Spinal AMPA receptors: Amenable players in central sensitization for chronic pain therapy?

References

• Collaborators G. Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990-2013: a systematic analysis for the global burden of disease study 2013. Lancet. 2015 Aug 22;386(9995):743–800.
   PubMed Web of Science ®Google Scholar
• Breivik H, Collett B, Ventafridda V, et al. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur J Pain. 2006 May;10(4):287–333.
   PubMed Web of Science ®Google Scholar
• Rice AS, Smith BH, Blyth FM. Pain and the global burden of disease. Pain. 2016 Apr;157(4):791–796.
   PubMed Web of Science ®Google Scholar
• Dahlhamer J, Lucas J, Zelaya C, et al. Prevalence of chronic pain and high-impact chronic pain among adults – United States, 2016. Morbidity Mortality Weekly Rep. 2018;67(36):1001–1006.
   PubMed Web of Science ®Google Scholar
• Goldberg DS, McGee SJ. Pain as a global public health priority. BMC Public Health. 2011 Oct;6(11):770.
   Google Scholar
• Treede RD, Rief W, Barke A, et al. Chronic pain as a symptom or a disease: the IASP classification of chronic pain for the international classification of diseases (ICD-11). Pain. 2019 Jan;160(1):19–27.
   PubMed Web of Science ®Google Scholar
• Scholz J, Finnerup NB, Attal N, et al. The IASP classification of chronic pain for ICD-11: chronic neuropathic pain. Pain. 2019 Jan;160(1):53–59.
   PubMed Web of Science ®Google Scholar
• Peirs C, Seal RP. Neural circuits for pain: recent advances and current views. Science. 2016 Nov 4;354(6312):578–584.
   PubMed Web of Science ®Google Scholar
• Kuner R. Central mechanisms of pathological pain. Nat Med. 2010 Nov;16(11):1258–1266.
   PubMed Web of Science ®Google Scholar
• Bushnell MC, Ceko M, Low LA. Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci. 2013 Jul;14(7):502–511.
   PubMed Web of Science ®Google Scholar
• Chater TE, Goda Y. The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front Cell Neurosci. 2014;8:401.
   PubMed Web of Science ®Google Scholar
• Henley JM, Wilkinson KA. Synaptic AMPA receptor composition in development, plasticity and disease. Nat Rev Neurosci. 2016 Jun;17(6):337–350.
   PubMed Web of Science ®Google Scholar
• Beneyto M, Meador-Woodruff JH. Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J Comp Neurol. 2004 Jan 19;468(4):530–554.
   PubMed Web of Science ®Google Scholar
• Kopach O, Extrasynaptic VN. AMPA receptors in the dorsal horn: evidence and functional significance. Brain Res Bull. 2013 Apr;93:47–56.
   PubMed Web of Science ®Google Scholar
• Tao YX. AMPA receptor trafficking in inflammation-induced dorsal horn central sensitization. Neurosci Bull. 2012 Apr;28(2):111–120.
   PubMed Web of Science ®Google Scholar
• Qiu S, Zhang M, Liu Y, et al. GluA1 phosphorylation contributes to postsynaptic amplification of neuropathic pain in the insular cortex. J Neurosci. 2014 Oct 1;34(40):13505–13515.
   PubMed Web of Science ®Google Scholar
• Gangadharan V, Wang R, Ulzhöfer B, et al. Peripheral calcium-permeable AMPA receptors regulate chronic inflammatory pain in mice. J Clin Invest. 2011 Apr;121(4):1608–1623.
   PubMed Web of Science ®Google Scholar
• Garry EM, Moss A, Rosie R, et al. Specific involvement in neuropathic pain of AMPA receptors and adapter proteins for the GluR2 subunit. Mol Cell Neurosci. 2003 Sep;24(1):10–22.
