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. 1994 Aug;68(8):4785–4796. doi: 10.1128/jvi.68.8.4785-4796.1994

n-Butyrate, a cell cycle blocker, inhibits the replication of polyomaviruses and papillomaviruses but not that of adenoviruses and herpesviruses.

F F Shadan 1, L M Cowsert 1, L P Villarreal 1
PMCID: PMC236418  PMID: 8035479

Abstract

Small DNA viruses are dependent on the interaction of early proteins (such as large T antigen) with host p53 and Rb to bring about the G1-to-S cell cycle transition. The large DNA viruses are less dependent on host regulatory genes since additional early viral proteins (such as viral DNA polymerase, DNA metabolic enzymes, and other replication proteins) are involved in DNA synthesis. A highly conserved domain of large T antigen (similar to the p53-binding region) exclusively identifies papovavirus, parvovirus, and papillomaviruses from all other larger DNA viruses and implies a conserved interaction with host regulatory genes. In this report, we show that 3 to 6 mM butyrate, a general cell cycle blocker implicated in inhibition of the G1-to-S transition, inhibits DNA replication of polyomavirus and human papillomavirus type 11 but not the replication of larger DNA viruses such as adenovirus types 2 and 5, herpes simplex virus type 1, Epstein-Barr virus, and cytomegalovirus, which all bypass the butyrate-mediated cell cycle block. This butyrate effect on polyomavirus replication is not cell type specific, nor does it depend on the p53 or Rb gene, as inhibition was seen in fibroblasts with intact or homozygous deleted p53 or Rb, 3T6 cells, keratinocytes, C2C12 myoblasts, and 3T3-L1 adipocytes. In addition, butyrate did not inhibit expression of polyomavirus T antigen. The antiviral effect of butyrate involves a form of imprinted state, since pretreatment of cells with 3 mM butyrate inhibits human papillomavirus type 11 DNA replication for at least 96 h after its removal. Butyrate, therefore, serves as a molecular tool in dissecting the life cycle of smaller DNA viruses from that of the larger DNA viruses in relation to the cell cycle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abboud M. M., Horwitz M. S. The DNA polymerases associated with the adenovirus type 2 replication complex: effect of 2'-3'-dideoxythymidine-5'-triphosphate on viral DNA synthesis. Nucleic Acids Res. 1979 Mar;6(3):1025–1039. doi: 10.1093/nar/6.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anisimová E., Prachová K., Roubal J., Vonka V. Effects of n-butyrate and phorbol ester (TPA) on induction of Epstein-Barr virus antigens and cell differentiation. Arch Virol. 1984;81(3-4):223–237. doi: 10.1007/BF01309995. [DOI] [PubMed] [Google Scholar]
  3. Anisimová E., Saemundsen A. K., Roubal J., Vonka V., Klein G. Effects of n-butyrate on Epstein-Barr virus-carrying lymphoma lines. J Gen Virol. 1982 Jan;58(Pt 1):163–171. doi: 10.1099/0022-1317-58-1-163. [DOI] [PubMed] [Google Scholar]
  4. Atencio I. A., Shadan F. F., Zhou X. J., Vaziri N. D., Villarreal L. P. Adult mouse kidneys become permissive to acute polyomavirus infection and reactivate persistent infections in response to cellular damage and regeneration. J Virol. 1993 Mar;67(3):1424–1432. doi: 10.1128/jvi.67.3.1424-1432.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Balk S., Gunther H., Morisi A. Butyrate reversibly arrests the proliferation of normal and Rous sarcoma virus-infected chicken heart mesenchymal cells. Life Sci. 1984 Feb 20;34(8):803–808. doi: 10.1016/0024-3205(84)90388-6. [DOI] [PubMed] [Google Scholar]
