Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Aug 30;91(18):8641–8645. doi: 10.1073/pnas.91.18.8641

Expression of a specific marker of avian programmed cell death in both apoptosis and necrosis.

P A Fernandez 1, R J Rotello 1, Z Rangini 1, A Doupe 1, H C Drexler 1, J Yuan 1
PMCID: PMC44662  PMID: 8078937

Abstract

Apoptosis and necrosis are two types of cell death with different morphologic features. We report here the isolation of a monoclonal antibody, BV2, that specifically recognizes cells undergoing developmental programmed cell death in different tissues of the chicken and zebra-finch embryos. The antigen recognized by BV2 monoclonal antibody is detected in vitro in primary chicken embryonic fibroblasts induced to die by actinomycin D, as well as fibroblasts induced to die by chemical anoxia. The expression of this specific antigen during necrosis appears to require active protein synthesis. These findings provide evidence that cells from different embryonic tissues undergoing programmed cell death during vertebrate development express similar antigens and indicate that apoptosis and necrosis may share similar biochemical features.

Full text

PDF
8641

Images in this article

Selected References

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

  1. Alnemri E. S., Fernandes T. F., Haldar S., Croce C. M., Litwack G. Involvement of BCL-2 in glucocorticoid-induced apoptosis of human pre-B-leukemias. Cancer Res. 1992 Jan 15;52(2):491–495. [PubMed] [Google Scholar]
  2. Bandyk M. G., Sawczuk I. S., Olsson C. A., Katz A. E., Buttyan R. Characterization of the products of a gene expressed during androgen-programmed cell death and their potential use as a marker of urogenital injury. J Urol. 1990 Feb;143(2):407–413. doi: 10.1016/s0022-5347(17)39975-5. [DOI] [PubMed] [Google Scholar]
  3. Batistatou A., Greene L. A. Internucleosomal DNA cleavage and neuronal cell survival/death. J Cell Biol. 1993 Aug;122(3):523–532. doi: 10.1083/jcb.122.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Briehl M. M., Miesfeld R. L. Isolation and characterization of transcripts induced by androgen withdrawal and apoptotic cell death in the rat ventral prostate. Mol Endocrinol. 1991 Oct;5(10):1381–1388. doi: 10.1210/mend-5-10-1381. [DOI] [PubMed] [Google Scholar]
  5. Buckley I. K. A light and electron microscopic study of thermally injured cultured cells. Lab Invest. 1972 Feb;26(2):201–209. [PubMed] [Google Scholar]
  6. Carnegie J. A., McCully M. E., Robertson H. A. Embedment in glycol methacrylate at low temperature allows immunofluorescent localization of a labile tissue protein. J Histochem Cytochem. 1980 Apr;28(4):308–310. doi: 10.1177/28.4.6768792. [DOI] [PubMed] [Google Scholar]
  7. Cheung J. Y., Bonventre J. V., Malis C. D., Leaf A. Calcium and ischemic injury. N Engl J Med. 1986 Jun 26;314(26):1670–1676. doi: 10.1056/NEJM198606263142604. [DOI] [PubMed] [Google Scholar]
  8. Ellis R. E., Yuan J. Y., Horvitz H. R. Mechanisms and functions of cell death. Annu Rev Cell Biol. 1991;7:663–698. doi: 10.1146/annurev.cb.07.110191.003311. [DOI] [PubMed] [Google Scholar]
  9. Fesus L., Thomazy V., Falus A. Induction and activation of tissue transglutaminase during programmed cell death. FEBS Lett. 1987 Nov 16;224(1):104–108. doi: 10.1016/0014-5793(87)80430-1. [DOI] [PubMed] [Google Scholar]
  10. Harrigan M. T., Baughman G., Campbell N. F., Bourgeois S. Isolation and characterization of glucocorticoid- and cyclic AMP-induced genes in T lymphocytes. Mol Cell Biol. 1989 Aug;9(8):3438–3446. doi: 10.1128/mcb.9.8.3438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell. 1991 Jun 28;65(7):1107–1115. doi: 10.1016/0092-8674(91)90007-l. [DOI] [PubMed] [Google Scholar]
  12. Hennet T., Bertoni G., Richter C., Peterhans E. Expression of BCL-2 protein enhances the survival of mouse fibrosarcoid cells in tumor necrosis factor-mediated cytotoxicity. Cancer Res. 1993 Mar 15;53(6):1456–1460. [PubMed] [Google Scholar]
  13. Hockfield S. A Mab to a unique cerebellar neuron generated by immunosuppression and rapid immunization. Science. 1987 Jul 3;237(4810):67–70. doi: 10.1126/science.3603010. [DOI] [PubMed] [Google Scholar]
  14. Humphrey C. D., Pittman F. E. A simple methylene blue-azure II-basic fuchsin stain for epoxy-embedded tissue sections. Stain Technol. 1974 Jan;49(1):9–14. doi: 10.3109/10520297409116929. [DOI] [PubMed] [Google Scholar]
  15. Hunter E. Biological techniques for avian sarcoma viruses. Methods Enzymol. 1979;58:379–393. doi: 10.1016/s0076-6879(79)58153-1. [DOI] [PubMed] [Google Scholar]
