Effects of NB001 and gabapentin on irritable bowel syndrome-induced behavioral anxiety and spontaneous pain

Molecular Brain

Volumn 7, Issue 1, 2014, Pages

  Zhang, Ming Ming ^a,b   Liu, Shui Bing ^b,c   Chen, Tao ^a,c   Koga, Kohei ^b,c   Zhang, Ting ^a   Li, Yun Qing ^a   Zhuo, Min ^b,c  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF TORONTO   (Canada)

^c XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Anxiety; Irritable bowel syndrome; Spontaneous pain; Visceral pain; Zymosan

Indexed keywords

ADENYLATE CYCLASE INHIBITOR; ANALGESIC AGENT; GABAPENTIN; NB 001; PROTEIN FOS; UNCLASSIFIED DRUG; ZYMOSAN; SODIUM CHLORIDE;

ADULT; AMYGDALOID NUCLEUS; ANALGESIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ANXIETY; ARTICLE; BRAIN REGION; BRAIN STEM; COGNITION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EMOTION; FOREBRAIN; INSULA; IRRITABLE COLON; MALE; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OPEN FIELD TEST; PAIN ASSESSMENT; PARABRACHIAL NUCLEUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBCORTEX; UPREGULATION; VISCERAL PAIN; ANIMAL TISSUE; ANXIETY DISORDER;

ADENOSINE TRIPHOSPHATE; AMINES; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CYCLOHEXANECARBOXYLIC ACIDS; GAMMA-AMINOBUTYRIC ACID; INJECTIONS, INTRAPERITONEAL; IRRITABLE BOWEL SYNDROME; MALE; MICE; MICE, INBRED C57BL; PAIN; PROTO-ONCOGENE PROTEINS C-FOS; UP-REGULATION; VISCERAL PAIN; ZYMOSAN;

ANIMALIA;

EID: 84903695709     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-7-47     Document Type: Article

References (82)