  6. Barker D. E., Roizman B. Identification of three genes nonessential for growth in cell culture near the right terminus of the unique sequences of long component of herpes simplex virus 1. Virology. 1990 Aug;177(2):684–691. doi: 10.1016/0042-6822(90)90534-x. [DOI] [PubMed] [Google Scholar]
  7. Bohan C., York D., Srinivasan A. Sodium butyrate activates human immunodeficiency virus long terminal repeat--directed expression. Biochem Biophys Res Commun. 1987 Nov 13;148(3):899–905. doi: 10.1016/s0006-291x(87)80217-6. [DOI] [PubMed] [Google Scholar]
  8. Botchan M., Berg L., Reynolds J., Lusky M. The bovine papillomavirus replicon. Ciba Found Symp. 1986;120:53–67. doi: 10.1002/9780470513309.ch5. [DOI] [PubMed] [Google Scholar]
  9. Braithwaite A. W., Sturzbecher H. W., Addison C., Palmer C., Rudge K., Jenkins J. R. Mouse p53 inhibits SV40 origin-dependent DNA replication. Nature. 1987 Oct 1;329(6138):458–460. doi: 10.1038/329458a0. [DOI] [PubMed] [Google Scholar]
  10. Brown D. D. The role of stable complexes that repress and activate eucaryotic genes. Cell. 1984 Jun;37(2):359–365. doi: 10.1016/0092-8674(84)90366-0. [DOI] [PubMed] [Google Scholar]
  11. Bruce J. H., Ramirez A., Lin L., Agarwal R. P. Effects of cyclic AMP and butyrate on cell cycle, DNA, RNA, and purine synthesis of cultured astrocytes. Neurochem Res. 1992 Apr;17(4):315–320. doi: 10.1007/BF00974571. [DOI] [PubMed] [Google Scholar]
  12. Campisi J., Medrano E. E., Morreo G., Pardee A. B. Restriction point control of cell growth by a labile protein: evidence for increased stability in transformed cells. Proc Natl Acad Sci U S A. 1982 Jan;79(2):436–440. doi: 10.1073/pnas.79.2.436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Charollais R. H., Buquet C., Mester J. Butyrate blocks the accumulation of CDC2 mRNA in late G1 phase but inhibits both the early and late G1 progression in chemically transformed mouse fibroblasts BP-A31. J Cell Physiol. 1990 Oct;145(1):46–52. doi: 10.1002/jcp.1041450108. [DOI] [PubMed] [Google Scholar]
  14. Chou J., Kern E. R., Whitley R. J., Roizman B. Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science. 1990 Nov 30;250(4985):1262–1266. doi: 10.1126/science.2173860. [DOI] [PubMed] [Google Scholar]
  15. Contreras-Salazar B., Ehlin-Henriksson B., Klein G., Masucci M. G. Up regulation of the Epstein-Barr virus (EBV)-encoded membrane protein LMP in the Burkitt's lymphoma line Daudi after exposure to n-butyrate and after EBV superinfection. J Virol. 1990 Nov;64(11):5441–5447. doi: 10.1128/jvi.64.11.5441-5447.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cooper J. A., Whyte P. RB and the cell cycle: entrance or exit? Cell. 1989 Sep 22;58(6):1009–1011. doi: 10.1016/0092-8674(89)90495-9. [DOI] [PubMed] [Google Scholar]
  17. D'Anna J. A., Tobey R. A., Gurley L. R. Concentration-dependent effects of sodium butyrate in Chinese hamster cells: cell-cycle progression, inner-histone acetylation, histone H1 dephosphorylation, and induction of an H1-like protein. Biochemistry. 1980 Jun 10;19(12):2656–2671. doi: 10.1021/bi00553a019. [DOI] [PubMed] [Google Scholar]
  18. Daniell E., Burg J. L., Fedor M. J. DNA and histone synthesis of butyrate-inhibited BSC-1 cells infected with SV40. Virology. 1982 Jan 15;116(1):196–206. doi: 10.1016/0042-6822(82)90413-5. [DOI] [PubMed] [Google Scholar]