   PubMed Web of Science ®Google Scholar
• Katano T, Furue H, Okuda-Ashitaka E, et al. N-ethylmaleimide-sensitive fusion protein (NSF) is involved in central sensitization in the spinal cord through GluR2 subunit composition switch after inflammation. Eur J Neurosci. 2008 Jun;27(12):3161–3170.
   PubMed Web of Science ®Google Scholar
• Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain. 2009 Sep;10(9):895–926.
   PubMed Web of Science ®Google Scholar
• Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science. 2000 Jun 9;288(5472):1765–1769.
   PubMed Web of Science ®Google Scholar
• Kopach O, Krotov V, Shysh A, et al. Spinal PKCα inhibition and gene-silencing for pain relief: AMPAR trafficking at the synapses between primary afferents and sensory interneurons. Sci Rep. 2018 Jul 6;8(1):10285.
   PubMedGoogle Scholar
• Park JS, Yaster M, Guan X, et al. Role of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors in complete Freund’s adjuvant-induced inflammatory pain. Mol Pain. 2008 Dec 30;4:67.
   PubMed Web of Science ®Google Scholar
• Sorkin LS, Yaksh TL, Doom CM. Mechanical allodynia in rats is blocked by a Ca2+ permeable AMPA receptor antagonist. Neuroreport. 1999 Nov 26;10(17):3523–3526.
   PubMed Web of Science ®Google Scholar
• Gwak YS, Kang J, Leem JW, et al. Spinal AMPA receptor inhibition attenuates mechanical allodynia and neuronal hyperexcitability following spinal cord injury in rats. J Neurosci Res. 2007 Aug 15;85(11):2352–2359.
   PubMed Web of Science ®Google Scholar
• Chen SR, Zhou HY, Byun HS, et al. Nerve injury increases GluA2-lacking AMPA receptor prevalence in spinal cords: functional significance and signaling mechanisms. J Pharmacol Exp Ther. 2013 Dec;347(3):765–772.
   PubMed Web of Science ®Google Scholar
• Jin HC, Keller AJ, Jung JK, et al. Epidural tezampanel, an AMPA/kainate receptor antagonist, produces postoperative analgesia in rats. Anesth Analg. 2007 Oct;105(4):1152–1159. table of contents.
   PubMed Web of Science ®Google Scholar
• Lee HJ, Pogatzki-Zahn EM, Brennan TJ. The effect of the AMPA/kainate receptor antagonist LY293558 in a rat model of postoperative pain. J Pain. 2006 Oct;7(10):768–777.
   PubMed Web of Science ®Google Scholar
• Zahn PK, Pogatzki-Zahn EM, Brennan TJ. Spinal administration of MK-801 and NBQX demonstrates NMDA-independent dorsal horn sensitization in incisional pain. Pain. 2005 Apr;114(3):499–510.
   PubMed Web of Science ®Google Scholar
• Kopach O, Viatchenko-Karpinski V, Belan P, et al. Development of inflammation-induced hyperalgesia and allodynia is associated with the upregulation of extrasynaptic AMPA receptors in tonically firing lamina II dorsal horn neurons. Front Physiol. 2012;3:391.
   PubMed Web of Science ®Google Scholar
• Kopach O, Krotov V, Goncharenko J, et al. Inhibition of spinal Ca(2+)-permeable AMPA receptors with dicationic compounds alleviates persistent inflammatory pain without adverse effects. Front Cell Neurosci. 2016;10:50.
   PubMed Web of Science ®Google Scholar
• Hartmann B, Ahmadi S, Heppenstall PA, et al. The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron. 2004 Nov 18;44(4):637–650.
   PubMed Web of Science ®Google Scholar
• Zhang B, Tao F, Liaw WJ, et al. Effect of knock down of spinal cord PSD-93/chapsin-110 on persistent pain induced by complete Freund’s adjuvant and peripheral nerve injury. Pain. 2003 Nov;106(1–2):187–196.
   PubMed Web of Science ®Google Scholar
• Park JS, Voitenko N, Petralia RS, et al. Persistent inflammation induces GluR2 internalization via NMDA receptor-triggered PKC activation in dorsal horn neurons. J Neurosci. 2009 Mar 11;29(10):3206–3219.
