Time-Resolved Imaging Reveals Heterogeneous Landscapes of Nanomolar Ca2+ in Neurons and Astroglia

Neuron

Volumn 88, Issue 2, 2015, Pages 277-288

  Zheng, Kaiyu ^a   Bard, Lucie ^a   Reynolds, James P ^a   King, Claire ^a   Jensen, Thomas P ^a   Gourine, Alexander V ^b   Rusakov, Dmitri A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALCIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLEACHING; CALCIUM CELL LEVEL; CELL AGING; CELL COMMUNICATION; CELL FUNCTION; CONTROLLED STUDY; DENDRITE; GAP JUNCTION; LIGHT SCATTERING; MACROGLIA; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RESTING STATE NETWORK; TEMPERATURE; VISCOSITY; ANIMAL; ASTROCYTE; CHEMISTRY; MULTIPHOTON MICROSCOPY; NANOTECHNOLOGY; ORGAN CULTURE TECHNIQUE; PROCEDURES; SPRAGUE DAWLEY RAT; TIME LAPSE IMAGING;

ANIMALS; ASTROCYTES; CALCIUM; MALE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NANOTECHNOLOGY; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; TIME-LAPSE IMAGING;

EID: 84944875744     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.09.043     Document Type: Article

References (57)

1. Baker A.J., Brandes R., Schreur J.H.M., Camacho S.A., Weiner M.W. Protein and acidosis alter calcium-binding and fluorescence spectra of the calcium indicator indo-1. Biophys. J. 1994, 67:1646-1654.
2. Battisti A., Digman M.A., Gratton E., Storti B., Beltram F., Bizzarri R. Intracellular pH measurements made simple by fluorescent protein probes and the phasor approach to fluorescence lifetime imaging. Chem. Commun. (Camb.) 2012, 48:5127-5129.
3. Baylor S.M., Hollingworth S. Calcium indicators and calcium signalling in skeletal muscle fibres during excitation-contraction coupling. Prog. Biophys. Mol. Biol. 2011, 105:162-179.
4. Cossart R., Aronov D., Yuste R. Attractor dynamics of network UP states in the neocortex. Nature 2003, 423:283-288.
5. 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.
6. 2+ influx and bouton size at small central synapses. PLoS Biol. 2012, 10:e1001396.
7. Faas G.C., Raghavachari S., Lisman J.E., Mody I. Calmodulin as a direct detector of Ca2+ signals. Nat. Neurosci. 2011, 14:301-304.
8. 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.
9. Gee J.M., Smith N.A., Fernandez F.R., Economo M.N., Brunert D., Rothermel M., Morris S.C., Talbot A., Palumbos S., Ichida J.M., et al. Imaging activity in neurons and glia with a Polr2a-based and cre-dependent GCaMP5G-IRES-tdTomato reporter mouse. Neuron 2014, 83:1058-1072.
10. Giaume C., Koulakoff A., Roux L., Holcman D., Rouach N. Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 2010, 11:87-99.
11. Grienberger C., Konnerth A. Imaging calcium in neurons. Neuron 2012, 73:862-885.
12. Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
13. Halassa M.M., Haydon P.G. Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 2010, 72:335-355.
14. Henneberger C., Papouin T., Oliet S.H., Rusakov D.A. Long-term potentiation depends on release of D-serine from astrocytes. Nature 2010, 463:232-236.
15. Ho A., Shen J. Presenilins in synaptic function and disease. Trends Mol. Med. 2011, 17:617-624.
16. Kanemaru K., Sekiya H., Xu M., Satoh K., Kitajima N., Yoshida K., Okubo Y., Sasaki T., Moritoh S., Hasuwa H., et al. In vivo visualization of subtle, transient, and local activity of astrocytes using an ultrasensitive Ca(2+) indicator. Cell Rep. 2014, 8:311-318.
17. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J. Physiol. 1968, 195:481-492.
18. Kip S.N., Gray N.W., Burette A., Canbay A., Weinberg R.J., Strehler E.E. Changes in the expression of plasma membrane calcium extrusion systems during the maturation of hippocampal neurons. Hippocampus 2006, 16:20-34.
19. Koester H.J., Baur D., Uhl R., Hell S.W. Ca2+ fluorescence imaging with pico- and femtosecond two-photon excitation: signal and photodamage. Biophys. J. 1999, 77:2226-2236.
20. Koldenkova V.P., Nagai T. Genetically encoded Ca2+ indicators: Properties and evaluation. Biochimica Et Biophysica Acta-Molecular Cell Research 2013, 1833:1787-1797.
21. Konishi M., Olson A., Hollingworth S., Baylor S.M. Myoplasmic binding of fura-2 investigated by steady-state fluorescence and absorbance measurements. Biophys. J. 1988, 54:1089-1104.
22. Kuchibhotla K.V., Lattarulo C.R., Hyman B.T., Bacskai B.J. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 2009, 323:1211-1215.
23. Lisman J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl. Acad. Sci. USA 1989, 86:9574-9578.
24. Maravall M., Mainen Z.F., Sabatini B.L., Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 2000, 78:2655-2667.
25. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
26. Matthews E.A., Schoch S., Dietrich D. Tuning local calcium availability: cell-type-specific immobile calcium buffer capacity in hippocampal neurons. J. Neurosci. 2013, 33:14431-14445.
27. Nishiyama M., Hong K., Mikoshiba K., Poo M.M., Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 2000, 408:584-588.
28. Noguchi J., Nagaoka A., Watanabe S., Ellis-Davies G.C.R., Kitamura K., Kano M., Matsuzaki M., Kasai H. In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice. J. Physiol. 2011, 589:2447-2457.
29. Oertner T.G., Sabatini B.L., Nimchinsky E.A., Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 2002, 5:657-664.
30. Oh M.M., Oliveira F.A., Waters J., Disterhoft J.F. Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons. J. Neurosci. 2013, 33:7905-7911.
31. Oheim M., Beaurepaire E., Chaigneau E., Mertz J., Charpak S. Two-photon microscopy in brain tissue: parameters influencing the imaging depth. J. Neurosci. Methods 2001, 111:29-37.
32. Otsu Y., Couchman K., Lyons D.G., Collot M., Agarwal A., Mallet J.-M., Pfrieger F.W., Bergles D.E., Charpak S. Calcium dynamics in astrocyte processes during neurovascular coupling. Nat. Neurosci. 2015, 18:210-218.
33. Parpura V., Verkhratsky A. Homeostatic function of astrocytes: Ca(2+) and Na(+) signalling. Transl. Neurosci. 2012, 3:334-344.
34. Perea G., Navarrete M., Araque A. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 2009, 32:421-431.
35. Pohle J., Bischofberger J. Supralinear dendritic Ca(2+) signalling in young developing CA1 pyramidal cells. J. Physiol. 2014, 592:4931-4949.
36. Poskanzer K.E., Yuste R. Astrocytic regulation of cortical UP states. Proc. Natl. Acad. Sci. USA 2011, 108:18453-18458.
37. Ross W.N. Understanding calcium waves and sparks in central neurons. Nat. Rev. Neurosci. 2012, 13:157-168.
38. Ruiz A., Fabian-Fine R., Scott R., Walker M.C., Rusakov D.A., Kullmann D.M. GABAA receptors at hippocampal mossy fibers. Neuron 2003, 39:961-973.
39. Rusakov D.A. Disentangling calcium-driven astrocyte physiology. Nat. Rev. Neurosci. 2015, 16:226-233.
40. 2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J. Neurosci. 2006, 26:7071-7081.
41. Sharma S., Quintana A., Findlay G.M., Mettlen M., Baust B., Jain M., Nilsson R., Rao A., Hogan P.G. An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature 2013, 499:238-242.
42. 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. 2012, 15:70-80.
43. 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.
44. 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.
45. Sylantyev S., Jensen T.P., Ross R.A., Rusakov D.A. Cannabinoid- and lysophosphatidylinositol-sensitive receptor GPR55 boosts neurotransmitter release at central synapses. Proc. Natl. Acad. Sci. USA 2013, 110:5193-5198.
46. Toescu E.C., Verkhratsky A. The importance of being subtle: small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell 2007, 6:267-273.
47. Tønnesen J., Katona G., Rózsa B., Nägerl U.V. Spine neck plasticity regulates compartmentalization of synapses. Nat. Neurosci. 2014, 17:678-685.
48. Tsien R.Y. Fluorescent probes of cell signaling. Annu. Rev. Neurosci. 1989, 12:227-253.
49. Tsuji T., Yoshida S., Yoshida A., Uchiyama S. Cationic fluorescent polymeric thermometers with the ability to enter yeast and mammalian cells for practical intracellular temperature measurements. Anal. Chem. 2013, 85:9815-9823.
50. Ueda Y., Kwok S., Hayashi Y. Application of FRET probes in the analysis of neuronal plasticity. Front. Neural Circuits 2013, 7:163.
51. Volterra A., Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 2005, 6:626-640.
52. Wilms C.D., Eilers J. Photo-physical properties of Ca2+-indicator dyes suitable for two-photon fluorescence-lifetime recordings. J. Microsc. 2007, 225:209-213.
53. Wilms C.D., Schmidt H., Eilers J. Quantitative two-photon Ca2+ imaging via fluorescence lifetime analysis. Cell Calcium 2006, 40:73-79.
54. Wu L.G., Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 1994, 14:645-654.
55. Wu Y., Stefl M., Olzyńska A., Hof M., Yahioglu G., Yip P., Casey D.R., Ces O., Humpolíčková J., Kuimova M.K. Molecular rheometry: direct determination of viscosity in Lo and Ld lipid phases via fluorescence lifetime imaging. Phys. Chem. Chem. Phys. 2013, 15:14986-14993.
56. Zhabotinsky A.M., Camp R.N., Epstein I.R., Lisman J.E. Role of the neurogranin concentrated in spines in the induction of long-term potentiation. J. Neurosci. 2006, 26:7337-7347.
57. Zheng K., Levitt J.A., Suhling K., Rusakov D.A. Monitoring Nanoscale Mobility of Small Molecules in Organized Brain Tissue with Time-Resolved Fluorescence Anisotropy Imaging. Nanoscale Imaging of Synapses 2014, 125-143. Springer.