Activation of Erythropoietin Receptors by Friend Viral Gp55 and by Erythropoietin and Down-modulation by the Murine Fv-2r Resistance Gene

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1990 Dec 1

PMID 2175917

Citations 33

Authors

M E Hoatlin

S L Kozak

F Lilly

A Chakraborti

C A Kozak

D Kabat

Affiliations

Soon will be listed here.

Abstract

The leukemogenic membrane glycoprotein (gp55) encoded by Friend spleen focus-forming virus appears to bind to erythropoietin receptors (EpoR) sto stimulate erythroblastosis [Li, J.-P., D'Andrea, A.D., Lodish, H.F. & Baltimore, D. (1990) Nature (London) 343, 762-764]. To directly compare the effects of gp55 with erythropoietin (Epo), we produced retrovirions that encode either gp55, Epo, or EpoR. After infection with EpoR virus, interleukin 3-dependent DA-3 cells bound 125I-labeled Epo and grew without interleukin 3 in the presence of Epo. These latter cells, but not parental DA-3 cells, became factor-independent after superinfection either with Epo virus or with Friend spleen focus-forming virus. In addition, Epo virus caused a disease in mice that mimicked Friend erythroleukemia. Although Fv-2r homozygotes are susceptible to all other retroviral diseases, they are resistant to both Epo viral and Friend viral erythroleukemias. These results indicate that both gp55 and Epo stimulate EpoR and that the Fv-2 gene encodes a protein that controls response to these ligands. However, the Fv-2 protein is not EpoR because the corresponding genes map to opposite ends of mouse chromosome 9. These results have important implications for understanding signal transduction by EpoR and the role of host genetic variation in controlling susceptibility to an oncogenic protein.

Citing Articles

Reassessment of murine APOBEC1 as a retrovirus restriction factor in vivo.

Barrett B, Guo K, Harper M, Li S, Heilman K, Davidson N Virology. 2014; 468-470:601-608.

PMID: 25303118 PMC: 4430097. DOI: 10.1016/j.virol.2014.09.006.

Friend Spleen Focus-Forming Virus Activates the Tyrosine Kinase sf-Stk and the Transcription Factor PU.1 to Cause a Multi-Stage Erythroleukemia in Mice.

Cmarik J, Ruscetti S Viruses. 2011; 2(10):2235-2257.

PMID: 21994618 PMC: 3185572. DOI: 10.3390/v2102235.

Effects of type I interferons on Friend retrovirus infection.

Gerlach N, Schimmer S, Weiss S, Kalinke U, Dittmer U J Virol. 2006; 80(7):3438-44.

PMID: 16537611 PMC: 1440373. DOI: 10.1128/JVI.80.7.3438-3444.2006.

Helix packing and orientation in the transmembrane dimer of gp55-P of the spleen focus forming virus.

Liu W, Crocker E, Constantinescu S, Smith S Biophys J. 2005; 89(2):1194-202.

PMID: 15894629 PMC: 1366604. DOI: 10.1529/biophysj.104.057844.

Analysis of integration sites of Jaagsiekte sheep retrovirus in ovine pulmonary adenocarcinoma.

Cousens C, Bishop J, Philbey A, Gill C, Palmarini M, Carlson J J Virol. 2004; 78(16):8506-12.

PMID: 15280459 PMC: 479065. DOI: 10.1128/JVI.78.16.8506-8512.2004.

References

Egrie J, COTES P, Lane J, Gaines Das R, Tam R . Development of radioimmunoassays for human erythropoietin using recombinant erythropoietin as tracer and immunogen. J Immunol Methods. 1987; 99(2):235-41. DOI: 10.1016/0022-1759(87)90133-5. View

Holt C, Osorio K, Lilly F . Friend virus-specific cytotoxic T lymphocytes recognize both gag and env gene-encoded specificities. J Exp Med. 1986; 164(1):211-26. PMC: 2188214. DOI: 10.1084/jem.164.1.211. View

HOGGAN M, Halden N, Buckler C, Kozak C . Genetic mapping of the mouse c-fms proto-oncogene to chromosome 18. J Virol. 1988; 62(3):1055-6. PMC: 253666. DOI: 10.1128/JVI.62.3.1055-1056.1988. View

Del Rizzo D, Eskinazi D, AXELRAD A . Negative regulation of DNA synthesis in early erythropoietic progenitor cells (BFU-E) by a protein purified from the medium of C57BL/6 mouse marrow cells. Proc Natl Acad Sci U S A. 1988; 85(12):4320-4. PMC: 280420. DOI: 10.1073/pnas.85.12.4320. View

Bestwick R, Kozak S, Kabat D . Overcoming interference to retroviral superinfection results in amplified expression and transmission of cloned genes. Proc Natl Acad Sci U S A. 1988; 85(15):5404-8. PMC: 281765. DOI: 10.1073/pnas.85.15.5404. View

Semenza G, Traystman M, Gearhart J, Antonarakis S . Polycythemia in transgenic mice expressing the human erythropoietin gene. Proc Natl Acad Sci U S A. 1989; 86(7):2301-5. PMC: 286900. DOI: 10.1073/pnas.86.7.2301. View

DAndrea A, Lodish H, Wong G . Expression cloning of the murine erythropoietin receptor. Cell. 1989; 57(2):277-85. DOI: 10.1016/0092-8674(89)90965-3. View

Gliniak B, Kabat D . Leukemogenic membrane glycoprotein encoded by Friend spleen focus-forming virus: transport to cell surfaces and shedding are controlled by disulfide-bonded dimerization and by cleavage of a hydrophobic membrane anchor. J Virol. 1989; 63(9):3561-8. PMC: 250945. DOI: 10.1128/JVI.63.9.3561-3568.1989. View

Kabat D . Molecular biology of Friend viral erythroleukemia. Curr Top Microbiol Immunol. 1989; 148:1-42. DOI: 10.1007/978-3-642-74700-7_1. View

10.

Geib R, Seaward M, Stevens M, Cho C, Majumdar M . RB virus: a strain of Friend virus that produces a 'Friend virus-like' disease in Fv-2rr mice. Virus Res. 1989; 14(2):161-73. DOI: 10.1016/0168-1702(89)90036-1. View

11.

Frank S, Taylor B, Lusis A . Linkage of the mouse LDL receptor gene on chromosome 9. Genomics. 1989; 5(3):646-8. DOI: 10.1016/0888-7543(89)90037-2. View

12.

Ruscetti S, Janesch N, Chakraborti A, Sawyer S, HANKINS W . Friend spleen focus-forming virus induces factor independence in an erythropoietin-dependent erythroleukemia cell line. J Virol. 1990; 64(3):1057-62. PMC: 249217. DOI: 10.1128/JVI.64.3.1057-1062.1990. View

13.

Li J, DAndrea A, Lodish H, Baltimore D . Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature. 1990; 343(6260):762-4. DOI: 10.1038/343762a0. View

14.

Kozak S, Kabat D . Ping-pong amplification of a retroviral vector achieves high-level gene expression: human growth hormone production. J Virol. 1990; 64(7):3500-8. PMC: 249616. DOI: 10.1128/JVI.64.7.3500-3508.1990. View

15.

Miller D, Adam M, Miller A . Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol Cell Biol. 1990; 10(8):4239-42. PMC: 360961. DOI: 10.1128/mcb.10.8.4239-4242.1990. View

16.

AXELRAD A, STEEVES R . ASSAY FOR FRIEND LEUKEMIA VIRUS: RAPID QUANTITATIVE METHOD BASED ON ENUMERATION OF MACROSCOPIC SPLEEN FOCI IN MICE. Virology. 1964; 24:513-8. DOI: 10.1016/0042-6822(64)90199-0. View

17.

Lilly F . Fv-2: identification and location of a second gene governing the spleen focus response to Friend leukemia virus in mice. J Natl Cancer Inst. 1970; 45(1):163-9. View

18.

Paskind M, Weinberg R, Baltimore D . Dependence of Moloney murine leukemia virus production on cell growth. Virology. 1975; 67(1):242-8. DOI: 10.1016/0042-6822(75)90421-3. View

19.

Sherton C, Evans L, Polonoff E, Kabat D . Relationship of Friend murine leukemia virus production to growth and hemoglobin synthesis in cultured erythroleukemia cells. J Virol. 1976; 19(1):118-25. PMC: 354838. DOI: 10.1128/JVI.19.1.118-125.1976. View

20.

Steeves R, Lilly F . Interactions between host and viral genomes in mouse leukemia. Annu Rev Genet. 1977; 11:277-96. DOI: 10.1146/annurev.ge.11.120177.001425. View