NMDA receptor mediates chronic visceral pain induced by neonatal noxious somatic stimulation

European Journal of Pharmacology

Volumn 744, Issue , 2015, Pages 28-35

  Miranda, Adrian ^a   Mickle, Aaron ^a   Bruckert, Mitchell ^a   Kannampalli, Pradeep ^a   Banerjee, Banani ^a   Sengupta, Jyoti N ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Neonatal pain; NMDA; Visceral hyperalgesia

Indexed keywords

4 PHOSPHONOMETHYLPIPECOLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PIPECOLIC ACID DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLON DILATATION; CONTROLLED STUDY; DRUG MECHANISM; GASTROCNEMIUS MUSCLE; HYPERALGESIA; LUMBOSACRAL SPINE; MALE; MUSCLE FUNCTION; NEUROMUSCULAR FUNCTION; NEWBORN; NOCICEPTIVE STIMULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SPINAL CORD NERVE CELL; VISCERAL PAIN; ANIMAL; CHEMICALLY INDUCED; CHRONIC PAIN; DRUG EFFECTS; METABOLISM; PROCEDURES; SENSORY NERVE CELL; SPINAL CORD; SPRAGUE DAWLEY RAT; STIMULATION;

ANIMALS; ANIMALS, NEWBORN; CHRONIC PAIN; HYPERALGESIA; MALE; NEURONS, AFFERENT; PHYSICAL STIMULATION; PIPECOLIC ACIDS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD; VISCERAL PAIN;

EID: 84918795742     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.09.034     Document Type: Article

References (52)

