Skip to main content
Top
Published in: Molecular Pain 1/2009

Open Access 01-12-2009 | Research

Roles of the AMPA receptor subunit GluA1 but not GluA2 in synaptic potentiation and activation of ERK in the anterior cingulate cortex

Authors: Hiroki Toyoda, Ming-Gao Zhao, Bettina Ulzhöfer, Long-Jun Wu, Hui Xu, Peter H Seeburg, Rolf Sprengel, Rohini Kuner, Min Zhuo

Published in: Molecular Pain | Issue 1/2009

Login to get access

Abstract

Cortical areas including the anterior cingulate cortex (ACC) are important for pain and pleasure. Recent studies using genetic and physiological approaches have demonstrated that the investigation of basic mechanism for long-term potentiation (LTP) in the ACC may reveal key cellular and molecular mechanisms for chronic pain in the cortex. Glutamate N-methyl D-aspartate (NMDA) receptors in the ACC are critical for the induction of LTP, including both NR2A and NR2B subunits. However, cellular and molecular mechanisms for the expression of ACC LTP have been less investigated. Here, we report that the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunit, GluA1 but not GluA2 contributes to LTP in the ACC using genetic manipulated mice lacking GluA1 or GluA2 gene. Furthermore, GluA1 knockout mice showed decreased extracellular signal-regulated kinase (ERK) phosphorylation in the ACC in inflammatory pain models in vivo. Our results demonstrate that AMPA receptor subunit GluA1 is a key mechanism for the expression of ACC LTP and inflammation-induced long-term plastic changes in the ACC.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kandel ER: The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294: 1030–1038.PubMedCrossRef Kandel ER: The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294: 1030–1038.PubMedCrossRef
3.
go back to reference Hyman SE, Malenka RC, Nestler EJ: Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29: 565–598.PubMedCrossRef Hyman SE, Malenka RC, Nestler EJ: Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29: 565–598.PubMedCrossRef
4.
go back to reference Bliss TV, Collingridge GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361: 31–39.PubMedCrossRef Bliss TV, Collingridge GL: A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361: 31–39.PubMedCrossRef
6.
go back to reference Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M: Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 2005, 1: 6.PubMedCentralPubMedCrossRef Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M: Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 2005, 1: 6.PubMedCentralPubMedCrossRef
7.
go back to reference Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M: Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci 2001, 4: 164–169.PubMedCrossRef Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M: Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci 2001, 4: 164–169.PubMedCrossRef
8.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
9.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
10.
11.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
12.
go back to reference Shum FW, Wu LJ, Zhao MG, Toyoda H, Xu H, Ren M, Pinaud R, Ko SW, Lee YS, Kaang BK, Zhuo M: Alteration of cingulate long-term plasticity and behavioral sensitization to inflammation by environmental enrichment. Learn Mem 2007, 14: 304–312.PubMedCentralPubMedCrossRef Shum FW, Wu LJ, Zhao MG, Toyoda H, Xu H, Ren M, Pinaud R, Ko SW, Lee YS, Kaang BK, Zhuo M: Alteration of cingulate long-term plasticity and behavioral sensitization to inflammation by environmental enrichment. Learn Mem 2007, 14: 304–312.PubMedCentralPubMedCrossRef
13.
go back to reference Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, et al.: Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47: 859–872.PubMedCrossRef Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, et al.: Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47: 859–872.PubMedCrossRef
14.
