Cited by 355T-cell and Retrovirus StudiesHIV Research and TreatmentCholesterol and Lipid Metabolism

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A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor

Bates, Paul, Young, John A.T., Varmus, Harold E.·1993·Cell

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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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Lai, 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
“…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).”
MethodInfluential
Chapter 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
Avian sarcoma and leukosis virus-receptor interactions: From classical genetics to novel insights into virus–cell membrane fusion
Barnard, R. J. O., Elleder, D., & Young, J. A. T. (2005) · Virology · doi:10.1016/j.virol.2005.09.021 · Cited by 99
“The first of the genes identified by this method was tva (Bates et al., 1993; Young et al., 1993).”
MethodSelf-citation
Sorting Mechanisms Regulating Membrane Protein Traffic in the Apical Transcytotic Pathway of Polarized MDCK Cells
Gibson, 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
“(Bates et al., 1993) and expressing human TR with BH-RCAS(A)-pIgR.”
Method
The small GTPase Rac1 links the Kaposi sarcoma–associated herpesvirus vGPCR to cytokine secretion and paracrine neoplasia
Montaner, 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
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
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
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
“Human 293 cells and CEFs were grown as previously described (4, 26, 27).”
Self-citation
Identification 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
Self-citation
Receptor-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
Self-citation
The 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
“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].”
Background
Two Retroviral Entry Pathways Distinguished by Lipid Raft Association of the Viral Receptor and Differences in Viral Infectivity
Narayan, 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
Self-citation
The Receptor for the Subgroup C Avian Sarcoma and Leukosis Viruses, Tvc, Is Related to Mammalian Butyrophilins, Members of the Immunoglobulin Superfamily
Elleder, 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 90
“The ASLV(A) receptors (Tva) are related to the family of lowdensity lipoprotein receptors (LDLR) (8, 57).”
BackgroundInfluential
Introns and exons
Patthy, L. (1994) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(94)90108-2 · Cited by 84
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 82
“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-citation
Assessing Tumor Progression Factors by Somatic Gene Transfer into a Mouse Model: Bcl-xL Promotes Islet Tumor Cell Invasion
Du, Y. N., Lewis, B. C., Hanahan, D., & VARMUS, H. E. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050276 · Cited by 86
“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-citation
Broad host range of human T-cell leukemia virus type 1 demonstrated with an improved pseudotyping system
Sutton, R. E., & Littman, D. R. (1996) · Journal of Virology · doi:10.1128/jvi.70.10.7322-7326.1996 · Cited by 83
“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.”
Method
Astrocytes Give Rise to Oligodendrogliomas and Astrocytomas after Gene Transfer of Polyoma Virus Middle T Antigen in Vivo
Holland, 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
“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.”
Background
Herpes 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
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
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
Zingler, K., & Young, J. A. T. (1996) · Journal of Virology · doi:10.1128/jvi.70.11.7510-7516.1996 · Cited by 75
“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-citation
Cell 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
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
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 77
“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…”
Influential
Prions and related neurological diseases
Pocchiari, M. (1994) · Molecular Aspects of Medicine · doi:10.1016/0098-2997(94)90042-6 · Cited by 74
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
Rong, L., & Bates, P. F. (1995) · Journal of Virology · doi:10.1128/jvi.69.8.4847-4853.1995 · Cited by 68
“Two alternatively spliced transcripts encoding functional receptors were derived from the quail gene by utilizing an exon trapping protocol (2).”
BackgroundMethodInfluentialSelf-citation
Retrovirus receptors
Sommerfelt, M. A. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-12-3049 · Cited by 71
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 65
“…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
The viral envelope is a major determinant for the induction of lymphoid and myeloid tumours by avian leukosis virus subgroups A and J, respectively
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
“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).”
Chimeric molecules employing horseradish peroxidase as reporter enzyme for protein localization in the electron microscope
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
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
Self-citation
Association 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
Low pH Is Required for Avian Sarcoma and Leukosis Virus Env-Induced Hemifusion and Fusion Pore Formation but Not for Pore Growth
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
“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-citation
A 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
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
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
Keratin 6a marks mammary bipotential progenitor cells that can give rise to a unique tumor model resembling human normal-like breast cancer
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 62
“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).”
Method
Quantitative imaging of endosome acidification and single retrovirus fusion with distinct pools of early endosomes
Padilla‐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
“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).”
Background
Retroviral Insertional Mutagenesis Identifies a Small Protein Required for Synthesis of Diphthamide, the Target of Bacterial ADP-Ribosylating Toxins
Liu, S., & Leppla, S. H. (2003) · Molecular Cell · doi:10.1016/j.molcel.2003.08.003 · Cited by 61
The receptor for the subgroup A avian leukosis-sarcoma viruses binds to subgroup A but not to subgroup C envelope glycoprotein
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
“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)
ORCID: Bates, Paul
Young, John A.T.
Varmus, Harold E.
Venue: Cell
Publisher: Elsevier BV
Published: 1993-09
Volume: 74
Issue: 6
Pages: 1043-1051
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/0092-8674(93)90726-7
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › 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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A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor

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