Acid-sensing ion channels contribute to synaptic transmission and inhibit cocaine-evoked plasticity

Nature Neuroscience

Volumn 17, Issue 8, 2014, Pages 1083-1091

  Kreple, Collin J ^a   Lu, Yuan ^a   Taugher, Rebecca J ^b   Schwager Gutman, Andrea L ^c   Du, Jianyang ^a   Stump, Madeliene ^a,b   Wang, Yimo ^a   Ghobbeh, Ali ^a   Fan, Rong ^a   Cosme, Caitlin V ^c   Sowers, Levi P ^a   Welsh, Michael J ^a,b,c,d   Radley, Jason J ^b,c   Lalumiere, Ryan T ^b,c   Wemmie, John A ^a,b,e  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c University of Iowa   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1A; COCAINE; GLUTAMATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL MODEL; ARTICLE; CELL DENSITY; CELL FUNCTION; CELL STRUCTURE; CONDITIONED PLACE PREFERENCE TEST; DENDRITIC SPINE; DRUG DEPENDENCE; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HUMAN; HYPOTHESIS; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; STATE DEPENDENT LEARNING; SYNAPTIC TRANSMISSION;

ACID SENSING ION CHANNELS; ANIMALS; BEHAVIOR, ANIMAL; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONAL PLASTICITY; NUCLEUS ACCUMBENS; RATS; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 84905090174     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3750     Document Type: Article

References (54)

1. Russo, S.J. et al. The addicted synapse: Mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267-276 (2010
2. Luscher, C.&Malenka, R.C. Drug-evoked synaptic plasticity in addiction: From molecular changes to circuit remodeling. Neuron 69, 650-663 (2011
3. Kalivas, P.W. The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572 (2009
4. Wemmie, J.A., Taugher, R.J.&Kreple, C.J. Acid-sensing ion channels in pain and disease. Nat. Rev. Neurosci. 14, 461-471 (2013
5. Jasti, J., Furukawa, H., Gonzales, E.B.&Gouaux, E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 449, 316-323 (2007
6. Hesselager, M., Timmermann, D.B.&Ahring, P.K. pH-dependency and desensitization kinetics of heterologously expressed combinations of ASIC subunits. J. Biol. Chem. 279, 11006-11015 (2004
7. Benson, C.J. et al. Heteromultimerics of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc. Natl. Acad. Sci. USA 99, 2338-2343 (2002
8. Askwith, C.C., Wemmie, J.A., Price, M.P., Rokhlina, T.&Welsh, M.J. Acid-sensing ion channel 2 (ASIC2) modulates ASIC1 H+-Activated currents in hippocampal neurons. J. Biol. Chem. 279, 18296-18305 (2004
9. Wemmie, J.A. et al. The acid-Activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34, 463-477 (2002
10. Wemmie, J.A. et al. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci 23, 5496-5502 (2003
11. Ziemann, A.E. et al. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell 139, 1012-1021 (2009
12. Wemmie, J.A. et al. Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc. Natl. Acad. Sci. USA 101, 3621-3626 (2004
13. Zha, X.M., Wemmie, J.A., Green, S.H.&Welsh, M.J. Acid-sensing ion channel 1a is a postsynaptic proton receptor that affects the density of dendritic spines. Proc. Natl. Acad. Sci. USA 103, 16556-16561 (2006
14. Zha, X.M. et al. ASIC2 subunits target acid-sensing ion channels to the synapse via an association with PSD-95. J. Neurosci. 29, 8438-8446 (2009
15. Baron, A. et al. Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1. J. Biol. Chem. 277, 50463-50468 (2002
16. Wu, P.Y. et al. Acid-sensing ion channel-1a is not required for normal hippocampal LTP and spatial memory. J. Neurosci. 33, 1828-1832 (2013
17. Cho, J.H.&Askwith, C.C. Presynaptic release probability is increased in hippocampal neurons from ASIC1 knockout mice. J. Neurophysiol. 99, 426-441 (2008
18. Alvarez De La Rosa, D. et al. Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J. Physiol. 546, 77-87 (2003
19. Huston, J.P., Silva, M.A., Topic, B.&Muller, C.P. What?s conditioned in conditioned place preference? Trends Pharmacol. Sci. 34, 162-166 (2013
20. Napier, T.C., Herrold, A.A.&De Wit, H. Using conditioned place preference to identify relapse prevention medications. Neurosci. Biobehav. Rev. 37, 2081-2086 (2013
21. White, N.M., Chai, S.C.&Hamdani, S. Learning the morphine conditioned cue preference: Cue configuration determines effects of lesions. Pharmacol. Biochem. Behav. 81, 786-796 (2005
22. Coryell, M.W. et al. Restoring Acid-sensing ion channel-1a in the amygdala of knock-out mice rescues fear memory but not unconditioned fear responses. J. Neurosci. 28, 13738-13741 (2008
23. DeVries, S.H. Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron 32, 1107-1117 (2001
24. Miesenböck, G., De Angelis, D.A.&Rothman, J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195 (1998
25. Palmer, M.J., Hull, C., Vigh, J.&von Gersdorff, H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J. Neurosci. 23, 11332-11341 (2003
26. Vessey, J.P. et al. Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J. Neurosci. 25, 4108-4117 (2005
27. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C.&Lazdunski, M. A proton-gated cation channel involved in acid-sensing. Nature 386, 173-177 (1997
28. Krishtal, O.A., Osipchuk, Y.V., Shelest, T.N.&Smirnoff, S.V. Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res. 436, 352-356 (1987
29. Gillessen, T.&Alzheimer, C. Amplification of EPSPs by low Ni2+- and amiloride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J. Neurophysiol. 77, 1639-1643 (1997
30. Manev, H., Bertolino, M.&DeErausquin, G. Amiloride blocks glutamate-operated cationic channels and protects neurons in culture from glutamate-induced death. Neuropharmacology 29, 1103-1110 (1990
31. Price, M.P. et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407, 1007-1011 (2000
32. Escoubas, P. et al. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J. Biol. Chem. 275, 25116-25121 (2000
33. Sherwood, T.W., Lee, K.G., Gormley, M.G.&Askwith, C.C. Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J. Neurosci. 31, 9723-9734 (2011
34. Shah, G.N. et al. Carbonic anhydrase IV and XIV knockout mice: Roles of the respective carbonic anhydrases in buffering the extracellular space in brain. Proc. Natl. Acad. Sci. USA 102, 16771-16776 (2005
35. Harris, K.M.&Kater, S.B. Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341-371 (1994
36. Dietz, D.M. et al. Rac1 is essential in cocaine-induced structural plasticity of nucleus accumbens neurons. Nat. Neurosci. 15, 891-896 (2012
37. Conrad, K.L. et al. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454, 118-121 (2008
38. Mameli, M. et al. Cocaine-evoked synaptic plasticity: Persistence in the VTA triggers adaptations in the NAc. Nat. Neurosci. 12, 1036-1041 (2009
39. Kourrich, S., Rothwell, P.E., Klug, J.R.&Thomas, M.J. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J. Neurosci. 27, 7921-7928 (2007
40. Moussawi, K. et al. Reversing cocaine-induced synaptic potentiation provides enduring protection from relapse. Proc. Natl. Acad. Sci. USA 108, 385-390 (2011
41. Eisch, A.J. et al. Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: A role in depression. Biol. Psychiatry 54, 994-1005 (2003
42. Shirayama, Y., Chen, A.C., Nakagawa, S., Russell, D.S.&Duman, R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22, 3251-3261 (2002
43. Miesenbock, G., De Angelis, D.A.&Rothman, J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195 (1998
44. Beg, A.A., Ernstrom, G.G., Nix, P., Davis, M.W.&Jorgensen, E.M. Protons act as a transmitter for muscle contraction in C. elegans. Cell 132, 149-160 (2008
45. Zeng, W.Z.&Xu, T.L. Proton production, regulation and pathophysiological roles in the mammalian brain. Neurosci. Bull. 28, 1-13 (2012
46. Zha, X.M. Acid-sensing ion channels: Trafficking and synaptic function. Mol. Brain 6, 1 (2013
47. Lee, K.W. et al. Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc. Natl. Acad. Sci. USA 103, 3399-3404 (2006
48. Golden, S.A.&Russo, S.J. Mechanisms of psychostimulant-induced structural plasticity. Cold Spring Harb. Perspect. Med. 2, a011957 (2012
49. Christoffel, D.J. et al. IkappaB kinase regulates social defeat stress-induced synaptic and behavioral plasticity. J. Neurosci. 31, 314-321 (2011
50. Jiang, Q., Wang, C.M., Fibuch, E.E., Wang, J.Q.&Chu, X.P. Differential regulation of locomotor activity to acute and chronic cocaine administration by acid-sensing ion channel 1a and 2 in adult mice. Neuroscience 246, 170-178 (2013
51. Radley, J.J., Anderson, R.M., Hamilton, B.A., Alcock, J.A.&Romig-Martin, S.A. Chronic stress-induced alterations of dendritic spine subtypes predict functional decrements in an hypothalamo-pituitary- Adrenal-inhibitory prefrontal circuit. J. Neurosci. 33, 14379-14391 (2013
52. Radley, J.J. et al. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J. Comp. Neurol. 507, 1141-1150 (2008
53. Rodriguez, A., Ehlenberger, D.B., Dickstein, D.L., Hof, P.R.&Wearne, S.L. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3, e1997 (2008
54. LaLumiere, R.T., Smith, K.C.&Kalivas, P.W. Neural circuit competition in cocaine-seeking: Roles of the infralimbic cortex and nucleus accumbens shell. Eur. J. Neurosci. 35, 614-622 (2012