1887

Abstract

Murine leukaemia virus has been suggested to contribute to both autoimmune disease and leukaemia in the NZB mouse and in the (NZB × NZW) F1 (abbreviated B/W) mouse. However, with apparently only xenotropic but no ecotropic virus constitutively expressed in these mice, few mechanisms could explain the aetiology of either disease in either mouse strain. Because pseudotyped and/or inducible ecotropic virus may play a role, we surveyed the ability of murine leukaemia virus in NZB, NZW and B/W mice to infect and form a provirus. From the spleen of NZB mice, we isolated circular cDNA of xenotropic and polytropic virus, which indicates ongoing infection by these viruses. From a B/W lymphoma, we isolated and determined the complete sequence of a putative ecotropic NZW virus. From B/W mice, we recovered endogenous retroviral integration sites (tags) from the hyperproliferating cells of the spleen and the peritoneum. The tagged genes seemed to be selected to aid cellular proliferation, as several of them are known cancer genes. The insertions are consistent with the idea that endogenous retrovirus contributes to B-cell hyperproliferation and progression to lymphoma in B/W mice.

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2015-11-01
2024-04-23
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References

  1. Akagi K., Suzuki T., Stephens R.M., Jenkins N.A., Copeland N.G. 2004; RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res 32:D523–D527 [View Article][PubMed]
    [Google Scholar]
  2. Bae Y., Kingsman S.M., Kingsman A.J. 1997; Functional dissection of the Moloney murine leukemia virus envelope protein gp70. 71:2092–2099[PubMed]
    [Google Scholar]
  3. Baliji S., Liu Q., Kozak C.A. 2010; Common inbred strains of the laboratory mouse that are susceptible to infection by mouse xenotropic gammaretroviruses and the human-derived retrovirus XMRV. J Virol 84:12841–12849 [View Article][PubMed]
    [Google Scholar]
  4. Baudino L., Yoshinobu K., Morito N., Kikuchi S., Fossati-Jimack L., Morley B.J., Vyse T.J., Hirose S., Jørgensen T.N., other authors. 2008; Dissection of genetic mechanisms governing the expression of serum retroviral gp70 implicated in murine lupus nephritis. J Immunol 181:2846–2854 [View Article][PubMed]
    [Google Scholar]
  5. Beck-Engeser G.B., Eilat D., Harrer T., Jäck H.M., Wabl M. 2009; Early onset of autoimmune disease by the retroviral integrase inhibitor raltegravir. Proc Natl Acad Sci U S A 106:20865–20870 [View Article][PubMed]
    [Google Scholar]
  6. Beck-Engeser G.B., Eilat D., Wabl M. 2011; An autoimmune disease prevented by anti-retroviral drugs. Retrovirology 8:91 [View Article][PubMed]
    [Google Scholar]
  7. Bernatsky S., Ramsey-Goldman R., Rajan R., Boivin J.F., Joseph L., Lachance S., Cournoyer D., Zoma A., Manzi S., other authors. 2005; Non-Hodgkin's lymphoma in systemic lupus erythematosus. Ann Rheum Dis 64:1507–1509 [View Article][PubMed]
    [Google Scholar]
  8. Bolland S., Ravetch J.V. 2000; Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 13:277–285 [View Article][PubMed]
    [Google Scholar]
  9. Bonham L., Wolgamot G., Miller A.D. 1997; Molecular cloning of Mus dunni endogenous virus: an unusual retrovirus in a new murine viral interference group with a wide host range. J Virol 71:4663–4670[PubMed]
    [Google Scholar]
  10. Chattopadhyay S.K., Lander M.R., Rands E., Lowy D.R. 1980; Structure of endogenous murine leukemia virus DNA in mouse genomes. Proc Natl Acad Sci U S A 77:5774–5778 [View Article][PubMed]
