Murine Leukemia Viruses with Recombinant env Genes: A Discussion of Their Role in Leukemogenesis

  • Nancy G. Famulari
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 103)


In 1951 Ludwik Gross reported experiments which demonstrated the viral etiology of certain murine leukemias. His work identified the presence of an infectious agent in cell-free extracts of AKR thymomas which could transmit leukemia to C3Hf/Bi mice (Gross 1951). Subsequent electron microscopic analysis demonstrated the presence of virus particles with the characteristic type c morphology of murine leukemia virus in both preparations of AKR thymomas and of leukemias induced in C3Hf/Bi mice by Gross’ protocol (Dmochowski and Grey 1957; Bernhard 1960). In the ensuing 30 years it has become obvious that the murine leukemia viruses (MuLV) are a polymorphic family of infectious agents, heterogeneous in their ability to induce disease in mice and even in their ability to infect and replicate in mouse cells (for review see Stephenson 1980). Host range classes of MuLV have been defined that are ecotropic, i.e., infectious for mouse cells, and xenotropic, i.e., infectious for cells of heterologous species but not for mouse cells. In addition, it has become clear that MuLV are maintained in the murine population predominantly via vertical transmission of endogenous viral loci carried by the mouse genome, rather than by horizontal transmission of infectious virus. These viral loci consist of complete and partial viral genomes, the expression of which can result in production of infectious virus or in synthesis of viral gene products in the absence of virus replication. A great deal of effort has been directed toward characterization of the repertoire of MuLV that exists in the mouse, and toward identification of the factors which influence the complex virus-host interaction which governs their expression in vivo (for review see Lilly and Pincus 1973; Old and Stockert 1977; Jolicoeur 1979). One outcome of these investigations has been the identification by Hartley and co-workers (1977) of the particular class of leukemogenic MuLV which Gross assayed in his early experiments.


Murine Leukemia Virus Friend Virus Nonpathogenic Isolate Moloney Leukemia Virus Mink Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anand R, Lilly F, Ruscetti S (1981) Viral protein expression in producer and nonproducer clones of Friend erythroleukemia cell lines. J Virol 37: 654–660PubMedGoogle Scholar
  2. Armstrong MYK, Ruddle NH, Lipman MB, Pierce SK, Richards FF (1977) Role of endogenous murine leukemia virus in immunologically triggered lymphoreticular tumors. I. Development and use of oncogenic cell-free preparations serially passage in vivo. J Natl Cancer Inst 58: 67–72PubMedGoogle Scholar
  3. Armstrong MYK, Weininger RB, Binder D, Himsel CA, Richards FR (1980) Role of endogenous murine leukemia virus in immunologically triggered lymphoreticular tumors II. Isolation of B-tropic mink cell focus-inducing (MCF) marine leukemia virus. Virology 104: 164–173PubMedGoogle Scholar
  4. Axelrad AA, Steeves RA (1964) Assay for Friend leukemia virus: rapid quantitative method based on enumeration of macroscopic spleen foci in mice. Virology 24: 513–518PubMedGoogle Scholar
  5. Barbacid M, Troxler DH, Scolnick EM, Aaronson SA (1978) Analysis of translational products of Friend strain of spleen focus-forming virus. J Virol 27: 826–830PubMedGoogle Scholar
  6. Bedigian HG, Taylor BA, Meier H (1981) Expression of murine leukemia viruses in the highly lymphomatous BXH-2 recombinant inbred mouse strain. J Virol 39: 632–640PubMedGoogle Scholar
  7. Bentvelzen P, Aarssen AM, Brinkhof J (1972) Defectivity of Rauscher murine erythroblastosis virus. Nature 239: 122–123Google Scholar
  8. Bernhard W (1960) The detection and study of tumor viruses with the electron microscope. Cancer Res 20: 712–727PubMedGoogle Scholar
  9. Bernstein A, Mak TW, Stephenson JR (1977) The Friend virus genome: evidence for the stable association of MuLV sequences and sequences involved in erythroleukemia transformation. Cell 12: 287–294PubMedGoogle Scholar
  10. Billelo JA, Colletta G, Warnecke G, Koch G, Frisby D, Pragnell IB, Ostertag W (1980) Analysis of the expression of spleen focus-forming virus, (SFFV)-related RNA and gp55, a Friend and Rauscher virus-specific protein. Virology 107: 331–344Google Scholar
