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. 1984 Jul;51(1):63–70. doi: 10.1128/jvi.51.1.63-70.1984

Leukemia induction by a new strain of Friend mink cell focus-inducing virus: synergistic effect of Friend ecotropic murine leukemia virus.

B Chesebro, K Wehrly, J Nishio, L Evans
PMCID: PMC254400  PMID: 6202886

Abstract

A new strain of Friend recombinant mink cell focus-inducing retrovirus, FMCF -1-E, was found to induce leukemias in NFS and IRW mice. Although the isolate was obtained from a stock of FMCF -1 ( Troxler et al., J. Exp. Med. 148:639-653, 1978), FMCF -1-E was distinguishable from FMCF -1 by oligonucleotide fingerprinting and antigenic analysis, using monoclonal antibodies. These analyses suggested that FMCF -1-E is a distinct FMCF isolate rather than a simple variant of FMCF -1. After neonatal inoculation, the latency for leukemia induction was 3 to 8 months. A similar long latency was also seen when Friend murine leukemia virus 57 was inoculated into adult (6-week-old) IRW mice. However, sequential inoculation of FMCF -1-E at birth followed by Friend murine leukemia 57 at 6 weeks of age led to a shortened latency period (2.5 to 4 months). Only neonatal inoculation of Friend murine leukemia virus 57 was able to induce a more rapid appearance of leukemia. The leukemia cell type in the majority of cases, regardless of virus inoculation protocol, was erythroid, but occasional myeloid, lymphoid, and mixed leukemias were also observed. In contrast to NFS and IRW mice, BALB/c mice were resistant to leukemia induction by FMCF -1-E and also showed some transient resistance to leukemia induction by Friend murine leukemia virus 57.

