Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1983 Jan 25;11(2):441–460. doi: 10.1093/nar/11.2.441

The structure of nucleoprotein cores released from adenovirions.

M E Vayda, A E Rogers, S J Flint
PMCID: PMC325724  PMID: 6828374

Abstract

The morphology, protein composition and DNA organization of nucleoprotein core complexes isolated from type 5 adenovirions have been examined by electron microscopy and biochemical techniques. The morphology of such core structures is in some ways strikingly similar to that exhibited by cellular chromatin. 'Native' core preparations contain compact and less highly-folded forms: the latter appear as thick fibres, 150-300A in diameter. Upon exposure to 0.4M NaCl, adenovirus cores undergo a transition to a beaded string form, reminiscent of nucleosomes. Of the three arginine-rich proteins, polypeptides V, VII and mu present in 'native' cores, only polypeptide VII remains associated with viral DNA in the presence of 0.4M NaCl. We therefore conclude that the nucleosome-like beads are constructed solely of polypeptide VII. The results of micrococcal nuclease digestion experiments suggest that polypeptide VII is sufficient to protect some 100-300bp of adenoviral DNA.

Full text

PDF
441

Images in this article

444Image
on p.444
445Image
on p.445
448Image
on p.448
449Image
on p.449
452Image
on p.452
454Image
on p.454

Selected References

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

  1. Anderson C. W., Baum P. R., Gesteland R. F. Processing of adenovirus 2-induced proteins. J Virol. 1973 Aug;12(2):241–252. doi: 10.1128/jvi.12.2.241-252.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baczko K., Neumann R., Doerfler W. Intracellular forms of adenovirus DNA. VII. Excision of viral sequences from cellular DNA in adenovirus type 2-infected KB cells. Virology. 1978 Apr;85(2):557–567. doi: 10.1016/0042-6822(78)90461-0. [DOI] [PubMed] [Google Scholar]
  3. Bina-Stein M., Simpson R. T. Specific folding and contraction of DNA by histones H3 and H4. Cell. 1977 Jul;11(3):609–618. doi: 10.1016/0092-8674(77)90078-2. [DOI] [PubMed] [Google Scholar]
  4. Binger M. H., Flint S. J., Rekosh D. M. Expression of the gene encoding the adenovirus DNA terminal protein precursor in productively infected and transformed cells. J Virol. 1982 May;42(2):488–501. doi: 10.1128/jvi.42.2.488-501.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown D. T., Westphal M., Burlingham B. T., Winterhoff U., Doerfler W. Structure and composition of the adenovirus type 2 core. J Virol. 1975 Aug;16(2):366–387. doi: 10.1128/jvi.16.2.366-387.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown M., Weber J. Virion core-like organization of intranuclear adenovirus chromatin late in infection. Virology. 1980 Nov;107(1):306–310. doi: 10.1016/0042-6822(80)90297-4. [DOI] [PubMed] [Google Scholar]
  7. Camerini-Otero R. D., Sollner-Webb B., Felsenfeld G. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel. Cell. 1976 Jul;8(3):333–347. doi: 10.1016/0092-8674(76)90145-8. [DOI] [PubMed] [Google Scholar]
  8. Clark R. J., Felsenfeld G. Structure of chromatin. Nat New Biol. 1971 Jan 27;229(4):101–106. doi: 10.1038/newbio229101a0. [DOI] [PubMed] [Google Scholar]
  9. Coelingh J. P., Monfoort C. H., Rozijn T. H., Leuven J. A., Schiphof R., Steyn-Parvé E. P., Braunitzer G., Schrank B., Ruhfus A. The complete amino acid sequence of the basic nuclear protein of bull spermatozoa. Biochim Biophys Acta. 1972 Nov 28;285(1):1–14. doi: 10.1016/0005-2795(72)90174-2. [DOI] [PubMed] [Google Scholar]
  10. Corden J., Engelking H. M., Pearson G. D. Chromatin-like organization of the adenovirus chromosome. Proc Natl Acad Sci U S A. 1976 Feb;73(2):401–404. doi: 10.1073/pnas.73.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Daniell E., Groff D. E., Fedor M. J. Adenovirus chromatin structure at different stages of infection. Mol Cell Biol. 1981 Dec;1(12):1094–1105. doi: 10.1128/mcb.1.12.1094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dingwall C., Lomonossoff G. P., Laskey R. A. High sequence specificity of micrococcal nuclease. Nucleic Acids Res. 1981 Jun 25;9(12):2659–2673. doi: 10.1093/nar/9.12.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. EPSTEIN M. A. Observations on the fine structure of type 5 adenovirus. J Biophys Biochem Cytol. 1959 Dec;6:523–526. doi: 10.1083/jcb.6.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Everitt E., Lutter L., Philipson L. Structural proteins of adenoviruses. XII. Location and neighbor relationship among proteins of adenovirion type 2 as revealed by enzymatic iodination, immunoprecipitation and chemical cross-linking. Virology. 1975 Sep;67(1):197–208. doi: 10.1016/0042-6822(75)90417-1. [DOI] [PubMed] [Google Scholar]
  15. Everitt E., Sundquist B., Pettersson U., Philipson L. Structural proteins of adenoviruses. X. Isolation and topography of low molecular weight antigens from the virion of adenovirus type 2. Virology. 1973 Mar;52(1):130–147. doi: 10.1016/0042-6822(73)90404-2. [DOI] [PubMed] [Google Scholar]
  16. Flint S. J., Gallimore P. H., Sharp P. A. Comparison of viral RNA sequences in adenovirus 2-transformed and lytically infected cells. J Mol Biol. 1975 Jul 25;96(1):47–68. doi: 10.1016/0022-2836(75)90181-3. [DOI] [PubMed] [Google Scholar]
  17. Frearson P. M., Crawford L. V. Polyoma virus basic proteins. J Gen Virol. 1972 Feb;14(2):141–155. doi: 10.1099/0022-1317-14-2-141. [DOI] [PubMed] [Google Scholar]
  18. Green M., Piña M., Kimes R., Wensink P. C., MacHattie L. A., Thomas C. A., Jr Adenovirus DNA. I. Molecular weight and conformation. Proc Natl Acad Sci U S A. 1967 May;57(5):1302–1309. doi: 10.1073/pnas.57.5.1302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hosokawa K., Sung M. T. Isolation and characterization of an extremely basic protein from adenovirus type 5. J Virol. 1976 Mar;17(3):924–934. doi: 10.1128/jvi.17.3.924-934.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hörz W., Altenburger W. Sequence specific cleavage of DNA by micrococcal nuclease. Nucleic Acids Res. 1981 Jun 25;9(12):2643–2658. doi: 10.1093/nar/9.12.2643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Igo-Kemenes T., Hörz W., Zachau H. G. Chromatin. Annu Rev Biochem. 1982;51:89–121. doi: 10.1146/annurev.bi.51.070182.000513. [DOI] [PubMed] [Google Scholar]
  22. Itzhaki R. F. The arrangement of proteins on the deoxyribonucleic acid in chromatin. Biochem J. 1971 Nov;125(1):221–224. doi: 10.1042/bj1250221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Keene M. A., Elgin S. C. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure. Cell. 1981 Nov;27(1 Pt 2):57–64. doi: 10.1016/0092-8674(81)90360-3. [DOI] [PubMed] [Google Scholar]
  24. Kistler W. S., Geroch M. E., Williams-Ashman H. G. Specific basic proteins from mammalian testes. Isolation and properties of small basic proteins from rat testes and epididymal spermatozoa. J Biol Chem. 1973 Jul 10;248(13):4532–4543. [PubMed] [Google Scholar]
  25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  26. Lake R. S., Barban S., Salzman N. P. Resolutions and identification of the core deoxynucleoproteins of the simian virus 40. Biochem Biophys Res Commun. 1973 Sep 18;54(2):640–647. doi: 10.1016/0006-291x(73)91471-x. [DOI] [PubMed] [Google Scholar]
  27. Laver W. G. Isolation of an arginine-rich protein from particles of adenovirus type 2. Virology. 1970 Jul;41(3):488–500. doi: 10.1016/0042-6822(70)90170-4. [DOI] [PubMed] [Google Scholar]
  28. Laver W. G., Pereira H. G., Russell W. C., Valentine R. C. Isolation of an internal component from adenovirus type 5. J Mol Biol. 1968 Nov 14;37(3):379–386. doi: 10.1016/0022-2836(68)90109-5. [DOI] [PubMed] [Google Scholar]
  29. Laver W. G., Suriano J. R., Green M. Adenovirus proteins. II. N-terminal amino acid analysis. J Virol. 1967 Aug;1(4):723–728. doi: 10.1128/jvi.1.4.723-728.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lawn R. M., Fritsch E. F., Parker R. C., Blake G., Maniatis T. The isolation and characterization of linked delta- and beta-globin genes from a cloned library of human DNA. Cell. 1978 Dec;15(4):1157–1174. doi: 10.1016/0092-8674(78)90043-0. [DOI] [PubMed] [Google Scholar]
  31. Lilley D. M., Pardon J. F. Structure and function of chromatin. Annu Rev Genet. 1979;13:197–233. doi: 10.1146/annurev.ge.13.120179.001213. [DOI] [PubMed] [Google Scholar]
  32. Lischwe M. A., Sung M. T. A histone-like protein from adenovirus chromatin. Nature. 1977 Jun 9;267(5611):552–554. doi: 10.1038/267552a0. [DOI] [PubMed] [Google Scholar]
  33. McGhee J. D., Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. doi: 10.1146/annurev.bi.49.070180.005343. [DOI] [PubMed] [Google Scholar]
  34. Nermut M. V., Harpst J. A., Russell W. C. Electron microscopy of adenovirus cores. J Gen Virol. 1975 Jul;28(1):49–58. doi: 10.1099/0022-1317-28-1-49. [DOI] [PubMed] [Google Scholar]
  35. Nermut M. V. Structural elements in adenovirus cores. Evidence for a "core shell" and linear structures in "relaxed" cores. Arch Virol. 1979;62(2):101–116. doi: 10.1007/BF01318063. [DOI] [PubMed] [Google Scholar]
  36. Olins A. L., Olins D. E. Spheroid chromatin units (v bodies). Science. 1974 Jan 25;183(4122):330–332. doi: 10.1126/science.183.4122.330. [DOI] [PubMed] [Google Scholar]
  37. Oudet P., Gross-Bellard M., Chambon P. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell. 1975 Apr;4(4):281–300. doi: 10.1016/0092-8674(75)90149-x. [DOI] [PubMed] [Google Scholar]
  38. Pettersson U., Sambrook J. Amount of viral DNA in the genome of cells transformed by adenovirus type 2. J Mol Biol. 1973 Jan;73(1):125–130. doi: 10.1016/0022-2836(73)90164-2. [DOI] [PubMed] [Google Scholar]
  39. Prage L., Pettersson U., Höglund S., Lonberg-Holm K., Philipson L. Structural proteins of adenoviruses. IV. Sequential degradation of the adenovirus type 2 virion. Virology. 1970 Oct;42(2):341–358. doi: 10.1016/0042-6822(70)90278-3. [DOI] [PubMed] [Google Scholar]
  40. Prage L., Pettersson U., Philipson L. Internal basic proteins in adenovirus. Virology. 1968 Nov;36(3):508–511. doi: 10.1016/0042-6822(68)90178-5. [DOI] [PubMed] [Google Scholar]
  41. Prage L., Pettersson U. Structural proteins of adenoviruses. VII. Purification and properties of an arginine-rich core protein from adenovirus type 2 and type 3. Virology. 1971 Aug;45(2):364–373. doi: 10.1016/0042-6822(71)90337-0. [DOI] [PubMed] [Google Scholar]
  42. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  43. Ris H., Kubai D. F. Chromosome structure. Annu Rev Genet. 1970;4:263–294. doi: 10.1146/annurev.ge.04.120170.001403. [DOI] [PubMed] [Google Scholar]
  44. Robinson A. J., Younghusband H. B., Bellett A. J. A circula DNA-protein complex from adenoviruses. Virology. 1973 Nov;56(1):54–69. doi: 10.1016/0042-6822(73)90287-0. [DOI] [PubMed] [Google Scholar]
  45. Roblin R., Härle E., Dulbecco R. Polyoma virus proteins. 1. Multiple virion components. Virology. 1971 Sep;45(3):555–566. doi: 10.1016/0042-6822(71)90171-1. [DOI] [PubMed] [Google Scholar]
  46. Russell W. C., McIntosh K., Skehel J. J. The preparation and properties of adenovirus cores. J Gen Virol. 1971 Apr;11(1):35–46. doi: 10.1099/0022-1317-11-1-35. [DOI] [PubMed] [Google Scholar]
  47. Schick J., Baczko K., Fanning E., Groneberg J., Burger H., Doerfler W. Intracellular forms of adenovirus DNA: integrated form of adenovirus DNA appears early in productive infection. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1043–1047. doi: 10.1073/pnas.73.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sergeant A., Tigges M. A., Raskas H. J. Nucleosome-like structural subunits of intranuclear parental adenovirus type 2 DNA. J Virol. 1979 Mar;29(3):888–898. doi: 10.1128/jvi.29.3.888-898.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Sharp P. A., Moore C., Haverty J. L. The infectivity of adenovirus 5 DNA-protein complex. Virology. 1976 Dec;75(2):442–456. doi: 10.1016/0042-6822(76)90042-8. [DOI] [PubMed] [Google Scholar]
  50. Sollner-Webb B., Camerini-Otero R. D., Felsenfeld G. Chromatin structure as probed by nucleases and proteases: evidence for the central role of histones H3 and H4. Cell. 1976 Sep;9(1):179–193. doi: 10.1016/0092-8674(76)90063-5. [DOI] [PubMed] [Google Scholar]
  51. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  52. Tate V. E., Philipson L. Parental adenovirus DNA accumulates in nucleosome-like structures in infected cells. Nucleic Acids Res. 1979 Jun 25;6(8):2769–2785. doi: 10.1093/nar/6.8.2769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Thach S. S., Collins M. L., Thach R. E. Electron microscopy of single and double stranded nucleic acid: a new technique. J Ultrastruct Res. 1976 Apr;55(1):70–78. doi: 10.1016/s0022-5320(76)80082-2. [DOI] [PubMed] [Google Scholar]
  54. Tyndall C., Younghusband H. B., Bellett A. J. Some adenovirus DNA is associated with the DNA of permissive cells during productive or restricted growth. J Virol. 1978 Jan;25(1):1–10. doi: 10.1128/jvi.25.1.1-10.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Walter G., Maizel J. V., Jr The polypeptides of adenovirus. IV. Detection of early and late virus-induced polypeptides and their distribution in subcellular fractions. Virology. 1974 Feb;57(2):402–408. doi: 10.1016/0042-6822(74)90180-9. [DOI] [PubMed] [Google Scholar]
  56. Weber J., Begin M., Carstens E. B. Genetic analysis of adneovirus type 2. IV. Coordinate regulation of polypeptides 80K, IIIa, and V. Virology. 1977 Feb;76(2):709–724. doi: 10.1016/0042-6822(77)90253-7. [DOI] [PubMed] [Google Scholar]
  57. Weber J. Genetic analysis of adenovirus type 2 III. Temperature sensitivity of processing viral proteins. J Virol. 1976 Feb;17(2):462–471. doi: 10.1128/jvi.17.2.462-471.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wu C., Bingham P. M., Livak K. J., Holmgren R., Elgin S. C. The chromatin structure of specific genes: I. Evidence for higher order domains of defined DNA sequence. Cell. 1979 Apr;16(4):797–806. doi: 10.1016/0092-8674(79)90095-3. [DOI] [PubMed] [Google Scholar]
  59. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]
  60. van der Eb A. J., van Kesteren L. W., van Bruggen E. F. Structural properties of adenovirus DNA's. Biochim Biophys Acta. 1969 Jun 17;182(2):530–541. doi: 10.1016/0005-2787(69)90205-6. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES