Mouse APOBEC3 interferes with autocatalytic cleavage of murine leukemia virus Pr180gag-pol precursor and inhibits Pr65gag processing


Autoři: Yoshiyuki Hakata aff001;  Jun Li aff001;  Takahiro Fujino aff003;  Yuki Tanaka aff003;  Rie Shimizu aff001;  Masaaki Miyazawa aff001
Působiště autorů: Department of Immunology, Kindai University Faculty of Medicine, Osaka-Sayama, Osaka, Japan aff001;  Ijunkai Medical Oncology, Endoscopy Clinic, Sakai-ku, Sakai, Osaka, Japan aff002;  Division of Analytical Bio-Medicine, Advanced Research Support Center (ADRES), Ehime University, Shitsukawa, Toon, Ehime, Japan aff003;  Kindai University Anti-Aging Center, Higashiosaka, Osaka, Japan aff004
Vyšlo v časopise: Mouse APOBEC3 interferes with autocatalytic cleavage of murine leukemia virus Pr180gag-pol precursor and inhibits Pr65gag processing. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008173
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008173

Souhrn

Mouse APOBEC3 (mA3) inhibits murine leukemia virus (MuLV) replication by a deamination-independent mechanism in which the reverse transcription is considered the main target process. However, other steps in virus replication that can be targeted by mA3 have not been examined. We have investigated the possible effect of mA3 on MuLV protease-mediated processes and found that mA3 binds both mature viral protease and Pr180gag-pol precursor polyprotein. Using replication-competent MuLVs, we also show that mA3 inhibits the processing of Pr65 Gag precursor. Furthermore, we demonstrate that the autoprocessing of Pr180gag-pol is impeded by mA3, resulting in reduced production of mature viral protease. This reduction appears to link with the above inefficient Pr65gag processing in the presence of mA3. Two major isoforms of mA3, exon 5-containing and -lacking ones, equally exhibit this antiviral activity. Importantly, physiologically expressed levels of mA3 impedes both Pr180gag-pol autocatalysis and Pr65gag processing. This blockade is independent of the deaminase activity and requires the C-terminal region of mA3. These results suggest that the above impairment of Pr180gag-pol autoprocessing may significantly contribute to the deaminase-independent antiretroviral activity exerted by mA3.

Klíčová slova:

293T cells – Immunoblotting – Proteases – Transfection – Viral replication – Virions – Reverse transcription


Zdroje

1. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, et al. APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature. 2005;433(7024):430–3. Epub 2005/01/28. doi: 10.1038/nature03238 15674295.

2. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, et al. DNA deamination mediates innate immunity to retroviral infection. Cell. 2003;113(6):803–9. Epub 2003/06/18. doi: 10.1016/s0092-8674(03)00423-9 12809610.

3. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature. 2003;424(6944):99–103. Epub 2003/06/17. doi: 10.1038/nature01709 12808466.

4. Suspene R, Aynaud MM, Koch S, Pasdeloup D, Labetoulle M, Gaertner B, et al. Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J Virol. 2011;85(15):7594–602. Epub 2011/06/03. doi: 10.1128/JVI.00290-11 21632763

5. Vartanian JP, Guetard D, Henry M, Wain-Hobson S. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science. 2008;320(5873):230–3. Epub 2008/04/12. 320/5873/230 doi: 10.1126/science.1153201 18403710.

6. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature. 2003;424(6944):94–8. Epub 2003/06/17. doi: 10.1038/nature01707 12808465

7. Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature. 2002;418(6898):646–50. Epub 2002/08/09. doi: 10.1038/nature00939 12167863.

8. Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol. 2005;22(2):367–77. Epub 2004/10/22. doi: 10.1093/molbev/msi026 15496550.

9. LaRue RS, Jonsson SR, Silverstein KA, Lajoie M, Bertrand D, El-Mabrouk N, et al. The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals. BMC Mol Biol. 2008;9:104. Epub 2008/11/20. doi: 10.1186/1471-2199-9-104 19017397

10. Apolonia L, Schulz R, Curk T, Rocha P, Swanson CM, Schaller T, et al. Promiscuous RNA binding ensures effective encapsidation of APOBEC3 proteins by HIV-1. PLoS Pathog. 2015;11(1):e1004609. Epub 2015/01/16. doi: 10.1371/journal.ppat.1004609 25590131

11. Burnett A, Spearman P. APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 virus-like particles in an RNA-dependent process requiring the NC basic linker. J Virol. 2007;81(10):5000–13. Epub 2007/03/09. doi: 10.1128/JVI.02237-06 17344295

12. Huthoff H, Autore F, Gallois-Montbrun S, Fraternali F, Malim MH. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 2009;5(3):e1000330. Epub 2009/03/07. doi: 10.1371/journal.ppat.1000330 19266078

13. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, Ono A, et al. Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem. 2004;279(34):35822–8. Epub 2004/06/24. doi: 10.1074/jbc.M405761200 15210704.

