Skip to main content
PMC home page
Mediators of Inflammation logoLink to Mediators of Inflammation
. 1995 Jan;4(1):5–15. doi: 10.1155/S0962935195000020

Apoptosis and inflammation

C Haanen 1, I Vermes 1,✉
PMCID: PMC2365613  PMID: 18475609

Abstract

During the last few decades it has been recognized that cell death is not the consequence of accidental injury, but is the expression of a cell suicide programme. Kerr et al. (1972) introduced the term apoptosis. This form of cell death is under the influence of hormones, growth factors and cytokines, which depending upon the receptors present on the target cells, may activate a genetically controlled cell elimination process. During apoptosis the cell membrane remains intact and the cell breaks into apoptotic bodies, which are phagocytosed. Apoptosis, in contrast to necrosis, is not harmful to the host and does not induce any inflammatory reaction. The principal event that leads to inflammatory disease is cell damage, induced by chemical/physical injury, anoxia or starvation. Cell damage means leakage of cell contents into the adjacent tissues, resulting in the capillary transmigration of granulocytes to the injured tissue. The accumulation of neutrophils and release of enzymes and oxygen radicals enhances the inflammatory reaction. Until now there has been little research into the factors controlling the accumulation and the tissue load of granulocytes and their histotoxic products in inflammatory processes. Neutrophil apoptosis may represent an important event in the control of intlamtnation. It has been assumed that granulocytes disintegrate to apoptotic bodies before their fragments are removed by local macrophages. Removal of neutrophils from the inflammatory site without release of granule contents is of paramount importance for cessation of inflammation. In conclusion, apoptotic cell death plays an important role in inflammatory processes and in the resolution of inflammatory reactions. The facts known at present should stimulate further research into the role of neutrophil, eosinophil and macrophage apoptosis in inflammatory diseases.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Alison M. R., Sarraf C. E. Apoptosis: a gene-directed programme of cell death. J R Coll Physicians Lond. 1992 Jan;26(1):25–35. [PMC free article] [PubMed] [Google Scholar]
  2. Ameisen J. C., Capron A. Cell dysfunction and depletion in AIDS: the programmed cell death hypothesis. Immunol Today. 1991 Apr;12(4):102–105. doi: 10.1016/0167-5699(91)90092-8. [DOI] [PubMed] [Google Scholar]
  3. Araki S., Shimada Y., Kaji K., Hayashi H. Apoptosis of vascular endothelial cells by fibroblast growth factor deprivation. Biochem Biophys Res Commun. 1990 May 16;168(3):1194–1200. doi: 10.1016/0006-291x(90)91155-l. [DOI] [PubMed] [Google Scholar]
  4. Barres B. A., Hart I. K., Coles H. S., Burne J. F., Voyvodic J. T., Richardson W. D., Raff M. C. Cell death and control of cell survival in the oligodendrocyte lineage. Cell. 1992 Jul 10;70(1):31–46. doi: 10.1016/0092-8674(92)90531-g. [DOI] [PubMed] [Google Scholar]
  5. Begley C. G., Lopez A. F., Nicola N. A., Warren D. J., Vadas M. A., Sanderson C. J., Metcalf D. Purified colony-stimulating factors enhance the survival of human neutrophils and eosinophils in vitro: a rapid and sensitive microassay for colony-stimulating factors. Blood. 1986 Jul;68(1):162–166. [PubMed] [Google Scholar]
  6. Bishop C. J., Moss D. J., Ryan J. M., Burrows S. R. T lymphocytes in infectious mononucleosis. II. Response in vitro to interleukin-2 and establishment of T cell lines. Clin Exp Immunol. 1985 Apr;60(1):70–77. [PMC free article] [PubMed] [Google Scholar]
  7. Bonta I. L., Ben-Efraim S. Involvement of inflammatory mediators in macrophage antitumor activity. J Leukoc Biol. 1993 Dec;54(6):613–626. doi: 10.1002/jlb.54.6.613. [DOI] [PubMed] [Google Scholar]
