Transient Opening of the Mitochondrial Permeability Transition Pore Induces Microdomain Calcium Transients in Astrocyte Processes

Neuron

Volumn 93, Issue 3, 2017, Pages 587-605.e7

  Agarwal, Amit ^a   Wu, Pei Hsun ^a   Hughes, Ethan G ^a,c   Fukaya, Masahiro ^b   Tischfield, Max A ^a,d   Langseth, Abraham J ^a   Wirtz, Denis ^a   Bergles, Dwight E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

astrocyte; ATP; calcium; cortex; in vivo; metabolism; microdomain; mitochondria; two photon

Indexed keywords

CALCIUM ION; COPPER ZINC SUPEROXIDE DISMUTASE; INOSITOL TRISPHOSPHATE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MUTANT PROTEIN; REACTIVE OXYGEN METABOLITE; CALCIUM; CARRIER PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; CELL METABOLISM; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; GLIA CELL; IN VIVO STUDY; MALE; MITOCHONDRIAL STRESS; MOUSE; NERVE DEGENERATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN FUNCTION; ANIMAL; GENETICS; METABOLISM; MITOCHONDRION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ASTROCYTES; CALCIUM; ENDOPLASMIC RETICULUM; INOSITOL 1,4,5-TRISPHOSPHATE; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE-1;

EID: 85010876934     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.12.034     Document Type: Article

References (52)

1. Araque, A., Carmignoto, G., Haydon, P.G., Oliet, S.H.R., Robitaille, R., Volterra, A., Gliotransmitters travel in time and space. Neuron 81 (2014), 728–739.
2. Bánsághi, S., Golenár, T., Madesh, M., Csordás, G., RamachandraRao, S., Sharma, K., Yule, D.I., Joseph, S.K., Hajnóczky, G., Isoform- and species-specific control of inositol 1,4,5-trisphosphate (IP3) receptors by reactive oxygen species. J. Biol. Chem. 289 (2014), 8170–8181.
3. Bélanger, M., Allaman, I., Magistretti, P.J., Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14 (2011), 724–738.
4. Bernardi, P., Petronilli, V., The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J. Bioenerg. Biomembr. 28 (1996), 131–138.
5. Cavelier, P., Attwell, D., Neurotransmitter depletion by bafilomycin is promoted by vesicle turnover. Neurosci. Lett. 412 (2007), 95–100.
6. 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. 14 (2011), 1276–1284.
7. Freeman, M.R., Rowitch, D.H., Evolving concepts of gliogenesis: a look way back and ahead to the next 25 years. Neuron 80 (2013), 613–623.
8. Ganat, Y.M., Silbereis, J., Cave, C., Ngu, H., Anderson, G.M., Ohkubo, Y., Ment, L.R., Vaccarino, F.M., Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 26 (2006), 8609–8621.
9. González-Barroso, M.M., Fleury, C., Levi-Meyrueis, C., Zaragoza, P., Bouillaud, F., Rial, E., Deletion of amino acids 261-269 in the brown fat uncoupling protein converts the carrier into a pore. Biochemistry 36 (1997), 10930–10935.
10. Grosche, J., Matyash, V., Möller, T., Verkhratsky, A., Reichenbach, A., Kettenmann, H., Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat. Neurosci. 2 (1999), 139–143.
11. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X., et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264 (1994), 1772–1775.
12. Haydon, P.G., GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2 (2001), 185–193.
13. Hems, D.A., Whitton, P.D., Control of hepatic glycogenolysis. Physiol. Rev. 60 (1980), 1–50.
14. Hertz, L., Peng, L., Dienel, G.A., Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J. Cereb. Blood Flow Metab. 27 (2007), 219–249.
15. Hou, T., Wang, X., Ma, Q., Cheng, H., Mitochondrial flashes: new insights into mitochondrial ROS signalling and beyond. J. Physiol. 592 (2014), 3703–3713.
16. Ichas, F., Jouaville, L.S., Mazat, J.P., Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89 (1997), 1145–1153.
17. Jackson, J.G., Robinson, M.B., Reciprocal regulation of mitochondrial dynamics and calcium signaling in astrocyte processes. J. Neurosci. 35 (2015), 15199–15213.
18. 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. 8 (2014), 311–318.
19. Khakh, B.S., McCarthy, K.D., Astrocyte calcium signaling: from observations to functions and the challenges therein. Cold Spring Harb. Perspect. Biol., 7, 2015, a020404.
20. Kosaka, T., Hama, K., Three-dimensional structure of astrocytes in the rat dentate gyrus. J. Comp. Neurol. 249 (1986), 242–260.
21. Krauss, S., Zhang, C.-Y., Lowell, B.B., The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell Biol. 6 (2005), 248–261.
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 323 (2009), 1211–1215.
23. Kuga, N., Sasaki, T., Takahara, Y., Matsuki, N., Ikegaya, Y., Large-scale calcium waves traveling through astrocytic networks in vivo. J. Neurosci. 31 (2011), 2607–2614.
24. 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. 96 (2005), 1274–1281.
25. Li, B., Chauvin, C., De Paulis, D., De Oliveira, F., Gharib, A., Vial, G., Lablanche, S., Leverve, X., Bernardi, P., Ovize, M., et al. Inhibition of complex I regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D. Biochim. Biophys. Acta 1817 (2012), 1628–1634.
26. Liu, J., Lillo, C., Jonsson, P.A., Vande Velde, C., Ward, C.M., Miller, T.M., Subramaniam, J.R., Rothstein, J.D., Marklund, S., Andersen, P.M., et al. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43 (2004), 5–17.
27. Lovatt, D., Sonnewald, U., Waagepetersen, H.S., Schousboe, A., He, W., Lin, J.H.-C., Han, X., Takano, T., Wang, S., Sim, F.J., et al. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J. Neurosci. 27 (2007), 12255–12266.
28. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13 (2010), 133–140.
29. Magistretti, P.J., Allaman, I., A cellular perspective on brain energy metabolism and functional imaging. Neuron 86 (2015), 883–901.
30. Mailloux, R.J., Harper, M.-E., Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins. Trends Endocrinol. Metab. 23 (2012), 451–458.
31. Naga, K.K., Sullivan, P.G., Geddes, J.W., High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J. Neurosci. 27 (2007), 7469–7475.
32. Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H., Przedborski, S., Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10 (2007), 615–622.
33. Nett, W.J., Oloff, S.H., McCarthy, K.D., Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J. Neurophysiol. 87 (2002), 528–537.
34. Nimmerjahn, A., Mukamel, E.A., Schnitzer, M.J., Motor behavior activates Bergmann glial networks. Neuron 62 (2009), 400–412.
35. Parone, P.A., Da Cruz, S., Han, J.S., McAlonis-Downes, M., Vetto, A.P., Lee, S.K., Tseng, E., Cleveland, D.W., Enhancing mitochondrial calcium buffering capacity reduces aggregation of misfolded SOD1 and motor neuron cell death without extending survival in mouse models of inherited amyotrophic lateral sclerosis. J. Neurosci. 33 (2013), 4657–4671.
36. Paukert, M., Agarwal, A., Cha, J., Doze, V.A., Kang, J.U., Bergles, D.E., Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82 (2014), 1263–1270.
37. Paulsen, R.E., Contestabile, A., Villani, L., Fonnum, F., An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J. Neurochem. 48 (1987), 1377–1385.
38. 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. 28 (2008), 4967–4973.
39. Rizzuto, R., Nakase, H., Darras, B., Francke, U., Fabrizi, G.M., Mengel, T., Walsh, F., Kadenbach, B., DiMauro, S., Schon, E.A., A gene specifying subunit VIII of human cytochrome c oxidase is localized to chromosome 11 and is expressed in both muscle and non-muscle tissues. J. Biol. Chem. 264 (1989), 10595–10600.
40. Rizzuto, R., Pinton, P., Carrington, W., Fay, F.S., Fogarty, K.E., Lifshitz, L.M., Tuft, R.A., Pozzan, T., Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280 (1998), 1763–1766.
41. Rizzuto, R., De Stefani, D., Raffaello, A., Mammucari, C., Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 13 (2012), 566–578.
42. Rungta, R.L., Bernier, L.P., Dissing-Olesen, L., Groten, C.J., LeDue, J.M., Ko, R., Drissler, S., MacVicar, B.A., Ca2+ transients in astrocyte fine processes occur via Ca2+ influx in the adult mouse hippocampus. Glia 64 (2016), 2093–2103.
43. Schildge, S., Bohrer, C., Beck, K., Schachtrup, C., Isolation and culture of mouse cortical astrocytes. J. Vis. Exp., 71, 2013, e50079.
44. 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. 15 (2011), 70–80.
45. 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. 141 (2013), 633–647.
46. Srinivasan, R., Huang, B.S., Venugopal, S., Johnston, A.D., Chai, H., Zeng, H., Golshani, P., Khakh, B.S., Ca(2+) signaling in astrocytes from Ip3r2(-/-) mice in brain slices and during startle responses in vivo. Nat. Neurosci. 18 (2015), 708–717.
47. Stephen, T.L., Higgs, N.F., Sheehan, D.F., Al Awabdh, S., López-Doménech, G., Arancibia-Carcamo, I.L., Kittler, J.T., Miro1 regulates activity-driven positioning of mitochondria within astrocytic processes apposed to synapses to regulate intracellular calcium signaling. J. Neurosci. 35 (2015), 15996–16011.
48. 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 6 (2009), 875–881.
49. Ververken, D., Van Veldhoven, P., Proost, C., Carton, H., De Wulf, H., On the role of calcium ions in the regulation of glycogenolysis in mouse brain cortical slices. J. Neurochem. 38 (1982), 1286–1295.
50. Wang, W., Fang, H., Groom, L., Cheng, A., Zhang, W., Liu, J., Wang, X., Li, K., Han, P., Zheng, M., et al. Superoxide flashes in single mitochondria. Cell 134 (2008), 279–290.
51. Ward, S.M., Ordog, T., Koh, S.D., Baker, S.A., Jun, J.Y., Amberg, G., Monaghan, K., Sanders, K.M., Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J. Physiol. 525 (2000), 355–361.
52. Yoneda, S., Takano, H., Takaki, M., Suzuki, H., Properties of spontaneously active cells distributed in the submucosal layer of mouse proximal colon. J. Physiol. 542 (2002), 887–897.