    [Google Scholar]
  11. Datta S.K., Manny N., Andrzejewski C., André-Schwartz J., Schwartz R.S. 1978a; Genetic studies of autoimmunity and retrovirus expression in crosses of New Zealand black mice I. Xenotropic virus. J Exp Med 147:854–871 [View Article][PubMed]
    [Google Scholar]
  12. Datta S.K., McConahey P.J., Manny N., Theofilopoulos A.N., Dixon F.J., Schwartz R.S. 1978b; Genetic studies of autoimmunity and retrovirus expression in crosses of New Zealand black mice. II. The viral envelope glycoprotein gp70. J Exp Med 147:872–881 [View Article][PubMed]
    [Google Scholar]
  13. Datta S.K., Thomas C.Y., Nicklas J.A., Coffin J.M. 1983; Thymic epithelial genotype influences the production of recombinant leukemogenic retroviruses in mice. J Virol 47:33–45[PubMed]
    [Google Scholar]
  14. DesGroseillers L., Jolicoeur P. 1983; Physical mapping of the Fv-1 tropism host range determinant of BALB/c murine leukemia viruses. J Virol 48:685–696[PubMed]
    [Google Scholar]
  15. Drappa J., Brot N., Elkon K.B. 1993; The Fas protein is expressed at high levels on CD4+CD8+ thymocytes and activated mature lymphocytes in normal mice but not in the lupus-prone strain, MRL lpr/lpr. Proc Natl Acad Sci U S A 90:10340–10344 [View Article][PubMed]
    [Google Scholar]
  16. Dühren-von Minden M., Übelhart R., Schneider D., Wossning T., Bach M.P., Buchner M., Hofmann D., Surova E., Follo M., other authors. 2012; Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature 489:309–312 [View Article][PubMed]
    [Google Scholar]
  17. Elder J.H., Gautsch J.W., Jensen F.C., Lerner R.A., Chused T.M., Morse H.C., Hartley J.W., Rowe W.P. 1980; Differential expression of two distinct xenotropic viruses in NZB mice. Clin Immunol Immunopathol 15:493–501 [View Article][PubMed]
    [Google Scholar]
  18. Frankel W.N., Stoye J.P., Taylor B.A., Coffin J.M. 1990; A linkage map of endogenous murine leukemia proviruses. Genetics 124:221–236[PubMed]
    [Google Scholar]
  19. Frankel W.N., Lee B.K., Stoye J.P., Coffin J.M., Eicher E.M. 1992; Characterization of the endogenous nonecotropic murine leukemia viruses of NZB/B1NJ and SM/J inbred strains. Mamm Genome 2:110–122 [View Article][PubMed]
    [Google Scholar]
  20. Gourley M.F., Kisch W.J., Mojcik C.F., King L.B., Krieg A.M., Steinberg A.D. 1994; Role of endogenous retroviruses in autoimmune diseases. Tohoku J Exp Med 173:105–114 [View Article][PubMed]
    [Google Scholar]
  21. Hara I., Izui S., McConahey P.J., Elder J.H., Jensen F.C., Dixon F.J. 1981; Induction of high serum levels of retroviral env gene products (gp70) in mice by bacterial lipopolysaccharide. Proc Natl Acad Sci U S A 78:4397–4401 [View Article][PubMed]
    [Google Scholar]
  22. Hara I., Izui S., Dixon F.J. 1982; Murine serum glycoprotein gp70 behaves as an acute phase reactant. J Exp Med 155:345–357 [View Article][PubMed]
    [Google Scholar]
  23. Herr W. 1984; Nucleotide sequence of AKV murine leukemia virus. J Virol 49:471–478[PubMed]
    [Google Scholar]
  24. Hibbs M.L., Tarlinton D.M., Armes J., Grail D., Hodgson G., Maglitto R., Stacker S.A., Dunn A.R. 1995; Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83:301–311 [View Article][PubMed]
    [Google Scholar]
  25. Jäck H.M., Beck-Engeser G., Lee G., Wofsy D., Wabl M. 1992; Tumorigenesis mediated by an antigen receptor. Proc Natl Acad Sci U S A 89:8482–8486 [View Article][PubMed]
    [Google Scholar]