  8. Cohen J. J. Apoptosis. Immunol Today. 1993 Mar;14(3):126–130. doi: 10.1016/0167-5699(93)90214-6. [DOI] [PubMed] [Google Scholar]
  9. Cohen J. J., Duke R. C., Fadok V. A., Sellins K. S. Apoptosis and programmed cell death in immunity. Annu Rev Immunol. 1992;10:267–293. doi: 10.1146/annurev.iy.10.040192.001411. [DOI] [PubMed] [Google Scholar]
  10. Collins M. K., Marvel J., Malde P., Lopez-Rivas A. Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents. J Exp Med. 1992 Oct 1;176(4):1043–1051. doi: 10.1084/jem.176.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Collins M. K., Marvel J., Malde P., Lopez-Rivas A. Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents. J Exp Med. 1992 Oct 1;176(4):1043–1051. doi: 10.1084/jem.176.4.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dieken E. S., Miesfeld R. L. Transcriptional transactivation functions localized to the glucocorticoid receptor N terminus are necessary for steroid induction of lymphocyte apoptosis. Mol Cell Biol. 1992 Feb;12(2):589–597. doi: 10.1128/mcb.12.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dinarello C. A., Wolff S. M. The role of interleukin-1 in disease. N Engl J Med. 1993 Jan 14;328(2):106–113. doi: 10.1056/NEJM199301143280207. [DOI] [PubMed] [Google Scholar]
  14. Drago J., Murphy M., Carroll S. M., Harvey R. P., Bartlett P. F. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2199–2203. doi: 10.1073/pnas.88.6.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Duke R. C., Cohen J. J. IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells. Lymphokine Res. 1986 Fall;5(4):289–299. [PubMed] [Google Scholar]
  16. Edwards S. N., Buckmaster A. E., Tolkovsky A. M. The death programme in cultured sympathetic neurones can be suppressed at the posttranslational level by nerve growth factor, cyclic AMP, and depolarization. J Neurochem. 1991 Dec;57(6):2140–2143. doi: 10.1111/j.1471-4159.1991.tb06434.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Evan G. I., Littlewood T. D. The role of c-myc in cell growth. Curr Opin Genet Dev. 1993 Feb;3(1):44–49. doi: 10.1016/s0959-437x(05)80339-9. [DOI] [PubMed] [Google Scholar]
  19. Evan G. I., Wyllie A. H., Gilbert C. S., Littlewood T. D., Land H., Brooks M., Waters C. M., Penn L. Z., Hancock D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 1992 Apr 3;69(1):119–128. doi: 10.1016/0092-8674(92)90123-t. [DOI] [PubMed] [Google Scholar]
  20. Fesus L. Apoptosis. Immunol Today. 1992 Aug;13(8):A16–A17. doi: 10.1016/0167-5699(92)90059-G. [DOI] [PubMed] [Google Scholar]
  21. Golstein P., Ojcius D. M., Young J. D. Cell death mechanisms and the immune system. Immunol Rev. 1991 Jun;121:29–65. doi: 10.1111/j.1600-065x.1991.tb00822.x. [DOI] [PubMed] [Google Scholar]
  22. Gottlieb E., Haffner R., von Rüden T., Wagner E. F., Oren M. Down-regulation of wild-type p53 activity interferes with apoptosis of IL-3-dependent hematopoietic cells following IL-3 withdrawal. EMBO J. 1994 Mar 15;13(6):1368–1374. doi: 10.1002/j.1460-2075.1994.tb06390.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gougeon M. L., Olivier R., Garcia S., Guetard D., Dragic T., Dauguet C., Montagnier L. Mise en évidence d'un processus d'engagement vers la mort cellulaire par apoptose dans les lymphocytes de patients infectés par le VIH. C R Acad Sci III. 1991;312(11):529–537. [PubMed] [Google Scholar]
  24. Groux H., Torpier G., Monté D., Mouton Y., Capron A., Ameisen J. C. Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med. 1992 Feb 1;175(2):331–340. doi: 10.1084/jem.175.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Harrington E. A., Bennett M. R., Fanidi A., Evan G. I. c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 1994 Jul 15;13(14):3286–3295. doi: 10.1002/j.1460-2075.1994.tb06630.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Haslett C. Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes. Clin Sci (Lond) 1992 Dec;83(6):639–648. doi: 10.1042/cs0830639. [DOI] [PubMed] [Google Scholar]
