Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway

Neuron

Volumn 82, Issue 2, 2014, Pages 413-429

  Haustein, Martin D ^a   Kracun, Sebastian ^a   Lu, Xiao Hong ^b   Shih, Tiffany ^c   Jackson Weaver, Olan ^a   Tong, Xiaoping ^a   Xu, Ji ^a   Yang, X William ^b   O'Dell, Thomas J ^a   Marvin, Jonathan S ^d   Ellisman, Mark H ^c   Bushong, Eric A ^c   Looger, Loren L ^d   Khakh, Baljit S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIALS; ANIMALS; ASTROCYTES; CALCIUM SIGNALING; EXCITATORY AMINO ACID AGENTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOSSY FIBERS, HIPPOCAMPAL; RECEPTORS, GABA-B; RECEPTORS, METABOTROPIC GLUTAMATE; SODIUM CHANNEL BLOCKERS;

EID: 84898688510     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.02.041     Document Type: Article

References (47)

1. 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.
2. Agulhon C., Fiacco T.A., McCarthy K.D. Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 2010, 327:1250-1254.
3. 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. 10.3389/fphar.2012.00139.
4. Amaral D., Lavenex P. Hippocampal neuroanatomy. The Hippocampus Book, Chapter 3 2007, 37-114. Oxford University Press, Oxford. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
5. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
6. Caiati M.D. Is GABA co-released with glutamate from hippocampal mossy fiber terminals?. J.Neurosci. 2013, 33:1755-1756.
7. Chen T.W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
8. D'Ascenzo M., Fellin T., Terunuma M., Revilla-Sanchez R., Meaney D.F., Auberson Y.P., Moss S.J., Haydon P.G. mGluR5 stimulates gliotransmission in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 2007, 104:1995-2000.
9. Deerinck T.J., Bushong E.A., Lev-Ram V., Shu X., Tsien R.Y., Ellisman M.H. Enhancing serial block-face scanning electron microscopy to enable high resolution 3-D nanohistology of cells and tissues. Microsc. Microanal. 2010, 16:1138-1139. 10.1017/S1431927610055170.
10. Di Castro M.A., Chuquet J., Liaudet N., Bhaukaurally K., Santello M., Bouvier D., Tiret P., Volterra A. Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 2011, 14:1276-1284.
11. 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 insitu does not affect neuronal excitatory synaptic activity. Neuron 2007, 54:611-626.
12. Gordon G.R., Iremonger K.J., Kantevari S., Ellis-Davies G.C., MacVicar B.A., Bains J.S. Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 2009, 64:391-403.
13. Gutiérrez R. The dual glutamatergic-GABAergic phenotype of hippocampal granule cells. Trends Neurosci. 2005, 28:297-303.
14. Huang Y.H., Sinha S.R., Tanaka K., Rothstein J.D., Bergles D.E. Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J.Neurosci. 2004, 24:4551-4559.
15. Kanai Y., Clémençon B., Simonin A., Leuenberger M., Lochner M., Weisstanner M., Hediger M.A. The SLC1 high-affinity glutamate and neutral amino acid transporter family. Mol. Aspects Med. 2013, 34:108-120.
16. Kang J., Jiang L., Goldman S.A., Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1998, 1:683-692.
17. Khakh B.S., North R.A. Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 2012, 76:51-69.
18. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J.Struct. Biol. 1996, 116:71-76.
19. Kuffler S.W. Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on the glial membrane potential. Proc. R. Soc. Lond. B Biol. Sci. 1967, 168:1-21.
20. Li X., Zima A.V., Sheikh F., Blatter L.A., Chen J. Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1,4,5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ. Res. 2005, 96:1274-1281.
21. Li D., Agulhon C., Schmidt E., Oheim M., Ropert N. New toolsfor investigating astrocyte-to-neuron communication. Front. Cell Neurosci 2013, 7:193.
22. Marvin J.S., Borghuis B.G., Tian L., Cichon J., Harnett M.T., Akerboom J., Gordus A., Renninger S.L., Chen T.W., Bargmann C.I., et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 2013, 10:162-170.
23. Panatier A., Vallée 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.
24. Petravicz J., Fiacco T.A., McCarthy K.D. Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J.Neurosci. 2008, 28:4967-4973.
25. Reeves A.M., Shigetomi E., Khakh B.S. Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps. J.Neurosci. 2011, 31:9353-9358.
26. Regan M.R., Huang Y.H., Kim Y.S., Dykes-Hoberg M.I., Jin L., Watkins A.M., Bergles D.E., Rothstein J.D. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J.Neurosci. 2007, 27:6607-6619.
27. Richler E., Chaumont S., Shigetomi E., Sagasti A., Khakh B.S. Tracking transmitter-gated P2X cation channel activation invitro and invivo. Nat. Methods 2008, 5:87-93.
28. Rollenhagen A., Lübke J.H. The morphology of excitatory central synapses: from structure to function. Cell Tissue Res. 2006, 326:221-237.
29. Rollenhagen A., Sätzler K., Rodríguez E.P., Jonas P., Frotscher M., Lübke J.H. Structural determinants of transmission at large hippocampal mossy fiber synapses. J.Neurosci. 2007, 27:10434-10444.
30. Rothstein J.D., Dykes-Hoberg M., Pardo C.A., Bristol L.A., Jin L., Kuncl R.W., Kanai Y., Hediger M.A., Wang Y., Schielke J.P., Welty D.F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996, 16:675-686.
31. Ruiz A.J., Kullmann D.M. Ionotropic receptors at hippocampal mossy fibers: roles in axonal excitability, synaptic transmission, and plasticity. Front. Neural Circuits 2012, 6:112. Published online Jan 9, 2013. 10.3389/fncir.2012.00112.
32. Rusakov D.A., Zheng K., Henneberger C. Astrocytes as regulators of synaptic function: a quest for the Ca2+ master key. Neuroscientist 2011, 17:513-523.
33. Shigetomi E., Bowser D.N., Sofroniew M.V., Khakh B.S. Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J.Neurosci. 2008, 28:6659-6663.
34. Shigetomi E., Kracun S., Sofroniew M.V., Khakh B.S. A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat. Neurosci. 2010, 13:759-766.
35. Shigetomi E., Tong X., Kwan K.Y., Corey D.P., Khakh B.S. TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat. Neurosci. 2011, 15:70-80.
36. Shigetomi E., Bushong E.A., Haustein M.D., Tong X., Jackson-Weaver O., Kracun S., Xu J., Sofroniew M.V., Ellisman M.H., Khakh B.S. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J.Gen. Physiol. 2013, 141:633-647.
37. Shigetomi E., Jackson-Weaver O., Huckstepp R.T., O'Dell T.J., Khakh B.S. TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J.Neurosci. 2013, 33:10143-10153.
38. Spruston N., McBain C. Structural and functional properties of hippocampal neurons. The Hippocampus Book 2007, Oxford University Press, Oxford. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
39. Sun W., McConnell E., Pare J.F., Xu Q., Chen M., Peng W., Lovatt D., Han X., Smith Y., Nedergaard M. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 2013, 339:197-200.
40. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 2009, 6:875-881.
41. Tian L., Akerboom J., Schreiter E.R., Looger L.L. Neural activity imaging with genetically encoded calcium indicators. Prog. Brain Res. 2012, 196:79-94.
42. Tong X., Shigetomi E., Looger L.L., Khakh B.S. Genetically encoded calcium indicators and astrocyte calcium microdomains. Neuroscientist 2013, 19:274-291.
43. Walker M.C., Ruiz A., Kullmann D.M. Do mossy fibers release GABA?. Epilepsia 2002, 43(Suppl 5):196-202.
44. Wang X., Lou N., Xu Q., Tian G.F., Peng W.G., Han X., Kang J., Takano T., Nedergaard M. Astrocytic Ca2+ signaling evoked by sensory stimulation invivo. Nat. Neurosci. 2006, 9:816-823.
45. Wilke S.A., Antonios J.K., Bushong E.A., Badkoobehi A., Malek E., Hwang M., Terada M., Ellisman M.H., Ghosh A. Deconstructing complexity: serial block-face electron microscopic analysis of the hippocampal mossy fiber synapse. J.Neurosci. 2013, 33:507-522.
46. Zariwala H.A., Borghuis B.G., Hoogland T.M., Madisen L., Tian L., De Zeeuw C.I., Zeng H., Looger L.L., Svoboda K., Chen T.W. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging invivo. J.Neurosci. 2012, 32:3131-3141.
47. Zeng W., Mak D.O., Li Q., Shin D.M., Foskett J.K., Muallem S. A new mode of Ca2+ signaling by G protein-coupled receptors: gating of IP3 receptor Ca2+ release channels by Gbetagamma. Curr. Biol. 2003, 13:872-876.