go back to reference Toyoda H, Zhao MG, Xu H, Wu LJ, Ren M, Zhuo M: Requirement of extracellular signal-regulated kinase/mitogen-activated protein kinase for long-term potentiation in adult mouse anterior cingulate cortex. Mol Pain 2007, 3: 36.PubMedCentralPubMedCrossRef Toyoda H, Zhao MG, Xu H, Wu LJ, Ren M, Zhuo M: Requirement of extracellular signal-regulated kinase/mitogen-activated protein kinase for long-term potentiation in adult mouse anterior cingulate cortex. Mol Pain 2007, 3: 36.PubMedCentralPubMedCrossRef
15.
go back to reference Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M: Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 2002, 5: 573–579.PubMedCrossRef Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M: Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 2002, 5: 573–579.PubMedCrossRef
16.
go back to reference Wu LJ, Zhang XH, Fukushima H, Zhang F, Wang H, Toyoda H, Li BM, Kida S, Zhuo M: Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca 2+ /calmodulin-dependent protein kinase IV. Eur J Neurosci 2008, 27: 1923–1932.PubMedCrossRef Wu LJ, Zhang XH, Fukushima H, Zhang F, Wang H, Toyoda H, Li BM, Kida S, Zhuo M: Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca 2+ /calmodulin-dependent protein kinase IV. Eur J Neurosci 2008, 27: 1923–1932.PubMedCrossRef
17.
go back to reference Sah P, Nicoll RA: Mechanisms underlying potentiation of synaptic transmission in rat anterior cingulate cortex in vitro. J Physiol 1991, 433: 615–630.PubMedCentralPubMedCrossRef Sah P, Nicoll RA: Mechanisms underlying potentiation of synaptic transmission in rat anterior cingulate cortex in vitro. J Physiol 1991, 433: 615–630.PubMedCentralPubMedCrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference Wei F, Li P, Zhuo M: Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999, 19: 9346–9354.PubMed Wei F, Li P, Zhuo M: Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999, 19: 9346–9354.PubMed
20.
go back to reference Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS: Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 1996, 16: 1982–1989.PubMed Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS: Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 1996, 16: 1982–1989.PubMed
21.
go back to reference Tsuzuki K, Lambolez B, Rossier J, Ozawa S: Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons. J Neurochem 2001, 77: 1650–1659.PubMedCrossRef Tsuzuki K, Lambolez B, Rossier J, Ozawa S: Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons. J Neurochem 2001, 77: 1650–1659.PubMedCrossRef
22.
go back to reference Petralia RS, Wenthold RJ: Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 1992, 318: 329–354.PubMedCrossRef Petralia RS, Wenthold RJ: Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 1992, 318: 329–354.PubMedCrossRef
24.
go back to reference Frey MC, Sprengel R, Nevian T: Activity pattern-dependent long-term potentiation in neocortex and hippocampus of GluA1 (GluR-A) subunit-deficient mice. J Neurosci 2009, 29: 5587–5596.PubMedCrossRef Frey MC, Sprengel R, Nevian T: Activity pattern-dependent long-term potentiation in neocortex and hippocampus of GluA1 (GluR-A) subunit-deficient mice. J Neurosci 2009, 29: 5587–5596.PubMedCrossRef
25.
go back to reference Jensen V, Kaiser KM, Borchardt T, Adelmann G, Rozov A, Burnashev N, Brix C, Frotscher M, Andersen P, Hvalby O, et al.: A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J Physiol 2003, 553: 843–856.PubMedCentralPubMedCrossRef Jensen V, Kaiser KM, Borchardt T, Adelmann G, Rozov A, Burnashev N, Brix C, Frotscher M, Andersen P, Hvalby O, et al.: A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J Physiol 2003, 553: 843–856.PubMedCentralPubMedCrossRef
26.
go back to reference Romberg C, Raffel J, Martin L, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM, Paulsen O: Induction and expression of GluA1 (GluR-A)-independent LTP in the hippocampus. Eur J Neurosci 2009, 29: 1141–1152.PubMedCentralPubMedCrossRef Romberg C, Raffel J, Martin L, Sprengel R, Seeburg PH, Rawlins JN, Bannerman DM, Paulsen O: Induction and expression of GluA1 (GluR-A)-independent LTP in the hippocampus. Eur J Neurosci 2009, 29: 1141–1152.PubMedCentralPubMedCrossRef
27.
