A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor
Abstract
Cellular receptors are required for efficient entry of retroviruses into cells. We previously cloned a chicken gene responsible for susceptibility to the retrovirus subgroup A Rous sarcoma virus (RSV(A)). Here we have isolated the quail homolog and generated two alternatively spliced processed genes encoding cellular receptors for RSV(A). Predicted products of the processed genes appear to be small membrane-associated proteins with identical 83 amino acid extracellular domains but different membrane anchors. Within the extracellular domain is a region closely related to the ligand-binding repeat of the low density lipoprotein receptor (LDLR). Expression of either processed gene renders mammalian cells specifically susceptible to RSV(A). Antibodies directed against the receptor block subgroup A infection of avian cells via endogenous receptors and have no effect on entry of other RSV subgroups. Thus, small LDLR-related proteins are cellular receptors for RSV(A).
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LRAD3, pg800 and pg950 may define a new sub-family of receptors closely related to the LDL receptor by the presence of one or more LDLa repeats in their extracellular domains, but which lack the other LDL receptor family motifs.
“Thus, LRAD3, pg800 and pg950 may define a new sub-family of receptors which are closely related to the LDL receptor by the presence of one or more LDLa repeats in their extracellular domains, but which lack the other LDL receptor family motifs.”
From LRAD3, A Novel Low-Density Lipoprotein Receptor Family Member That Modulates Amyloid Precursor Protein Trafficking (2011) · cites this paper as Bates et al., 1993
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“The retroviral RCASBP(A) (replication competent avian sarcoma-leukosis virus long terminal repeat with splice acceptor, Bryan RSV polymerase and subgroup A envelope)-expression vector derived from subgroup A avian sarcoma-leukosis virus can be used to produce high-titer viral stocks in chicken DF-1 fibroblasts and del…”
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“After selection of transfected MDCK cells with 500 Ixg/ml geneticin (Gibco BRL, Gaithersburg, MD), individual clones which stably express the RSV(A) receptor were identified by Western blotting using antisera against the receptor (Bates et al., 1993).”
BackgroundMethodInfluentialVLDLR and ApoER2 are receptors for multiple alphaviruses
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“…and Sufficient for Basolateral Sorting Using a retroviral vector derived from RSV(A) (Hughes et al., 1990), mutant human TR were stably expressed in MDCK cells in which the RSV(A) receptor (Bates et al., 1993) had been expressed, rendering them susceptible to infection (Odorizzi et al., 1996).”
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“The receptor for Subgroup A is related to the low density lipoprotein receptor (Bates et al., 1993) and that for Subgroups B and D is a member of the tumor necrosis factor family (Brojatsch et al.”
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“No GFP labeling was observed in the brains of animals that did not encode TVA (Nkx2.”
InfluentialFederspiel, M. J., & Hughes, S. H. (1997) · PubMed · Cited by 121 · see citing works
Hernandez, L. D., Peters, R. J., Delos, S. E., Young, J. A. T., Agard, D. A., & White, J. M. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.6.1455 · Cited by 119 · see citing works
“Because Tva is related to the LDL receptor (Bates et al., 1993), it was possible that sTva itself has an affinity for li-”
BackgroundMethodInfluentialSelf-citationLewis, B. C., Klimstra, D. S., & VARMUS, H. E. (2003) · Genes & Development · doi:10.1101/gad.1140403 · Cited by 114 · see citing works
“Transgenic mice and animal care The elastase-tv-a transgene was constructed in pbluescript SK(+) by placing a 500-bp HindIII/BamHI rat elastase promoter fragment encompassing nucleotides −500 to +8 (gift of Ray MacDonald) proximal to a 1.2-kb BamHI fragment containing the 800-bp tv-a cDNA fused to SV40 intron and poly…”
MethodInfluentialSelf-citationValsesia‐Wittmann, S., Drynda, A., Deléage, G., Aumailley, M., Heard, J., Danos, O., Verdier, G., & Cosset, F. (1994) · Journal of Virology · doi:10.1128/jvi.68.7.4609-4619.1994 · Cited by 113 · see citing works
“The subgroup A receptor has recently been cloned (61) and belongs to the low-density lipoprotein receptor family (4).”
