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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Receptors for Relaxin Family Peptides
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Method
Identification and characterization of the viral interaction determinant of the subgroup A avian leukosis virus receptor
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Background
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Background
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Background
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BackgroundMethodInfluentialSelf-citation
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BackgroundInfluential
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BackgroundInfluential
Ligand-receptor interactions of the low density lipoprotein receptor-related protein, a multi-ligand endocytic receptor
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Background
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Expression of transduced genes in mice generated by infecting blastocysts with avian leukosis virus-based retroviral vectors.
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BackgroundSelf-citation
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Background
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“pCB6 Tva950 (5) and pCB6 Tva* (31) are cytomegalovirus promoter expression plasmids for either the wild type or a mutant form of the subgroup A avian sarcoma and leukosis virus receptor, respectively.”
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Background
Specific teratogenic effects of different retinoic acid isomers and analogs in the developing anterior central nervous system of zebrafish
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“chicken Tva homologue, are related to the low-density lipoprotein receptor family (4, 5, 41).”
Background
A Cell Fusion-Based Screening Method Identifies Glycosylphosphatidylinositol-Anchored Protein Ly6e as the Receptor for Mouse Endogenous Retroviral Envelope Syncytin-A
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BackgroundMethodInfluential
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Self-citation
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“The Tva protein belongs to the family of low-density lipoprotein receptors (LDLRs) (6, 48) and determines susceptibility to the subgroup A ASLVs.”
Background
A Fifteen-Amino-Acid TVB Peptide Serves as a Minimal Soluble Receptor for Subgroup B Avian Leukosis and Sarcoma Viruses
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Self-citation
Residues 28 to 39 of the Extracellular Loop 1 of Chicken Na+/H+Exchanger Type I Mediate Cell Binding and Entry of Subgroup J Avian Leukosis Virus
Guan, X., Zhang, Y., Yu, M., Ren, C., Gao, Y., Yun, B., Liu, Y., Wang, Y., Qi, X., Liu, C., et al. (2017) · Journal of Virology · doi:10.1128/jvi.01627-17 · Cited by 35
“The receptor of ALV-A is Tva, which is most related to the family of the low-density lipoprotein receptors (15, 16).”
Background
Analysis of the murine ecotropic leukemia virus receptor reveals a common biochemical determinant on diverse cell surface receptors that is essential to retrovirus entry
Malhotra, S., Scott, A. G., Zavorotinskaya, T., & Albritton, L. M. (1996) · Journal of Virology · doi:10.1128/jvi.70.1.321-326.1996 · Cited by 35
“A similar motif involving essential acidic and nearby hydrophobic residues has been identified in the virus binding sites of other polytopic retrovirus receptors, e.g., of the ALV-A receptor (Asp-46–Glu-47–Trp-48) (54) and the GALV–FeLV receptor (Asp-550 or Glu-550 and Val-554) (20, 41, 51).”
BackgroundInfluential
A soluble form of a receptor for subgroup A avian leukosis and sarcoma viruses (ALSV-A) blocks infection and binds directly to ALSV-A
Connolly, L., Zingler, K., & Young, J. A. T. (1994) · Journal of Virology · doi:10.1128/jvi.68.4.2760-2764.1994 · Cited by 35
“the receptor are highly modified and run as a broad smear on protein gels (3).”
BackgroundInfluentialSelf-citation
Quantitative Evaluation of DNA Methylation Patterns for ALVE and TVB Genes in a Neoplastic Disease Susceptible and Resistant Chicken Model
Yu, Y., Zhang, H., Tian, F., Bacon, L. D., Zhang, Y., Zhang, W., & Song, J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001731 · Cited by 33
“TVA and TVC encode the cellular receptors for ALV of subgroup A and C, respectively, TVB is the cellular receptor gene for ALV of subgroup B, D and E [25,26].”
