Apoptosis pp 97-115 | Cite as

Ion Signalling in Apoptosis

  • Pierluigi Nicotera
  • Boris Zhivotovsky
  • Giorgio Bellomo
  • Sten Orrenius
Part of the Pezcoller Foundation Symposia book series (PFSO, volume 5)

Abstract

Apoptosis (Kerr et al., 1972; Wyllie et al., 1980), a genetically controlled cell deletion process modulates organ development (Ellis and Horvitz, 1986) and immune cell ontogenesis (Smith et al., 1989) in a predestined fashion. In the adult organism, the apoptotic program is activated to kill neoplastic cells (Trauth et al., 1989) influencing the rate of tumor cell population expansion (Arends and Wyllie, 1991). On the other hand, apoptosis can be evoked in a number of pathological states. Thus, immuno-competent cells are inappropriately eliminated by apoptosis in HIV infection (Groux et al., 1992), whereas viruses (Rao et al., 1992) and bacterial toxins (Fiorentini et al, 1993) can directly elicit an apoptotic response in target cells. Finally, exposure to ionizing radiation (Zhivotovsky et al., 1981 and 1993b) or chemical toxicants (McConkey et al., 1988; Aw et al., 1990) can accelerate apoptosis in immature T cells.

Keywords

Apoptotic Body Endonuclease Activation Chromatin Loop Thymocyte Apoptosis Apoptotic Body Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alnemri, E.S. and Litwack, G., 1990, Activation of internucleosomal DNA cleavage in human CEM lymphocytes by glucocorticoid and novobiocin, J. Biol. Chem., 265: 17323–17333.PubMedGoogle Scholar
  2. Arends, M.J., Morris, R.G. and Wyllie, A.H., 1990, Apoptosis- The role of the endonuclease, Amer. J. Pathol., 136: 593–608.Google Scholar
  3. Arends, M.J. and Wyllie, A.H., 1991, Apoptosis: mechanisms and roles in pathology, Int. Rev. Exper. Pathol., 32: 223–254.Google Scholar
  4. Aw, T.Y., Nicotera, P., Manzo, L. and Orrenius, S., 1990, Tributyltin stimulates apoptosis in rat thymocytes, Arch. Biochem. Biophys., 283: 46–50.PubMedCrossRefGoogle Scholar
  5. Barry, M.A. and Eastman, A., 1993, Identification of deoxyribonuclease II as an endonuclease involved in apoptosis, Arch. Biochem. Biophys., 300: 440–445.PubMedCrossRefGoogle Scholar
  6. Bartlett, J.D., Luethy, J.D., Carlson, S.G., Sollott, S.J. and Holbrook, N.J., 1992, Calcium ionophore A23187 induces expression of the growth arrest and DNA damage inducible CCAAT/enhancer-binding protein (C/EBP)-related gene, gadd 153., J. Biol. Chem 267: 20465–20470.Google Scholar
  7. Beletsky, I.P., Matyasova, J., Nikonova, L.V., Skalka, M. and Umansky, S.R., 1989, On the role of Ca2+-Mg2+-dependent endonuclease in the post-irradiation degradation of chromatin in lymphoid tissues, Gen. Physiol. Biophys., 8: 381–389.PubMedGoogle Scholar
  8. Bellomo, G., Perotti, M., Taddei, F., Mirabelli, F., Finardi, G., Nicotera, P. and Orrenius, S., 1992, Tumor necrosis factor a induces apoptosis in mammary adenocarcinoma cells by an increase in intranuclear free Ca2+ concentration and DNA fragmentation, Cancer Res., 52: 1342–1346.PubMedGoogle Scholar
  9. Brown, D.G., Sun, X. and Cohen, G.M., 1993, Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation, J. Biol. Chem., 268: 3037–3039.PubMedGoogle Scholar
  10. Brüne, B., Hartzeil, P., Nicotera, P. and Orrenius, S., 1991, Spermine prevents endonuclease activation and apoptosis in thymocytes, Exp. Cell Res., 195: 323–329.PubMedCrossRefGoogle Scholar
