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Molecular Brain
Published in: Molecular Brain 1/2014

Open Access 01-12-2014 | Research article

Postsynaptic insertion of AMPA receptor onto cortical pyramidal neurons in the anterior cingulate cortex after peripheral nerve injury

Authors: Tao Chen, Wen Wang, Yu-Lin Dong, Ming-Ming Zhang, Jian Wang, Kohei Koga, Yong-Hui Liao, Jin-Lian Li, Timotheus Budisantoso, Ryuichi Shigemoto, Makoto Itakura, Richard L Huganir, Yun-Qing Li, Min Zhuo

Published in: Molecular Brain | Issue 1/2014

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Abstract

Long-term potentiation (LTP) is the key cellular mechanism for physiological learning and pathological chronic pain. Postsynaptic accumulation of AMPA receptor (AMPAR) GluA1 plays an important role for injury-related cortical LTP. However, there is no direct evidence for postsynaptic GluA1 insertion or accumulation after peripheral injury. Here we report nerve injury increased the postsynaptic expression of AMPAR GluA1 in pyramidal neurons in the layer V of the anterior cingulate cortex (ACC), including the corticospinal projecting neurons. Electrophysiological recordings show that potentiation of postsynaptic responses was reversed by Ca2+ permeable AMPAR antagonist NASPM. Finally, behavioral studies show that microinjection of NASPM into the ACC inhibited behavioral sensitization caused by nerve injury. Our findings provide direct evidence that peripheral nerve injury induces postsynaptic GluA1 accumulation in cingulate cortical neurons, and inhibits postsynaptic GluA1 accumulation which may serve as a novel target for treating neuropathic pain.
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Literature
1.
Zhuo M: Silent glutamatergic synapses and long-term facilitation in spinal dorsal horn neurons. Prog Brain Res. 2000, 129: 101-113. 10.1016/S0079-6123(00)29008-0.PubMedCrossRef
2.
Zhuo M: Long-term potentiation in the anterior cingulate cortex and chronic pain. Philos Trans R Soc Lond B Biol Sci. 2014, 369: 20130146-10.1098/rstb.2013.0146.PubMedPubMedCentralCrossRef
3.
Anggono V, Huganir RL: Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol. 2012, 22: 461-469. 10.1016/j.conb.2011.12.006.PubMedPubMedCentralCrossRef
4.
Bliss TV, Collingridge GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993, 361: 31-39. 10.1038/361031a0.PubMedCrossRef
5.
Collingridge GL, Isaac JT, Wang YT: Receptor trafficking and synaptic plasticity. Nat Rev Neurosci. 2004, 5: 952-962. 10.1038/nrn1556.PubMedCrossRef
6.
Cooke SF, Bliss TV: Plasticity in the human central nervous system. Brain. 2006, 129: 1659-1673. 10.1093/brain/awl082.PubMedCrossRef
7.
Lu W, Roche KW: Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol. 2012, 22: 470-479. 10.1016/j.conb.2011.09.008.PubMedPubMedCentralCrossRef
8.
Zhuo M: Cortical excitation and chronic pain. Trends Neurosci. 2008, 31: 199-207. 10.1016/j.tins.2008.01.003.PubMedCrossRef
9.
10.
Qiu S, Chen T, Koga K, Guo YY, Xu H, Song Q, Wang JJ, Descalzi G, Kaang BK, Luo JH, Zhuo M, Zhao MG: An increase in synaptic NMDA receptors in the insular cortex contributes to neuropathic pain. Sci Signal. 2013, 6: ra34-PubMedCrossRef
11.
Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M: Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci. 2008, 28: 7445-7453. 10.1523/JNEUROSCI.1812-08.2008.PubMedPubMedCentralCrossRef
12.
Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, Zhuo M: Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J Neurosci. 2006, 26: 8923-8930. 10.1523/JNEUROSCI.2103-06.2006.PubMedCrossRef
13.
Zhuo M: A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Mol Cells. 2007, 23: 259-271.PubMed
14.
Bie B, Brown DL, Naguib M: Increased synaptic GluR1 subunits in the anterior cingulate cortex of rats with peripheral inflammation. Eur J Pharmacol. 2010, 653: 26-31. 10.1016/j.ejphar.2010.11.027.PubMedCrossRef
