Asymmetric Chromosomal Distribution of Endogenous Retrovirus Loci in Chickens and Mice

  • Allan Tereba
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 107)


Retrovirus-like sequences have been found in the genomes of a large number of species (Coffin 1982). These sequences are inherited in a Mendelian fashion, appear to be stable loci, and can be considered an integral part of an individual’s genetic makeup. However, analysis of related species (Frisby etal. 1979) and some related sublines (Rowe and Kozak 1980) has revealed that these sequences are probably due to rare integration events following infections of gamete or embryonic tissue. The genetic loci resulting from this unique occurrence in animal virology provide an excellent opportunity to observe the interactions of exogenously introduced DNA with a vertebrate genome in a multitude of cell types and at different stages of differentiation


Long Terminal Repeat Murine Leukemia Virus Somatic Cell Hybrid White Leghorn Chicken Viral Locus 
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. Aaronson SA, Stephenson JR (1973) Independent segregation of loci for activation of biologi-cally distinguishable RNA C–type viruses in mouse cells. Proc Natl Acad Sci USA 70: 2055–2058CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ada G, Humphrey JH, Askonas BA, McDevitt HO, Nossal GJV (1966) Correlation of grain counts with radioactivity (125I and tritium) in autoradiography. Exp Cell Res 41: 557–572CrossRefPubMedGoogle Scholar
  3. Astrin SM (1978) Endogenous viral genes of the White Leghorn chicken: common site of residence and sites associated with specific phenotypes of viral gene expression. Proc Natl Acad Sci, USA 75: 5941–5945CrossRefPubMedPubMedCentralGoogle Scholar
  4. Astrin SM, Robinson HL (1979) Gs, an allele of chickens for endogenous avian leukosis viral antigens, segregates with ev3, a genetic locus that contains structural genes for virus. J Virol 31: 420–425PubMedPubMedCentralGoogle Scholar
  5. Astrin SM, Crittenden LB, Buss EG (1979) Ev3, a structural gene locus for endogenous virus, segregates with the gs+chf+ phenotype in matings of line 63 chickens. Virology 99: 1–9CrossRefPubMedGoogle Scholar
  6. Astrin SM, Crittenden LB, Buss EG (1980) Ev2, a genetic locus containing structural genes for endogenous virus, codes for Rous-associated virus type 0 produced by line 12 chickens. J Virol 33: 250–255PubMedPubMedCentralGoogle Scholar
  7. Bacon LD (1979) Origin of inbred and genetically defined strains of chickens. In: Altman PL, Katz DD (eds) Inbred and genetically defined strains of laboratory animals. Federation of American Societies for Experimental Biology, Bethesda, p 607Google Scholar
  8. Baker B, Robinson H, Varmus HE, Bishop JM (1981) Analysis of endogenous avian retrovirus DNA and RNA: viral and cellular determinants of retrovirus gene expression. Virology 114: 8–22CrossRefPubMedGoogle Scholar
  9. Barbacid M, Robbins KC, Hino S, Aaronson SA (1978) Genetic recombination between mouse type C RNA viruses: a mechanism for endogenous viral gene amplication in mammalian cells. Proc Natl Acad Sci USA 75: 923–927CrossRefPubMedPubMedCentralGoogle Scholar
  10. Besmer P, Olshevsky U, Baltimore D, Dolberg D, Fan H (1979) Virus-like 30S RNA in mouse cells. J Virol 29: 1168–1176PubMedPubMedCentralGoogle Scholar
  11. Breindl M, Doehmer J, Willecke K, Dausman J, Jaenisch R (1979) Germ line integration of Moloney leukemia virus: identification of the chromosomal integration site. Proc Natl Acad Sci USA 76: 1938–1942CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brown E (1906) Races of domestic poultry. Arnold, London, p 40Google Scholar
  13. Canaani E, Aaronson SA (1979) Restriction enzyme analysis of mouse cellular type C viral DNA: emergence of new viral sequences in spontaneous AKR/J lymphomas. Proc Natl Acad Sci USA 76: 1677–1681CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chattopadhyay SK, Rowe WP, Teich NM, Lowy DR (1975) Definitive evidence that the murine C-type virus inducing locus AKV-1 is viral genetic material. Proc Natl Acad Sci USA 72: 906–910CrossRefPubMedPubMedCentralGoogle 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: 465–483CrossRefPubMedGoogle Scholar