  11. Chafouleas, J.G., Lagace, L., Bolton, W.E., Boyd, A.E. and Means, A.R., 1984, Changes in calmodulin and its mRNA accompany reentry of quiescent (GO) cells into the cell cycle., Cell, 36: 73–81.PubMedCrossRefGoogle Scholar
  12. Clark, D.J. and Thomas, J.O., 1986, Salt-dependent co-operative interaction of histone H1 with linear DNA, J. Mol. Biol., 187: 569–580.PubMedCrossRefGoogle Scholar
  13. Cohen, G.M., Sun, X., Snowden, R.T., Dinsdale, D. and Skilleter, D.N., 1992, Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation, Biochem. J., 286: 331–334.PubMedGoogle Scholar
  14. Crabtree, G.R., 1989, Contingent genetic regulatory events in T-lymphocyte activation., Science, 243: 355–361.PubMedCrossRefGoogle Scholar
  15. Dowd, D.R., MacDonald, P.N., Komm, B.S., Haussler, M.R. and Miesfeld, R.L., 1992, Stable expression of the calbindin-D28K complementary DNA interferes with the apoptotic pathway in lymphocytes, Mol. Endocrin., 6: 1843–1848.CrossRefGoogle Scholar
  16. Dowd, D.R., MacDonald, P.N., Komm, B.S., Maussler, M.R. and Miesfeld, R., 1991, Evidence for early induction of calmodulin gene expression in lymphocytes undergoing glucocorticoid-mediated apoptosis, J. Biol. Chem., 266: 18423–18426.PubMedGoogle Scholar
  17. Dypbukt, J. M., Ankarcrona, M. Burkitt, M., Sjöholm Å, Ström, K., Orrenius S., and Nicotera, P., 1993, Different proooxidant levels stimulate cell growth, activate apoptosis, or produce necrosis in insulinsecreting RINm5F cells. J. Biol. Chem. Submitted for publication.Google Scholar
  18. Elias, L. and Berry, C.O.A., 1991, Induction of differentiation by tumour necrosis factor In HL-60 cells is associated with the formation of large DNA fragments., Leukemia, 5: 879–885.PubMedGoogle Scholar
  19. Ellis, H.M. and Horvitz, H.R., 1986, Genetic control of programmed cell death in the Nematode C. Elegans, Cell, 44: 817–829.PubMedCrossRefGoogle Scholar
  20. Ericsson, C., Grossbach, U., Björkroth, B. and Daneholt, B., 1990, Presence of histone H1 on an active Balbiani ring gene, Cell, 60: 73–83.PubMedCrossRefGoogle Scholar
  21. Evan, G.I., Wyllie, A.H., Gilbert, C.S., Littlewood, T.D., Land, H., Brooks, M., Waters, C.M., Penn, L.Z. and Hancock, D.C., 1992, Induction of apoptosis in fibroblasts by c-myc protein, Cell, 69: 19–128.CrossRefGoogle Scholar
  22. Fiorentini, C., Donelli, G., Nicotera, P. and Thelestam, M., 1993, Clostridium difficile toxin A elicits Ca2+-independent cytotoxic effects in cultured normal rat intestinal crypt cells, Infect. Immun., 61: 300–306.Google Scholar
  23. Gaido, M.L. and Cidlowski, J.A., 1991, Identification, purification, and characterization calcium- dependent endonuclease (NUC18) from apoptotic rat thymocytes., J. Biol. Chem., 266: 18580–18585.PubMedGoogle Scholar
  24. Gradwohl, G., Menissier de Murcia, J.M., Molinete, M. and Simonin, F., 1990, The second zinc-finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA, Proc. Natl. Acad. Sci. USA, 87: 2990–2994.PubMedCrossRefGoogle Scholar
  25. Groux, H., Torpier, G., Monté, D., Mouton, Y., Capron, A. and Amesien, J.C., 1992, Activation-induced death by apoptosis in CD4+ T cells from human immunoficiency virus-infected asymptomatic individuals., J. Exp. Med., 175: 331–340.PubMedCrossRefGoogle Scholar
  26. Guo, X. and Cole, R.D., 1989, Chromatin aggregation changes substantially as pH varies within the physiological range., J. Biol. Chem., 264: 11653–11657.PubMedGoogle Scholar
  27. Hechtenberg, S. and Beyersmann, D., 1993, Differential control of frealcium and free zinc levels in isolated bovine liver nuclei., Biochem. J., 289: 757–760.PubMedGoogle Scholar
  28. Helgason, C.D., Shi, L., Greenberg, A.H., Shi, Y., Bromley, P., Cotter, T.C., Green, D.R. and Bleackley, R.C., 1993, DNA fragmentation induced by cytotoxic-T lymphocytes can result in target cell death., Exp. Cell. Res., 206: 302–310.PubMedCrossRefGoogle Scholar
  29. Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R.D. and Korsmayer, S.J., 1990, Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death., Nature, 348: 334–336.PubMedCrossRefGoogle Scholar
  30. Inesi, G. and Sagara, Y., 1992, Thapsigargin, a high affinity and global inhibitor of intracellular Ca2+ transport ATPases., Arch. Biochem. Biophys., 298: 313–317.PubMedCrossRefGoogle Scholar
  31. Jiang, S., Chow, S.C., Nicotera, P. and Orrenius, S., 1993, Intracellular Ca2+ signals activate apoptosis in thymocytes. Studies using the Ca2+-ATPase inhibitor, thapsigargin, J. Biol. Chem. Submitted for publication.Google Scholar
  32. Jin, Y. and Cole, R.D., 1986, Exchange of H1 histone depends on aggregation of chromatin, not simply on ionic strength., J. Biol. Chem., 261: 15805–15812.PubMedGoogle Scholar
  33. Jones, D.P., McConkey, D.J., Nicotera, P. and Orrenius, S., 1989, Calcium-activated DNA fragmentation in rat liver nuclei, J. Biol. Chem., 264: 6398–6403.PubMedGoogle Scholar
  34. Juntti-Berggren, L., Larsson, O., Rorsman, P., Ämmälä, C., Bokvist, K., Wåhlander, K., Nicotera, P., Dypbukt, J., Orrenius, S., Hallberg, A. and Berggren, P., 1993, Increased activity of L-type Ca2+ channels exposed to serum from patients with type I diabetes, Science, 261: 86–90.PubMedCrossRefGoogle Scholar
  35. Kawabata, H., Anzai, N., Masutani, H., Hirama, T., Yoshida, Y. and Okuma, M., 1993, Detection of Mg2+-dependent endonuclease activity In myeloid leukemia cell nuclei capable of producing internucleosomal DNA cleavage, Biochem. Biophys. Res. Commun., 191: 247–254.PubMedCrossRefGoogle Scholar
  36. Käs, E., Poljac, L., Adachi, Y. and Laemmli, U.K., 1993, A model for chromatin opening: stimulation of topoisomerase II and restriction enzyme cleavage of chromatin by distamycin, EMBO J., 12: 115–126.PubMedGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Kyprianou, N. and Isaacs, J.T., 1988, Activation of programmed cell death in the rat ventral prostate after castration., Endocrinol., 122: 552–562.CrossRefGoogle Scholar
  39. McCabe, M.J., Jiang, S. and Orrenius, S., 1993, Chelation of intracellular zinc triggers apoptosis in mature thymocytes., Lab. Invest., 69: 101–110.PubMedGoogle Scholar
  40. McConkey, D.J., Chow, S.C., Orrenius, S. and Jondal, M., 1990, NK cell-induced cytotoxicity is dependent on a Ca2+ increase in the target, FASEB J., 4: 2661–2664.PubMedGoogle Scholar
  41. McConkey, D.J., Hartzell, P., Duddy, S.K., Håkansson, H. and Orrenius, S., 1988, 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin kills immature thymocytes by Ca2+-mediated endonuclease activation, Science, 242: 256–258.PubMedCrossRefGoogle Scholar
  42. McConkey, D.J., Hartzell, P., Nicotera, P. and Orrenius, S., 1989, Calcium-activated DNA fragmentation kills immature thymocytes, FASEB J., 3: 1843–1849.PubMedGoogle Scholar
  43. Morgan, J.I. and Curran, T., 1986, Role of ion flux in the control of c-fosexpression., Nature, 322: 552–555.PubMedCrossRefGoogle Scholar
  44. Nicotera, P., Bellomo, G. and Orrenius S., 1992, Calcium-mediated mechanisms in chemically-induced cell death, Annu. Rev. Pharmacol. Toxicol., 32: 449–470.PubMedCrossRefGoogle Scholar
  45. Nicotera, P., McConkey, D.J., Jones, D.P. and Orrenius, S., 1989, ATP stimulates Ca2+ uptake and increases the free Ca2+ concentration in isolated rat liver nuclei, Proc. Natl. Acad. Sci. U. S. A., 86: 453–457.PubMedCrossRefGoogle Scholar
  46. Nicotera, P., Orrenius, S., Nilsson, T. and Berggren, P.O., 1990, An inositol 1,4,5-trisphosphate-sensitive Ca2+ pool in liver nuclei, Proc. Natl. Acad. Sci. U. S. A., 87: 6858–6862.PubMedCrossRefGoogle Scholar
  47. Oberhammer, F.A., Pavelka, M., Sharma, S., Tiefenbacher, R., Purchio, A.F., Bursch, W. and Schulte-Hermann, R., 1992, Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor β 1, Proc. Natl. Acad. Sci. USA, 89: 5408–5412.PubMedCrossRefGoogle Scholar
  48. Oberhammer, F., Wilso, J.W., Dive, C., Morris, I.D., Hickman J.A., Wakeling, A.E., Walker, P.R., and Sikorska, M, 1993, Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation, EMBO J., 12: 3679–3684.PubMedGoogle Scholar
  49. Peitsch, M.C., Polzar, B., Stephan, H., Crompton, T., MacDonald, H.R., Mannherz, H.G. and Tschopp, J., 1993, Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death)., EMBO J., 12: 371–377.PubMedGoogle Scholar
  50. Pfaffle, P., Gerlach, V., Bunzel, L. and Jackson, V., 1990, In Vitro evidence that transcription-induced stress causes nucleosome dissolution and regeneration., J. Biol. Chem., 265: 16830–16840.PubMedGoogle Scholar
  51. Planas-Silva, M.D. and Means, A.R., 1992, Expresson of a constitutive form of calcium/calmodulin dependent protein kinase II leads to arrest of the cell cycle in G2., EMBO J., 11: 507–517.PubMedGoogle Scholar
  52. Prütz, W.A., Butler, J. and Land, E.J., 1990, Interaction of copper(I) with nucleic acids., Int. J. Radiat. Biol., 58: 215–234.PubMedCrossRefGoogle Scholar
  53. Rao, L., Debbas, M., Sabbatini, P., Hockenbery, D., Korsmeyer, S. and White, E., 1992, The adenovirus E1A protein induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins, Proc. Natl. Acad. Sci. USA, 89: 7742–7746.PubMedCrossRefGoogle Scholar
  54. Roy, C., Brown, D.L., Little, J.E., Valentine, B.K., Walker, P.R., Sikorska, M., Leblanc, J. and Chali, N., 1992, The topoisomerase II inhibitor teniposide (VM-26) induces apoptosis in unstimulated mature murine lymphocytes, Exper. Cell. Res., 200: 416–424.CrossRefGoogle Scholar
  55. Samuel, M., Zhu, C.X., Villanueva, G.D. and Tse-Dinh, Y.C., 1993, Effect of zinc removal on the conformation of Escherichia Coli DNA topoisomerase I., Arch. Biochem. Biophys., 300: 302–308.PubMedCrossRefGoogle Scholar
  56. Savill, J., Fadok, V., Henson, P. and Haslett, C., 1993, Phagocyte recognition of cells undergoing apoptosis., Immunol. Today, 14: 131–136.PubMedCrossRefGoogle Scholar
  57. Schwartz, L.M., Kosz, L. and Kay, B.K., 1990, Gene activation is required for developmentally programmed cell death., Proc. Natl. Acad. Sci. USA, 87: 6594–6598.PubMedCrossRefGoogle Scholar
  58. Seiliev, A.A., Zvonareva, N.B., Zhivotovsky, B.D. and Hanson, K.P., 1992, Determination of some nuclear deoxyribonucleases in X-irradiated rat thymocytes, Radiat. Environ. Biophys., 31: 123–132.PubMedCrossRefGoogle Scholar
