Astrocyte calcium microdomains are inhibited by Bafilomycin A1 and cannot be replicated by low-level Schaffer collateral stimulation in situ

Cell Calcium

Volumn 55, Issue 1, 2014, Pages 1-16

  Sun, Min Yu ^a,b   Devaraju, Prakash ^a   Xie, Alison Xiaoqiao ^a   Holman, Isabelle ^a   Samones, Emmelyn ^a   Murphy, Thomas R ^a   Fiacco, Todd A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Bafilomycin A1; Calcium; Group I mGluRs; MEPSC

Indexed keywords

BAFILOMYCIN A1; CALCIUM ION; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; METABOTROPIC RECEPTOR 1; POTASSIUM ION; TETRODOTOXIN; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MEMBRANE; CELL MICRODOMAIN; CELL SIZE; COMPARATIVE STUDY; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; INTRACELLULAR SIGNALING; LATENT PERIOD; MOLECULAR DYNAMICS; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REPRODUCIBILITY; SCHAFFER COLLATERAL; SENSORY NERVE CELL; SOMATIC CELL; STRATUM RADIATUM; SYNAPSE VESICLE; WHOLE CELL PATCH CLAMP; ANIMAL TISSUE; BRAIN SLICE; CELL ACTIVITY; CELL ASSAY; CELL COMPARTMENTALIZATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; HIPPOCAMPUS; NERVE POTENTIAL; POLYMERASE CHAIN REACTION; QUALITATIVE ANALYSIS; SCHAFFER COLLATERAL STIMULATION;

BAFILOMYCIN A1; CALCIUM; GROUP I MGLURS; MEPSC;

ACTION POTENTIALS; ANIMALS; ASTROCYTES; CALCIUM; CALCIUM SIGNALING; ENZYME INHIBITORS; GLUTAMIC ACID; MACROLIDES; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS;

EID: 84896736690     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2013.10.004     Document Type: Article

References (52)

1. Fatatis A., Russell J.T. Spontaneous changes in intracellular calcium concentration in type I astrocytes from rat cerebral cortex in primary culture. Glia 1992, 5:95-104.
2. Charles A.C. Glia-neuron intercellular calcium signaling. Dev. Neurosci. 1994, 16:196-206.
3. Harris-White M.E., Zanotti S.A., Frautschy S.A., Charles A.C. Spiral intercellular calcium waves in hippocampal slice cultures. J. Neurophysiol. 1998, 79:1045-1052.
4. 2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat. Neurosci. 2001, 4:803-812.
5. Aguado F., Espinosa-Parrilla J.F., Carmona M.A., Soriano E. Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J. Neurosci. 2002, 22:9430-9444.
6. Nett W.J., Oloff S.H., McCarthy K.D. Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J. Neurophysiol. 2002, 87:528-537.
7. 2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 2011, 14:1276-1284.
8. Hirase H., Qian L., Bartho P., Buzsaki G. Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 2004, 2:E96.
9. Nimmerjahn A., Kirchhoff F., Kerr J.N., Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 2004, 1:31-37.
10. 2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 2006, 9:816-823.
11. 2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J. Neurosci. 2008, 28:4967-4973.
12. Takata N., Mishima T., Hisatsune C., Nagai T., Ebisui E., Mikoshiba K., Hirase H. Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J. Neurosci. 2011, 31:18155-18165.
13. Agulhon C., Petravicz J., McMullen A.B., Sweger E.J., Minton S.K., Taves S.R., Casper K.B., Fiacco T.A., McCarthy K.D. What is the role of astrocyte calcium in neurophysiology?. Neuron 2008, 59:932-946.
14. Carmignoto G., Pasti L., Pozzan T. On the role of voltage-dependent calcium channels in calcium signaling of astrocytes in situ. J. Neurosci. 1998, 18:4637-4645.
15. Agulhon C., Sun M.Y., Murphy T., Myers T., Lauderdale K., Fiacco T.A. Calcium Signaling and Gliotransmission in Normal vs. reactive astrocytes. Front. Pharmacol. 2012, 3:139.
16. 2+ oscillations. Neuroscience 2003, 120:979-992.
17. Zur Nieden R., Deitmer J.W. The role of metabotropic glutamate receptors for the generation of calcium oscillations in rat hippocampal astrocytes in situ. Cereb. Cortex 2006, 16:676-687.
18. Porter J.T., McCarthy K.D. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 1996, 16:5073-5081.
19. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat. Neurosci. 1999, 2:44-49.
20. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
21. Araque A., Li N., Doyle R.T., Haydon P.G. SNARE protein-dependent glutamate release from astrocytes. J. Neurosci. 2000, 20:666-673.
22. Zhou Q., Petersen C.C., Nicoll R.A. Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol 2000, 525(Pt 1):195-206.
23. de Ligt R.A., Kourounakis A.P., Ijzerman A.P. Inverse agonism at G protein-coupled receptors: (patho)physiological relevance and implications for drug discovery. Br. J. Pharmacol. 2000, 130:1-12.
24. Hermans E., Challiss R.A. Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors: prototypic family C G-protein-coupled receptors. Biochem. J. 2001, 359:465-484.
25. Panatier A., Vallee J., Haber M., Murai K.K., Lacaille J.C., Robitaille R. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 2011, 146:785-798.
26. Nizar K., et al. In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J. Neurosci. 2013, 33:8411-8422.
27. Fiacco T.A., McCarthy K.D. Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J. Neurosci. 2004, 24:722-732.
28. Xie A.X., Sun M.Y., Murphy T., Lauderdale K., Tiglao E., Fiacco T.A. Bidirectional scaling of astrocytic metabotropic glutamate receptor signaling following long-term changes in neuronal firing rates. PLoS ONE 2012, 7:e49637.
29. Honsek S.D., Walz C., Kafitz K.W., Rose C.R. Astrocyte calcium signals at Schaffer collateral to CA1 pyramidal cell synapses correlate with the number of activated synapses but not with synaptic strength. Hippocampus 2012, 22:29-42.
30. Honsek S.D., Walz C., Kafitz K.W., Rose C.R. Astrocyte calcium signals at Schaffer collateral to CA1 pyramidal cell synapses correlate with the number of activated synapses but not with synaptic strength. Hippocampus 2012, 22:29-42.
31. Takahashi A., Camacho P., Lechleiter J.D., Herman B. Measurement of intracellular calcium. Physiol. Rev. 1999, 79:1089-1125.
32. Devaraju P., Sun M.Y., Myers T.L., Lauderdale K., Fiacco T.A. Astrocytic group I mGluR-dependent potentiation of astrocytic glutamate and potassium uptake. J. Neurophysiol. 2013, 109:2404-2414.
33. Zur Nieden R., Deitmer J.W. The role of metabotropic glutamate receptors for the generation of calcium oscillations in rat hippocampal astrocytes in situ. Cereb. Cortex 2006, 16:676-687.
34. Garaschuk O., Milos R.I., Konnerth A. Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat. Protoc. 2006, 1:380-386.
35. Bernardinelli Y., Salmon C., Jones E.V., Farmer W.T., Stellwagen D., Murai K.K. Astrocytes display complex and localized calcium responses to single-neuron stimulation in the hippocampus. J. Neurosci. 2011, 31:8905-8919.
36. Raastad M., Storm J.F., Andersen P. Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 1992, 4:113-117.
37. Bergles D.E., Jahr C.E. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 1997, 19:1297-1308.
38. Milligan G. Constitutive activity and inverse agonists of G protein-coupled receptors: a current perspective. Mol. Pharmacol. 2003, 64:1271-1276.
39. Bond R.A., Ijzerman A.P. Recent developments in constitutive receptor activity and inverse agonism, and their potential for GPCR drug discovery. Trends Pharmacol. Sci. 2006, 27:92-96.
40. Porter J.T., McCarthy K.D. Astrocytic neurotransmitter receptors in situ and in vivo. Prog. Neurobiol. 1997, 51:439-455.
41. 2+-elevating muscarinic cholinergic and histaminergic receptors in situ. J. Neurochem. 2000, 74:555-563.
42. 2+ elevations in astrocytes in hippocampal slices. J. Neurosci. 2002, 22:2443-2450.
43. Oka M., Wada M., Wu Q., Yamamoto A., Fujita T. Functional expression of metabotropic GABAB receptors in primary cultures of astrocytes from rat cerebral cortex. Biochem. Biophys. Res. Commun. 2006, 341:874-881.
44. Serrano A., Haddjeri N., Lacaille J.C., Robitaille R. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J. Neurosci. 2006, 26:5370-5382.
45. Bekar L.K., He W., Nedergaard M. Locus coeruleus alpha-adrenergic-mediated activation of cortical astrocytes in vivo. Cereb. Cortex 2008, 18:2789-2795.
46. Navarrete M., Araque A. Endocannabinoids mediate neuron-astrocyte communication. Neuron 2008, 57:883-893.
47. Hertz L., Lovatt D., Goldman S.A., Nedergaard M. Adrenoceptors in brain: cellular gene expression and effects on astrocytic metabolism and [Ca(2+)]i. Neurochem. Int. 2010, 57:411-420.
48. Dombeck D.A., Khabbaz A.N., Collman F., Adelman T.L., Tank D.W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 2007, 56:43-57.
49. Schummers J., Yu H., Sur M. Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 2008, 320:1638-1643.
50. Navarrete M., Perea G., Fernandez de Sevilla D., Gomez-Gonzalo M., Nunez A., Martin E.D., Araque A. Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol. 2012, 10:e1001259.
51. Patrushev I., Gavrilov N., Turlapov V., Semyanov A. Subcellular location of astrocytic calcium stores favors extrasynaptic neuron-astrocyte communication. Cell Calcium 2013, 54:343-349.
52. Fiacco T.A., Agulhon C., Taves S.R., Petravicz J., Casper K.B., Dong X., Chen J., McCarthy K.D. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 2007, 54:611-626.