Astrocytic Gq-GPCR-linked IP3R-Dependent Ca2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo

Journal of Neuroscience

Volumn 34, Issue 39, 2014, Pages 13139-13150

  Bonder, Daniel E ^a   McCarthy, Ken D ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocyte; Blood flow; Calcium; DREADD; In vivo; IP3

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GQ PROTEIN; INOSITOL 1, 4, 5 TRISPHOSPHATE RECEPTOR; NERVE PROTEIN; UNCLASSIFIED DRUG; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD FLOW; BLOOD RHEOLOGY; CALCIUM SIGNALING; CONTROLLED STUDY; CORTICAL BLOOD FLOW; FEMALE; FLUORESCENCE IMAGING; FLUORESCENCE IMMUNOCHEMISTRY; GENE DELETION; HYPEREMIA; IMMUNOCHEMISTRY; IN VIVO STUDY; LASER MICROSCOPY; MALE; MOUSE; MULTIPHOTON MICROSCOPY; NERVOUS SYSTEM FUNCTION; NEUROVASCULAR COUPLING; NONHUMAN; VISUAL CORTEX; VISUAL STIMULATION; ANIMAL; BRAIN CIRCULATION; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; ASTROCYTES; CALCIUM SIGNALING; CEREBROVASCULAR CIRCULATION; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MICE; MICE, INBRED C57BL; VISUAL CORTEX;

EID: 84907292027     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2591-14.2014     Document Type: Article

References (78)

1. 2+ signaling. Science 327:1250 -1254. CrossRef Medline
2. Agulhon C, Boyt KM, Xie AX, Friocourt F, Roth BL, McCarthy KD (2013) Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol 591: 5599-5609. CrossRef Medline
3. 2+ elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450. Medline
4. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL (2007) Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A 104:5163- 5168. CrossRef Medline
5. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232- 243. CrossRef Medline
6. Bekar LK, He W, Nedergaard M (2008) Locus coeruleus alpha-adrenergicmediated activation of cortical astrocytes in vivo. Cereb Cortex 18:2789- 2795. CrossRef Medline
7. Bekar LK, Wei HS, Nedergaard M (2012) The locus coeruleusnorepinephrine network optimizes coupling of cerebral blood volume with oxygen demand. J Cereb Blood Flow Metab 32:2135-2145. CrossRef Medline
8. Brew H, Attwell D (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327:707-709. CrossRef Medline
9. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2010) Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc 5:247-254. CrossRef Medline
10. Cauli B, Hamel E (2010) Revisiting the role of neurons in neurovascular coupling. Front Neuroenergetics 2:9. CrossRef Medline
11. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E (2004) Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24:8940-8949. CrossRef Medline
12. Chen N, Sugihara H, Sharma J, Perea G, Petravicz J, Le C, Sur M (2012) Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes. Proc Natl Acad Sci U S A 109:E2832-E2841. CrossRef Medline
13. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295-300. CrossRef Medline
14. Di Castro MA, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, Bouvier D, Tiret P, Volterra A (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14:1276 -1284. CrossRef Medline
15. Ding F, O'Donnell J, Thrane AS, Zeppenfeld D, Kang H, Xie L, Wang F, Nedergaard M (2013) α1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice. Cell Calcium 54:387-394. CrossRef Medline
16. Drew PJ, Shih AY, Driscoll JD, Knutsen PM, Blinder P, Davalos D, Akassoglou K, Tsai PS, Kleinfeld D (2010) Chronic optical access through a polished and reinforced thinned skull. Nat Methods 7:981-984. CrossRef Medline
17. Duffy S, MacVicar BA (1995) Adrenergic calcium signaling in astrocyte networks within the hippocampal slice. J Neurosci 15:5535-5550. Medline
18. Dunn KM, Hill-Eubanks DC, Liedtke WB, NelsonMT (2013) TRPV4 channels stimulate Ca2+-induced Ca2+release in astrocytic endfeet and amplify neurovascular coupling responses. Proc Natl Acad Sci U S A 110: 6157-6162. CrossRef Medline
19. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X, Chen J, McCarthy KD (2007) Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54:611- 626. CrossRef Medline
20. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT (2006) Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9:1397-1403. CrossRef Medline
21. Girouard H, Bonev AD, Hannah RM, Meredith A, Aldrich RW, Nelson MT (2010) Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad SciU S A 107:3811-3816. CrossRef Medline
22. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-749. CrossRef Medline
23. Gregorian C, Nakashima J, Le Belle J, Ohab J, Kim R, Liu A, Smith KB, Groszer M, Garcia AD, Sofroniew MV, Carmichael ST, Kornblum HI, Liu X, Wu H (2009) Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. J Neurosci 29:1874 -1886. CrossRef Medline
24. Haustein MD, Kracun S, Lu XH, Shih T, Jackson-Weaver O, Tong X, Xu J, Yang XW, O'Dell TJ, Marvin JS, Ellisman MH, Bushong EA, Looger LL, Khakh BS (2014) Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway. Neuron 82:413- 429. CrossRef Medline
25. He L, Linden DJ, Sapirstein A (2012) Astrocyte inositol triphosphate receptor type 2 and cytosolic phospholipase A2 alpha regulate asteriole responses in mouse neocortical brain slices. PLoS One 7:e42194. CrossRef Medline
26. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hübener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L (2009) Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4:1128 -1144. CrossRef Medline
27. Howarth C (2014) The contribution of astrocytes to the regulation of cerebral blood flow. Front Neurosci 8:103. CrossRef Medline
28. Kim SG, Ogawa S (2012) Biophysical and physiological origins of blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 32:1188 -1206. CrossRef Medline
29. Kocharyan A, Fernandes P, Tong XK, Vaucher E, Hamel E (2008) Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation. J Cereb Blood Flow Metab 28:221-231. CrossRef Medline
30. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-1056. Medline
31. Langer J, RoseCR (2009) Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859 -5877. CrossRef Medline
32. Li X, Zima AV, Sheikh F, Blatter LA, Chen J (2005) 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 96:1274 -1281. CrossRef Medline
33. Lind BL, Brazhe AR, Jessen SB, Tan FC, Lauritzen MJ (2013) Rapid stimulus-evoked astrocyte Ca2+elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc Natl Acad Sci U S A 110: E4678-E4687. CrossRef Medline
34. Masamoto K, Fukuda M, Vazquez A, Kim SG (2009) Dose-dependent effect of isoflurane on neurovascular coupling in rat cerebral cortex. Eur J Neurosci 30:242-250. CrossRef Medline
35. Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP (2010) The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58:1094 -1103. CrossRef Medline
36. Mc Caslin AF, Chen BR, Radosevich AJ, Cauli B, HillmanEM (2011) In vivo 3D morphology of astrocyte-vasculature interactions in the somatosensory cortex: implications for neurovascular coupling. J Cereb Blood Flow Metab 31:795- 806. CrossRef Medline
37. Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26:2862-2870. CrossRef Medline
38. Mishra A, Hamid A, Newman EA (2011) Oxygen modulation of neurovascular coupling in the retina. Proc Natl Acad Sci U S A 108:17827-17831. CrossRef Medline
39. Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195-199. CrossRef Medline
40. Navarrete M, Perea G, Fernandez de Sevilla D, Gómez-Gonzalo M, Núñez A, Martín ED, Araque A (2012) Astrocytes mediate in vivo cholinergicinduced synaptic plasticity. PLoS Biol 10:e1001259. CrossRef Medline
41. Newman EA (2005) Calcium increases in retinal glial cells evoked by lightinduced neuronal activity. J Neurosci 25:5502-5510. CrossRef Medline
42. Newman EA (2013) Functional hyperemia and mechanisms of neurovascular coupling in the retinal vasculature. J Cereb Blood Flow Metab 33: 1685-1695. CrossRef Medline
43. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1:31-37. CrossRef Medline
44. Nizar K, Uhlirova H, Tian P, Saisan PA, Cheng Q, Reznichenko L, Weldy KL, Steed TC, Sridhar VB, MacDonald CL, Cui J, Gratiy SL, Sakadzić S, Boas DA, Beka TI, Einevoll GT, Chen J, Masliah E, Dale AM, Silva GA, et al. (2013) In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J Neurosci 33:8411- 8422. CrossRef Medline
45. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFPexpressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72- 86. CrossRef Medline
46. Panatier A, Vallée J, Haber M, Murai KK, Lacaille JC, Robitaille R (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785-798. CrossRef Medline
47. Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE (2014) Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82:1263-1270. CrossRef Medline
48. Paulson OB, Newman EA (1987) Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 237:896-898. CrossRef Medline
49. 2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci 28:4967- 4973. CrossRef Medline
50. Petzold GC, Murthy VN (2011) Role of astrocytes in neurovascular coupling. Neuron 71:782-797. CrossRef Medline
51. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16:5073-5081. Medline
52. Roy CS, Sherrington CS (1890) On the regulation of the blood-supply of the brain. J Physiol 11:85-158.17. Medline
53. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF, Lyden PD, Kleinfeld D (2006) Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol 4:e22. CrossRef Medline
54. Schulz K, Sydekum E, Krueppel R, Engelbrecht CJ, Schlegel F, Schröter A, Rudin M, Helmchen F (2012) Simultaneous BOLD fMRI and fiberoptic calcium recording in rat neocortex. Nat Methods 9:597- 602. CrossRef Medline
55. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638- 1643. CrossRef Medline
56. Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS (2012) TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat Neurosci 15:70-80. CrossRef Medline
57. Shigetomi E, Bushong EA, Haustein MD, Tong X, Jackson-Weaver O, Kracun S, Xu J, Sofroniew MV, Ellisman MH, Khakh BS (2013) Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141: 633-647. CrossRef Medline
58. Stobart JL, Lu L, Anderson HD, Mori H, Anderson CM (2013) Astrocyteinduced cortical vasodilation is mediated by D-serine and endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 110:3149 -3154. CrossRef Medline
59. Straub SV, Bonev AD, Wilkerson MK, Nelson MT (2006) Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J Gen Physiol 128:659-669. CrossRef Medline
60. Sun MY, Devaraju P, Xie AX, Holman I, Samones E, Murphy TR, Fiacco TA (2014) Astrocyte calcium microdomains are inhibited by Bafilomycin A1 and cannot be replicated by low-level Schaffer collateral stimulation in situ. Cell Calcium 55:1-16. CrossRef Medline
61. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M (2013) Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197- 200. CrossRef Medline
62. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260 -267. CrossRef Medline
63. Takano T, He W, Han X, Wang F, Xu Q, Wang X, Oberheim Bush NA, Cruz N, Dienel GA, Nedergaard M (2014) Rapid manifestation of reactive astrogliosis in acute hippocampal brain slices. Glia 62:78 -95. CrossRef Medline
64. Takata N, Mishima T, Hisatsune C, Nagai T, Ebisui E, Mikoshiba K, HiraseH (2011) Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J Neurosci 31:18155-18165. CrossRef Medline
65. 2+ signaling in astrocytes. PLoS One 8:e66525. CrossRef Medline
66. Thrane AS, Rangroo Thrane V, Zeppenfeld D, Lou N, Xu Q, Nagelhus EA, Nedergaard M (2012) General anesthesia selectively disrupts astrocyte calcium signaling in the awake mouse cortex. Proc Natl Acad Sci U S A 109:18974 -18979. CrossRef Medline
67. Tian P, Teng IC, May LD, Kurz R, Lu K, Scadeng M, Hillman EM, De Crespigny AJ, D'Arceuil HE, Mandeville JB, Marota JJ, Rosen BR, Liu TT, Boas DA, Buxton RB, Dale AM, Devor A (2010) Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc Natl Acad Sci U S A 107:15246 -15251. CrossRef Medline
68. Volterra A, Liaudet N, Savtchouk I (2014) Astrocyte Ca(2)(+) signalling: an unexpected complexity. Nat Rev Neurosci 15:327-335. CrossRef Medline
69. Wang F, Smith NA, Xu Q, Fujita T, Baba A, Matsuda T, Takano T, Bekar L, Nedergaard M (2012) Astrocytes modulate neural network activity by Ca(2)+-dependent uptake of extracellular K+. Sci Signal 5:ra26. CrossRef Medline
70. 2+ signaling triggers astrocytic glutamate release. J Neurosci 33: 17404-17412. CrossRef Medline
71. Wang X, Lou N, Xu Q, Tian GF, Peng WG, Han X, Kang J, Takano T, Nedergaard M (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9:816-823. CrossRef Medline
72. Wess J, Nakajima K, Jain S (2013) Novel designer receptors to probe GPCR signaling and physiology. Trends Pharmacol Sci 34:385-392. CrossRef Medline
73. Winship IR, Plaa N, Murphy TH (2007) Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J Neurosci 27:6268-6272. CrossRef Medline
74. Witthoft A, Filosa JA, Karniadakis GE (2013) Potassium buffering in the neurovascular unit: models and sensitivity analysis. Biophys J 105:2046- 2054. CrossRef Medline
75. Xu HT, Pan F, Yang G, GanWB (2007) Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat Neurosci 10:549 -551. CrossRef Medline
76. Yang G, Pan F, Parkhurst CN, Grutzendler J, GanWB (2010) Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat Protoc 5:201-208. CrossRef Medline
77. Zhou M, Xu G, Xie M, Zhang X, Schools GP, Ma L, Kimelberg HK, Chen H (2009) TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. J Neurosci 29:8551- 8564. CrossRef Medline
78. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50. Medline