  27. Hefti F., Knusel B. Chronic administration of nerve growth factor and other neurotrophic factors to the brain. Neurobiol Aging. 1988 Sep-Dec;9(5-6):689–690. doi: 10.1016/s0197-4580(88)80133-7. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Her E., Frazer J., Austen K. F., Owen W. F., Jr Eosinophil hematopoietins antagonize the programmed cell death of eosinophils. Cytokine and glucocorticoid effects on eosinophils maintained by endothelial cell-conditioned medium. J Clin Invest. 1991 Dec;88(6):1982–1987. doi: 10.1172/JCI115524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hernández-Caselles T., Stutman O. Immune functions of tumor necrosis factor. I. Tumor necrosis factor induces apoptosis of mouse thymocytes and can also stimulate or inhibit IL-6-induced proliferation depending on the concentration of mitogenic costimulation. J Immunol. 1993 Oct 15;151(8):3999–4012. [PubMed] [Google Scholar]
  31. Hogquist K. A., Nett M. A., Unanue E. R., Chaplin D. D. Interleukin 1 is processed and released during apoptosis. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8485–8489. doi: 10.1073/pnas.88.19.8485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hollstein M., Sidransky D., Vogelstein B., Harris C. C. p53 mutations in human cancers. Science. 1991 Jul 5;253(5015):49–53. doi: 10.1126/science.1905840. [DOI] [PubMed] [Google Scholar]
  33. Itoh N., Nagata S. A novel protein domain required for apoptosis. Mutational analysis of human Fas antigen. J Biol Chem. 1993 May 25;268(15):10932–10937. [PubMed] [Google Scholar]
  34. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S., Sameshima M., Hase A., Seto Y., Nagata S. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell. 1991 Jul 26;66(2):233–243. doi: 10.1016/0092-8674(91)90614-5. [DOI] [PubMed] [Google Scholar]
  35. Jacobson M. D., Burne J. F., Raff M. C. Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J. 1994 Apr 15;13(8):1899–1910. doi: 10.1002/j.1460-2075.1994.tb06459.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kabelitz D., Pohl T., Pechhold K. Activation-induced cell death (apoptosis) of mature peripheral T lymphocytes. Immunol Today. 1993 Jul;14(7):338–339. doi: 10.1016/0167-5699(93)90231-9. [DOI] [PubMed] [Google Scholar]
  37. Kamb A., Gruis N. A., Weaver-Feldhaus J., Liu Q., Harshman K., Tavtigian S. V., Stockert E., Day R. S., 3rd, Johnson B. E., Skolnick M. H. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994 Apr 15;264(5157):436–440. doi: 10.1126/science.8153634. [DOI] [PubMed] [Google Scholar]
  38. Kannan Y., Usami K., Okada M., Shimizu S., Matsuda H. Nerve growth factor suppresses apoptosis of murine neutrophils. Biochem Biophys Res Commun. 1992 Jul 31;186(2):1050–1056. doi: 10.1016/0006-291x(92)90853-d. [DOI] [PubMed] [Google Scholar]
  39. Kappler J. W., Roehm N., Marrack P. T cell tolerance by clonal elimination in the thymus. Cell. 1987 Apr 24;49(2):273–280. doi: 10.1016/0092-8674(87)90568-x. [DOI] [PubMed] [Google Scholar]
  40. Kastan M. B., Onyekwere O., Sidransky D., Vogelstein B., Craig R. W. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 1991 Dec 1;51(23 Pt 1):6304–6311. [PubMed] [Google Scholar]
  41. Kerr J. F., Wyllie A. H., Currie A. R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972 Aug;26(4):239–257. doi: 10.1038/bjc.1972.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kessler J. A., Ludlam W. H., Freidin M. M., Hall D. H., Michaelson M. D., Spray D. C., Dougherty M., Batter D. K. Cytokine-induced programmed death of cultured sympathetic neurons. Neuron. 1993 Dec;11(6):1123–1132. doi: 10.1016/0896-6273(93)90225-g. [DOI] [PubMed] [Google Scholar]