1. T. Abe, S. Matsumura, T. Katano, T. Mabuchi, K. Takagi, L. Xu, A. Yamamoto, K. Hattori, T. Yagi, M. Watanabe, T. Nakazawa, T. Yamamoto, M. Mishina, Y. Nakai, and S. Ito Fyn kinase-mediated phosphorylation of NMDA receptor NR2B subunit at Tyr1472 is essential for maintenance of neuropathic pain Eur. J. Neurosci. 22 2005 1445 1454
2. B. Banerjee, B.K. Medda, Y. Zheng, H. Miller, A. Miranda, J.N. Sengupta, and R. Shaker Alterations in N-methyl-d-aspartate receptor subunits in primary sensory neurons following acid-induced esophagitis in cats Am. J. Physiol. Gastrointest. Liver Physiol. 296 2009 66 77
3. L. Becerra, R.J. Schwartzman, R.T. Kiefer, P. Rohr, E.A. Moulton, D. Wallin, G. Pendse, S. Morris, and D. Borsook CNS Measures of pain responses pre- and post-anesthetic ketamine in a patient with complex regional pain syndrome Pain Med. 10 2009 1526 1537
4. S. Beggs, C. Torsney, L.J. Drew, and M. Fitzgerald The postnatal reorganization of primary afferent input and dorsal horn cell receptive fields in the rat spinal cord is an activity-dependent process Eur. J. Neurosci. 16 2002 1249 1258
5. S.J. Boxall, S.W. Thompson, A. Dray, A.H. Dickenson, and L. Urban Metabotropic glutamate receptor activation contributes to nociceptive reflex activity in the rat spinal cord in vitro Neuroscience 74 1996 13 20
6. K.M. Brown, J.R. Wrathall, R.P. Yasuda, and B.B. Wolfe Quantitative measurement of glutamate receptor subunit protein expression in the postnatal rat spinal cord Brain Res. Dev. Brain Res. 137 2002 127 133
7. P.J. Castroman, and T.J. Ness Ketamine, an N-methyl-d-aspartate receptor antagonist, inhibits the spinal neuronal responses to distension of the rat urinary bladder Anesthesiology 96 2002 1410 1419
8. S.N. Davies, and D. Lodge Evidence for involvement of N-methylaspartate receptors in 'wind-up' of class 2 neurones in the dorsal horn of the rat Brain Res. 424 1987 402 406
9. A.H. Dickenson, and A.F. Sullivan Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation Neuropharmacology 26 1987 1235 1238
10. J. Fan, X. Wu, Z. Cao, S. Chen, C. Owyang, and Y. Li Up-regulation of anterior cingulate cortex NR2B receptors contributes to visceral pain responses in rats Gastroenterology 136 2009 1732 1740
11. G.A. Gaudreau, and V. Plourde Involvement of N-methyl-d-aspartate (NMDA) receptors in a rat model of visceral hypersensitivity Behav. Brain Res. 150 2004 185 189
12. C. Gaunitz, A. Schuttler, C. Gillen, and C. Allgaier Formalin-induced changes of NMDA receptor subunit expression in the spinal cord of the rat Amino Acids 23 2002 177 182
13. S.J. Geng, F.F. Liao, W.H. Dang, X. Ding, X.D. Liu, J. Cai, J.S. Han, Y. Wan, and GG. Xing Contribution of the spinal cord BDNF to the development of neuropathic pain by activation of the NR2B-containing NMDA receptors in rats with spinal nerve ligation Exp. Neurol. 222 2010 256 266
14. X. Gonda Basic pharmacology of NMDA receptors Curr. Pharm. Des. 18 2012 1558 1567
15. G.J. Hathway, D. Vega-Avelaira, and M. Fitzgerald A critical period in the supraspinal control of pain: opioid-dependent changes in brainstem rostroventral medulla function in preadolescence Pain 153 2012 775 783
16. H. Iwata, T. Takasusuki, S. Yamaguchi, and Y. Hori NMDA receptor 2B subunit-mediated synaptic transmission in the superficial dorsal horn of peripheral nerve-injured neuropathic mice Brain Res. 1135 2007 92 101
17. Y. Ji, and R.J. Traub Differential effects of spinal CNQX on two populations of dorsal horn neurons responding to colorectal distension in the rat Pain 99 2002 217 222
18. C.M. Kozlowski, C. Bountra, and D. Grundy The effect of fentanyl, DNQX and MK-801 on dorsal horn neurones responsive to colorectal distension in the anaesthetized rat Neurogastroenterol. Motil. 12 2000 239 247
19. B. Laube, H. Hirai, M. Sturgess, H. Betz, and J. Kuhse Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit Neuron 18 1997 493 503
20. J. Li, J.A. McRoberts, H.S. Ennes, M. Trevisani, P. Nicoletti, Y. Mittal, and E.A. Mayer Experimental colitis modulates the functional properties of NMDA receptors in dorsal root ganglia neurons Am. J. Physiol. Gastrointest. Liver Physiol. 29 2006 219 228
21. S. Li, J. Cao, X. Yang, Z.W. Suo, L. Shi, Y.N. Liu, H.B. Yang, and X.D. Hu NR2B phosphorylation at tyrosine 1472 in spinal dorsal horn contributed to N-methyl-d-aspartate-induced pain hypersensitivity in mice J. Neurosci. Res. 89 2011 1869 1876
22. Y. Li, X. Zhang, H. Liu, Z. Cao, S. Chen, B. Cao, and J. Liu Phosphorylated CaMKII post-synaptic binding to NR2B subunits in the anterior cingulate cortex mediates visceral pain in visceral hypersensitive rats J. Neurochem. 121 2012 662 671
23. M.S. Lidow, Z.M. Song, and K. Ren Long-term effects of short-lasting early local inflammatory insult Neuroreport 12 2001 399 403
24. C. Lin, and E.D. Al-Chaer Long-term sensitization of primary afferents in adult rats exposed to neonatal colon pain Brain Res. 971 2003 73 82
25. X.G. Liu, and J. Sandkühler Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-d-aspartic acid receptor blockage Neurosci. Lett. 191 1995 43 46
26. A. Mickle, M. Sood, Z. Zhang, G. Shahmohammadi, J.N. Sengupta, and A. Miranda Antinociceptive effects of melatonin in a rat model of post-inflammatory visceral hyperalgesia: a centrally mediated process Pain 149 2010 555 564
27. A. Miranda, S. Peles, R. Shaker, C. Rudolph, and J.N. Sengupta Neonatal nociceptive somatic stimulation differentially modifies the activity of spinal neurons in rats and results in altered somatic and visceral sensation J. Physiol. 572 2006 775 787
28. A. Miranda, S. Peles, C. Rudolph, R. Shaker, and J.N. Sengupta Altered visceral sensation in response to somatic pain in the rat Gastroenterology 126 2004 1082 1089
29. A. Miranda, A. Mickle, J. Schmidt, Z. Zhang, R. Shaker, B. Banerjee, and J.N. Sengupta Neonatal cystitis-induced colonic hypersensitivity in adult rats: a model of viscero-visceral convergence Neurogastroenterol. Motil. 23 2011 683
30. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540
31. T.J. Ness, and G.F. Gebhart Acute inflammation differentially alters the activity of two classes of rat spinal visceral nociceptive neurons Neurosci. Lett. 281 2000 131 134
32. T.J. Ness, and G.F. Gebhart Interactions between visceral and cutaneous nociception in the rat. I. Noxious cutaneous stimuli inhibit visceral nociceptive neurons and reflexes J. Neurophysiol. 66 1991 20 28
33. T.J. Ness, and G.F. Gebhart Interactions between visceral and cutaneous nociception in the rat. II. Noxious visceral stimuli inhibit cutaneous nociceptive neurons and reflexes J. Neurophysiol. 66 1991 29 39
34. T.J. Ness, and G.F. Gebhart Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat J. Neurophysiol. 57 1987 1867 1892
35. T.J. Ness, and G.F. Gebhart Inflammation enhances reflex and spinal neuron responses to noxious visceral stimulation in rats Am. J. Physiol. Gastrointest. Liver Physiol. 280 2001 649 657
36. P. Park, A. Volianskis, T.M. Sanderson, Z.A. Bortolotto, D.E. Jane, M. Zhuo, B.K. Kaang, and G.L. Collingridge NMDA receptor-dependent long-term potentiation comprises a family of temporally overlapping forms of synaptic plasticity that are induced by different patterns of stimulation Philos. Trans. R. Soc. Lond B Biol. Sci. 369 2013 20130131
37. S. Peles, A. Miranda, R. Shaker, and J.N. Sengupta Acute nociceptive somatic stimulus sensitizes neurons in the spinal cord to colonic distension in the rat J. Physiol. 560 2004 291 302
38. X.X. Qu, J. Cai, M.J. Li, Y.N. Chi, F.F. Liao, F.Y. Liu, Y. Wan, J.S. Han, and G.G. Xing Role of the spinal cord NR2B-containing NMDA receptors in the development of neuropathic pain Exp. Neurol. 215 2009 298 307
39. M. Randic, M.C. Jiang, and R. Cerne Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord J. Neurosci. 13 1993 5228 5241
40. K. Ren, V. Anseloni, S.P. Zou, E.B. Wade, S.I. Novikova, and M. Ennis Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult Pain 110 2004 588 596
41. K. Ren, and R. Dubner NMDA receptor antagonists attenuate Mechanical hyperalgesia in rats with unilateral inflammation of the hindpaw Neurosci. Lett. 163 1993 22 26
42. M. Sheng, J. Cummings, L.A. Roldan, Y.N. Jan, and L.Y. Jan Changing subunit composition of heteromeric NMDA receptors during development of rat cortex Nature 368 1994 144 147
43. C. Torsney, and M.J. Fitzgerald Age-dependent effects of peripheral inflammation on the electrophysiological properties of neonatal rat dorsal horn neurons Neurophysiol 87 2002 1311 1317
44. R.J. Traub, M.S. Gold, R. Dubner, and M.S. Lidow Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult Pain 110 2004 588 596
45. M. Tsuruoka, and W.D. Willis Jr Descending modulation from the region of the locus coeruleus on nociceptive sensitivity in rat model of inflammatory hyperalgesia Brain Res. 743 1996 86 92
46. C. Ultenius, B. Linderoth, B.A. Meyerson, and J. Wallin Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat Neurosci. Lett. 399 2006 85 90
47. C.E. Urch, W. Rahman, and A.H. Dickenson Electrophysiological studies on the role of the NMDA receptor in nociception in the developing rat spinal cord Dev. Brain Res. 126 2001 81 89
48. L. Virgo, J. Dekkers, G.Z. Mentis, R. Navarrete, and J. de Belleroche Changes in expression of NMDA receptor subunits in the rat lumbar spinal cord following neonatal nerve injury Neuropathol. Appl. Neurobiol. 26 2000 258 272
49. R.P. Willert, C.J. Woolf, A.R. Hobson, C. Delaney, D.G. Thompson, and Q. Aziz The development and maintenance of human visceral pain hypersensitivity is dependent on the N-methyl-d-aspartate receptor Gastroenterology 126 2004 683 692
50. J.A. Wilson, E.M. Garry, H.A. Anderson, R. Rosie, L.A. Colvin, R. Mitchell, and S.M. Fleetwood-Walker NMDA receptor antagonist treatment at the time of nerve injury prevents injury-induced changes in spinal NR1 and NR2B subunit expression and increases the sensitivity of residual pain behaviours to subsequently administered NMDA receptor antagonists Pain 117 2005 421 432
51. Y. Yoshimura, T. Ohmura, and Y. Komatsu Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex J. Neurosci. 23 2003 6557 6566
52. M. Zhuo Plasticity of NMDA receptor NR2B subunit in memory and chronic pain (Review) Mol. Brain 2 2009 4 15