Activation of Programmed Cell Death by Calcium: Protection against Cell Death by the Calcium Binding Protein, Calbindin-D28k

  • Sylvia Christakos
  • Frank Barletta
  • Michael Huening
  • Jody Kohut
  • Mihali Raval-Pandya

Abstract

Calcium has been known to be a potent second messenger for a wide range of cellular processes from fertilization to cell death. It has been implicated in the regulation of protein kinases, phosphatases, protease activity, chromatin structure and transcription as well as in the regulation of muscle contraction, nerve transmission, cytoskeletal organization, cell cycle progression and differentiation (Berridge, 1997; Berridge et al., 1998). Calcium homeostasis is tightly regulated such that any exogenous or internally generated calcium load is rapidly controlled to maintain calcium balance. Calcium ions signal from outside to inside by raising the intracellular cytosolic calcium concentration. An increase in cytosolic calcium can also occur inside the cell by release from stores. The mitochondria and the endoplasmic reticulum cross talk with each other to modulate the cytosolic calcium concentration. Thus an interplay among membrane components, intracellular organelles, calcium pumps and ion channels exists. Although calcium signaling is complex and incorporates multiple factors, it has been suggested that the ability of the calcium ion to interact with a family of calcium binding proteins (Kd = 10−8–10−10 M), known as EF-hand proteins, can play an important role in the transduction of the calcium signal into a biological response (Christakos et al., 1989, 1997; Heizmann and Braun, 1992; Heizmann and Hunziker, 1991; Schafer and Heizmann, 1996; Zimmer et al., 1995). This family of calcium binding proteins consists of over 200 members and is characterized by the EF-hand structural motif.

Keywords

Ischemia Dementia Cysteine Luminal Glucocorticoid 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andressen, C, Blumcke, I. and Celio, M.R., 1993, Calcium binding proteins: Selective markers of nerve cells, Cell Tissue Res. 271, 181–208.PubMedCrossRefGoogle Scholar
  2. Asai, A., Qiu, J.-H., Narita, Y., Chi, S., Saito, N., Shinoura, N., Hamada, H., Kuchino, Y. and Kirino, T., 1999, High level calcineurin activity predisposes neuronal cells to apoptosis, J. Biol. Chem. 274, 34450–34458.PubMedCrossRefGoogle Scholar
  3. Ashkanezi, A. and Dixit, V.M., 1998, Death receptors: Signaling and modulation, Science 281, 1305–1308.CrossRefGoogle Scholar
  4. Baimbridge, K.G., Mody, I. and Miller, J.J., 1985, Reduction of rat hippocampal calcium binding protein following commissural, amygdala, septal, perforant path and olfactory bulb kindling, Epilepsia 26, 460–465.PubMedCrossRefGoogle Scholar
  5. Bellido, T., Han, L., Huening, M., Barger, S.W., Manolagas, S.C. and Christakos, S., 1998, Calbindin-D28k is expressed in osteoblastic cells and suppresses their apoptosis by inhibiting caspase 3 activity, J. Bone Min. Res. 23(Suppl. 1), S177.Google Scholar
  6. Berridge, M.J., 1997, The AM and FM of calcium signaling, Nature 386, 759–760.PubMedCrossRefGoogle Scholar
  7. Berridge, M.J., Bootman, M.D. and Lipp, P., 1998, Calcium — A life and death signal, Nature 395, 645–648.PubMedCrossRefGoogle Scholar
  8. Bossy-Wetzel, E., Newmeyer, D.D. and Green, D.R., 1998, Mitochondrial cytochrome c release in apoptois occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization, Embo J. 17, 37–49.PubMedCrossRefGoogle Scholar
  9. Celio, M.R., 1990, Calbindin and parvalbumin in the rat nervous system, Neuroscience 35, 375–475.PubMedCrossRefGoogle Scholar
  10. Chan, S.L. and Mattson, M.P., 1999, Caspase and calpain substrates: Roles in synaptic plasticity and cell death, J. Neurosci. Res. 58, 167–190.PubMedCrossRefGoogle Scholar
  11. Chan-Palay, V., Hochli, M., Savaskan, E. and Hungerecker, G., 1993, Calbindin-D28k and monoamine oxidase A immunoreactive neurons in the nucleus basalis of Meynert in senile dementia of the Alzheimer type and Parkinson’s disease, Dementia 4, 1–15.PubMedGoogle Scholar
  12. Christakos, S., Gabrielides, C. and Rhoten W.B., 1989, Vitamin D-dependent calcium binding proteins: Chemistry, distribution, functional considerations and molecular biology, Endo. Rev. 10, 84–107.CrossRefGoogle Scholar
  13. Christakos, S., Beck, J.D. and Hyllner, S.J., 1997, Calbindin-D28k, in Vitamin D, D. Feldman, F. Glorieux and J.W. Pike (eds.), Academic Press, San Diego, CA, pp. 209–221.Google Scholar
  14. Cohen, G.M., 1997, Caspases: The executioners of apoptosis, Biochem. J. 326, 1–16.PubMedGoogle Scholar
  15. Collazo, D., Takahashi, H. and McKay, R.D.G., 1992, Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus, Neuron 9, 643–656.PubMedCrossRefGoogle Scholar
  16. Dawson, T.M., Steiner, J.P., Dawson, V.L., Dinerman, J.L., Uhl, G.R. and Snyder, S.H., 1993, Immunosuppressent FK 506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity, Proc. Natl. Acad. Sci. USA 90, 9808–9812.PubMedCrossRefGoogle Scholar
  17. Donato, R., 1999, Functional roles of S100 proteins, calcium binding proteins of the EF-hand type, Biochim. Biophys. Acta 1450, 191–231.PubMedCrossRefGoogle Scholar
  18. Dowd, D.R. and Miesfeld, R.L., 1992, Cyclic AMP-induced apoptotic pathways in lymphocytes share distal events, Mol. Cell. Biol 12, 3600–3608.PubMedGoogle Scholar
  19. Dowd, D.R., MacDonald, P.N., Komm, B.S., Haussler, M.R. and Miesfeld, R.L., 1991, Evidence for early induction of calmodulin gene expression in lymphocytes undergoing glucocorticoid-mediated apoptosis, J. Biol. Chem. 266, 18423–18426.PubMedGoogle Scholar
  20. Dowd, D.R., MacDonald, PN., Komm, B.S., Haussler, M.R. and Miesfeld, R.L., 1992, Stable expression of calbindin-D28k complementary DNA interferes with the apoptotic pathway in lymphocytes, Mol. Endo. 6, 1843–1848.CrossRefGoogle Scholar
  21. Elliott, E.M. and Sapolsky, R.M., 1992, Corticosterone enhances kainic acid-induced calcium elevation in cultured hippocampal neurons, J. Neurochem. 59, 1033–1040.PubMedCrossRefGoogle Scholar
  22. Elliott, E.M. and Sapolsky, R.M., 1993, Corticosterone impairs hippocampal neuronal calcium regulation — Possible mediating mechanisms, Brain Res. 602, 84–90.PubMedCrossRefGoogle Scholar
  23. Feldman, S.C. and Christakos, S., 1983, Vitamin D-dependent calcium binding protein in rat brain: Biochemical and immunocytochemical characterization, Endocrinology 112, 290–302.PubMedCrossRefGoogle Scholar
  24. Freund, T.F., Buzsaki, G., Leon, A., Baimbridge, K.G. and Somogyi, P., 1990, Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia, Exp. Brain Res. 83, 55–66.PubMedCrossRefGoogle Scholar
  25. Gaido, M.L. and Cidlowski, J.A., 1991, Identification, purification and characterization of a calcium-dependent endonuclease (NUC 18) from apoptotic rat thymocytes, J. Biol. Chem. 266, 18580–18585.PubMedGoogle Scholar
  26. Garruto, R.M., Fukatsu, R., Yanagihara, R., Gajdusek, D.C., Hook, G. and Fiori, C.E., 1984, Imaging of calcium and aluminum in neurofibrillary tangle-bearing neurons in parkinsonism-dementia of Guam, Proc. Natl. Acad. Sci. USA 81, 1875–1879.PubMedCrossRefGoogle Scholar
  27. Goodman, J.H., Wasterlain, CG., Massarweh, W.F., Dean, E., Sollas, A.L. and Sloviter, R.S., 1993, Calbindin-D28k immunoreactivity and selective vulnerability to ischemia in dentate gyrus of developing rat, Brain Res. 606, 309–314.PubMedCrossRefGoogle Scholar
  28. Green, D.R., 1998, Apoptotic pathways: The roads to ruin, Cell 94, 695–698.PubMedCrossRefGoogle Scholar
  29. Guo, Q., Sopher, B.L., Pham, D.G., Furukawa, K., Robinson, N., Martin, G.M. and Mattson, M.P., 1997, Alzheimer’s presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid ß-peptide: Involvement of calcium and oxyradicals, J. Neurosci. 17, 4212–4222.PubMedGoogle Scholar
  30. Guo, Q., Christakos, S., Robinson, N. and Mattson, M.P., 1998, Calbindin-D28k blocks the proapoptotic actions of mutant presenilin: Reduced oxidative stress and preserved mitochondrial function, Proc. Natl. Acad. Sci. USA 95, 3227–3232.PubMedCrossRefGoogle Scholar
  31. Heizmann, C.W. and Braun, K., 1992, Changes in Ca2+-binding proteins in human neurodegenerative disorders, Trends Neurosci. Res. 15, 259–264.CrossRefGoogle Scholar
  32. Heizmann, C.W. and Hunziker, W., 1991, Intracellular calcium binding proteins: More sites than insights, Trends Biochem. Sci. 16, 98–103.PubMedCrossRefGoogle Scholar
  33. Hirsch, E.C., 1992, Why are nigral catecholaminergic neurons more vulnerable than other cells in Parkinson’s disease?, Ann. Neurol. 32, S88–S93.PubMedCrossRefGoogle Scholar
  34. Ho, B.-K., Alexianu, M.E., Colom, L.V., Mohamed, A.H., Serrano, F. and Appel, S.H., 1996, Expression of calbindin-D28k cDNA prevents amyotropohic lateral sclerosis IgG-mediated cytotoxicity, Proc. Natl Acad. Sci. USA 93, 6796–6801.PubMedCrossRefGoogle Scholar
  35. Hu, J., Ferreira, A. and Van Eldik, L.J., 1997, S100 induces neuronal cell death through nitric oxide release from astrocytes, J. Neurochem. 69, 2294–2300.PubMedCrossRefGoogle Scholar
  36. Iacopino, A.M. and Christakos, S., 1990a, Specific reduction of neuronal calcium binding protein (calbindin-D28k) gene expression in aging and neurodegenerative diseases, Proc. Natl. Acad. Sci. USA 87, 4078–4082.PubMedCrossRefGoogle Scholar
  37. Iacopino, A.M. and Christakos, S., 1990b, Corticosterone regulates calbindin-D28k mRNA and protein levels in rat hippocampus, J. Biol. Chem. 265, 10177–10180.PubMedGoogle Scholar
  38. Ip, N.Y., Li, Y., Yancopoulos, G.D. and Lindsay, R.M., 1993, Cultured hippocampal neurons show responses to BDNF, NT-3 and NT-4 but not NGF, J. Neurosci. 13, 3394–3405.PubMedGoogle Scholar
  39. James, P., Vorherr, T. and Carafoli, E., 1995, Calmodulin-binding domains: Just two faced or multi-faceted?, Trends Biochem. Sci. 20, 38–42.PubMedCrossRefGoogle Scholar