  11. Bosselman RA, van Griensven LJLD, Vogt M, Verma IM (1979) Genome organization of retro-viruses VI. Heteroduplex analysis of ecotropic and xenotropic sequences of Moloney mink cell focus-inducing virus RNA obtained from either a cloned isolate or a thymoma cell line. J Virol 32: 968–978PubMedGoogle Scholar
  12. Bosselman RA, van Griensven LJLD, Vogt M, Verma IM (1980) Genome organization of retro-viruses IX. Analysis of the genomes of Friend spleen focus-forming (F-SFFV) and helper murine leukemia viruses by heteroduplex-formation. Virology 102: 234–239PubMedGoogle Scholar
  13. Buchhagen DL, Pincus T, Stutman O, Fleissner E (1976) Leukemogenic activity of murine type C viruses after long-term passage in vitro. Int J Cancer 18: 835–842PubMedGoogle Scholar
  14. Buchhagen DL, Pedersen FS, Crowther RL, Haseltine WA (1980) Most sequence differences between the genome of the Akv virus and a leukemogenic Gross A virus passaged in vitro are located near the 3’ terminus. Proc Nati Acad Sci USA 77: 4359–4363Google Scholar
  15. Chattopadhyay SK, Lander MR, Gupta S, Rands E, Lowy DR (1981) Origin of mink cytopathic focus-forming (MCF) viruses: comparison with ecotropic and xenotropic murine leukemia virus genomes. Virology 113: 465–483PubMedGoogle Scholar
  16. Chattopadhyay SK, Cloyd MW, Linemeyer DL, Lander R, Rands E, Lowy DR (1982) Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas Nature 295: 25–31Google Scholar
  17. Chien Y-H, Verma IM, Shih TY, Scolnick EM, Davidson N (1978) Heteroduplex analysis of the sequence relations between the RNAs of mink cell focus-inducing and murine leukemia viruses. J Virol 28: 352–360PubMedGoogle Scholar
  18. Cleveland D, Fischer SG, Kirschner MW, Laemmli VK (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem 252: 1102–1106PubMedGoogle Scholar
  19. Cloyd MW, Hartley JW, Rowe WP (1979) Cell-surface antigens associated with recombinant mink cell focus-inducing murine leukemia viruses. J Exp Med 149: 702–712PubMedGoogle Scholar
  20. Cloyd MW, Hartley JW, Rowe WP (1980) Lymphomagenicity of recombinant mink cell focus-inducing murine leukemia viruses. J Exp Med 151: 542–552PubMedGoogle Scholar
  21. Cloyd MW, Hartley JW, Rowe WP (1981) Genetic study of lymphoma induction by AKR mink cell focus-inducing virus in AKR and NFS crosses. J Exp Med 154: 450–458PubMedGoogle Scholar
  22. DeLarco JE, Rapp UR, Todaro GJ (1978) Cell surface receptors for ecotropic MuLV: detection and tissue distribution of free receptors in vivo. Int J Cancer 21: 356–360Google Scholar
  23. Devare SG, Rapp VR, Todaro GJ, Stephenson JR (1978) Acquisition of oncogenicity by endogenous mouse type C viruses: effects of variations in envand gaggenes. J Virol 28: 457–465PubMedGoogle Scholar
  24. Dmochowski L, Grey CE (1957) Subcellular structures of possible viral origin in some mammalian tumors. Ann NY Acad Sci 68: 559–615PubMedGoogle Scholar
  25. Donoghue DJ, Rothenberg E, Hopkins N, Baltimore D, Sharp PA (1978) Heteroduplex analysis of the nonhomology region between Moloney MuLV and the dual host range derivative HIX virus. Cell 14: 959–970PubMedGoogle Scholar
  26. Dresler S, Ruta M, Murray MJ, Kabat D (1979) Glycoprotein encoded by the Friend spleen focus-forming virus. J Virol 30: 564–575PubMedGoogle Scholar
  27. Elder JH, Gautsch JW, Jensen FC, Lerner RA, Hartley JW, Rowe WP (1977) Biochemical evidence that MCF murine leukemia viruses are envelope (env)gene recombinants. Proc Nati Acad Sci USA 74: 4676–4680Google Scholar
  28. Evans LH, Duesberg PH, Troxler DH, Scolnick EM (1979) Spleen focus-forming Friend virus: identification of genomic RNA and its relationship to helper virus RNA. J Virol 31: 133–146PubMedGoogle Scholar
  29. Evans L, Nunn M, Duesberg PH, Troxler D, Scolnick E (1980) RNAs of defective and nondefective components of Friend anemia and polycythemia virus strains identified and compared. Cold Spring Harbor Symp Quant Biol 44: 823–835PubMedGoogle Scholar
  30. Fagg B, Vehmeyer K, Ostertag W, Jasmine C, Klein B (1980) In: Rossi G (ed) In vivo and in vitro erythropoiesis: the Friend system. Elsevier, Amsterdam pp 163–172Google Scholar
  31. Faller DV, Hopkins N (1978) T1 oligonucleotide maps of Moloney and HIX murine leukemia viruses. Virology 90: 265–273PubMedGoogle Scholar
  32. Faller DV, Rommelaere J, Hopkins N (1978) Large T1 oligonucleotides of Moloney leukemia virus missing in an envgene recombinant, HIX, are present on an intracellular 21S Moloney viral RNA species. Proc Natl Acad Sci USA 75: 2964–2968PubMedGoogle Scholar
