confers susceptibility on the otherwise resistant host. New World quails are also susceptible to new avian leukosis virus subgroup J variants but resistant to subgroups A and B and weakly susceptible to subgroups C and D of avian sarcoma/leukosis virus due to obvious defects of the respective receptors. Our results suggest that the avian leukosis virus subgroup J could be transmitted to New World quails and establish a natural reservoir of circulating virus with a potential for further evolution. IMPORTANCE: Since its spread in broiler chickens in China and Southeast Asia in 2000, ALV-J remains a major enzootic challenge for the poultry industry. Although the virus diversifies rapidly in the poultry, its spillover and circulation in wild bird species has been prevented by the resistance of most species to ALV-J. It is, nevertheless, important to understand the evolution of the virus and its potential host range in wild birds. Because resistance to avian retroviruses is due particularly to receptor incompatibility, we studied Na+/H+ exchanger 1, the receptor for ALV-J. In New World quails, we found a receptor compatible with virus entry, and we confirmed the susceptibilities of four New World quail species in vitro We propose that a prospective molecular epidemiology study be conducted to identify species with the potential to become reservoirs for ALV-J.

Department of Viral and Cellular Genetics Institute of Molecular Genetics Academy of Sciences of the Czech Republic Prague Czech Republic

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Weiss RA. 1992. Cellular receptors and viral glycoproteins involved in retrovirus entry, p 1–108. In Levy JA. (ed), Retroviridae, vol 2 Plenum Press, New York, NY.

Barnard RJO, Elleder D, Young JAT. 2006. Avian sarcoma and leukosis virus-receptor interactions: from classical genetics to novel insights into virus-cell membrane vision. Virology 344:25–29. doi:10.1016/j.virol.2005.09.021. PubMed DOI

Kozak CA. 2011. Naturally occurring polymorphisms of the mouse gammaretrovirus receptors CAT-1 and XPR1 alter virus tropism and pathogenicity. Adv Virol 2011:975801. doi:10.1155/2011/975801. PubMed DOI PMC

Watanabe S, Kawamura M, Odahara Y, Anai Y, Ochi H, Nakagawa S, Endo Y, Tsujimoto H, Nishigaki K. 2013. Phylogenetic and structural diversity in the feline leukemia virus env gene. PLoS One 8:e61009. doi:10.1371/journal.pone.0061009. PubMed DOI PMC

Tailor CS, Nouri A, Lee CG, Kozak C, Kabat D. 1999. Cloning and characterization of a cell surface receptor for xenotropic and polytropic murine leukemia viruses. Proc Natl Acad Sci U S A 96:927–932. doi:10.1073/pnas.96.3.927. PubMed DOI PMC

Yan Y, Liu Q, Kozak C. 2009. Six host range variants of the xenotropic/polytropic gammaretroviruses define determinants for entry in the XPR1 cell surface receptor. Retrovirology 6:87. doi:10.1186/1742-4690-6-87. PubMed DOI PMC

Martin C, Buckler-White A, Wollenberg K, Kozak CA. 2013. The avian XPR1 gammaretrovirus receptor is under positive selection and is disabled in bird species in contact with virus-infected wild mice. J Virol 87:10094–10104. doi:10.1128/JVI.01327-13. PubMed DOI PMC

Humes D, Emery S, Laws E, Overbaugh J. 2012. A species-specific amino acid difference in the macaque CD4 receptor restricts replication by global circulating HIV-1 variants representing viruses from recent infection. J Virol 86:12472–12483. doi:10.1128/JVI.02176-12. PubMed DOI PMC

Meyerson NR, Rowley PA, Swan CH, Le DT, Wilkerson GK, Sawyer SL. 2014. Positive selection of primate genes that promote HIV-1 replication. Virology 454–455:291–298. doi:10.1016/j.virol.2014.02.029. PubMed DOI PMC

Meyerson NR, Sharma A, Wilkerson GK, Overbaugh J, Sawyer SL. 2015. Identification of owl monkey CD4 receptors broadly compatible with early-stage HIV-1 isolates. J Virol 89:8611–8622. doi:10.1128/JVI.00890-15. PubMed DOI PMC

Payne LN, Brown SR, Bumstead N, Howes K, Frazier JA, Thouless ME. 1991. A novel subgroup of exogenous avian leukosis virus in chickens. J Gen Virol 72:801–807. doi:10.1099/0022-1317-72-4-801. PubMed DOI

Sacco MA, Howes K, Smith LP, Nair VK. 2004. Assessing the roles of endogenous retrovirus EAV-HP in avian leukosis virus subgroup J emergence and tolerance. J Virol 78:10525–10535. doi:10.1128/JVI.78.19.10525-10535.2004. PubMed DOI PMC

Chai N, Bates P. 2006. Na+/H+ exchanger type 1 is a receptor for pathogenic subgroup J avian leukosis virus. Proc Natl Acad Sci U S A 103:5531–5536. doi:10.1073/pnas.0509785103. PubMed DOI PMC