  40. Jilka, R.L., Weinstein, R.S., Bellido, T., Parfitt, A.M. and Manolagas, S.C., 1998, Osteoblast programmed cell death (apoptosis): Modulation by growth factors and cytokines, J. Bone Miner. Res. 13, 793–802.PubMedCrossRefGoogle Scholar
  41. Keller, B.U., The role of intracellular calcium signaling in motoneuron function and disease, this book.Google Scholar
  42. Khan, A.A., Soloski, M.J., Sharp, A.H., Schilling, G., Sabatini, D.M., Li, S.H., Ross, CA. and Snyder, S.H., 1996, Lymphocyte apoptosis: Medition by increased type 3 inositol 1,4,5-triphosphate receptor, Science 273, 503–507.PubMedCrossRefGoogle Scholar
  43. Kligman, D. and Marshak, D.R., 1985, Purification and characterization of a neurite extension factor from bovine brain, Proc. Natl. Acad. Sci. USA 82, 7136–7139.PubMedCrossRefGoogle Scholar
  44. Kroemer, G., Dallaporta, B. and Resche-Rigon, M., 1998, The mitochondrial death/life regulator in apoptosis and necrosis, Annu. Rev. Physiol. 60, 619–642.PubMedCrossRefGoogle Scholar
  45. Li, H. and Yuan, J., 1999, Decifering the pathways of life and death. Curr. Opin. Cell Biol. 11, 261–266.PubMedCrossRefGoogle Scholar
  46. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X., 1997, Cytochrome c and dATP-dependent formation of Apaf-l/caspase-9 complex initiates an apoptosis protease cascade, Cell 91, 479–489.PubMedCrossRefGoogle Scholar
  47. Magloczky, Z.S., Halasz, P., Vajda, J., Czirjak, S. and Freund, T.F., 1997, Loss of calbindin-D28k immunoreactivity from dentate granule cells in human temporal lobe epilepsy, Neuroscience 76, 377–385.PubMedCrossRefGoogle Scholar
  48. Maguire-Zeiss, K.A., Li, Z.W., Shimoda, L.M.N. and Hamill, R.W, 1995, Calbindin D28k mRNA in hippocampus, superior temoral gyrus and cerebellum: Comparison between control and Alzheimer’s disease subjects, Mol. Brain Res. 30, 362–366.PubMedCrossRefGoogle Scholar
  49. Maki, M., Penta-EF-hand (PEF) proteins and calsenilin/DREAM: Involvement of the new EF-hand calcium-binding proteins in apoptosis and signal transduction, this book.Google Scholar
  50. Malhotra, A., 1994, Role of regulatory proteins (troponin-tropomyosin) in pathological states, Mol Cell Biochem. 135, 43–50.PubMedCrossRefGoogle Scholar
  51. Mariggio, M.A., Fulle, S., Calissano, P., Nicoletti, I. and Fano, G., 1994, The brain protein SlOOab inuces apoptosis in PC12 cells, Neurosci. 60, 29–35.CrossRefGoogle Scholar
  52. Mattson, M.P., 1997, Cellular actions of β-amyloid precursor protein and its soluble and fibrillogenic peptide derivatives, Physiol. Rev. 77, 1081–1132.PubMedGoogle Scholar
  53. Mattson, M.P., Rychlik, B., Chu, C. and Christakos S., 1991, Evidence for calcium reducing and excitoprotective roles for the calcium binding protein calbindin-D28k in hippocampal neurons, Neuron 6, 41–51.PubMedCrossRefGoogle Scholar
  54. Mattson, M.P., Chang, B., Baldwin, S., Smith-Swintosky, V.L., Keller, J., Geddes, J.V., Scheff, S.W. and Christakos, S., 1995, Brain injury and tumor necrosis factors induce calbindin-D28k in astrocytes: Evidence for a cytoprotective response, J. Neurosci. Res. 42, 357–370.PubMedCrossRefGoogle Scholar
  55. Mattson, M.P., Furukawa, K., Bruce, A.J., Mark, R.J. and Blanc, E.M., 1996, Calcium homeostasis and free radical metabolism as convergence points in the pathophysiology of dementia, in Molecular Mechanisms of Dementia, W. Wasco and R. E. Tanzi (eds.), Humana Press, Totowa, NJ, pp. 103–143.CrossRefGoogle Scholar