  26. Jenkins N.A., Copeland N.G., Taylor B.A., Lee B.K. 1982; Organization, distribution, and stability of endogenous ecotropic murine leukemia virus DNA sequences in chromosomes of Mus musculus. J Virol 43:26–36[PubMed]
    [Google Scholar]
  27. Jern P., Stoye J.P., Coffin J.M. 2007; Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses. PLoS Genet 3:2014–2022 [View Article][PubMed]
    [Google Scholar]
  28. Knight-Krajewski S., Welsh C.F., Liu Y., Lyons L.S., Faysal J.M., Yang E.S., Burnstein K.L. 2004; Deregulation of the Rho GTPase, Rac1, suppresses cyclin-dependent kinase inhibitor p21(CIP1) levels in androgen-independent human prostate cancer cells. Oncogene 23:5513–5522 [View Article][PubMed]
    [Google Scholar]
  29. Knittel G., Metzner M., Beck-Engeser G., Kan A., Ahrends T., Eilat D., Huppi K., Wabl M. 2014; Insertional hypermutation in mineral oil-induced plasmacytomas. Eur J Immunol 44:2785–2801 [View Article][PubMed]
    [Google Scholar]
  30. Kozak C.A. 1985; Analysis of wild-derived mice for Fv-1 and Fv-2 murine leukemia virus restriction loci: a novel wild mouse Fv-1 allele responsible for lack of host range restriction. J Virol 55:281–285[PubMed]
    [Google Scholar]
  31. Kozak C.A., Chakraborti A. 1996; Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance. Virology 225:300–305 [View Article][PubMed]
    [Google Scholar]
  32. Lamagna C., Scapini P., van Ziffle J.A., DeFranco A.L., Lowell C.A. 2013; Hyperactivated MyD88 signaling in dendritic cells, through specific deletion of Lyn kinase, causes severe autoimmunity and inflammation. Proc Natl Acad Sci U S A 110:E3311–E3320 [View Article][PubMed]
    [Google Scholar]
  33. Lamagna C., Hu Y., DeFranco A.L., Lowell C.A. 2014; B cell-specific loss of Lyn kinase leads to autoimmunity. J Immunol 192:919–928 [View Article][PubMed]
    [Google Scholar]
  34. Lamont C., Culp P., Talbott R.L., Phillips T.R., Trauger R.J., Frankel W.N., Wilson M.C., Coffin J.M., Elder J.H. 1991; Characterization of endogenous and recombinant proviral elements of a highly tumorigenic AKR cell line. J Virol 65:4619–4628[PubMed]
    [Google Scholar]
  35. Lerner R.A., Wilson C.B., Villano B.C., McConahey P.J., Dixon F.J. 1976; Endogenous oncornaviral gene expression in adult and fetal mice: quantitative, histologic, and physiologic studies of the major viral glycorprotein, gp70. J Exp Med 143:151–166 [View Article][PubMed]
    [Google Scholar]
  36. Levy J.A. 1974; Autoimmunity and neoplasia. The possible role of C-type viruses. Am J Clin Pathol 62:258–280[PubMed]
    [Google Scholar]
  37. Lo B., Zhang K., Lu W., Zheng L., Zhang Q., Kanellopoulou C., Zhang Y., Liu Z., Fritz J.M., other authors. 2015; Patients with LRBA deficiency show CTLA4 loss and immune dysregulation responsive to abatacept therapy. Science 349:436–440 [View Article][PubMed]
    [Google Scholar]
  38. Lötscher M., Recher M., Lang K.S., Navarini A., Hunziker L., Santimaria R., Glatzel M., Schwarz P., Böni J., Zinkernagel R.M. 2007; Induced prion protein controls immune-activated retroviruses in the mouse spleen. PLoS One 2:e1158 [View Article][PubMed]
    [Google Scholar]
  39. Mackay F., Woodcock S.A., Lawton P., Ambrose C., Baetscher M., Schneider P., Tschopp J., Browning J.L. 1999; Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190:1697–1710 [View Article][PubMed]
    [Google Scholar]
  40. Mikkers H., Allen J., Knipscheer P., Romeijn L., Hart A., Vink E., Berns A. 2002; High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat Genet 32:153–159 [View Article][PubMed]
