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. 1985 Nov;56(2):439–448. doi: 10.1128/jvi.56.2.439-448.1985

Molecular composition of the adenovirus type 2 virion.

J van Oostrum, R M Burnett
PMCID: PMC252598  PMID: 4057357

Abstract

The representation of the different structural polypeptides within the adenovirus virion has been accurately determined, and the particle molecular weight has been derived. A stoichiometric analysis was performed with [35S]methionine as a radiolabel, and analytical sodium dodecyl sulfate-polyacrylamide gel electrophoresis was used to separate the polypeptides. The recently available sequence of the adenovirus type 2 genome was used to determine the number of methionines in each polypeptide. The resulting relative representation was placed on an absolute scale by using the known number of hexon polypeptides per virion. The analysis provides new information on the composition of the vertex region, which has been the subject of some controversy. Penton base was found to be present in 60 copies, distributed as pentamers at each of the 12 vertices. Three fiber monomers were associated with one penton base to form the penton complex. Polypeptide IX was present in 240 copies per virion and 12 copies per group-of-nine hexons, supporting a model proposed earlier for the distribution of this protein. The location of polypeptide IX explains the dissociation of the virus outer capsid into groups-of-nine hexons. The penton base was microheterogeneous, and the relative amounts suggest that the symmetry mismatch, which occurs within the penton complex between base and fiber, is resolved by the synthesis of penton base polypeptides from two closely spaced start codons.

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Selected References

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

  1. Akusjärvi G., Aleström P., Pettersson M., Lager M., Jörnvall H., Pettersson U. The gene for the adenovirus 2 hexon polypeptide. J Biol Chem. 1984 Nov 25;259(22):13976–13979. [PubMed] [Google Scholar]
  2. Akusjärvi G., Persson H. Gene and mRNA for precursor polypeptide VI from adenovirus type 2. J Virol. 1981 May;38(2):469–482. doi: 10.1128/jvi.38.2.469-482.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aleström P., Akusjärvi G., Lager M., Yeh-kai L., Pettersson U. Genes encoding the core proteins of adenovirus type 2. J Biol Chem. 1984 Nov 25;259(22):13980–13985. [PubMed] [Google Scholar]
  4. Aleström P., Akusjärvi G., Perricaudet M., Mathews M. B., Klessig D. F., Pettersson U. The gene for polypeptide IX of adenovirus type 2 and its unspliced messenger RNA. Cell. 1980 Mar;19(3):671–681. doi: 10.1016/s0092-8674(80)80044-4. [DOI] [PubMed] [Google Scholar]
  5. Anderson C. W., Lewis J. B. Amino-terminal sequence of adenovirus type 2 proteins: hexon, fiber, component IX, and early protein 1B-15K. Virology. 1980 Jul 15;104(1):27–41. doi: 10.1016/0042-6822(80)90363-3. [DOI] [PubMed] [Google Scholar]
  6. Bloemendal H. The vertebrate eye lens. Science. 1977 Jul 8;197(4299):127–138. doi: 10.1126/science.877544. [DOI] [PubMed] [Google Scholar]
  7. Boudin M. L., Boulanger P. Antibody-triggered dissociation of adenovirus penton capsomer. Virology. 1981 Sep;113(2):781–786. doi: 10.1016/0042-6822(81)90208-7. [DOI] [PubMed] [Google Scholar]
  8. Boudin M. L., D'Halluin J. C., Cousin C., Boulanger P. Human adenovirus type 2 protein IIIa. II. Maturation and encapsidation. Virology. 1980 Feb;101(1):144–156. doi: 10.1016/0042-6822(80)90491-2. [DOI] [PubMed] [Google Scholar]
  9. Boudin M. L., Moncany M., D'Halluin J. C., Boulanger P. A. Isolation and characterization of adenovirus type 2 vertex capsomer (penton base). Virology. 1979 Jan 15;92(1):125–138. doi: 10.1016/0042-6822(79)90219-8. [DOI] [PubMed] [Google Scholar]
  10. Boulanger P. A., Devaux C., Loucheux-Lefebvre M. H. Comparative optical properties of free and assembled hexon capsomeres of human adenovirus type 2. FEBS Lett. 1977 Dec 20;85(1):52–56. doi: 10.1016/0014-5793(78)81246-0. [DOI] [PubMed] [Google Scholar]
  11. Boulanger P., Lemay P., Blair G. E., Russell W. C. Characterization of adenovirus protein IX. J Gen Virol. 1979 Sep;44(3):783–800. doi: 10.1099/0022-1317-44-3-783. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Burnett R. M., Grütter M. G., White J. L. The structure of the adenovirus capsid. I. An envelope model of hexon at 6 A resolution. J Mol Biol. 1985 Sep 5;185(1):105–123. doi: 10.1016/0022-2836(85)90186-x. [DOI] [PubMed] [Google Scholar]
  14. Burnett R. M. The structure of the adenovirus capsid. II. The packing symmetry of hexon and its implications for viral architecture. J Mol Biol. 1985 Sep 5;185(1):125–143. doi: 10.1016/0022-2836(85)90187-1. [DOI] [PubMed] [Google Scholar]
  15. Challberg M. D., Desiderio S. V., Kelly T. J., Jr Adenovirus DNA replication in vitro: characterization of a protein covalently linked to nascent DNA strands. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5105–5109. doi: 10.1073/pnas.77.9.5105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  17. Colby W. W., Shenk T. Adenovirus type 5 virions can be assembled in vivo in the absence of detectable polypeptide IX. J Virol. 1981 Sep;39(3):977–980. doi: 10.1128/jvi.39.3.977-980.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Devaux C., Berthet-Colominas C., Timmins P. A., Boulanger P., Jacrot B. Crystal packing and stoichiometry of the fibre protein of adenovirus type 2. J Mol Biol. 1984 Apr 25;174(4):729–737. doi: 10.1016/0022-2836(84)90094-9. [DOI] [PubMed] [Google Scholar]
  19. Devaux C., Zulauf M., Boulanger P., Jacrot B. Molecular weight of adenovirus serotype 2 capsomers. A new characterization. J Mol Biol. 1982 Apr 25;156(4):927–939. doi: 10.1016/0022-2836(82)90148-6. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Ginsberg H. S., Pereira H. G., Valentine R. C., Wilcox W. C. A proposed terminology for the adenovirus antigens and virion morphological subunits. Virology. 1966 Apr;28(4):782–783. doi: 10.1016/0042-6822(66)90271-6. [DOI] [PubMed] [Google Scholar]
  23. Green M. Oncogenic viruses. Annu Rev Biochem. 1970;39:701–756. doi: 10.1146/annurev.bi.39.070170.003413. [DOI] [PubMed] [Google Scholar]
  24. Green N. M., Wrigley N. G., Russell W. C., Martin S. R., McLachlan A. D. Evidence for a repeating cross-beta sheet structure in the adenovirus fibre. EMBO J. 1983;2(8):1357–1365. doi: 10.1002/j.1460-2075.1983.tb01592.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Grütter M., Franklin R. M. Studies on the molecular weight of the adenovirus type 2 hexon and its subunit. J Mol Biol. 1974 Oct 15;89(1):163–178. doi: 10.1016/0022-2836(74)90168-5. [DOI] [PubMed] [Google Scholar]
  26. Jörnvall H. Acetylation of Protein N-terminal amino groups structural observations on alpha-amino acetylated proteins. J Theor Biol. 1975 Nov;55(1):1–12. doi: 10.1016/s0022-5193(75)80105-6. [DOI] [PubMed] [Google Scholar]
  27. Jörnvall H., Akusjärvi G., Aleström P., von Bahr-Lindström H., Pettersson U., Appella E., Fowler A. V., Philipson L. The adenovirus hexon protein. The primary structure of the polypeptide and its correlation with the hexon gene. J Biol Chem. 1981 Jun 25;256(12):6181–6186. [PubMed] [Google Scholar]
  28. Jörnvall H., Ohlsson H., Philipson L. An acetylated N-terminus of adenovirus type 2 hexon protein. Biochem Biophys Res Commun. 1974 Jan 23;56(2):304–310. doi: 10.1016/0006-291x(74)90842-0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Laver W. G., Wrigley N. G., Pereira H. G. Removal of pentons from particles of adenovirus type 2. Virology. 1969 Nov;39(3):599–604. doi: 10.1016/0042-6822(69)90111-1. [DOI] [PubMed] [Google Scholar]
  31. Lemay P., Boudin M. L., Milleville M., Boulanger P. Human adenovirus type 2 protein IIIa. I. Purification and characterization. Virology. 1980 Feb;101(1):131–143. doi: 10.1016/0042-6822(80)90490-0. [DOI] [PubMed] [Google Scholar]
  32. Maizel J. V., Jr, White D. O., Scharff M. D. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology. 1968 Sep;36(1):115–125. doi: 10.1016/0042-6822(68)90121-9. [DOI] [PubMed] [Google Scholar]
  33. Mautner V., Pereira H. G. Crystallization of a second adenovirus protein (the fibre). Nature. 1971 Apr 16;230(5294):456–457. doi: 10.1038/230456a0. [DOI] [PubMed] [Google Scholar]
  34. Nevins J. R., Chen-Kiang S. Processing of adenovirus nuclear RNA to mRNA. Adv Virus Res. 1981;26:1–35. doi: 10.1016/s0065-3527(08)60419-4. [DOI] [PubMed] [Google Scholar]
  35. Newcomb W. W., Boring J. W., Brown J. C. Ion etching of human adenovirus 2: structure of the core. J Virol. 1984 Jul;51(1):52–56. doi: 10.1128/jvi.51.1.52-56.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Oberg B., Saborio J., Persson T., Everitt E., Philipson L. Identification of the in vitro translation products of adenovirus mRNA by immunoprecipitation. J Virol. 1975 Jan;15(1):199–207. doi: 10.1128/jvi.15.1.199-207.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pereira H. G., Valentine R. C., Russell W. C. Crystallization of an adenovirus protein (the hexon). Nature. 1968 Aug 31;219(5157):946–947. doi: 10.1038/219946a0. [DOI] [PubMed] [Google Scholar]
  38. Pereira H. G., Wrigley N. G. In vitro reconstitution, hexon bonding and handedness of incomplete adenovirus capsid. J Mol Biol. 1974 Jan 5;85(4):617–630. doi: 10.1016/0022-2836(74)90319-2. [DOI] [PubMed] [Google Scholar]
  39. Philipson L. Structure and assembly of adenoviruses. Curr Top Microbiol Immunol. 1984;109:1–52. doi: 10.1007/978-3-642-69460-8_1. [DOI] [PubMed] [Google Scholar]
  40. Pustell J., Kafatos F. C. A convenient and adaptable package of DNA sequence analysis programs for microcomputers. Nucleic Acids Res. 1982 Jan 11;10(1):51–59. doi: 10.1093/nar/10.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. ROWE W. P., HUEBNER R. J., GILMORE L. K., PARROTT R. H., WARD T. G. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc Soc Exp Biol Med. 1953 Dec;84(3):570–573. doi: 10.3181/00379727-84-20714. [DOI] [PubMed] [Google Scholar]
  42. Roberts R. J., O'Neill K. E., Yen C. T. DNA sequences from the adenovirus 2 genome. J Biol Chem. 1984 Nov 25;259(22):13968–13975. [PubMed] [Google Scholar]
  43. 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]
  44. Russell W. C., Precious B. Nucleic acid-binding properties of adenovirus structural polypeptides. J Gen Virol. 1982 Nov;63(Pt 1):69–79. doi: 10.1099/0022-1317-63-1-69. [DOI] [PubMed] [Google Scholar]
  45. Smith K. O., Gehle W. D., Trousdale M. D. Architecture of the Adenovirus Capsid. J Bacteriol. 1965 Jul;90(1):254–261. doi: 10.1128/jb.90.1.254-261.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sung M. T., Lischwe M. A., Richards J. C., Hosokawa K. Adenovirus chromatin I. Isolation and characterization of the major core protein VII and precursor Pro-VII. J Biol Chem. 1977 Jul 25;252(14):4981–4987. [PubMed] [Google Scholar]
  47. Tremblay M. L., Déry C. V., Talbot B. G., Weber J. In vitro cleavage specificity of the adenovirus type 2 proteinase. Biochim Biophys Acta. 1983 Mar 16;743(2):239–245. doi: 10.1016/0167-4838(83)90220-0. [DOI] [PubMed] [Google Scholar]
  48. Tsernoglou D., Tucker A. D., Van der Vliet P. C. Crystallization of a fragment of the adenovirus DNA binding protein. J Mol Biol. 1984 Jan 15;172(2):237–239. doi: 10.1016/s0022-2836(84)80042-x. [DOI] [PubMed] [Google Scholar]
  49. Williams J. F. Enhancement of adenovirus plaque formation on HeLa cells by magnesium chloride. J Gen Virol. 1970 Dec;9(3):251–255. doi: 10.1099/0022-1317-9-3-251. [DOI] [PubMed] [Google Scholar]

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