  16. Coffin J (1982) Endogenous viruses. In: Weiss R, Teich N, Varmus H, Coffin J (eds). RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 1109–1203Google Scholar
  17. Cohen JC, Varmus HE (1979) Endogenous mammary tumor virus DNA varies among wild mice and segregates during inbreeding. Nature 278: 418–423CrossRefPubMedGoogle Scholar
  18. Crittenden LB, Astrin SM (1981) Independent segregation of evl and evlO, genetic loci for spontaneous production of endogenous avian retroviruses. Virology 110: 120–127CrossRefPubMedGoogle Scholar
  19. Ertl HH, Feinendegen LE, Heiniger HJ (1970) Iodine-125, a tracer in cell biology: physical properties and biological aspects. Phys Med Biol 15: 447–456CrossRefPubMedGoogle Scholar
  20. Frisby DT, Weiss RA, Roussel M, Stehelin D (1979) The distribution of endogenous chicken retrovirus sequences in the DNA of galliform birds does not coincide with avian phytogenetic relationships. Cell 17: 623–634CrossRefPubMedGoogle Scholar
  21. Hayward WS, Braverman SB, Astrin SM (1980) Transcriptional products and DNA structure of endogenous avian proviruses. Cold Spring Harbor Symp Quant Biol 44: 1111–1122CrossRefPubMedGoogle Scholar
  22. Hishinuma F, DeBona PJ, Astrin SM, Skalka AM (1981) Nucleotide sequence of acceptor site and termini of integrated avian endogenous pro virus evl: integration creates a 6 bp repeat of host DNA. Cell 23: 155–164CrossRefPubMedGoogle Scholar
  23. Hughes SH, Shank PR, Spector DH, Kung H–J, Bishop JM, Varmus HE, Vogt PK, Breitman ML (1978) Proviruses of avian sarcoma virus are terminally redundant co-extensive with unintegrated linear DNA, and integrate at many sites. Cell 15: 1397–1410CrossRefPubMedGoogle Scholar
  24. Hughes SH, Stubblefield E, Payvar F, Engel JD, Dodgson JB, Spector D, Cordell B, Schimke RT, Varmus HE (1979a) Gene localization by chromosome fractionation: globin genes are on at least two chromosomes and three estrogen-inducible genes are on three chromosomes. Proc Natl Acad Sei USA 76: 1348–1352CrossRefGoogle Scholar
  25. Hughes SH, Farhang P, Spector D, Schimke RT, Robinson HL, Payne GS, Bishop JM, Varmus HE (1979b) Heterogeneity of genetic loci in chickens: analysis of endogenous viral and nonviral genes by cleavage of DNA with restriction endonucleases. Cell 18: 347–359CrossRefPubMedGoogle Scholar
  26. Hughes SH, Bishop JM, Varmus HE (1981) Organization of the endogenous proviruses of chickens: implications for origin and expression. Virology 108: 189–207CrossRefPubMedGoogle Scholar
  27. Ihle JN, Joseph DR, Domotor JJ Jr (1979) Genetic linkage of C3H/HJ and BALB/c endogenous ecotropic C-type viruses to phosphoglucomutase-1 on chromosome 5. Science 204: 71–73CrossRefPubMedGoogle Scholar
  28. Jaenisch R (1980) Germ line integration and Mendelian transmission of exogenous type C viruses. In: Stephenson J (ed) Molecular biology of RNA tumor viruses. Academic, New York, pp 131–162Google Scholar
  29. Jaenisch R, Jähner D, Nobis P, Simon I, Lohler J, Harbers K, Grotkopp G (1981) Chromosomal position and activation of retroviral genomes inserted into the germline of mice. Cell 24: 519–529CrossRefPubMedGoogle Scholar
  30. Jähner D, Jaenisch R (1980) Integration of Moloney leukaemia virus into the germ line of mice: correlation between site of integration and virus activation. Nature 287: 456–458CrossRefPubMedGoogle Scholar
  31. Jenkins NA, Copeland NG, Taylor BA, Lee BK (1981) Dilute(d) coat colour mutation of DBA/2J mice is associated with the site of integration of an ecotropic MuLV genome. Nature 293: 370–374CrossRefPubMedGoogle Scholar
  32. Jenkins NA, Copeland N, Lee B, Taylor B (1982) In: Weiss R, Teich N, Varmus H, Coffin J (eds) RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 1150–1151Google Scholar
