Advertisement

Acute Avian Leukemia Viruses as Tools to Study Hematopoietic Cell Differentiation

  • K. M. McNagny
  • T. Graf
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 212)

Abstract

Hematopoiesis is a multistep process during which an uncommitted, self-renewing progenitor divides and differentiates along one of eight distinct lineages, each with a unique function and each expressing a unique complement of proteins enabling them to carry out these functions. In adult vertebrates, multipotent hematopoietic precursors reside within the microenvironment of the bone marrow where they undergo a progressive maturation and commitment to one of several lymphoid and nonlymphoid cell lineages. Regulation of normal hematopoietic development requires an intricate set of cues from stromal cells involving signaling via soluble growth factors, cell-cell and cell-extracellular matrix interactions (Quesenberry 1992). Analysis of the cellular intermediates in these differentiation pathways has been greatly facilitated by the development of in vitro colony forming assays for multipotent and monopotent hematopoietic precursors and the identification of cytokines which regulate their growth and differentiation (Metcale 1984, 1988). Nevertheless, analysis of the molecular mechanisms governing differentiation and commitment to a given lineage has been technically difficult as bone marrow precursors are present in relatively low frequency and reagents allowing their isolation have only recently been developed. In addition, obtaining clonal precursor cells in sufficient numbers for biochemical analysis has been problematic since these precursors have a limited life span in vitro.

Keywords

Erythroid Cell Erythroid Progenitor Erythroid Differentiation Permissive Temperature Helper Virus 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barettino D, Bugge TH, Bartunek P, Vivanco-Ruiz MD, Sonntag-Buck V, Beug H, Zenke M, Stunnenberg HG (1993) Unligated T3R, but not its oncogenic variant, v-erbA, suppresses RAR-dependent transactivation by titrating out RXR. EMBO J 12: 1343–1354PubMedGoogle Scholar
  2. Barth CF, Humphries EH (1988a) Expression of v-rel induces B-cell lines that reflect the diversity of avian immunoglobulin heavy-and light-chain rearrangements. Mol Cell Biol 8: 5358–5368PubMedGoogle Scholar
  3. Barth CF, Humphries EH (1988b) A nonimmunosupressive helper virus allows high efficiency induction of B cell lymphomas by reticuloendotheliosis virus strain T.J Exp Med 167: 89–108Google Scholar
  4. Barth CF, Ewert DL, Olson W C, Humphries EH (1990) Reticuloendotheliosis virus REV-T(REV-Alinduced Neoplasia: development of tumors within the T-Iymphoid and myeloid lineages. J Virol 64: 6054–6062PubMedGoogle Scholar
  5. Beug H, and Graf T (1989). Co-operation between viral oncogenes in avian erythroid and myeloid leukemia. Eur J Clin Invest 19: 491–502PubMedGoogle Scholar
  6. Beug H, von Kirchbach A, Döderlein G, Conscience J.-F, Graf T (1979) Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18: 375–390PubMedGoogle Scholar
  7. Beug H, Müller H, Grieser S, Doederlein G, Graf T (1981) Hematopoietic cells transformed in vitro by REV-T avian reticuloendotheliosis virus express characteristics of very immature lymphoid cells. Virology 115: 295–309PubMedGoogle Scholar
  8. Beug H, Palmieri S, Freudenstein C, Hanswalter Z, Graf T (1982) Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by is mutants of avian erythroblastosis virus. Cell 28: 907–919PubMedGoogle Scholar
