Spleen Focus-Forming Virus: Relationship of an Altered Envelope Gene to the Development of a Rapid Erythroleukemia

  • S. Ruscetti
  • L. Wolff
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 112)


In the 26 years since “Friend virus” was discovered (Friend 1957), we have learned a considerable amount about this virus complex and the role of the various components in the development of erythroleukemia in the mouse. The biological and molecular cloning of these viral components has been pivotal in carrying out these studies. Separation in rodent fibroblasts of Friend murine leukemia virus (F-MuLV) and the defective spleen focus-forming virus (SFFV) has led to the conclusion that SFFV is responsible for the rapid erythroleukemia occurring in adult mice, while the role of F-MuLV in the adult is to act as a helper for the replicative functions that the defective SFFV lacks. Molecular cloning of SFFV as well as the isolation of biological mutants of SFFV has allowed for the localization of the region of the viral genome involved in pathogenicity. This region includes almost exclusively the envelope gene of SFFV. The focus of this review, therefore, will be on studies of the envelope gene of various SFFVs and their translational products.


Erythroid Differentiation Helper Virus Envelope Gene Friend Virus Erythroid Precursor 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. Amanuma H, Akiko K, Obata M, Sagata N, Ikawa Y (1983) Complete nucleotide sequence of the gene for the specific glycoprotein (gp55) of Friend spleen focus-forming virus. Proc Natl Acad Sci USA 80:3913–3917PubMedGoogle Scholar
  2. 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
  3. 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
  4. 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
  5. Bernstein A, Mak TW, Stephenson JR (1977) The Friend virus genome: evidence for the stable association of MuLV sequences and sequences involved in erythroleukemic transformation. Cell 12:287–294PubMedGoogle Scholar
  6. Bestwick R, Ruta M, Kiessling A, Faust C, Linemeyer D, Scolnick E, Kabat D (1983) Genetic structure of Rauscher spleen focus-forming virus. J Virol 45:1217–1222PubMedGoogle Scholar
  7. Bilello 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 107:331–344PubMedGoogle Scholar
  8. Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77:1496–1500PubMedGoogle Scholar
  9. Bosselman RA, Van Griensven LJLD, Vogt M, Verma I (1980) Genome organization of retroviruses 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
  10. Bosselman RA, van Straaten F, Van Beveren C, Verma IM, Vogt M (1982) Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA. J Virol 44:19–31PubMedGoogle Scholar
  11. Chattopadhyay SK, Cloyd MW, Linemeyer DL, Lander MR, Rands E, Lowy DR (1982) Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas. Nature 295:25–31PubMedGoogle Scholar
  12. Chesebro B, Portis JL, Wehrly K, Nishio J (1983) Effect of murine host genotype on MCF virus expression, latency and leukemia cell type of leukemias induced by Friend murine leukemia helper virus. Virology 128:221–233PubMedGoogle Scholar
  13. Clark SP, Mak TW (1982) Nucleotide sequences of the murine retrovirus Friend SFFVP long terminal repeats: identification of a structure with extensive dyad symmetry 5´ to the TATA box. Nucleic Acids Res 10:3315–3330PubMedGoogle Scholar
  14. Clark SP, Mak TW (1983) Complete nucleotide sequences of an infectious clone of Friend spleen focus-forming provirus: gp55 is an envelope fusion glycoprotein. Proc Natl Acad Sci USA 80:5037–5041PubMedGoogle Scholar
  15. Dexter TM, Scott D, Teich NM (1977) Infection of bone marrow cells in vitro with FLV: effects on stem cell proliferation, differentiation and leukemogenic capacity. Cell 12:355–364PubMedGoogle Scholar
  16. Dexter TM, Allen TD, Scott D, Teich NM (1979) Isolation and characterization of a bipotential haematopoietic cell line. Nature 227:471–474Google Scholar
  17. Dexter TM, Allen TD, Testa NG, Scolnick E (1981) Friend disease in vitro. J Exp Med 154:594–608PubMedGoogle Scholar