  56. Meier, T.J., Ho, D.Y. and Sapolsky, R.M., 1997, Increased expression of calbindin-D28k via hepes simplex virus amplicon vector decreases calcium ion mobilization and enhances neuronal survival after hypoglycemic challenge,. J. Neurochem. 69, 1039–1047.PubMedCrossRefGoogle Scholar
  57. Meldolesi, J. and Pozzan, T., 1998, The endoplasmic reticulum Ca2+ store: A view from the lumen, Trends Biol Sci. 23, 10–14.CrossRefGoogle Scholar
  58. Minghetti, P.P., Cancela, L., Fujisawa, Y., Theofan, G. and Norman, A.W, 1988, Molecular structure of the chicken vitamin D-induced calbindin-D28k gene reveals eleven exons, six Ca2+-binding domains and numerous promoter regulatory elements, Mol. Endocrinol. 2, 355–367.PubMedCrossRefGoogle Scholar
  59. Molinari, M. and Carafoli, E., 1997, Calpain: A cytosolic proteinase active at the membrane, J. Membr. Biol. 156, 1–8.PubMedCrossRefGoogle Scholar
  60. Montpied, P., Winsky, L., Dailey, J.W., Jobe, P.C. and Jacobowitz, D.M., 1995, Alteration in levels of expression of brain calbindin-D28k and calretinin mRNA in genetically epilepsy-prone rates, Epilepsia 36, 911–921.PubMedCrossRefGoogle Scholar
  61. Nagerl, U.V. and Mody, I., 1998, Calcium-dependent inactivation of high-threshold calcium currents in human dentate gyrus granule cells, J. Physiol. 509(1), 39–45.PubMedCrossRefGoogle Scholar
  62. Neamati, N., Fernandez, A., Wright, S., Kiefer, J. and McConkey, D.J., 1995, Degradation of lamin B1 precedes oligonucleosomal DNA in apoptotic thymocytes and isolated thymocyte nuclei, J. Immunol. 154, 3788–3795PubMedGoogle Scholar
  63. Nishimura, M., Yu, G. and St George-Hyslop, PH., 1999, Biology of presenilins as causitive molecules for Alzheimer disease, Clin. Genet. 55, 219–225.PubMedCrossRefGoogle Scholar
  64. Nixon, R.A., Saito, K.I., Grynspan, F., Griffin, W.R., Katayama, S., Honda, T., Mohan, P.S., Shea, T.B. and Beermann, M., 1994, Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer’s disease, Ann. NY Acad. Sci. 747, 77–91.PubMedCrossRefGoogle Scholar
  65. Ono, Y., Hata, S., Sorimachi, H. and Suzuki, K., Calcium and muscle disease: Pathophysiology of calpains and limb-girdle muscular distrophy Type 2a (LGMD2A), this book.Google Scholar
  66. Parmentier, M., Lawson, D.E. and Vassart, G., 1987, Human 27-kDa calbindin complementary DNA sequence. Evolutionary and functional implications, Eur. J. Biochem. 170, 207–215.PubMedCrossRefGoogle Scholar
  67. Pasteeis, J.L., Pochet, R., Surardt, L., Hubeau, C., Chirnoaga, M., Parmentier, M. and Lawson, D.E., 1986, Ultrastructural localization of brain ‘vitamin D-dependent’ calcium binding proteins, Brain Res. 384, 294–303.CrossRefGoogle Scholar
  68. Phillips, R.C., Meier, T.J., Giuli, L.C., McLaughlin, J.R., Ho, D.Y. and Sapolsky, R.M., 1999, Calbindin D28k gene transfer via herpes simplex virus amplicon vector decreases hippocampal damage in vivo following neurotoxic insults, J. Neurochem. 73, 1200–1205.PubMedCrossRefGoogle Scholar
  69. Rami, A., Rabie, A., Thomasset, M. and Krieglstein, J., 1992, Calbindin-D28k and ischemic damage of pyramidal cells in rat hippocampus, J. Neurosci. Res. 31, 89–95.PubMedCrossRefGoogle Scholar
