Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Apoptosis and Its Role in Human Disease

Bio/Technology volume 12, pages 487–493 (1994)Cite this article

Abstract

In a landmark paper published over two decades ago, Kerr et al. proposed the term apoptosis “for a hitherto little recognized mechanism of controlled cell deletion, which appears to play a complementary but opposite role to mitosis in the regulation of animal cell populations”1. In the ensuing years, this natural cell death process was studied at the basic science level, primarily with a view to understanding its roles in cancer and in the development and maintenance of the immune system. More recently, however, evidence has suggested a role for the failure of normal apoptosis control in many of the major diseases of the industrialized world. Though complex, apoptosis appears amenable to therapeutic intervention. The range of modern pharmaceutical strategies available to treat such disregulated gene-directed processes offers promise for advances in the control of cancer, immune system and neurodegenerative disorders, heart disease, and perhaps even the aging process itself.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Kerr, J.F.R., Wyllie, A.H. and Currie, A.R. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239–257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kerr, J.F.R. 1971. Shrinkage necrosis: a distinct mode of cellular death. J. Pathol. 105: 13–20.

    CAS  PubMed  Google Scholar 

  3. Kerr, J.F.R. 1965. A histochemical study of hypertrophy and ischaemic injury of rat liver with special reference to changes in lysosomes. J. Pathol. Bacteriol. 90: 419–455.

    CAS  PubMed  Google Scholar 

  4. Kerr, J.F.R. and Harmon, B.V. 1991. Definition and incidence of apoptosis: an historical perspective, p. 5–29. In: Apoptosis: The Molecular Basis of cell Death. L. D. Tomei and F. O. Cope (Eds.). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  5. Raff, M.C. 1993. Social controls on cell survival and cell death. Nature 356: 397–400.

    Google Scholar 

  6. Martin, S.J., Green, D.R. and Cotter, T.G. 1994. Dicing with death: dissecting the components of the apoptosis machinery. Trends Biochem. Sci. 19: 26–30.

    CAS  PubMed  Google Scholar 

  7. Furuya, Y., Berges, R., Lundmo, P. and Isaacs, J.T. 1994. Cell proliferation, p53 gene expression and intracellular calcium in programmed death: prostate model, p. 231–252. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  8. Buttke, T.M. and Sandstrom, P.A. 1994. Oxidative stress as a mediator of apoptosis. Immunology Today 15: 7–10.

    CAS  PubMed  Google Scholar 

  9. Sugarman, B.J., Aggarwal, B.B., Hass, P.E., Figari, I.S. Jr and Shepard, H.M. 1985. Recombinant human tumor necrosis factor-alpha: effects on proliferation of normal and transformed cells in vitro. Science 230: 943–945.

    CAS  PubMed  Google Scholar 

  10. Alderson, M.R., Armitage, R.J., Maraskovsky, E., Tough, T.W., Roux, E., Schooley, K., Ramsdell, F. and Lynch, D.H. 1993. Fas transduces activation signals in normal human T lymphocytes. J. Exp. Med. 178: 2231–2235.

    CAS  PubMed  Google Scholar 

  11. Kane, D.J., Sarafian, T.A., Anton, R., Hahn, H., Gralla, E.B., Valentine, J.S., Ord, T. and Bredesen, D.E. 1993. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262: 1274–1277.

    CAS  PubMed  Google Scholar 

  12. Hockenbery, D.M., Oltvai, Z.N., Yin, X.-M., Milliman, C.L. and Kors-meyer, S.J. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241–251.

    CAS  PubMed  Google Scholar 

  13. Kanter, P., Leister, K.J., Tomei, L.D., Wenner, P.A. and Wenner, C.E. 1984. Epidermal growth factor and tumor promoters prevent DNA fragmentation by different mechanisms. Biochem. Biophys. Res. Commun. 118: 392–399.

    CAS  PubMed  Google Scholar 

  14. Peppelenbosch, M.P., Tertoolen, L.G.J., Hage, W.J. and de Laat, S.W. 1993. Epidermal growth factor-induced actin remodeling is regulated by 5-lipoxy-genase and cyclooxygenase products. Cell 74: 565–575.

    CAS  PubMed  Google Scholar 

  15. Kanter, P.M. and Schwartz, H.S. 1980. Post-repair DNA damage in X-irradiated cultured human tumour cells. Int. J. Radial. Biol. 38: 483–493.

    CAS  Google Scholar 

  16. Tomei, L.D., Shapiro, J.P. and Cope, F.O. 1993. Apoptosis in C3H/10T1/2 mouse embryonic cells: evidence for internucleosomal DNA modification in the absence of double-strand cleavage. Proc. Natl. Acad. Sci. USA 90: 853–857.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Leister, K.J., Wenner, C.E. and Tomei, L.D. 1985. Correlation of ouabain-sensitive ion movements with cell cycle activation. Proc. Natl. Acad. Sci. USA 82: 1599–1603.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Morisaki, N., Tomei, L.D., Milo, G.E. and Cornwell, D.G. 1985. Role of prostanoids and lipid peroxides as mediators of the 12-O-tetradecanoylphorbol-13-acetate effect on cell growth. Lipids 20: 602–610.

    CAS  PubMed  Google Scholar 

  19. Witz, G. 1991. Active oxygen species as factors in multistage carcinogenesis. Proc. Soc. Exp. Biol. Med. 198: 675–682.

    CAS  PubMed  Google Scholar 

  20. Tomei, L.D. and Cope, F.O. 1991. p. 1–3. In: Apoptosis: The Molecular Basis of cell Death. L. D. Tomei and F. O. Cope (Eds.). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  21. Tomei, L.D., Cheney, J.C. and Wenner, C.E. 1981. The effect of phorbol esters on the proliferation of C3H-10T1/2 mouse fibroblasts: consideration of both stimulatory and inhibitory effects. J. Cell. Physiol. 107: 385–389.

    CAS  PubMed  Google Scholar 

  22. Hanada, M., Krajewski, S., Tanaka, S., Cazals-Hatem, D., Spengler, B.A., Ross, R.A., Biedler, J.L. and Reed, J.C. 1993. Regulation of Bcl-2 oncopro-tein levels with differentiation of human neuroblastoma cells. Cancer Res. 53: 4978–4986.

    CAS  PubMed  Google Scholar 

  23. Tomei, L.D., Cope, F.O. and Barr, P.J. 1994. Apoptosis: aging and phenorypic fidelity p. 377–396. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  24. Williams, G.T. and Smith, C.A. 1993. Molecular regulation of apoptosis: genetic controls on cell death. Cell 74: 777–779.

    CAS  PubMed  Google Scholar 

  25. Tenniswood, M., Taillefer, D., Lakins, J., Guenette, R., Mooibroek, M., Daehlin, L. and Welsh, J. 1994. Control of gene expression during apoptosis in hormone dependent tissues p. 283–311. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  26. Carson, D.A. and Ribeire, J.M. 1993. Apoptosis and disease. Lancet 341: 1251–1254.

    CAS  PubMed  Google Scholar 

  27. El-Deiry, W.S., Tokino, T., Velculescu, V.E., Levy, D.B., Parsons, R., Trent, J.M., Lin, D., Mercer, W.E., Kinzler, K.W. and Vogelstein, B. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817–825.

    CAS  PubMed  Google Scholar 

  28. Harper, J., Adami, G.R., Wei, N., Keyomarsi, K. and Elledge, S.J. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805–816.

    CAS  PubMed  Google Scholar 

  29. Lane, D.P. 1992. p53, guardian of the genome. Science 358: 15–16.

    CAS  Google Scholar 

  30. Tsujimoto, Y., Finger, L.R., Tunis, J., Nowell, P.C. and Croce, C.M. 1984. Cloning of the chromosomic break point of neoplastic B cells with the t(14;18) chromosome translocation. Science 226: 1097–1099.

    CAS  PubMed  Google Scholar 

  31. Hengartner, M.O. and Horvitz, H.R. 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76: 665–676.

    CAS  PubMed  Google Scholar 

  32. Reed, J.C., Stein, C., Subasinghe, C., Haldar, S., Croce, C.M., Yum, S. and Cohen, J. 1990. Anti-sense-mediated inhibition of BCL2 proto-oncogene expression and leukemic cell growth: comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res. 50: 6565–6570.

    CAS  PubMed  Google Scholar 

  33. Karp, J.E. and Broder, S. 1994. New directions in molecular medicine. Cancer Res. 54: 653–665.

    CAS  PubMed  Google Scholar 

  34. Pezzella, F., Turley, H., Kuzu, I., Tungekar, M.F., Dunnill, M.S., Pierce, C.B., Harries, A., Gatter, K.C. and Mason, D.Y. 1993. bcl-2 protein in non-small-cell lung carcinoma. New Eng. J. Med. 329: 690–694.