1. Role of visceral afferent mechanisms in functional bowel disorders. Mayer EA, Raybould HE, Gastroenterology 1990 99 1688 1704
2. Visceral pain. Cervero F, Laird JM, Lancet 1999 353 2145 2148 (Pubitemid 29278493)
3. The pharmacology of gastrointestinal nociceptive pathways. Blackshaw LA, Gebhart GF, Curr Opin Pharmacol 2002 2 642 649 (Pubitemid 35476914)
4. Visceral pain: a review of experimental studies. Ness TJ, Gebhart GF, Pain 1990 41 167 234 (Pubitemid 20179930)
5. Mechanisms underlying visceral hypersensitivity in irritable bowel syndrome. Barbara G, Cremon C, De Giorgio R, Dothel G, Zecchi L, Bellacosa L, Carini G, Stanghellini V, Corinaldesi R, Curr Gastroenterol Rep 2011 13 308 315
6. Activation of guanylate cyclase-C attenuates stretch responses and sensitization of mouse colorectal afferents. Feng B, Kiyatkin ME, La JH, Ge P, Solinga R, Silos-Santiago I, Gebhart GF, J Neurosci 2013 33 9831 9839
7. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. Neural and neuro-immune mechanisms of visceral hypersensitivity in irritable bowel syndrome. Feng B, La JH, Schwartz ES, Gebhart GF, Am J Physiol Gastrointest Liver Physiol 2012 302 1085 G1098
8. Development, plasticity and modulation of visceral afferents. Christianson JA, Bielefeldt K, Altier C, Cenac N, Davis BM, Gebhart GF, High KW, Kollarik M, Randich A, Undem B, Vergnolle N, Brain Res Rev 2009 60 171 186
9. Understanding the signaling and transmission of visceral nociceptive events. Cervero F, Laird JM, J Neurobiol 2004 61 45 54 (Pubitemid 39287769)
10. Anxiety and depression comorbidities in irritable bowel syndrome (IBS): a systematic review and meta-analysis. Fond G, Loundou A, Hamdani N, Boukouaci W, Dargel A, Oliveira J, Roger M, Tamouza R, Leboyer M, Boyer L, Eur Arch Psychiatry Clin Neurosci 2014 Epub ahead of print
11. The epidemiology of irritable bowel syndrome. Canavan C, West J, Card T, Clin Epidemiol 2014 6 71 80
12. Visceral pain hypersensitivity in functional gastrointestinal disorders. Farmer AD, Aziz Q, Br Med Bull 2009 91 123 136
13. Psychological problems in gastroenterology outpatients: A South Australian experience. Psychological co-morbidity in IBD, IBS and hepatitis C. Mikocka-Walus AA, Turnbull DA, Andrews JM, Moulding NT, Wilson IG, Harley HA, Hetzel DJ, Holtmann GJ, Clin Pract Epidemiol Ment Health 2008 4 15
14. Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Dinan TG, Quigley EM, Ahmed SM, Scully P, O'Brien S, O'Mahony L, O'Mahony S, Shanahan F, Keeling PW, Gastroenterology 2006 130 304 311 (Pubitemid 43202030)
15. Stress and visceral pain: focusing on irritable bowel syndrome. Fukudo S, Pain 2013 154 Suppl 1 63 S70
16. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M, Neuron 2005 47 859 872 (Pubitemid 41266952)
17. Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Descalzi G, Li XY, Chen T, Mercaldo V, Koga K, Zhuo M, Mol Brain 2012 5 6
18. Cortical excitation and chronic pain. Zhuo M, Trends Neurosci 2008 31 199 207
19. An increase in synaptic NMDA receptors in the insular cortex contributes to neuropathic pain. Qiu S, Chen T, Koga K, Guo YY, Xu H, Song Q, Wang JJ, Descalzi G, Kaang BK, Luo JH, Zhuo M, Zhao MG, Sci Signal 2013 6 a34
20. Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M, Nat Neurosci 2001 4 164 169 (Pubitemid 32125261)
21. Pain and emotion interactions in subregions of the cingulate gyrus. Vogt BA, Nat Rev Neurosci 2005 6 533 544 (Pubitemid 40942820)
22. Long-term potentiation in the anterior cingulate cortex and chronic pain. Zhuo M, Philos Trans R Soc Lond B Biol Sci 2014 369 20130146
23. Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Kim SS, Wang H, Li XY, Chen T, Mercaldo V, Descalzi G, Wu LJ, Zhuo M, Mol Brain 2011 4 6
24. Brain responses to visceral stimuli reflect visceral sensitivity thresholds in patients with irritable bowel syndrome. Larsson MB, Tillisch K, Craig AD, Engstrom M, Labus J, Naliboff B, Lundberg P, Strom M, Mayer EA, Walter SA, Gastroenterology 2012 142 463 472 e463