  19. Daniell E. Cells inhibited by n-butyrate support adenovirus replication. Virology. 1980 Dec;107(2):514–519. doi: 10.1016/0042-6822(80)90318-9. [DOI] [PubMed] [Google Scholar]
  20. DeCaprio J. A., Ludlow J. W., Figge J., Shew J. Y., Huang C. M., Lee W. H., Marsilio E., Paucha E., Livingston D. M. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell. 1988 Jul 15;54(2):275–283. doi: 10.1016/0092-8674(88)90559-4. [DOI] [PubMed] [Google Scholar]
  21. DePolo N. J., Villarreal L. P. Aphidicolin-resistant polyomavirus and subgenomic cellular DNA synthesis occur early in the differentiation of cultured myoblasts to myotubes. J Virol. 1993 Jul;67(7):4169–4181. doi: 10.1128/jvi.67.7.4169-4181.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Deppert W., Steinmayer T. Metabolic stabilization of p53 in SV40-transformed cells correlates with expression of the transformed phenotype but is independent from complex formation with SV40 large T antigen. Curr Top Microbiol Immunol. 1989;144:77–83. doi: 10.1007/978-3-642-74578-2_9. [DOI] [PubMed] [Google Scholar]
  23. Deppert W., Steinmayer T., Richter W. Cooperation of SV40 large T antigen and the cellular protein p53 in maintenance of cell transformation. Oncogene. 1989 Sep;4(9):1103–1110. [PubMed] [Google Scholar]
  24. Fakharzadeh S. S., Trusko S. P., George D. L. Tumorigenic potential associated with enhanced expression of a gene that is amplified in a mouse tumor cell line. EMBO J. 1991 Jun;10(6):1565–1569. doi: 10.1002/j.1460-2075.1991.tb07676.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Farmer G., Bargonetti J., Zhu H., Friedman P., Prywes R., Prives C. Wild-type p53 activates transcription in vitro. Nature. 1992 Jul 2;358(6381):83–86. doi: 10.1038/358083a0. [DOI] [PubMed] [Google Scholar]
  26. Felsani A., Maione R., Ricci L., Amati P. Coordinate expression of myogenic functions and polyoma virus replication. Cold Spring Harb Symp Quant Biol. 1985;50:753–757. doi: 10.1101/sqb.1985.050.01.093. [DOI] [PubMed] [Google Scholar]
  27. Gannon J. V., Lane D. P. p53 and DNA polymerase alpha compete for binding to SV40 T antigen. Nature. 1987 Oct 1;329(6138):456–458. doi: 10.1038/329456a0. [DOI] [PubMed] [Google Scholar]
  28. Goldberg Y. P., Leaner V. D., Parker M. I. Elevation of large-T antigen production by sodium butyrate treatment of SV40-transformed WI-38 fibroblasts. J Cell Biochem. 1992 May;49(1):74–81. doi: 10.1002/jcb.240490113. [DOI] [PubMed] [Google Scholar]
  29. Hiebert S. W., Chellappan S. P., Horowitz J. M., Nevins J. R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 1992 Feb;6(2):177–185. doi: 10.1101/gad.6.2.177. [DOI] [PubMed] [Google Scholar]
  30. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  31. Howard M. A., Wardwell S., Albert D. M. Effect of butyrate and corticosteroids on retinoblastoma in vitro and in vivo. Invest Ophthalmol Vis Sci. 1991 May;32(6):1711–1713. [PubMed] [Google Scholar]
  32. Iseki S., Baserga R. Effect of butyrate on adenovirus infection in semipermissive cells. Virology. 1983 Jan 15;124(1):188–191. doi: 10.1016/0042-6822(83)90304-5. [DOI] [PubMed] [Google Scholar]
  33. Ito Y., Kawanishi M., Harayama T., Takabayashi S. Combined effect of the extracts from Croton tiglium, Euphorbia lathyris or Euphorbia tirucalli and n-butyrate on Epstein-Barr virus expression in human lymphoblastoid P3HR-1 and Raji cells. Cancer Lett. 1981 Apr;12(3):175–180. doi: 10.1016/0304-3835(81)90066-5. [DOI] [PubMed] [Google Scholar]
  34. Jones T. R., Muzithras V. P., Gluzman Y. Replacement mutagenesis of the human cytomegalovirus genome: US10 and US11 gene products are nonessential. J Virol. 1991 Nov;65(11):5860–5872. doi: 10.1128/jvi.65.11.5860-5872.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kallin B., Luka J., Klein G. Immunochemical characterization of Epstein-Barr virus-associated early and late antigens in n-butyrate-treated P3HR-1 cells. J Virol. 1979 Dec;32(3):710–716. doi: 10.1128/jvi.32.3.710-716.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kawanishi M., Sugawara K., Ito Y. Epstein-Barr virus-induced early polypeptides in Raji and NC37 cells activated by diterpene ester TPA in combination with N-butyrate. Virology. 1981 Dec;115(2):406–409. doi: 10.1016/0042-6822(81)90123-9. [DOI] [PubMed] [Google Scholar]
  37. Kawasaki S., Diamond L., Baserga R. Induction of cellular deoxyribonucleic acid synthesis in butyrate-treated cells by simian virus 40 deoxyribonucleic acid. Mol Cell Biol. 1981 Nov;1(11):1038–1047. doi: 10.1128/mcb.1.11.1038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Krokan H., Schaffer P., DePamphilis M. L. Involvement of eucaryotic deoxyribonucleic acid polymerases alpha and gamma in the replication of cellular and viral deoxyribonucleic acid. Biochemistry. 1979 Oct 2;18(20):4431–4443. doi: 10.1021/bi00587a025. [DOI] [PubMed] [Google Scholar]
  39. Levine A. J., Momand J., Finlay C. A. The p53 tumour suppressor gene. Nature. 1991 Jun 6;351(6326):453–456. doi: 10.1038/351453a0. [DOI] [PubMed] [Google Scholar]
  40. Longnecker R., Miller C. L., Miao X. Q., Marchini A., Kieff E. The only domain which distinguishes Epstein-Barr virus latent membrane protein 2A (LMP2A) from LMP2B is dispensable for lymphocyte infection and growth transformation in vitro; LMP2A is therefore nonessential. J Virol. 1992 Nov;66(11):6461–6469. doi: 10.1128/jvi.66.11.6461-6469.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ludlow J. W., DeCaprio J. A., Huang C. M., Lee W. H., Paucha E., Livingston D. M. SV40 large T antigen binds preferentially to an underphosphorylated member of the retinoblastoma susceptibility gene product family. Cell. 1989 Jan 13;56(1):57–65. doi: 10.1016/0092-8674(89)90983-5. [DOI] [PubMed] [Google Scholar]
  42. Ludlow J. W., Shon J., Pipas J. M., Livingston D. M., DeCaprio J. A. The retinoblastoma susceptibility gene product undergoes cell cycle-dependent dephosphorylation and binding to and release from SV40 large T. Cell. 1990 Feb 9;60(3):387–396. doi: 10.1016/0092-8674(90)90590-b. [DOI] [PubMed] [Google Scholar]
  43. Luka J., Kallin B., Klein G. Induction of the Epstein-Barr virus (EBV) cycle in latently infected cells by n-butyrate. Virology. 1979 Apr 15;94(1):228–231. doi: 10.1016/0042-6822(79)90455-0. [DOI] [PubMed] [Google Scholar]
  44. Martinez J., Georgoff I., Martinez J., Levine A. J. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes Dev. 1991 Feb;5(2):151–159. doi: 10.1101/gad.5.2.151. [DOI] [PubMed] [Google Scholar]