   PubMed Web of Science ®Google Scholar
• Youn DH, Royle G, Kolaj M, et al. Enhanced LTP of primary afferent neurotransmission in AMPA receptor GluR2-deficient mice. Pain. 2008 May;136(1–2):158–167.
   PubMed Web of Science ®Google Scholar
• Jia Z, Agopyan N, Miu P, et al. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron. 1996 Nov;17(5):945–956.
   PubMed Web of Science ®Google Scholar
• Brusa R, Zimmermann F, Koh DS, et al. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science. 1995 Dec 8;270(5242):1677–1680.
   PubMed Web of Science ®Google Scholar
• Lamsa KP, Heeroma JH, Somogyi P, et al. Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science. 2007 Mar 2;315(5816):1262–1266.
   PubMed Web of Science ®Google Scholar
• Meng Y, Zhang Y, Jia Z. Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron. 2003 Jul 3;39(1):163–176.
   PubMed Web of Science ®Google Scholar
• Zamanillo D, Sprengel R, Hvalby O, et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science. 1999 Jun 11;284(5421):1805–1811.
   PubMed Web of Science ®Google Scholar
• Bannerman DM, Borchardt T, Jensen V, et al. Somatic accumulation of GluA1-AMPA receptors leads to selective cognitive impairments in mice. Front Mol Neurosci. 2018;11:199.
   PubMed Web of Science ®Google Scholar
• Reisel D, Bannerman DM, Schmitt WB, et al. Spatial memory dissociations in mice lacking GluR1. Nat Neurosci. 2002 Sep;5(9):868–873.
   PubMed Web of Science ®Google Scholar
• Schmitt WB, Deacon RM, Seeburg PH, et al. A within-subjects, within-task demonstration of intact spatial reference memory and impaired spatial working memory in glutamate receptor-A-deficient mice. J Neurosci. 2003 May 1;23(9):3953–3959.
   PubMed Web of Science ®Google Scholar
• Ikeda H, Heinke B, Ruscheweyh R, et al. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science. 2003 Feb 21;299(5610):1237–1240.
   PubMed Web of Science ®Google Scholar
• Randić M, Jiang MC, Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci. 1993 Dec;13(12):5228–5241.
   PubMed Web of Science ®Google Scholar
• Henneberger C, Bard L, Panatier A, et al. LTP induction boosts glutamate spillover by driving withdrawal of perisynaptic astroglia. Neuron. 2020 Dec;108(5):919-936.
   Web of Science ®Google Scholar
• Kopach O, Zheng K, Rusakov DA. Optical monitoring of glutamate release at multiple synapses in situ detects changes following LTP induction. Mol Brain. 2020 Mar 13;13(1):39.
   PubMed Web of Science ®Google Scholar
• Ikeda H, Stark J, Fischer H, et al. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science. 2006 Jun 16;312(5780):1659–1662.
   PubMed Web of Science ®Google Scholar
• Understanding SJ. LTP in pain pathways. Mol Pain. 2007 Apr;3(3):9.
   PubMedGoogle Scholar
• Zhang XC, Zhang YQ, Zhao ZQ. Involvement of nitric oxide in long-term potentiation of spinal nociceptive responses in rats. Neuroreport. 2005 Aug 1;16(11):1197–1201.
   PubMed Web of Science ®Google Scholar
• Isaac JT, Ashby MC, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron. 2007 Jun 21;54(6):859–871.
   PubMed Web of Science ®Google Scholar
• Lu W, Shi Y, Jackson AC, et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron. 2009 Apr 30;62(2):254–268.
   PubMed Web of Science ®Google Scholar
• Wenthold RJ, Petralia RS, Blahos J II, et al. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci. 1996 Mar 15;16(6):1982–1989.