Background
Structural Requirements for Major Histocompatibility Complex Class II Invariant Chain Trafficking in Polarized Madin-Darby Canine Kidney Cells
Odorizzi, G., & Trowbridge, I. S. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.18.11757 · Cited by 33
Nef Can Enhance the Infectivity of Receptor-Pseudotyped Human Immunodeficiency Virus Type 1 Particles
Pizzato, M., Popova, E., & Göttlinger, H. (2008) · Journal of Virology · doi:10.1128/jvi.01150-08 · Cited by 36
“Tva is a small type I membrane glycoprotein that is unrelated to CD4 or to other retroviral receptors and binds tightly to the RSV-A glycoprotein EnvA (10, 27).”
Background
Molecular biology of hepatitis C infection
Drazan, K. E. (2000) · Liver Transplantation · doi:10.1053/jlts.2000.6449 · Cited by 32
Retracted
Herpes Simplex Virus DNA Replication and Genome Maturation
Weller, S. K. (2014) · ASM Press eBooks · doi:10.1128/9781555818302.ch14 · Cited by 32
Using the RCAS-TVA System to Model Human Cancer in MicePreprint
Ahronian, L. G., & Lewis, B. C. (2014) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top069831 · Cited by 32
“Expression of either isoform in mammalian cells is sufficient to permit infection by ASLV-A and RCAS viruses (Bates et al. 1993).”
Background
Metabolism Regulates Exposure of Pancreatic Islets to Circulating Molecules In Vivo
Michau, A., Hodson, D. J., Fontanaud, P., Guillou, A., Espinosa-Carrasco, G., Molino, F., Peters, C. J., Robinson, I. C. A. F., Tissier, P. L., Mollard, P., et al. (2015) · Diabetes · doi:10.2337/db15-1168 · Cited by 31
“7-kb rat insulin promoter (RIP) sequence upstream of the TVAIRES-mCherry gene, followed by the 39 untranslated region of the rat prolactin gene (hGH minigene was not used) (22,23), and was microinjected into the pronucleus of fertilized oocytes of superovulated (CBA/Ca 3 C57BL/ 10)F1 mice.”
Method
Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity
Federspiel, M. J. (2019) · Viruses · doi:10.3390/v11060497 · Cited by 31
“Tva proteins are related to low-density lipoprotein receptors (LDLR) and are receptors for ASLV(A) [37,38].”
Background
The Host Cell Sulfonation Pathway Contributes to Retroviral Infection at a Step Coincident with Provirus Establishment
Bruce, J. W., Ahlquist, P., & Young, J. A. T. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000207 · Cited by 31
“To determine if the defect associated with the IM2 cell line is specific for the MLV vector, wild-type CHO-K1 cells and mutant IM2 cells were engineered to express TVA800, the cellular receptor for an avian retrovirus, subgroup A avian sarcoma and leukosis viruses (ASLV-A) [ 45 ,46].”
BackgroundSelf-citation
Animal models of melanoma: a somatic cell gene delivery mouse model allows rapid evaluation of genes implicated in human melanoma
McKinney, A. J., & Holmen, S. L. (2011) · 癌症：英文版 · doi:10.5732/cjc.011.10007 · Cited by 31
A model for studying megakaryocyte development and biology
Murphy, G. J., & Leavitt, A. D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3065 · Cited by 31
A Study of Low pH-Induced Refolding of Env of Avian Sarcoma and Leukosis Virus into a Six-Helix Bundle
Markosyan, R. M., Bates, P. F., Cohen, F., & Melikyan, G. B. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.047696 · Cited by 31
“ASLV-A utilizes a relatively small membrane protein, designated Tva (Bates et al., 1993).”