    CAS  PubMed  Google Scholar 

  35. McArdle, A.H., Reid, E.C., Laplante, M.P. and Freeman, C.R. 1986. Prophylaxis against radiation injury. Arch. Surg. 121: 879–885.

    CAS  PubMed  Google Scholar 

  36. Tomei, L.D. and Cope, F.O. 1991. Nutrient inhibition of radiation-induced apoptosis in intestinal epithelial cells: possible mechanisms of action p. 105–112. In: The Role of Nutrients in Cancer Treatment. Report of the Ninth Ross Conference on Medical Research, Ross Laboratories, Columbus, Ohio.

    Google Scholar 

  37. Adachi, M., Tefferi, A., Greipp, P.R., Kipps, T.J. and Tsujimoto, Y. 1990. Preferential linkage of bcl-2 to immunoglobulin light-chain gene in chronic lymphocytic leukemia. J. Exp. Med. 171: 559–564.

    CAS  PubMed  Google Scholar 

  38. Bursch, W., Lauer, B., Timmerman-Trosiener, I., Barthel, G., Schuppler, J. and Schulte-Hermann, R. 1984. Controlled death (apoptosis) of normal and putative preneoplastic cells in rat liver following withdrawal of tumor promoters. Carcin-ogenesis 5: 453–460.

    CAS  Google Scholar 

  39. Miyashita, T. and Reed, J.C. 1993. Bcl-2 oncoprotein blocks chemotherapy-induced apoptosis in a human leukemia cell line. Blood 81: 151–157.

    CAS  PubMed  Google Scholar 

  40. Linnick, M.D., Zobrist, H.R. and Hatfield, M.D. 1993. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24: 2002–2009.

    Google Scholar 

  41. Mattson, M.P., Cheng, B., Davis, D., Bryant, K., Leiberburg, I. and Rydel, R.E. 1992. Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neuroscience 12: 376–389.

    CAS  Google Scholar 

  42. Schehr, R.S. 1994. Therapeutic approaches to Alzheimer's disease. Bio/Technology 12: 140–144.

    CAS  Google Scholar 

  43. Olson, L. 1993. NGF and the treatment of Alzheimer's disease. Exp. Neur. 124: 5–15.

    CAS  Google Scholar 

  44. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O. and Tagliavini, F. 1993. Neurotoxicity of a prion protein fragment. Nature 362: 543–546.

    CAS  PubMed  Google Scholar 

  45. Meyn, M.S. 1994. Ataxia-telangiectasia, cell cycle checkpoints and programmed cell death in the cellular response to DNA damage. Cancer Res., submitted for publication.

  46. Tomei, L.D., Umansky, S.R., Bathurst, I.C. and Barr, P.J. 1993. Therapeutic intervention and apoptosis. p. 16–17. In: Apoptosis in AIDS and Cancer, Montagnier, L. and Tomei, L. D. (Eds.).

    Google Scholar 

  47. Gianni, L., Corden, B.J. and Myers, C.E. 1983. The biochemical basis of anthracyclin toxicity and antitumor activity. Rev. Biochem. Toxicol. 5: 1–82.

    CAS  Google Scholar 

  48. Ameison, J.C. and Capron, A. 1991. Cell dysfunction and depletion in AIDS: the programmed cell death hypothesis. Immunol. Today 12: 102–105.

    Google Scholar 

  49. Gougeon, M.-L. and Montagnier, L. 1993. Apoptosis in AIDS. Science 260: 1269–1270.

    CAS  PubMed  Google Scholar 

  50. Gougeon, M.-L. and Montagnier, L. 1994. Apoptosis in peripheral T lymphocytes during HIV infection: influence of superantigens and correlation with AIDS pathogenesis. p. 5–18. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  51. Meyaard, L., Otto, S.A., Jonker, R.R., Mijnster, M.J., Keet, R. and Miedema, F. 1992. Programmed death of T Cells in HIV-1 infection. Science 257: 217–219.

    CAS  PubMed  Google Scholar 

  52. Krowka, J.F., Cuevas, B., Ascher, M.S. and Sheppard, H.W. 1994. Peripheral blood lymphocytes of HIV-infected individuals exhibit elevated levels of the Fas antigen and rapid induction of apoptosis, submitted for publication.