Venugopal K, Howes K, Flannery DMJ, Payne LN. 2000. Isolation of acutely transforming subgroup J avian leukosis viruses that induce erythroblastosis and myelocytomatosis. Avian Pathol 29:497–503. doi:10.1080/030794500750047252. PubMed DOI

Payne LN, Nair V. 2012. The long view: 40 years of avian leukosis research. Avian Pathol 41:11–19. doi:10.1080/03079457.2011.646237. PubMed DOI

Malhotra S, Justice J, Lee N, Li Y, Zavala G, Ruano M, Morgan R, Beemon K. 2015. Complete genome sequence of an American avian leukosis virus subgroup J isolate that causes hemangiomas and myeloid leukosis. Genome Announc 3:e01586-14. doi:10.1128/genomeA.01586-14. PubMed DOI PMC

Jiang L, Zeng X, Hua Y, Gao Q, Fan Z, Chai H, Wang Q, Qi X, Wang Y, Gao H, Gao Y, Wang X. 2014. Genetic diversity and phylogenetic analysis of glycoprotein gp85 of avian leukosis virus subgroup J wild-bird isolates from Northeast China. Arch Virol 159:1821–1826. doi:10.1007/s00705-014-2004-8. PubMed DOI

Zeng X, Liu L, Hao R, Han C. 2014. Detection and molecular characterization of J subgroup avian leukosis virus in wild ducks in China. PLoS One 9:e94980. doi:10.1371/journal.pone.0094980. PubMed DOI PMC

Payne LN, Howes K, Gillespie AM, Smith LM. 1992. Host range of Rous sarcoma virus pseudotype RSV(HPRS-103) in 12 avian species: support for a new avian retrovirus envelope subgroup, designated J. J Gen Virol 73:2995–2997. doi:10.1099/0022-1317-73-11-2995. PubMed DOI

Kučerová D, Plachý J, Reinišová M, Šenigl F, Trejbalová K, Geryk J, Hejnar J. 2013. Nonconserved tryptophan 38 of the cell surface receptor for subgroup J avian leukosis virus discriminates sensitive from resistant avian species. J Virol 87:8399–8407. doi:10.1128/JVI.03180-12. PubMed DOI PMC

Reinišová M, Plachý J, Kučerová D, Šenigl F, Vinkler M, Hejnar J. 2016. Genetic diversity of NHE1, receptor for subgroup J avian leukosis virus, in domestic chicken and wild anseriform species. PLoS One 11:e0150589. doi:10.1371/journal.pone.0150589. PubMed DOI PMC

Zingler K, Bélanger C, Peters R, Agard E, Young JAT. 1995. Identification and characterization of the viral interaction determinant of the subgroup A avian leukosis virus receptor. J Virol 69:4261–4266. PubMed PMC

Zingler K, Young JAT. 1996. Residue Trp-48 of Tva is critical for viral entry but not for high-affinity binding to the SU glycoprotein of subgroup A avian leukosis and sarcoma viruses. J Virol 70:7510–7516. PubMed PMC

Halley YA, Dowd SE, Decker JE, Seabury PM, Bhattarai E, Johnson CD, Rollins D, Tizard IR, Brightsmith DJ, Peterson MJ, Taylor JF, Seabury CM. 2014. A draft de novo genome assembly for the northern bobwhite (Colinus virginianus) reveals evidence for a rapid decline in effective population size beginning in the Late Pleistocene. PLoS One 9:e90240. doi:10.1371/journal.pone.0090240. PubMed DOI PMC

Knauss DJ, Young JAT. 2002. A fifteen-amino-acid TVB peptide serves as a minimal soluble receptor for subgroup B avian leukosis and sarcoma viruses. J Virol 76:5404–5410. doi:10.1128/JVI.76.11.5404-5410.2002. PubMed DOI PMC

Adkins HB, Brojatsch J, Young JAT. 2000. Identification and characterization of a shared TNFR-related receptor for subgroup B, D, and E avian leukosis viruses reveal cysteine residues required specifically for subgroup E viral entry. J Virol 74:3572–3578. doi:10.1128/JVI.74.8.3572-3578.2000. PubMed DOI PMC

Elleder D, Stepanets V, Melder DC, Šenigl F, Geryk J, Pajer P, Plachý J, Hejnar J, Svoboda J, Federspiel MJ. 2005. The receptor for the subgroup C avian sarcoma and leukosis viruses, Tvc, is related to mammalian butyrophilins, members of the immunoglobulin superfamily. J Virol 79:10408–10419. doi:10.1128/JVI.79.16.10408-10419.2005. PubMed DOI PMC

Munguia A, Federspiel MJ. 2008. Efficient subgroup C avian sarcoma and leukosis virus receptor activity requires the IgV domain of the Tvc receptor and proper display on the cell membrane. J Virol 82:11419–11428. doi:10.1128/JVI.01408-08. PubMed DOI PMC

Dimcheff DE, Drovetski SV, Mindell DP. 2002. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol Phylogenet Evol 24:203–215. doi:10.1016/S1055-7903(02)00230-0. PubMed DOI

Smith EJ, Shi L, Tu Z. 2005. Gallus gallus agrecan gene-based phylogenetic analysis of selected avian groups. Genetica 124:23–32. doi:10.1007/s10709-004-5184-4. PubMed DOI

Kaiser VB, van Tuinen M, Ellegren H. 2007. Insertion events of CR1 retrotransposable elements elucidate the phylogenetic branching order in Galliform birds. Mol Biol Evol 24:338–347. doi:10.1093/molbev/msl164. PubMed DOI

Reinišová M, Plachý J, Trejbalová K, Šenigl F, Kučerová D, Geryk J, Svoboda J, Hejnar J. 2012. Intronic deletions that disrupt mRNA splicing of the tva receptor gene result in decreased susceptibility to infection by avian sarcoma and leukosis virus subgroup A. J Virol 86:2021–2030. doi:10.1128/JVI.05771-11. PubMed DOI PMC

Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, MacDonald ME, Stuhlmann H, Koup RA, Landau NR. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367–377. doi:10.1016/S0092-8674(00)80110-5. PubMed DOI

Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M. 1996. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722–725. doi:10.1038/382722a0. PubMed DOI

Chen Z, Kwon D, Jin Z, Monard S, Telfer P, Jones MS, Lu CY, Aguilar RF, Ho DD, Marx PA. 1998. Natural infection of a homozygous delta24 CCR5 red-capped mangabey with an R2b-tropic simian immunodeficiency virus. J Exp Med 188:2057–2065. doi:10.1084/jem.188.11.2057. PubMed DOI PMC

Palacios E, Digilio L, McClure HM, Chen Z, Marx PA, Goldsmith MA, Grant RM. 1998. Parallel evolution of CCR5-null phenotypes in humans and in a natural host of simian immunodeficiency virus. Curr Biol 8:943–946. doi:10.1016/S0960-9822(07)00378-8. PubMed DOI

Riddick NE, Hermann EA, Loftin LM, Elliott ST, Wey WC, Cervasi B, Taaffe J, Engram JC, Li B, Else JG, Li Y, Hahn BH, Derdeyn CA, Sodora DL, Apetrei C, Paiardini M, Silvestri G, Collman RG. 2010. A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor use in vivo. PLoS Pathog 6:e1001064. doi:10.1371/journal.ppat.1001064. PubMed DOI PMC

Nehyba J, Svoboda J, Karakoz I, Geryk J, Hejnar J. 1990. Ducks: a new experimental host system for studying persistent infection with avian leukaemia retroviruses. J Gen Virol 71:1937–1945. doi:10.1099/0022-1317-71-9-1937. PubMed DOI

Stepanets V, Vernerová Z, Vilhelmová M, Geryk J, Hejnar J, Svoboda J. 2001. Amyloid A amyloidosis in non-infected and avian leukosis virus-C persistently infected inbred ducks. Avian Pathol 30:33–42. doi:10.1080/03079450020023177. PubMed DOI

Dimcheff DE, Drovetski SV, Krishnan M, Mindell DP. 2000. Cospeciation and horizontal transmission of avian sarcoma and leukosis virus gag genes in galliform birds. J Virol 74:3984–3995. doi:10.1128/JVI.74.9.3984-3995.2000. PubMed DOI PMC

Dimcheff DE, Krishnan M, Mindell DP. 2001. Evolution and characterization of tetraonine endogenous retrovirus: a new virus related to avian sarcoma and leukosis viruses. J Virol 75:2002–2009. doi:10.1128/JVI.75.4.2002-2009.2001. PubMed DOI PMC

Federspiel MJ, Hughes SH. 1997. Retroviral gene delivery. Methods Cell Biol 52:167–177. PubMed

Himly M, Foster DN, Bottoli I, Iacovoni JS, Vogt PK. 1998. The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248:295–304. doi:10.1006/viro.1998.9290. PubMed DOI

Moscovici C, Moscovici MG, Jimenez H, Lai MM, Hayman MJ, Vogt PK. 1977. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell 11:95–103. doi:10.1016/0092-8674(77)90320-8. PubMed DOI

Reinišová M, Šenigl F, Yin X, Plachý J, Geryk J, Elleder D, Svoboda J, Federspiel MJ, Hejnar J. 2008. A single-amino-acid substitution in the TvbS1 receptor results in decreased susceptibility to infection by avian sarcoma and leukosis virus subgroups B and D and resistance to infection by subgroup E in vitro and in vivo. J Virol 82:2097–2105. doi:10.1128/JVI.02206-07. PubMed DOI PMC

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis, version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197. PubMed DOI PMC

Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520. PubMed DOI

Pond SLK, Frost SDW. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533. doi:10.1093/bioinformatics/bti320. PubMed DOI

Yang ZH, Wong WSW, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. doi:10.1093/molbev/msi097. PubMed DOI

Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. doi:10.1093/molbev/msm088. PubMed DOI

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