   PubMed Web of Science ®Google Scholar
• Pelkey KA, Barksdale E, Craig MT, et al. Pentraxins coordinate excitatory synapse maturation and circuit integration of parvalbumin interneurons. Neuron. 2015 Mar 18;85(6):1257–1272.
   PubMed Web of Science ®Google Scholar
• Zhu JJ, Esteban JA, Hayashi Y, et al. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci. 2000 Nov;3(11):1098–1106.
   PubMed Web of Science ®Google Scholar
• Engelman HS, Allen TB, MacDermott AB. The distribution of neurons expressing calcium-permeable AMPA receptors in the superficial laminae of the spinal cord dorsal horn. J Neurosci. 1999 Mar 15;19(6):2081–2089.
   PubMed Web of Science ®Google Scholar
• Petralia RS, Wang YX, Mayat E, et al. Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol. 1997 Sep 1;385(3):456–476.
   PubMed Web of Science ®Google Scholar
• Todd AJ. Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci. 2010 Dec;11(12):823–836.
   PubMed Web of Science ®Google Scholar
• Nagy GG, Al-Ayyan M, Andrew D, et al. Widespread expression of the AMPA receptor GluR2 subunit at glutamatergic synapses in the rat spinal cord and phosphorylation of GluR1 in response to noxious stimulation revealed with an antigen-unmasking method. J Neurosci. 2004 Jun 23;24(25):5766–5777.
   PubMed Web of Science ®Google Scholar
• Polgár E, Watanabe M, Hartmann B, et al. Expression of AMPA receptor subunits at synapses in laminae I-III of the rodent spinal dorsal horn. Mol Pain. 2008 Jan;23(4):5.
   Google Scholar
• Brown KM, Wrathall JR, Yasuda RP, et al. Quantitative measurement of glutamate receptor subunit protein expression in the postnatal rat spinal cord. Brain Res Dev Brain Res. 2002 Aug 30;137(2):127–133.
   PubMedGoogle Scholar
• Nichols ML, Allen BJ, Rogers SD, et al. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science. 1999 Nov 19;286(5444):1558–1561.
   PubMed Web of Science ®Google Scholar
• Kopach O, Kao SC, Petralia RS, et al. Inflammation alters trafficking of extrasynaptic AMPA receptors in tonically firing lamina II neurons of the rat spinal dorsal horn. Pain. 2011 Apr;152(4):912–923.
   PubMed Web of Science ®Google Scholar
• Masugi-Tokita M, Tarusawa E, Watanabe M, et al. Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci. 2007 Feb 21;27(8):2135–2144.
   PubMed Web of Science ®Google Scholar
• Tanaka J, Matsuzaki M, Tarusawa E, et al. Number and density of AMPA receptors in single synapses in immature cerebellum. J Neurosci. 2005 Jan 26;25(4):799–807.
   PubMed Web of Science ®Google Scholar
• Matsuzaki M, Ellis-Davies GC, Nemoto T, et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci. 2001 Nov;4(11):1086–1092.
   PubMed Web of Science ®Google Scholar
• Momiyama A, Silver RA, Hausser M, et al. The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol. 2003 May 15;549(Pt 1):75–92.
   PubMed Web of Science ®Google Scholar
• Lu CR, Hwang SJ, Phend KD, et al. Primary afferent terminals in spinal cord express presynaptic AMPA receptors. J Neurosci. 2002 Nov 1;22(21):9522–9529.
   PubMed Web of Science ®Google Scholar
• Lee CJ, Bardoni R, Tong CK, et al. Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron. 2002 Jul 3;35(1):135–146.
   PubMed Web of Science ®Google Scholar
• Keinänen K, Wisden W, Sommer B, et al. A family of AMPA-selective glutamate receptors. Science. 1990 Aug 3;249(4968):556–560.
   PubMed Web of Science ®Google Scholar
• Sommer B, Keinänen K, Verdoorn TA, et al. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science. 1990 Sep 28;249(4976):1580–1585.
   PubMed Web of Science ®Google Scholar
• Greger IH, Khatri L, Kong X, et al. AMPA receptor tetramerization is mediated by Q/R editing. Neuron. 2003 Nov 13;40(4):763–774.
   PubMed Web of Science ®Google Scholar
• Burnashev N, Monyer H, Seeburg PH, et al. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron. 1992 Jan;8(1):189–198.
   PubMed Web of Science ®Google Scholar
• Traynelis SF, Wollmuth LP, McBain CJ, et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev. 2010 Sep;62(3):405–496.
   PubMed Web of Science ®Google Scholar
• Cull-Candy S, Kelly L, Farrant M. Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol. 2006 Jun;16(3):288–297.
   PubMed Web of Science ®Google Scholar
• Kopach O, Viatchenko-Karpinski V, Atianjoh FE, et al. PKCα is required for inflammation-induced trafficking of extrasynaptic AMPA receptors in tonically firing lamina II dorsal horn neurons during the maintenance of persistent inflammatory pain. J Pain. 2013 Feb;14(2):182–192.
   PubMed Web of Science ®Google Scholar
• Vikman KS, Rycroft BK, Christie MJ. Switch to Ca2+-permeable AMPA and reduced NR2B NMDA receptor-mediated neurotransmission at dorsal horn nociceptive synapses during inflammatory pain in the rat. J Physiol. 2008 Jan 15;586(2):515–527.
   PubMed Web of Science ®Google Scholar
• Choquet D, Triller A. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci. 2003 4;Apr(4):251–265.
   Google Scholar
• Penn AC, Zhang CL, Georges F, et al. Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors. Nature. 2017 Sep 21;549(7672):384–388.
   PubMed Web of Science ®Google Scholar
• Makino H, Malinow R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron. 2009 Nov 12;64(3):381–390.
   PubMed Web of Science ®Google Scholar
• Park M, Penick EC, Edwards JG, et al. Recycling endosomes supply AMPA receptors for LTP. Science. 2004 Sep 24;305(5692):1972–1975.
   PubMed Web of Science ®Google Scholar
• Wu D, Bacaj T, Morishita W, et al. Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP. Nature. 2017 Apr 20;544(7650):316–321.
   PubMed Web of Science ®Google Scholar
• Galan A, Laird JM, Cervero F. In vivo recruitment by painful stimuli of AMPA receptor subunits to the plasma membrane of spinal cord neurons. Pain. 2004 Dec;112(3):315–323.
   PubMed Web of Science ®Google Scholar
• Larsson M, Broman J. Translocation of GluR1-containing AMPA receptors to a spinal nociceptive synapse during acute noxious stimulation. J Neurosci. 2008 Jul 9;28(28):7084–7090.
   PubMed Web of Science ®Google Scholar
• Choi JI, Svensson CI, Koehrn FJ, et al. Peripheral inflammation induces tumor necrosis factor dependent AMPA receptor trafficking and Akt phosphorylation in spinal cord in addition to pain behavior. Pain. 2010 May;149(2):243–253.
   PubMed Web of Science ®Google Scholar
• Pezet S, Marchand F, D’Mello R, et al. Phosphatidylinositol 3-kinase is a key mediator of central sensitization in painful inflammatory conditions. J Neurosci. 2008 Apr 16;28(16):4261–4270.
   PubMed Web of Science ®Google Scholar
• Kohno T, Wang H, Amaya F, et al. Bradykinin enhances AMPA and NMDA receptor activity in spinal cord dorsal horn neurons by activating multiple kinases to produce pain hypersensitivity. J Neurosci. 2008 Apr 23;28(17):4533–4540.
   PubMed Web of Science ®Google Scholar
• Liu T, Jiang CY, Fujita T, et al. Enhancement by interleukin-1β of AMPA and NMDA receptor-mediated currents in adult rat spinal superficial dorsal horn neurons. Mol Pain. 2013 Mar 28;9:16.
   PubMed Web of Science ®Google Scholar
• Ferguson AR, Christensen RN, Gensel JC, et al. Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J Neurosci. 2008 Oct 29;28(44):11391–11400.
   PubMed Web of Science ®Google Scholar
• Leonoudakis D, Zhao P, Beattie EC. Rapid tumor necrosis factor alpha-induced exocytosis of glutamate receptor 2-lacking AMPA receptors to extrasynaptic plasma membrane potentiates excitotoxicity. J Neurosci. 2008 Feb 27;28(9):2119–2130.
   PubMed Web of Science ®Google Scholar
• Schnell E, Sizemore M, Karimzadegan S, et al. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13902–13907.
   PubMed Web of Science ®Google Scholar
• Nair D, Hosy E, Petersen JD, et al. Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J Neurosci. 2013 Aug 7;33(32):13204–13224.
   PubMed Web of Science ®Google Scholar
• Opazo P, Labrecque S, Tigaret CM, et al. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron. 2010 Jul 29;67(2):239–252.
   PubMed Web of Science ®Google Scholar
• Taylor BK, Sinha GP, Donahue RR, et al. Opioid receptors inhibit the spinal AMPA receptor Ca(2+) permeability that mediates latent pain sensitization. Exp Neurol. 2019 Apr;314:58–66.
   PubMed Web of Science ®Google Scholar
• Woodhams SG, Markus R, Gowler PRW, et al. Cell type-specific super-resolution imaging reveals an increase in calcium-permeable AMPA receptors at spinal peptidergic terminals as an anatomical correlate of inflammatory pain. Pain. 2019 Nov;160(11):2641–2650.
   PubMed Web of Science ®Google Scholar
• Banke TG, Greenwood JR, Christensen JK, et al. Identification of amino acid residues in GluR1 responsible for ligand binding and desensitization. J Neurosci. 2001 May 1;21(9):3052–3062.
   PubMed Web of Science ®Google Scholar
• Körber C, Werner M, Hoffmann J, et al. Stargazin interaction with alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptors is critically dependent on the amino acid at the narrow constriction of the ion channel. J Biol Chem. 2007 Jun 29;282(26):18758–18766.
   PubMed Web of Science ®Google Scholar
• Osten P, Khatri L, Perez JL, et al. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron. 2000 Aug;27(2):313–325.
   PubMed Web of Science ®Google Scholar
• Fang L, Wu J, Zhang X, et al. Increased phosphorylation of the GluR1 subunit of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor in rats following intradermal injection of capsaicin. Neuroscience. 2003;122(1):237–245.
   PubMed Web of Science ®Google Scholar
• Fang L, Wu J, Lin Q, et al. Protein kinases regulate the phosphorylation of the GluR1 subunit of AMPA receptors of spinal cord in rats following noxious stimulation. Brain Res Mol Brain Res. 2003 Oct 21;118(1–2):160–165.
   PubMedGoogle Scholar
• Miletic G, Hermes JL, Bosscher GL, et al. Protein kinase C gamma-mediated phosphorylation of GluA1 in the postsynaptic density of spinal dorsal horn neurons accompanies neuropathic pain, and dephosphorylation by calcineurin is associated with prolonged analgesia. Pain. 2015 Dec;156(12):2514–2520.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wu J, Guo R, et al. Surgical incision induces phosphorylation of AMPA receptor GluR1 subunits at Serine-831 sites and GluR1 trafficking in spinal cord dorsal horn via a protein kinase Cγ-dependent mechanism. Neuroscience. 2013 Jun 14;240:361–370.
   PubMed Web of Science ®Google Scholar
• Boehm J, Kang MG, Johnson RC, et al. Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron. 2006 Jul 20;51(2):213–225.
   PubMed Web of Science ®Google Scholar
• Peng HY, Chang CH, Tsai SJ, et al. Protein kinase A-dependent spinal α-amino-3-hydroxy-5-methyl-4-isoxazoleproprionate-receptor trafficking mediates capsaicin-induced colon-urethra cross-organ reflex sensitization. Anesthesiology. 2011 Jan;114(1):70–83.
