AMPA receptor subunits expression and phosphorylation in cingulate cortex in rats following esophageal acid exposure

Neurogastroenterology and Motility

Volumn 25, Issue 12, 2013, Pages

  Banerjee, B ^a   Medda, B K ^a   Pochiraju, S ^a   Kannampalli, P ^a   Lang, I M ^a   Sengupta, J N ^a   Shaker, R ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

AMPA receptor subunits; Anterior cingulate cortex (ACC); CaMKII; GluA1; Midcingulate cortex (MCC); Postsynaptic densities (PSDs)

Indexed keywords

1 (1 ADAMANTYLMETHYLAMMONIO) 5 TRIMETHYLAMMONIOPENTANE DIBROMIDE; AMPA RECEPTOR; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN ELECTROPHYSIOLOGY; CINGULATE GYRUS; CONTROLLED STUDY; EXPOSURE; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; MALE; MICROINJECTION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR UPREGULATION; STOMACH ACID;

AMPA RECEPTOR SUBUNITS; ANTERIOR CINGULATE CORTEX (ACC); CAMKII; GLUA1; MIDCINGULATE CORTEX (MCC); POSTSYNAPTIC DENSITIES (PSDS);

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; ESOPHAGUS; GYRUS CINGULI; HYDROCHLORIC ACID; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA;

EID: 84888063018     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12233     Document Type: Article

References (47)

1. Fass R, Tougas G. Functional heartburn: the stimulus, the pain, and the brain. Gut 2002; 51: 885-92.
2. Mayer EA, Collins SM. Evolving pathophysiologic models of functional gastrointestinal disorders. Gastroenterology 2002; 122: 2032-48.
3. Mayer EA, Naliboff BD, Craig AD. Neuroimaging of the brain-gut axis: from basic understanding to treatment of functional GI disorders. Gastroenterology 2006; 131: 1925-42.
4. Lawal A, Kern M, Sanjeevi A et al. Neurocognitive processing of esophageal central sensitization in the insula and cingulate gyrus. Am J Physiol Gastrointest Liver Physiol 2008; 294: G787-94.
5. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005; 9: 463-84.
6. Hobson AR, Aziz Q. Modulation of visceral nociceptive pathways. Curr Opin Pharmacol 2007; 7: 593-7.
7. Sikes RW, Vogt LJ, Vogt BA. Distribution and properties of visceral nociceptive neurons in rabbit cingulate cortex. Pain 2008; 135: 160-74.
8. Wu LJ, Steenland HW, Kim SS et al. Enhancement of presynaptic glutamate release and persistent inflammatory pain by increasing neuronal cAMP in the anterior cingulate cortex. Mol Pain 2008; 4: 40.
9. Wu X, Gao J, Yan J, Fan J, Owyang C, Li Y. Role for NMDA receptors in visceral nociceptive transmission in the anterior cingulate cortex of viscerally hypersensitive rats. Am J Physiol Gastrointest Liver Physiol 2008; 294: G918-27.
10. Cao Z, Wu X, Chen S et al. Anterior cingulate cortex modulates visceral pain as measured by visceromotor responses in viscerally hypersensitive rats. Gastroenterology 2008; 134: 535-43.
11. Banerjee B, Medda BK, Schmidt J, Lang IM, Sengupta JN, Shaker R. Neuronal plasticity in the cingulate cortex of rats following esophageal acid exposure in early life. Gastroenterology 2011; 141: 544-52.
12. 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; 44: 637-50.
13. Jones TL, Sorkin LS. Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate receptors mediate development, but not maintenance, of secondary allodynia evoked by first-degree burn in the rat. J Pharmacol Exp Ther 2004; 310: 223-9.
14. Pogatzki EM, Niemeier JS, Sorkin LS, Brennan TJ. Spinal glutamate receptor antagonists differentiate primary and secondary mechanical hyperalgesia caused by incision. Pain 2003; 105: 97-107.
15. + -permeable non-NMDA glutamate receptor antagonists. Anesthesiology 2001; 95: 965-73.
16. 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; 4: 67.
17. Xu H, Wu LJ, Wang H et al. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 2008; 28: 7445-53.
18. Bie B, Brown DL, Naguib M. Increased synaptic GluR1 subunits in the anterior cingulate cortex of rats with peripheral inflammation. Eur J Pharmacol 2011; 653: 26-31.
19. Wang Y, Wu J, Wu Z, Lin Q, Yue Y, Fang L. Regulation of AMPA receptors in spinal nociception. Mol Pain 2010; 6: 5.
20. Banerjee B, Medda BK, Schmidt J et al. Altered expression of P2X3 in vagal and spinal afferents following esophagitis in rats. Histochem Cell Biol 2009; 132: 585-97.
21. Villasana LE, Klann E, Tejada-Simon MV. Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J Neurosci Methods 2006; 158: 30-6.
22. Kopach O, Kao SC, Petralia RS, Belan P, Tao YX, Voitenko N. Inflammation alters trafficking of extrasynaptic AMPA receptors in tonically firing lamina II neurons of the rat spinal dorsal horn. Pain 2011; 152: 912-23.
23. Daniels BA, Wood L, Tremblay F, Baldridge WH. Functional evidence for D-serine inhibition of non-N-methyl-D-aspartate ionotropic glutamate receptors in retinal neurons. Eur J Neurosci 2012; 35: 56-65.
24. Fortin DA, Srivastava T, Dwarakanath D et al. Brain-derived neurotrophic factor activation of CaM-kinase kinase via transient receptor potential canonical channels induces the translation and synaptic incorporation of GluA1-containing calcium-permeable AMPA receptors. J Neurosci 2012; 32: 8127-37.
25. Fang L, Wu J, Zhang X, Lin Q, Willis WD. 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: 237-45.
26. Fang L, Wu J, Lin Q, Willis WD. 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; 118: 160-5.
27. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science 1992; 258: 597-603.
28. Collingridge GL, Bliss TV. Memories of NMDA receptors and LTP. Trends Neurosci 1995; 18: 54-6.
29. Wisden W, Seeburg PH. Mammalian ionotropic glutamate receptors. Curr Opin Neurobiol 1993; 3: 291-8.
30. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994; 17: 31-108.
31. Appleby VJ, Correa SA, Duckworth JK et al. LTP in hippocampal neurons is associated with a CaMKII-mediated increase in GluA1 surface expression. J Neurochem 2011; 116: 530-43.
32. Toyoda H, Zhao MG, Ulzhofer B et al. 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.
33. 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; 112: 315-23.
34. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002; 25: 103-26.
35. Kennedy MJ, Ehlers MD. Organelles and trafficking machinery for postsynaptic plasticity. Annu Rev Neurosci 2006; 29: 325-62.
36. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 2000; 20: 89-102.
37. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, Malinow R. Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 2006; 51: 213-25.
38. Lu Y, Sun YN, Wu X et al. Role of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor subunit GluR1 in spinal dorsal horn in inflammatory nociception and neuropathic nociception in rat. Brain Res 2008; 1200: 19-26.
39. Wang Y, Mu X, Wu J et al. Differential roles of phosphorylated AMPA receptor GluR1 subunits at Serine-831 and Serine-845 sites in spinal cord dorsal horn in a rat model of post-operative pain. Neurochem Res 2011; 36: 170-6.
40. Chung HJ, Xia J, Scannevin RH, Zhang X, Huganir RL. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci 2000; 20: 7258-67.
41. Matsuda S, Launey T, Mikawa S, Hirai H. Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 2000; 19: 2765-74.
42. 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; 29: 3206-19.
43. 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: 2262-7.
44. Shi SH, Hayashi Y, Petralia RS et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999; 284: 1811-6.
45. Leonard AS, Davare MA, Horne MC, Garner CC, Hell JW. SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 1998; 273: 19518-24.
46. Chen L, Chetkovich DM, Petralia RS et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 2000; 408: 936-43.
47. Li Y, Zhang X, Liu H et al. Phosphorylated CaMKII post-synaptic binding to NR2B subunits in the anterior cingulate cortex mediates visceral pain in visceral hypersensitive rats. J Neurochem 2012; 121: 662-71.