  33. Jolicoeur P, Rassant E, Kozak C, Ruddle F, Baltimore D (1980) Distribution of endogenous murine leukemia virus DNA sequences among mouse chromosomes. J Virol 33:1229– 1235Google Scholar
  34. Ju G, Skalka AM (1980) Nucleotide sequence analysis of the long terminal repeat (LTR) of avian retroviruses: structural similarities with transposable elements. Cell 22: 379–386CrossRefPubMedGoogle Scholar
  35. Kozak CA, Rowe WP (1978) Genetic mapping of xenotropic leukemia virus–inducing loci in two mouse strains. Science 199: 1448–1449CrossRefPubMedGoogle Scholar
  36. Kozak CA, Rowe WP (1979) Genetic mapping of the ecotropic murine leukemia virus-inducing locus of BALB/c mouse to chromosome 5. Science 204: 69–71CrossRefPubMedGoogle Scholar
  37. Kozak CA, Rowe WP (1980 a) Genetic mapping of xenotropic murine leukemia virus-inducing loci in five mouse strains. J Exp Med 152: 219–228Google Scholar
  38. Kozak CA, Rowe WP (1980b) Genetic mapping of the ecotropic virus–inducing locus AKV-2 of the AKR mouse. J Exp Med 152: 1419–1423CrossRefPubMedGoogle Scholar
  39. Kozak CA, Rowe WP (1982) Genetic mapping of ecotropic murine leukemia virus-induced loci in six inbred strains. J Exp Med 155: 524–534CrossRefPubMedGoogle Scholar
  40. Levy JA (1978) Xenotropic type C viruses. Curr Top Microbiol Immunol 79: 109–213Google Scholar
  41. Long CA, Dumaswala UJ, Tancin SL, Vaidya AB (1980) Organization and expression of endogenous murine mammary tumor virus genes in mice congenic at the H-2 complex. Virology 103: 167–177CrossRefPubMedGoogle Scholar
  42. Michalides RE, Wagenaar E, Groner B, Hynes NE (1981) Mammary tumor virus pro viral DNA in normal murine tissue and non-virally induced mammary tumors. J Virol 39: 367–376PubMedPubMedCentralGoogle Scholar
  43. Morris VL, Medeiros E, Ringold GM, Bishop JM, Varmus HE (1977) Comparison of mouse mammary tumor virus-specific DNA in inbred, wild and Asian mice and in tumors and normal organs from inbred mice. J Mol Biol 114: 73–91CrossRefPubMedGoogle Scholar
  44. Morris VL, Kozak C, Cohen JC, Shank PR, Jolicoeur P, Ruddle F, Varmus HE (1979) Endogenous mouse mammary tumor virus DNA is distributed among multiple mouse chromosomes. Virology 92: 46–55CrossRefPubMedGoogle Scholar
  45. Morse HC III, Chused TM, Hartley JW, Mathieson BJ, Sharrow SO, Taylor BA (1979) Expression of xenotropic murine leukemia viruses as cell-surface gp70 in genetic crosses between strains DBA/2 and C57BL/6. J Exp Med 149: 1183–1196CrossRefPubMedGoogle Scholar
  46. Nüsse R, DeMoes J, Hilkens J, Van Nie R (1980) Localization of a gene for expression of mouse mammary tumor virus antigens in the GR/Mtv-2- mouse strain. J Exp Med 152: 712–719CrossRefPubMedGoogle Scholar
  47. Ohno S (1961) Sex chromosomes and microchromosomes of Gallus domesticus. Chromosoma 11: 484–498CrossRefPubMedGoogle Scholar
  48. Old LJ, Stockert E (1977) Immunogenetics of cell surface antigens of mouse leukemia. Annu Rev Genet 11: 127–160CrossRefPubMedGoogle Scholar
  49. Padgett TG, Stubblefield E, Varmus HE (1977) Chicken macrochromosomes contain an endogenous provirus and microchromosomes contain sequences related to the transforming gene of ASV. Cell 10: 649–657CrossRefPubMedGoogle Scholar
  50. Pincus T (1980) The endogenous murine type C virus. In: Stephenson J (ed) Molecular biology of RNA tumor viruses: Academic, New York, pp 77–130Google Scholar
  51. Potter M, Klein J (1979) Genealogy of the more commonly used inbred mouse strains. In: Altman PL, Katz DD (eds) Inbred and genetically defined strains of laboratory animals. Federation of American Societies for Experimental Biology, Bethesda, p 16Google Scholar
  52. Robinson HL, Astrin SM, Salazar FH (1979) V–15B, an allele of chickens for the production of a noninfectious avian leukosis virus. Virology 99: 10–20CrossRefPubMedGoogle Scholar
  53. Rommelaere J, Faller DV, Hopkins N (1977) RNase Trresistant oligonucleotides of AKV-1 and AKV-2 type C viruses of AKR mice. J Virol 24: 690–694PubMedPubMedCentralGoogle Scholar
  54. Rovigatti UG, Astrin SM (1983) Avian endogenous viral genes. Curr Top Microbiol Immunol 103: 1–21PubMedGoogle Scholar
  55. Rowe WP (1972) Studies of genetic transmission of murine leukemia viruses by AKR mice. I crosses with Fv-ln strains of mice. J Exp Med 136: 1272–1285CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rowe WP, Kozak CA (1980) Germ–line reinsertions of AKR murine leukemia virus genomes in AKV-1 congenic mice. Proc Natl Acad Sei USA 77: 4871–4874CrossRefGoogle Scholar
  57. Rowe WP, Hartley JW, Bremmer T (1972) Genetic mapping of a murine leukemia virus-inducing locus of AKR mice. Science 178: 860–862CrossRefPubMedGoogle Scholar
  58. Scolnick EM, Vass WC, Howk RS, Duesberg PH (1979) Defective retrovirus-like 30S RNA species of rat and mouse cells are infectious if packaged by C helper virus. J Virol 29: 964–972PubMedPubMedCentralGoogle Scholar
  59. Smith EJ, Crittenden LB (1981) Segregation of chicken endogenous viral loci evl and ev\2 with the expression of infectious subgroup E avian leukosis viruses. Virology 112: 370–373Google Scholar
  60. Somes RG Jr (1979) New linkage groups and revised chromosome map of the domestic fowl. J Hered 69: 401–403Google Scholar
  61. Steffen D, Weinberg RA (1978) The integrated genome of murine leukemia virus. Cell 15: 1003–1010CrossRefPubMedGoogle Scholar
  62. Stephenson JR, Aaronson SA (1973) Segregation of loci for C-type virus induction in strains of mice with high and low incidence of leukemia. Science 180: 865–866CrossRefPubMedGoogle Scholar
  63. Stephenson JR, Tronick SR, Reynolds RK, Aaronson SA (1974) Isolation and characterization of C-type viral gene products of virus–negative mouse cells. J Exp Med 139: 427–438CrossRefPubMedPubMedCentralGoogle Scholar
  64. Stockert E, Old LJ, Boyse EA (1971) The GIX system. A cell surface allo-antigen associated with murine leukemia virus; implication regarding chromosomal integration of the viral genome. J Exp Med 133: 1334–1355Google Scholar
  65. Stubblefield E, Oro J (1982) The isolation of specific chicken macrochromosomes by zonal centrifugation and flow sorting. Cytometry 2: 273–281CrossRefGoogle Scholar
  66. Temin HM (1980) Origin of retroviruses from cellular movable genetic elements. Cell 21: 599–600CrossRefPubMedGoogle Scholar
  67. Tereba A (1981) S’-Terminal deletions are a common feature of endogenous retrovirus loci located on chromosome 1 of White Leghorn chickens. J Virol 40: 920–926PubMedPubMedCentralGoogle Scholar
  68. Tereba A, Astrin SM (1980) Chromosomal localization of ev-1, a frequently occurring endogenous retrovirus locus in White Leghorn chickens, by in situ hybridization. J Virol 35: 888–894PubMedPubMedCentralGoogle Scholar
  69. Tereba A, Astrin SM (1982) Chromosomal clustering of five endogenous retrovirus loci in White Leghorn chickens. J Virol 43: 737–740PubMedPubMedCentralGoogle Scholar
  70. Tereba A, Lai MMC (1982) Cell oncogenes are located on the large microchromosomes in chicken cells. Virology 116: 654–657CrossRefPubMedGoogle Scholar
  71. Tereba A, Lai MMC, Murti KG (1979) Chromosome 1 contains the endogenous RAV-0 retrovirus sequences in chicken cells. Proc Natl Acad Sci, USA 76: 6486–6490Google Scholar
  72. Tereba A, Crittenden LB, Astrin SM (1981) Chromosomal localization of three endogenous retrovirus loci associated with virus production in White Leghorn chickens. J Virol 39: 282–289PubMedPubMedCentralGoogle Scholar
  73. Traina VL, Taylor BA, Cohen JC (1981) Genetic mapping of endogenous mouse mammary tumor viruses: locus characterization, segregation, and chromosomal distribution. J Virol 40: 735–744PubMedPubMedCentralGoogle Scholar
  74. Van Nie R, Verstraeten AA (1975) Studies of genetic transmission of mammary tumor virus by C3Hf mice. Int J Cancer 16: 922–931CrossRefPubMedGoogle Scholar
  75. Verstraeten AA, Van Nie R (1978) Genetic transmission of mammary tumor virus by the DBAf mouse strain. Int J Cancer 21: 473–475CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1983

Authors and Affiliations

  • Allan Tereba
    • 1
  1. 1.St. Jude Children’s Research HospitalMemphisUSA

Personalised recommendations