15.
Chen T, Koga K, Descalzi G, Qiu S, Wang J, Zhang LS, Zhang ZJ, He XB, Qin X, Xu FQ, Hu J, Wei F, Huganir RL, Li YQ, Zhuo M: Postsynaptic potentiation of corticospinal projecting neurons in the anterior cingulate cortex after nerve injury. Mol Pain. 2014, 10: 33-10.1186/1744-8069-10-33.PubMedPubMedCentralCrossRef
16.
Toyoda H, Wu LJ, Zhao MG, Xu H, Zhuo M: Time-dependent postsynaptic AMPA GluR1 receptor recruitment in the cingulate synaptic potentiation. Dev Neurobiol. 2007, 67: 498-509. 10.1002/dneu.20380.PubMedCrossRef
17.
Toyoda H, Zhao MG, Ulzhofer B, Wu LJ, Xu H, Seeburg PH, Sprengel R, Kuner R, Zhuo M: Roles of the AMPA receptor subunit GluA1 but not GluA2 in synaptic potentiation and activation of ERK in the anterior cingulate cortex. Mol Pain. 2009, 5: 46-10.1186/1744-8069-5-46.PubMedPubMedCentralCrossRef
18.
Derkach VA, Oh MC, Guire ES, Soderling TR: Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci. 2007, 8: 101-113. 10.1038/nrn2055.PubMedCrossRef
19.
Rumpel S, LeDoux J, Zador A, Malinow R: Postsynaptic receptor trafficking underlying a form of associative learning. Science. 2005, 308: 83-88. 10.1126/science.1103944.PubMedCrossRef
20.
Takahashi T, Svoboda K, Malinow R: Experience strengthening transmission by driving AMPA receptors into synapses. Science. 2003, 299: 1585-1588. 10.1126/science.1079886.PubMedCrossRef
21.
Naskar S, Wan H, Kemenes G: pT305-CaMKII stabilizes a learning-induced increase in AMPA receptors for ongoing memory consolidation after classical conditioning. Nat Commun. 2014, 5: 3967-10.1038/ncomms4967.PubMedPubMedCentralCrossRef
22.
Bredt DS, Nicoll RA: AMPA receptor trafficking at excitatory synapses. Neuron. 2003, 40: 361-379. 10.1016/S0896-6273(03)00640-8.PubMedCrossRef
23.
24.
Hu H, Real E, Takamiya K, Kang MG, Ledoux J, Huganir RL, Malinow R: Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell. 2007, 131: 160-173. 10.1016/j.cell.2007.09.017.PubMedCrossRef
25.
Malenka RC: Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci. 2003, 1003: 1-11. 10.1196/annals.1300.001.PubMedCrossRef
26.
Shi S, Hayashi Y, Esteban JA, Malinow R: Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 2001, 105: 331-343. 10.1016/S0092-8674(01)00321-X.PubMedCrossRef
27.
Masugi-Tokita M, Shigemoto R: High-resolution quantitative visualization of glutamate and GABA receptors at central synapses. Curr Opin Neurobiol. 2007, 17: 387-393. 10.1016/j.conb.2007.04.012.PubMedCrossRef
28.
29.
Benke TA, Luthi A, Isaac JT, Collingridge GL: Modulation of AMPA receptor unitary conductance by synaptic activity. Nature. 1998, 393: 793-797. 10.1038/31709.PubMedCrossRef
30.
Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M: Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science. 2010, 330: 1400-1404. 10.1126/science.1191792.PubMedCrossRef
31.
Clem RL, Barth A: Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron. 2006, 49: 663-670. 10.1016/j.neuron.2006.01.019.PubMedCrossRef
32.
Chen T, Lu JS, Song Q, Liu MG, Koga K, Descalzi G, Li YQ, Zhuo M: Pharmacological Rescue of Cortical Synaptic and Network Potentiation in a Mouse Model for Fragile X Syndrome. Neuropsychopharmacology. 2014, 39: 1955-1967. 10.1038/npp.2014.44.PubMedPubMedCentralCrossRef
33.
Kang SJ, Liu MG, Chen T, Ko HG, Baek GC, Lee HR, Lee K, Collingridge GL, Kaang BK, Zhuo M: Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. J Neurosci. 2012, 32: 11318-11329. 10.1523/JNEUROSCI.0146-12.2012.PubMedCrossRef
34.
Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, Petralia RS, Wenthold RJ, Gallagher M, Huganir RL: Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 2003, 112: 631-643. 10.1016/S0092-8674(03)00122-3.PubMedCrossRef
35.
36.
Calejesan AA, Kim SJ, Zhuo M: Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain. 2000, 4: 83-96. 10.1053/eujp.1999.0158.PubMedCrossRef