  9. Beug H, Leutz A, Kahn P, Graf T ( 1984 Ts mutants of E26 leukemia virus allow transformed myeloblasts, but not erythroblasts or fibroblasts to differentiate at the nonpermissive temperature. Cell 39: 579–588PubMedGoogle Scholar
  10. Beug H, Hayman MJ, Graf T, Benedict SH, Wallbank AM, Vogt PK (1985a) S13, a rapidly oncogenic replication-defective avian retrovirus. Virology 145: 141–153PubMedGoogle Scholar
  11. Beug H, Kahn P, Doederlein G, Hayman MJ, Graf T (1985b) Characterization of hematopoietic cells transformed in vitro by AEV-H, a v-erbB-containing avian erythroblastosis virus. Springer Berlin Heidelberg New YorkGoogle Scholar
  12. Beug H, Blundell P, Graf T (1987) Reversibility of differentiation and proliferative capacity in avian myelomonocytic cells transformed by tsE26 leukemia virus. Genes Dev 1: 277–286PubMedGoogle Scholar
  13. Beug H, Müllner EW, Hayman MJ (1994) Insights into erythroid differentiation obtained from studies on avian erythroblastosis virus. Cur Opin Cell Biol 6: 816–824Google Scholar
  14. Bhat NK, Fisher R, Fujiwara S, Ascione R, Papas T (1987) Temporal and tissue-specific expression of mouse ets genes. Proc Natl Acad Sci USA 84: 3161–3165PubMedGoogle Scholar
  15. Bister K, Loliger, H.-C, Duesberg PH (1979) Oligonucleotide map or and protein of CMII:detection of conserved and nonconserved genetic elements in avian acute leukemia viruses CMII, MC29, and MH2. J Virol 32: 208–219PubMedGoogle Scholar
  16. Boehmelt G, Madruga J, Dörfler P, Briegel K, Schwarz H, Enrietto P, Zenke M (1995) Dendritic cell progenitor is transformed by a conditional v-Rel estrogen receptor fusion protein v-ReIER. Cell 80: I - 20Google Scholar
  17. Boehmelt G,Walker A, Kabrun N, Mellitzer G, Beug H, Zenke M, Enrietto P (1992) Hormone-regulated v-rel estrogen receptor fusion protein: reversible induction of cell transformation and cellular gene expression. EMBO J 11: 4641–4652PubMedGoogle Scholar
  18. Bose HR (1992) The Rel family: models for transcriptional regulation and oncogenic transformation. Bioch Bioph Acta 1114: 1–17Google Scholar
  19. Burk O, Mink S, Ringwald M, Klempnauer K.-H (1993) Synergistic activation of the chicken mim-1 gene by v-Myb and C/EBP transcription factors. EMBO J 12: 2027–2038PubMedGoogle Scholar
  20. Capobianco A, Gilmore T (1993). A conditional mutant of v-Rel containing sequences from the human eostrogen receptor. Virology 193: 160–170PubMedGoogle Scholar
  21. Choi O.-R, Trainor C, Graf T, Beug H, Engel JD (1986). A single amino acid substitution in v-erb8 confers a thermolabile phenotype tots 167 avian erythoblastosis virus-transformed erythroid cells. Mol Cell Bio 6: 1751–1759.Google Scholar
  22. Coll J, Righi M, deTaisne C, Dissous C, Gegonne G, Stehelin D (1983) Molecular cloning of the avian acute transforming retrovirus MH2 reveals a novel cell-derived sequence (v-mill) in addition to the myc oncogene. EMBO 2: 2189–2194.Google Scholar
  23. Damm K, Thompson CC, Evans RM (1989) Protein encoded by v-erbA functions as a thyroid-hormone receptor antagonist. Nature 339: 593–597PubMedGoogle Scholar
  24. Denhez F, Heimann B, d’Auriol L, Graf T, Coquillaud M, Coll J, Galibert F, Moelling K, Stehelin D, Ghysdael J (1988) Replacement of lys 622 in the ATP binding domain of P100gag-mil abolishes the in vitro autophosporylation of the protein and the biological properties of the v-mil oncogene of MH2 virus. EMBO J 7: 541–546PubMedGoogle Scholar
  25. Disela C, Glineur C, Bugge T, Sap J, Stengl G, Dodgson J, Stunnenberg H, Beug H, Zenke M (1991) v-erbA overexpression is required to extinguish c-erbA function in erythroid cell differentiation and regulation of the erbA target gene CAII. Genes Dev 5: 2033–2047PubMedGoogle Scholar