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Selected References

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  1. Besmer P., Baltimore D. Mechanism of restriction of ecotropic and xenotropic murine leukemia viruses and formation of pseudotypes between the two viruses. J Virol. 1977 Mar;21(3):965–973. doi: 10.1128/jvi.21.3.965-973.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chatis P. A., Holland C. A., Hartley J. W., Rowe W. P., Hopkins N. 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):4408–4411. doi: 10.1073/pnas.80.14.4408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chattopadhyay S. K., Cloyd M. W., Linemeyer D. L., Lander M. R., Rands E., Lowy D. R. Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas. Nature. 1982 Jan 7;295(5844):25–31. doi: 10.1038/295025a0. [DOI] [PubMed] [Google Scholar]
  4. Chattopadhyay S. K., Lander M. R., Gupta S., Rands E., Lowy D. R. Origin of mink cytopathic focus-forming (MCF) viruses:comparison with ecotropic and xenotropic murine leukemia virus genomes. Virology. 1981 Sep;113(2):465–483. doi: 10.1016/0042-6822(81)90175-6. [DOI] [PubMed] [Google Scholar]
  5. Chesebro B., Britt W., Evans L., Wehrly K., Nishio J., Cloyd M. Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of friend MCF and Friend ecotropic murine leukemia virus. Virology. 1983 May;127(1):134–148. doi: 10.1016/0042-6822(83)90378-1. [DOI] [PubMed] [Google Scholar]
  6. Chesebro B., Portis J. L., Wehrly K., Nishio J. Effect of murine host genotype on MCF virus expression, latency, and leukemia cell type of leukemias induced by Friend murine leukemia helper virus. Virology. 1983 Jul 15;128(1):221–233. doi: 10.1016/0042-6822(83)90332-x. [DOI] [PubMed] [Google Scholar]
  7. Chesebro B., Wehrly K., Cloyd M., Britt W., Portis J., Collins J., Nishio J. Characterization of mouse monoclonal antibodies specific for Friend murine leukemia virus-induced erythroleukemia cells: friend-specific and FMR-specific antigens. Virology. 1981 Jul 15;112(1):131–144. doi: 10.1016/0042-6822(81)90619-x. [DOI] [PubMed] [Google Scholar]
  8. Chesebro B., Wehrly K., Stimpfling J. Host genetic control of recovery from Friend leukemia virus-induced splenomegaly: mapping of a gene within the major histocompatability complex. J Exp Med. 1974 Dec 1;140(6):1457–1467. doi: 10.1084/jem.140.6.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chien Y. H., Verma I. M., Shih T. Y., Scolnick E. M., Davidson N. Heteroduplex analysis of the sequence relations between the RNAs of mink cell focus-inducing and murine leukemia viruses. J Virol. 1978 Oct;28(1):352–360. doi: 10.1128/jvi.28.1.352-360.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cloyd M. W., Hartley J. W., Rowe W. P. Genetic study of lymphoma induction by AKR mink cell focus-inducing virus in AKR x NFS crosses. J Exp Med. 1981 Aug 1;154(2):450–457. doi: 10.1084/jem.154.2.450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cloyd M. W., Hartley J. W., Rowe W. P. Lymphomagenicity of recombinant mink cell focus-inducing murine leukemia viruses. J Exp Med. 1980 Mar 1;151(3):542–552. doi: 10.1084/jem.151.3.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DesGroseillers L., Rassart E., Jolicoeur P. Thymotropism of murine leukemia virus is conferred by its long terminal repeat. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4203–4207. doi: 10.1073/pnas.80.14.4203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans L. H., Britt W. J. An immunological focus assay for murine leukemia viruses on viable attached cell lines. Virology. 1983 Aug;129(1):212–217. doi: 10.1016/0042-6822(83)90408-7. [DOI] [PubMed] [Google Scholar]
  14. Evans L. H., Cloyd M. W. Generation of mink cell focus-forming viruses by Friend murine leukemia virus: recombination with specific endogenous proviral sequences. J Virol. 1984 Mar;49(3):772–781. doi: 10.1128/jvi.49.3.772-781.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Evans L., Nunn M., Duesberg P. H., Troxler D., Scolnick E. RNAs of defective and nondefective components of Friend anemia and polycythemia virus strains identified and compared. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):823–835. doi: 10.1101/sqb.1980.044.01.087. [DOI] [PubMed] [Google Scholar]