37.
Bee LA, Dickenson AH: Descending facilitation from the brainstem determines behavioural and neuronal hypersensitivity following nerve injury and efficacy of pregabalin. Pain. 2008, 140: 209-223. 10.1016/j.pain.2008.08.008.PubMedCrossRef
38.
Svensson CI, Tran TK, Fitzsimmons B, Yaksh TL, Hua XY: Descending serotonergic facilitation of spinal ERK activation and pain behavior. FEBS Lett. 2006, 580: 6629-6634. 10.1016/j.febslet.2006.11.012.PubMedPubMedCentralCrossRef
39.
Zhuo M, Gebhart GF: Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J Neurophysiol. 1997, 78: 746-758.PubMed
40.
Zhuo M, Gebhart GF: Modulation of noxious and non-noxious spinal mechanical transmission from the rostral medial medulla in the rat. J Neurophysiol. 2002, 88: 2928-2941. 10.1152/jn.00005.2002.PubMedCrossRef
41.
Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE, Zhuo M: Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature. 1999, 397: 161-164. 10.1038/16469.PubMedCrossRef
42.
Li P, Zhuo M: Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature. 1998, 393: 695-698. 10.1038/31496.PubMedCrossRef
43.
Kerchner GA, Wilding TJ, Li P, Zhuo M, Huettner JE: Presynaptic kainate receptors regulate spinal sensory transmission. J Neurosci. 2001, 21: 59-66.PubMed
44.
Liauw J, Wu LJ, Zhuo M: Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. J Neurophysiol. 2005, 94: 878-882. 10.1152/jn.01205.2004.PubMedCrossRef
45.
Wang H, Xu H, Wu LJ, Kim SS, Chen T, Koga K, Descalzi G, Gong B, Vadakkan KI, Zhang X, Kaang BK, Zhuo M: Identification of an adenylyl cyclase inhibitor for treating neuropathic and inflammatory pain. Sci Transl Med. 2011, 3: 65-a63
46.
Vadakkan KI, Jia YH, Zhuo M: A behavioral model of neuropathic pain induced by ligation of the common peroneal nerve in mice. J Pain. 2005, 6: 747-756. 10.1016/j.jpain.2005.07.005.PubMedCrossRef
47.
Tillu DV, Gebhart GF, Sluka KA: Descending facilitatory pathways from the RVM initiate and maintain bilateral hyperalgesia after muscle insult. Pain. 2008, 136: 331-339. 10.1016/j.pain.2007.07.011.PubMedPubMedCentralCrossRef
48.
Harris KM, Landis DM: Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience. 1986, 19: 857-872. 10.1016/0306-4522(86)90304-0.PubMedCrossRef
49.
Chen T, Hui R, Wang XL, Zhang T, Dong YX, Li YQ: Origins of endomorphin-immunoreactive fibers and terminals in different columns of the periaqueductal gray in the rat. J Comp Neurol. 2008, 509: 72-87. 10.1002/cne.21728.PubMedCrossRef
50.
Hui R, Wang W, Chen T, Lu BC, Li H, Zhang T, Wu SX, Li YQ: Origins of endomorphin-2 immunopositive fibers and terminals in the spinal dorsal horn of the rat. Neuroscience. 2010, 169: 422-430. 10.1016/j.neuroscience.2010.05.006.PubMedCrossRef
51.
Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M: Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron. 2005, 47: 859-872. 10.1016/j.neuron.2005.08.014.PubMedCrossRef
52.
Traynelis SF, Silver RA, Cull-Candy SG: Estimated conductance of glutamate receptor channels activated during EPSCs at the cerebellar mossy fiber-granule cell synapse. Neuron. 1993, 11: 279-289. 10.1016/0896-6273(93)90184-S.PubMedCrossRef
53.
Wu LJ, Zhao MG, Toyoda H, Ko SW, Zhuo M: Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol. 2005, 94: 1805-1813. 10.1152/jn.00091.2005.PubMedCrossRef
Metadata
Title
Postsynaptic insertion of AMPA receptor onto cortical pyramidal neurons in the anterior cingulate cortex after peripheral nerve injury
Authors
Tao Chen
Wen Wang
Yu-Lin Dong
Ming-Ming Zhang
Jian Wang
Kohei Koga
Yong-Hui Liao
Jin-Lian Li
Timotheus Budisantoso
Ryuichi Shigemoto
Makoto Itakura
Richard L Huganir
Yun-Qing Li
Min Zhuo
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Molecular Brain / Issue 1/2014
Electronic ISSN: 1756-6606
DOI
https://doi.org/10.1186/s13041-014-0076-8

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