  45. Medrano E. E., Pardee A. B. Prevalent deficiency in tumor cells of cycloheximide-induced cycle arrest. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4123–4126. doi: 10.1073/pnas.77.7.4123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Mietz J. A., Unger T., Huibregtse J. M., Howley P. M. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein. EMBO J. 1992 Dec;11(13):5013–5020. doi: 10.1002/j.1460-2075.1992.tb05608.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Mitsudomi T., Kimura G. Effects of sodium n-butyrate on entry into S phase in resting rat 3Y1 cells infected with simian virus 40. J Virol. 1985 Dec;56(3):951–957. doi: 10.1128/jvi.56.3.951-957.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Momand J., Zambetti G. P., Olson D. C., George D., Levine A. J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell. 1992 Jun 26;69(7):1237–1245. doi: 10.1016/0092-8674(92)90644-r. [DOI] [PubMed] [Google Scholar]
  49. Moreno J. P., Villarreal L. P. Analysis of cellular DNA synthesis during polyoma virus infection of mice: acute infection fails to induce cellular DNA synthesis. Virology. 1992 Feb;186(2):463–474. doi: 10.1016/0042-6822(92)90011-d. [DOI] [PubMed] [Google Scholar]
  50. Perry M. E., Levine A. J. Tumor-suppressor p53 and the cell cycle. Curr Opin Genet Dev. 1993 Feb;3(1):50–54. doi: 10.1016/s0959-437x(05)80340-5. [DOI] [PubMed] [Google Scholar]
  51. Pouillart P., Cerutti I., Ronco G., Villa P., Chany C. Action protectrice du butyrate-3 monoacétone glucose, prodrogue de l'acide n-butyrique, contre l'effet létal du virus de l'encéphalomyocardite de la souris. C R Acad Sci III. 1992;314(2):49–54. [PubMed] [Google Scholar]
  52. Pouillart P., Cerutti I., Ronco G., Villa P., Chany C. Enhancement by stable butyrate derivatives of antitumor and antiviral actions of interferon. Int J Cancer. 1992 Jun 19;51(4):596–601. doi: 10.1002/ijc.2910510416. [DOI] [PubMed] [Google Scholar]
  53. Radsak K., Fuhrmann R., Franke R. P., Schneider D., Kollert A., Brücher K. H., Drenckhahn D. Induction by sodium butyrate of cytomegalovirus replication in human endothelial cells. Arch Virol. 1989;107(1-2):151–158. doi: 10.1007/BF01313887. [DOI] [PubMed] [Google Scholar]
  54. Rochford R., Moreno J. P., Peake M. L., Villarreal L. P. Enhancer dependence of polyomavirus persistence in mouse kidneys. J Virol. 1992 Jun;66(6):3287–3297. doi: 10.1128/jvi.66.6.3287-3297.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Roman A. Alteration in the simian virus 40 maturation pathway after butyrate-induced hyperacetylation of histones. J Virol. 1982 Dec;44(3):958–962. doi: 10.1128/jvi.44.3.958-962.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Roubal J., Luka J., Klein G. Effect of retinoic acid (RA) on the Epstein-Barr virus (EBV)-inducing effect of sodium butyrate. Cancer Lett. 1980 Jan;8(3):209–212. doi: 10.1016/0304-3835(80)90003-8. [DOI] [PubMed] [Google Scholar]
  57. Saemundsen A. K., Kallin B., Klein G. Effect of n-butyrate on cellular and viral DNA synthesis in cells latently infected with Epstein-Barr virus. Virology. 1980 Dec;107(2):557–561. doi: 10.1016/0042-6822(80)90326-8. [DOI] [PubMed] [Google Scholar]
  58. Shadan F. F., Villarreal L. P. Coevolution of persistently infecting small DNA viruses and their hosts linked to host-interactive regulatory domains. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4117–4121. doi: 10.1073/pnas.90.9.4117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Shen D. W., Real F. X., DeLeo A. B., Old L. J., Marks P. A., Rifkind R. A. Protein p53 and inducer-mediated erythroleukemia cell commitment to terminal cell division. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5919–5922. doi: 10.1073/pnas.80.19.5919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Staiano-Coico L., Steinberg M., Higgins P. J. Epidermal cell-shape regulation and subpopulation kinetics during butyrate-induced terminal maturation of normal and SV40-transformed human keratinocytes: epithelial models of differentiation therapy. Int J Cancer. 1990 Oct 15;46(4):733–738. doi: 10.1002/ijc.2910460430. [DOI] [PubMed] [Google Scholar]
