Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1992 May;66(5):3198–3205. doi: 10.1128/jvi.66.5.3198-3205.1992

A block in release of progeny virus and a high particle-to-infectious unit ratio contribute to poor growth of enteric adenovirus types 40 and 41 in cell culture.

M Brown 1, H L Wilson-Friesen 1, F Doane 1
PMCID: PMC241087  PMID: 1373207

Abstract

The fastidious enteric adenovirus (FEAd) types 40 (Ad40) and 41 (Ad41) are found in stool specimens of infants and young children in association with gastroenteritis. Although they can be isolated routinely from clinical specimens by using 293 cells, they are propagated with variable success in cell lines which support the replication of other adenovirus serotypes. HeLa cells are generally considered to be nonpermissive for the replication of FEAds, but in this study, Ad40 and Ad41 grew to comparable titers in individual 293 and HeLa cells. However, virus was not efficiently released from infected HeLa cells and thus did not undergo multiple cycles of infection in HeLa cell cultures. The block in virus release was not overcome in KB18 cells which, like 293 cells, constitutively express proteins encoded by the E1B region of a subgroup C adenovirus (in this case Ad2). Moreover, it was apparent from these studies that Ad40 and Ad41 have particle-to-infectious unit ratios several orders of magnitude greater than that for Ad5, even in 293 cells which express the E1A and E1B proteins of Ad5 and are considered to be permissive for replication of the FEAds. Neither the block in release of progeny virus nor the high particle-to-infectious unit ratio is explained solely by the defect in expression of the E1B 55K protein identified by Mautner et al. (V. Mautner, N. MacKay, and V. Steinthorsdottir, Virology 171:619-622, 1989; V. Mautner, N. MacKay, and K. Morris, Virology 179:129-138, 1990).

Full text

PDF
3198

Images in this article

3199Image
on p.3199
3200Image
on p.3200
3201Image
on p.3201

Selected References

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

  1. Anderson K. P., Fennie E. H. Adenovirus early region 1A modulation of interferon antiviral activity. J Virol. 1987 Mar;61(3):787–795. doi: 10.1128/jvi.61.3.787-795.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Babiss L. E., Young C. S., Fisher P. B., Ginsberg H. S. Expression of adenovirus E1a and E1b gene products and the Escherichia coli XGPRT gene in KB cells. J Virol. 1983 May;46(2):454–465. doi: 10.1128/jvi.46.2.454-465.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernards R., Vaessen M. J., Van der Eb A. J., Sussenbach J. S. Construction and characterization of an adenovirus type 5/adenovirus type 12 recombinant virus. Virology. 1983 Nov;131(1):30–38. doi: 10.1016/0042-6822(83)90530-5. [DOI] [PubMed] [Google Scholar]
  4. Bernards R., de Leeuw M. G., Houweling A., van der Eb A. J. Role of the adenovirus early region 1B tumor antigens in transformation and lytic infection. Virology. 1986 Apr 15;150(1):126–139. doi: 10.1016/0042-6822(86)90272-2. [DOI] [PubMed] [Google Scholar]
  5. Brown M. Laboratory identification of adenoviruses associated with gastroenteritis in Canada from 1983 to 1986. J Clin Microbiol. 1990 Jul;28(7):1525–1529. doi: 10.1128/jcm.28.7.1525-1529.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown M., Petric M., Middleton P. J. Diagnosis of fastidious enteric adenoviruses 40 and 41 in stool specimens. J Clin Microbiol. 1984 Sep;20(3):334–338. doi: 10.1128/jcm.20.3.334-338.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown M. Selection of nonfastidious adenovirus species in 293 cells inoculated with stool specimens containing adenovirus 40. J Clin Microbiol. 1985 Aug;22(2):205–209. doi: 10.1128/jcm.22.2.205-209.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brüggemann U., Klenk H. D., Doerfler W. Increased infectivity of extracellular adenovirus type 12. J Virol. 1985 Jul;55(1):117–125. doi: 10.1128/jvi.55.1.117-125.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Falck-Pedersen E., Logan J. Regulation of poly(A) site selection in adenovirus. J Virol. 1989 Feb;63(2):532–541. doi: 10.1128/jvi.63.2.532-541.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gary G. W., Jr, Hierholzer J. C., Black R. E. Characteristics of noncultivable adenoviruses associated with diarrhea in infants: a new subgroup of human adenoviruses. J Clin Microbiol. 1979 Jul;10(1):96–103. doi: 10.1128/jcm.10.1.96-103.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Glasgow L. A. Cytomegalovirus interference in vitro. Infect Immun. 1974 Apr;9(4):702–707. doi: 10.1128/iai.9.4.702-707.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977 Jul;36(1):59–74. doi: 10.1099/0022-1317-36-1-59. [DOI] [PubMed] [Google Scholar]
  13. Green M., Piña M., Kimes R. C. Biochemical studies on adenovirus multiplication. XII. Plaquing efficiencies of purified human adenoviruses. Virology. 1967 Mar;31(3):562–565. doi: 10.1016/0042-6822(67)90241-3. [DOI] [PubMed] [Google Scholar]
  14. Hashimoto S., Sakakibara N., Kumai H., Nakai M., Sakuma S., Chiba S., Fujinaga K. Fastidious human adenovirus type 40 can propagate efficiently and produce plaques on a human cell line, A549, derived from lung carcinoma. J Virol. 1991 May;65(5):2429–2435. doi: 10.1128/jvi.65.5.2429-2435.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ishino M., Ohashi Y., Emoto T., Sawada Y., Fujinaga K. Characterization of adenovirus type 40 E1 region. Virology. 1988 Jul;165(1):95–102. doi: 10.1016/0042-6822(88)90662-9. [DOI] [PubMed] [Google Scholar]
  16. Jansen-Durr P., Mondésert G., Kédinger C. Replication-dependent activation of the adenovirus major late promoter is mediated by the increased binding of a transcription factor to sequences in the first intron. J Virol. 1989 Dec;63(12):5124–5132. doi: 10.1128/jvi.63.12.5124-5132.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kidd A. H., Madeley C. R. In vitro growth of some fastidious adenoviruses from stool specimens. J Clin Pathol. 1981 Feb;34(2):213–216. doi: 10.1136/jcp.34.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kitajewski J., Schneider R. J., Safer B., Munemitsu S. M., Samuel C. E., Thimmappaya B., Shenk T. Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 alpha kinase. Cell. 1986 Apr 25;45(2):195–200. doi: 10.1016/0092-8674(86)90383-1. [DOI] [PubMed] [Google Scholar]
  19. Krajden M., Brown M., Petrasek A., Middleton P. J. Clinical features of adenovirus enteritis: a review of 127 cases. Pediatr Infect Dis J. 1990 Sep;9(9):636–641. [PubMed] [Google Scholar]
