UCCB01-125, a dimeric inhibitor of PSD-95, reduces inflammatory pain without disrupting cognitive or motor performance: Comparison with the NMDA receptor antagonist MK-801

Neuropharmacology

Volumn 67, Issue , 2013, Pages 193-200

  Andreasen, Jesper T ^a   Bach, Anders ^a   Gynther, Mikko ^a   Nasser, Arafat ^b   Mogensen, Jesper ^c   Strømgaard, Kristian ^a   Pickering, Darryl S ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Behaviour; Cognition; Inflammatory pain; Mice; NMDA antagonism; PSD 95 inhibition

Indexed keywords

ANALGESIC AGENT; DIZOCILPINE; POSTSYNAPTIC DENSITY PROTEIN 95; UCCB 01 125; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTION; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG HYPERSENSITIVITY; DRUG MEGADOSE; DRUG SAFETY; DRUG SCREENING; DRUG STRUCTURE; FEMALE; FOOD PREFERENCE; HYPERALGESIA; INFLAMMATORY PAIN; LONG TERM MEMORY; MENTAL PERFORMANCE; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REFERENCE MEMORY; WORKING MEMORY;

ANIMALS; COGNITION; DIMERIZATION; DIZOCILPINE MALEATE; ENZYME INHIBITORS; FEMALE; GUANYLATE KINASE; INFLAMMATION; INFLAMMATION MEDIATORS; MEMBRANE PROTEINS; MICE; MOTOR SKILLS; OLIGOPEPTIDES; PAIN; POLYETHYLENE GLYCOLS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84873394344     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.11.006     Document Type: Article

References (62)