  33. Famulari NG, English KJ (1981) Env gene products of AKR dualtropic viruses: examination of peptide maps and cell surface expression. J Virol 40:971–976PubMedGoogle Scholar
  34. Famulari NG, Jelalian K (1979) Cell surface expression of the envgene polyprotein of dualtropic MCF murine leukemia virus. J Virol 30: 720–728PubMedGoogle Scholar
  35. Famulari NG, Tung J-S, O’Donnell PV, Fleissner E (1980) Murine leukemia virus env-gene expression in preleukemia thymocytes and leukemia cells of AKR strain mice. Cold Spring Harbor Symp Quant Biol 44: 1281–1287PubMedGoogle Scholar
  36. Famulari NG, Koehne CF, O’Donnell PV (1982) Leukemogenesis by Gross passage A murine leukemia virus: expression of viruses with recombinant envgenes in transformed cells. Proc Nati Acad Sci USA 79: 3872–3876Google Scholar
  37. Fieldsteel AH, Dawson PJ, Kurahara C (1971) In vivo and in vitro recovery of defective Friend virus by various leukemia viruses. Int J Cancer 8: 304–309PubMedGoogle Scholar
  38. Fischinger PJ, Nomura S, Bolognesi DP (1975) A novel murine oncornavirus with dual eco-and xenotropic properties. Proc Natl Acad Sci USA 72: 5150–5155PubMedGoogle Scholar
  39. Fischinger PJ, Frankel AE, Elder JH, Lerner RA, Ihle JN, Bolognesi DP (1978) Biological, immunological, and biochemical evidence thatHIX virus is a recombinant between Moloney leukemia virus and a murine xenotropic C-type virus. Virology 90: 241–254PubMedGoogle Scholar
  40. Fowler AK, Twardzik DR, Reed CD, Weislow OS, Hellman A (1977) Binding characteristics of Rauscher leukemia virus envelope glycoprotein gp71 to murine lymphoid cells. J Virol 24: 729–735PubMedGoogle Scholar
  41. Friend C (1957) Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia. J Exp Med 105: 302–318Google Scholar
  42. Furth J, Seibold HR, Rathbone RR (1933) Experimental studies on lymphomatosis of mice. Am J Cancer 19: 521–604Google Scholar
  43. Green N, Hiai H, Elder JH, Schwartz RS, Khiroya RH, Thomas CY, Tsichlis PN, Coffin JM (1980) Expression of leukemogenic recombinant viruses associated with a recessive gene in HRS/J mice. J Exp Med 152: 249–264PubMedGoogle Scholar
  44. Gross L (1951) “Spontaneous” leukemia developing in C3H mice following inoculation in infancy, with AK leukemic extracts or AK embryos. Proc Soc Exp Biol Med 76:27–32PubMedGoogle Scholar
  45. Gross L (1957) Development and serial cell-free passage of a highly potent strain of mouse leukemia virus. Proc Soc Exp Biol Med 94: 767–771PubMedGoogle Scholar
  46. Gross L (1970) Oncogenic viruses. 2nd edn. Pergamon, OxfordGoogle Scholar
  47. Gross L, Dreyfuss Y (1978) Relative loss of oncogenic potency of mouse leukemia virus (Gross) after prolonged propagation in tissue culture. Proc Natl Acad Sci USA 75: 3989–3992PubMedGoogle Scholar
  48. Haas M, Patch V (1980) Genomic masking and rescue of dualtropic murine leukemia viruses: role of pseudotype virions in viral lymphomagenesis. J Virol 35: 583–591PubMedGoogle Scholar
  49. Hamada K, Yanagihara K, Kamiya K, Seyama T, Yokoro K (1981) Leukemogenicity and cell transformation mechanisms in vitro by Gross murine leukemia virus: analysis of virus subpopulations. J Virol 38: 327–335PubMedGoogle Scholar
  50. Hankins WD, Krantz SB (1975) In vitro expression of erythroid differentiation induced by Friend polycythemia virus. Nature 253: 731–734PubMedGoogle Scholar
  51. Hankins WD, Troxler D (1980) Polycythemia and anemia-inducing erythroleukemia viruses exhibit differential erythroid transforming effects in vitro. Cell 22: 693–699PubMedGoogle Scholar
  52. Hartley JW, Rowe WP, Capps WI, Heubner RS (1969) Isolation of naturally occurring viruses of the murine leukemia virus group in tissue culture. J Virol 3: 126–132PubMedGoogle Scholar
  53. Hartley JW, Wolford NK, Old LJ, Rowe WP (1977) A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci USA 74: 789–792PubMedGoogle Scholar
  54. Hiai H, Morrissey R, Khiroya R, Schwartz RS (1977) Selective expression of xenotropic virus in congenic HRS/J (hairless mice). Nature 270: 247–249PubMedGoogle Scholar
  55. Hoffman PM, Davidson NF, Ruscetti SK, Chused TM, Morse HC (1981) Wild mouse ecotropic murine leukemia virus infection of inbred mice: dualtropic virus expression precedes the onset of paralysis and lymphoma. J Virol 39: 597–602PubMedGoogle Scholar
  56. Horoszewicz JS, Leung SS, Carter WA (1975) Friend leukemia: rapid development of erythropoietin-independent hematopoietic precursors. J Natl Cancer Inst 54: 265–267PubMedGoogle Scholar
  57. Housman D, Levenson R, Volloch V, Tsiftsoglou A, Gusella J, Parker D, Kernen J, Mitrani A, Weeks V, Witte O, Besmer P (1980) Control of proliferation and differentiation in cells transformed by Friend virus. Cold Spring Harbor Symp Quant Biol 44: 1177–1185PubMedGoogle Scholar
  58. Huebner R.1, Gilden RV, Toni R, Hill PR, Trimmer TW, Fish DC, Sass B (1976) Prevention of spontaneous leukemia in AKR mice by type-specific immunosuppression of endogenous virogenes. Proc Natl Acad Sci USA 73: 4633–4635Google Scholar
  59. Ihle JN, Lee JC (1982) Possible immunological mechanisms in C-type viral leukemogenesis in mice. Curr Top Microbiol Immunol 98: 85–101PubMedGoogle Scholar
  60. Ishimoto A, Adachi A, Sakai K, Yorifuji T, Tsuruta S (1981) Rapid emergence of mink cell focus-forming (MCF) virus in various mice infected with NB-tropic Friend virus. Virology 113: 644–655PubMedGoogle Scholar
  61. Jaenisch R (1976) Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci USA 73: 1260–1264PubMedGoogle Scholar
  62. Jaenisch R (1979) Moloney leukemia virus gene expression and gene amplification in preleukemic and leukemic BALB/Mo mice. Virology 93: 80–90PubMedGoogle Scholar
  63. Jaenisch R, Fan H, Croker B (1975) Infection of preimplantation mouse embryos and of newborn mice with leukemia virus: tissue distribution of viral DNA and RNA and leukemogenesis in the adult animal. Proc Nall Acad Sci USA 72: 4008–4012Google Scholar
  64. Jahner D, Stuhimann H, Jaenisch R (1980) Conformation of free and of integrated Moloney leukemia virus proviral DNA in preleukemic and leukemic BALB/Mo mice. Virology 101: 111–123PubMedGoogle Scholar
  65. Jolicoeur P (1979) The Fv-1gene of the mouse and its control of murine leukemia virus replication. Curr Top Microbiol Immunol 86: 67–122PubMedGoogle Scholar
  66. Jolicoeur P, Rosenberg N, Cotellessa A, Baltimore D (1978) Leukemogenicity of clonal isolates of murine leukemia viruses. J Nail Cancer Inst 60: 1473–1476Google Scholar
  67. Kabat D, Ruta M, Murray MJ, Polonoff E (1980) Immunoselection of mutants deficient in cell surface glycoproteins encoded by murine erythroleukemia viruses. Proc Nati Acad Sci USA 77: 57–67Google Scholar
  68. Kaplan HS (1967) On the natural history of the murine leukemias: presidential address. Cancer Res 27: 1325–1340PubMedGoogle Scholar
  69. Kaplan HS, Yaffe D (1960) Accelerated development of Strain Ak/n mouse lymphomas by cell-free tissue and tumor extracts. Proc Am Assoc Cancer Res 3: 332Google Scholar
  70. Kaplan PL, Topp WC, Ozanne B (1981) Simian virus 40 induces the production of a polypeptide transforming factor(s). Virology 108: 484–490PubMedGoogle Scholar
  71. Kawashima K, Ikeda H, Stockert E, Takahashi T, Old LJ (1976a) Age-related changes in cell surface antigens of preleukemic AKR thymocytes. J Exp Med 144: 193–208Google Scholar
  72. Kawashima K, Ikeda H, Hartley JW, Stockert E, Rowe WP, Old LJ (1976b) Changes in expression of murine leukemia virus antigens and production of xenotropic virus in the late preleukemic period in AKR mice. Proc Natl Acad Sci USA 73: 4680–4684Google Scholar
  73. Kelly M, Lung ML, Holland CA, Herr W, Corbin V, Chattopadhyay S, Lowy DR, Hopkins N (1983) A comparison of nucleotide sequences of the p15(E) gene and LTR of Akv and MCF 247 murine C-type viruses. J Virol 45:Jan issueGoogle Scholar
  74. Kemp MC, Basak S, Compans RW (1979) Glycopeptides of murine leukemia viruses. I. Comparison of two ecotropic viruses. J Virol 31: 1–7PubMedGoogle Scholar
  75. Kemp MC, Famulari NG, O’Donnell PV, Compans RW (1980) Glycopeptides of murine leukemia viruses. II. Comparison of xenotropic and dualtropic viruses. J Virol 34: 154–161PubMedGoogle Scholar
  76. Kemp MC, Famulari NG, Compans RW (1981) Glycopeptides of murine leukemia viruses. III. Glycosylation of envprecursor glycoproteins. J Virol 39: 463–470PubMedGoogle Scholar
  77. Lee JC, Ihle JN (1979) Mechanisms of C-type viral leukemogenesis I. Correlation of in vitro lymphocyte blastogenesis to viremia and leukemia. J Immunol 123: 2354–2358Google Scholar
  78. Lee JC, Ihle JN (1981a) Chronic immune stimulation is required for Moloney leukemia virus-induced lymphomas. Nature 289: 407–409Google Scholar