25. Amitriptyline reduces rectal pain related activation of the anterior cingulate cortex in patients with irritable bowel syndrome. Morgan V, Pickens D, Gautam S, Kessler R, Mertz H, Gut 2005 54 601 607 (Pubitemid 40559240)
26. Abnormal forebrain activity in functional bowel disorder patients with chronic pain. Kwan CL, Diamant NE, Pope G, Mikula K, Mikulis DJ, Davis KD, Neurology 2005 65 1268 1277 (Pubitemid 41508222)
27. Enhanced affect/cognition-related brain responses during visceral placebo analgesia in irritable bowel syndrome patients. Lee HF, Hsieh JC, Lu CL, Yeh TC, Tu CH, Cheng CM, Niddam DM, Lin HC, Lee FY, Chang FY, Pain 2012 153 1301 1310
28. Affective disturbances modulate the neural processing of visceral pain stimuli in irritable bowel syndrome: an fMRI study. Elsenbruch S, Rosenberger C, Enck P, Forsting M, Schedlowski M, Gizewski ER, Gut 2010 59 489 495
29. Colorectal distension-induced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Gibney SM, Gosselin RD, Dinan TG, Cryan JF, Neuroscience 2010 165 675 683
30. Central representation of visceral and cutaneous hypersensitivity in the irritable bowel syndrome. Verne GN, Himes NC, Robinson ME, Gopinath KS, Briggs RW, Crosson B, Price DD, Pain 2003 103 99 110 (Pubitemid 36579090)
31. A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Zhuo M, Molecules and cells 2007 23 259 271 (Pubitemid 47181042)
32. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. Wei F, Li P, Zhuo M, J Neurosci 1999 19 9346 9354 (Pubitemid 30228088)
33. Targeting neuronal adenylyl cyclase for the treatment of chronic pain. Zhuo M, Drug Discov Today 2012 17 573 582
34. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M, J Neurosci 2008 28 7445 7453
35. Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. Liauw J, Wu LJ, Zhuo M, J Neurophysiol 2005 94 878 882 (Pubitemid 40923296)
36. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M, Science 2010 330 1400 1404
37. Identification of an adenylyl cyclase inhibitor for treating neuropathic and inflammatory pain. Wang H, Xu H, Wu LJ, Kim SS, Chen T, Koga K, Descalzi G, Gong B, Vadakkan KI, Zhang X, Kaang BK, Zhuo M, Sci Transl Med 2011 3 65ra63
38. Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, Xu HM, Chen ZF, Storm DR, Muglia LJ, Zhuo M, Neuron 2002 36 713 726 (Pubitemid 35346762)
39. Genetic reduction of chronic muscle pain in mice lacking calcium/calmodulin-stimulated adenylyl cyclases. Vadakkan KI, Wang H, Ko SW, Zastepa E, Petrovic MJ, Sluka KA, Zhuo M, Mol Pain 2006 2 7
40. Intracolonic zymosan produces visceral hyperalgesia in the rat that is mediated by spinal NMDA and non-NMDA receptors. Coutinho SV, Meller ST, Gebhart GF, Brain Res 1996 736 7 15 (Pubitemid 26356457)
41. Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Jones RC 3rd, Otsuka E, Wagstrom E, Jensen CS, Price MP, Gebhart GF, Gastroenterology 2007 133 184 194 (Pubitemid 47031128)
42. The safety and effectiveness of newer antiepileptics: a comparative postmarketing cohort study. Acharya NV, Pickering RM, Wilton LW, Shakir SA, J Clin Pharmacol 2005 45 385 393
43. Long-term regulation of voltage-gated Ca(2+) channels by gabapentin. Kang MG, Felix R, Campbell KP, FEBS Lett 2002 528 177 182 (Pubitemid 35258020)
44. EFNS guidelines on the pharmacological treatment of neuropathic pain: 2010 revision. Attal N, Cruccu G, Baron R, Haanpaa M, Hansson P, Jensen TS, Nurmikko T, Eur J Neurol 2010 17 1113 e1188
45. Fos, nociception and the dorsal horn. Coggeshall RE, Prog Neurobiol 2005 77 299 352 (Pubitemid 41815592)
46. Acute colitis induces neurokinin 1 receptor internalization in the rat lumbosacral spinal cord. Zhang MM, Ji W, Pei LY, Wang W, Chen T, Li H, Zhang T, Wu SX, Li YQ, PLoS One 2013 8 59234