  43. Kizaki H., Nakada S., Ohnishi Y., Azuma Y., Mizuno Y., Tadakuma T. Tumour necrosis factor-alpha enhances cAMP-induced programmed cell death in mouse thymocytes. Cytokine. 1993 Jul;5(4):342–347. doi: 10.1016/1043-4666(93)90066-e. [DOI] [PubMed] [Google Scholar]
  44. Kobayashi S., Teramura M., Sugawara I., Oshimi K., Mizoguchi H. Interleukin-11 acts as an autocrine growth factor for human megakaryoblastic cell lines. Blood. 1993 Feb 15;81(4):889–893. [PubMed] [Google Scholar]
  45. Koury M. J., Bondurant M. C. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science. 1990 Apr 20;248(4953):378–381. doi: 10.1126/science.2326648. [DOI] [PubMed] [Google Scholar]
  46. Koury M. J., Bondurant M. C. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science. 1990 Apr 20;248(4953):378–381. doi: 10.1126/science.2326648. [DOI] [PubMed] [Google Scholar]
  47. Kroemer G., Martínez C. Mechanisms of self tolerance. Immunol Today. 1992 Oct;13(10):401–404. doi: 10.1016/0167-5699(92)90090-t. [DOI] [PubMed] [Google Scholar]
  48. Kyprianou N., English H. F., Davidson N. E., Isaacs J. T. Programmed cell death during regression of the MCF-7 human breast cancer following estrogen ablation. Cancer Res. 1991 Jan 1;51(1):162–166. [PubMed] [Google Scholar]
  49. Lane D. P. Cancer. p53, guardian of the genome. Nature. 1992 Jul 2;358(6381):15–16. doi: 10.1038/358015a0. [DOI] [PubMed] [Google Scholar]
  50. Laurent-Crawford A. G., Krust B., Muller S., Rivière Y., Rey-Cuillé M. A., Béchet J. M., Montagnier L., Hovanessian A. G. The cytopathic effect of HIV is associated with apoptosis. Virology. 1991 Dec;185(2):829–839. doi: 10.1016/0042-6822(91)90554-o. [DOI] [PubMed] [Google Scholar]
  51. Lenardo M. J. Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature. 1991 Oct 31;353(6347):858–861. doi: 10.1038/353858a0. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Liu Y. J., Joshua D. E., Williams G. T., Smith C. A., Gordon J., MacLennan I. C. Mechanism of antigen-driven selection in germinal centres. Nature. 1989 Dec 21;342(6252):929–931. doi: 10.1038/342929a0. [DOI] [PubMed] [Google Scholar]
  54. Liu Y. J., Mason D. Y., Johnson G. D., Abbot S., Gregory C. D., Hardie D. L., Gordon J., MacLennan I. C. Germinal center cells express bcl-2 protein after activation by signals which prevent their entry into apoptosis. Eur J Immunol. 1991 Aug;21(8):1905–1910. doi: 10.1002/eji.1830210819. [DOI] [PubMed] [Google Scholar]
  55. Lotem J., Sachs L. Hematopoietic cytokines inhibit apoptosis induced by transforming growth factor beta 1 and cancer chemotherapy compounds in myeloid leukemic cells. Blood. 1992 Oct 1;80(7):1750–1757. [PubMed] [Google Scholar]
  56. Louis J. C., Magal E., Takayama S., Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science. 1993 Jan 29;259(5095):689–692. doi: 10.1126/science.8430320. [DOI] [PubMed] [Google Scholar]
  57. MacDonald H. R., Lees R. K. Programmed death of autoreactive thymocytes. Nature. 1990 Feb 15;343(6259):642–644. doi: 10.1038/343642a0. [DOI] [PubMed] [Google Scholar]
  58. Maltzman W., Czyzyk L. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol Cell Biol. 1984 Sep;4(9):1689–1694. doi: 10.1128/mcb.4.9.1689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Mangan D. F., Mergenhagen S. E., Wahl S. M. Apoptosis in human monocytes: possible role in chronic inflammatory diseases. J Periodontol. 1993 May;64(5 Suppl):461–466. [PubMed] [Google Scholar]
  60. Mangan D. F., Robertson B., Wahl S. M. IL-4 enhances programmed cell death (apoptosis) in stimulated human monocytes. J Immunol. 1992 Mar 15;148(6):1812–1816. [PubMed] [Google Scholar]
  61. Mangan D. F., Welch G. R., Wahl S. M. Lipopolysaccharide, tumor necrosis factor-alpha, and IL-1 beta prevent programmed cell death (apoptosis) in human peripheral blood monocytes. J Immunol. 1991 Mar 1;146(5):1541–1546. [PubMed] [Google Scholar]