  26. Downward J, Yarden Y, Mayes E, Scrace G, Totty N, Stockwell P, Ulrich A, Schlessinger J, Waterfield MD (1984) Close similarity of epidermal growth factor receptor and v-erbB oncogene protein sequences. Nature 307: 521–527PubMedGoogle Scholar
  27. Duprey SP, Boettiger D (1985) Developmental regulation of c-myb in normal myeloid progenitor cells. Proc Natl Acad Sci USA 1985: 6937–6941Google Scholar
  28. Frampton J, McNagny KM, Sieweke M, Philip A, Smith G, Graf T (1995) Myb DNA binding is required to block thrombocytic differentiation of Myb-Ets transformed multipotent haematopoietic progenitors. EMBO J 14: 2866–2875PubMedGoogle Scholar
  29. Frykberg L, Palmieri S, Beug H, Graf T, Hayman MJ, Vennström B (1983) Transforming Capacities of avian erythroblastosis virus mutants deleted in the erbA or erbB oncogenes. Cell 32: 227–238PubMedGoogle Scholar
  30. Frykberg L, Metz T, Brady G, Introna M, Beug H, Vennstrom B, Graf T (1988) A point mutation in the DNA binding of the v-myb oncogene of E26 virus confers temperature sensitivity for transformation of myelomonocytic cells Oncogene Res 3: 3131–322Google Scholar
  31. Gandrillon O, Jurdic P, Pain B, Desbois C, Madjar JJ, Moscovici MG, Moscovivi C, Samarut J (1989) Expression of the v-erbA product, an altered nuclear hormone receptor, is sufficient to transform erythrocytic cells in vitro. Cell 58: 115–121Google Scholar
  32. Gazzolo L, Moscovici C, Moscovici MG, Samarut J (1979) Response of hemopoietic cells to avian acute leukemia viruses: effects on the differentiation of the target cells. Cell 16: 627–638PubMedGoogle Scholar
  33. Gilmore T D (1991) Malignant transformation by mutant Rel proteins. Trends Genet 7: 312–322Google Scholar
  34. Golay J, Introna M, Graf T (1988) A single point mutation in the v-ets oncogene affects both erythroid and myelomoncytic cell differentiation. Cell 55: 1147–1158PubMedGoogle Scholar
  35. Gonda TJ, Sheiness DK, Bishop JM (1982) Transcripts from the cellular homologs of retroviral oncogenes:distribution among chicken tissues. Mol Cell Biol 2: 617–624PubMedGoogle Scholar
  36. Graf T, Beug H (1978) Avian leukemia viruses:interaction with their target cells in vitro and in vivo. Biochim Biophys Acta 516: 269–299PubMedGoogle Scholar
  37. Graf T, Stéhelin D (1982) Avian leukemia viruses: oncogenes and genome structure. Biochim Biophys Acta 651: 245–271PubMedGoogle Scholar
  38. Graf T, Ade N, Beug H (1978) Temperature-sensitive mutant of avian erytroblastosis virus suggests a block of differentiation as mechanism of leukaemongenesis. Nature 247: 496–501Google Scholar
  39. Graf T, von Kirchbach A, Beug H (1981) Characterization of the hematopoietic targetcells of AEV, MC29 and AMV avian acute leukemia viruses. Exp Cell Res 131: 331–343Google Scholar
  40. Graf T, von Weizsecker F, Grieser S, Coll J, Stehelin D, Patschinsky T, Bister K., Bechade C, Calothy G, Leutz A (1986) v-mill induces autocrine growth and enhanced tumorigenicity in v-myc-transformed avian macrophages. Cell 45: 357–364Google Scholar
  41. Graf T, McNagny K, Brady G, Frampton J (1992) Chicken ‘erythroid cells transformed by the gag-mybets-encoding E26 leukemia virus are multipotent. Cell 70: 201–213PubMedGoogle Scholar
  42. Hayman MJ, Meyer S, Martin F, Steinlein P, Beug H (1993) Self-renewal and differentiation of normal avian erythroid progenitor cells: regulatory roles of the TGF/a/c-erbB and SCF/c-Kit receptors. Cell 74: 157–169PubMedGoogle Scholar