  20. 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]
  21. Mautner V., Mackay N., Morris K. Enteric adenovirus type 40: expression of E1B mRNA and proteins in permissive and nonpermissive cells. Virology. 1990 Nov;179(1):129–138. doi: 10.1016/0042-6822(90)90282-v. [DOI] [PubMed] [Google Scholar]
  22. Mautner V., Mackay N., Steinthorsdottir V. Complementation of enteric adenovirus type 40 for lytic growth in tissue culture by E1B 55K function of adenovirus types 5 and 12. Virology. 1989 Aug;171(2):619–622. doi: 10.1016/0042-6822(89)90634-x. [DOI] [PubMed] [Google Scholar]
  23. Perron-Henry D. M., Herrmann J. E., Blacklow N. R. Isolation and propagation of enteric adenoviruses in HEp-2 cells. J Clin Microbiol. 1988 Aug;26(8):1445–1447. doi: 10.1128/jcm.26.8.1445-1447.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pieniazek D., Pieniazek N. J., Macejak D., Coward J., Rayfield M., Luftig R. B. Differential growth of human enteric adenovirus 41 (TAK) in continuous cell lines. Virology. 1990 Jan;174(1):239–249. doi: 10.1016/0042-6822(90)90072-y. [DOI] [PubMed] [Google Scholar]
  25. Pieniazek D., Pieniazek N. J., Macejak D., Luftig R. B. Enteric adenovirus 41 (Tak) requires low serum for growth in human primary cells. Virology. 1990 Sep;178(1):72–80. doi: 10.1016/0042-6822(90)90380-a. [DOI] [PubMed] [Google Scholar]
  26. Retter M., Middleton P. J., Tam J. S., Petric M. Enteric adenoviruses: detection, replication, and significance. J Clin Microbiol. 1979 Oct;10(4):574–578. doi: 10.1128/jcm.10.4.574-578.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rowe D. T., Graham F. L., Branton P. E. Intracellular localization of adenovirus type 5 tumor antigens in productively infected cells. Virology. 1983 Sep;129(2):456–468. doi: 10.1016/0042-6822(83)90183-6. [DOI] [PubMed] [Google Scholar]
  28. Samuel C. E. Antiviral actions of interferon. Interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology. 1991 Jul;183(1):1–11. doi: 10.1016/0042-6822(91)90112-o. [DOI] [PubMed] [Google Scholar]
  29. Steinthorsdottir V., Mautner V. Enteric adenovirus type 40:E1B transcription map and identification of novel E1A-E1B cotranscripts in lytically infected cells. Virology. 1991 Mar;181(1):139–149. doi: 10.1016/0042-6822(91)90478-t. [DOI] [PubMed] [Google Scholar]
  30. Takiff H. E., Straus S. E. Early replicative block prevents the efficient growth of fastidious diarrhea- associated adenoviruses in cell culture. J Med Virol. 1982;9(2):93–100. doi: 10.1002/jmv.1890090203. [DOI] [PubMed] [Google Scholar]
  31. Takiff H. E., Straus S. E., Garon C. F. Propagation and in vitro studies of previously non-cultivable enteral adenoviruses in 293 cells. Lancet. 1981 Oct 17;2(8251):832–834. doi: 10.1016/s0140-6736(81)91104-1. [DOI] [PubMed] [Google Scholar]
  32. Thomas G. P., Mathews M. B. DNA replication and the early to late transition in adenovirus infection. Cell. 1980 Nov;22(2 Pt 2):523–533. doi: 10.1016/0092-8674(80)90362-1. [DOI] [PubMed] [Google Scholar]
  33. Uhnoo I., Wadell G., Svensson L., Johansson M. E. Importance of enteric adenoviruses 40 and 41 in acute gastroenteritis in infants and young children. J Clin Microbiol. 1984 Sep;20(3):365–372. doi: 10.1128/jcm.20.3.365-372.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ujfalusi M. J., Kidd A. H., Schoub B. D. EM study of fastidious adenovirus type 40 replication in vitro. Arch Virol. 1984;79(3-4):307–309. doi: 10.1007/BF01310820. [DOI] [PubMed] [Google Scholar]
  35. Witt D. J., Bousquet E. B. Comparison of enteric adenovirus infection in various human cell lines. J Virol Methods. 1988 Aug;20(4):295–308. doi: 10.1016/0166-0934(88)90133-4. [DOI] [PubMed] [Google Scholar]
  36. de Jong J. C., Wigand R., Kidd A. H., Wadell G., Kapsenberg J. G., Muzerie C. J., Wermenbol A. G., Firtzlaff R. G. Candidate adenoviruses 40 and 41: fastidious adenoviruses from human infant stool. J Med Virol. 1983;11(3):215–231. doi: 10.1002/jmv.1890110305. [DOI] [PubMed] [Google Scholar]
  37. van Loon A. E., Gilardi P., Perricaudet M., Rozijn T. H., Sussenbach J. S. Transcriptional activation by the E1A regions of adenovirus types 40 and 41. Virology. 1987 Sep;160(1):305–307. doi: 10.1016/0042-6822(87)90080-8. [DOI] [PubMed] [Google Scholar]
  38. van der Avoort H. G., Wermenbol A. G., Zomerdijk T. P., Kleijne J. A., van Asten J. A., Jensma P., Osterhaus A. D., Kidd A. H., de Jong J. C. Characterization of fastidious adenovirus types 40 and 41 by DNA restriction enzyme analysis and by neutralizing monoclonal antibodies. Virus Res. 1989 Feb;12(2):139–157. doi: 10.1016/0168-1702(89)90060-9. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES