Sodium signaling and astrocyte energy metabolism

GLIA

Volumn 64, Issue 10, 2016, Pages 1667-1676

  Chatton, Jean Yves ^a   Magistretti, Pierre J ^b,c   Barros, L Felipe ^d  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c EPFL   (Switzerland)

^d CENTRO DE ESTUDIOS CIENTÍFICOS CECS   (Chile)

Author keywords

glycolysis; lactate; membrane transport; mitochondria; Na,K ATPase; neuron glia interactions; syncytium

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); LACTIC ACID; SODIUM;

ASTROCYTE; CELL INTERACTION; CELL METABOLISM; CELLULAR DISTRIBUTION; ENERGY METABOLISM; GLIA CELL; GLYCOLYSIS; MEMBRANE TRANSPORT; MITOCHONDRION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SODIUM CELL LEVEL; SYNCYTIUM;

EID: 84985032137     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22971     Document Type: Review

References (86)

1. Anderson CM, Bergher JP, Swanson RA. 2004. ATP-induced ATP release from astrocytes. J Neurochem 88:246–256.
2. Annunziato L, Boscia F, Pignataro G. 2013. Ionic transporter activity in astrocytes, microglia, and oligodendrocytes during brain ischemia. J Cereb Blood Flow Metab 33:969–982.
3. Azarias G, Chatton JY. 2011. Selective ion changes during spontaneous mitochondrial transients in intact astrocytes. PLoS One 6:e28505.
4. Azarias G, Perreten H, Lengacher S, Poburko D, Demaurex N, Magistretti PJ, Chatton J-Y. 2011. Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes. J Neurosci 31:3550–3559.
5. + transients in individual mitochondria of intact astrocytes. Glia 56:342–353.
6. Barros LF, Martinez C. 2007. An enquiry into metabolite domains. Biophys J 92:3878–3884.
7. + responses in astrocytes. Glia 54:460–470.
8. +-mediated metabolic waves. Proc Natl Acad Sci USA 101:14937–14942.
9. + and a delayed and persistent effect of glutamate. J Neurosci 31:4709–4713.
10. Blomstrand F, Giaume C. 2006. Kinetics of endothelin-induced inhibition and glucose permeability of astrocyte gap junctions. J Neurosci Res 83:996–1003.
11. Brand MD, Nicholls DG. 2011. Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312.
12. Charles A. 2005. Reaching out beyond the synapse: Glial intercellular waves coordinate metabolism. Sci STKE 2005:pe6.
13. + dynamics in mouse cortical astrocytes: Implications for cellular bioenergetics. Eur J Neurosci 12:3843–3853.
14. Chatton J-Y, Pellerin L, Magistretti PJ. 2003. GABA uptake into astrocytes is not associated with significant metabolic cost: Implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci USA 100:12456–12461.
15. Choi HB, Gordon GR, Zhou N, Tai C, Rungta RL, Martinez J, Milner TA, Ryu JK, McLarnon JG, Tresguerres M, Levin LR, Buck J, MacVicar BA. 2012. Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 75:1094–1104.
16. Cholet N, Pellerin L, Welker E, Lacombe P, Seylaz J, Magistretti P, Bonvento G. 2001. Local injection of antisense oligonucleotides targeted to the glial glutamate transporter GLAST decreases the metabolic response to somatosensory activation. J Cereb Blood Flow Metab 21:404–412.
17. +-induced increase in Gap junctional communication between mouse spinal cord astrocytes. J Neurosci 21:6635–6643.
18. Dienel GA. 2012. Brain lactate metabolism: The discoveries and the controversies. J Cereb Blood Flow Metab 32:1107–1138.
19. - concentration in relation to changes in the size of the extracellular space. Exp Brain Res 46:73–84.
20. DiNuzzo M, Mangia S, Maraviglia B, Giove F. 2010. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: Evidence from mathematical modeling. J Cereb Blood Flow Metab 30:586–602.
21. Donnan F. 1911. Theorie der Membrangleichgewichte und Membranpotentiale bei Vorhandensein von nicht dialysierenden Elektrolyten. Ein Beitrag zur physikalisch-chemischen Physiologie. Zeitschrift Für Elektrochemie Angew Phys Chem 17:572–581.
22. Erecinska M, Silver IA. 1994. Ions and energy in mammalian brain. Prog Neurobiol 43:37–71.
23. +-ATPase pump. Biochem J 460:353–361.
24. Genda EN, Jackson JG, Sheldon AL, Locke SF, Greco TM, O'Donnell JC, Spruce LA, Xiao R, Guo W, Putt M, Seeholzer S, Ischiropoulos H, Robinson MB. 2011. Co-compartmentalization of the astroglial glutamate transporter, GLT-1, with glycolytic enzymes and mitochondria. J Neurosci 31:18275–18288.
25. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N. 2010. Astroglial networks: A step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11:87–99.
26. Goyal MS, Hawrylycz M, Miller JA, Snyder AZ, Raichle ME. 2014. Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 19:49–57.
27. Guthrie PB, Knappenberger J, Segal M, Bennett MVL, Charles AC, Kater SB. 1999. ATP released from astrocytes mediates glial calcium waves. J Neurosci 19:520–528.
28. Hall CN, Klein-Flugge MC, Howarth C, Attwell D. 2012. Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J Neurosci 32:8940–8951.
29. Heinemann U, Lux HD. 1975. Undershoots following stimulus-induced rises of extracellular potassium concentration in cerebral cortex of cat. Brain Res 93:63–76.
30. +-ATPase. Neurosci Lett 138:188–192.
31. Honsa P, Pivonkova H, Harantova L, Butenko O, Kriska J, Dzamba D, Rusnakova V, Valihrach L, Kubista M, Anderova M. 2014. Increased expression of hyperpolarization-activated cyclic nucleotide-gated (HCN) channels in reactive astrocytes following ischemia. Glia 62:2004–2021.
32. Huang C, Hu ZL, Wu WN, Yu DF, Xiong QJ, Song JR, Shu Q, Fu H, Wang F, Chen JG. 2010. Existence and distinction of acid-evoked currents in rat astrocytes. Glia 58:1415–1424.
33. Hwang EM, Kim E, Yarishkin O, Woo DH, Han KS, Park N, Bae Y, Woo J, Kim D, Park M, Lee CJ, Park JY. 2014. A disulphide-linked heterodimer of TWIK-1 and TREK-1 mediates passive conductance in astrocytes. Nat Commun 5:3227.
34. Jackson JG, O'Donnell JC, Krizman E, Robinson MB. 2015. Displacing hexokinase from mitochondrial voltage-dependent anion channel impairs GLT-1-mediated glutamate uptake but does not disrupt interactions between GLT-1 and mitochondrial proteins. J Neurosci Res 93:999–1008.
35. Jolivet R, Coggan JS, Allaman I, Magistretti PJ. 2015. Multi-timescale modeling of activity-dependent metabolic coupling in the neuron-glia-vasculature ensemble. PLoS Comput Biol 11:e1004036.
36. Karus C, Mondragao MA, Ziemens D, Rose CR. 2015. Astrocytes restrict discharge duration and neuronal sodium loads during recurrent network activity. Glia 63:936–957.
37. Kofuji P, Newman EA. 2004. Potassium buffering in the central nervous system. Neuroscience 129:1045–1056.
38. Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y. 2011. Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci 31:2607–2614.
39. Langer J, Rose CR. 2009. Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol (Lond) 587:5859–5877.
40. Langer J, Stephan J, Theis M, Rose CR. 2012. Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ. Glia 60:239–252.
41. + clearance and volume responses. Glia 62:608–622.
42. Lerchundi R, Fernandez-Moncada I, Contreras-Baeza Y, Sotelo-Hitschfeld T, Machler P, Wyss MT, Stobart J, Baeza-Lehnert F, Alegria K, Weber B, Barros LF. 2015. NH4+ triggers the release of astrocytic lactate via mitochondrial pyruvate shunting. Proc Natl Acad Sci USA 112:11090–11095.
43. +-dependent glutamate uptake. J Neurosci 18:9620–9628.
44. Liang D, Bhatta S, Gerzanich V, Simard JM. 2007. Cytotoxic edema: Mechanisms of pathological cell swelling. Neurosurg Focus 22:E2.
45. Loaiza A, Porras OH, Barros LF. 2003. Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337–7342.
46. Ma L, Zhang X, Chen H. 2011. TWIK-1 two-pore domain potassium channels change ion selectivity and conduct inward leak sodium currents in hypokalemia. Sci Signal 4:ra37.
47. Mächler P, Wyss MT, Elsayed M, Stobart J, Gutierrez R, von Faber-Castell A, Kaelin V, Zuend M, San Martin A, Romero-Gomez I, Baeza-Lehnert F, Lengacher S, Schneider BL, Aebischer P, Magistretti PJ, Barros LF, Weber B. 2015. In vivo evidence for a lactate gradient from astrocytes to neurons. Cell Metab 23:94–102.
48. Macknight AD, Leaf A. 1977. Regulation of cellular volume. Physiol Rev 57:510–573.
49. Magistretti PJ, Allaman I. 2015. A cellular perspective on brain energy metabolism and functional imaging. Neuron 86:883–901.
50. + dynamics and ATP hydrolysis in astrocytes. J Neural Transm 112:77–85.
51. Martinez C, Kalise D, Barros LF. 2010. General requirement for harvesting antennae at ca and h channels and transporters. Front Neuroenerg 2:27.
52. Massa PT, Mugnaini E. 1982. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: A freeze-fracture study. Neuroscience 7:523–538.
53. McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR. 1996. Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 66:386–393.
54. Mercer RW, Dunham PB. 1981. Membrane-bound ATP fuels the Na/K pump. Studies on membrane-bound glycolytic enzymes on inside-out vesicles from human red cell membranes. J Gen Physiol 78:547–568.
55. Nimmerjahn A, Mukamel EA, Schnitzer MJ. 2009. Motor behavior activates Bergmann glial networks. Neuron 62:400–412.
56. Nuriya M, Yasui M. 2013. Endfeet serve as diffusion-limited subcellular compartments in astrocytes. J Neurosci 33:3692–3698.
57. Patel AB, Lai JC, Chowdhury GM, Hyder F, Rothman DL, Shulman RG, Behar KL. 2014. Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle. Proc Natl Acad Sci USA 111:5385–5390.
58. Pellerin L, Magistretti PJ. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625–10629.
59. Pellerin L, Magistretti PJ. 2012. Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32:1152–1166.
60. Pivovarova NB, Pozzo-Miller LD, Hongpaisan J, Andrews SB. 2002. Correlated calcium uptake and release by mitochondria and endoplasmic reticulum of CA3 hippocampal dendrites after afferent synaptic stimulation. J Neurosci 22:10653–10661.
61. 2+ cosignaling in the stimulation of the glucose transporter GLUT1 in cultured astrocytes. Glia 56:59–68.
62. Pozzo-Miller LD, Pivovarova NB, Leapman RD, Buchanan RA, Reese TS, Andrews SB. 1997. Activity-dependent calcium sequestration in dendrites of hippocampal neurons in brain slices. J Neurosci 17:8729–8738.
63. Raichle ME, MacLeod A, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. 2001. A default mode of brain function. Proc Natl Acad Sci USA 98:676–682.
64. Rash JE, Yasumura T, Davidson KG, Furman CS, Dudek FE, Nagy JI. 2001. Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord. Cell Commun Adhes 8:315–320.
65. + signals in spines and dendrites. J Neurosci 21:4207–4214.
66. Rose CR, Ransom BR. 1996. Intracellular sodium homeostasis in rat hippocampal astrocytes. J Physiol (Lond) 491:291–305.
67. + concentration in astrocytes. Glia 20:299–307.
68. Rose CR, Ransom BR. 1997b. Regulation of intracellular sodium in cultured rat hippocampal neurones. J Physiol (Lond) 499:573–587.
69. + homeostasis in rat spinal cord astrocytes. J Neurosci 18:3554–3562.
70. Rose EM, Koo JC, Antflick JE, Ahmed SM, Angers S, Hampson DR. 2009. Glutamate transporter coupling to Na,K-ATPase. J Neurosci 29:8143–8155.
71. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C. 2008. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551–1555.
72. Ruffin VA, Salameh AI, Boron WF, Parker MD. 2014. Intracellular pH regulation by acid–base transporters in mammalian neurons. Front Physiol 5:43.
73. +. J Neurosci 31:14264–14271.
74. Saab AS, Tzvetanova ID, Nave KA. 2013. The role of myelin and oligodendrocytes in axonal energy metabolism. Curr Opin Neurobiol 23:1065–1072.
75. San Martin A, Sotelo-Hitschfeld T, Lerchundi R, Fernandez-Moncada I, Ceballo S, Valdebenito R, Baeza-Lehnert F, Alegria K, Contreras-Baeza Y, Garrido-Gerter P, Romero-Gomez I, Barros LF. 2014. Single-cell imaging tools for brain energy metabolism: A review. Neurophotonics 1:011004.
76. Schwarzlander M, Murphy MP, Duchen MR, Logan DC, Fricker MD, Halestrap AP, Muller FL, Rizzuto R, Dick TP, Meyer AJ, Sweetlove LJ. 2012. Mitochondrial “flashes”: A radical concept repHined. Trends Cell Biol 22:503–508.
77. + ATPase in mammalian astrocytes. Glia 21:35–45.
78. Skou JC. 1989. The influence of some cations on an adenosine triphosphatase from peripheral nerves. 1957. Biochim Biophys Acta 1000:439–446.
79. Tress O, Maglione M, May D, Pivneva T, Richter N, Seyfarth J, Binder S, Zlomuzica A, Seifert G, Theis M, Dere E, Kettenmann H, Willecke K. 2012. Panglial gap junctional communication is essential for maintenance of myelin in the CNS. J Neurosci 32:7499–7518.
80. + concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60:605–614.
81. Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, Raichle ME. 2010. Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci USA 107:17757–17762.
82. Vlassenko AG, Vaishnavi SN, Couture L, Sacco D, Shannon BJ, Mach RH, Morris JC, Raichle ME, Mintun MA. 2010. Spatial correlation between brain aerobic glycolysis and amyloid-beta (Abeta) deposition. Proc Natl Acad Sci USA 107:17763–17767.
83. Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton J-Y, Magistretti PJ, Pellerin L. 2003. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37:275–286.
84. Warburg O. 1956. On the origin of cancer cells. Science 123:309–314.
85. Weber B, Barros LF. 2015. The astrocyte: Powerhouse and recycling center. Cold Spring Harb Perspect Biol 7:a020396.
86. Xu G, Wang W, Kimelberg HK, Zhou M. 2010. Electrical coupling of astrocytes in rat hippocampal slices under physiological and simulated ischemic conditions. Glia 58:481–493.