  18. Dresler S, Ruta M, Murray MJ, Kabat D (1979) Glycoprotein encoded by the Friend spleen focus- forming virus. J Virol 30:564–575PubMedGoogle Scholar
  19. 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
  20. 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
  21. Fagg B, Ostertag W (1982) Friend erythroleukemia virus complex: role of viral components in modifying erythroid differentiation in mice. J Natl Cancer Inst 68:457–460PubMedGoogle Scholar
  22. Famulari NG (1983) Murine leukemia viruses with recombinant env genes: a discussion of their role in leukemogenesis. In: Vogt PK, Koprowski H (eds) Retroviruses 1. Springer, Berlin Heidelberg New York, pp 76–108 (Current topics in microbiology and immunology, vol 103)Google Scholar
  23. Fredrickson T, Tambourin P, Wendling F, Jasmin C, Smajda F (1975) Target cell of the polycythemia- inducing Friend virus: studies with myleran. J Natl Cancer Inst 55:443–446PubMedGoogle Scholar
  24. Friend C (1957) Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia. J Exp Med 105:307–318PubMedGoogle Scholar
  25. Friend C, Haddad JR (1960) Tumor formation with transplants of spleen or liver from mice with virus-induced leukemia. J Natl Cancer Inst 25:1279–1289PubMedGoogle Scholar
  26. Friend C, Sher W, Holland JG, Sato T (1971) Hemoglobin synthesis in murine virus-induced leukemia cells in vitro: stimulation of erythroid differentiation by dimethylsulfoxide. Proc Natl Acad Sci USA 68:378–382PubMedGoogle Scholar
  27. Gillis S, Ruscetti SK, Gillis AE, Troxler DH, Scolnick EM, Smith KA (1979) The spleen focus- forming virus (SFFV)-specific neoantigen shares cross-reactive determinants with mink cell focus- inducing (MCF) virus gp70. Virology 96:421–428PubMedGoogle Scholar
  28. Green N, Shinnick TM, Owen W, Ponticelli A, Sutcliff JG, Lerner RA (1981) Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proc Natl Acad Sci USA 78:6023–6027PubMedGoogle Scholar
  29. Greenberger JS, Davisson PB, Gans PJ, Moloney WC (1979) In vitro induction of continuous acute promyelocytic leukemia cell lines by Friend or Abelson murine virus. Blood 53:987–1001PubMedGoogle Scholar
  30. Gregory CJ, McCulloch EA, Till JE (1973) Erythropoietic progenitors capable of colony formation in culture: state of differentiation. J Cell Physiol 81:411–420PubMedGoogle Scholar
  31. Hankins WD, Krantz SB (1975) In vitro expression of erythroid differentiation induced by Friend polycythemia virus. Nature 253:731–732PubMedGoogle Scholar
  32. Hankins WD, Kratz SB (1980) Helper virus is not required for in vitro erythroid transformation of hematopoietic cells by Friend virus. Proc Natl Acad Sci USA 77:5287–5291PubMedGoogle Scholar
  33. Hankins WD, Troxler D (1980) Polycythemia- and anemia-inducing erythroleukemia viruses exhibit differential erythroid transforming effects in vitro. Cell 22:693–699PubMedGoogle Scholar
  34. Hankins WD, Kost TA, Khoury MJ, Krantz SB (1978) Erythroid bursts produced by Friend leukemia virus in vitro. Nature 276:506–508PubMedGoogle Scholar
  35. Holland CA, Wozney J, Hopkins N (1983) Nucleotide sequence of the gp70 gene of murine retrovirus MCF 247. J Virol 47:413–420PubMedGoogle Scholar
  36. Horoszewicz JS, Leong SS, Carter WA (1975) Friend leukemia: rapid development of erythropoietin- independent hematopoietic precursors. J Natl Cancer Inst 54:265–267PubMedGoogle Scholar
  37. Ikawa Y, Yoshida M, Yoshikura H (1978) Identification of proteins specific to Friend strain of spleen focus forming virus (SFFV). Proc Jpn Acad 54:651–656Google Scholar
  38. Ikawa Y, Kobayashi Y, Obinata M, Harada F, Hino S, Yoshikura H (1980) RNA sequences and proteins specific to Friend strain of spleen focus-forming virus. Cold Spring Harbor Symp Quant Biol 44:875–885PubMedGoogle Scholar
  39. Iscove NN (1978) Erythropoietin-independent stimulation of early erythropoiesis in adult bone marrow cultures by conditioned medium from lectin-stimulated mouse spleen cells. In: Golde DW, Cline MJ, Metcalf D, Fox CF (eds) Hematopoietic cell differentiation. Academic, New York, pp 37–52Google Scholar
  40. Johnson CS, Marcelletti J, Longley C, Furmanski P (1982) Inhibition of normal erythropoiesis in mice with Friend virus induced erythroleukemia. Exp Hematol 10:743–753PubMedGoogle Scholar
  41. Kaminchik J, Hankins WD, Ruscetti SK, Linemeyer DL, Scolnick EM (1982) Molecular cloning of biologically active proviral DNA of the anemia-inducing strain of spleen focus-forming virus. J Virol 44:922–931PubMedGoogle Scholar
  42. Kemp MC, Basak S, Compans RW (1979) Glycopeptides of murine leukemia virus. I. Comparison of two ecotropic viruses. J Virol 31:1–7PubMedGoogle Scholar
  43. Kemp MC, Famulari NG, O’Donnell PV, Compans RW (1980) Glycopeptides of murine leukemia virus II. Comparison of xenotropic and dualtropic viruses. J Virol 34:154–161PubMedGoogle Scholar
  44. Kemp MC, Famulari NG, Compans RW (1981) Glycopeptides of murine leukemia virus III. Glycosy- lation of env precursor glycoproteins. J Virol 39:463–470PubMedGoogle Scholar
  45. Klein G (ed) (1982) Advances in viral oncology, vol 2. Raven, New YorkGoogle Scholar
  46. Koch W, Hunsmann G, Friedrich R (1983) Nucleotide sequence of the envelope gene of Friend murine leukemia virus. J Virol 45:1–9PubMedGoogle Scholar
  47. Koch W, Zimmermann W, Oliff A, Friedrich R (1984) 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 49:828–840PubMedGoogle Scholar
  48. Kost TA, Koury MJ, Hankins WD, Krantz SB (1979) Target cells for Friend virus-induced erythroid bursts in vitro. Cell 18:145–152PubMedGoogle Scholar
  49. Kost TA, Hankins WD, Krantz SB (1980) Combined effect of Friend polycythemia virus and erythropoietin on erythroid burst formation in vitro. Exp Hematol 8:248–258PubMedGoogle Scholar
  50. Kost TA, Koury MJ, Krantz SB (1981) Mature erythroid burst forming units are target cells for Friend virus-induced erythroid bursts. Virology 108:309–317PubMedGoogle Scholar
  51. Koury MJ, Bondurant MC, Duncan DT, Krantz SB, Hankins WD (1982) Specific differentiation events induced by erythropoietin in cells infected in vitro with the anemia strain of Friend virus. Proc Natl Acad Sci USA 79:635–639PubMedGoogle Scholar
  52. Langdon WY, Hoffman PM, Silver JE, Buckler CE, Hartley JW, Ruscetti SK, Morse HC (1983 a) Identification of a spleen focus-forming virus in erythroleukemic mice infected with a wild-mouse ecotropic murine leukemia virus. J Virol 46:230–238PubMedGoogle Scholar
  53. Langdon WY, Ruscetti SK, Silver JE, Hankins WD, Buckler CE, Morse HC (1983 b) Cas spleen focus-forming virus. II. Further biological and biochemical characterization. J Virol 47:329–336PubMedGoogle Scholar
  54. Lenz J, Crowther R, Straceski A, Haseltine W (1982) Nucleotide sequence of the Akv env gene. J Virol 42:519–529PubMedGoogle Scholar
  55. Levy SB, Blankstein LA, Vinton EC, Chamber TJ (1979) In: Ikawa Y, Odaka T (eds) Oncogenic viruses and host cell genes. Academic, New York, pp 409–428Google Scholar
  56. Liao S, Axelrad AA (1975) Erythropoietin-independent erythroid colony formation in vitro by hemopoietic cells of mice infected with Friend virus. Int J Cancer 15:467–482PubMedGoogle Scholar
  57. Linemeyer DL, Ruscetti SK, Menke JG, Scolnick EM (1980) Recovery of biologically active spleen focus-forming virus from molecularly cloned spleen focus-forming virus-pB322 circular DNA by cotransfection with infectious type C retroviral DNA. J Virol 35:710–721PubMedGoogle Scholar
  58. 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 Natl Acad Sci USA 78:1401–1405PubMedGoogle Scholar
  59. Linemeyer DL, Menke JG, Ruscetti SK, Evans LH, Scolnick EM (1982) Envelope gene sequences which encode the gp52 protein of spleen focus-forming virus are required for the induction of erythroid cell proliferation. J Virol 43:223–233PubMedGoogle Scholar
  60. Lyles DS, McConnell KA (1981) Subcellular localization of the env-related glycoproteins in Friend erythroleukemia cells. J Virol 39:263–272PubMedGoogle Scholar
  61. MacDonald ME, Reynolds FH, Van de Ven WJM, Stephenson JR, Mak TW, Bernstein A (1980a) Anemia- and polycythemia-inducing isolates of Friend spleen focus-forming virus. Biological and molecular evidence for two distinct viral genomes. J Exp Med 151:1447–1492Google Scholar
  62. MacDonald ME, Mak TW, Bernstein A (1980 b) Erythroleukemia induction by replication-competent type-C viruses cloned from the anemia- and polycythemia-inducing isolates of Friend leukemia virus. J Exp Med 151:1493–1503PubMedGoogle Scholar
  63. MacDonald ME, Johnson GR, Bernstein A (1981) Different pseudotypes of Friend spleen focus- forming virus induce polycythemia and erythropoietin-independent colony formation in serum-free medium. Virology 110:231–236PubMedGoogle Scholar
  64. Machida CA, Bestwick RK, Kabat D (1984) Reduced leukemogenicity caused by mutations in the membrane glycoprotein gene of Rauscher spleen focus-forming virus. J Virol 49:394–402PubMedGoogle Scholar
  65. Mager D, Mak TW, Bernstein A (1980) Friend leukemia virus-transformed cells, unlike normal stem cells, form spleen colonies in S1/S1d mice. Nature 288:592–594PubMedGoogle Scholar
  66. Mager DL, Mak TW, Bernstein A (1981) Quantitative colony method for tumorigenic cells transformed by two distinct strains of Friend leukemia virus. Proc Natl Acad Sci USA 78:1703–1707PubMedGoogle Scholar
  67. Metcalf D, Furth J, Buffett RF (1959) Pathogenesis of mouse leukemia caused by Friend virus. Cancer Res 19:52–60PubMedGoogle Scholar
  68. Mirand EA (1967) Virus-induced erythropoiesis in hypertransfused polycythemic mice. Science 156:832–833PubMedGoogle Scholar
  69. Mirand EA, Prentice TC, Hoffmann JG (1961) Effect of Friend virus in Swiss and DBA/1 mice on 59Fe uptake. Proc Soc Exp Biol Med 106:423–426PubMedGoogle Scholar
  70. Mirand EA, Steeves RA, Ayila L, Grace JT (1968 a) Spleen focus formation by polycythemic strains of Friend leukemia virus. Proc Soc Exp Biol Med 127:900–904PubMedGoogle Scholar
  71. Mirand EA, Steeves RA, Lange RD, Grace JT (1968b) Virus-induced polycythemia in mice: erythropoiesis without erythropoietin. Proc Soc Exp Biol Med 128:844–849PubMedGoogle Scholar
  72. Neel BG, Hayward WS, Robinson HL, Fang J, Astrin S (1981) Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell 23:323–334PubMedGoogle Scholar
  73. Niho Y, Shibuya T, Mak TW (1982) Modulation of erythropoiesis by the helper-independent Friend leukemia virus F-MuLV. J Exp Med 156:146–158PubMedGoogle Scholar
  74. Opitz V, Seidel HJ (1978) Studies on the target cell for the Friend virus (FV-P) strain using the CFU-E technique. Blut 37:183–192PubMedGoogle Scholar
  75. Ostertag W, Melderis H, Steinheider G, Kluge N, Dube S (1972) Synthesis of mouse hemoglobin and globin mRNA in leukaemic cell cultures. Nature 239:231–234Google Scholar
  76. Payne GS, Courtneidge SA, Crittenden LB, Fadly AM, Bishop JM, Varmus HE (1981) Analysis of avian leukosis virus DNA and RNA in bursal tumors: viral gene expression is not required for maintenance of the tumor state. Cell 23:311–322PubMedGoogle Scholar
  77. Peschle C, Colletta G, Covelli A, Ciccariello R, Migliaccio G, Rossi GB (1981) The erythropoietic component of Friend virus erythroleukemias : role of erythropoietic hormones and SFFV genome. In : Rovoltella R, Pontieri G, Rovera G, Basilico C, Gallo RC, Subak-Sharpe J (eds) Expression of differentiated functions in cancer cells. Raven, New York, pp 311–321Google Scholar
  78. Pinter A, Honnen WJ (1983) Topography of murine leukemia virus envelope protein: characterization of transmembrane components. J Virol 46:1056–1060PubMedGoogle Scholar
  79. Pluznik DH, Sachs L (1964) Quantitation of a murine leukemia virus with a spleen colony assay. J Natl Cancer Inst 35:535–564Google Scholar
  80. Portis JL, Britt WJ, Evans LH, Chesebro B (1983) An antibody produced during graft-versus host reaction recognizes an erythroid differentiation antigen. Leukemia Rev 1:211–212Google Scholar
  81. Racevskis J, Koch G (1978) Synthesis and processing of viral proteins in Friend erythroleukemia cell lines. Virology 87:354–365PubMedGoogle Scholar
  82. Rauscher FJ (1962) A virus-induced disease of mice characterized by erythrocytopoiesis and lymphoid leukemia. J Natl Cancer Inst 29:515–543PubMedGoogle Scholar
  83. Rein A (1982) Interference grouping of murine leukemia viruses: a distinct receptor for the MCF- recombinant viruses on mouse cells. Virology 120:251–257PubMedGoogle Scholar
  84. Rossi GB, Peschle C (1980) Enhanced proliferation and migration of BFU-E and erythropoietin- independence of CFU-E expression in FLV-infected mice: comparative studies on anemic and polycythemic strain. In: Rossi GB (ed) In vivo and in vitro erythropoiesis: the Friend system. Elsevier, Amsterdam, pp 139–149Google Scholar
  85. Rothman JE, Fine RE (1980) Coated vesicles transport newly synthesized membrane glycoproteins from endoplasmic reticulum to plasma membrane in two successive stages. Proc Natl Acad Sci USA 77:780–784PubMedGoogle Scholar
  86. Ruscetti SK, Scolnick EM (1983) Expression of a transformation-related protein (p53) in the malignant stage of Friend virus-induced diseases. J Virol 46:1022–1026PubMedGoogle Scholar
  87. Ruscetti S, Linemeyer D, Feild J, Troxler D, Scolnick E (1978) Type-specific radioimmunoassays for the gp70s of mink cell focus-inducing murine leukemia viruses : expression of a cross-reacting antigen in cells infected with the Friend strain of the spleen focus-forming virus. J Exp Med 148:654–663PubMedGoogle Scholar
  88. Ruscetti S, 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 crossreactivity with the gp70 found in mink cell focus-inducing virus particles. J Virol 30:787–798PubMedGoogle Scholar
  89. Ruscetti S, Troxler D, Linemeyer D, Scolnick E (1980) Three laboratory strains of spleen focus- forming virus: comparison of their genomes and translational products. J Virol 33:140–151PubMedGoogle Scholar
  90. Ruscetti S, Davis L, Feild J, Oliff A (1981 a) 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 154:907–920PubMedGoogle Scholar
  91. Ruscetti SK, Feild JA, Scolnick EM (1981 b) Polycythaemia- and anaemia-inducing strains of spleen focus-forming virus differ in post-translational processing of envelope-related glycoproteins. Nature 294:663–665PubMedGoogle Scholar
  92. Ruta M, Kabat D (1980) Plasma membrane glycoproteins encoded by cloned Rauscher and Friend spleen focus-forming viruses. J Virol 35:844–853PubMedGoogle Scholar
  93. 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
  94. Ruta M, Bestwick R, Machida C, Kabat D (1983) Loss of leukemogenicity caused by mutations in the membrane glycoprotein structural gene of Friend spleen focus-forming virus. Proc Natl Acad Sci USA 80:4704–4708PubMedGoogle Scholar
  95. Sassa S, Takaku F, Nakao K (1968) Regulation of erythropoiesis in the Friend leukemia mouse. Blood 31:758–765PubMedGoogle Scholar
  96. Schmidt M (1982) Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology 116:327–338PubMedGoogle Scholar
  97. Schmidt MFG, Schlesinger MJ (1980) Relationship of fatty acid attachment to the translation and maturation of vesicular stomatitis and Sindbis virus membrane glycoproteins. J Biol Chem 255:3334–3339PubMedGoogle Scholar
  98. 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
  99. Shibuya T, Mak TW (1983) Isolation and induction of erythroleukemia cell lines with properties of erythroid progenitor burst-forming cell (BFU-E) and erythroid precursor cell (CFU-E). Proc Natl Acad Sci USA 80:3721–3725PubMedGoogle Scholar
  100. Srinivas RV, Compans RW (1983) Glycosylation and intracellular transport of spleen focus-forming virus glycoproteins. Virology 125:274–286PubMedGoogle Scholar
  101. Srinivas RV, Compans RW (1983) Membrane association and defective transport of spleen focus- forming virus glycoproteins. J Biol Chem 258:14718–14724PubMedGoogle Scholar
  102. Steeves RA, Mirand EA, Thomson S, Avila L (1969) Enhancement of spleen focus formation and virus replication in Friend virus-infected mice. Cancer Res 29:1111–1116PubMedGoogle Scholar
  103. Steinheider G, Seidel HJ, Kreja L (1979) Comparison of the biological effects of anemia inducing and polycythemia inducing Friend virus complex. Experientia 35:1173–1175PubMedGoogle Scholar
  104. Tambourin P, Wendling F (1971) Malignant transformation and erythroid differentiation by polycythaemia-inducing Friend virus. Nature 234:230–233Google Scholar
  105. Tambourin P, Wendling F (1975) Target cell for oncogenic action of polycythaemia-inducing Friend virus. Nature 256:320–322PubMedGoogle Scholar
  106. Tambourin PE, Wendling F, Jasmin C, Smadja-Joffe F (1979) The physiopathology of Friend leukemia. Leuk Res 3:117–129PubMedGoogle Scholar
  107. Tambourin P, Wendling F, Moreau-Gachelin F, Charon M, Bucau-Varlet P (1980) Friend leukemia: a multi-step malignant disease. In: Rossi GB (ed) In vivo and in vitro erythropoiesis: the Friend system. Elsevier, Amsterdam, pp 127–138Google Scholar
  108. Troxler DH, Scolnick EM (1978) Rapid leukemia induced by cloned Friend strain of replicating murine type-C virus. Virology 85:17–27PubMedGoogle Scholar
  109. Troxler DH, Parks WP, Vass WC, Scolnick EM (1977 a) Isolation of a fibroblast nonproducer cell line containing the Friend strain of the spleen focus-forming virus. Virology 76:602–615PubMedGoogle Scholar
  110. Troxler DH, Boyars JK, Parks WP, Scolnick EM (1977 b) Friend strain of spleen focus-forming virus: a recombinant between mouse type C ecotropic viral sequences and sequences related to xenotropic virus. J Virol 22:361–372PubMedGoogle Scholar
  111. Troxler DH, Lowy D, Howk R, Young H, Scolnick EM (1977 c) 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 USA 74:4671–4675PubMedGoogle Scholar
  112. 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
  113. Wagemaker G (1978) Induction of erythropoietin responsiveness in vitro. In: Golde DW, Cline MJ, Metcalf D, Fox CF (eds) Hematopoietic cell differentiation. Academic, New York, pp 109–118Google Scholar
  114. Weiss R, Teich N, Varmus H, Coffin J (eds) (1982) RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring HarborGoogle Scholar
  115. Wendling F, Moreau-Gachelin F, Tambourin P (1981) Emergence of tumorigenic cells during the course of Friend virus leukemias. Proc Natl Acad Sci USA 78:3614–3618PubMedGoogle Scholar
  116. Wolff L, Koller R, Ruscetti S (1982) Monoclonal antibody to spleen focus-forming virus-encoded gp52 provides probe for the amino-terminal region of retroviral envelope proteins that confers dual tropism and xenotropism. J Virol 43:472–481PubMedGoogle Scholar
  117. Wolff L, Scolnick E, Ruscetti S (1983) Envelope gene of the Friend spleen focus-forming virus: deletion and insertions in 3´ gp70/pl 5E-encoding region have resulted in unique features in the primary structure of its protein product. Proc Natl Acad Sci USA 80:4718–4722PubMedGoogle Scholar
  118. Wolff L, Hubbert N, Ruscetti S (1984) Structural analysis of the spleen focus-forming virus envelope gene product. Virology 133:376–385PubMedGoogle Scholar
  119. Yamamoto Y, Gamble CL, Clark SP, Joyner A, Shibuya T, MacDonald ME, Mager D, Bernstein A, Mak TW (1981) Clonal analysis of early and late stages of erythroleukemia induced by molecular clones of integrated spleen focus-forming virus. Proc Natl Acad Sci USA 78:6893–6897PubMedGoogle Scholar
  120. Yoshida M, Yoshikura H (1980) Analysis of spleen focus-forming virus-specific RNA sequences coding for spleen focus-forming virus-specific glycoprotein with a molecular weight of 55,000 (gp55). J Virol 33:587–596PubMedGoogle Scholar
  121. Yoshida M, Yoshikura H (1981) A glycoprotein specified by spleen focus-forming virus in three cell lines varies in molecular size and peptide composition, but retains both xenotropic and ecotropic MuLV antigenicity. J Gen Virol 52:183–188PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1984

Authors and Affiliations

  • S. Ruscetti
    • 1
  • L. Wolff
    • 1
  1. 1.Laboratory of GeneticsNational Cancer InstituteBethesdaUSA

Personalised recommendations