Calbindin-D(28k) falls to protect hippocampal neurons against ischemia in spite of its cytoplasmic calcium buffering properties: Evidence from calbindin-D(28k) knockout mice

Neuroscience

Volumn 85, Issue 2, 1998, Pages 361-373

  Klapstein, G J ^a   Vietla, S ^a   Lieberman, D N ^a   Gray, P A ^a   Airaksinen, M S ^b   Thoenen, H ^b   Meyer, M ^b   Mody, I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Apoptosis; Calcium buffering; Ischemia hypoxia; Neuronal vulnerability; Oxygen glucose deprivation; TUNEL

Indexed keywords

BUFFER; CALBINDIN; CALCIUM; CALCIUM BINDING PROTEIN; GLUCOSE; OXYGEN; ION CHANNEL; N METHYLASPARTIC ACID; NERVE PROTEIN;

ACTION POTENTIAL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE; HIPPOCAMPUS; ISCHEMIA; MOUSE; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; ANIMAL; BRAIN ISCHEMIA; CYTOPLASM; DRUG EFFECT; IN VITRO STUDY; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PATHOLOGY; VASCULARIZATION;

ANIMALS; BRAIN ISCHEMIA; BUFFERS; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CYTOPLASM; GLUCOSE; HIPPOCAMPUS; ION CHANNELS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; OXYGEN;

EID: 0032107048     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00632-5     Document Type: Article

References (55)

1. Airaksinen M. S., Eilers J., Garaschuk O., Thoenen H., Konnerth A., Meyer M. Ataxia and altered dendritic calcium signalling in mice carrying a targeted nullmutation of the calbindin-D28k gene. Proc. natn. Acad. Sci. U.S.A. 94:1997;1488-1493.
2. 28k-deficient mice: lack of evidence for a neuroprotective role of endogenous calbindin in MPTP-treated and weaver mice. Eur. J. Neurosci. 9:1997;120-127.
3. Baimbridge K. G. Calcium-binding proteins in the dentate gyrus. Epilepsy Res. 7(Suppl.):1992;211-220.
4. Baimbridge K. G., Celio M. R., Rogers J. H. Calcium-binding proteins in the nervous system. Trends Neurosci. 15:1992;303-308.
5. Barone F. C., Knudsen D. J., Nelson A. H., Feuerstein G. Z., Willette R. N. Mouse strain differences in susceptibility to cerebral ischemia are related to cerebral vascular anatomy. J. cerebr. Blood Flow Metab. 13:1993;683-692.
6. Bielefeldt K., Jackson M. B. A calcium-activated potassium channel causes frequency-dependent action-potential failures in a mammalian nerve terminal. J. Neurophysiol. 70:1993;284-298.
7. 28k and parvalbumin in rat sensory neurones. J. Physiol., Lond. 472:1993;341-357.
8. Chard P. S., Jordan J., Marcuccilli C. J., Miller R. J., Leiden J. M., Roos R. P., Ghadge G. D. Regulation of excitatory transmission at hippocampal synapses by calbindin D28k. Proc. natn. Acad. Sci. U.S.A. 92:1995;5144-5148.
9. Charriaut-Marlangue C., Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. NeuroReport. 7:1995;61-64.
10. Cheng B., Christakos S., Mattson M. P. Tumor necrosis factors protect neurons against metabolic- excitotoxic insults and promote maintenance of calcium homeostasis. Neuron. 12:1994;139-153.
11. Choi D. W. Calcium and excitotoxic neuronal injury. Ann. N.Y. Acad. Sci. 747:1994;162-171.
12. Choi D. W. Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18:1995;58-60.
13. Ehlers M. D., Zhang S., Bernhardt J. P., Huganir R. L. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell. 84:1996;745-755.
14. Freund T. F., Buzsáki G., Leon A., Baimbridge K. G., Somogyi P. Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Expl Brain Res. 83:1990;55-66.
15. Gavrieli Y., Sherman Y., Ben-Sasson S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
16. Ghosh A., Greenberg M. E. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 268:1995;239-247.
17. Goodman J. H., Wasterlain C. G., Massarweh W. F., Dean E., Sollas A. L., Sloviter R. S. Calbindin-D28k immunoreactivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat. Brain Res. 606:1993;309-314.
18. 28K cDNA prevents amyotrophic lateral sclerosis IgG-mediated cytotoxicity. Proc. natn. Acad. Sci. U.S.A. 93:1996;6796-6801.
19. Honkaniemi J., Massa S. M., Breckinridge M., Sharp F. R. Global ischemia induces apoptosis-associated genes in hippocampus. Molec. Brain Res. 42:1996;79-88.
20. Huang Z., Huang P. L., Panahian N., Dalkara T., Fishman M. C., Moskowitz M. A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
21. Hyrc K., Handran S. D., Rothman S. M., Goldberg M. P. Ionized intracellular calcium concentration predicts excitotoxic neuronal death: observations with low-affinity fluorescent calcium indicators. J. Neurosci. 17:1997;6669-6677.
22. Iacopino A. M., Christakos S., German D., Sonsalla P. K., Altar C. A. Calbindin-D28K-containing neurons in animal models of neurodegeneration: possible protection from excitotoxicity. Molec. Brain Res. 13:1992;251-261.
23. Isayama K., Pitts L. H., Nishimura M. C. Evaluation of 2,3,5-triphenyltetrazolium chloride staining to delineate rat brain infarcts. Stroke. 22:1991;1394-1398.
24. Köhr G., De Koninck Y., Mody I. Properties of NMDA receptor channels in neurons acutely isolated from epileptic (kindled) rats. J. Neurosci. 13:1993;3612-3627.
25. Köhr G., Mody I. Endogenous intracellular calcium buffering and the activation/inactivation of HVA calcium currents in rat dentate gyrus granule cells. J. gen. Physiol. 98:1991;941-967.
26. 28k: role in determining intrinsically generated firing patterns in rat supraoptic neurones. J. Physiol., Lond. 488:1995;601-608.
27. 2+-dependent phosphatase. Nature. 369:1994;235-239.
28. Lledo P. M., Somasundaram B., Morton A. J., Emson P. C., Mason W. T. Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron. 9:1992;943-954.
29. 2+-sensitive outward current in a vertebrate neurone. Nature. 300:1982;185-188.
30. Martin R. L., Lloyd H. G., Cowan A. I. The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends Neurosci. 17:1994;251-257.
31. Mattson M. P., Rychlik B., Chu C., Christakos S. Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron. 6:1991;41-51.
32. Medina I., Filippova N., Bakhramov A., Bregestovski P. Calcium-induced inactivation of NMDA receptor-channels evolves independently of run-down in cultured rat brain neurones. J. Physiol., Lond. 495:1996;411-427.
33. Medina I., Filippova N., Charton G., Rougeole S., Ben-Ari Y., Khrestchatisky M., Bregestovski P. Calcium-dependent inactivation of heteromeric NMDA receptor-channels expressed in human embryonic kidney cells. J. Physiol., Lond. 482:1995;567-573.
34. Meldrum B. S. Cytoprotective therapies in stroke. Curr. Opin. Neurol. 8:1995;15-23.
35. 2+ homeostasis. Prog. Neurobiol. 37:1991;255-285.
36. Mockel V., Fischer G. Vulnerability to excitotoxic stimuli of cultured rat hippocampal neurons containing the calcium-binding proteins calretinin and calbindin D28K. Brain Res. 648:1994;109-120.
37. 2+ release. Trends pharmac. Sci. 16:1995;356-359.
38. Panahian N., Yoshida T., Huang P. L., Hedley-Whyte E. T., Dalkara T., Fishman M. C., Moskowitz M. A. Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience. 72:1996;343-354.
39. Pochet R., Lawson D. E. M. and Heizmann C. W., eds. (1990) Calcium binding proteins in normal and transformed cells. Adv. exp. Med. Biol. Vol. 269, 1-223. Plenum, New York.
40. Protti D. A., Uchitel O. D. P/Q-type calcium channels activate neighboring calcium-dependent potassium channels in mouse motor nerve terminals. Pflügers Arch. 434:1997;406-412.
41. Regehr W. G., Delaney K. R., Tank D. W. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14:1994;523-537.
42. Riedel G. Function of metabotropic glutamate receptors in learning and memory. Trends Neurosci. 19:1996;219-224.
43. Roberts W. M., Jacobs R. A., Hudspeth A. J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10:1990;3664-3684.
44. Robitaille R., Garcia M. L., Kaczorowski G. J., Charlton M. P. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron. 11:1993;645-655.
45. Schmidt-Kastner R., Freund T. F. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience. 40:1991;599-636.
46. Sloviter R. S. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. comp. Neurol. 280:1989;183-196.
47. Staley K. J., Otis T. S., Mody I. Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J. Neurophysiol. 67:1992;1346-1358.
48. Storm J. F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83:1990;161-187.
49. Tank D. W., Regehr W. G., Delaney K. R. A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. J. Neurosci. 15:1995;7940-7952.
50. Tong G., Shepherd D., Jahr C. E. Synaptic desensitization of NMDA receptors by calcineurin. Science. 267:1995;1510-1512.
51. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron. 11:1993;221-235.
52. Velisek L., Moshe S. L., Stanton P. K. Resistance of hippocampal synaptic transmission to hypoxia in carbonic anhydrase II-deficient mice. Brain Res. 671:1995;245-253.
53. 2+ oscillations. Biophys. J. 67:1994;447-456.
54. Yang G., Kitagawa K., Matsushita K., Mabuchi T., Yagita Y., Yanagihara T., Matsumoto M. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Res. 752:1997;209-218.
55. Zhou Z., Neher E. Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J. Physiol., Lond. 469:1993;245-273.