  70. Reeves, R.H., 1994, Astrocytosis and axonal proliferation in the hippocampus of S100b transgenic mice, Proc. Natl. Acad. Sci. USA 91, 5359–5363.PubMedCrossRefGoogle Scholar
  71. Rogers, J.H., 1987, Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons, J. Cell Biol 105, 1343–1353.PubMedCrossRefGoogle Scholar
  72. Schafer, B.W. and Heizmann, C.W., 1996, The S100 family of EF-hand calcium binding proteins: Functions and pathology, Trends Biochem. Sci. 21, 134–140.PubMedGoogle Scholar
  73. Selinfreund, R.H., Barger, S.W., Pledger, W.J. and Van Eldik, L.J., 1991, Neurotrophic protein S100 stimulates glial cell proliferation, Proc. Natl Acad. Sci. USA 88, 3554–3558.PubMedCrossRefGoogle Scholar
  74. Strynadka, N.C.J, and James, M.N.G., 1989, Crystal structures of the helix-loop-helix calcium binding proteins, Annu. Rev. Biochem. 58, 951–998.PubMedCrossRefGoogle Scholar
  75. Suarez-Pinzon, W., Rabinovitch, A., Strynadka, K., Sooy, K. and Christakos, S., 1999, Cytokine mediated apoptotic destruction of pancreatic β cells, a cause of insulin dependent diabetes, is inhibited by calbindin-D28k, J. Bone Miner. Res. 14(Suppl. 1), S327.Google Scholar
  76. Sutherland, M.K., Wong, L., Somerville, M.J., Yoong, L.K.K., Bergeron, C., Parmentier, M. and McLachlan, D.R., 1993, Reduction of calbindin-28k mRNA levels in Alzheimer as compared to Huntington hippocampus, Mol. Brain Res. 18, 32–42.PubMedCrossRefGoogle Scholar
  77. Tufty, R.M. and Kretsinger, R.H., 1975, Troponin and parvalbumin calcium binding regions predicted in myosin light chain and T4 lysozyme, Science 187, 167–169.PubMedCrossRefGoogle Scholar
  78. Wang, K.K., Nath, R. and Posner, A., 1996, An alpha-mercapto acrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective, Proc. Natl. Acad. Sci. USA 93, 6687–6692.PubMedCrossRefGoogle Scholar
  79. Wasserman, R.H., 1985, Nomenclature of the vitamin D induced calcium binding proteins, in Vitamin D: Chemical, Biochemical and Clinical Update, A.W. Norman, K. Schaefer, H.G. Grigoleit and D.V. Herrath (eds.), de Gruyter, Berlin, pp. 321–322.Google Scholar
  80. Wernyj, R.P., Mattson, M.P. and Christakos, S., 1999, Expression of calbindin-D28k in C6 glial cells stabilizes intracellular calcium levels and protects against apoptosis induced by calcium ionophore and amyloid β-peptide, Mol. Brain Res. 64, 69–79.PubMedCrossRefGoogle Scholar
  81. Winningham-Major, F., Staecker, J.L., Barger, S.W., Coats, S. and Van Eldik, L.J., 1989, Neurite extension and neuronal survival activities of recombinant S100 proteins that differ in the content and position of cysteine residues, J. Cell. Biol. 109, 3036–3071.CrossRefGoogle Scholar
  82. Zamzami, N., Marchetti, P., Castedo, M., Hirsch, T., Susin, S.A., Mose, B. and Kroemer, G., 1996, Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis, FEBS Lett. 384, 53–57.PubMedCrossRefGoogle Scholar
  83. Zimmer, D.B., Cornwall, E.H., Landar, A. and Song, W, 1995, S100 protein family: Function and expression, Brain Res. Bull. 37, 417–429.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Sylvia Christakos
    • 1
  • Frank Barletta
    • 1
  • Michael Huening
    • 1
  • Jody Kohut
    • 1
  • Mihali Raval-Pandya
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyUMDNJ-New Jersey Medical SchoolNewarkUSA

Personalised recommendations