14. Chiu YL, Greene WC. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annual review of immunology. 2008;26:317–53. Epub 2008/02/29. doi: 10.1146/annurev.immunol.26.021607.090350 18304004.

15. Hultquist JF, Lengyel JA, Refsland EW, LaRue RS, Lackey L, Brown WL, et al. Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J Virol. 2011;85(21):11220–34. Epub 2011/08/13. doi: 10.1128/JVI.05238-11 21835787

16. Ooms M, Brayton B, Letko M, Maio SM, Pilcher CD, Hecht FM, et al. HIV-1 Vif adaptation to human APOBEC3H haplotypes. Cell Host Microbe. 2013;14(4):411–21. Epub 2013/10/22. doi: 10.1016/j.chom.2013.09.006 24139399.

17. Refsland EW, Hultquist JF, Harris RS. Endogenous origins of HIV-1 G-to-A hypermutation and restriction in the nonpermissive T cell line CEM2n. PLoS Pathog. 2012;8(7):e1002800. Epub 2012/07/19. doi: 10.1371/journal.ppat.1002800 22807680

18. Refsland EW, Hultquist JF, Luengas EM, Ikeda T, Shaban NM, Law EK, et al. Natural polymorphisms in human APOBEC3H and HIV-1 Vif combine in primary T lymphocytes to affect viral G-to-A mutation levels and infectivity. PLoS Genet. 2014;10(11):e1004761. Epub 2014/11/21. doi: 10.1371/journal.pgen.1004761 25411794

19. Bishop KN, Verma M, Kim EY, Wolinsky SM, Malim MH. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 2008;4(12):e1000231. Epub 2008/12/06. doi: 10.1371/journal.ppat.1000231 19057663

20. Boi S, Kolokithas A, Shepard J, Linwood R, Rosenke K, Van Dis E, et al. Incorporation of mouse APOBEC3 into murine leukemia virus virions decreases the activity and fidelity of reverse transcriptase. J Virol. 2014;88(13):7659–62. Epub 2014/04/11. doi: 10.1128/JVI.00967-14 24719421

21. Holmes RK, Koning FA, Bishop KN, Malim MH. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem. 2007;282(4):2587–95. Epub 2006/11/24. doi: 10.1074/jbc.M607298200 17121840.

22. Iwatani Y, Chan DS, Wang F, Maynard KS, Sugiura W, Gronenborn AM, et al. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 2007;35(21):7096–108. Epub 2007/10/19. doi: 10.1093/nar/gkm750 17942420

23. MacMillan AL, Kohli RM, Ross SR. APOBEC3 inhibition of mouse mammary tumor virus infection: the role of cytidine deamination versus inhibition of reverse transcription. J Virol. 2013;87(9):4808–17. Epub 2013/03/02. doi: 10.1128/JVI.00112-13 23449789

24. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, et al. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol. 2005;15(2):166–70. Epub 2005/01/26. doi: 10.1016/j.cub.2004.12.068 15668174.

25. Sanchez-Martinez S, Aloia AL, Harvin D, Mirro J, Gorelick RJ, Jern P, et al. Studies on the restriction of murine leukemia viruses by mouse APOBEC3. PLoS One. 2012;7(5):e38190. Epub 2012/06/06. doi: 10.1371/journal.pone.0038190 22666481

26. Chaurasiya KR, McCauley MJ, Wang W, Qualley DF, Wu T, Kitamura S, et al. Oligomerization transforms human APOBEC3G from an efficient enzyme to a slowly dissociating nucleic acid-binding protein. Nat Chem. 2014;6(1):28–33. Epub 2013/12/19. doi: 10.1038/nchem.1795 24345943

27. Wang X, Ao Z, Chen L, Kobinger G, Peng J, Yao X. The cellular antiviral protein APOBEC3G interacts with HIV-1 reverse transcriptase and inhibits its function during viral replication. J Virol. 2012;86(7):3777–86. Epub 2012/02/04. doi: 10.1128/JVI.06594-11 22301159

28. Pollpeter D, Parsons M, Sobala AE, Coxhead S, Lang RD, Bruns AM, et al. Deep sequencing of HIV-1 reverse transcripts reveals the multifaceted antiviral functions of APOBEC3G. Nature microbiology. 2018;3(2):220–33. Epub 2017/11/22. doi: 10.1038/s41564-017-0063-9 29158605

29. Miyazawa M, Tsuji-Kawahara S, Kanari Y. Host genetic factors that control immune responses to retrovirus infections. Vaccine. 2008;26(24):2981–96. Epub 2008/02/08. doi: 10.1016/j.vaccine.2008.01.004 18255203.