  43. Hermann T, Hoffman B, Piedrafita FJ, Zhang XK, Pfahl M (1993) V-erbA requires auxiliary proteins for dominant negative activity. Oncogene 8: 55–65PubMedGoogle Scholar
  44. Hrdlickova R, Nehyba J, Humphries EH (1944) In vivo evolution of c-re/ oncogenic potential. J Virol 68: 2371–2382Google Scholar
  45. Hu W-S, Temin HM (1990) Retroviral replication and reverse transcription. Science 250: 1227–1233PubMedGoogle Scholar
  46. Huff JL, Jelinek MA, Borgman CA, Lansing TJ, Parsons JT (1993) The protooncogene c-sea encodes a transmembrane protein-tyrosine kinase related to the Met/hepatocyte growth factor/scatter factor receptor. Proc Natl Acad Sci USA 90: 6140–6144PubMedGoogle Scholar
  47. Introna M, Golay J, Frampton J, Nakano T, Ness S, Graf T (1990) Mutations in v-myb alter the differentiation of myelomonocytic cells transformed by the oncogene. Cell 63: 1287–1297Google Scholar
  48. Jansen HW, Ruckert B, Lurz R, Bister K (1983) Two unrelated cell-derived sequences in the genome of avian leukemia and carcinoma inducing retrovirus MH2. EMBO J 2: 1969–1975PubMedGoogle Scholar
  49. Kabrun N, Enrietto PJ (1994) The Rel family of proteins in oncogenesis and differentiation. Semin Cancer Biol. 5: 103–112PubMedGoogle Scholar
  50. Kahn P, Leutz A, Graf T (1986) Individual and combined effects of viral oncogenes in hematopoietic cells. Berlin Heidelberg New YorkGoogle Scholar
  51. Kan NC, Flordellis CS, Garon GF, Deusberg PH, Papas TS (1983) Avian carcinoma virus MH2 contains a transformation specific sequence, mhtand shares the myc sequence with MC29, CMI I, and OK10 viruses. Proc Natl Acad Sci USA 80: 6566–6570PubMedGoogle Scholar
  52. Katz S, Kowenz-Leutz E, Müller C, Meese K, Ness SA, Leutz A (1993) The NF-M transcription factor is related to C/EBP3 and plays a role in signal transduction, differentiation, and leukemogenesis of avian myelomonocytic cells. EMBO J 12: 1321–1332PubMedGoogle Scholar
  53. Kim S, Humphries EH, Tjoelker L, Carlson L, Thompson CB (1990) Ongoing diversification of the rearranged immunoglobulin light-chain gene in a bursal lymphoma cell line. Mol Cell Biol 10: 3224–3231PubMedGoogle Scholar
  54. Knight J, Zenke M, Disela C, Kowenz E, Vogt P, Engel JD, Hayman MJ, Beug H (1988) Temperature-sensitive v-sea transformed erythroblasts: a model system to study gene expression during erythroid differentiation. Genes Dev 2: 247–258PubMedGoogle Scholar
  55. Kraut N, Frampton J, McNagny KM, Graf T (1994) A functional Ets DNA-binding domian is required to maintain multipotency of hematopoietic progenitors transformed by Myb-Ets. Genes Dev 8: 33–44PubMedGoogle Scholar
  56. Kraut N, Frampton J, Graf T (1995) Rem-1, a putative direct target gene of the Myb-Ets fusion oncoprotein in haematopoietic progenitors, is a member of the recoverin family. Oncogene 10: 1027–1036PubMedGoogle Scholar
  57. Kleessa H, Frampton J, Graf T (1995) GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts, Genes Dev 9: 1250–1262Google Scholar
  58. Lax I, Johnson A, Howk R, Sap J, Bellot F, Winkler M, Ulrich A, Vennström B, Schlessinger J, Givol D (1988) Chicken epidermal growth factor (EGF) receptor: cDNA cloning, expression in mouse cells and differential binding of EGF and transforming growth factor-alpha. Mol Cell Biol 8: 1970–1978.PubMedGoogle Scholar
  59. Leprince D, Gegonne A, Coll J, de Taisne C, Schneeberger A, Lagrou C, Stehelin D (1983) A putative second cell-derived oncogene of the avian leukemia retrovirus E26. Nature 306: 395–397PubMedGoogle Scholar