  59. Smeyne, R.J., Vendrell, M., Hayward, M., Baker, S.J., Miao, G.G., Schilling, K., Robertson, L.M., Curran, T. and Morgan, J.I., 1993, Continuous c-fosexpression precedes programmed cell death in vivo., Nature, 363: 166–169.CrossRefGoogle Scholar
  60. Smith, C.A., Williams, G.T., Kingston, R., Jenkinson, E.J. and Owen, J.J.T., 1989, Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures., Nature, 337: 181–184.PubMedCrossRefGoogle Scholar
  61. Snyder, R.D., 1989, Polyamine depletion is asssociated with altered chromatin structure in HeLa cells, Biochem. J., 260: 697–704.PubMedGoogle Scholar
  62. Thastrup, O., Cullen, P.J., Dröbak, B, Hanley, M.R. and Dawson, A. 1990, Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase., Proc. Natl. Acad. Sci. USA, 87: 2466–2470.PubMedCrossRefGoogle Scholar
  63. Trauth, B.C., Klas, C., Peters, A.M.J., Matzku, S., Moller, P., Falk, W., Debatin, K. and Krammer, P.H., 1989, Monoclonal antibody-mediated tumor regression by induction of apoptosis., Science, 245:301–305.PubMedCrossRefGoogle Scholar
  64. Villeponteau, B., Pribyl, T.M., Grant, M.H. and Martinson, H.G., Novobiocin induces the in vivo cleavage of active gene sequences in intact cells, 1986, J. Biol. Chem., 261: 10359–10365.PubMedGoogle Scholar
  65. Walker, P.R., Smith, C, Youdale, T., Leblave, J., Whitfield, J.F. and Sikoska, M., 1991, Topoisomerase II reactive chemotherapeutic drugs induce apoptosis in thymocytes, Cancer Res., 51: 1078–1085.PubMedGoogle Scholar
  66. White, B.A. and Bancroft, C. (1987) Cheung, W.Y. (ed.) Calcium and Cell Functions, Academic Press, New York, pp. 109–132.Google Scholar
  67. Wu, C., Bingham, P.M., Livak, K.J., Holmgren, R. and Elgin, S.C.R., 1979, The chromatin structure of specific genes: I. Evidence for higher order domains of defined DNA sequence, Cell, 16: 797–806.PubMedCrossRefGoogle Scholar
  68. Wyllie, A.H., 1980, Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation, Nature, 284: 555–556.PubMedCrossRefGoogle Scholar
  69. Wyllie, A.H., Kerr, J.F.R. and Currie, A.R., 1980, Cell death: The significance of apoptosis, Int. Rev. Ctyol., 68: 251–305.CrossRefGoogle Scholar
  70. Yonish-Rouach, E., Resnitzky, D., Lotem, J., Sachs, L., Kinchi, A. and Oren, M., 1991, Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6, Nature, 352: 345–347.PubMedCrossRefGoogle Scholar
  71. Zhivotovsky, B., Cedervall, B., Nicotera, P. and Orrenius, S., 1993a, Ca2+-dependent formation of large molecular weight DNA fragments in thymocyte apoptosis. Submitted for publication.Google Scholar
  72. Zhivotovsky, B., Nicotera, P., Bellomo, G., Hanson, K. and Orrenius, S., 1993b, Ca2+ and endonuclease activation in radiation-induced lymphoid cell death., Exp. Cell. Res, 207: 163–170.PubMedCrossRefGoogle Scholar
  73. Zhivotovsky, B.D., Zvonareva, N.B. and Hanson, K.P., 1981, Characteristics of rat thymus chromatin degradation products after whole-body X irradiation, Int. J. Radiat. Biol, 39: 437–440.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • Pierluigi Nicotera
    • 1
  • Boris Zhivotovsky
    • 1
  • Giorgio Bellomo
    • 2
  • Sten Orrenius
    • 1
  1. 1.Institute of Environmental Medicine, Division of ToxicologyKarolinska InstituteStockholmSweden
  2. 2.Department of Experimental Medicine and Oncology, Institute of General PathologyUniversity of TorinoTorinoItaly

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