  62. Mapara M. Y., Bargou R., Zugck C., Döhner H., Ustaoglu F., Jonker R. R., Krammer P. H., Dörken B. APO-1 mediated apoptosis or proliferation in human chronic B lymphocytic leukemia: correlation with bcl-2 oncogene expression. Eur J Immunol. 1993 Mar;23(3):702–708. doi: 10.1002/eji.1830230320. [DOI] [PubMed] [Google Scholar]
  63. Mekori Y. A., Oh C. K., Metcalfe D. D. IL-3-dependent murine mast cells undergo apoptosis on removal of IL-3. Prevention of apoptosis by c-kit ligand. J Immunol. 1993 Oct 1;151(7):3775–3784. [PubMed] [Google Scholar]
  64. Metcalf D., Merchav S. Effects of GM-CSF deprivation on precursors of granulocytes and macrophages. J Cell Physiol. 1982 Sep;112(3):411–418. doi: 10.1002/jcp.1041120315. [DOI] [PubMed] [Google Scholar]
  65. 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]
  66. Migliorati G., Nicoletti I., Pagliacci M. C., D'Adamio L., Riccardi C. Interleukin-2 induces apoptosis in mouse thymocytes. Cell Immunol. 1993 Jan;146(1):52–61. doi: 10.1006/cimm.1993.1005. [DOI] [PubMed] [Google Scholar]
  67. Miura M., Zhu H., Rotello R., Hartwieg E. A., Yuan J. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 1993 Nov 19;75(4):653–660. doi: 10.1016/0092-8674(93)90486-a. [DOI] [PubMed] [Google Scholar]
  68. Newell M. K., Haughn L. J., Maroun C. R., Julius M. H. Death of mature T cells by separate ligation of CD4 and the T-cell receptor for antigen. Nature. 1990 Sep 20;347(6290):286–289. doi: 10.1038/347286a0. [DOI] [PubMed] [Google Scholar]
  69. Nuñez G., London L., Hockenbery D., Alexander M., McKearn J. P., Korsmeyer S. J. Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. J Immunol. 1990 May 1;144(9):3602–3610. [PubMed] [Google Scholar]
  70. Oehm A., Behrmann I., Falk W., Pawlita M., Maier G., Klas C., Li-Weber M., Richards S., Dhein J., Trauth B. C. Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. Sequence identity with the Fas antigen. J Biol Chem. 1992 May 25;267(15):10709–10715. [PubMed] [Google Scholar]
  71. Oliner J. D., Kinzler K. W., Meltzer P. S., George D. L., Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature. 1992 Jul 2;358(6381):80–83. doi: 10.1038/358080a0. [DOI] [PubMed] [Google Scholar]
  72. Ormerod M. G., Collins M. K., Rodriguez-Tarduchy G., Robertson D. Apoptosis in interleukin-3-dependent haemopoietic cells. Quantification by two flow cytometric methods. J Immunol Methods. 1992 Aug 30;153(1-2):57–65. doi: 10.1016/0022-1759(92)90305-d. [DOI] [PubMed] [Google Scholar]
  73. Panayiotidis P., Ganeshaguru K., Jabbar S. A., Hoffbrand A. V. Interleukin-4 inhibits apoptotic cell death and loss of the bcl-2 protein in B-chronic lymphocytic leukaemia cells in vitro. Br J Haematol. 1993 Nov;85(3):439–445. doi: 10.1111/j.1365-2141.1993.tb03330.x. [DOI] [PubMed] [Google Scholar]
  74. Perry M. E., Levine A. J. Tumor-suppressor p53 and the cell cycle. Curr Opin Genet Dev. 1993 Feb;3(1):50–54. doi: 10.1016/s0959-437x(05)80340-5. [DOI] [PubMed] [Google Scholar]
  75. Raff M. C. Social controls on cell survival and cell death. Nature. 1992 Apr 2;356(6368):397–400. doi: 10.1038/356397a0. [DOI] [PubMed] [Google Scholar]
  76. 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]
  77. Rodriguez-Tarduchy G., Collins M., López-Rivas A. Regulation of apoptosis in interleukin-3-dependent hemopoietic cells by interleukin-3 and calcium ionophores. EMBO J. 1990 Sep;9(9):2997–3002. doi: 10.1002/j.1460-2075.1990.tb07492.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Rotello R. J., Lieberman R. C., Lepoff R. B., Gerschenson L. E. Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU 486. Am J Pathol. 1992 Feb;140(2):449–456. [PMC free article] [PubMed] [Google Scholar]