go back to reference Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, et al.: Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 1999, 284: 1805–1811.PubMedCrossRef Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, et al.: Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 1999, 284: 1805–1811.PubMedCrossRef
28.
go back to reference Kakegawa W, Yuzaki M: A mechanism underlying AMPA receptor trafficking during cerebellar long-term potentiation. Proc Natl Acad Sci USA 2005, 102: 17846–17851.PubMedCentralPubMedCrossRef Kakegawa W, Yuzaki M: A mechanism underlying AMPA receptor trafficking during cerebellar long-term potentiation. Proc Natl Acad Sci USA 2005, 102: 17846–17851.PubMedCentralPubMedCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference Zhuo M: Glutamate receptors and persistent pain: targeting forebrain NR2B subunits. Drug Discov Today 2002, 7: 259–267.PubMedCrossRef Zhuo M: Glutamate receptors and persistent pain: targeting forebrain NR2B subunits. Drug Discov Today 2002, 7: 259–267.PubMedCrossRef
31.
go back to reference Zhuo M: A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Mol Cells 2007, 23: 259–271.PubMed Zhuo M: A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Mol Cells 2007, 23: 259–271.PubMed
32.
go back to reference Zhuo M: Molecular mechanisms of pain in the anterior cingulate cortex. J Neurosci Res 2006, 84: 927–933.PubMedCrossRef Zhuo M: Molecular mechanisms of pain in the anterior cingulate cortex. J Neurosci Res 2006, 84: 927–933.PubMedCrossRef
33.
go back to reference Crair MC, Malenka RC: A critical period for long-term potentiation at thalamocortical synapses. Nature 1995, 375: 325–328.PubMedCrossRef Crair MC, Malenka RC: A critical period for long-term potentiation at thalamocortical synapses. Nature 1995, 375: 325–328.PubMedCrossRef
34.
go back to reference Buonomano DV, Merzenich MM: Cortical plasticity: from synapses to maps. Annu Rev Neurosci 1998, 21: 149–186.PubMedCrossRef Buonomano DV, Merzenich MM: Cortical plasticity: from synapses to maps. Annu Rev Neurosci 1998, 21: 149–186.PubMedCrossRef
35.
go back to reference Isaac JT, Crair MC, Nicoll RA, Malenka RC: Silent synapses during development of thalamocortical inputs. Neuron 1997, 18: 269–280.PubMedCrossRef Isaac JT, Crair MC, Nicoll RA, Malenka RC: Silent synapses during development of thalamocortical inputs. Neuron 1997, 18: 269–280.PubMedCrossRef
36.
go back to reference Wei F, Zhuo M: Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J Physiol 2001, 532: 823–833.PubMedCentralPubMedCrossRef Wei F, Zhuo M: Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J Physiol 2001, 532: 823–833.PubMedCentralPubMedCrossRef
37.
38.
go back to reference Zhuo M: Canadian Association of Neuroscience review: Cellular and synaptic insights into physiological and pathological pain. EJLB-CIHR Michael Smith Chair in Neurosciences and Mental Health lecture. Can J Neurol Sci 2005, 32: 27–36.PubMedCrossRef Zhuo M: Canadian Association of Neuroscience review: Cellular and synaptic insights into physiological and pathological pain. EJLB-CIHR Michael Smith Chair in Neurosciences and Mental Health lecture. Can J Neurol Sci 2005, 32: 27–36.PubMedCrossRef
39.
go back to reference Cao H, Gao YJ, Ren WH, Li TT, Duan KZ, Cui YH, Cao XH, Zhao ZQ, Ji RR, Zhang YQ: Activation of extracellular signal-regulated kinase in the anterior cingulate cortex contributes to the induction and expression of affective pain. J Neurosci 2009, 29: 3307–3321.PubMedCentralPubMedCrossRef Cao H, Gao YJ, Ren WH, Li TT, Duan KZ, Cui YH, Cao XH, Zhao ZQ, Ji RR, Zhang YQ: Activation of extracellular signal-regulated kinase in the anterior cingulate cortex contributes to the induction and expression of affective pain. J Neurosci 2009, 29: 3307–3321.PubMedCentralPubMedCrossRef
40.
41.
go back to reference Johansen JP, Fields HL, Manning BH: The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA 2001, 98: 8077–8082.PubMedCentralPubMedCrossRef Johansen JP, Fields HL, Manning BH: The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA 2001, 98: 8077–8082.PubMedCentralPubMedCrossRef
42.
go back to reference Lee DE, Kim SJ, Zhuo M: Comparison of behavioral responses to noxious cold and heat in mice. Brain Res 1999, 845: 117–121.PubMedCrossRef Lee DE, Kim SJ, Zhuo M: Comparison of behavioral responses to noxious cold and heat in mice. Brain Res 1999, 845: 117–121.PubMedCrossRef