30. Okeoma CM, Lovsin N, Peterlin BM, Ross SR. APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature. 2007;445(7130):927–30. Epub 2007/01/30. doi: 10.1038/nature05540 17259974.

31. Okeoma CM, Petersen J, Ross SR. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J Virol. 2009;83(7):3029–38. Epub 2009/01/21. doi: 10.1128/JVI.02536-08 19153233

32. Santiago ML, Montano M, Benitez R, Messer RJ, Yonemoto W, Chesebro B, et al. Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science. 2008;321(5894):1343–6. Epub 2008/09/06. doi: 10.1126/science.1161121 18772436

33. Takeda E, Tsuji-Kawahara S, Sakamoto M, Langlois MA, Neuberger MS, Rada C, et al. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J Virol. 2008;82(22):10998–1008. Epub 2008/09/13. doi: 10.1128/JVI.01311-08 18786991

34. Li J, Hakata Y, Takeda E, Liu Q, Iwatani Y, Kozak CA, et al. Two genetic determinants acquired late in Mus evolution regulate the inclusion of exon 5, which alters mouse APOBEC3 translation efficiency. PLoS Pathog. 2012;8(1):e1002478. Epub 2012/01/26. doi: 10.1371/journal.ppat.1002478 22275865

35. Sanville B, Dolan MA, Wollenberg K, Yan Y, Martin C, Yeung ML, et al. Adaptive evolution of Mus Apobec3 includes retroviral insertion and positive selection at two clusters of residues flanking the substrate groove. PLoS Pathog. 2010;6:e1000974. Epub 2010/07/10. doi: 10.1371/journal.ppat.1000974 20617165

36. Langlois MA, Kemmerich K, Rada C, Neuberger MS. The AKV murine leukemia virus is restricted and hypermutated by mouse APOBEC3. J Virol. 2009;83(22):11550–9. Epub 2009/09/04. doi: 10.1128/JVI.01430-09 19726503

37. Hakata Y, Landau NR. Reversed functional organization of mouse and human APOBEC3 cytidine deaminase domains. J Biol Chem. 2006;281(48):36624–31. Epub 2006/10/06. doi: 10.1074/jbc.M604980200 17020885.

38. Browne EP, Littman DR. Species-specific restriction of apobec3-mediated hypermutation. J Virol. 2008;82(3):1305–13. Epub 2007/11/23. doi: 10.1128/JVI.01371-07 18032489

39. Nair S, Sanchez-Martinez S, Ji X, Rein A. Biochemical and biological studies of mouse APOBEC3. J Virol. 2014;88(7):3850–60. Epub 2014/01/24. doi: 10.1128/JVI.03456-13 24453360

40. Rulli SJ Jr., Mirro J, Hill SA, Lloyd P, Gorelick RJ, Coffin JM, et al. Interactions of murine APOBEC3 and human APOBEC3G with murine leukemia viruses. J Virol. 2008;82(13):6566–75. Epub 2008/05/02. doi: 10.1128/JVI.01357-07 18448535

41. Conticello SG, Harris RS, Neuberger MS. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol. 2003;13(22):2009–13. Epub 2003/11/15. doi: 10.1016/j.cub.2003.10.034 14614829.

42. Kao S, Khan MA, Miyagi E, Plishka R, Buckler-White A, Strebel K. The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity. J Virol. 2003;77(21):11398–407. Epub 2003/10/15. doi: 10.1128/JVI.77.21.11398-11407.2003 14557625

43. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B, et al. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell. 2003;114(1):21–31. Epub 2003/07/16. doi: 10.1016/s0092-8674(03)00515-4 12859895.

44. Marin M, Rose KM, Kozak SL, Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med. 2003;9(11):1398–403. Epub 2003/10/07. doi: 10.1038/nm946 14528301.

45. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem. 2004;279(9):7792–8. Epub 2003/12/16. doi: 10.1074/jbc.M313093200 14672928.

46. Sheehy AM, Gaddis NC, Malim MH. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med. 2003;9(11):1404–7. Epub 2003/10/07. doi: 10.1038/nm945 14528300.

47. Stopak K, de Noronha C, Yonemoto W, Greene WC. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell. 2003;12(3):591–601. Epub 2003/10/07. doi: 10.1016/s1097-2765(03)00353-8 14527406.

48. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, et al. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science. 2003;302(5647):1056–60. Epub 2003/10/18. doi: 10.1126/science.1089591 14564014.

49. Kolokithas A, Rosenke K, Malik F, Hendrick D, Swanson L, Santiago ML, et al. The glycosylated Gag protein of a murine leukemia virus inhibits the antiretroviral function of APOBEC3. J Virol. 2010;84(20):10933–6. Epub 2010/08/13. doi: 10.1128/JVI.01023-10 20702647

50. Nitta T, Lee S, Ha D, Arias M, Kozak CA, Fan H. Moloney murine leukemia virus glyco-gag facilitates xenotropic murine leukemia virus-related virus replication through human APOBEC3-independent mechanisms. Retrovirology. 2012;9:58. Epub 2012/07/26. doi: 10.1186/1742-4690-9-58 22828015

51. Stavrou S, Nitta T, Kotla S, Ha D, Nagashima K, Rein AR, et al. Murine leukemia virus glycosylated Gag blocks apolipoprotein B editing complex 3 and cytosolic sensor access to the reverse transcription complex. Proc Natl Acad Sci U S A. 2013;110(22):9078–83. Epub 2013/05/15. doi: 10.1073/pnas.1217399110 23671100

52. Abudu A, Takaori-Kondo A, Izumi T, Shirakawa K, Kobayashi M, Sasada A, et al. Murine retrovirus escapes from murine APOBEC3 via two distinct novel mechanisms. Curr Biol. 2006;16(15):1565–70. Epub 2006/08/08. doi: 10.1016/j.cub.2006.06.055 16890533.

53. Yoshinaka Y, Katoh I, Copeland TD, Oroszlan S. Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon. Proc Natl Acad Sci U S A. 1985;82(6):1618–22. Epub 1985/03/01. doi: 10.1073/pnas.82.6.1618 3885215

54. Pettit SC, Everitt LE, Choudhury S, Dunn BM, Kaplan AH. Initial cleavage of the human immunodeficiency virus type 1 GagPol precursor by its activated protease occurs by an intramolecular mechanism. J Virol. 2004;78(16):8477–85. Epub 2004/07/29. doi: 10.1128/JVI.78.16.8477-8485.2004 15280456

55. Zybarth G, Carter C. Domains upstream of the protease (PR) in human immunodeficiency virus type 1 Gag-Pol influence PR autoprocessing. J Virol. 1995;69(6):3878–84. Epub 1995/06/01. 7745738

56. Pettit SC, Lindquist JN, Kaplan AH, Swanstrom R. Processing sites in the human immunodeficiency virus type 1 (HIV-1) Gag-Pro-Pol precursor are cleaved by the viral protease at different rates. Retrovirology. 2005;2:66. Epub 2005/11/03. doi: 10.1186/1742-4690-2-66 16262906

57. Tsuji-Kawahara S, Kawabata H, Matsukuma H, Kinoshita S, Chikaishi T, Sakamoto M, et al. Differential requirements of cellular and humoral immune responses for Fv2-associated resistance to erythroleukemia and for regulation of retrovirus-induced myeloid leukemia development. J Virol. 2013;87(24):13760–74. Epub 2013/10/11. doi: 10.1128/JVI.02506-13 24109240

58. Oliff AI, Hager GL, Chang EH, Scolnick EM, Chan HW, Lowy DR. Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol. 1980;33(1):475–86. Epub 1980/01/01. 6245244

59. Richardson J, Corbin A, Pozo F, Orsoni S, Sitbon M. Sequences responsible for the distinctive hemolytic potentials of Friend and Moloney murine leukemia viruses are dispersed but confined to the psi-gag-PR region. J Virol. 1993;67(9):5478–86. Epub 1993/09/01. 8350407

60. Mehta HV, Jones PH, Weiss JP, Okeoma CM. IFN-alpha and lipopolysaccharide upregulate APOBEC3 mRNA through different signaling pathways. J Immunol. 2012;189(8):4088–103. Epub 2012/09/14. doi: 10.4049/jimmunol.1200777 22972924

61. Bukovsky A, Gottlinger H. Lack of integrase can markedly affect human immunodeficiency virus type 1 particle production in the presence of an active viral protease. J Virol. 1996;70(10):6820–5. Epub 1996/10/01. 8794322

62. Quillent C, Borman AM, Paulous S, Dauguet C, Clavel F. Extensive regions of pol are required for efficient human immunodeficiency virus polyprotein processing and particle maturation. Virology. 1996;219(1):29–36. Epub 1996/05/01. doi: 10.1006/viro.1996.0219 8623542.