  79. Rothenberg M. E., Owen W. F., Jr, Silberstein D. S., Woods J., Soberman R. J., Austen K. F., Stevens R. L. Human eosinophils have prolonged survival, enhanced functional properties, and become hypodense when exposed to human interleukin 3. J Clin Invest. 1988 Jun;81(6):1986–1992. doi: 10.1172/JCI113547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Rouvier E., Luciani M. F., Golstein P. Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity. J Exp Med. 1993 Jan 1;177(1):195–200. doi: 10.1084/jem.177.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Sandow B. A., West N. B., Norman R. L., Brenner R. M. Hormonal control of apoptosis in hamster uterine luminal epithelium. Am J Anat. 1979 Sep;156(1):15–35. doi: 10.1002/aja.1001560103. [DOI] [PubMed] [Google Scholar]
  82. Saukkonen K., Sande S., Cioffe C., Wolpe S., Sherry B., Cerami A., Tuomanen E. The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J Exp Med. 1990 Feb 1;171(2):439–448. doi: 10.1084/jem.171.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Saunders J. W., Jr Death in embryonic systems. Science. 1966 Nov 4;154(3749):604–612. doi: 10.1126/science.154.3749.604. [DOI] [PubMed] [Google Scholar]
  84. Savill J. S., Wyllie A. H., Henson J. E., Walport M. J., Henson P. M., Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest. 1989 Mar;83(3):865–875. doi: 10.1172/JCI113970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Schwartzman R. A., Cidlowski J. A. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev. 1993 Apr;14(2):133–151. doi: 10.1210/edrv-14-2-133. [DOI] [PubMed] [Google Scholar]
  86. Shaw P., Bovey R., Tardy S., Sahli R., Sordat B., Costa J. Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4495–4499. doi: 10.1073/pnas.89.10.4495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Smith C. A., Williams G. T., Kingston R., Jenkinson E. J., Owen J. J. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature. 1989 Jan 12;337(6203):181–184. doi: 10.1038/337181a0. [DOI] [PubMed] [Google Scholar]
  88. Spivak J. L., Pham T., Isaacs M., Hankins W. D. Erythropoietin is both a mitogen and a survival factor. Blood. 1991 Mar 15;77(6):1228–1233. [PubMed] [Google Scholar]
  89. Stern M., Meagher L., Savill J., Haslett C. Apoptosis in human eosinophils. Programmed cell death in the eosinophil leads to phagocytosis by macrophages and is modulated by IL-5. J Immunol. 1992 Jun 1;148(11):3543–3549. [PubMed] [Google Scholar]
  90. Stürzbecher H. W., Maimets T., Chumakov P., Brain R., Addison C., Simanis V., Rudge K., Philp R., Grimaldi M., Court W. p53 interacts with p34cdc2 in mammalian cells: implications for cell cycle control and oncogenesis. Oncogene. 1990 Jun;5(6):795–781. [PubMed] [Google Scholar]
  91. Svrzic D., Schubert D. Insulin-like growth factor 1 supports embryonic nerve cell survival. Biochem Biophys Res Commun. 1990 Oct 15;172(1):54–60. doi: 10.1016/s0006-291x(05)80172-x. [DOI] [PubMed] [Google Scholar]
  92. Südhof T. C., De Camilli P., Niemann H., Jahn R. Membrane fusion machinery: insights from synaptic proteins. Cell. 1993 Oct 8;75(1):1–4. [PubMed] [Google Scholar]
  93. Takeda Y., Watanabe H., Yonehara S., Yamashita T., Saito S., Sendo F. Rapid acceleration of neutrophil apoptosis by tumor necrosis factor-alpha. Int Immunol. 1993 Jun;5(6):691–694. doi: 10.1093/intimm/5.6.691. [DOI] [PubMed] [Google Scholar]
  94. Takeda Y., Watanabe H., Yonehara S., Yamashita T., Saito S., Sendo F. Rapid acceleration of neutrophil apoptosis by tumor necrosis factor-alpha. Int Immunol. 1993 Jun;5(6):691–694. doi: 10.1093/intimm/5.6.691. [DOI] [PubMed] [Google Scholar]
  95. Terai C., Kornbluth R. S., Pauza C. D., Richman D. D., Carson D. A. Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J Clin Invest. 1991 May;87(5):1710–1715. doi: 10.1172/JCI115188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Tushinski R. J., Oliver I. T., Guilbert L. J., Tynan P. W., Warner J. R., Stanley E. R. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell. 1982 Jan;28(1):71–81. doi: 10.1016/0092-8674(82)90376-2. [DOI] [PubMed] [Google Scholar]