  16. Kloner R. A., Ganote C. E., Whalen D. A., Jr, Jennings R. B. Effect of a transient period of ischemia on myocardial cells. II. Fine structure during the first few minutes of reflow. Am J Pathol. 1974 Mar;74(3):399–422. [PMC free article] [PubMed] [Google Scholar]
  17. Laiho K. U., Trump B. F. Studies on the pathogenesis of cell injury: effects of inhibitors of metabolism and membrane function on the mitochondria of Ehrlich ascites tumor cells. Lab Invest. 1975 Feb;32(2):163–182. [PubMed] [Google Scholar]
  18. Martin S. J. Apoptosis: suicide, execution or murder? Trends Cell Biol. 1993 May;3(5):141–144. doi: 10.1016/0962-8924(93)90128-n. [DOI] [PubMed] [Google Scholar]
  19. Miyashita T., Reed J. C. bcl-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res. 1992 Oct 1;52(19):5407–5411. [PubMed] [Google Scholar]
  20. Neidle S., Pearl L. H., Skelly J. V. DNA structure and perturbation by drug binding. Biochem J. 1987 Apr 1;243(1):1–13. doi: 10.1042/bj2430001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nicotera P., Thor H., Orrenius S. Cytosolic-free Ca2+ and cell killing in hepatoma 1c1c7 cells exposed to chemical anoxia. FASEB J. 1989 Jan;3(1):59–64. doi: 10.1096/fasebj.3.1.2910738. [DOI] [PubMed] [Google Scholar]
  22. Oppenheim R. W. Cell death during development of the nervous system. Annu Rev Neurosci. 1991;14:453–501. doi: 10.1146/annurev.ne.14.030191.002321. [DOI] [PubMed] [Google Scholar]
  23. Owens G. P., Hahn W. E., Cohen J. J. Identification of mRNAs associated with programmed cell death in immature thymocytes. Mol Cell Biol. 1991 Aug;11(8):4177–4188. doi: 10.1128/mcb.11.8.4177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Prieto A., Kornblith P. L., Pollen D. A. Electrical recordings from meningioma cells during cytolytic action of antibody and complement. Science. 1967 Sep 8;157(3793):1185–1187. doi: 10.1126/science.157.3793.1185. [DOI] [PubMed] [Google Scholar]
  25. Rennie P. S., Bruchovsky N., Buttyan R., Benson M., Cheng H. Gene expression during the early phases of regression of the androgen-dependent Shionogi mouse mammary carcinoma. Cancer Res. 1988 Nov 15;48(22):6309–6312. [PubMed] [Google Scholar]
  26. Rotello R. J., Fernandez P. A., Yuan J. Anti-apogens and anti-engulfens: monoclonal antibodies reveal specific antigens on apoptotic and engulfment cells during chicken embryonic development. Development. 1994 Jun;120(6):1421–1431. doi: 10.1242/dev.120.6.1421. [DOI] [PubMed] [Google Scholar]
  27. Sawczuk I. S., Hoke G., Olsson C. A., Connor J., Buttyan R. Gene expression in response to acute unilateral ureteral obstruction. Kidney Int. 1989 Jun;35(6):1315–1319. doi: 10.1038/ki.1989.128. [DOI] [PubMed] [Google Scholar]
  28. Schwartz L. M., Myer A., Kosz L., Engelstein M., Maier C. Activation of polyubiquitin gene expression during developmentally programmed cell death. Neuron. 1990 Oct;5(4):411–419. doi: 10.1016/0896-6273(90)90080-y. [DOI] [PubMed] [Google Scholar]
  29. Searle J., Kerr J. F., Bishop C. J. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu. 1982;17(Pt 2):229–259. [PubMed] [Google Scholar]
  30. Sentman C. L., Shutter J. R., Hockenbery D., Kanagawa O., Korsmeyer S. J. bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell. 1991 Nov 29;67(5):879–888. doi: 10.1016/0092-8674(91)90361-2. [DOI] [PubMed] [Google Scholar]
  31. Strasser A., Harris A. W., Cory S. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell. 1991 Nov 29;67(5):889–899. doi: 10.1016/0092-8674(91)90362-3. [DOI] [PubMed] [Google Scholar]
  32. Tsujimoto Y. Stress-resistance conferred by high level of bcl-2 alpha protein in human B lymphoblastoid cell. Oncogene. 1989 Nov;4(11):1331–1336. [PubMed] [Google Scholar]
  33. Virtanen I., Ekblom P., Laurila P. Subcellular compartmentalization of saccharide moieties in cultured normal and malignant cells. J Cell Biol. 1980 May;85(2):429–434. doi: 10.1083/jcb.85.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wyllie A. H., Kerr J. F., Currie A. R. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306. doi: 10.1016/s0074-7696(08)62312-8. [DOI] [PubMed] [Google Scholar]
  35. Zhong L. T., Sarafian T., Kane D. J., Charles A. C., Mah S. P., Edwards R. H., Bredesen D. E. bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4533–4537. doi: 10.1073/pnas.90.10.4533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. van de Velde S. Fluorescent microscopy of glycol methacrylate-embedded tissue. Am J Clin Pathol. 1980 Jan;73(1):119–121. doi: 10.1093/ajcp/73.1.119. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES