Skip to main content
SpringerLink
Log in

Cell Volume Regulation and the Movement of Ions during Apoptosis

  • Chapter
Cell Death in Reproductive Physiology

Part of the book series: Proceedings in the Serono Symposia USA Series ((SERONOSYMP))

Abstract

Apoptosis is a physiological mode of cell death in which cells are removed or eliminated from the body in response to a given signal or stimulus (1). Apoptosis, also known as programmed cell death, can be distinguished from accidental cell death, referred to as necrosis, by a unique set of characteristics that includes cell shrinkage, nuclear condensation, internucleosomal DNA cleavage, and apoptotic body formation (2). Although many studies have focused on the biochemical (i.e., internucleosomal DNA cleavage) and morphological (i.e., apoptotic body formation) characteristics of apoptosis, relatively few have examined the characteristic cell shrinkage associated with programmed cell death. The distinctive feature of volume loss during this form of cell death was observed from the very first reports of apoptosis (3, 4), and subsequently, cell shrinkage has been observed in all well-defined examples of apoptosis. Thus, the loss of cell volume, along with internucleosomal DNA cleavage, reflects key components of the programmed cell death process.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 16.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Schwartzman RA, Cidlowski JA. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 1993; 14: 133–51.

    PubMed  CAS  Google Scholar 

  2. Martin SJ, Green DR, Cotter TG. Dicing with death: dissecting the components of the apoptotic machinery. Trends Biochem Sci 1994; 19: 26–30.

    Article  PubMed  CAS  Google Scholar 

  3. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239–57.

    Article  PubMed  CAS  Google Scholar 

  4. Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980; 284: 555–6.

    Article  PubMed  CAS  Google Scholar 

  5. Sten-Knudson O. Passive transport processes. In: Giebisch G, Tosteson DC, Ussing HH, eds. Membrane transport in biology. Vol. I. Concepts and Models. Berlin and New York: Springer-Verlag, 1978: 5–113.

    Google Scholar 

  6. Wilson TH. Ionic permeability and osmotic swelling of cells. Science 1954; 120: 104–5.

    Article  PubMed  CAS  Google Scholar 

  7. Leaf A. On the mechanism of fluid exchange of tissues in vitro. Biochem J 1956; 62: 241–8.

    PubMed  CAS  Google Scholar 

  8. Skou JC. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochem Biophys Acta 1957; 23: 294–401.

    Article  Google Scholar 

  9. Proverbio F, Duque JA, Proverbio T, Malin R. Cell volume-sensitive Na+-ATPase activity in rat kidney cortex cell membranes. Biochem Biophys Acta 1988; 941: 107–10.

    Article  PubMed  CAS  Google Scholar 

  10. Parker JC. Dog red blood cells: adjustment of density in vivo. J Gen Physiol 1973; 62: 147–56.

    Article  PubMed  CAS  Google Scholar 

  11. Al-Habori M. Cell volume and ion transport regulation. Int J Biochem 1994; 26: 319–34.

    Article  PubMed  CAS  Google Scholar 

  12. Hoffmann EK. Volume regulation in cultured cells. Curr Top Membr Transport 1987; 30: 125–80.

    Article  Google Scholar 

  13. McManus TJ, Haas M, Starke C, Lytle CW. The duck red cell model of volume-sensitive chloride-dependent cation transport. Anno NY Acad Sci 1985; 456: 183–6.

    Article  CAS  Google Scholar 

  14. Lauf PK. K+:C1- cotransport: sulfhydryls, divalent cations and the mechanism of volume regulation. J Membr Biol 1985; 88: 1–13.

    Article  PubMed  CAS  Google Scholar 

  15. Hall AC, Ellory JC. Effects of high hydrostatic pressure on “passive” monovalent cation transport in human red cells. J Membr Biol 1986; 94: 1–17.

    Article  PubMed  CAS  Google Scholar 

  16. Cala PM. Volume regulation by amphiuma red blood cells: characteristics of volume-sensitive K/H and Na/H exchange. Mo1 Physiol 1985; 8: 199–214.

    CAS  Google Scholar 

  17. Grinstein S, Rothstein A, Sarkadi B, Gelfand EW. Responses of lymphocytes to anisotonic media: volume-regulating behavior. Am J Physiol 1984;246:C204–15.

    PubMed  CAS  Google Scholar 

  18. Sarkadi B, Mack E, Rothstein A. Ionic events during the volume response of human peripheral blood lymphocytes to hypotonic media. I. Distinctions between volume-activated Cl-and K+ conductance pathways. J Gen Physiol 1984; 83: 497–512.

    Article  PubMed  CAS  Google Scholar 

  19. Sarkadi B, Mack E, Rothstein A. Ionic events during the volume response of human peripheral blood lymphocytes to hypotonic media. II. Volume-and time-dependent activation and inactivation of ion transport pathways. J Gen Physiol 1984; 83: 513–27.

    Article  PubMed  CAS  Google Scholar 

  20. Hoffmann EK, Simonsen LO, Lambert IH. Volume-induced increase of K+ and C1- permeabilities in Ehrlich ascites tumour cells: role of internal Ca2+. J Membr Biol 1984; 78: 211–22.

    Article  PubMed  CAS  Google Scholar 

  21. Banderali U, Roy G. Activation of K+ and Cl-channels in MDCK cells during volume regulation in hypotonic media. J Membr Biol 1992; 126: 219–34.

    PubMed  CAS  Google Scholar 

  22. Davis CW, Finn AL. Interactions of sodium transport, cell volume, and calcium in frog urinary bladder. J Gen Physiol 1987; 89: 687–702.

    Article  PubMed  CAS  Google Scholar 

  23. Duhm J, Gobel BO. Na+-K+ transport and volume of rat erythrocytes under dietary K+ deficiency. Am J Physiol 1984;246:C20–9.

    PubMed  CAS  Google Scholar 

  24. O’Neil WC. Volume-sensitive Cl--dependent K transport in human erythrocytes. Am J Physiol 1987; 258: F1657–65.

    Google Scholar 

  25. Levinson C. Regulatory volume increase in Ehrlich ascites tumour cells is mediated by the 1Na:1K:2C1 cotransport system. J Membr Biol 1992; 126: 277–84.

    PubMed  CAS  Google Scholar 

  26. Grinstein S, Clarke CA, Dupre A, Rothstein A. Volume-induce increase of anion permeability in human lymphocytes. J Gen Physiol 1982; 80: 801–23.

    Article  PubMed  CAS  Google Scholar 

  27. Grinstein S, Goetz JD, Cohen S, Rothstein A, Gelfand EW. Regulation of Na+/H+ exchange in lymphocytes. Ann NYAcad Sci 1985; 456: 207–19.

    Article  CAS  Google Scholar 

  28. Lang F, Stehle T, Haussinger D. Water, K+, H+, lactate and glucose fluxes during cell volume regulation in perfused rat liver. Pflugers Arch 1989; 413: 209–16.

    Article  PubMed  CAS  Google Scholar 

  29. Ericson AC, Spring KR. Volume regulation by necturus gallbladder: apical Na+-H+ and C1--HCO3 exchange. Am J Physiol 1982;243:C146–50.

    PubMed  CAS  Google Scholar 

  30. Cheung RK, Grinstein S, Gelfand EW. Volume regulation by human lymphocytes: identification of differences between the two major lymphocyte subpopulations. J Clin Invest 1992; 70: 632–38.

    Article  Google Scholar 

  31. Grinstein S, Clarke CA, Rothstein A, Gelfand EW. Volume-induced anion conductance in human B lymphocytes is cation independent. Am J Physiol 1983;245: C160–3.

    PubMed  CAS  Google Scholar 

  32. Roti-Roti LW, Rothstein A. Adaptation of mouse leukemic cells (L5178Y) to anisotonic media. I. Cell volume regulation. Exp Cell Res 1973; 79: 295–310.