63. Tachedjian G, Moore KL, Goff SP, Sluis-Cremer N. Efavirenz enhances the proteolytic processing of an HIV-1 pol polyprotein precursor and reverse transcriptase homodimer formation. FEBS Lett. 2005;579(2):379–84. Epub 2005/01/12. doi: 10.1016/j.febslet.2004.11.099 15642347.

64. Oroszlan S, Luftig RB. Retroviral proteinases. Current topics in microbiology and immunology. 1990;157:153–85. Epub 1990/01/01. doi: 10.1007/978-3-642-75218-6_6 2203608.

65. Vogt VM. Proteolytic processing and particle maturation. Current topics in microbiology and immunology. 1996;214:95–131. Epub 1996/01/01. doi: 10.1007/978-3-642-80145-7_4 8791726.

66. Tsuji-Kawahara S, Chikaishi T, Takeda E, Kato M, Kinoshita S, Kajiwara E, et al. Persistence of viremia and production of neutralizing antibodies differentially regulated by polymorphic APOBEC3 and BAFF-R loci in friend virus-infected mice. J Virol. 2010;84(12):6082–95. Epub 2010/04/09. doi: 10.1128/JVI.02516-09 20375169

67. Mukhopadhyaya R, Richardson J, Nazarov V, Corbin A, Koller R, Sitbon M, et al. Different abilities of Friend murine leukemia virus (MuLV) and Moloney MuLV to induce promonocytic leukemia are due to determinants in both psi-gag-PR and env regions. J Virol. 1994;68(8):5100–7. Epub 1994/08/01. 7518530

68. Sitbon M, Sola B, Evans L, Nishio J, Hayes SF, Nathanson K, et al. Hemolytic anemia and erythroleukemia, two distinct pathogenic effects of Friend MuLV: mapping of the effects to different regions of the viral genome. Cell. 1986;47(6):851–9. Epub 1986/12/26. doi: 10.1016/0092-8674(86)90800-7 3465451.

69. Miyazawa M, Nishio J, Chesebro B. Genetic control of T cell responsiveness to the Friend murine leukemia virus envelope antigen. Identification of class II loci of the H-2 as immune response genes. J Exp Med. 1988;168(5):1587–605. Epub 1988/11/01. doi: 10.1084/jem.168.5.1587 3141552

70. Qiu LQ, Lai WS, Stumpo DJ, Blackshear PJ. Mouse Embryonic Fibroblast Cell Culture and Stimulation. Bio-protocol. 2016;6(13). Epub 2017/06/03. doi: 10.21769/BioProtoc.1859 28573158

71. Lander MR, Chattopadhyay SK. A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ectropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J Virol. 1984;52(2):695–8. Epub 1984/11/01. 6092693

72. Chesebro B, Britt W, Evans L, Wehrly K, Nishio J, Cloyd M. Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of friend MCF and Friend ecotropic murine leukemia virus. Virology. 1983;127(1):134–48. Epub 1983/05/01. doi: 10.1016/0042-6822(83)90378-1 6305011.

73. Chesebro B, Wehrly K, Cloyd M, Britt W, Portis J, Collins J, et al. Characterization of mouse monoclonal antibodies specific for Friend murine leukemia virus-induced erythroleukemia cells: friend-specific and FMR-specific antigens. Virology. 1981;112(1):131–44. Epub 1981/07/15. doi: 10.1016/0042-6822(81)90619-x 6787798.

74. McAtee FJ, Portis JL. Monoclonal antibodies specific for wild mouse neurotropic retrovirus: detection of comparable levels of virus replication in mouse strains susceptible and resistant to paralytic disease. J Virol. 1985;56(3):1018–22. Epub 1985/12/01. 3877818

75. Robertson MN, Miyazawa M, Mori S, Caughey B, Evans LH, Hayes SF, et al. Production of monoclonal antibodies reactive with a denatured form of the Friend murine leukemia virus gp70 envelope protein: use in a focal infectivity assay, immunohistochemical studies, electron microscopy and western blotting. J Virol Methods. 1991;34(3):255–71. Epub 1991/10/01. doi: 10.1016/0166-0934(91)90105-9 1744218.

76. Miyazawa M, Fujisawa R, Ishihara C, Takei YA, Shimizu T, Uenishi H, et al. Immunization with a single T helper cell epitope abrogates Friend virus-induced early erythroid proliferation and prevents late leukemia development. J Immunol. 1995;155(2):748–58. Epub 1995/07/15. 7541823.

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