43.
go back to reference Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, Xu HM, Chen ZF, Storm DR, Muglia LJ, Zhuo M: Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 2002, 36: 713–726.PubMedCrossRef Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, Xu HM, Chen ZF, Storm DR, Muglia LJ, Zhuo M: Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 2002, 36: 713–726.PubMedCrossRef
44.
go back to reference Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FW, Zerbinatti CV, Bu G, et al.: Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J Neurosci 2005, 25: 11107–11116.PubMedCrossRef Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FW, Zerbinatti CV, Bu G, et al.: Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J Neurosci 2005, 25: 11107–11116.PubMedCrossRef
45.
go back to reference Wu LJ, Steenland HW, Kim SS, Isiegas C, Abel T, Kaang BK, Zhuo M: Enhancement of presynaptic glutamate release and persistent inflammatory pain by increasing neuronal cAMP in the anterior cingulate cortex. Mol Pain 2008, 4: 40.PubMedCentralPubMedCrossRef Wu LJ, Steenland HW, Kim SS, Isiegas C, Abel T, Kaang BK, Zhuo M: Enhancement of presynaptic glutamate release and persistent inflammatory pain by increasing neuronal cAMP in the anterior cingulate cortex. Mol Pain 2008, 4: 40.PubMedCentralPubMedCrossRef
46.
go back to reference Wei F, Xia XM, Tang J, Ao H, Ko S, Liauw J, Qiu CS, Zhuo M: Calmodulin regulates synaptic plasticity in the anterior cingulate cortex and behavioral responses: a microelectroporation study in adult rodents. J Neurosci 2003, 23: 8402–8409.PubMed Wei F, Xia XM, Tang J, Ao H, Ko S, Liauw J, Qiu CS, Zhuo M: Calmodulin regulates synaptic plasticity in the anterior cingulate cortex and behavioral responses: a microelectroporation study in adult rodents. J Neurosci 2003, 23: 8402–8409.PubMed
48.
go back to reference Yang Y, Wang XB, Frerking M, Zhou Q: Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci USA 2008, 105: 11388–11393.PubMedCentralPubMedCrossRef Yang Y, Wang XB, Frerking M, Zhou Q: Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci USA 2008, 105: 11388–11393.PubMedCentralPubMedCrossRef
49.
go back to reference Phillips KG, Hardingham NR, Fox K: Postsynaptic action potentials are required for nitric-oxide-dependent long-term potentiation in CA1 neurons of adult GluR1 knock-out and wild-type mice. J Neurosci 2008, 28: 14031–14041.PubMedCentralPubMedCrossRef Phillips KG, Hardingham NR, Fox K: Postsynaptic action potentials are required for nitric-oxide-dependent long-term potentiation in CA1 neurons of adult GluR1 knock-out and wild-type mice. J Neurosci 2008, 28: 14031–14041.PubMedCentralPubMedCrossRef
50.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
51.
go back to reference Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R: Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999, 284: 1811–1816.PubMedCrossRef Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R: Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999, 284: 1811–1816.PubMedCrossRef
52.
go back to reference Passafaro M, Piech V, Sheng M: Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 2001, 4: 917–926.PubMedCrossRef Passafaro M, Piech V, Sheng M: Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 2001, 4: 917–926.PubMedCrossRef
53.
go back to reference Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R: Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000, 287: 2262–2267.PubMedCrossRef Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R: Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000, 287: 2262–2267.PubMedCrossRef
54.
go back to reference Mack V, Burnashev N, Kaiser KM, Rozov A, Jensen V, Hvalby O, Seeburg PH, Sakmann B, Sprengel R: Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 2001, 292: 2501–2504.PubMedCrossRef Mack V, Burnashev N, Kaiser KM, Rozov A, Jensen V, Hvalby O, Seeburg PH, Sakmann B, Sprengel R: Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 2001, 292: 2501–2504.PubMedCrossRef
55.
go back to reference Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R: Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110: 443–455.PubMedCrossRef Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R: Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110: 443–455.PubMedCrossRef
56.
go back to reference Song I, Huganir RL: Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 2002, 25: 578–588.PubMedCrossRef Song I, Huganir RL: Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 2002, 25: 578–588.PubMedCrossRef
57.
go back to reference Shepherd JD, Huganir RL: The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 2007, 23: 613–643.PubMedCrossRef Shepherd JD, Huganir RL: The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 2007, 23: 613–643.PubMedCrossRef
58.
go back to reference Derkach VA, Oh MC, Guire ES, Soderling TR: Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 2007, 8: 101–113.PubMedCrossRef Derkach VA, Oh MC, Guire ES, Soderling TR: Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 2007, 8: 101–113.PubMedCrossRef
59.
go back to reference Malinow R, Malenka RC: AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25: 103–126.PubMedCrossRef Malinow R, Malenka RC: AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25: 103–126.PubMedCrossRef
60.
go back to reference Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, et al.: Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 1996, 17: 945–956.PubMedCrossRef Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, et al.: Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 1996, 17: 945–956.PubMedCrossRef
61.
go back to reference Meng Y, Zhang Y, Jia Z: Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 2003, 39: 163–176.PubMedCrossRef Meng Y, Zhang Y, Jia Z: Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 2003, 39: 163–176.PubMedCrossRef
62.
go back to reference Hartmann B, Ahmadi S, Heppenstall PA, Lewin GR, Schott C, Borchardt T, Seeburg PH, Zeilhofer HU, Sprengel R, Kuner R: The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 2004, 44: 637–650.PubMedCrossRef Hartmann B, Ahmadi S, Heppenstall PA, Lewin GR, Schott C, Borchardt T, Seeburg PH, Zeilhofer HU, Sprengel R, Kuner R: The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 2004, 44: 637–650.PubMedCrossRef
63.
go back to reference Karim F, Wang CC, Gereau RWt: Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 2001, 21: 3771–3779.PubMed Karim F, Wang CC, Gereau RWt: Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 2001, 21: 3771–3779.PubMed
64.
go back to reference Ji RR, Befort K, Brenner GJ, Woolf CJ: ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 2002, 22: 478–485.PubMed Ji RR, Befort K, Brenner GJ, Woolf CJ: ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 2002, 22: 478–485.PubMed
65.
go back to reference Shimshek DR, Bus T, Grinevich V, Single FN, Mack V, Sprengel R, Spergel DJ, Seeburg PH: Impaired reproductive behavior by lack of GluR-B containing AMPA receptors but not of NMDA receptors in hypothalamic and septal neurons. Mol Endocrinol 2006, 20: 219–231.PubMedCrossRef Shimshek DR, Bus T, Grinevich V, Single FN, Mack V, Sprengel R, Spergel DJ, Seeburg PH: Impaired reproductive behavior by lack of GluR-B containing AMPA receptors but not of NMDA receptors in hypothalamic and septal neurons. Mol Endocrinol 2006, 20: 219–231.PubMedCrossRef
66.
go back to reference Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY: Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 2002, 34: 289–300.PubMedCrossRef Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY: Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 2002, 34: 289–300.PubMedCrossRef
Metadata
Title
Roles of the AMPA receptor subunit GluA1 but not GluA2 in synaptic potentiation and activation of ERK in the anterior cingulate cortex
Authors
Hiroki Toyoda
Ming-Gao Zhao
Bettina Ulzhöfer
Long-Jun Wu
Hui Xu
Peter H Seeburg
Rolf Sprengel
Rohini Kuner
Min Zhuo
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Molecular Pain / Issue 1/2009
Electronic ISSN: 1744-8069
DOI
https://doi.org/10.1186/1744-8069-5-46

Other articles of this Issue 1/2009

Molecular Pain 1/2009 Go to the issue