  53. Garchon, H.J. 1992. Non-MHC-linked genes in autoimmune diseases. Curr. Opin. Immunol. 4: 716–722.

    CAS  PubMed  Google Scholar 

  54. Cheng, J., Zhou, T., Liu, C., Shapiro, J.P., Brauer, M.J., Kiefer, M.C., Barr, P.J. and Mountz, J.D. 1994. A soluble form of the Fas molecule protects cells from Fas-mediated apoptosis. Science 263: 1759–1762.

    CAS  PubMed  Google Scholar 

  55. Mountz, J.D. and Gause, W.C. 1993. Murine models of autoimmune disease and Sjogren's syndrome. Curr. Opinion Rheumatol. 5: 557–569.

    CAS  Google Scholar 

  56. Zychlinski, A., Prevost, M.C. and Sansonetti, P.J. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167–169.

    Google Scholar 

  57. Lee, F.D. 1993. Importance of apoptosis in the histopathology of drug related lesions in the large intestine. J. Clin. Pathology 46: 118–122.

    CAS  Google Scholar 

  58. Chlebowski, R.T., Beall, G., Grosvenor, M., Lillington, L., Weintraub, N., Ambler, C., Richards, E.W., Abbruzzese, B.C., McCamish, M.A. and Cope, F.O. 1993. Long-term effects of early nutritional support with new enterotropic peptide-based formula vs. standard enteral formula in HIV-infected patients: randomized prospective trial. Nutrition 9: 507–512.

    CAS  PubMed  Google Scholar 

  59. Veis, D.J., Sorenson, C.M., Shutter, J.R. and Korsmeyer, S.J. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75: 229–240.

    CAS  PubMed  Google Scholar 

  60. Koury, M.J. and Bondurant, M.C. 1990. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor Cella. Science 248: 378–381.

    CAS  PubMed  Google Scholar 

  61. Golstein, P., Ojcius, D.M. and Young, J.D. 1992. Cell death mechanisms and the immune system. Immunol. Rev. 121: 29–65.

    Google Scholar 

  62. Cohen, J.J., Duke, R.C., Fadok, V.A. and Sellins, K. 1992. Apoptosis and programmed cell death in immunity. Ann. Rev. Immunol. 10: 267–293.

    CAS  Google Scholar 

  63. Banda, N.K., Bernier, J., Kurahara, D.K., Kurrie, R., Haigwood, N., Sekaly, R.P. and Finkel, T.H. 1992. Cross-linking by HIV gp120 primes T cells for activation-induced apoptosis. J. Exp. Med. 176: 1099–1106.

    CAS  PubMed  Google Scholar 

  64. Cohen, P.L. and Eisenberg, R.A. 1992. The Ipr and gld genes in systemic autoimmunity: life and death in the Fas lane. Immunol. Today 13: 427–428.

    CAS  PubMed  Google Scholar 

  65. White, E. and Gooding, L.R. 1994. Regulation of apoptosis by human adenoviruses. p. 111–142. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  66. Heintz, N. 1993. Cell death and the cell cycle: a relationship between transformation and neurodegeneration? Trends Biochem. Sci. 18: 157–159.

    CAS  PubMed  Google Scholar 

  67. Hickman, J.A. 1992. Apoptosis induced by anticancer drugs. Cancer Metastasis Rev. 11: 121–139.

    CAS  PubMed  Google Scholar 

  68. Medawar, P.B. 1946. Old age and natural death. Modern Quarterly 2: 30–49. Reprinted in The Uniqueness of the Individual (ed. P. B. Medawar), pp. 1–27. Methuen and Co., London, 1957.

    Google Scholar 

  69. Medawar, P.B. 1952. An unsolved problem in biology. Lewis, London. Reprinted in The Uniqueness of the Individual (ed. P. B. Medawar), pp. 28–54. Methuen and Co., London, 1957.

    Google Scholar 

  70. Rose, M.R. 1991. Evolutionary Biology of Aging. Oxford University Press, New York, New York.

  71. Franceschi, C., Monti, D., Rosario Scarfi, M., Zeni, P., Temperani, P., Emilia, G., Sansoni, P., Lioi, M. B., Troiano, L., Agnesini, C., Salvioli, S. and Cossarizza, A. 1992. Genomic instability and aging: studies in centenarians (successful aging) and in patients with Down's syndrome (accelerated aging). Ann. New York Acad. Sci. 663: 4–16.