    CAS  Google Scholar 

  33. Hempling HG, Thompson S, Dupre A. Osmotic properties of human lymphocytes. J Cell Physiol 1977; 93: 293–302.

    Article  PubMed  CAS  Google Scholar 

  34. Grinstein S, Clarke CA, Rothstein A. Activation of Na+/H+ exchange in lymphocytes by osmotically-induced volume changes and by cytoplasmic acidification. J Gen Physiol 1983; 82: 619–38.

    Article  PubMed  CAS  Google Scholar 

  35. Hughes Jr. FM, Cidlowski JA. Regulation of apoptosis in S49 cells. J Steroid Biochem Molec Biol 1994; 49: 303–10.

    Article  PubMed  CAS  Google Scholar 

  36. Thomas N, Bell PA. Glucocorticoid-induced cell-size changes and nuclear fragility in rat thymocytes. Mo1 Cell Endocrinol 1981; 22: 71–84.

    Article  CAS  Google Scholar 

  37. Wyllie AH, Morris RG. Hormone-induced cell death. Purification and properties of thymocytes undergoing apoptosis after glucocorticoid treatment. Am J Path 1982; 109: 78–87.

    PubMed  CAS  Google Scholar 

  38. Morris RG, Hargreaves AD, Duvall E, Wyllie AH. Hormone-induced cell death. 2. Surface changes in thymocytes undergoing apoptosis. Am J Path 1984; 115: 426–36.

    PubMed  CAS  Google Scholar 

  39. Benson RSP, Heer S, Dive C, Watson AJM. Characteristics of cell volume loss in CEM-C7A cells during dexamethasone-induced apoptosis. Am J Physiol 1996;270:C1190–1203.

    PubMed  CAS  Google Scholar 

  40. Ohyama H, Yamada T, Watanabe I. Cell volume reduction associated with interphase death in rat thymocytes. Radiat Res 1981; 85: 333–9.

    Article  PubMed  CAS  Google Scholar 

  41. Ohyama H, Yamada T, Ohkawa A, Watanabe I. Radiation-induced formation of apoptotic bodies in rat thymus. Radiat Res 1985; 101: 123–30.

    Article  PubMed  CAS  Google Scholar 

  42. Klassen NV, Walker PR, Ross CK, Cygler J, Lach B. Two-stage cell shrinkage and the OER for radiation-induced apoptosis of rat thymocytes. Int J Radiat Biol 1993; 64: 571–81.

    Article  PubMed  CAS  Google Scholar 

  43. Beauvais F, Michel L, Dubertret L. Human eosinophils in culture undergo a striking and rapid shrinkage during apoptosis. Role of K+ channels. J Leukoc Biol 1995; 57: 851–5.

    PubMed  CAS  Google Scholar 

  44. Willman, CL, Stewart CC. General principles of multiparameter flow cytometric analysis: applications of flow cytometry in the diagnostic pathology laboratory. Semin Diagnostic Pathol 1989; 6: 3–12.

    CAS  Google Scholar 

  45. Bonner CD, Cidlowski JA. The absence of volume regulatory mechanisms contributes to the rapid activation of apoptosis in thymocytes. Am J Physiol 1996;271:C950–61.

    Google Scholar 

  46. Cidlowski JA, King KL, Evans-Storms RB, Montague JW, Bonner CD, Hughes FM Jr. The biochemistry and molecular biology of glucocorticoid-induced apoptosis in the immune system. Recent Horm Res 1996; 52: 1–35.

    Google Scholar 

  47. Swat W, Ignatowicz L, Kisielow P. Detection of apoptosis of immature CD4+8+ thymocytes by flow cytometry. J Immunol Meth 1991; 137: 79–87.

    Article  CAS  Google Scholar 

  48. Darzynkiewicz Z, Bruno S, Del Bino G, Gorczyca W, Hotz MA, Lassota P, Traganos F. Features of aoptotic cells measured by flow cytometry. Cytometry 1992; 13: 795808.

    Google Scholar 

  49. Wesselborg S, Kabelitz D. Activation-driven death of human T cell clones: time course kinetics of the induction of cell shrinkage, DNA fragmentation, and cell death. Cell Immunol 1993; 148: 234–41.

    Article  PubMed  CAS  Google Scholar 

  50. Barbiero G, Duranti F, Bonelli G, Amenta JS, Baccino FM. Intracellular ionic variations in the apoptotic death of L cells by inhibitors of cell cycle progression. Expt Cell Res 1995; 217: 410–8.

    Article  CAS  Google Scholar 

  51. Jonas D, Walev I, Berger T, Liebetrau M, Palmer M, Bhakdi S. Novel path to apoptosis: small transmembrane pores created by Staphylococcal alpha-toxin in T lymphocytes evokes internucleosomal DNA degradation. Infect Immun 1994; 62: 1304–12.

    PubMed  CAS  Google Scholar 

  52. Zhu WH, Loh TT. Effects of Na+/H+ antiport and intracellular pH in the regulation of HL-60 cell apoptosis. Biochim Biophys Acta 1995; 1269: 122–8.

    Article  PubMed  Google Scholar 

  53. Li J, Eastman A. Apoptosis in an interleukin-2-dependent cytotixic T-lymphocyte cell line is associated with intracellular acidification. J Biol Chem 1995; 270: 3203–11.

    Article  PubMed  CAS  Google Scholar 

  54. Wilcock C, Chahwala SB, Hickman JA. Selective inhibition by bis(2chloroethyl)methylamine (nitrogen mustard) of the Na+/K+/C1- cotransporter of murine L12 10 leukemia cells. Biochim Biophys Acta 1988; 946: 368–78.

    Article  PubMed  CAS  Google Scholar 

  55. Yun CHC, Tse CM, Nath sk, Levine SA, Brant SR, Donowitz M. Mammalian Na+/ H+ exchanger gene family: structure and function studies. Am J Physiol 1995, 269: G1–11.

    PubMed  CAS  Google Scholar 

  56. Sardet, C, Counillon, L, Franchi, A, Pouyssegur, J. Growth factors induce phosphorylation of the Na+/H+ antiporter, a glycoprotein of 110 kD. Science 1990; 247: 723–6.

    Article  PubMed  CAS  Google Scholar 

  57. Haussinger D, Lang F, Gerok W. Regulation of cell function by the cellular hydration state. Am J Physiol 1994;267:E343–55.

    PubMed  CAS  Google Scholar 

  58. Wu G, Flynn NE. Regulation of glutamine and glucose metabolism by cell volume in lymphocytes and macrophages. Biochem Biophys Acta 1995; 1243: 343–50.

    Article  PubMed  Google Scholar 

  59. D’Mello SR, Galli C, Ciotti T, Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 1993; 90: 10989–93.

    Article  PubMed  Google Scholar 

  60. Kumar S. ICE-like proteases in apoptosis. Trends Biochem Sci 1995; 20: 198–202.

    Article  PubMed  CAS  Google Scholar 

  61. Walev I, Reske K, Parer M, Valeva A, Bhakdi S. Potassium-inhibited processing of IL-lb in human monocytes. EMBO 1995; 14: 1607–14.

    CAS  Google Scholar 

Download references

Authors
  1. Carl D. Bortner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John A. Cidlowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Vincent Center for Reproductive Biology, Massachusetts General Hospital, Boston, MA, 02114, USA

    Jonathan L. Tilly Ph.D.

  2. Center for Research on Reproduction and Women’s Health, University of Pennsylvania School of Medicine, Philadelphia, PA, 19104, USA

    Jerome F. Strauss III M.D., Ph.D.

  3. W. Alton Jones Cell Science Center, Lake Placid, NY, 12946, USA

    Martin Tenniswood Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer Science+Business Media New York

About this chapter

Cite this chapter

Bortner, C.D., Cidlowski, J.A. (1997). Cell Volume Regulation and the Movement of Ions during Apoptosis. In: Tilly, J.L., Strauss, J.F., Tenniswood, M. (eds) Cell Death in Reproductive Physiology. Proceedings in the Serono Symposia USA Series. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-1944-6_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-1944-6_18

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7351-6

  • Online ISBN: 978-1-4612-1944-6

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation