Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1995 Jun;69(6):3955–3958. doi: 10.1128/jvi.69.6.3955-3958.1995

Apoptosis as a cause of death in measles virus-infected cells.

L M Esolen 1, S W Park 1, J M Hardwick 1, D E Griffin 1
PMCID: PMC189125  PMID: 7745753

Abstract

To determine the mechanism of measles virus-induced cell death, we studied the infection of Vero cells and monocytic cell lines with wild-type (Chicago-1) and vaccine (Edmonston) strains of measles virus. DNA fragmentation indicative of apoptosis was apparent by flow cytometry, agarose gel electrophoresis, and electron microscopy. Within syncytia, DNA strand breaks were demonstrated by end labeling with terminal transferase and then by visualization.

Full Text

The Full Text of this article is available as a PDF (590.9 KB).

Selected References

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

  1. Ansari B., Coates P. J., Greenstein B. D., Hall P. A. In situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol. 1993 May;170(1):1–8. doi: 10.1002/path.1711700102. [DOI] [PubMed] [Google Scholar]
  2. Clem R. J., Fechheimer M., Miller L. K. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 1991 Nov 29;254(5036):1388–1390. doi: 10.1126/science.1962198. [DOI] [PubMed] [Google Scholar]
  3. Collins S. J., Gallo R. C., Gallagher R. E. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature. 1977 Nov 24;270(5635):347–349. doi: 10.1038/270347a0. [DOI] [PubMed] [Google Scholar]
  4. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M. A., Lassota P., Traganos F. Features of apoptotic cells measured by flow cytometry. Cytometry. 1992;13(8):795–808. doi: 10.1002/cyto.990130802. [DOI] [PubMed] [Google Scholar]
  5. Dive C., Gregory C. D., Phipps D. J., Evans D. L., Milner A. E., Wyllie A. H. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim Biophys Acta. 1992 Feb 3;1133(3):275–285. doi: 10.1016/0167-4889(92)90048-g. [DOI] [PubMed] [Google Scholar]
  6. ENDERS J. F., PEEBLES T. C. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc Soc Exp Biol Med. 1954 Jun;86(2):277–286. doi: 10.3181/00379727-86-21073. [DOI] [PubMed] [Google Scholar]
  7. Eckhardt T. A rapid method for the identification of plasmid desoxyribonucleic acid in bacteria. Plasmid. 1978 Sep;1(4):584–588. doi: 10.1016/0147-619x(78)90016-1. [DOI] [PubMed] [Google Scholar]
  8. Esolen L. M., Ward B. J., Moench T. R., Griffin D. E. Infection of monocytes during measles. J Infect Dis. 1993 Jul;168(1):47–52. doi: 10.1093/infdis/168.1.47. [DOI] [PubMed] [Google Scholar]
  9. Gougeon M. L., Garcia S., Heeney J., Tschopp R., Lecoeur H., Guetard D., Rame V., Dauguet C., Montagnier L. Programmed cell death in AIDS-related HIV and SIV infections. AIDS Res Hum Retroviruses. 1993 Jun;9(6):553–563. doi: 10.1089/aid.1993.9.553. [DOI] [PubMed] [Google Scholar]
  10. Henderson S., Huen D., Rowe M., Dawson C., Johnson G., Rickinson A. Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8479–8483. doi: 10.1073/pnas.90.18.8479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Heneen W. K., Nichols W. W., Levan A., Norrby E. Studies on syncytia formation in a cell line (LU 106) of human origin after treatment with measles virus. Hereditas. 1967;57(3):369–372. doi: 10.1111/j.1601-5223.1967.tb02121.x. [DOI] [PubMed] [Google Scholar]
  12. Hussey G. D., Klein M. A randomized, controlled trial of vitamin A in children with severe measles. N Engl J Med. 1990 Jul 19;323(3):160–164. doi: 10.1056/NEJM199007193230304. [DOI] [PubMed] [Google Scholar]
  13. Iwata M., Mukai M., Nakai Y., Iseki R. Retinoic acids inhibit activation-induced apoptosis in T cell hybridomas and thymocytes. J Immunol. 1992 Nov 15;149(10):3302–3308. [PubMed] [Google Scholar]
  14. Jeurissen S. H., Wagenaar F., Pol J. M., van der Eb A. J., Noteborn M. H. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol. 1992 Dec;66(12):7383–7388. doi: 10.1128/jvi.66.12.7383-7388.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaufmann S. H., Desnoyers S., Ottaviano Y., Davidson N. E., Poirier G. G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993 Sep 1;53(17):3976–3985. [PubMed] [Google Scholar]
  16. Lazebnik Y. A., Kaufmann S. H., Desnoyers S., Poirier G. G., Earnshaw W. C. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature. 1994 Sep 22;371(6495):346–347. doi: 10.1038/371346a0. [DOI] [PubMed] [Google Scholar]
