The five highly related envelope subgroups of the avian sarcoma and leukosis viruses (ASLVs), subgroup A [ASLV(A)] to ASLV(E), are thought to have evolved from an ancestral envelope glycoprotein yet utilize different cellular proteins as receptors. Alleles encoding the subgroup A ASLV receptors (Tva), members of the low-density lipoprotein receptor family, and the subgroup B, D, and E ASLV receptors (Tvb), members of the tumor necrosis factor receptor family, have been identified and cloned. However, alleles encoding the subgroup C ASLV receptors (Tvc) have not been cloned. Previously, we established a genetic linkage between tvc and several other nearby genetic markers on chicken chromosome 28, including tva. In this study, we used this information to clone the tvc gene and identify the Tvc receptor. A bacterial artificial chromosome containing a portion of chicken chromosome 28 that conferred susceptibility to ASLV(C) infection was identified. The tvc gene was identified on this genomic DNA fragment and encodes a 488-amino-acid protein most closely related to mammalian butyrophilins, members of the immunoglobulin protein family. We subsequently cloned cDNAs encoding Tvc that confer susceptibility to infection by subgroup C viruses in chicken cells resistant to ASLV(C) infection and in mammalian cells that do not normally express functional ASLV receptors. In addition, normally susceptible chicken DT40 cells were resistant to ASLV(C) infection after both tvc alleles were disrupted by homologous recombination. Tvc binds the ASLV(C) envelope glycoproteins with low-nanomolar affinity, an affinity similar to that of binding of Tva and Tvb with their respective envelope glycoproteins. We have also identified a mutation in the tvc gene in line L15 chickens that explains why this line is resistant to ASLV(C) infection.

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

Zobrazit více v PubMed

Adkins, H. B., S. C. Blacklow, and J. A. T. Young. 2001. Two functionally distinct forms of a retroviral receptor explain the nonreciprical receptor interference among subgroups B, D, and E avian leukosis viruses. J. Virol. 75:3520-3526. PubMed PMC

Adkins, H. B., J. Brojatsch, J. Naughton, M. M. Rolls, J. M. Pesola, and J. A. T. Young. 1997. Identification of a cellular receptor for subgroup E avian leukosis virus. Proc. Natl. Acad. Sci. USA 94:11617-11622. PubMed PMC

Adkins, H. B., J. Brojatsch, and J. A. T. Young. 2000. Identification and characterization of a shared TNFR-related receptor for subgroup B, D, and E avain leukosis viruses reveal cysteine residues required specifically for subgroup E viral entry. J. Virol. 74:3572-3578. PubMed PMC

Arakawa, H., D. Lodygin, and J.-M. Buerstedde. 2001. Mutant loxP vectors for selectable marker recycle and conditional knock-outs. BMC Biotechnology 1:7. PubMed PMC

Baker, A., and M. Cotten. 1997. Delivery of bacterial artificial chromosomes into mammalian cells with psoralen-inactivated adenovirus carrier. Nucleic Acid Res. 25:1950-1956. PubMed PMC

Barnard, R. J., and J. A. T. Young. 2003. Alpharetrovirus envelope-receptor interactions. Curr. Top. Microbiol. Immunol. 281:107-136. PubMed

Bateman, A., L. Coin, R. Durbin, R. D. Finn, V. Hollich, S. Griffiths-Jones, A. Khanna, M. Marshall, S. Moxon, E. L. Sonnhammer, D. J. Studholme, C. Yeats, and S. R. Eddy. 2004. The Pfam protein famalies database. Nucleic Acid Res. 32:D138-D141. PubMed PMC

Bates, P., J. A. T. Young, and H. E. Varmus. 1993. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell 74:1043-1051. PubMed

Belanger, C., K. Zingler, and J. A. Young. 1995. Importance of cysteines in the LDLR-related domain of the subgroup A avian leukosis and sarcoma virus receptor for viral entry. J. Virol. 69:1019-1024. PubMed PMC

Bendtsen, J. D., H. Nielson, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795. PubMed

Boardman, P. E., J. Sanz-Ezquerro, I. M. Overton, D. W. Burt, E. Bosch, W. T. Fong, C. Tickle, W. R. Brown, S. A. Wilson, and S. J. Hibbard. 2002. A comprehensive collection of chicken cDNAs. Curr. Biol. 12:1965-1969. PubMed

Bova, C. A., J. P. Manfredi, and R. Swanstrom. 1986. Env genes of avian retroviruses: nucleotide sequence and molecular recombinants define host range determinants. Virology 152:343-354. PubMed

Bova, C. A., J. C. Olsen, and R. Swanstrom. 1988. The avian retrovirus env gene family: molecular analysis of host range and antigenic variants. J. Virol. 62:75-83. PubMed PMC

Brojatsch, J., J. Naughton, M. M. Rolls, K. Zingler, and J. A. T. Young. 1996. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avain leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845-855. PubMed

Brown, D. W., and H. L. Robinson. 1988. Influence of env and long terminal repeat sequences on the tissue tropism of avian leukosis viruses. J. Virol. 62:4828-4831. PubMed PMC

Buerstedde, J.-M., and S. Takeda. 1991. Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67:179-188. PubMed

Cogburn, L. A., R. Morgan, and J. Burnside. 2003. Expressed sequence tags, DNA chip technology and gene expression profiling, p. 629-645. In W. M. Muir and S. E. Aggrey (ed.), Poultry genetics, breeding and biotechnology. CABI Publishing, Wallingford, United Kingdom.

Compte, E., P. Pontarotti, Y. Collette, M. Lopez, and D. Olive. 2004. Characterization of BT3 molecules belonging to the B7 family expressed immune cells. Eur. J. Immunol. 34:2089-2099. PubMed

Diamond, L. 1967. Two spontaneously transformed cell lines derived from the same hamster embryo culture. Int. J. Cancer 2:143-152. PubMed

Dorner, A. J., and J. M. Coffin. 1986. Determinants for receptor interaction and cell killing on the avian retrovirus glycoprotein gp85. Cell 45:365-374. PubMed

Dorner, A. J., J. P. Stoye, and J. M. Coffin. 1985. Molecular basis of host range variation in avian retroviruses. J. Virol. 53:32-39. PubMed PMC

Elleder, D., D. C. Melder, K. Trejbalova, J. Svoboda, and M. J. Federspiel. 2004. Two different molecular defects in the Tva receptor gene explain the resistance of two tvar lines of chickens to infection by subgroup A avain sarcoma and leukosis viruses. J. Virol. 78:13489-13500. PubMed PMC

Elleder, D., J. Plachy, J. Hejnar, J. Geryk, and J. Svoboda. 2004. Close linkage of genes encoding receptors for subgroups A and C of avian sarcoma/leucosis virus on chicken chromosome 28. Anim. Genet. 35:176-181. PubMed

Federspiel, M. J., and S. H. Hughes. 1997. Retroviral gene delivery. Methods Cell Biol. 52:179-214. PubMed

Green, S., I. Issemann, and E. Sheer. 1988. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 16:369. PubMed PMC

Hala, K., and J. Plachy. 1997. Inbred strains of chickens, p. 2286-2292. In I. Lefkovitz (ed.), Immunology methods manual. Academic Press, London, United Kingdom.

Hillier, L. W., W. Miller, E. Birney, et al. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertabrate evolution. Nature 432:695-716. PubMed

Himly, M., D. N. Foster, I. Bottoli, J. S. Iacovoni, and P. K. Vogt. 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. PubMed

Holmen, S. L., and M. J. Federspiel. 2000. Selection of a subgroup A avian leukosis virus [ALV(A)] envelope resistant to soluble ALV(A) surface glycoprotein. Virology 273:364-373. PubMed

Holmen, S. L., D. C. Melder, and M. J. Federspiel. 2001. Identification of key residues in subgroup A avian leukosis virus envelope determining receptor binding affinity and infectivity of cells expressing chicken or quail Tva receptor. J. Virol. 75:726-737. PubMed PMC

Holmen, S. L., D. W. Salter, W. S. Payne, J. B. Dodgson, S. H. Hughes, and M. J. Federspiel. 1999. Soluble forms of the subgroup A avian leukosis virus [ALV(A)] receptor Tva significantly inhibit ALV(A) infection in vitro and in vivo. J. Virol. 73:10051-10060. PubMed PMC

Hunter, E. 1997. Viral entry and receptors, p. 71-120. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. PubMed

Kingston, R. E., C. A. Chen, and H. Okayama. 1989. Introduction of DNA into eukaryotic cells, p. 911-919. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 1. John Wiley & Sons, Inc., New York, N.Y.

Klucking, S., H. B. Adkins, and J. A. T. Young. 2002. Resistance of infection by subgroup B, D, and E avian sarcoma and leukosis viruses is explained by a premature stop codon within a resistance allele of the tvb receptor gene. J. Virol. 76:7918-7921. PubMed PMC

Klucking, S., and J. A. T. Young. 2004. Amino acid residues Tyr-67, Asn-72, and Asp-73 of the Tvb receptor are important for subgroup E avian sarcoma and leukosis virus interaction. Virology 318:371-380. PubMed

Kvaratskhelia, M., P. K. Clark, S. Hess, D. C. Melder, M. J. Federspiel, and S. H. Hughes. 2004. Identification of glycosylation sites in the SU component of the avian sarcoma/leukosis virus envelope glycoprotein (subgroup A) by mass spectrometry. Virology 326:171-181. PubMed

Marchler-Bauer, A., J. B. Anderson, C. DeWeese-Scott, N. D. Fedorova, L. Y. Geer, S. He, D. I. Hurwitz, J. D. Jackson, A. R. Jacobs, C. J. Lanczycki, C. A. Liebert, C. Liu, T. Madej, G. H. Marchler, R. Mazumder, A. N. Nikolskaya, A. R. Panchenko, B. S. Rao, B. A. Shoemaker, V. Simonyan, J. S. Song, P. A. Thiessen, S. Vasudevan, Y. Wang, R. A. Yamashita, J. J. Yin, and S. H. Bryant. 2003. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 31:383-387. PubMed PMC

Melder, D. C., V. S. Pankratz, and M. J. Federspiel. 2003. Evolutionary pressure of a receptor competitor selects different subgroup A avian leukosis virus escape variants with altered receptor interactions. J. Virol. 77:10504-10514. PubMed PMC

Ogg, S. L., A. K. Weldon, L. Dobbie, A. J. H. Smith, and I. H. Mather. 2004. Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. Proc. Natl. Acad. Sci. USA 101:10084-10089. PubMed PMC

Pani, P. K. 1974. Close linkage between genetic loci controlling response to fowl subgroup A and subgroup C sarcoma viruses. J. Gen. Virol. 22:187-195. PubMed

Payne, L. N., and P. K. Pani. 1971. Evidence for linkage between genetic loci controlling response of fowl to subgroup A and subgroup C sarcoma viruses. J. Gen. Virol. 13:253-259. PubMed

Rainey, G. J. A., A. Natonson, L. F. Maxfield, and J. M. Coffin. 2003. Mechanisms of avian retroviral host range extension. J. Virol. 77:6709-6719. PubMed PMC

Rhodes, D. A., M. Stammers, G. Malcherel, S. Beck, and J. Trowsdale. 2001. The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71:351-362. PubMed

Robinson, H. L., L. Ramamoorthy, K. Collart, and D. W. Brown. 1993. Tissue tropism of avian leukosis viruses: analyses for viral DNA and proteins. Virology 193:443-445. PubMed

Rong, L., and P. Bates. 1995. Analysis of the subgroup A avian sarcoma and leukosis virus receptor: the 40-residue, cysteine-rich, low-density lipoprotein receptor repeat motif of Tva is sufficient to mediate viral entry. J. Virol. 69:4847-4853. PubMed PMC

Rong, L., A. Edinger, and P. Bates. 1997. Role of basic residues in the subgroup-determining region of the subgroup A avian sarcoma and leukosis virus envelope in receptor binding and infection. J. Virol. 71:3458-3465. PubMed PMC

Rong, L., K. Gendron, B. Strohl, R. Shenoy, R. J. Wool-Lewis, and P. Bates. 1998. Characterization of determinants for envelope binding and infection in Tva, the subgroup A avian sarcoma and leukosis virus receptor. J. Virol. 72:4552-4559. PubMed PMC

Schaefer-Klein, J., I. Givol, E. V. Barsov, J. M. Whitcomb, M. VanBrocklin, D. N. Foster, M. J. Federspiel, and S. H. Hughes. 1998. The EV-0-derived cell line DF-1 supports efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248:305-311. PubMed

Smith, E. J., A. M. Fadly, and W. Okazaki. 1979. An enzyme-linked immunoabsorbant assay for detecting avian leukosis sarcoma viruses. Avian Dis. 23:698-707. PubMed

Taplitz, R. A., and J. M. Coffin. 1997. Selection of an avian retrovirus mutant with extended receptor usage. J. Virol. 71:7814-7819. PubMed PMC

Tsichlis, P. N., and J. M. Coffin. 1980. Recombinants between endogenous and exogenous avian tumor viruses: role of the C region and other portions of the genome in the control of replication and transformation. J. Virol. 33:238-249. PubMed PMC

Tsichlis, P. N., K. F. Conklin, and J. M. Coffin. 1980. Mutant and recombinant avian retroviruses with extended host range. Proc. Natl. Acad. Sci. USA 77:536-540. PubMed PMC

Weiss, R. 1982. Experimental biology and assay of RNA tumor viruses, p. 209-260. In R. Weiss, N. Teich, H. Varmus, and J. Coffin (ed.), RNA tumor viruses, vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

Weiss, R. A. 1992. Cellular receptors and viral glycoproteins involved in retrovirus entry, p. 1-108. In J. A. Levy (ed.), The retroviruses, vol. 2. Plenum Press, New York, N.Y.

Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119. PubMed

Young, J. A. T. 2001. Virus entry and uncoating, p. 87-103. In D. M. Knipe and P. M. Howley (ed.), Fields virology, vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.

Young, J. A. T., P. Bates, and H. E. Varmus. 1993. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J. Virol. 67:1811-1816. PubMed PMC

Zingler, K., C. Belanger, R. Peters, D. Agard, and J. A. T. Young. 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., and J. A. T. Young. 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

Rapid adaptive evolution of avian leukosis virus subgroup J in response to biotechnologically induced host resistance

Knock-Out of Retrovirus Receptor Gene Tva in the Chicken Confers Resistance to Avian Leukosis Virus Subgroups A and K and Affects Cobalamin (Vitamin B12)-Dependent Level of Methylmalonic Acid

The avian retroviral receptor Tva mediates the uptake of transcobalamin bound vitamin B12 (cobalamin)

The Current View of Retroviruses as Seen from the Shoulders of a Giant

The Novel Avian Leukosis Virus Subgroup K Shares Its Cellular Receptor with Subgroup A

Genetic Resistance to Avian Leukosis Viruses Induced by CRISPR/Cas9 Editing of Specific Receptor Genes in Chicken Cells

Retroviral host range extension is coupled with Env-activating mutations resulting in receptor-independent entry

Identification of New World Quails Susceptible to Infection with Avian Leukosis Virus Subgroup J

On board a raft or boat in the retrovirus sea

Genetic Diversity of NHE1, Receptor for Subgroup J Avian Leukosis Virus, in Domestic Chicken and Wild Anseriform Species

Nonconserved tryptophan 38 of the cell surface receptor for subgroup J avian leukosis virus discriminates sensitive from resistant avian species

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

The core element of a CpG island protects avian sarcoma and leukosis virus-derived vectors from transcriptional silencing

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