  60. Leutz A, Beug H, Graf T (1984) Purification and characterization of cMGF, a novel chicken myelomoncytic growth factor. EMBO J 3: 3191–3197PubMedGoogle Scholar
  61. Leutz A, Damm K, Sterneck E, Kowenz E, Ness S, Frank R, Gausephol H, Pany YCE, Smart J, Hayman M, Graf T (1989) Molecular cloning of the chicken myelomoncytic growth factor. EMBO J 8: 175–181PubMedGoogle Scholar
  62. Lewis RBJM, Rub B, Nielsel DW, Garry RF, Hoelzer JD, Nazerian K, Bose HR (1981) Avian reticuloendotheliosis virus:identification of the hematopoietic target cell for transformation. Cell 25: 421–431PubMedGoogle Scholar
  63. Luciw PA, Leung LN (1992) Mechanisms of retrovirus replication. Plenum, New YorkGoogle Scholar
  64. Maldonado RL, Bose HR (1973) Relationship of reticuloendotheliosis virus to the avian tumor viruses:nucleic acid and polypeptide composition. J Virol 11: 741–747PubMedGoogle Scholar
  65. Marmor MD, Benater T, Ratcliffe MJH (1993) Retroviral transformation in vitro of chicken T cells expressing either a/ß or y/ST cell receptors by reticulendotheiliosis virus strain T.J Exp Med 177: 647–656Google Scholar
  66. McNagny KM, Lim F, Grieser S, Graf T (1992) Cell surface proteins of chicken hematopoietic progenitors, thrombocytes and eosinophils detected by novel monoclonal antibodies. Leukemia 6: 975–984PubMedGoogle Scholar
  67. Metcalf D (1984) The hematopoietic stimulating factors. Elsevier New YorkGoogle Scholar
  68. Metcalf D (1988) The molecular control of blood cells. Harvard University Press, CambridgeGoogle Scholar
  69. Metz T (1994) Oncogenes and erythroid differentiation. Semin Cancer Biol 5: 125–135PubMedGoogle Scholar
  70. Metz T, Graf T (1991a) Fusion of the nuclear oncoproteins v-myb and v-ets is required for the leukemogenicity of E26 virus. Cell 66: 95–105PubMedGoogle Scholar
  71. Metz T, Graf T (1991b) V-myb and v-ets transform chicken erythroid cells and cooperate both in trans and in cis to induce distinct differentiation phenotypes. Genes Dev. 5: 369–380PubMedGoogle Scholar
  72. Mizutani S, Temin HM (1973) Lack of serological relationship among DNA polymerases of avian leukosis-sarcoma viruses, reticuloendotheliosis virus, and chicken cells. J Virol. 12: 440–448PubMedGoogle Scholar
  73. Moelling K, Gelderblom H, Pauli G, Friis R, Bauer H (1975) A comparative study of the avian reticuloendotheliosis virus:relationship to murine leukemia virus and viruses of the avian sarcomaleukosis complex. Virology 65: 546–557.PubMedGoogle Scholar
  74. Moelling K, Heimann B, Beimling P, Rapp UR, Sander T (1984) Serine and threonine-specific protein protein kinase activities of purified gag-mil and gag-raf proteins. Nature 312: 558–561PubMedGoogle Scholar
  75. Morgan BA, lzpisua-Belmonte J-C, Duboule D, Tabin CJ (1992) Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358: 236–239PubMedGoogle Scholar
  76. Morrison LE, Boehmelt G, Beug H, Enrietto P (1991) Expression of v-rel in a replication competent virus:transformation and biochemical characterization. Oncogene 6: 1657–1666PubMedGoogle Scholar
  77. Moscovici C, Gazzolo L (1982) Transformation of hemopoietic cells with avian leukemia viruses. In: Klein G (ed) Advances in viral oncology. Raven, New York; pp 83–106Google Scholar
  78. Moscovici MG, Jurdic P, Samarut J, Gazzolo L, Mura CV, Moscovici C (1983) Characteristics of the hemopoietic target cells for the avian leukemia virus E26. Virology 129: 65–78PubMedGoogle Scholar
  79. Mucenski MI, Mclain K, Kier AB, Swerdlow SH, Schreiner CM, Miller TA, Pietryga DW, Scott WJ, Potter SS (1991) A functional c-myb gene is required for normal mouse fetal hepatic hematopoiesis. Cell 65: 677–689PubMedGoogle Scholar
  80. Ness SA, Engel JD (1994) Vintage reds and whites:combinatorial transcription factor utilization in hematopoietic differentiation. Cur Opin Gen Dev 4: 718–724Google Scholar
  81. Ness S, Beug H, Graf T (1987) v-myb dominance over v-myc in doulby transformed chick myelomoncytic cells. Cell 51: 41–50PubMedGoogle Scholar
  82. Ness SA, Marknell A, Graf T (1989) The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell 59: 1115–1125PubMedGoogle Scholar
  83. Ness SA, Kowenz-Leutz E, Casini T, Graf T, Leutz A (1993) Myb and NF-M:combinatorial activators of myeloid genes in heterologous cell types. Genes Dev. 7: 749–759PubMedGoogle Scholar
  84. Nunn M, Seeburg PH, Moscovici C, Duesberg PH (1983) Tripartite structure of the avian erythroblastosis virus E26 transforming gene. Nature 306: 391–395PubMedGoogle Scholar
  85. Pain B, Melet F, Jurdic P, Samarut J (1990) The carbonic anhydrase II gene, a gene regulated by thyroid hormone and erythropoietin, is repressed by the v-erbA oncogene in erythrocytic cells. New Biol 2: 284–294PubMedGoogle Scholar
  86. Pain B, Woods CM, Saez J, Flickinger T, Raines M, Peyrol S, Moscovici C, Moscovici MG, Kung HJ, Jurdic P, Lazarides E, Samarut J (1991) EGF-R as a hematopoietic growth factor receptor: the c-erbB product is present in chicken erythrocytic progenitors and controls their self-renewal. Cell 65: 37–46PubMedGoogle Scholar
  87. Pathak VK, Temin HM (1990a) Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shutte vectro after a single replication cycle: deletions and deletions with insertions. Proc Natl Acad Sci USA 87: 6024–6028PubMedGoogle Scholar
  88. Pathak VK, Temin HM (1990b). Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vectro after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc Natl Acad Sci USA 87: 6019–6023PubMedGoogle Scholar
  89. Payne LN (1992). Biology of avian retroviruses. Plenum, New YorkGoogle Scholar
  90. Pessano S, Gazzolo L, Moscivici C (1979). The effect of tumor promoter on avian leukemic cells. Microbiologica 2: 379–392Google Scholar
  91. Quesenberry PJ (1992). Stroma-dependent hematolympoietic stem cells. Springer, Berlin Heidelberg New YorkGoogle Scholar
  92. Radke K, Beug H, Kornfeld S, Graf T (1982). Transformation of both erythroid and myeloid cells by E26, an avian leukemia virus that contains the myb gene. Cell 31: 643–653PubMedGoogle Scholar
  93. Roussel M, Saule S, Lagrou C, Rommens C, Beug H, Graf T, Stehelin D (1979). Three new types of viral oncogenes of cellular origin specific haematopoietic cell transfromation. Nature 281: 452–455PubMedGoogle Scholar
  94. Samarut J, Gazzolo L (1982). Target cells infected by avian erythroblastosis virus differentiate and become transformed. Cell 28: 921–929PubMedGoogle Scholar
  95. Sap J, Munoz A, Damm K, Goldberg Y, Ghysdael J, Leutz A, Beug H, Vennström B (1986). The c-erbA protein is a high affinity receptor for thyroid hormone. Nature 324: 635–640PubMedGoogle Scholar
  96. Sap J, Munoz A, Schmitt J, Stunnenberg H, Vennström B (1989). Repression of transcription mediated at a thyroid hormone response element by the v-erbA oncogene product. Nature 340: 242–244PubMedGoogle Scholar
  97. Sarkar S, Gilmore TD (1993). Transformation by the vRel oncoprotein requires sequences carboxyterminal to the Rel homology domain. Oncogene 8: 2245–2252PubMedGoogle Scholar
