Home LiteratureArticle Details
PMID: 9348342 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Activity-dependent calcium sequestration in dendrites of hippocampal neurons in brain slices.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 17 ·No. 22 ·1997-11-15 ·Pages 8729-38

Pozzo-Miller LD, Pivovarova NB, Leapman RD, Buchanan RA, Reese TS, Andrews SB

Abstract

Synaptic activity-dependent changes in the spatio-temporal distribution of calcium ions regulate important neuronal functions such as dendritic integration and synaptic plasticity, but the processes that terminate the free Ca2+ transients associated with these changes remain unclear. We have characterized at the electron microscopic level the intracellular compartments involved in buffering free Ca2+ transients in dendritic cytoplasm of CA3 neurons by measuring the larger changes in the concentrations of total Ca that persist for several minutes after neuronal activity. Quantitative energy-dispersive x-ray microanalysis of cryosections from hippocampal slice cultures rapidly frozen 3 min after afferent synaptic activity identified a subset of dendritic endoplasmic reticulum (ER) as a high-capacity Ca2+ buffer. Calcium sequestration by cisterns of this subset of ER was graded, reversible, and dependent on a thapsigargin-sensitive Ca2+-ATPase. Sequestration was so robust that after repetitive high-frequency stimulation the Ca content of responsive ER cisterns increased as much as 20-fold. These results demonstrate that a subpopulation of ER is the major dendritic Ca sequestration compartment in the minutes after neuronal activity.

MeSH Terms
Animals Calcium/metabolism Calcium-Transporting ATPases/metabolism Cell Compartmentation/physiology Dendrites/enzymology,ultrastructure Electron Probe Microanalysis Endoplasmic Reticulum/metabolism Excitatory Postsynaptic Potentials/physiology Fluorescent Dyes Hippocampus/cytology,metabolism Neurons/enzymology,ultrastructure Organ Culture Techniques Rats Synapses/chemistry,physiology
Chemicals
Fluorescent Dyes Calcium-Transporting ATPases Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Pozzo-Miller L D
Laboratory of Neurobiology, National Institute of Neurological Diseases and Stroke, National Institutes of Health, Bethesda, Maryland 20892, USA.
Pivovarova N B
Leapman R D
Buchanan R A
Reese T S
Andrews S B
References (53)
53 references, click to expand
  1. Localization of calcium in presynaptic nerve terminals. An ultrastructural and electron microprobe analysis.
    J Cell Biol. 1980 May;85(2):228-41 PMID: 7372706
  2. Calcium transport and buffering in neurons.
    Trends Neurosci. 1988 Oct;11(10):438-43 PMID: 2469161
  3. A reevaluation of the role of mitochondria in neuronal Ca2+ homeostasis.
    J Neurochem. 1996 Jan;66(1):403-11 PMID: 8522981
  4. ELECTRON MICROSCOPY AFTER RAPID FREEZING ON A METAL SURFACE AND SUBSTITUTION FIXATION.
    Anat Rec. 1964 Jul;149:381-5 PMID: 14208983
  5. Cytoplasmic structure in organotypic cultures of rat hippocampus prepared by rapid freezing and freeze-substitution fixation.
    Synapse. 1993 Mar;13(3):195-205 PMID: 8497806
  6. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat.
    J Neurosci. 1997 Jan 1;17(1):190-203 PMID: 8987748
  7. Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones.
    J Physiol. 1997 Jul 1;502 ( Pt 1):13-30 PMID: 9234194
  8. Quantitative dark-field mass analysis of ultrathin cryosections in the field-emission scanning transmission electron microscope.
    Scanning Microsc Suppl. 1994;8:13-23; discussion 23-4 PMID: 7638482
  9. Calcium signalling in neurons.
    Trends Neurosci. 1988 Oct;11(10):415-9 PMID: 2469157
  10. Calcium channels, stores, and oscillations.
    Annu Rev Cell Biol. 1990;6:715-60 PMID: 2177344
  11. Ca2+ release from intracellular stores induced by afferent stimulation of CA3 pyramidal neurons in hippocampal slices.
    J Neurophysiol. 1996 Jul;76(1):554-62 PMID: 8836243
  12. Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7510-4 PMID: 7519781
  13. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons.
    Nature. 1992 May 21;357(6375):244-6 PMID: 1350327
  14. Activity-dependent accumulation of calcium in Purkinje cell dendritic spines.
    Proc Natl Acad Sci U S A. 1988 Mar;85(5):1682-5 PMID: 3422755
  15. An FCCP-sensitive Ca2+ store in bullfrog sympathetic neurons and its participation in stimulus-evoked changes in [Ca2+]i.
    J Neurosci. 1994 Jul;14(7):4007-24 PMID: 8027759
  16. Inositol 1,4,5-trisphosphate receptors: immunohistochemical localization to discrete areas of rat central nervous system.
    Neuroscience. 1993 Apr;53(4):927-42 PMID: 8389431
  17. Calcium content of mitochondria and endoplasmic reticulum in liver frozen rapidly in vivo.
    Nature. 1985 Apr 18-24;314(6012):622-5 PMID: 3990795
  18. Tetrodotoxin-resistant sodium channels.
    Cell Mol Neurobiol. 1994 Jun;14(3):227-44 PMID: 7712513
  19. A simple method for organotypic cultures of nervous tissue.
    J Neurosci Methods. 1991 Apr;37(2):173-82 PMID: 1715499
  20. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons.
    J Physiol. 1995 May 15;485 ( Pt 1):1-20 PMID: 7658365
  21. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels.
    Neuron. 1992 Dec;9(6):1163-73 PMID: 1361128
  22. The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons.
    Mol Biol Cell. 1995 Oct;6(10):1315-32 PMID: 8573789
  23. Mitochondria and Na+/Ca2+ exchange buffer glutamate-induced calcium loads in cultured cortical neurons.
    J Neurosci. 1995 Feb;15(2):1318-28 PMID: 7869100
  24. Optical imaging of cytosolic calcium, electrophysiology, and ultrastructure in pyramidal neurons of organotypic slice cultures from rat hippocampus.
    Neuroimage. 1993 Sep;1(2):109-20 PMID: 9343562
  25. Spatially and functionally distinct Ca2+ stores in sarcoplasmic and endoplasmic reticulum.
    Science. 1997 Mar 14;275(5306):1643-8 PMID: 9054358
  26. Molecular and cellular physiology of intracellular calcium stores.
    Physiol Rev. 1994 Jul;74(3):595-636 PMID: 8036248
  27. Calcium-containing organelles display unique reactivity to chemical stimulation in cultured hippocampal neurons.
    J Neurosci. 1997 Mar 1;17(5):1670-82 PMID: 9030626
  28. Intracellular calcium homeostasis.
    Annu Rev Biochem. 1987;56:395-433 PMID: 3304139
  29. Characteristics and function of Ca(2+)- and inositol 1,4,5-trisphosphate-releasable stores of Ca2+ in neurons.
    Neuroscience. 1992;46(2):251-73 PMID: 1311812
  30. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites.
    Science. 1995 Apr 14;268(5208):297-300 PMID: 7716524
  31. Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells.
    Neuron. 1996 Jan;16(1):219-28 PMID: 8562086
  32. The control of neuronal Ca2+ homeostasis.
    Prog Neurobiol. 1991;37(3):255-85 PMID: 1947178
  33. Endoplasmic reticulum sequesters calcium in the squid giant axon.
    Science. 1978 Dec 22;202(4374):1300-3 PMID: 725607
  34. Dual action of thapsigargin on calcium mobilization in sensory neurons: inhibition of Ca2+ uptake by caffeine-sensitive pools and blockade of plasmalemmal Ca2+ channels.
    Neuroscience. 1995 Apr;65(4):1109-18 PMID: 7617166
  35. Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons.
    J Neurophysiol. 1995 Sep;74(3):1335-42 PMID: 7500154
  36. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria.
    Science. 1993 Oct 29;262(5134):744-7 PMID: 8235595
  37. Micromolar Ca2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice.
    Neuron. 1995 Jun;14(6):1223-31 PMID: 7605633
  38. Neuronal Ca2+ stores: activation and function.
    Trends Neurosci. 1995 Jul;18(7):299-306 PMID: 7571010
  39. Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons.
    J Neurosci. 1994 Jan;14(1):348-56 PMID: 8283242
  40. Inositol 1,4,5-trisphosphate and ryanodine receptor distributions and patterns of acetylcholine- and caffeine-induced calcium release in cultured mouse hippocampal neurons.
    J Neurosci. 1995 Apr;15(4):2592-608 PMID: 7722617
  41. Quantitative scanning transmission electron microscopy of ultrathin cryosections: subcellular organelles in rapidly frozen liver and cerebellar cortex.
    J Struct Biol. 1993 May-Jun;110(3):244-55 PMID: 8373705
  42. Thickness measurement of hydrated and dehydrated cryosections by EELS.
    Microsc Res Tech. 1996 Feb 15;33(3):241-50 PMID: 8652882
  43. Mitochondrial participation in the intracellular Ca2+ network.
    J Cell Biol. 1997 Feb 24;136(4):833-44 PMID: 9049249
  44. Characterization of Ca2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors.
    J Physiol. 1993 Sep;469:693-716 PMID: 8271224
  45. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release.
    J Cell Biol. 1979 May;81(2):275-300 PMID: 38256
  46. Glutamate impairs neuronal calcium extrusion while reducing sodium gradient.
    Neuron. 1994 Feb;12(2):295-300 PMID: 7906528
  47. Calcium-induced calcium release in cerebellar Purkinje cells.
    Neuron. 1994 Mar;12(3):663-73 PMID: 7512352
  48. The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation.
    Neuron. 1993 Nov;11(5):817-23 PMID: 7902109
  49. Quantitative electron probe microanalysis of biological thin sections: methods and validity.
    Ultramicroscopy. 1976 Sep-Oct;1(4):317-39 PMID: 1028201
  50. The localization and assay of chemical elements by microprobe methods.
    Q Rev Biophys. 1983 Aug;16(3):279-339 PMID: 6322217
  51. Three-dimensional visualization of the smooth endoplasmic reticulum in Purkinje cell dendrites.
    J Neurosci. 1993 Nov;13(11):4636-46 PMID: 8229189
  52. Elemental distribution in striated muscle and the effects of hypertonicity. Electron probe analysis of cryo sections.
    J Cell Biol. 1977 Sep;74(3):828-57 PMID: 302837
  53. Analysis of directly frozen macromolecules and tissues in the field-emission STEM.
    J Microsc. 1991 Jan;161(Pt 1):3-19 PMID: 2016736
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-11-15
Pages
8729-38
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573076
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2