    CAS  Google Scholar 

  72. Monti, D., Troiano, L., Grassilli, E., Agnesini, C., Tropea, F., Barbieri, D., Capri, M., Cristafalo, E.A., Salvioli, S., Ronhetti, I., Bellomo, G., Cossarizza, A. and Franceschi, C. 1992. Cell proliferation and cell death in immuno-senescence. Ann. New York Acad. Sci. 663: 250–261.

    CAS  Google Scholar 

  73. Michie, C.A., McLean, A., Alcock, C. and Beverley, P. C.L. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature 360: 264–265.

    CAS  PubMed  Google Scholar 

  74. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 25: 585–621.

    Google Scholar 

  75. Itoh, N., Yonehara, S., Ishii, A., Yonehara, M., Mizushima, S.-I., Sameshimi, M., Hase, A., Seto, Y. and Nagata, S. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66: 233–243.

    CAS  PubMed  Google Scholar 

  76. Oehm, A., Behrmann, I., Falk, W., Pawlita, M., Maier, G., Klas, C., Li-Weber, M., Richards, S., Dhein, J., Trauth, B.C., Ponsting, H. and Krammer, P. 1992. Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. J. Biol. Chem. 267: 10709–10715.

    CAS  PubMed  Google Scholar 

  77. Vincent, J.L., Bakker, J., Marecaux, G., Schandene, L., Kahn, R.J. and Dupont, E. 1992. Administration of anti-TNF antibody improves left ventricular function in septic shock patients. Results of a pilot study. Chest 101: 810–815.

    CAS  PubMed  Google Scholar 

  78. Lindsay, R.M., Altar, C.A., Cedarbaum, J.M., Hyman, C. and Wiegand, S.J. 1993. The therapeutic potential of neurotrophic factors in the treatment of Parkinson's disease. Exp. Neur. 124: 103–118.

    CAS  Google Scholar 

  79. Ogasawara, J., Watanabe-Fukunaga, R., Adachi, M., Matsuzawa, A., Kasugai, T., Kitamura, Y., Itoh, N., Suda, T. and Nagata, S. 1993. Lethal effect of the anti-Fas antibody in mice. Nature 364: 806–809.

    CAS  PubMed  Google Scholar 

  80. Suda, T., Takahashi, T., Golstein, P. and Nagata, S. 1993. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 75: 1169–1178.

    CAS  PubMed  Google Scholar 

  81. Meredith, J.E., Fazeli, B. and Schwartz, M.A. 1993 The extra cellular matrix as a cell survival factor. Mol. Biol. of the Cell 4: 953–961.

    CAS  Google Scholar 

  82. Sarin, A., Adams, D.H. and Henkart, P.A. 1993. Protease inhibitors selectively block T cell receptor triggered programmed cell death in a murine T cell hybridoma and activated peripheral T cells. J. Exp. Med. 178: 1693–1700.

    CAS  PubMed  Google Scholar 

  83. Miura, M., Zhu, H., Rotello, R., Hartwieg, E. A. and Yuan, J. 1994. Induction of apoptosis in flbroblasts by IL-lB-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75: 653–660.

    Google Scholar 

  84. Piacentini, M., Davies, P.J.A. and Fesus, L. 1994. Tissue transglutaminases in cells undergoing apoptosis. p. 143–163. In: Apoptosis II: The Molecular Basis of Apoptosis in Disease. L. D. Tomei and F. O. Cope (Eds. ). Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  85. Tartaglia, L.A. and Goeddel, D.V. 1992. Two TNF receptors. Immunol. Today 13: 151–153.

    CAS  PubMed  Google Scholar 

  86. Rabizadeh, S., Oh, J., Zhong, L.-T., Yang, J., Bitler, C.M., Butcher, L.L. and Bredesen, D.E. 1992. Induction of apoptosis by the low-affinity NGF receptor. Science 261: 345–348.

    Google Scholar 

  87. Farrah, T. and Smith, C.A. 1992. Emerging cytokine family. Nature 358: 26.

    CAS  PubMed  Google Scholar 

  88. Nakamura, Y., Komatsu, N. and Nakauchi, H. 1992. A truncated erythropoietin receptor that fails to prevent programmed cell death of erythroid cells. Science 257: 1138–1141.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. LXR Biotechnology Inc., 1401 Marina Way South, Richmond, CA, 94804

    Philip J. Barr & L. David Tomei

Authors
  1. Philip J. Barr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. David Tomei
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barr, P., Tomei, L. Apoptosis and Its Role in Human Disease. Nat Biotechnol 12, 487–493 (1994). https://doi.org/10.1038/nbt0594-487

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt0594-487

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing