Home LiteratureArticle Details
PMID: 1850020 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Mechanism of leukemogenesis induced by mink cell focus-forming murine leukemia viruses.

Journal of virology ·Vol. 65 ·No. 5 ·1991-05-00 ·Pages 2408-14

Li JP, Baltimore D

Abstract

The Friend or Moloney mink cell focus-forming (MCF) virus encodes a recombinant-type envelope glycoprotein, gp70, that is closely related to the membrane glycoprotein, gp55, of Friend spleen focus-forming virus (SFFV). We have shown previously that gp55 has the ability to activate cell growth by binding to the cellular receptor for erythropoietin. Here we show that gp70 encoded by either the Friend or Moloney MCF virus also binds to the erythropoietin receptor and that coexpression of the receptor and gp70 in an interleukin-3 (IL-3)-dependent cell line can activate IL-3-independent growth. Furthermore, when the cDNA for the human IL-2 receptor beta chain, which is related by sequence to the erythropoietin receptor, was introduced into this cell line, it became growth factor independent after infection either with SFFV or with one of the two MCF viruses but not with an ecotropic virus. Based on these observations, we propose a mechanism for the early stage of leukemogenesis induced by the MCF-type murine leukemia viruses.

MeSH Terms
Animals Cell Division Cell Line Cell Transformation, Neoplastic Cell Transformation, Viral Electrophoresis, Polyacrylamide Gel Erythropoietin/metabolism Friend murine leukemia virus/metabolism,physiology Humans Interleukin-3/pharmacology Leukemia/microbiology Mice Mink Cell Focus-Inducing Viruses/metabolism,physiology Moloney murine leukemia virus/metabolism,physiology Receptors, Cell Surface/metabolism Receptors, Erythropoietin Receptors, Interleukin-2/metabolism Retroviridae Proteins, Oncogenic/metabolism Viral Envelope Proteins/metabolism
Chemicals
Interleukin-3 Receptors, Cell Surface Receptors, Erythropoietin Receptors, Interleukin-2 Retroviridae Proteins, Oncogenic Viral Envelope Proteins Erythropoietin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Li J P
Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02142.
Baltimore D
References (60)
60 references, click to expand
  1. Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia.
    J Exp Med. 1957 Apr 1;105(4):307-18 PMID: 13416470
  2. Different recombinant murine leukemia viruses use different cell surface receptors.
    Virology. 1984 Jul 15;136(1):144-52 PMID: 6330990
  3. Erythropoietin receptor and interleukin-2 receptor beta chain: a new receptor family.
    Cell. 1989 Sep 22;58(6):1023-4 PMID: 2550142
  4. Spi-1 is a putative oncogene in virally induced murine erythroleukaemias.
    Nature. 1988 Jan 21;331(6153):277-80 PMID: 2827041
  5. An enhancer sequence instability that diversifies the cell repertoire for expression of a murine leukemia virus.
    Virology. 1988 Jun;164(2):350-61 PMID: 2835856
  6. Overcoming interference to retroviral superinfection results in amplified expression and transmission of cloned genes.
    Proc Natl Acad Sci U S A. 1988 Aug;85(15):5404-8 PMID: 2840658
  7. Specific hybridization probes demonstrate fewer xenotropic than mink cell focus-forming murine leukemia virus env-related sequences in DNAs from inbred laboratory mice.
    J Virol. 1986 May;58(2):359-66 PMID: 3009853
  8. Abelson virus abrogation of interleukin-3 dependence in a lymphoid cell line.
    Mol Cell Biol. 1986 Nov;6(11):4133-5 PMID: 3025637
  9. Role of a membrane glycoprotein in Friend virus erythroleukemia: nucleotide sequences of nonleukemogenic mutant and spontaneous revertant viruses.
    J Virol. 1986 Feb;57(2):534-8 PMID: 3003385
  10. The membrane glycoprotein of Friend spleen focus-forming virus: evidence that the cell surface component is required for pathogenesis and that it binds to a receptor.
    J Virol. 1987 Sep;61(9):2782-92 PMID: 3039169
  11. The four classes of endogenous murine leukemia virus: structural relationships and potential for recombination.
    J Virol. 1987 Sep;61(9):2659-69 PMID: 3039159
  12. Sequences responsible for erythroid and lymphoid leukemia in the long terminal repeats of Friend-mink cell focus-forming and Moloney murine leukemia viruses.
    J Virol. 1987 Jun;61(6):1861-6 PMID: 3033317
  13. Different murine cell lines manifest unique patterns of interference to superinfection by murine leukemia viruses.
    Virology. 1985 Feb;141(1):119-29 PMID: 2983494
  14. A restricted cytoplasmic region of IL-2 receptor beta chain is essential for growth signal transduction but not for ligand binding and internalization.
    Cell. 1989 Dec 1;59(5):837-45 PMID: 2590941
  15. Distinct segments within the enhancer region collaborate to specify the type of leukemia induced by nondefective Friend and Moloney viruses.
    J Virol. 1989 Jan;63(1):328-37 PMID: 2783259
  16. Interleukin-2 receptor beta chain gene: generation of three receptor forms by cloned human alpha and beta chain cDNA's.
    Science. 1989 May 5;244(4904):551-6 PMID: 2785715
  17. Tissue-specific transcription preference as a determinant of cell tropism and leukaemogenic potential of murine retroviruses.
    Nature. 1984 Nov 8-14;312(5990):159-62 PMID: 6095084
  18. A 3' end fragment encompassing the transcriptional enhancers of nondefective Friend virus confers erythroleukemogenicity on Moloney leukemia virus.
    J Virol. 1984 Oct;52(1):248-54 PMID: 6090701
  19. Disease specificity of nondefective Friend and Moloney murine leukemia viruses is controlled by a small number of nucleotides.
    J Virol. 1987 Mar;61(3):693-700 PMID: 3468264
  20. Envelope gene and long terminal repeat determine the different biological properties of Rauscher, Friend, and Moloney mink cell focus-inducing viruses.
    J Virol. 1985 Jul;55(1):184-92 PMID: 4009793
  21. Murine interleukin 2 receptor beta chain: dysregulated gene expression in lymphoma line EL-4 caused by a promoter insertion.
    Proc Natl Acad Sci U S A. 1990 Mar;87(5):1806-10 PMID: 2155425
  22. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor.
    Nature. 1990 Feb 22;343(6260):762-4 PMID: 2154701
  23. Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA.
    J Virol. 1982 Oct;44(1):19-31 PMID: 7143566
  24. Proviruses are adjacent to c-myc in some murine leukemia virus-induced lymphomas.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):2097-101 PMID: 6326104
  25. Envelope gene of the Friend spleen focus-forming virus: deletion and insertions in 3' gp70/p15E-encoding region have resulted in unique features in the primary structure of its protein product.
    Proc Natl Acad Sci U S A. 1983 Aug;80(15):4718-22 PMID: 6308646
  26. Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion.
    Cell. 1984 May;37(1):113-22 PMID: 6327047
  27. Leukemia induction by a new strain of Friend mink cell focus-inducing virus: synergistic effect of Friend ecotropic murine leukemia virus.
    J Virol. 1984 Jul;51(1):63-70 PMID: 6202886
  28. Monoclonal antibody to spleen focus-forming virus-encoded gp52 provides a probe for the amino-terminal region of retroviral envelope proteins that confers dual tropism and xenotropism.
    J Virol. 1982 Aug;43(2):472-81 PMID: 6180179
  29. Role of endogenous murine leukemia virus in immunologically triggered lymphoreticular tumors. II. Isolation of B-tropic mink cell focus-inducing (MCF) murine leukemia virus.
    Virology. 1980 Jul 15;104(1):164-73 PMID: 6156538
  30. Loss of leukemogenicity caused by mutations in the membrane glycoprotein structural gene of Friend spleen focus-forming virus.
    Proc Natl Acad Sci U S A. 1983 Aug;80(15):4704-8 PMID: 6308644
  31. Role for the 3' end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4408-11 PMID: 6308622
  32. Friend murine leukemia virus-induced leukemia is associated with the formation of mink cell focus-inducing viruses and is blocked in mice expressing endogenous mink cell focus-inducing xenotropic viral envelope genes.
    J Exp Med. 1981 Sep 1;154(3):907-20 PMID: 6268733
  33. Cloning and characterization of an envelope-specific probe from xenotropic murine leukemia proviral DNA.
    J Virol. 1982 Jan;41(1):228-36 PMID: 6283115
  34. Rapid emergence of mink cell focus-forming (MCF) virus in various mice infected with NB-tropic friend virus.
    Virology. 1981 Sep;113(2):644-55 PMID: 6267802
  35. Biological activity of the spleen focus-forming virus is encoded by a molecularly cloned subgenomic fragment of spleen focus-forming virus DNA.
    Proc Natl Acad Sci U S A. 1981 Mar;78(3):1401-5 PMID: 6262795
  36. Nucleotide sequence of the 3' end of MCF 247 murine leukemia virus.
    J Virol. 1983 Jan;45(1):291-8 PMID: 6296437
  37. Lymphomagenicity of recombinant mink cell focus-inducing murine leukemia viruses.
    J Exp Med. 1980 Mar 1;151(3):542-52 PMID: 6244357
  38. Non-thymic malignant lymphomas induced in C57BL/6 mice by cloned dualtropic viruses isolated from hematopoietic stromal cell lines.
    Eur J Cancer. 1980 Jul;16(7):909-17 PMID: 6253301
  39. Recovery of biologically active spleen focus-forming virus from molecularly cloned spleen focus-forming virus-pBR322 circular DNA by cotransfection with infectious type C retroviral DNA.
    J Virol. 1980 Sep;35(3):710-21 PMID: 6252333
  40. Complete nucleotide sequence of an infectious clone of Friend spleen focus-forming provirus: gp55 is an envelope fusion glycoprotein.
    Proc Natl Acad Sci U S A. 1983 Aug;80(16):5037-41 PMID: 6576374
  41. Chromosomal mapping of the mink cell focus-inducing and xenotropic env gene family in the mouse.
    Proc Natl Acad Sci U S A. 1983 Oct;80(20):6298-302 PMID: 6578510
  42. Rauscher "mink cell focus-inducing" (MCF) virus causes erythroleukemia in mice: its isolation and properties.
    Virology. 1980 Mar;101(2):376-88 PMID: 6928730
  43. Heterogeneous metabolism and subcellular localization of a potentially leukemogenic membrane glycoprotein encoded by Friend erythroleukemia virus. Isolation of viral and cellular processing mutants.
    J Biol Chem. 1982 Jan 10;257(1):126-34 PMID: 7053362
  44. Expression of leukemogenic recombinant viruses associated with a recessive gene in HRS/J mice.
    J Exp Med. 1980 Aug 1;152(2):249-64 PMID: 7400758
  45. AKR leukemogenesis: identification and biological significance of thymic lymphoma receptors for AKR retroviruses.
    Cell. 1979 May;17(1):65-75 PMID: 222476
  46. Properties of "mink cell focus-inducing" (MCF) virus isolated from spontaneous lymphoma lines of BALB/c mice carrying Moloney leukemia virus as an endogenous virus.
    Virology. 1979 Feb;93(1):226-36 PMID: 219598
  47. Helper-independent mink cell focus-inducing strains of Friend murine type-C virus: potential relationship to the origin of replication-defective spleen focus-forming virus.
    J Exp Med. 1978 Sep 1;148(3):639-53 PMID: 212504
  48. Biological, immunological, and biochemical evidence that HIX virus is a recombinant between Moloney leukemia virus and a murine xenotropic C type virus.
    Virology. 1978 Oct 15;90(2):241-54 PMID: 214945
  49. Biochemical evidence that MCF murine leukemia viruses are envelope (env) gene recombinants.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4676-80 PMID: 200928
  50. Friend strain of spleen focus-forming virus is a recombinant between ecotropic murine type C virus and the env gene region of xenotropic type C virus.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4671-5 PMID: 200927
  51. Identification of virus found in mouse lymphomas induced by HIX murine oncornavirus.
    J Virol. 1978 May;26(2):532-5 PMID: 207900
  52. Isolation of a fibroblast nonproducer cell line containing the Friend strain of the spleen focus-forming virus.
    Virology. 1977 Feb;76(2):602-15 PMID: 190768
  53. A new class of murine leukemia virus associated with development of spontaneous lymphomas.
    Proc Natl Acad Sci U S A. 1977 Feb;74(2):789-92 PMID: 191826
  54. Molecular analysis of the envelope gene and long terminal repeat of Friend mink cell focus-inducing virus: implications for the functions of these sequences.
    J Virol. 1984 Mar;49(3):828-40 PMID: 6321768
  55. Characterization of the env gene and long terminal repeat of molecularly cloned Friend mink cell focus-inducing virus DNA.
    J Virol. 1984 Jun;50(3):813-21 PMID: 6328011
  56. Complete nucleotide sequence of the gene for the specific glycoprotein (gp55) of Friend spleen focus-forming virus.
    Proc Natl Acad Sci U S A. 1983 Jul;80(13):3913-7 PMID: 6306650
  57. A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas.
    Nature. 1983 Mar 31-Apr 6;302(5907):445-9 PMID: 6300684
  58. The envelope gene and long terminal repeat sequences contribute to the pathogenic phenotype of helper-independent Friend viruses.
    J Virol. 1984 Sep;51(3):788-94 PMID: 6088801
  59. Molecular cloning of biologically active Rauscher spleen focus-forming virus and the sequences of its env gene and long terminal repeat.
    J Virol. 1984 Sep;51(3):695-705 PMID: 6088793
  60. Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6460-4 PMID: 3413107
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/JVI.65.5.2408-2414.1991
Published
1991-05-00
Pages
2408-14
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC240593
Subset
IM
Grants
NIAID NIH HHS · AI 22346 · United States
External Links
PubMed source DOI: 10.1128/JVI.65.5.2408-2414.1991 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2