    [Google Scholar]
  41. Mitchell R.S., Beitzel B.F., Schroder A.R., Shinn P., Chen H., Berry C.C., Ecker J.R., Bushman F.D. 2004; Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2:E234 [View Article][PubMed]
    [Google Scholar]
  42. Montfort A., de Badts B., Douin-Echinard V., Martin P.G., Iacovoni J., Nevoit C., Therville N., Garcia V., Bertrand M.A., other authors. 2009; FAN stimulates TNF(alpha)-induced gene expression, leukocyte recruitment, and humoral response. J Immunol 183:5369–5378 [View Article][PubMed]
    [Google Scholar]
  43. Moroni C., Schumann G. 1975; Lipopolysaccharide induces C-type virus in short term cultures of BALB/c spleen cells. Nature 254:60–61 [View Article][PubMed]
    [Google Scholar]
  44. Nitschke L., Carsetti R., Ocker B., Köhler G., Lamers M.C. 1997; CD22 is a negative regulator of B-cell receptor signalling. Curr Biol 7:133–143 [View Article][PubMed]
    [Google Scholar]
  45. O'Keefe T.L., Williams G.T., Davies S.L., Neuberger M.S. 1996; Hyperresponsive B cells in CD22-deficient mice. Science 274:798–801 [View Article][PubMed]
    [Google Scholar]
  46. Otipoby K.L., Andersson K.B., Draves K.E., Klaus S.J., Farr A.G., Kerner J.D., Perlmutter R.M., Law C.L., Clark E.A. 1996; CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 384:634–637 [View Article][PubMed]
    [Google Scholar]
  47. Peng B., Sherr D.H., Mahboudi F., Hardin J., Wu Y.H., Sharer L., Raveché E.S. 1994; A cultured malignant B-1 line serves as a model for Richter's syndrome. J Immunol 153:1869–1880[PubMed]
    [Google Scholar]
  48. Rassa J.C., Meyers J.L., Zhang Y., Kudaravalli R., Ross S.R. 2002; Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc Natl Acad Sci U S A 99:2281–2286 [View Article][PubMed]
    [Google Scholar]
  49. Rosenke K., Lavignon M., Malik F., Kolokithas A., Hendrick D., Virtaneva K., Peterson K., Evans L.H. 2012; Profound amplification of pathogenic murine polytropic retrovirus release from coinfected cells. J Virol 86:7241–7248 [View Article][PubMed]
    [Google Scholar]
  50. Sato S., Miller A.S., Inaoki M., Bock C.B., Jansen P.J., Tang M.L., Tedder T.F. 1996; CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5:551–562 [View Article][PubMed]
    [Google Scholar]
  51. Satoh M., Kuroda Y., Yoshida H., Behney K.M., Mizutani A., Akaogi J., Nacionales D.C., Lorenson T.D., Rosenbauer R.J., Reeves W.H. 2003; Induction of lupus autoantibodies by adjuvants. J Autoimmun 21:1–9 [View Article][PubMed]
    [Google Scholar]
  52. Sokol M., Wabl M., Ruiz I.R., Pedersen F.S. 2014; Novel principles of gamma-retroviral insertional transcription activation in murine leukemia virus-induced end-stage tumors. Retrovirology 11:36 [View Article][PubMed]
    [Google Scholar]
  53. Sosa M.S., Lopez-Haber C., Yang C., Wang H., Lemmon M.A., Busillo J.M., Luo J., Benovic J.L., Klein-Szanto A., other authors. 2010; Identification of the Rac-GEF P-Rex1 as an essential mediator of ErbB signaling in breast cancer. Mol Cell 40:877–892 [View Article][PubMed]
    [Google Scholar]
  54. Stall A.M., Fariñas M.C., Tarlinton D.M., Lalor P.A., Herzenberg L.A., Strober S., Herzenberg L.A. 1988; Ly-1 B-cell clones similar to human chronic lymphocytic leukemias routinely develop in older normal mice and young autoimmune (New Zealand Black-related) animals. Proc Natl Acad Sci U S A 85:7312–7316 [View Article][PubMed]
    [Google Scholar]
