Genetically encoded proton sensors reveal activity-dependent pH changes in neurons

Frontiers in Molecular Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Raimondo, Joseph V ^a   Irkle, Agnese ^a   Wefelmeyer, Winnie ^a   Newey, Sarah E ^a   Akerman, Colin J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cl sensor; DeGFP4; E2GFP; Epilepsy; Genetic reporters; intracellular pH; Neural activity; PH sensors

Indexed keywords

ACIDITY; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ACTIVITY; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PH; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; TEMPORAL LOBE EPILEPSY;

EID: 84864000951     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00068     Document Type: Article

References (56)

1. Abad, M. F. C., Di Benedetto, G., Magalhães, P. J., Filippin, L., and Pozzan, T. (2004). Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J. Biol. Chem. 279, 11521-11529.
2. Ahmed, Z., and Connor, J. A. (1980). Intracellular pH changes induced by calcium influx during electrical activity in molluscan neurons. J. Gen. Physiol. 75, 403-426.
3. Anderson, W. W., Lewis, D. V., Swartzwelder, H. S., and Wilson, W. A. (1986). Magnesium-free medium activates seizure-like events in the rat hippocampal slice. Brain Res. 398, 215-219.
4. Arosio, D., Ricci, F., Marchetti, L., Gualdani, R., Albertazzi, L., and Beltram, F. (2010). Simultaneous intracellular chloride and pH measurements using a GFP-based sensor. Nat. Methods 7, 516-518.
5. Avoli, M., D'Antuono, M., Louvel, J., Köhling, R., Biagini, G., Pumain, R., D'Arcangelo, G., and Tancredi, V. (2002). Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog. Neurobiol. 68, 167-207.
6. Avoli, M., Drapeau, C., Perreault, P., Louvel, J., and Pumain, R. (1990). Epileptiform activity induced by low chloride medium in the CA1 subfield of the hippocampal slice. J. Neurophysiol. 64, 1747-1757.
7. Awaji, T., and Hirasawa, A. (2001). Novel green fluorescent protein-based ratiometric indicators for monitoring pH in defined intracellular microdomains. Biochem. Biophys. Res. Commun. 289, 457-462.
8. Bizzarri, R., Arcangeli, C., Arosio, D., Ricci, F., Faraci, P., Cardarelli, F., and Beltram, F. (2006). Development of a novel GFP-based ratiometric excitation and emission pH indicator for intracellular studies. Biophys. J. 90, 3300-3314.
9. Bizzarri, R., Serresi, M., Luin, S., and Beltram, F. (2009). Green fluorescent protein based pH indicators for in vivo use: a review. Anal. Bioanal. Chem. 393, 1107-1122.
10. 3-. Am. J. Physiol. 255, C844-C856.
11. Bregestovski, P., Waseem, T., and Mukhtarov, M. (2009). Genetically encoded optical sensors for monitoring of intracellular chloride and chloride-selective channel activity. Front. Mol. Neurosci. 2:15. doi: 10.3389/neuro.02.015.2009
12. Caspers, H., and Speckmann, E. (1972). Cerebral pO2, pCO2 and pH: changes during convulsive activity and their significance for spontaneous arrest of seizures. Epilepsia 13, 699-725.
13. Chamberlin, N. L., and Dingledine, R. (1988). GABAergic inhibition and the induction of spontaneous epileptiform activity by low chloride and high potassium in the hippocampal slice. Brain Res. 445, 12-18.
14. Chesler, M. (2003). Regulation and modulation of pH in the brain. Physiol. Rev. 83, 1183.
15. 2+ current in mammalian cone photoreceptors. Neuron 32, 1107-1117.
16. Denker, S. P., and Barber, D. L. (2002). Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J. Cell Biol. 159, 1087-1096.
17. Doyon, N., Prescott, S. A., Castonguay, A., Godin, A. G., Kröger, H., and De Koninck, Y. (2011). Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. PLoS Comput. Biol. 7:e1002149. doi: 10.1371/ journal.pcbi.1002149
18. Drapeau, P., and Nachshen, D. A. (1988). Effects of lowering extracellular and cytosolic pH on calcium fluxes, cytosolic calcium levels, and transmitter release in presynap-tic nerve terminals isolated from rat. J. Gen. Physiol. 91, 305-315.
19. Dulla, C. G., Dobelis, P., Pearson, T., Frenguelli, B. G., Staley, K. J., and Masino, S. A. (2005). Adenosine and ATP link PCO2 to cortical excitability via pH. Neuron 48, 1011-1023.
20. Esposito, A., Gralle, M., Dani, M. A. C., Lange, D., and Wouters, F. S. (2008). pHlameleons: a family of FRET-based protein sensors for quantitative pH imaging. Biochemistry 47, 13115-13126.
21. Gatto, C., and Milanick, M. (1993). Inhibition of the red blood cell calcium pump by eosin and other fluorescein analogues. Am. J. Physiol. Cell Physiol. 264, C1577-C1586.
22. Grichtchenko, I., and Chesler, M. (1994). Depolarization-induced acid secretion in gliotic hippocampal slices. Neuroscience 62, 1057-1070.
23. Griesbeck, O., Baird, G. S., Campbell, R. E., Zacharias, D. A., and Tsien, R. Y. (2001). Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188-29194.
24. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
25. 2+ in cultured rat hippocampal slices. Brain Res. 815, 294-303.