1. K.O. Aley, G. McCarter, and J.D. Levine Nitric oxide signaling in pain and nociceptor sensitization in the rat J. Neurosci. 18 1998 7008 7014
2. A. Bach, C.N. Chi, G.F. Pang, L. Olsen, A.S. Kristensen, P. Jemth, and K. Strømgaard Design and synthesis of highly potent and plasma-stable dimeric inhibitors of the PSD-95-NMDA receptor interaction Angew. Chem. Int. Ed. Engl. 48 51 2009 9685 9689
3. A. Bach, B.H. Clausen, M. Møller, B. Vestergaard, C.N. Chi, A. Round, P.L. Sørensen, K.B. Nissen, J.S. Kastrup, M. Gajhede, P. Jemth, A.S. Kristensen, P. Lundström, K.L. Lambertsen, and K. Strømgaard A high-affinity, dimeric inhibitor of PSD-95 bivalently interacts with PDZ1-2 and protects against ischemic brain damage Proc. Natl. Acad. Sci. U. S. A. 109 9 2012 3317 3322
4. M. Backonja, G. Arndt, K.A. Gombar, B. Check, and M. Zimmermann Response of chronic neuropathic pain syndromes to ketamine: a preliminary study Pain 56 1994 51 57
5. M.K. Boettger, N. Uceyler, M. Zelenka, A. Schmitt, A. Reif, Y. Chen, and C. Sommer Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice Eur. J. Pain 11 7 2007 810 818
6. A. Boultadakis, and N. Pitsikas Effects of the nitric oxide synthase inhibitor L-NAME on recognition and spatial memory deficits produced by different NMDA receptor antagonists in the rat Neuropsychopharmacology 35 12 2010 2357 2366
7. J.E. Brenman, D.S. Chao, S.H. Gee, A.W. Mcgee, S.E. Craven, D.R. Santillano, Z. Wu, F. Huang, H. Xia, M.F. Peters, S.C. Froehner, and D.S. Bredt Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains Cell 84 1996 757 767
8. A.J. Carter Many agents that antagonize the NMDA receptor-channel complex in vivo also cause disturbances of motor coordination J. Pharmacol. Exp. Ther. 269 2 1994 573 580
9. E. Català, E. Reig, M. Artes, L. Aliaga, J.S. Lopez, and J.L. Segu Prevalence of pain in the Spanish population: telephone survey in 5000 homes Eur. J. Pain 6 2002 133 140
10. Centers for Disease Control MMWR Morb. Mortal Wkly. Rep. 54 2005 113 139
11. K.S. Christopherson, B.J. Hillier, W.A. Lim, and D.S. Bredt PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain J. Biol. Chem. 274 1999 27467 27473
12. C.F. Chan, W.Z. Sun, J.K. Lin, and S.Y. Lin-Shiau Activation of transcription factors of nuclear factor kappa B, activator protein-1 and octamer factors in hyperalgesia Eur. J. Pharmacol. 402 2000 61 68
13. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J. Neurosci. Methods 53 1994 55 63
14. S.R. Chaplan, A.B. Malmberg, and T.L. Yaksh Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat J. Pharmacol. Exp. Ther. 280 1997 829 838
15. P.F. Chapman, C.M. Atkins, M.T. Allen, J.E. Haley, and J.E. Steinmetz Inhibition of nitric oxide synthesis impairs two different forms of learning Neuroreport 3 1992 567 570
16. Y. Chen, M.K. Boettger, A. Reif, A. Schmitt, N. Uçeyler, and C. Sommer Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice Mol. Pain 6 2010 13
17. R.A. Clark, M. Shoaib, K.N. Hewitt, S.C. Stanford, and S.T. Bate A comparison of InVivoStat with other statistical software packages for analysis of data generated from animal experiments J. Psychopharmacol. 2011 10.1177/0269881111420313
18. Y.C. Chu, Y. Guan, J. Skinner, S.N. Raja, R.A. Johns, and Y.X. Tao Effect of genetic knockout or pharmacologic inhibition of neuronal nitric oxide synthase on complete Freund's adjuvant-induced persistent pain Pain 119 2005 113 123
19. S.N. Davies, and D. Lodge Evidence for involvement of N-methyl-D-aspartate receptors in 'wind-up' of class 2 neurones in the dorsal horn of the rat Brain Res. 424 1987 402 406
20. W.J. Dixon Efficient analysis of experimental observations Annu. Rev. Pharmacol. Toxicol. 20 1980 441 462
21. R. D'Mello, F. Marchand, S. Pezet, S.B. McMahon, and A.H. Dickenson Perturbing PSD-95 interactions with NR2B-subtype receptors attenuates spinal nociceptive plasticity and neuropathic pain Mol. Ther. 2011 10.1038/mt.2011.42
22. J. Dreyer, M. Schleicher, A. Tappe, K. Schilling, T. Kuner, G. Kusumawidijaja, W. Müller-Esterl, S. Oess, and R. Kuner Nitric oxide synthase (NOS)-interacting protein interacts with neuronal NOS and regulates its distribution and activity J. Neurosci. 24 46 2004 10454 10465
23. A.M. Elliott, B.H. Smith, K.I. Penny, W.C. Smith, and W.A. Chambers The epidemiology of chronic pain in the community Lancet 354 1999 1248 1252
24. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1 1988 47 59
25. J. Eriksen, M.K. Jensen, P. Sjogren, O. Ekholm, and N.K. Rasmussen Epidemiology of chronic non-malignant pain in Denmark Pain 106 2003 221 228
26. S.K. Florio, C. Loh, S.M. Huang, A.E. Iwamaye, K.F. Kitto, K.W. Fowler, J.A. Treiberg, J.S. Hayflick, J.M. Walker, C.A. Fairbanks, and Y. Lai Disruption of nNOS-PSD95 protein-protein interaction inhibits acute thermal hyperalgesia and chronic mechanical allodynia in rodents Br. J. Pharmacol. 158 2 2009 494 506
27. E.M. Garry, A. Moss, A. Delaney, F. O'Neill, J. Blakemore, J. Bowen, H. Husi, R. Mitchell, S.G. Grant, and S.M. Fleetwood-Walker Neuropathic sensitization of behavioral reflexes and spinal NMDA receptor/CaM kinase II interactions are disrupted in PSD-95 mutant mice Curr. Biol. 13 4 2003 321 328
28. W. Guo, F. Wei, S. Zou, M.T. Robbins, S. Sugiyo, T. Ikeda, J.C. Tu, P.F. Worley, R. Dubner, and K. Ren Group I metabotropic glutamate receptor NMDA receptor coupling and signaling cascade mediate spinal dorsal horn NMDA receptor 2B tyrosine phosphorylation associated with inflammatory hyperalgesia J. Neurosci. 24 2004 9161 9173 http://invivostat.co.uk/
29. L. Halcák, O. Pechánová, Z. Zigová, L. Klemová, M. Novacký, and I. Bernátová Inhibition of NO synthase activity in nervous tissue leads to decreased motor activity in the rat Physiol. Res. 49 2000 143 149
30. E. Jørum, T. Warncke, and A. Stubhaug Cold allodynia and hyperalgesia in neuropathic pain: the effect of N-methyl-D-aspartate (NMDA) receptor antagonist ketamine-a double-blind, cross-over comparison with alfentanil and placebo Pain 101 2003 229 235
31. J.C. Kalvass, and T.S. Maurer Influence of nonspecific brain and plasma binding on CNS exposure: implications for rational drug discovery Biopharm. Drug Dispos 23 2002 327 338
32. Y.I. Kim, H.S. Na, Y.W. Yoon, H.C. Han, K.H. Ko, and S.K. Hong NMDA receptors are important for both mechanical and thermal allodynia from peripheral nerve injury in rats Neuroreport 8 1997 2149 2153
33. J.H. Krystal, L.P. Karper, J.P. Seibyl, G.K. Freeman, R. Delaney, J.D. Bremmer, G.R. Heninger, M.B. Bowers Jr., and D.S. Charney Sub-anesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive and neuroendocrine responses Arch. Gen. Psychiatry 51 1994 199 214
34. B.W. LeBlanc, M. Iwata, A.P. Mallon, C.N. Rupasinghe, D.J. Goebel, J. Marshall, M.R. Spaller, and C.Y. Saab A cyclic peptide targeted against PSD-95 blocks central sensitization and attenuates thermal hyperalgesia Neuroscience 167 2 2010 490 500
35. Z.D. Luo, and D. Cizkova The role of nitric oxide in nociception Curr. Rev. Pain 4 2000 459 466
36. A.B. Malmberg, and T.L. Yaksh Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats Pain 54 1993 291 300
37. J. Mao, D.D. Price, R.L. Hayes, J. Lu, D.J. Mayer, and H. Frenk Intrathecal treatment with dextrorphan or ketamine potently reduces pain-related behaviors in a rat model of peripheral mononeuropathy Brain Res. 605 1993 164 168
38. J. Mao, D.D. Price, R.L. Hayes, J. Lu, and D.J. Mayer Differential roles of NMDA and non-NMDA receptor activation in induction and maintenance of thermal hyperalgesia in rats with painful peripheral mononeuropathy Brain Res. 598 1992 271 278
39. H.J. McQuay, D. Carroll, A.R. Jadad, C.J. Glynn, T. Jack, R.A. Moore, and P.J. Wiffeh Dextromethorphan for the treatment of neuropathic pain: a double-blind randomised controlled crossover trial with integral n-of-1 design Pain 59 1994 127 133
40. S.T. Meller, and G.F. Gebhart Nitric oxide (NO) and nociceptive processing in the spinal cord Pain 52 1993 127 136
41. A.K. Naik, S.K. Tandan, D. Kumar, and S.P. Dudhgaonkar Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats Eur. J. Pharmacol. 530 2006 59 69
42. C.O. Okere, and H. Kaba Increased expression of neuronal nitric oxide synthase mRNA in the accessory olfactory bulb during the formation of olfactory recognition memory in mice Eur. J. Neurosci. 12 12 2000 4552 4556
43. M.G. Osborne, and T.J. Coderre Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia Br. J. Pharmacol. 126 1999 1840 1846
44. V. Paul, and P. Ekambaram Involvement of nitric oxide in learning & memory processes Indian J. Med. Res. 133 2011 471 478
45. A.B. Petrenko, T. Yamakura, H. Baba, and K. Shimoji The role of N-methyl-D-aspartate (NMDA) receptors in pain: a review Anesth. Analg. 97 4 2003 1108 1116
46. S. Poole, F.Q. Cunha, and S.H. Ferreira Hyperalgesia from subcutaneous cytokines L.R. BirkhäuserWatkins, S.F. Maier, Cytokines and Pain Basel 1999 59 87
47. J.P. Redrobe, E.Ø. Nielsen, J.K. Christensen, D. Peters, D.B. Timmermann, and G.M. Olsen Alpha7 nicotinic acetylcholine receptor activation ameliorates scopolamine-induced behavioural changes in a modified continuous Y-maze task in mice Eur. J. Pharmacol. 602 1 2009 58 65
48. 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
49. J. Rodrigo, D.R. Springall, O. Uttenthal, M.L. Bentura, F. Abadia-Molina, V. Riveros-Moreno, R. Martínez-Murillo, J.M. Polak, and S. Moncada Localization of nitric oxide synthase in the adult rat brain Philos. Trans. R. Soc. Lond. B. Biol. Sci. 345 1312 1994 175 221
50. G. Sánchez-Andrade, B.M. James, and K.M. Kendrick Neural encoding of olfactory recognition memory J. Reprod. Dev. 51 5 2005 547 558
51. R. Sattler, Z. Xiong, W.Y. Lu, M. Hafner, J.F. MacDonald, and M. Tymianski Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein Science 284 5421 1999 1845 1848
52. F. Tao, Y.X. Tao, J.A. Gonzalez, M. Fang, P. Mao, and R.A. Johns Knockdown of PSD-95/SAP90 delays the development of neuropathic pain in rats Neuroreport 12 2001 3251 3255
53. F. Tao, Y.X. Tao, P. Mao, and R.A. Johns Role of postsynaptic density protein-95 in the maintenance of peripheral nerve injury-induced neuropathic pain in rats Neuroscience 117 2003 731 739
54. F. Tao, Y.X. Tao, C. Zhao, S. Doré, W.J. Liaw, S.N. Raja, and R.A. Johns Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia Neuroscience 128 2004 421 430
55. F. Tao, Q. Su, and R.A. Johns Cell-permeable peptide Tat-PSD-95 PDZ2 inhibits chronic inflammatory pain behaviors in mice Mol. Ther. 16 11 2008 1776 1782
56. T. Utkan, S.S. Gocmez, C. Ozer, N. Gacar, and F. Aricioglu Selective and nonselective neuronal NOS inhibitors impair cognitive function in the three panel runway and passive avoidance tasks in rats Pharmacol. Biochem. Behav. 101 4 2012 515 519
57. W.A. Verri Jr., T.M. Cunha, C.A. Parada, S. Poole, F.Q. Cunha, and S.H. Ferreira Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol. Ther. 112 2006 116 138
58. S.R. Vincent, J.A. Williams, P.B. Reiner, and A.el-D. el-Husseini Monitoring neuronal NO release in vivo in cerebellum, thalamus and hippocampus Prog. Brain Res. 118 1998 27 35
59. C. Wass, T. Archer, E. Palsson, K. Fejgin, A. Alexandersson, D. Klamer, J.A. Engel, and L. Svensson Phencyclidine affects memory in a nitric oxide-dependent manner: working and reference memory Behav. Brain Res. 174 2006 49 55
60. C.C. Wrenn, A.P. Harris, M.C. Saavedra, and J.N. Crawley Social transmission of food preference in mice: methodology and application to galanin-overexpressing transgenic mice Behav. Neurosci. 117 1 2003 21 31
61. X. Zou, Q. Lin, and W.D. Willis Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats Neuroscience 115 2002 775 786
62. L.B. Zou, K. Yamada, T. Tanaka, T. Kameyama, and T. Nabeshima Nitric oxide synthase inhibitors impair reference memory formation in a radial arm maze task in rats Neuropharmacology 37 1998 323 330