  16. Faller D. V., Hopkins N. T1 oligonucleotide maps of Moloney and HIX murine leukemia viruses. Virology. 1978 Oct 15;90(2):265–273. doi: 10.1016/0042-6822(78)90310-0. [DOI] [PubMed] [Google Scholar]
  17. Fischinger P. J., Ihle J. N., de Noronha F., Bolognesi D. P. Oncogenic and immunogenic potential of cloned HIX virus in mice and cats. Med Microbiol Immunol. 1977;164(1-3):119–129. doi: 10.1007/BF02121308. [DOI] [PubMed] [Google Scholar]
  18. Fischinger P. J., Nomura S., Bolognesi D. P. A novel murine oncornavirus with dual eco- and xenotropic properties. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5150–5155. doi: 10.1073/pnas.72.12.5150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gilden R. V., Rabin H. Mechanisms of viral tumorigenesis. Adv Virus Res. 1982;27:281–334. doi: 10.1016/s0065-3527(08)60437-6. [DOI] [PubMed] [Google Scholar]
  20. Gisselbrecht S., Fischinger P. J., Elder J. H., Levy J. P. Isolation of two novel envelope recombinant leukemogenic viruses from Moloney leukemia virus stocks. Int J Cancer. 1981;27(4):531–536. doi: 10.1002/ijc.2910270417. [DOI] [PubMed] [Google Scholar]
  21. Green N., Hiai H., Elder J. H., Schwartz R. S., Khiroya R. H., Thomas C. Y., Tsichlis P. N., Coffin J. M. Expression of leukemogenic recombinant viruses associated with a recessive gene in HRS/J mice. J Exp Med. 1980 Aug 1;152(2):249–264. doi: 10.1084/jem.152.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hartley J. W., Rowe W. P. Clonal cells lines from a feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology. 1975 May;65(1):128–134. doi: 10.1016/0042-6822(75)90013-6. [DOI] [PubMed] [Google Scholar]
  23. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Henderson I. C., Lieber M. M., Todaro G. J. Mink cell line Mv 1 Lu (CCL 64). Focus formation and the generation of "nonproducer" transformed cell lines with murine and feline sarcoma viruses. Virology. 1974 Jul;60(1):282–287. doi: 10.1016/0042-6822(74)90386-9. [DOI] [PubMed] [Google Scholar]
  25. Ishimoto A., Adachi A., Sakai K., Yorifuji T., Tsuruta S. Rapid emergence of mink cell focus-forming (MCF) virus in various mice infected with NB-tropic friend virus. Virology. 1981 Sep;113(2):644–655. doi: 10.1016/0042-6822(81)90193-8. [DOI] [PubMed] [Google Scholar]
  26. Ishimoto A., Hartley J. W., Rowe W. P. Detection and quantitation of phenotypically mixed viruses: mixing of ecotropic and xenotropic murine leukemia viruses. Virology. 1977 Sep;81(2):263–269. doi: 10.1016/0042-6822(77)90143-x. [DOI] [PubMed] [Google Scholar]
  27. Koch W., Hunsmann G., Friedrich R. Nucleotide sequence of the envelope gene of Friend murine leukemia virus. J Virol. 1983 Jan;45(1):1–9. doi: 10.1128/jvi.45.1.1-9.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lung M. L., Hartley J. W., Rowe W. P., Hopkins N. H. Large RNase T1-resistant oligonucleotides encoding p15E and the U3 region of the long terminal repeat distinguish two biological classes of mink cell focus-forming type C viruses of inbred mice. J Virol. 1983 Jan;45(1):275–290. doi: 10.1128/jvi.45.1.275-290.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. MacDonald M. E., Mak T. W., Bernstein A. Erythroleukemia induction by replication-competent type C viruses cloned from the anemia- and polycythemia-inducing isolates of Friend leukemia virus. J Exp Med. 1980 Jun 1;151(6):1493–1503. doi: 10.1084/jem.151.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Donnell P. V., Stockert E., Obata Y., Old L. J. Leukemogenic properties of AKR dualtropic (MCF) viruses: amplification of murine leukemia virus-related antigens on thymocytes and acceleration of leukemia development in AKR mice. Virology. 1981 Jul 30;112(2):548–563. doi: 10.1016/0042-6822(81)90301-9. [DOI] [PubMed] [Google Scholar]
  31. Oliff A. I., Hager G. L., Chang E. H., Scolnick E. M., Chan H. W., Lowy D. R. Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol. 1980 Jan;33(1):475–486. doi: 10.1128/jvi.33.1.475-486.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Oliff A., Ruscetti S. A 2.4-kilobase-pair fragment of the Friend murine leukemia virus genome contains the sequences responsible for friend murine leukemia virus-induced erythroleukemia. J Virol. 1983 Jun;46(3):718–725. doi: 10.1128/jvi.46.3.718-725.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Oliff A., Ruscetti S., Douglass E. C., Scolnick E. Isolation of transplantable erythroleukemia cells from mice infected with helper-independent Friend murine leukemia virus. Blood. 1981 Aug;58(2):244–254. [PubMed] [Google Scholar]