  55. Steeves R., Lilly F. 1977; Interactions between host and viral genomes in mouse leukemia. Annu Rev Genet 11:277–296 [View Article][PubMed]
    [Google Scholar]
  56. Stephenson J.R., Reynolds R.K., Tronick S.R., Aaronson S.A. 1975; Distribution of three classes of endogenous type-C RNA viruses among inbred strains of mice. Virology 67:404–414 [View Article][PubMed]
    [Google Scholar]
  57. Stetson D.B., Ko J.S., Heidmann T., Medzhitov R. 2008; Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134:587–598 [View Article][PubMed]
    [Google Scholar]
  58. Stevens A., Bock M., Ellis S., LeTissier P., Bishop K.N., Yap M.W., Taylor W., Stoye J.P. 2004; Retroviral capsid determinants of Fv1 NB and NR tropism. J Virol 78:9592–9598 [View Article][PubMed]
    [Google Scholar]
  59. Stoye J.P., Coffin J.M. 1987; The four classes of endogenous murine leukemia virus: structural relationships and potential for recombination. J Virol 61:2659–2669[PubMed]
    [Google Scholar]
  60. Tarlinton D., Stall A.M., Herzenberg L.A. 1988; Repetitive usage of immunoglobulin VH and D gene segments in CD5+ Ly-1 B clones of (NZB x NZW)F1 mice. EMBO J 7:3705–3710[PubMed]
    [Google Scholar]
  61. Uren A.G., Kool J., Matentzoglu K., de Ridder J., Mattison J., van Uitert M., Lagcher W., Sie D., Tanger E., other authors. 2008; Large-scale mutagenesis in p19(ARF)- and p53-deficient mice identifies cancer genes and their collaborative networks. Cell 133:727–741 [View Article][PubMed]
    [Google Scholar]
  62. von Schwedler U., Jäck H.M., Wabl M. 1990; Circular DNA is a product of the immunoglobulin class switch rearrangement. Nature 345:452–456 [View Article][PubMed]
    [Google Scholar]
  63. Welch H.C., Coadwell W.J., Ellson C.D., Ferguson G.J., Andrews S.R., Erdjument-Bromage H., Tempst P., Hawkins P.T., Stephens L.R. 2002; P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108:809–821 [View Article][PubMed]
    [Google Scholar]
  64. Wofsy D., Seaman W.E. 1987; Reversal of advanced murine lupus in NZB/NZW F1 mice by treatment with monoclonal antibody to L3T4. J Immunol 138:3247–3253[PubMed]
    [Google Scholar]
  65. Wu X., Li Y., Crise B., Burgess S.M. 2003; Transcription start regions in the human genome are favored targets for MLV integration. Science 300:1749–1751 [View Article][PubMed]
    [Google Scholar]
  66. Young G.R., Eksmond U., Salcedo R., Alexopoulou L., Stoye J.P., Kassiotis G. 2012; Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 491:774–778[PubMed]
    [Google Scholar]
  67. Yu P., Constien R., Dear N., Katan M., Hanke P., Bunney T.D., Kunder S., Quintanilla-Martinez L., Huffstadt U., other authors. 2005; Autoimmunity and inflammation due to a gain-of-function mutation in phospholipase C gamma 2 that specifically increases external Ca2+ entry. Immunity 22:451–465 [View Article][PubMed]
    [Google Scholar]
  68. Yu P., Lübben W., Slomka H., Gebler J., Konert M., Cai C., Neubrandt L., Prazeres da Costa O., Paul S., other authors. 2012; Nucleic acid-sensing Toll-like receptors are essential for the control of endogenous retrovirus viremia and ERV-induced tumors. Immunity 37:867–879 [View Article][PubMed]
    [Google Scholar]
  69. Zeng M., Hu Z., Shi X., Li X., Zhan X., Li X.D., Wang J., Choi J.H., Wang K.W., other authors. 2014; MAVS, cGAS, and endogenous retroviruses in T-independent B cell responses. Science 346:1486–1492 [View Article][PubMed]
    [Google Scholar]
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