BackgroundEstablishment of persistent hepatitis C virus infection and replication in vitro.
Seipp, S., Lorenz Theilmann, I., Goeser, T., Mueller, H. M., Pfaff, E., & Stremmel, W. (1997) · Journal of General Virology · doi:10.1099/0022-1317-78-10-2467 · Cited by 111 · see citing works
“Secondly, the LDL-receptor or receptor-related surface molecules are potential entry sites for other virions into cells, such as Rous sarcoma virus (Bates et al., 1993).”
BackgroundThe Absence of p53 Promotes Metastasis in a Novel Somatic Mouse Model for Hepatocellular Carcinoma
Lewis, B. C., Klimstra, D. S., Socci, N. D., Xu, S., Koutcher, J. A., & VARMUS, H. E. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.4.1228-1237.2005 · Cited by 110 · see citing works
“We therefore generated transgenic animals in which the receptor for ALSV-A, TVA, was produced specifically within the liver.”
BackgroundInfluentialSelf-citationHughes, S. H. (2004) · Folia Biologica · doi:10.14712/fb2004050030107 · Cited by 55 · see citing works
Blacklow, S. C., & Kim, P. S. (1996) · Nature Structural & Molecular Biology · doi:10.1038/nsb0996-758 · Cited by 103 · see citing works
Weiss, R. A., & Tailor, C. S. (1995) · Cell · doi:10.1016/0092-8674(95)90024-1 · Cited by 105 · see citing works
Filovirus Entry: A Novelty in the Viral Fusion World
Hunt, C. L., Lennemann, N. J., & Maury, W. J. (2012) · Viruses · doi:10.3390/v4020258 · Cited by 104 · see citing works
“One classical approach to identifying virus receptors that has been used is the introduction of a cDNA library from a permissive cell into a cell that is not permissive for the virus [38] [39] [40] .”
BackgroundTransmission, Evolution, and Endogenization: Lessons Learned from Recent Retroviral Invasions
Greenwood, A. D., Ishida, Y., O’Brien, S. P., Roca, A. L., & Eiden, M. V. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00044-17 · Cited by 103 · see citing works
Na + /H + exchanger type 1 is a receptor for pathogenic subgroup J avian leukosis virus
Chai, N., & Bates, P. F. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509785103 · Cited by 103 · see citing works
Self-citationLai, A., Le, D.-N., Paznekas, W. A., Gifford, W. D., Jabs, E. W., & Charles, A. C. (2006) · Journal of Cell Science · doi:10.1242/jcs.02770 · Cited by 102 · see citing works
“…render C6 cells susceptible to infection with virus, C6 cells were transfected with pCB6(0.95), an expression plasmid encoding the 157 amino acid isoform Tva receptor (gift from Dr Paul Bates, University of Pennsylvania, Philadelphia, PA) using Superfect transfection reagent (Bates et al., 1993).”
MethodInfluentialChapter 9 Retroviral Gene Delivery
Federspiel, M. J., & Hughes, S. H. (1997) · Methods in cell biology · doi:10.1016/s0091-679x(08)60379-9 · Cited by 101 · see citing works
Barnard, R. J. O., Elleder, D., & Young, J. A. T. (2005) · Virology · doi:10.1016/j.virol.2005.09.021 · Cited by 99 · see citing works
“The first of the genes identified by this method was tva (Bates et al., 1993; Young et al., 1993).”
MethodSelf-citationGibson, A., Futter, C. E., Maxwell, S., Allchin, E. H., Shipman, M., Kraehenbühl, J. P., Domingo, D., Odorizzi, G., Trowbridge, I. S., & Hopkins, C. R. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.1.81 · Cited by 98 · see citing works
“(Bates et al., 1993) and expressing human TR with BH-RCAS(A)-pIgR.”
MethodMontaner, S., Sodhi, A., Servitja, J., Ramsdell, A. K., Barac, A., Sawai, E. T., & Gutkind, J. S. (2004) · Blood · doi:10.1182/blood-2003-12-4436 · Cited by 97 · see citing works
Mechanisms of enveloped virus entry into animal cells
Klasse, P. J., Bron, R., & Marsh, M. (1998) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00002-7 · Cited by 94 · see citing works
Adkins, H. B., Brojatsch, J., & Young, J. A. T. (2000) · Journal of Virology · doi:10.1128/jvi.74.8.3572-3578.2000 · Cited by 93 · see citing works
“Human 293 cells and CEFs were grown as previously described (4, 26, 27).”
Self-citationIdentification of a cellular receptor for subgroup E avian leukosis virus
Adkins, H. B., Brojatsch, J., Naughton, J., Rolls, M. M., Pesola, J. M., & Young, J. A. T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11617 · Cited by 93 · see citing works
Self-citationReceptor-triggered membrane association of a model retroviral glycoprotein
Damico, R. L., Crane, J., & Bates, P. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.5.2580 · Cited by 93 · see citing works
Self-citationThe Receptor‐Binding Region of Human Apolipoprotein E Has Direct Anti‐Infective Activity
Dobson, C. B., Sales, S. D., Hoggard, P. G., Wozniak, M. A., & Crutcher, K. A. (2006) · The Journal of Infectious Diseases · doi:10.1086/499280 · Cited by 92 · see citing works
“Both viruses and LPs initially bind to the extracellular matrix (often heparan sulfate proteoglycans [HSPGs]) and then to specific cellular receptors [14]; some viruses use LP receptors to enter cells [15].”
BackgroundNarayan, S., Barnard, R. J. O., & Young, J. A. T. (2003) · Journal of Virology · doi:10.1128/jvi.77.3.1977-1983.2003 · Cited by 89 · see citing works
Self-citationElleder, D., Stepanets, V., Melder, D. C., Šenigl, F., Geryk, J., Pajer, P., Plachý, J., Hejnar, J., Svoboda, J., & Federspiel, M. J. (2005) · Journal of Virology · doi:10.1128/jvi.79.16.10408-10419.2005 · Cited by 88 · see citing works
“The ASLV(A) receptors (Tva) are related to the family of lowdensity lipoprotein receptors (LDLR) (8, 57).”
BackgroundInfluentialPatthy, L. (1994) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(94)90108-2 · Cited by 85 · see citing works
Development of an Avian Leukosis-Sarcoma Virus Subgroup A Pseudotyped Lentiviral Vector
Lewis, B. C., Chinnasamy, N., Morgan, R. A., & VARMUS, H. E. (2001) · Journal of Virology · doi:10.1128/jvi.75.19.9339-9344.2001 · Cited by 83 · see citing works
“ALSV utilizes glycoprotein receptors on the membrane surface, whereas VSV has been shown to fuse directly with membrane phospholipids (1, 17, 31, 33, 34).”
BackgroundSelf-citationDu, Y. N., Lewis, B. C., Hanahan, D., & VARMUS, H. E. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050276 · Cited by 82 · see citing works
“equipping pancreatic b cells with TVA, the cell surface receptor for subgroup A avian leukosis viruses [9,10], so that the cells are susceptible to the RCASBP vector [15] derived from those viruses.”
BackgroundSelf-citationSutton, R. E., & Littman, D. R. (1996) · Journal of Virology · doi:10.1128/jvi.70.10.7322-7326.1996 · Cited by 82 · see citing works
“Such an approach, used successfully to identify the cellular receptors of several other retroviruses (1, 2, 23, 26, 43), awaits identification of a cell line nonpermissive for HTLV-1 infection.”
MethodHolland, E. C., Li, Y., Celestino, J., Dai, C., Schaefer, L., Sawaya, R. A., & Fuller, G. N. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64615-9 · Cited by 81 · see citing works
“This vector is replication-competent in avian cells but will only infect mammalian cells expressing the RCAS receptor tv-a.(16) Generation of a producer cell line for RCAS-MTA was achieved by transfection of the chicken fibroblast cell line, DF-1.”
BackgroundHerpes simplex virus type 1 and Alzheimer’s disease
Dobson, C. B., & Itzhaki, R. F. (1999) · Neurobiology of Aging · doi:10.1016/s0197-4580(99)00055-x · Cited by 80 · see citing works
Genetic Control of Retrovirus Susceptibility in Mammalian Cells
Goff, S. P. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.094136 · Cited by 78 · see citing works
Zingler, K., & Young, J. A. T. (1996) · Journal of Virology · doi:10.1128/jvi.70.11.7510-7516.1996 · Cited by 75 · see citing works
“The Tva receptor has a small 83-amino-acid extracellular domain which contains a motif (residues 11 to 50) that is highly related to the seven ligand binding repeat regions of the lowdensity lipoprotein receptor (LDLR) (5).”
BackgroundSelf-citationCell Surface Receptors for Gammaretroviruses
Tailor, C. S., Lavillette, D., Marin, M., & Kabat, D. (2003) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-19012-4_2 · Cited by 76 · see citing works
Endocytosis Is a Critical Step in Entry of Subgroup B Avian Leukosis Viruses
Diaz‐Griffero, F., Hoschander, S. A., & Brojatsch, J. (2002) · Journal of Virology · doi:10.1128/jvi.76.24.12866-12876.2002 · Cited by 74 · see citing works
Evolution of Cell Recognition by Viruses: A Source of Biological Novelty with Medical Implications
Baranowski, É., Ruiz-Jarabo, C. M., Pariente, N., Verdaguer, N., & Domingo, E. (2003) · Advances in virus research · doi:10.1016/s0065-3527(03)62002-6 · Cited by 73 · see citing works
“Examples include Sindbis virus adapted to BHK cells (Klimstra et al., 1998), classical swine fever virus propagated in swine kidney cells (Hulst et al., 2000), and variants of human rhinovirus 89 adapted to HEp2 cells (Reischl et al., 2001; Vlasak et al., 2002) (Section II,B). decay-accelerating factor; EGFR, epiderma…”
InfluentialPrions and related neurological diseases
Pocchiari, M. (1994) · Molecular Aspects of Medicine · doi:10.1016/0098-2997(94)90042-6 · Cited by 74 · see citing works
Rong, L., & Bates, P. F. (1995) · Journal of Virology · doi:10.1128/jvi.69.8.4847-4853.1995 · Cited by 68 · see citing works
“Two alternatively spliced transcripts encoding functional receptors were derived from the quail gene by utilizing an exon trapping protocol (2).”
BackgroundMethodInfluentialSelf-citationSommerfelt, M. A. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-12-3049 · Cited by 71 · see citing works
Monosynaptic Tracing Success Depends Critically on Helper Virus Concentrations
Lavin, T. K., Jin, L., Lea, N. E., & Wickersham, I. R. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.00006 · Cited by 69 · see citing works
“…two exogenous proteins must be expressed before injection of the rabies virus: the receptor for EnvA (a quail cell surface protein called "TVA"[7]), to allow the modified rabies virus to infect the starting cells, and the deleted viral gene(s) (G, in the case of first-generation ("∆G")…”
Virus receptors: implications for pathogenesis and the design of antiviral agents
Norkin, L. C. (1995) · Clinical Microbiology Reviews · doi:10.1128/cmr.8.2.293 · Cited by 70 · see citing works
Chesters, P. M., Howes, K., Petherbridge, L., Evans, S., Payne, L. N., & Venugopal, K. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-10-2553 · Cited by 69 · see citing works
“The ALV-A receptor, encoded by the tva susceptibility allele, contains sequences related to the ligandbinding region of the low-density lipoprotein receptor (Bates et al., 1993).”
Hopkins, C. R., Gibson, A., Stinchcombe, J. C., & Futter, C. E. (2000) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(00)27265-0 · Cited by 68 · see citing works
Cell-specific viral targeting mediated by a soluble retroviral receptor-ligand fusion protein
Astrof, S., & Young, J. A. T. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.7063 · Cited by 67 · see citing works
Self-citationAssociation of low-density lipoprotein receptor polymorphisms and outcome of hepatitis C infection
Hennig, B. J., Hellier, S. C., Frodsham, A. J., Zhang, L., Klenerman, P., Knapp, S., Wright, M., Thomas, H. C., Thursz, M. R., & Hill, A. V. S. (2002) · Genes and Immunity · doi:10.1038/sj.gene.6363883 · Cited by 65 · see citing works
Melikyan, G. B., Barnard, R. J. O., Markosyan, R. M., Young, J. A. T., & Cohen, F. (2004) · Journal of Virology · doi:10.1128/jvi.78.7.3753-3762.2004 · Cited by 64 · see citing works
“Expressing the TVA and TVB receptors on cells deficient in the receptor renders those cells susceptible to infection by ASLV subgroup A (ASLV-A) or ASLV-B, respectively (2, 4, 8).”
Self-citationA Novel Mosaic Protein Containing LDL Receptor Elements Is Highly Conserved in Humans and Chickens
Mörwald, S., Yamazaki, H., Bujo, H., Kusunoki, J., Kanaki, T., Seimiya, K., Morisaki, N., Nimpf, J., Schneider, W. J., & Saitō, Y. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.5.996 · Cited by 64 · see citing works
Generation of RCAS Vectors Useful for Functional Genomic Analyses
Loftus, S. K. (2001) · DNA Research · doi:10.1093/dnares/8.5.221 · Cited by 64 · see citing works
α2‐Macroglobulin Receptor Mediates Binding and Cytotoxicity of Plant Ribosome‐Inactivating Proteins
Cavallaro, U., Nykjær, A., Nielsen, M. S., & Soria, M. R. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20795.x · Cited by 63 · see citing works
Bu, W., Chen, J., Morrison, G. D., Huang, S., Creighton, C. J., Huang, J., Chamness, G. C., Hilsenbeck, S. G., Roop, D. R., Leavitt, A. D., et al. (2011) · Oncogene · doi:10.1038/onc.2011.147 · Cited by 61 · see citing works
“To isolate live K6aþ cells, we placed tumor virus A (tva)—a gene encoding the cell-surface receptor for an avian leukosis virus, subgroup A (ALV/A) (Bates et al., 1993)—behind the K6a promoter in a BAC transgenic construct (Supplementary Figure 1).”
MethodPadilla‐Parra, S., Matos, P. M., Kondo, N., Marin, M., Santos, N. C., & Melikyan, G. B. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211714109 · Cited by 61 · see citing works
“Subtype A ASLV envelope glycoprotein (EnvA) becomes competent to mediate low-pH–dependent membrane fusion only after binding to the avian tumor virus receptor A (TVA receptor) (22, 23).”
BackgroundLiu, S., & Leppla, S. H. (2003) · Molecular Cell · doi:10.1016/j.molcel.2003.08.003 · Cited by 61 · see citing works
Gilbert, J. M., Bates, P. F., VARMUS, H. E., & White, J. M. (1994) · Journal of Virology · doi:10.1128/jvi.68.9.5623-5628.1994 · Cited by 61 · see citing works
“The parental 3T3 cell line is not infectible with either virus (1).”
BackgroundMethodInfluentialSelf-citation
- Authors
- Bates, P., Young, J. A. T., & Varmus, H. E.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1993-09
- Volume
- 74
- Issue
- 6
- Pages
- 1043-1051
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W1969563526
- Cited by
- 355
- References
- 38
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 4 · 2019: 6 · 2018: 3 · 2017: 10 · 2016: 3 · 2015: 13 · 2014: 11 · 2013: 12 · 2012: 8
- FWCI
- 6.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (2r35ca039832-08)
- National Cancer Institute (CA 39832)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Keywords
- cell receptors, LDL receptor, alternative splicing, membrane-associated proteins, chickens, quail, avian cells
- MeSH terms
- Amino Acid Sequence, Animals, Avian Sarcoma Viruses, Base Sequence, Cell Line, Chick Embryo, Chickens, Cloning, Molecular, DNA, Glutathione Transferase, Humans, Molecular Sequence Data, Plasmids, Quail, Receptors, LDL, Receptors, Virus, Recombinant Fusion Proteins, Transfection, Gene Library, 3T3 Cells, Sequence Homology, Amino Acid, Mice
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