  79. Lee JC, Ihle JN (1981b) Increased responses to lymphokines are correlated with preleukemia in mice inoculated with Moloney leukemia virus. Proc Nall Acad Sci USA 78: 7712–7716Google Scholar
  80. Lenz J, Crowther R, Klimenko S, Haseltine W (1982) Molecular cloning of a highly leukemogenic, ecotropic retrovirus from an AKR mouse. J Virol 43: 943–951PubMedGoogle Scholar
  81. Liao SK, Axelrad AA (1975) Erythropoietin-independent erythroid colony formation in vitro by hemopoietic cells of mice injected with Friend virus. Int J Cancer 15: 467–482PubMedGoogle Scholar
  82. Lilly F, Pincus T (1973) Genetic control of murine viral leukemogenesis. Adv Cancer Res 17: 231–277Google Scholar
  83. Lilly F, Steeves RA (1973) B-tropic Friend virus: A host range pseudotype of spleen focus-forming virus (SFFV). Virology 55: 363–370PubMedGoogle Scholar
  84. Lilly F, Duran-Reynals ML, Rowe WP (1975) Correlation of early murine leukemia virus titer and H-2 type with spontaneous leukemia in mice of the BALB/c X AKR cross: a genetic analysis. J Exp Med 141: 882–889PubMedGoogle Scholar
  85. Linemeyer DL, Ruscetti SK, Menke JG, Scolnick EM (1980) 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 35: 710–721PubMedGoogle Scholar
  86. Linemeyer DL, Ruscetti SK, Scolnick EM, Evans LH, Duesberg PH (1981) Biological activity of the spleen focus-forming virus is encoded by a molecularly cloned subgenomic fragment of spleen focus-forming virus DNA. Proc Nail Acad Sci USA 78: 1401–1405Google Scholar
  87. Linemeyer DL, Menke JG, Ruscetti SK, Evans LH, Scolnick EM (1982) Envelope gene sequences which encode the gp52 protein of the spleen focus-forming virus are required for the induction of erythroid cell proliferation. J Virol 43: 223–233PubMedGoogle Scholar
  88. Lung ML, Hering C, Hartley JW, Rowe WP, Hopkins N (1980) Analysis of the genomes of mink cell focus-inducing murine type-C viruses: a progress report. Cold Spring Harbor Symp Quant Biol 44: 1269–1274PubMedGoogle Scholar
  89. Lung ML, Hartley JW, Rowe WP, Hopkins NH (1983) Large RNase Tl-resistant oligonucleotides encoding p15(E) and the U3 region of the LTR distinguish two biological classes of MCF C-type viruses of inbred mice. J Virol 45:Jan issueGoogle Scholar
  90. Lyles DS, McConnell KA (1981) Subcellular localization of the env-related glycoproteins in Friend erythroleukemia cells. J Virol 39: 263–272PubMedGoogle Scholar
  91. Lynch CJ (1954) The R.I.L. strain of mice: its relation to the leukemic AK strain and AKR sub-strains. J Natl Cancer Inst 15: 161–176PubMedGoogle Scholar
  92. MacDonald ME, Mak TW, Bernstein A (1980a) Erythroleukemia induction by replication-competent type C viruses cloned from the anemia-and polycythemia-inducing isolates of Friend leukemia virus. J Exp Med 151: 1493–1503Google Scholar
  93. MacDonald ME, Reynolds Jr FH, van de Ven WJM, Stephenson JR, Mak TW, Bernstein A (1980b) Anemia- and polycythemia-inducing isolates of Friend spleen focus-forming virus. Biological and molecular evidence for two distinct viral genomes. J Exp Med 151: 1477–1492Google Scholar
  94. Mayer A, Duran-Reynals ML, Lilly F (1978) Fv-1 regulation of lymphoma development and of thymic, ecotropic and xenotropic MuLV expression in mice of the AKR/J X RF/J cross. Cell 15:429–435PubMedGoogle Scholar
  95. McGrath MS, Weissman IL (1979) AKR leukemogenesis: identification and biological significance of thymic lymphoma receptors for AKR retroviruses. Cell 17: 65–75PubMedGoogle Scholar
  96. McGrath MS, Pillemer E, Kooishra D, Weissman IL (1980a) The role of MuLV receptors on T-lymphoma cells in lymphoma cell proliferation. Cont Top Mol Immunol 11: 157–183Google Scholar
  97. McGrath MS, Pillemer E, Weissman IL (1980b) Murine leukemogenesis: monoclonal antibodies to T-cell determinants arrest T lymphoma cell proliferation. Nature 285: 259–261Google Scholar
  98. Meier H, Taylor BA, Cherry M, Huebner RJ (1973) Host-gene control of type-C RNA tumor virus expression and tumorigenesis in inbred mice. Proc Natl Acad Sci USA 70: 1450–1455PubMedGoogle Scholar
  99. Mirand EA, Steeves RA, Ayila L, Grace JT Jr (1968) Spleen focus formation by polycythemic strains of Friend leukemia virus. Proc Soc Exp Biol Med 127: 900–904PubMedGoogle Scholar
  100. Niman HL, Elder JH (1980) Molecular dissection of Rauscher virus gp70 by using monoclonal antibodies: localization of acquired sequences of related envelope gene recombinants. Proc Natl Acad Sci USA 77: 4524–4528PubMedGoogle Scholar
  101. Nishizuka Y, Nakakuki K (1968) Acceleration of leukemogenesis in AKR mice by grafts, cell suspensions, and cell-free centrifugates of thymuses from preleukemic AKR donors. Int J Cancer 3: 203–210PubMedGoogle Scholar
  102. Nobis P, Jaenisch R (1980) Passive immunotherapy prevents expression of endogenous Moloney virus and amplification of proviral DNA in BALB/Mo mice. Proc Nail Acad Sci USA 77: 3677–3681Google Scholar
  103. Nowinski RC, Doyle T (1977) Cellular changes in the thymuses of preleukemic AKR mice: correlation with changes in the expression of murine leukemia viruses. Cell 12: 341–353PubMedGoogle Scholar
  104. Nowinski RC, Hays EF (1978) Oncogenicity of AKR endogenous leukemia viruses. J Virol 27: 13–18PubMedGoogle Scholar
  105. Nowinski RC, Brown M, Doyle T, Prentice RL (1979) Genetic and viral factors influencing the development of spontaneous leukemia in AKR mice. Virology 96: 186–204PubMedGoogle Scholar
  106. Obata Y, Ikeda H, Stockert E, Boyse EA (1975) Relation of Ga antigen of thymocytes to envelope glycoprotein of murine leukemia virus. J Exp Med 141: 188–197PubMedGoogle Scholar
  107. Obata Y, Stockert E, DeLeo AB, O’Donnell PV, Snyder HW Jr, Old LJ (1981) GERLD: a cell surface antigen of the mouse related to xenotropic MuLV defined by naturally occurring antibody and monoclonal antibody. J Exp Med 154: 659–675PubMedGoogle Scholar
  108. O’Donnell PV, Nowinski RC (1980) Serological analysis of antigenic determinants on the envgene products of AKR dualtropic (MCF) murine leukemia viruses. Virology 107: 81–88PubMedGoogle Scholar
  109. O’Donnell PV, Stockert E (1976) Induction of GIX antigen and Gross cell surface antigen after infection by ecotropic and xenotropic murine leukemia viruses in vitro. J Virol 20: 545–554PubMedGoogle Scholar
  110. O’Donnell PV, Stockert E, Obata Y, DeLeo AB, Old LJ (1980) Murine leukemia virus-related cell surface antigens as serological markers of AKR ecotropic, xenotropic and dualtropic viruses. Cold Spring Harbor Symp Quant Biol 44: 1255–1263PubMedGoogle Scholar
  111. O’Donnell PV, Stockert E, Obata Y, Old LJ (1981) 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 112: 548–563PubMedGoogle Scholar
  112. O’Donnell PV, Nowinski RC, Stockert E (1982) Amplified expression of murine leukemia virus (MuLV)-coded antigens on thymocytes and leukemia cells of AKR mice after infection by dualtropic (MCF) MuLV. Virology 119: 450–464PubMedGoogle Scholar
  113. Old LJ, Stockert E (1977) Immunogenetics of cell surface antigens of mouse leukemia. Annu Rev Genet 11: 127–160PubMedGoogle Scholar
  114. Oliff AI, Hager GL, Chang EH, Scolnick EM, Chan 11W, Lowy DR (1980) Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol 33: 475–486Google Scholar
  115. Oliff A, Ruscetti S, Douglass EC, Scolnick E (1981) Isolation of transplantable erythroleukemia cells from mice infected with helper-independent Friend murine leukemia virus. Blood 58: 244–254PubMedGoogle Scholar
  116. Pedersen FS, Buchhagen DL, Chen CY, Hays EF, Haseltine WA (1980) Characterization of virus produced by a lymphoma induced by inoculation of AKR MCF 247 virus. J Virol 35: 211–218PubMedGoogle Scholar
  117. Pedersen FS, Crowther RL, Tenney DY, Reimold AM, Haseltine WA (1981) Novel leukemogenic retroviruses isolated from cell line derived from spontaneous AKR tumor. Nature 292: 167–170PubMedGoogle Scholar
  118. Pedersen FS, Crowther RL, Hays EF, Nowinski RC, Haseltine WA (1982) Structure of retroviral RNA’s produced by cell lines derived from spontaneous lymphomas of AKR mice. J Virol 41: 18–29PubMedGoogle Scholar
  119. Peters RL, Hartley JW, Spahn W, Rabstein LS, Whitmire CE, Turner HC, Huebner RJ (1972) Prevalence of the group-specific (gs) antigen and infectious virus expressions of the murine c-type RNA viruses during the life span of BALB/c Cr mice. Int J Cancer 10: 283–289PubMedGoogle Scholar
  120. Pinter A, Hornen WJ, Tung J-S, O’Donnell PV, Hammerling U (1982) Structural domains of endogenous murine leukemia virus gp70s containing specific antigenic determinants defined by monoclonal antibodies. Virology 116: 499–516PubMedGoogle Scholar
  121. Quint W, Quax W, van der Putten H, Berns A (1981) Characterization of AKR murine leukemia virus sequences in AKR mouse substrains and structure of integrated recombinant genomes in tumor tissue. J Virol 39: 1–10PubMedGoogle Scholar
  122. Racevskis J, Koch G (1977) Viral protein synthesis in Friend erythroleukemia cell lines. J Virol 21: 328–337PubMedGoogle Scholar