   PubMed Web of Science ®Google Scholar
• Jones TL, Sorkin LS, Activated PKA. PKC, but not CaMKIIalpha, are required for AMPA/Kainate-mediated pain behavior in the thermal stimulus model. Pain. 2005 Oct;117(3):259–270.
   PubMed Web of Science ®Google Scholar
• Fang L, Wu J, Lin Q, et al. Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization. J Neurosci. 2002 May 15;22(10):4196–4204.
   PubMed Web of Science ®Google Scholar
• Jones TL, Lustig AC, Sorkin LS. Secondary hyperalgesia in the postoperative pain model is dependent on spinal calcium/calmodulin-dependent protein kinase II alpha activation. Anesth Analg. 2007 Dec;105(6):1650–1656. table of contents.
   PubMed Web of Science ®Google Scholar
• Guire ES, Oh MC, Soderling TR, et al. Recruitment of calcium-permeable AMPA receptors during synaptic potentiation is regulated by CaM-kinase I. J Neurosci. 2008 Jun 4;28(23):6000–6009.
   PubMed Web of Science ®Google Scholar
• Barria A, Muller D, Derkach V, et al. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science. 1997 Jun 27;276(5321):2042–2045.
   PubMed Web of Science ®Google Scholar
• Lee HK, Takamiya K, Han JS, et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 2003 Mar 7;112(5):631–643.
   PubMed Web of Science ®Google Scholar
• Esteban JA, Shi SH, Wilson C, et al. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci. 2003 Feb;6(2):136–143.
   PubMed Web of Science ®Google Scholar
• Kopach O, Krotov V, Belan P, et al. Inflammatory-induced changes in synaptic drive and postsynaptic AMPARs in lamina II dorsal horn neurons are cell-type specific. Pain. 2015 Mar;156(3):428–438.
   PubMed Web of Science ®Google Scholar
• Kopach O, Medvediev V, Krotov V, et al. Opposite, bidirectional shifts in excitation and inhibition in specific types of dorsal horn interneurons are associated with spasticity and pain post-SCI. Sci Rep. 2017 Jul 19;7(1):5884.
   PubMedGoogle Scholar
• Yasaka T, Tiong SY, Hughes DI, et al. Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain. 2010 Nov;151(2):475–488.
   PubMed Web of Science ®Google Scholar
• Lu Y. Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J Neurosci. 2005 Apr 13;25(15):3900–3907.
   PubMed Web of Science ®Google Scholar
• Albuquerque C, Lee CJ, Jackson AC, et al. Subpopulations of GABAergic and non-GABAergic rat dorsal horn neurons express Ca2+-permeable AMPA receptors. Eur J Neurosci. 1999 Aug;11(8):2758–2766.
   PubMed Web of Science ®Google Scholar
• Kerr RC, Maxwell DJ, Todd AJ. GluR1 and GluR2/3 subunits of the AMPA-type glutamate receptor are associated with particular types of neurone in laminae I-III of the spinal dorsal horn of the rat. Eur J Neurosci. 1998 Jan;10(1):324–333.
   PubMed Web of Science ®Google Scholar
• Leitner J, Westerholz S, Heinke B, et al. Impaired excitatory drive to spinal GABAergic neurons of neuropathic mice. PLoS One. 2013;8(8):e73370.
   PubMed Web of Science ®Google Scholar
• Coull JA, Boudreau D, Bachand K, et al. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature. 2003 Aug 21;424(6951):938–942.
   PubMed Web of Science ®Google Scholar
• Hildebrand ME, Xu J, Dedek A, et al. Potentiation of synaptic GluN2B NMDAR currents by fyn kinase is gated through BDNF-mediated disinhibition in spinal pain processing. Cell Rep. 2016 Dec 6;17(10):2753–2765.
   PubMed Web of Science ®Google Scholar
• Moore KA, Kohno T, Karchewski LA, et al. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci. 2002 Aug 1;22(15):6724–6731.
   PubMed Web of Science ®Google Scholar
• Dedek A, Xu J, Kandegedara CM, et al. Loss of STEP61 couples disinhibition to N-methyl-d-aspartate receptor potentiation in rodent and human spinal pain processing. Brain. 2019 Jun 1;142(6):1535–1546.
   PubMedGoogle Scholar
• Inquimbert P, Moll M, Latremoliere A, et al. NMDA receptor activation underlies the loss of spinal dorsal horn neurons and the transition to persistent pain after peripheral nerve injury. Cell Rep. 2018 May 29;23(9):2678–2689.
   PubMed Web of Science ®Google Scholar
• Somers DL, Clemente FR. Dorsal horn synaptosomal content of aspartate, glutamate, glycine and GABA are differentially altered following chronic constriction injury to the rat sciatic nerve. Neurosci Lett. 2002 May 3;323(3):171–174.
   PubMed Web of Science ®Google Scholar
• Inquimbert P, Bartels K, Babaniyi OB, et al. Peripheral nerve injury produces a sustained shift in the balance between glutamate release and uptake in the dorsal horn of the spinal cord. Pain. 2012 Dec;153(12):2422–2431.
   PubMed Web of Science ®Google Scholar
• NJ E, CA R, Fine A, et al. Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron. 2003 Jun 5;38(5):797–804.
   PubMed Web of Science ®Google Scholar
• Malgaroli A, AE T, Wendland B, et al. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science. 1995 Jun 16;268(5217):1624–1628.
   PubMed Web of Science ®Google Scholar
• Lozovaya NA, Kopanitsa MV, Boychuk YA, et al. Enhancement of glutamate release uncovers spillover-mediated transmission by N-methyl-D-aspartate receptors in the rat hippocampus. Neuroscience. 1999;91(4):1321–1330.
   PubMed Web of Science ®Google Scholar
• Kerchner GA, Nicoll RA. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci. 2008 Nov;9(11):813–825.
   PubMed Web of Science ®Google Scholar
• Kullmann DM, Asztely F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 1998 Jan;21(1):8–14.
   PubMed Web of Science ®Google Scholar
• Twomey EC, Yelshanskaya MV, Vassilevski AA, et al. Mechanisms of channel block in. Neuron. 2018 Sep 5;99(5):956–968.e4.
   PubMed Web of Science ®Google Scholar
• Zaitsev AV, Kim KK, Fedorova IM, et al. Specific mechanism of use-dependent channel block of calcium-permeable AMPA receptors provides activity-dependent inhibition of glutamatergic neurotransmission. J Physiol. 2011 Apr 1;589(Pt 7):1587–1601.
   PubMed Web of Science ®Google Scholar
• Christensen NR, De Luca M, Lever MB, et al. A high-affinity, bivalent PDZ domain inhibitor complexes PICK1 to alleviate neuropathic pain. EMBO Mol Med. 2020 Jun 8;12(6):e11248.
   PubMed Web of Science ®Google Scholar
• Liu TY, Cheng Y, Qin XY, et al. Pharmacologically inhibiting GluR2 internalization alleviates neuropathic pain. Neurosci Bull. 2015 Oct;31(5):611–616.
   PubMed Web of Science ®Google Scholar
• Sullivan SJ, Farrant M, Cull-Candy SG. TARP γ-2 is required for inflammation-associated AMPA receptor plasticity within lamina ii of the spinal cord dorsal horn. J Neurosci. 2017 Jun 21;37(25):6007–6020.
   PubMed Web of Science ®Google Scholar
• Knopp KL, Simmons RMA, Guo W, et al. Modulation of TARP γ8-Containing AMPA Receptors as a Novel Therapeutic Approach for Chronic Pain. J Pharmacol Exp Ther. 2019 Jun;369(3):345–363.
   PubMed Web of Science ®Google Scholar