  61. Sugawara K., Kawanishi M., Ito Y. Epstein-barr virus-related DNA-binding proteins induced by n-butyrate in P3HR-1 cells. Virology. 1982 Jan 15;116(1):354–358. doi: 10.1016/0042-6822(82)90427-5. [DOI] [PubMed] [Google Scholar]
  62. Tanaka J., Sadanari H., Sato H., Fukuda S. Sodium butyrate-inducible replication of human cytomegalovirus in a human epithelial cell line. Virology. 1991 Nov;185(1):271–280. doi: 10.1016/0042-6822(91)90774-6. [DOI] [PubMed] [Google Scholar]
  63. Tang D. C., Taylor M. W. Memory of butyrate induction by the Moloney murine sarcoma virus enhancer-promoter element. Biochem Biophys Res Commun. 1992 Nov 30;189(1):141–147. doi: 10.1016/0006-291x(92)91536-y. [DOI] [PubMed] [Google Scholar]
  64. Toscani A., Soprano D. R., Soprano K. J. Sodium butyrate in combination with insulin or dexamethasone can terminally differentiate actively proliferating Swiss 3T3 cells into adipocytes. J Biol Chem. 1990 Apr 5;265(10):5722–5730. [PubMed] [Google Scholar]
  65. Villarreal L. P. Relationship of eukaryotic DNA replication to committed gene expression: general theory for gene control. Microbiol Rev. 1991 Sep;55(3):512–542. doi: 10.1128/mr.55.3.512-542.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Wawra E., Pöckl E., Müllner E., Wintersberger E. Effect of sodium butyrate on induction of cellular and viral DNA syntheses in polyoma virus-infected mouse kidney cells. J Virol. 1981 Jun;38(3):973–981. doi: 10.1128/jvi.38.3.973-981.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Weber P. C., Levine M., Glorioso J. C. Rapid identification of nonessential genes of herpes simplex virus type 1 by Tn5 mutagenesis. Science. 1987 May 1;236(4801):576–579. doi: 10.1126/science.3033824. [DOI] [PubMed] [Google Scholar]
  68. Weintraub H. Assembly and propagation of repressed and depressed chromosomal states. Cell. 1985 Oct;42(3):705–711. doi: 10.1016/0092-8674(85)90267-3. [DOI] [PubMed] [Google Scholar]
  69. Whyte P., Buchkovich K. J., Horowitz J. M., Friend S. H., Raybuck M., Weinberg R. A., Harlow E. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature. 1988 Jul 14;334(6178):124–129. doi: 10.1038/334124a0. [DOI] [PubMed] [Google Scholar]
  70. Wintersberger E., Mudrak I. Sodium butyrate inhibits the synthesis of the transformation related protein p 53 in 3T6 mouse fibroblasts. FEBS Lett. 1984 Jan 30;166(2):326–330. doi: 10.1016/0014-5793(84)80105-2. [DOI] [PubMed] [Google Scholar]
  71. Wintersberger E., Mudrak I., Wintersberger U. Butyrate inhibits mouse fibroblasts at a control point in the G1 phase. J Cell Biochem. 1983;21(3):239–247. doi: 10.1002/jcb.240210306. [DOI] [PubMed] [Google Scholar]
  72. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. doi: 10.1038/270725a0. [DOI] [PubMed] [Google Scholar]
  73. Yew P. R., Berk A. J. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature. 1992 May 7;357(6373):82–85. doi: 10.1038/357082a0. [DOI] [PubMed] [Google Scholar]
  74. van der Vliet P. C., Kwant M. M. Role of DNA polymerase gamma in adenovirus DNA replication. Nature. 1978 Nov 30;276(5687):532–534. doi: 10.1038/276532a0. [DOI] [PubMed] [Google Scholar]

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