  123. Racevskis J, Koch G (1978) Synthesis and processing of viral proteins in Friend erythroleukemia cell lines. Virology 87: 354–365PubMedGoogle Scholar
  124. Rapp UR, Todaro GJ (1978) Generation of oncogenic type C viruses: rapidly leukemogenic viruses derived from C3H mouse cells in vivo and in vitro. Proc Natl Acad Sci USA 75: 2468–2472PubMedGoogle Scholar
  125. Reddy EP, Dunn CY, Aaronson SA (1980) Different lymphoid cell targets for transformation by replication-competent Moloney and Rauscher mouse leukemia viruses. Cell 19: 663–669PubMedGoogle Scholar
  126. Rein A (1982) Interference grouping of murine leukemia viruses: a distinct receptor for the MCFrecombinant viruses on mouse cells. Virology 120: 251–257PubMedGoogle Scholar
  127. Rommelaere J, Faller DV, Hopkins N (1978) Characterization and mapping of RNase Tl-resistant oligonucleotides derived from the genomes of AKV and MCF murine leukemia viruses. Proc Natl Acad Sci USA 75: 495–499PubMedGoogle Scholar
  128. Rosenberg N, Baltimore D (1978) The effect of helper virus in Abelson virus-induced transformation of lymphoid cells. J Exp Med 147: 1126–1141PubMedGoogle Scholar
  129. Rosner M, Grinna LS, Robbins PW (1980) Differences in glycosylation patterns of closely related murine leukemia viruses. Proc Natl Acad Sci USA 77: 67–71PubMedGoogle Scholar
  130. Rowe WP (1973) Genetic factors in the natural history of murine leukemia virus infection: GHA Clowes Memorial Lecture. Cancer Res 33: 3061–3068PubMedGoogle Scholar
  131. Rowe WP, Pincus T (1972) Quantitative studies of naturally occurring murine leukemia virus infection of AKR mice. J Exp Med 135: 429–436PubMedGoogle Scholar
  132. Rowe WP, Cloyd MW, Hartley JW (1980) Status of the association of mink cell focus-inducing viruses with leukemogenesis. Cold Spring Harbor Symp Quant Biol 44: 1265–1268PubMedGoogle Scholar
  133. Rudali G, Duplan J-F, Latarjet R (1956) Latence des leucoses chez des souris injectees avec un extrait leucemique a-cellulaire AK. CR Soc Biol (Paris) 242: 837–839Google Scholar
  134. Ruscetti SK, Linemeyer D, Feild J, Troxler D, Scolnick EM (1979) Characterization of a protein found in cells infected with the spleen focus-forming virus that shares immunological cross-reactivity with the gp70 found in mink cell focus-inducing virus particles. J Virol 30: 787–798PubMedGoogle Scholar
  135. Ruscetti S, Troxler D, Linemeyer D, Scolnick EM (1980) Three laboratory strains of spleen focus- forming virus: comparison of their genomes and translation products. J Virol 33: 140–151PubMedGoogle Scholar
  136. Ruscetti S, Davis L, Feild J, Oliff A (1981a) 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 154: 907–920Google Scholar
  137. Ruscetti SK, Feild JA, Scolnick EM (1981b) Polycythemia-and anemia-inducing strains of spleen focus-forming virus differ in post translational processing of envelope-related glycoproteins. Nature 294: 663–665Google Scholar
  138. Ruta M, Kabat D (1980) Plasma membrane glycoproteins encoded by cloned Rauscher and Friend spleen focus-forming viruses. J Virol 35: 844–853PubMedGoogle Scholar
  139. Ruta M, Clarke S, Boswell B, Kabat D (1982) Heterogeneous metabolism and subcellular localization of a potentially leukemogenic membrane glycoprotein encoded by Friend erythroleukemia virus. J Biol Chem 257: 126–134PubMedGoogle Scholar
  140. Schafer W, Schwarz H, Thiel H-J, Fischinger PJ, Bolognesi DP (1977) Properties of mouse leukemia viruses XIV. Prevention of spontaneous AKR leukemia by treatment with group-specific antibody against the major virus gp71 glycoprotein. Virology 83: 207–210PubMedGoogle Scholar
  141. Schultz AM, Ruscetti SK, Scolnick EM, Oroszlan S (1980) The env-gene of the spleen focus-forming virus lacks expression of p15(E) determinants. Virology 107: 537–542PubMedGoogle Scholar
  142. Schwarz H, Fischinger PJ, Ihle JN, Thiel H-J, Weiland F, Bolognesi DP, Schafer W (1979) Properties of mouse leukemia viruses XVI. Suppression of spontaneous fatal leukemias in AKR mice by treatment with broadly reacting antibody against the viral glycoprotein gp71. Virology 93: 159–174PubMedGoogle Scholar
  143. Schwarz H, Ihle JN, Wecher E, Fischinger PJ, Thiel H-J, Bolognesi DP, Schafer W (1981) Properties of mouse leukemia viruses XVII. Factors required for successful treatment of spontaneous AKR leukemia by antibodies against gp71. Virology 111: 568–578PubMedGoogle Scholar
  144. Shih TY, Weeks MO, Troxler DH, Coffin JM, Scolnick EM (1978) Mapping host range-specific oligonucleotides within genomes of the ecotropic and mink cell focus-inducing strains of Moloney murine leukemia virus. J Virol 26: 71–83PubMedGoogle Scholar
  145. Steeves RA (1975) Spleen focus-forming virus in Friend and Rauscher leukemia virus preparations. J Nati Cancer Inst 54: 289–297Google Scholar
  146. Steeves RA, Mirand EA (1969) Separation of members of the Friend virus complex by sucrose gradient centrifugation. Proc Am Assoc Cancer Res 10: 86Google Scholar
  147. Steeves RA, Eckner RJ, Mirand EA, Priore RL (1971) Rapid assay of murine leukemia virus helper activity for Friend spleen focus forming virus. J Natl Cancer Inst 46: 1219–1228PubMedGoogle Scholar
  148. Stephenson JR (1980) Molecular biology of RNA tumor viruses. Academic Press, New YorkGoogle Scholar
  149. Stockert E, Old LJ, Boyse EA (1971) The Go(system: a cell surface allo-antigen associated with murine leukemia virus; implications regarding chromosomal integration of the viral genome. J Exp Med 133: 1334–1355PubMedGoogle Scholar
  150. Stockert E, DeLeo AB, O’Donnell PV, Obata Y, Old LJ (1979) GAKSL2: a new cell surface antigen of the mouse related to the dualtropic mink cell focus-inducing class of murine leukemia virus detected by naturally occurring antibody. J Exp Med 149: 200–215PubMedGoogle Scholar
  151. Tambourin PE, Wendling F, Jasmin C, Smadja-Joffe F (1979) The physiopathology of Friend leukemia. Leuk Res 3: 117–129PubMedGoogle Scholar
  152. Troxler DH, Scolnick EM (1978) Rapid leukemia induced by cloned Friend strain of replicating murine type-C virus. Virology 85: 17–27PubMedGoogle Scholar
  153. Troxler DH, Boyers JK, Parks WP, Scolnick EM (1977a) Friend strain of spleen focus-forming virus: a recombinant between mouse type C ecotropic viral sequences and sequences related to xenotropic virus. J Virol 22: 361–372Google Scholar
  154. Troxler DH, Lowy D, Howk R, Young H, Scolnick EM (1977b) Friend strain of spleen focus-forming virus is a recombinant between ecotropic murine type C virus and the envgene region of xenotropic type C virus. Proc Natl Acad Sci USA 74: 4671–4675Google Scholar
  155. Troxler DH, Parks WP, Vass WC, Scolnick EM (1977c) Isolation of a fibroblast nonproducer cell line containing the Friend strain of the spleen focus-forming virus. Virology 76: 602–615Google Scholar
  156. Troxler DH, Yuan E, Linemeyer D, Ruscetti S, Scolnick EM (1978) 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 148: 639–653PubMedGoogle Scholar
  157. Troxler DH, Ruscetti SK, Linemeyer DL, Scolnick EM (1980) Helper-independent and replication-defective erythroblastosis-inducing viruses contained within anemia-inducing Friend virus complex (FV-A). Virology 102: 28–45PubMedGoogle Scholar
  158. Tung J-S, Fleissner E (1980) Amplified envand gagproducts on AKR cells. Origin from different murine leukemia virus genomes. J Exp Med 151: 975–979PubMedGoogle Scholar
  159. Tung J-S, Vitetta ES, Fleissner E, Boyse EA (1975) Biochemical evidence linking the Gil(thymocyte surface antigen to the gp69/71 envelope glycoprotein of murine leukemia virus. J Exp Med 141: 198–205PubMedGoogle Scholar
  160. Tung J-S, Boyse EA, Shen F-W (1980) Influence of Fv-1alleles on cellular expression of gp70. J Exp Med 151: 980–983PubMedGoogle Scholar
  161. van der Putten H, Quint W, van Raiij J, Maandag ER, Verma IM, Berns A (1981) M-MuLV-induced leukemogenesis and structure of recombinant proviruses in tumors. Cell 24: 729–739PubMedGoogle Scholar
  162. Van Griensven LJ, Vogt M (1980) Rauscher “mink cell focus-inducing” (MCF) virus causes erythro-leukemia in mice: its isolation and properties. Virology 101: 376–388PubMedGoogle Scholar
  163. Vogt M (1979) 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 93: 226–236PubMedGoogle Scholar
  164. Weissman IL, McGrath MS (1982) Retrovirus lymphomagenesis: relationship of normal immune receptors to malignant cell proliferation. Curr Top Microbiol Immunol 98: 103–112PubMedGoogle Scholar
  165. Witte ON, Wirth DF (1979) Structure of murine leukemia virus envelope glycoprotein precursor. J Virol 29: 735–743PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1983

Authors and Affiliations

  • Nancy G. Famulari
    • 1
  1. 1.Department of Viral OncologyMemorial Sloan Kettering Cancer CenterNew YorkUSA

Personalised recommendations