26. Hablitz, J. J. (1984). Picrotoxin-induced epileptiform activity in hippocampus: role of endogenous versus synaptic factors. J. Neurophysiol. 51, 1011-1027.
27. Hamill, O. P., Bormann, J., and Sakmann, B. (1983). Activation of multiple-conductance state chloride channels in spinal neurones by glycine and GABA. Nature 305, 805-808.
28. Hanson, G. T., McAnaney, T. B., Park, E. S., Rendell, M. E. P., Yarbrough, D. K., Chu, S., Xi, L., Boxer, S. G., Montrose, M. H., and Remington, S. J. (2002). Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminary application. Biochemistry 41, 15477-15488.
29. Jayaraman, S., Haggie, P., Wachter, R. M., Remington, S. J., and Verkman, A. S. (2000). Mechanism and cellular applications of a green fluorescent protein-based halide sensor. J. Biol. Chem. 275, 6047-6050.
30. Krishtal, O. A., Osipchuk, Y. V., Shelest, T. N., and Smirnoff, S. V. (1987). Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res. 436, 352-356.
31. Kuner, T., and Augustine, G. J. (2000). A genetically encoded ratiomet-ric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 27, 447-459.
32. Makani, S., and Chesler, M. (2010). Rapid rise of extracellular pH evoked by neural activity is generated by the plasma membrane calcium ATPase. J. Neurophysiol. 103, 667.
33. Markova, O., Mukhtarov, M., Real, E., Jacob, Y., and Bregestovski, P. (2008). Genetically encoded chloride indicator with improved sensitivity. J. Neurosci. Methods 170, 67-76.
34. Miesenböck, G. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
35. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikurak, M., and Tsien, R. Y. (1997). Fluorescent indicators for calcium based on green fluorescent proteins and calmodulin. Nature 388, 883.
36. Mody, I., Lambert, J. D., and Heinemann, U. (1987). Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J. Neurophysiol. 57, 869-888.
37. Opie, L. (1965). Effect of extracellular pH on function and metabolism of isolated perfused rat heart. Am. J. Physiol. 209, 1075-1080.
38. Pasternack, M., Voipio, J., and Kaila, K. (1993). Intracellular carbonic anhy-drase activity and its role in GABA-induced acidosis in isolated rat hippocampal pyramidal neurones. Acta Physiol. Scand. 148, 229-231.
39. Putney, L. K., and Barber, D. L. (2003). Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J. Biol. Chem. 278, 44645-44649.
40. Rose, C. R., and Deitmer, J. W. (1995). Stimulus-evoked changes of extra-and intracellular pH in the leech central nervous system. II. Mechanisms and maintenance of pH homeostasis. J. Neurophysiol. 73, 132-140.
41. Schwiening, C. J., Kennedy, H. J., and Thomas, R. C. (1993). Calcium-hydrogen exchange by the plasma membrane Ca-ATPase of voltage-clamped snail neurons. Proc. Biol. Sci. 253, 285-289.
42. Stoppini, L., Buchs, P. A., and Muller, D. (1991). A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182.
43. 2+ in neocortical tissue of epileptic and primary nonepileptic patients. Brain Res. 733, 307-311.
44. Svichar, N., Esquenazi, S., Chen, H.-Y., and Chesler, M. (2011). Preemptive regulation of intracellular pH in hippocampal neurons by a dual mechanism of depolarization-induced alkalinization. J. Neurosci. 31, 6997-7004.
45. Tabb, J., Kish, P., Van Dyke, R., and Ueda, T. (1992). Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesic-ular pH. J. Biol. Chem. 267, 15412-15418.
46. Tramier, M., Zahid, M., Mevel, J.-C., Masse, M.-J., and Coppey-Moisan, M. (2006). Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microsc. Res. Tech. 69, 933-939.
47. Trapp, S., Luckermann, M., Brooks, P. A., and Ballanyi, K. (1996). Acidosis of rat dorsal vagal neurons in situ during spontaneous and evoked activity. J. Physiol. 496, 695-710.
48. Tsien, R. Y. (1998). The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544.
49. Urbanics, R., Leniger-Follert, E., and Ltibbers, D. (1978). Time course of changes of extracellular H+ and K+ activities during and after direct electrical stimulation of the brain cortex. Pflugers Arch. 53, 47-53.
50. 2+ loads. J. Neurophysiol. 72, 2563-2569.
51. Xiong, Z. Q., Saggau, P., and Stringer, J. L. (2000). Activity-dependent intracellular acidification correlates with the duration of seizure activity. J. Neurosci. 20, 1290.
52. Yamamoto, C., and Kawai, N. (1967). Seizure discharges evoked in vitro in thin section from guinea pig hippocampus. Science155, 341-342.
53. Yamamoto, C., and Kawai, N. (1968). Generation of the seizure discharge in thin sections from the guinea pig brain in chloride-free medium in vitro. Jpn. J. Physiol. 18, 620-631.
54. Yamamoto, C., and Kawai, N. (1969). Origin of the seizure discharge evoked in vitro in thin sections from the guinea pig dentate gyrus. Jpn. J. Physiol. 19, 119-129.
55. 2+ indicators. Science 557, 1888-1891.
56. Zucker, R. M., and Price, O. (2001). Evaluation of confocal microscopy system performance. Cytometry 44, 273-294.