  98. Schroedere C, Raynoschek C, Fuhrmann U, Damm K, Vennström B, Beug H (1990). The v-erbA oncogene causes repression of erythrocyte-specific genes and an immature, aberrant differentiation in normal erythroid progenitors. Oncogene 5: 1445–1453Google Scholar
  99. Schroeder C, Gibson L, Zenke M, Beug H (1992). Modulation of normal erythroid differentiation by the endogenous thyroid hormone and retinoic acid receptors: a possible target for v-erbA oncogen action, Oncogene 7: 217–227PubMedGoogle Scholar
  100. Schroeder C, Gibson L, Nordstrom C, Beug H (1993). The estrogen receptor cooperates with the TGFa receptor (c-erb8) in the regulation of chicken erythroid progenitor self-renewal. EMBO J 12: 951–960PubMedGoogle Scholar
  101. Steinlein P, Wessely O, Meyer S, Deiner E-M, Hayman MJ, Beug H (1995). Triggering the development of self-renewing erythroid progenitors. Curr Biol 5: 191–204PubMedGoogle Scholar
  102. Stephens RM, Rice NR, Hiebsch RR, Bose HR, Gilden RV (1983). Nucleotide sequence of v-rel: the oncogen of reticuloendotheliosis virus. Proc Natl Acad Sci USA 80: 6229–6233PubMedGoogle Scholar
  103. Sutrave P, Bonner TI, Rapp UR, Jansen HW, Patschinsky T, Bister K (1984). Nucleotide sequence of avian retroviral oncogene v-mil: homologue of murine retroviral oncogene v-raf. Nature 309: 85–88.PubMedGoogle Scholar
  104. Vandenbunder B, Pardanaud L, Jaffredo T, Mirabel MA, Stehelin D (1989). Complementary patterns of c-ets 1 c-myb and c-myc in the blood forming system of the chick embryo. Development 106: 265–274Google Scholar
  105. Vennström B, Bishop JM (1982). Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell 28: 135–143PubMedGoogle Scholar
  106. Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol DJ, Evand RM (1986). The c-erbA gene encodes a throid hormone receptor. Nature 324: 641–646PubMedGoogle Scholar
  107. Westin EH, Gallo RC, Arya SK, Eva A, Souza LM, Baluda MA, Aaronson SA, Wong-Staal F (1982) Differential expression of the AMV gene in human hematopoietic cells. Proc Natl Acad Sci USA 79: 2194–2198PubMedGoogle Scholar
  108. White DW, Roy A, Gilmore TD (1995). The v-Rel oncoprotein blocks apoptosis and proteolysis of IKBa in transformed chicken spleen cells. Oncogene 9: (in press)Google Scholar
  109. Yamamoto T, Nishida T, Mitajimi N, Kawai S, Ooi T, Toyoshima K (1983). The erbB gene of avian erythroblastosis virus is a member of the src gene family. Cell 35: 71–78PubMedGoogle Scholar
  110. Zenke M, Kahn P, Disela C, Vennström B, Leutz A, Keegan K, Hayman MJ, Choi HR, Yew N, Engle JD, Beug H (1988). V-erbA specifically supresses transcription of the avian erythrocyte anion transporter (band 3) gene. Cell 52: 107–119PubMedGoogle Scholar
  111. Zenke M, Munoz A, Sap J, Vennström B, Beug H (1990). V-erbA oncogene activation entails loss of hormone-dependent regulator activity of c-erbA. Cell 61: 1035–1049PubMedGoogle Scholar
  112. Zhang J, Termin HM (1993). Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication. Science 259: 234–238PubMedGoogle Scholar
  113. Zhang J, Bargmann W, Bose HRJ (1989). Rearrangement and diversification of immunoglobulin light-chain genes in lymphoid cells transformed by reticuloendotheliosis virus. Mol Cell Biol 9: 4970–4976PubMedGoogle Scholar
  114. Zhang J, Olson W, Ewert D, Bargmann W, Bose HRJ (1991). The v-rel oncogene of avian reticuloendotheliosis virus transforms immature and mature lymphoid cells of the B cell lineage in vitro. Virology 183: 457–466PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • K. M. McNagny
    • 1
  • T. Graf
    • 1
  1. 1.Differentiation ProgrammeEuropean Molecular Biology LaboratoryHeidelbergGermany

Personalised recommendations