  17. Levine B., Huang Q., Isaacs J. T., Reed J. C., Griffin D. E., Hardwick J. M. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature. 1993 Feb 25;361(6414):739–742. doi: 10.1038/361739a0. [DOI] [PubMed] [Google Scholar]
  18. Levy Y., Brouet J. C. Interleukin-10 prevents spontaneous death of germinal center B cells by induction of the bcl-2 protein. J Clin Invest. 1994 Jan;93(1):424–428. doi: 10.1172/JCI116977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meyaard L., Otto S. A., Jonker R. R., Mijnster M. J., Keet R. P., Miedema F. Programmed death of T cells in HIV-1 infection. Science. 1992 Jul 10;257(5067):217–219. doi: 10.1126/science.1352911. [DOI] [PubMed] [Google Scholar]
  20. Moench T. R., Griffin D. E., Obriecht C. R., Vaisberg A. J., Johnson R. T. Acute measles in patients with and without neurological involvement: distribution of measles virus antigen and RNA. J Infect Dis. 1988 Aug;158(2):433–442. doi: 10.1093/infdis/158.2.433. [DOI] [PubMed] [Google Scholar]
  21. Nichols W. W., Levan A., Aula P., Norrby E. Chromosome damage associated with the measles virus in vitro. Hereditas. 1965;54(1):101–118. doi: 10.1111/j.1601-5223.1965.tb02008.x. [DOI] [PubMed] [Google Scholar]
  22. Ohno K., Nakano T., Matsumoto Y., Watari T., Goitsuka R., Nakayama H., Tsujimoto H., Hasegawa A. Apoptosis induced by tumor necrosis factor in cells chronically infected with feline immunodeficiency virus. J Virol. 1993 May;67(5):2429–2433. doi: 10.1128/jvi.67.5.2429-2433.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oritani K., Kaisho T., Nakajima K., Hirano T. Retinoic acid inhibits interleukin-6-induced macrophage differentiation and apoptosis in a murine hematopoietic cell line, Y6. Blood. 1992 Nov 1;80(9):2298–2305. [PubMed] [Google Scholar]
  24. ROBERTS G. B., BAIN A. D. The pathology of measles. J Pathol Bacteriol. 1958 Jul;76(1):111–118. doi: 10.1002/path.1700760112. [DOI] [PubMed] [Google Scholar]
  25. Rahmathullah L., Underwood B. A., Thulasiraj R. D., Milton R. C., Ramaswamy K., Rahmathullah R., Babu G. Reduced mortality among children in southern India receiving a small weekly dose of vitamin A. N Engl J Med. 1990 Oct 4;323(14):929–935. doi: 10.1056/NEJM199010043231401. [DOI] [PubMed] [Google Scholar]
  26. Rao L., Debbas M., Sabbatini P., Hockenbery D., Korsmeyer S., White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7742–7746. doi: 10.1073/pnas.89.16.7742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rota J. S., Hummel K. B., Rota P. A., Bellini W. J. Genetic variability of the glycoprotein genes of current wild-type measles isolates. Virology. 1992 May;188(1):135–142. doi: 10.1016/0042-6822(92)90742-8. [DOI] [PubMed] [Google Scholar]
  28. SHERMAN F. E., RUCKLE G. In vivo and in vitro cellular changes specific for measles. AMA Arch Pathol. 1958 Jun;65(6):587–599. [PubMed] [Google Scholar]
  29. Takizawa T., Matsukawa S., Higuchi Y., Nakamura S., Nakanishi Y., Fukuda R. Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells. J Gen Virol. 1993 Nov;74(Pt 11):2347–2355. doi: 10.1099/0022-1317-74-11-2347. [DOI] [PubMed] [Google Scholar]
  30. Tsuchiya S., Yamabe M., Yamaguchi Y., Kobayashi Y., Konno T., Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer. 1980 Aug;26(2):171–176. doi: 10.1002/ijc.2910260208. [DOI] [PubMed] [Google Scholar]
  31. Ward B. J., Johnson R. T., Vaisberg A., Jauregui E., Griffin D. E. Cytokine production in vitro and the lymphoproliferative defect of natural measles virus infection. Clin Immunol Immunopathol. 1991 Nov;61(2 Pt 1):236–248. doi: 10.1016/s0090-1229(05)80027-3. [DOI] [PubMed] [Google Scholar]
  32. Williams G. T. Programmed cell death: apoptosis and oncogenesis. Cell. 1991 Jun 28;65(7):1097–1098. doi: 10.1016/0092-8674(91)90002-g. [DOI] [PubMed] [Google Scholar]
  33. Wyllie A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980 Apr 10;284(5756):555–556. doi: 10.1038/284555a0. [DOI] [PubMed] [Google Scholar]
  34. Wyllie A. H., Morris R. G., Smith A. L., Dunlop D. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol. 1984 Jan;142(1):67–77. doi: 10.1002/path.1711420112. [DOI] [PubMed] [Google Scholar]
  35. Zychlinsky A., Prevost M. C., Sansonetti P. J. Shigella flexneri induces apoptosis in infected macrophages. Nature. 1992 Jul 9;358(6382):167–169. doi: 10.1038/358167a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES