Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-13T04:56:57.480Z Has data issue: false hasContentIssue false
  • English
  • Français

Local influence of mitochondrial calcium transport in retinal amacrine cells

Published online by Cambridge University Press:  16 August 2007

MADHUMITA SEN ,
EMILY MCMAINS  and
EVANNA GLEASON
MADHUMITA SEN
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana Present Address: Mount Sinai School of Medicine, Department of Ophthalmology, New York, NY 10029
EMILY MCMAINS
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
EVANNA GLEASON
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
Get access Rights & Permissions [Opens in a new window]

Abstract

Ca2+-dependent synaptic transmission from retinal amacrine cells is thought to be initiated locally at dendritic processes. Hence, understanding the spatial and temporal impact of Ca2+ transport is fundamental to understanding how amacrine cells operate. Here, we provide the first examination of the local effects of mitochondrial Ca2+ transport in neuronal processes. By combining mitochondrial localization with measurements of cytosolic Ca2+, the local impacts of mitochondrial Ca2+ transport for two types of Ca2+ signals were investigated. Disruption of mitochondrial Ca2+ uptake with carbonyl cyanide 4-(trifluoromethoxy) phenylhydrazone (FCCP) produces cytosolic Ca2+ elevations. The amplitudes of these elevations decline with distance from mitochondria suggesting that they are related to mitochondrial Ca2+ transport. The time course of the FCCP-dependent Ca2+ elevations depend on the availability of ER Ca2+ and we provide evidence that Ca2+ is released primarily via nearby ryanodine receptors. These results indicate that interactions between the ER and mitochondria influence cytosolic Ca2+ in amacrine cell processes and cell bodies. We also demonstrate that the durations of glutamate-dependent Ca2+ elevations are dependent on their proximity to mitochondria in amacrine cell processes. Consistent with this observation, disruption of mitochondrial Ca2+ transport alters the duration of glutamate-dependent Ca2+ elevations near mitochondria but not at sites more than 10 μm away. These results indicate that mitochondria influence local Ca2+-dependent signaling in amacrine cell processes.

Keywords

Amacrine cellsCalcium signalingMitochondriaRyanodine receptorsGlutamate
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 5 , September 2007 , pp. 663 - 678
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Azuma, T., Enoki, R., Iwamuro, K., Kaneko, A. & Koizumi, A. (2004). Multiple spatiotemporal patterns of dendritic Ca2+ signals in goldfish retinal amacrine cells. Brain Research 1023, 64–73.CrossRefGoogle Scholar
Babcock, D.F. & Hille, B. (1998). Mitochondrial oversight of cellular Ca2+ signaling. Current Opinion in Neurobiology 8, 398–404.CrossRefGoogle Scholar
Baron, K.T. & Thayer, S.A. (1997). CGP37157 modulates mitochondrial Ca2+ homeostasis in cultured rat dorsal root ganglion neurons. European Journal of Pharmacology 340, 295–300.CrossRefGoogle Scholar
Beurg, M., Hafidi, A., Skinner, L.J., Ruel, J., Nouvian, R., Henaff, M., Puel, J.L., Aran, J.M. & Dulon, D. (2005). Ryanodine receptors and BK channels act as a presynaptic depressor of neurotransmission in cochlear inner hair cells. European Journal of Neuroscience 22, 1109–1119.CrossRefGoogle Scholar
Beutner, G., Sharma, V.K., Giovanucci, D.R., Yule, D.I. & Sheu, S.-S. (2001). Identification of a ryanodine receptor in rat heart mitochondria. Journal of Biological Chemistry 276, 21482–21488.CrossRefGoogle Scholar
Beutner, G., Sharma, V.K., Lin, L., Ryu, S.-Y., Dirksen, R.T. & Sheu, S.-S. (2005). Type 1 ryanodine receptor in cardiac mitochondria: Transducer of excitation-metabolism coupling. Biophysica Biochemica Acta 1717, 1–10.CrossRefGoogle Scholar
Billups, B. & Forsythe, I.D. (2002). Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. Journal of Neuroscience 22, 5840–5847.Google Scholar
Bilmen, J.G., Wootton, L.L., Godfrey, R.E., Smart, O.S. & Michelangeli, F. (2002). Inhibition of SERCA Ca2+ binding and phosphoryl transfer from ATP, by interfering with the pathway leading to the Ca2+ binding sites. European Journal of Biochemistry 269, 3678–3687.CrossRefGoogle Scholar
Bootman, M.D., Collins, T.J., Mackenzie, L., Roderick, H.L., Berridge, M.J. & Peppiatt, C.M. (2002). 2-Aminoethoxydiphenyl borate (2-APB) is a reliable blocker of store-operated Ca2+ entry but an inconsistent inhibitor of IP3-induced Ca2+ release. Faseb Journal 16, 1145–1150.CrossRefGoogle Scholar
Bose, D.D. & Thomas, D.W. (2006). 2-Aminoethoxydiphenyl borate (2-APB) stimulates a conformationally coupled calcium release pathway in the NG 115-401L neuronal cell line. Neuropharmacology 50, 532–539.CrossRefGoogle Scholar
Buckmann, J.F., Hernandez, H., Kress, G.J., Votyakova, T.V., Pal, S. & Reynolds, I.J. (2001). Mitotracker labeling in primary neuronal and astrocytic cultures: Influence of mitochondrial membrane potential and oxidants. Journal of Neuroscience Methods 104, 165–176.CrossRefGoogle Scholar
Caldetti, L., Bryson, E.J., Ciccone, C.A., Rable, K. & Thoreson, W.B. (2006). Calcium-induced calcium release in rod photoreceptor terminals boosts synaptic transmission during maintained depolarization. European Journal of Neuroscience 23, 2983–2990.CrossRefGoogle Scholar
Castonguay, A. & Robitaille, R. (2002). Xestospongin C is a potent inhibitor of SERCA at a vertebrate synapse. Cell Calcium 32, 39–47.CrossRefGoogle Scholar
Chang, D.T.W., Honick, A.S. & Reynolds, I.J. (2006). Mitochondrial trafficking to synapses in cultured primary cortical neurons. Journal of Neuroscience 26, 7035–7045.CrossRefGoogle Scholar
Chavez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca2+ influx through AMPA-type glutamate receptors. Nature 443, 705–708.CrossRefGoogle Scholar
Cox, D.A., Conforti, L., Sperelakis, N. & Matlib, M.A. (1993). Selectivity of inhibition of Na+-Ca2+ exchange of heart mitochondria by benzothiazepine CGP-37157. Journal of Cardiovascular Pharmacology 21, 595–599.CrossRefGoogle Scholar
Csordas, G., Thomas, A.P. & Hajńoczky, G. (1999). Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO Journal 18, 96–108.CrossRefGoogle Scholar
Csordas, G., Thomas, A.P. & Hajńoczky, G. (2001). Calcium signal transmission between ryanodine receptors and mitochondria in cardiac muscle. Trends in Cardiovascular Medicine 11, 269–275.CrossRefGoogle Scholar
Demaurex, N., Lew, D.P. & Krause, K.H. (1992). Cyclopiazonic acid depletes intracellular Ca2+ stores and activates an influx pathway for divalent cations in HL-60 cells. Journal of Biological Chemistry 267, 2318–2324.Google Scholar
Denk, W. & Detwiler, P.B. (1999). Optical recording of light-evoked calcium signals in the functionality intact retina. Proceedings of the National Academy of Sciences of the USA 96, 7035–7040.CrossRefGoogle Scholar
De Smet, P., Parys, J.B., Callewaert, G., Weidema, A.F., Hill, E., De Smedt, H., Erneux, C., Sorrentino, V. & Missiaen, L. (1999). Xestospongin C is an equally potent inhibitor of the inositol 1,4,5-trisphosphate receptor and the endoplasmic-reticulum Ca2+ pumps. Cell Calcium 26, 9–13.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society of London. Series B. Biological Sciences 166, 80–111.CrossRefGoogle Scholar
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479–506.CrossRefGoogle Scholar
Duchen, M.R. (2000). Mitochondria and calcium: from cell signaling to cell death. Journal of Physiology 529, 57–68.CrossRefGoogle Scholar
Emptage, N.J., Reid, C.A. & Fine, A. (2001). Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron 29, 197–208.CrossRefGoogle Scholar
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Fransson, S., Ruusala, A. & Aspenstrom, P. (2006). The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochemical and Biophysical Research Communications 34, 500–510.CrossRefGoogle Scholar
Friel, D. (2004). Interplay between ER Ca2+ uptake and release fluxes in neurons and its impact on Ca2+ dynamics. Biological Research 37, 665–674.CrossRefGoogle Scholar
Friel, D.D. & Tsien, R.W. (1994). An FCCP-sensitive Ca2+ store in bullfrog sympathetic neurons and its participation in stimulus-evoked changes in (Ca2+)i. Journal of Neuroscience 14, 4007–4024.Google Scholar
Gilabert, J.A., Bakowski, D. & Parekh, A.B. (2001). Energized mitochondria increase the dynamic range over which inositol 1, 4, 5-trisphosphate activates store-operated calcium influx. EMBO Journal 20, 2672–2679.CrossRefGoogle Scholar
Gleason, E., Borges, S. & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. Journal of Neuroscience 13, 2359–12370.Google Scholar
Gleason, E., Borges, S. & Wilson, M. (1994). Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux. Neuron 13, 1109–1117.CrossRefGoogle Scholar
Guilhoff, G.D., Jones, J. & Kolb, H. (1988). Organization of the inner plexiform layer of the turtle retina: An electron microscopic study. Journal of Comparative Neurology 272, 280–292.CrossRefGoogle Scholar
Guo, X., Macleod, G.T., Wellington, A., Hu, F., Panchumarthi, S., Schoenfield, M., Marin, L., Charlton, M.P., Atwood, H.L. & Zinsmaier, K.E. (2005). The GTPase Miro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47, 379–393.CrossRefGoogle Scholar
Hajnóczky, G., Hager, R. & Thomas, A.P. (1999). Mitochondria suppress local feedback activation of inositol 1, 4, 5-triphosphate receptors by Ca2+. Journal of Biological Chemistry 274, 14157–14162.CrossRefGoogle Scholar
Hajnóczky, G., Robb-Gaspers, L.D., Seitz, M.B. & Thomas, A.P. (1995). Decoding of cytosolic calcium oscillations in the mitochondria. Cell 11, 415–424.CrossRefGoogle Scholar
Halling, D.B., Aracena-Parks, P. & Hamilton, S.L. (2005). Regulation of voltage-gated Ca2+ channels by calmodulin. Science STKE, 315, re15.CrossRefGoogle Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.Google Scholar
Hoffpauir, B.K. & Gleason, E.L. (2002). Activation of mGluR5 modulates GABAA receptor function in retinal amacrine cells. Journal of Neurophysiology 88, 1766–1776.Google Scholar
Hollenbeck, P.J. & Saxton, W.M. (2005). The axonal transport of mitochondria. Journal of Cell Science 118, 5411–5419.CrossRefGoogle Scholar
Huba, R. & Hofmann, H.D. (1992). Transmitter-gated currents of GABAergic amacrine-like cells in chick retina cultures. Visual Neuroscience 6, 303–314.Google Scholar
Hurtado, J., Borges, S. & Wilson, M. (2002). Na+-Ca2+ exchanger controls the gain of the Ca2+ amplifier in the dendrites of amacrine cells. Journal of Neurophysiology 88, 2765–2777.CrossRefGoogle Scholar
Jouaville, L.S., Ichas, F., Holmuhamedov, E.L., Camacho, P. & Lechleiter, J.D. (1995). Synchronisation of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 377, 438–441.CrossRefGoogle Scholar
Koizumi, A., Hayashida, Y., Kiuchi, T., Yamada, Y., Fujii, A., Yagi, T. & Kaneko, A. (2005). The interdependence and independence of amacrine cell dendrites: Patch-clamp recordings and simulation studies on cultured GABAergic amacrine cells. Journal of Integrative Neuroscience 4, 363–380.CrossRefGoogle Scholar
Kolb, H. & Nelson, R. (1993). OFF-Alpha and OFF-Beta ganglion cells in the cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. Journal of Comparative Neurology 329, 85–110.Google Scholar
Korn, N., Scott, T.R., Pouser, DP. & Thurston, R.J. (2002). Production and characterization of a turkey sperm mitochondrial mono-clonal antibody and its usefulness for assessment of sperm integrity. Poultry Science 81, 1077–1085.CrossRefGoogle Scholar
Kreimborg, K., Lester, L., Medler, K. & Gleason, E. (2001). Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. Journal of Neurochemistry 77, 452–465.CrossRefGoogle Scholar
Krizaj, D., Lai, F.A. & Copenhagen, D.R. (2003). Ryanaodine stores and calcium regulation in the inner segments of salamander rods and cones. Journal of Physiology 547, 761–771.CrossRefGoogle Scholar
Landolfi, B., Curci, S., Debellis, L., Pozzan, T. & Hofer, A.M. (1998). Ca2+ Homeostasis in the agonist-sensitive internal store: Functional interactions between mitochondria and the ER measured In situ in intact cell. Journal of Cell Biology 142, 1235–1243.CrossRefGoogle Scholar
Lelli, A., Perin, P., Martini, M., Ciubotaru, C.D., Prigioni, I., Valli, P., Rossi, M.L. & Mammano, F. (2003). Presynaptic calcium stores modulate afferent release in vestibular hair cells. Journal of Neuroscience 23, 6894–6903.Google Scholar
Medler, K. & Gleason, E.L. (2002). Mitochondrial Ca2+ buffering regulates synaptic transmission between retinal amacrine cells. Journal of Neurophysiology 87, 1426–1439.CrossRefGoogle Scholar
Mironov, S.L. & Symonchuk, N. (2006). ER vesicles and mitochondria move and communicate at synapses. Journal of Cell Science 119, 4926–4934.CrossRefGoogle Scholar
Morris, R.L. & Hollenbeck, P.J. (1995). Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. Journal of Cell Biology 131, 1315–1326.CrossRefGoogle Scholar
Nassar, A. & Simpson, A.W. (2000). Elevation of mitochondrial calcium by ryanodine-sensitive calcium-induced calcium release. Journal of Biological Chemistry 275, 23661–23665.CrossRefGoogle Scholar
Otsu, H., Yamamoto, A., Maeda, N., Mikoshiba, K. & Tashiro, Y. (1990). Immunogold localization of inositol 1, 4, 5-trisphosphate (InsP3) receptor in mouse cerebeller Purkinje cells using three monoclonal antibodies. Cell Structure and Function 15, 163–173.CrossRefGoogle Scholar
Pacher, P., Csordas, P., Schneider, T. & Hajnóczky, G. (2000). Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. Journal of Physiology 529, 3553–3564.CrossRefGoogle Scholar
Rintoul, G.L., Filiano, A.J., Brocard, J.B., Kress, G.J. & Reynolds, I.J. (2003). Glutamate decreases mitochondrial size and movement in primary forebrain neurons. Journal of Neuroscience 23, 7881–7888.Google Scholar
Rizzuto, R., Duchen, M.R. & Pozzan, T. (2004). Flirting in little space: The ER/mitochondria Ca2+ liaison. Science's STKE 215, re1.CrossRefGoogle Scholar
Rizzuto, R., Pinton, P., Carrington, W., Fay, F.S., Fogarty, K.E., Lifshitz, L.M., Tuft, R.A. & Pozzan, T. (1998). Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280, 1763–1766.CrossRefGoogle Scholar
Rizzuto, R., Simpson, A.W.M., Brini, M. & Pozzan, T. (1992). Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358, 325–327.CrossRefGoogle Scholar
Robb-Gaspers, L.D., Burnett, P., Rutter, G.A., Denton, R.M., Rizzuto, R. & Thomas, A.P. (1998). Integrating cytosolic calcium signals into mitochondrial metabolic responses. EMBO Journal 17, 4987–5000.CrossRefGoogle Scholar
Satoh, T., Ross, C.A., Villa, A., Supattapone, S., Pozzan, T., Snyder, S.H. & Meldolesi, J. (1990). The inositol 1, 4, 5-trisphosphate receptor in cerebeller Purkinje cells: Quantitative immunogold labeling reveals concentration in an ER subcompartment. Journal of Cell Biology 111, 615–624.CrossRefGoogle Scholar
Savic, N. & Sciancalepore, M. (1998). Intracellular calcium stores modulate miniature GABA-mediated synaptic currents in neonatal rat hippocampal neurons. The European Journal of Neuroscience 10, 3379–3386.CrossRefGoogle Scholar
Sharma, V.K., Ramesh, V., Franzini-Armstrong, C. & Sheu, S.S. (2000). Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. Journal of Bioenergetics and Biomembranes 32, 97–104.CrossRefGoogle Scholar
Shields, C.R. & Lukasiewicz, P.D. (2003). Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. Journal of Neurophysiology 89, 2449–2458.CrossRefGoogle Scholar
Simpson, P.B., Mehotra, S., Lange, G.D. & Russell, J.T. (1997). High-density distribution of endoplasmic reticulum proteins and mitochondria at specialized Ca2+ release sites in oligodendrocyte processes. Journal of Biological Chemistry 272, 22654–22661.CrossRefGoogle Scholar
Solovyova, N., Fernyhough, P., Glazner, G. & Verkhratsky, A. (2002). Xestospongin C empties the ER calcium store but does not inhibit InsP3-induced Ca2+ release in cultured dorsal root ganglia neurons. Cell Calcium 32, 49–52.CrossRefGoogle Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C. & Gleason, E.L. (2002). Metabotropic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973–983.CrossRefGoogle Scholar
Stowers, R.S., Megeath, L.J., Gorska-Andrzejak, J., Meinertzhagen, I.A. & Schwarz, T.L. (2002). Axonal transport of mitochondria to synapses depends on Milton, a novel drosophila protein. Neuron 36, 1063–1077.CrossRefGoogle Scholar
Suryanarayanan, A. & Slaughter, M.M. (2006). Synaptic transmission mediated by internal calcium stores in rod photoreceptors. Journal of Neuroscience 26, 1759–1766.CrossRefGoogle Scholar
Suzuki, M., Muraki, K., Imaizumi, Y. & Watanabe, M. (1992). Cyclopiazonic acid, an inhibitor of the sarcoplasmic reticulum Ca2+-pump reduces Ca2+-dependent K+ currents in guinea-pig smooth muscle cells. British Journal of Pharmacology 107, 134–140.CrossRefGoogle Scholar
Szalai, G., Csordas, G., Hantash, B.M., Thomas, A.P. & Hajńoczky, G. (2000). Calcium signal transmission between ryanodine receptors and mitochondria. Journal of Biological Chemistry 275, 15305–15313.CrossRefGoogle Scholar
Tinel, H., Cancela, J.M., Mogami, H., Gerasimenko, J.V., Gerasimenko, O.V., Tepikin, A.V. & Peterson, O.H. (1999). Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytolsolic Ca2+ signals. EMBO Journal 18, 4999–5008.CrossRefGoogle Scholar
Uyama, Y., Imaizumi, Y. & Watanabe, M. (1992). Effects of cyclopiazonic acid, a novel Ca2+-ATPase inhibitor, on contractile responses in skinned ileal smooth muscle. British Journal of Pharmacology 106, 208–214.CrossRefGoogle Scholar
Vigh, J. & von Gersdorff, H. (2005). Prolonged reciprocal signaling via NMDA and GABA receptors at a retinal ribbon synapse. Journal of Neuroscience 25, 11412–11423.CrossRefGoogle Scholar
Warrier, A., Borges, S., Dalcino, D., Walters, C. & Wilson, M. (2005). Calcium from internal stores triggers GABA release from retinal amacrine cells. Journal of Neurophysiology 94, 4196–4208.CrossRefGoogle Scholar
White, R.J. & Reynolds, I.J. (1997). Mitochondria accumulate Ca2+ following intense glutamate stimulation of cultured rat forebrain neurons. Journal of Physiology 498, 31–47.CrossRefGoogle Scholar
Yang, F., He, X., Russel, J. & Lu, B. (2003). Ca2+ influx-independent synaptic potentiation mediated by mitochondrial Na+-Ca2+ exchanger and protein kinase C. Journal of Cell Biology 163, 511–523.Google Scholar
Yi, M., Weaver, D. & Hajnóczky, G. (2004). Control of mitochondrial motility and distribution by the calcium signal: A homeostatic circuit. Journal of Cell Biology 167, 661–672.Google Scholar
Zhao, F., Li, P., Chen, S.R.W., Louis, C.F. & Fruen, B.R. (2001). Dantrolene inhibition of ryanodine receptor Ca2+ release channels. The Journal of Biological Chemistry 276, 13810–13816.Google Scholar