  97. Umansky S. R. The genetic program of cell death. Hypothesis and some applications: transformation, carcinogenesis, ageing. J Theor Biol. 1982 Aug 21;97(4):591–602. doi: 10.1016/0022-5193(82)90360-5. [DOI] [PubMed] [Google Scholar]
  98. Vartio T., Seppä H., Vaheri A. Susceptibility of soluble and matrix fibronectins to degradation by tissue proteinases, mast cell chymase and cathepsin G. J Biol Chem. 1981 Jan 10;256(1):471–477. [PubMed] [Google Scholar]
  99. Vaux D. L., Cory S., Adams J. M. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature. 1988 Sep 29;335(6189):440–442. doi: 10.1038/335440a0. [DOI] [PubMed] [Google Scholar]
  100. Vermes I., Haanen C. Apoptosis and programmed cell death in health and disease. Adv Clin Chem. 1994;31:177–246. doi: 10.1016/s0065-2423(08)60336-4. [DOI] [PubMed] [Google Scholar]
  101. Watanabe-Fukunaga R., Brannan C. I., Copeland N. G., Jenkins N. A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 1992 Mar 26;356(6367):314–317. doi: 10.1038/356314a0. [DOI] [PubMed] [Google Scholar]
  102. Weiss S. J. Tissue destruction by neutrophils. N Engl J Med. 1989 Feb 9;320(6):365–376. doi: 10.1056/NEJM198902093200606. [DOI] [PubMed] [Google Scholar]
  103. Wielckens K., Delfs T. Glucocorticoid-induced cell death and poly[adenosine diphosphate(ADP)-ribosyl]ation: increased toxicity of dexamethasone on mouse S49.1 lymphoma cells with the poly(ADP-ribosyl)ation inhibitor benzamide. Endocrinology. 1986 Nov;119(5):2383–2392. doi: 10.1210/endo-119-5-2383. [DOI] [PubMed] [Google Scholar]
  104. Williams G. T., Smith C. A., Spooncer E., Dexter T. M., Taylor D. R. Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature. 1990 Jan 4;343(6253):76–79. doi: 10.1038/343076a0. [DOI] [PubMed] [Google Scholar]
  105. Wright S. C., Kumar P., Tam A. W., Shen N., Varma M., Larrick J. W. Apoptosis and DNA fragmentation precede TNF-induced cytolysis in U937 cells. J Cell Biochem. 1992 Apr;48(4):344–355. doi: 10.1002/jcb.240480403. [DOI] [PubMed] [Google Scholar]
  106. Wyllie A. H. Apoptosis. Death gets a brake. Nature. 1994 May 26;369(6478):272–273. doi: 10.1038/369272a0. [DOI] [PubMed] [Google Scholar]
  107. 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]
  108. Yamamoto C., Yoshida S., Taniguchi H., Qin M. H., Miyamoto H., Mizuguchi Y. Lipopolysaccharide and granulocyte colony-stimulating factor delay neutrophil apoptosis and ingestion by guinea pig macrophages. Infect Immun. 1993 May;61(5):1972–1979. doi: 10.1128/iai.61.5.1972-1979.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Yonish-Rouach E., Resnitzky D., Lotem J., Sachs L., Kimchi A., Oren M. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature. 1991 Jul 25;352(6333):345–347. doi: 10.1038/352345a0. [DOI] [PubMed] [Google Scholar]
  110. Yu H., Bauer B., Lipke G. K., Phillips R. L., Van Zant G. Apoptosis and hematopoiesis in murine fetal liver. Blood. 1993 Jan 15;81(2):373–384. [PubMed] [Google Scholar]
  111. Zubiaga A. M., Munoz E., Huber B. T. IL-4 and IL-2 selectively rescue Th cell subsets from glucocorticoid-induced apoptosis. J Immunol. 1992 Jul 1;149(1):107–112. [PubMed] [Google Scholar]
  112. von Boehmer H. Developmental biology of T cells in T cell-receptor transgenic mice. Annu Rev Immunol. 1990;8:531–556. doi: 10.1146/annurev.iy.08.040190.002531. [DOI] [PubMed] [Google Scholar]
  113. von Boehmer H. Thymic selection: a matter of life and death. Immunol Today. 1992 Nov;13(11):454–458. doi: 10.1016/0167-5699(92)90075-I. [DOI] [PubMed] [Google Scholar]

Articles from Mediators of Inflammation are provided here courtesy of Wiley

RESOURCES