  34. Portis J. L., McAtee F. J., Cloyd M. W. Monoclonal antibodies to xenotropic and MCF murine leukemia viruses derived during the graft-versus-host reaction. Virology. 1982 Apr 15;118(1):181–190. doi: 10.1016/0042-6822(82)90331-2. [DOI] [PubMed] [Google Scholar]
  35. Portis J. L., McAtee F. J. Monoclonal antibodies derived during graft-versus-host reaction. II. Antibodies detect unique determinants common to many MCF viruses. Virology. 1983 Apr 15;126(1):96–105. doi: 10.1016/0042-6822(83)90464-6. [DOI] [PubMed] [Google Scholar]
  36. Robinson H. L., Blais B. M., Tsichlis P. N., Coffin J. M. At least two regions of the viral genome determine the oncogenic potential of avian leukosis viruses. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1225–1229. doi: 10.1073/pnas.79.4.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rommelaere J., Faller D. V., Hopkins N. Characterization and mapping of RNase T1-resistant oligonucleotides derived from the genomes of Akv and MCF murine leukemia viruses. Proc Natl Acad Sci U S A. 1978 Jan;75(1):495–499. doi: 10.1073/pnas.75.1.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rowe W. P., Pugh W. E., Hartley J. W. Plaque assay techniques for murine leukemia viruses. Virology. 1970 Dec;42(4):1136–1139. doi: 10.1016/0042-6822(70)90362-4. [DOI] [PubMed] [Google Scholar]
  39. Ruscetti S., Feild J., Davis L., Oliff A. Factors determining the susceptibility of NIH swiss mice to erythroleukemia induced by Friend murine leukemia virus. Virology. 1982 Mar;117(2):357–365. doi: 10.1016/0042-6822(82)90475-5. [DOI] [PubMed] [Google Scholar]
  40. Shibuya T., Mak T. W. Host control of susceptibility to erythroleukemia and to the types of leukemia induced by Friend murine leukemia virus: initial and late stages. Cell. 1982 Dec;31(2 Pt 1):483–493. doi: 10.1016/0092-8674(82)90141-6. [DOI] [PubMed] [Google Scholar]
  41. Shih T. Y., Weeks M. O., Troxler D. H., Coffin J. M., Scolnick E. M. Mapping host range-specific oligonucleotides within genomes of the ecotropic and mink cell focus-inducing strains of Moloney murine leukemia virus. J Virol. 1978 Apr;26(1):71–83. doi: 10.1128/jvi.26.1.71-83.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Silver J. E., Fredrickson T. N. A new gene that controls the type of leukemia induced by Friend murine leukemia virus. J Exp Med. 1983 Aug 1;158(2):493–505. doi: 10.1084/jem.158.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Steeves R. A., Eckner R. J., Bennett M., Mirand E. A., Trudel P. J. Isolation and characterization of a lymphatic leukemia virus in the Friend virus complex. J Natl Cancer Inst. 1971 Jun;46(6):1209–1217. [PubMed] [Google Scholar]
  44. Troxler D. H., Parks W. P., Vass W. C., Scolnick E. M. Isolation of a fibroblast nonproducer cell line containing the Friend strain of the spleen focus-forming virus. Virology. 1977 Feb;76(2):602–615. doi: 10.1016/0042-6822(77)90242-2. [DOI] [PubMed] [Google Scholar]
  45. Troxler D. H., Scolnick E. M. Rapid leukemia induced by cloned friend strain of replicating murine type-C virus. Association with induction of xenotropic-related RNA sequences contained in spleen focus-forming virus. Virology. 1978 Mar;85(1):17–27. doi: 10.1016/0042-6822(78)90408-7. [DOI] [PubMed] [Google Scholar]
  46. Troxler D. H., Yuan E., Linemeyer D., Ruscetti S., Scolnick E. M. 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):639–653. doi: 10.1084/jem.148.3.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Vogt M. 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):226–236. doi: 10.1016/0042-6822(79)90290-3. [DOI] [PubMed] [Google Scholar]
  48. Vogt P. K., Ishizaki R. Reciprocal patterns of genetic resistance to avian tumor viruses in two lines of chickens. Virology. 1965 Aug;26(4):664–672. doi: 10.1016/0042-6822(65)90329-6. [DOI] [PubMed] [Google Scholar]
  49. van Griensven L. J., Vogt M. Rauscher "mink cell focus-inducing" (MCF) virus causes erythroleukemia in mice: its isolation and properties. Virology. 1980 Mar;101(2):376–388. doi: 10.1016/0042-6822(80)90451-1. [DOI] [PubMed] [Google Scholar]

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