MethodSelf-citation
A TVA–Single-Chain Antibody Fusion Protein Mediates Specific Targeting of a Subgroup A Avian Leukosis Virus Vector to Cells Expressing a Tumor-Specific Form of Epidermal Growth Factor Receptor
Astrof, S., Niederman, T. M. J., Carter, B. S., Mulligan, R. C., & Young, J. A. T. (2000) · Journal of Virology · doi:10.1128/jvi.74.20.9540-9545.2000 · Cited by 30
“293T-EGFRvIII cells (A through C) and 293T cells (D through F) were incubated with extracellular supernatant that contained (1) or lacked (2) TVAMR1 as indicated.”
BackgroundMethodSelf-citation
Retinoic acid-induced nNOS expression depends on a novel PI3K/Akt/DAX1 pathway in human TGW-nu-I neuroblastoma cells
Nagl, F., Schönhofer, K., Seidler, B., Mages, J., Allescher, H., Schmid, R. M., Schneider, G., & Saur, D. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00034.2009 · Cited by 29
“Bates (4) was cloned 3 of the cytomegalovirus (CMV) promoter of pIRES (Clontech) followed by removal of the IRES cassette and religation of the blunted vector.”
Method
Animal Models of Ovarian Cancer
Connolly, D. C. (2009) · Cancer treatment and research · doi:10.1007/978-0-387-98094-2_17 · Cited by 30
Design of Retroviral Expression Vectors
Comstock, K. E., Watson, N. F., & Olsen, J. C. (2003) · Humana Press eBooks · doi:10.1385/0-89603-480-1:207 · Cited by 29
The WDR11 complex is a receptor for acidic-cluster-containing cargo proteins
Deng, H., Jia, G., Li, P., Tang, Y., Zhao, L., Yang, Q., Zhao, J., Wang, J., Tu, Y., Yong, X., et al. (2024) · Cell · doi:10.1016/j.cell.2024.06.024 · Cited by 30
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
Koslová, A., Trefil, P., Mucksová, J., Krchlíková, V., Plachý, J., Krijt, J., Reinišová, M., Kučerová, D., Geryk, J., Kalina, J., et al. (2021) · Viruses · doi:10.3390/v13122504 · Cited by 28
“We now recognize four receptor proteins that are necessary for the host cell infection by ALV subgroups: Tva protein related to the low-density lipoprotein receptors (LDLR) [2,3], Tvb protein belonging to the tumor necrosis factor receptor family [4–6], Tvc protein similar to mammalian butyrophilins [7], and Tvj, whic…”
Background
Synchronized Retrovirus Fusion in Cells Expressing Alternative Receptor Isoforms Releases the Viral Core into Distinct Sub-cellular Compartments
Padilla‐Parra, S., Marin, M., Kondo, N., & Melikyan, G. B. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002694 · Cited by 28
“Considering that these isoforms have identical ectodomains [13,14] and exhibit a similar glycosylation pattern (data not shown), the difference in fusion efficiency is likely due to the properties of sub-cellular compartments harboring the virus at the time of fusion.”
Background
Genetic Modeling of Glioma Formation in Mice
Begemann, M., Fuller, G. N., & Holland, E. C. (2002) · Brain Pathology · doi:10.1111/j.1750-3639.2002.tb00428.x · Cited by 28
Importance of cysteines in the LDLR-related domain of the subgroup A avian leukosis and sarcoma virus receptor for viral entry
Bélanger, C., Zingler, K., & Young, J. A. T. (1995) · Journal of Virology · doi:10.1128/jvi.69.2.1019-1024.1995 · Cited by 28
“The fact that truncated receptors lacking the N-terminal portion of the LDLR-related domain were functional suggests that amino acid determinants required for subgroup A viral interaction might be contained within the C-terminal end of this domain.”
BackgroundMethodInfluentialSelf-citation
Identification of novel viral receptors with cell line expressing viral receptor-binding protein
Mei, M., Ye, J., Qin, A., Wang, L. Q., Hu, X., Qian, K., & Shao, H. (2015) · Scientific Reports · doi:10.1038/srep07935 · Cited by 27
“As a model system for viral entry, avian sarcoma/leukosis virus (ASLV, including A-J ten subgroups) has been studied intensively, and several important receptors for ASLV entry have been identified by traditional methods [11] [12] [13] [14] [15] .”
Method
Advances on genetic and genomic studies of ALV resistance
Mo, G., Wei, P., Hu, B., Nie, Q., & Zhang, X. (2022) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-022-00769-1 · Cited by 27
“The receptor for subgroup A and K avian leukosis virus The subgroup A avian leukosis virus (ALV-A) enters the cell through the Tva receptor, which belongs to the family of low-density lipoprotein receptors (LDLR) [69].”
Background
Gene transfer into chicken embryos by retrovirus vectors
Iba, H. (2000) · Development Growth & Differentiation · doi:10.1046/j.1440-169x.2000.00504.x · Cited by 27
“Env in subgroup A binds to a receptor that resembles the low-density lipoprotein receptor (LDLR; Bates et al. 1993) and this subgroup is most conveniently used as a vector.”
Sequencing the biology of entry: the retroviral Env gene
Swanstrom, R., Graham, W. D., & Zhou, S. (2017) · Current Topics in Microbiology and Immunology · doi:10.1007/82_2017_35 · Cited by 24
“After an effort of several years the first ALV receptor was cloned for subgroup A viruses and identified as being related to the low density lipoprotein receptor (Bates et al. 1993).”
Background
Cellular Entry of Retroviruses
Lindemann, D., Steffen, I., & Pöhlmann, S. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-7651-1_7 · Cited by 28
LRP1B functions as a receptor for Pseudomonas exotoxin
Pastrana, D. V., Hanson, A. J., Knisely, J. M., Bu, G., & FitzGerald, D. J. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2005.06.007 · Cited by 26
The solution structure of the viral binding domain of Tva, the cellular receptor for subgroup A avian leukosis and sarcoma virus1
Tonelli, M., Peters, R. J., James, T. L., & Agard, D. A. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)03086-1 · Cited by 26
Long-term labeling and imaging of synaptically connected neuronal networks in vivo using double-deletion-mutant rabies viruses
Jin, L., Sullivan, H. A., Zhu, M., Lavin, T. K., Matsuyama, M., Fu, X., Lea, N. E., Xu, R., Hou, Y., Rutigliani, L., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01545-8 · Cited by 30
“We began by making versions of our previously introduced second-generation (∆GL) rabies viral vectors 4 packaged with the avian retroviral envelope protein EnvA, for selective infection of cells engineered to express EnvA’s receptor, referred to as TVA (tumor virus a) 14,15 .”
Method
Intronic deletions of tva receptor gene decrease the susceptibility to infection by avian sarcoma and leukosis virus subgroup A
Chen, W., Liu, Y., Li, H., Chang, S., Shu, D., Zhang, H., Chen, F., & Xie, Q. (2015) · Scientific Reports · doi:10.1038/srep09900 · Cited by 25
Rabies Viral Vectors for Monosynaptic Tracing and Targeted Transgene Expression in NeuronsPreprint
Wickersham, I. R., & Sullivan, H. A. (2015) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot072389 · Cited by 25
“2003) The 293T-TVA800 cell line is derived from 293T and stably expresses the GPI-anchored isoform of TVA, the receptor for EnvA (Bates et al. 1993).”
BackgroundMethod
Lv4 Is a Capsid-Specific Antiviral Activity in Human Blood Cells That Restricts Viruses of the SIVMAC/SIVSM/HIV-2 Lineage Prior to Integration
Pizzato, M., McCauley, S. M., Neagu, M. R., Pertel, T., Firrito, C., Ziglio, S., Dauphin, A., Zufferey, M., Berthoux, L., & Luban, J. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005050 · Cited by 23
“Of these assays, the heterokaryon assay presented in Fig 10 gave us the clearest assessment of heterokaryon transduction efficiency; it exploits the specificity of the ALV/TVA interaction [77], and the clean spectral separation of GFP from the far-red fluorescent protein TagRFP-657 [73].”
Method
The Bipartite Sequence Motif in the N and C Termini of gp85 of Subgroup J Avian Leukosis Virus Plays a Crucial Role in Receptor Binding and Viral Entry
Zhang, Y., Yu, M., Xing, L., Liu, P., Chen, Y., Chang, F., Wang, S., Bao, Y., Farooque, M., Li, X., et al. (2020) · Journal of Virology · doi:10.1128/jvi.01232-20 · Cited by 24
“A receptor for ALV-A and ALV-K has been shown to be related to the low-density lipoprotein receptor called tva (14, 15).”
Background
Viral Membrane Fusion Proteins and RNA Sorting Mechanisms for the Molecular Delivery by Exosomes
Zubarev, I. V., Vladimirtsev, D., Vorontsova, M. V., Blatov, I., Shevchenko, K. G., Zvereva, S. D., Lunev, E. A., Файзулоев, Е. Б., & Barlev, N. (2021) · Cells · doi:10.3390/cells10113043 · Cited by 24
“Hepatitis C virus CD81 tetraspanin, scavenger receptor class B type I (SR-B1) Hepatocytes [106] CD81 increases the progression of prostate cancer [107] High SR-B1 expression is observe in lung adenocarcinoma [108] Rous sarcoma virus Vesicular stomatitis virus Low density lipoprotein receptor (LDLR) Bronchial epithelia…”
Background
Expression and disulfide‐bond connectivity of the second ligand‐binding repeat of the human LDL receptor
Bieri, S., Djordjevic, J. T., Jamshidi, N., Smith, R., & Kroon, P. A. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)00939-7 · Cited by 24
Localization of receptors in lipid rafts can inhibit signal transduction
Lim, K., & Yin, J. (2005) · Biotechnology and Bioengineering · doi:10.1002/bit.20464 · Cited by 24
Cell targeting by murine retroviral vectors
Karavanas, G. (1998) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(98)00007-9 · Cited by 24
Solution Structure of the Viral Receptor Domain of Tva and Its Implications in Viral Entry
Wang, Q.-Y., Huang, W., Dolmer, K., Gettins, P. G. W., & Rong, L. (2002) · Journal of Virology · doi:10.1128/jvi.76.6.2848-2856.2002 · Cited by 24
“Tva is a small membrane-associated glycoprotein (2).”
BackgroundMethodInfluential
The Role of a Conserved Acidic Residue in Calcium-dependent Protein Folding for a Low Density Lipoprotein (LDL)-A Module
Guo, Y. Q., Yu, X., Rihani, K., Wang, Q.-Y., & Rong, L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400157200 · Cited by 24
Targeting Retroviral Vector Infection to Cells That Express Heregulin Receptors Using a TVA–Heregulin Bridge Protein
Astrof, S., & Young, J. A. T. (2002) · Virology · doi:10.1006/viro.2001.1314 · Cited by 24
“1A), most probably because its TVA domain is extensively modified posttranslationally (Bates et al., 1993).”
BackgroundSelf-citation
Avian Leucosis Virus-Host Interaction: The Involvement of Host Factors in Viral Replication
Tang, S., Li, J., Chang, Y., & Lin, W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.907287 · Cited by 23
“Tva protein is the receptor shared by the ALV-A and ALV-K, possessing high homology with the ligand-binding region of the human low-density lipoprotein receptors (LDLR) (12, 13).”
Background
pH regulation in early endosomes and interferon-inducible transmembrane proteins control avian retrovirus fusion
Desai, T. M., Marin, M., Mason, C., & Melikyan, G. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.783878 · Cited by 21
“We applied the above time-of-addition strategy to examine the progression of ASLV pseudoviral particle (ASLVpp) fusion with CV-1-derived cells expressing either the full-length (TVA950) or the GPI-anchored (TVA800) TVA receptor (48, 49).”
Method

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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