47. Peripheral and central P2X receptor contributions to colon mechanosensitivity and hypersensitivity in the mouse. Shinoda M, Feng B, Gebhart GF, Gastroenterology 2009 137 2096 2104
48. Altered purinergic signaling in colorectal dorsal root ganglion neurons contributes to colorectal hypersensitivity. Shinoda M, La JH, Bielefeldt K, Gebhart GF, J Neurophysiol 2010 104 3113 3123
49. A new model of visceral pain and referred hyperalgesia in the mouse. Laird JM, Martinez-Caro L, Garcia-Nicas E, Cervero F, Pain 2001 92 335 342 (Pubitemid 32480163)
50. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Prut L, Belzung C, Eur J Pharmacol 2003 463 3 33 (Pubitemid 36205070)
51. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Carola V, D'Olimpio F, Brunamonti E, Mangia F, Renzi P, Behav Brain Res 2002 134 49 57 (Pubitemid 34912685)
52. The mouse light/dark box test. Bourin M, Hascoet M, Eur J Pharmacol 2003 463 55 65 (Pubitemid 36205072)
53. Genetic evidence for adenylyl cyclase 1 as a target for preventing neuronal excitotoxicity mediated by N-methyl-D-aspartate receptors. Wang H, Gong B, Vadakkan KI, Toyoda H, Kaang BK, Zhuo M, J Biol Chem 2007 282 1507 1517 (Pubitemid 47076580)
54. Neuronal mechanism for neuropathic pain. Zhuo M, Mol Pain 2007 3 14
55. Relative potency of pregabalin, gabapentin, and morphine in a mouse model of visceral pain. Shamsi Meymandi M, Keyhanfar F, Can J Anaesth 2013 60 44 49
56. The effects of gabapentin in two animal models of co-morbid anxiety and visceral hypersensitivity. O' Mahony SM, Coelho AM, Fitzgerald P, Lee K, Winchester W, Dinan TG, Cryan JF, Eur J Pharmacol 2011 667 169 174
57. Functional organization of the rodent parabrachial nucleus. Yamamoto T, Takemura M, Inui T, Torii K, Maeda N, Ohmoto M, Matsumoto I, Abe K, Ann N Y Acad Sci 2009 1170 378 382
58. Differential content of vesicular glutamate transporters in subsets of vagal afferents projecting to the nucleus tractus solitarii in the rat. Hermes SM, Colbert JF, Aicher SA, J Comp Neurol 2014 522 642 653
59. Irritable bowel syndrome in the United States: prevalence, symptom patterns and impact. Hungin AP, Chang L, Locke GR, Dennis EH, Barghout V, Aliment Pharmacol Ther 2005 21 1365 1375 (Pubitemid 40813683)
60. The prevalence, patterns and impact of irritable bowel syndrome: an international survey of 40,000 subjects. Hungin AP, Whorwell PJ, Tack J, Mearin F, Aliment Pharmacol Ther 2003 17 643 650 (Pubitemid 36418887)
61. Effects of chronic electroacupuncture on depression- and anxiety-like behaviors in rats with chronic neuropathic pain. Li Q, Yue N, Liu SB, Wang ZF, Mi WL, Jiang JW, Wu GC, Yu J, Wang YQ, Evid Based Complement Alternat Med 2014 2014 158987
62. Persistent nociception induces anxiety-like behavior in rodents: Role of endogenous neuropeptide S. Zhang S, Jin X, You Z, Wang S, Lim G, Yang J, McCabe M, Li N, Marota J, Chen L, Mao J, Pain 2014 Epub ahead of print
63. Time-dependent analysis of nociception and anxiety-like behavior in rats submitted to persistent inflammation of the temporomandibular joint. Do Nascimento GC, Leite-Panissi CR, Physiol Behav 2014 125 1 7
64. Cognitive and emotional control of pain and its disruption in chronic pain. Bushnell MC, Ceko M, Low LA, Nat Rev Neurosci 2013 14 502 511
65. Association of depression and anxiety alone and in combination with chronic musculoskeletal pain in primary care patients. Bair MJ, Wu J, Damush TM, Sutherland JM, Kroenke K, Psychosom Med 2008 70 890 897
66. Does severe acute pain provoke lasting changes in attentional and emotional mechanisms of pain-related processing? A longitudinal study. Dimova V, Horn C, Parthum A, Kunz M, Schofer D, Carbon R, Griessinger N, Sittl R, Lautenbacher S, Pain 2013 154 2737 2744
67. Uncertainty and anticipation in anxiety: an integrated neurobiological and psychological perspective. Grupe DW, Nitschke JB, Nat Rev Neurosci 2013 14 488 501
68. Behavioral indices of ongoing pain are largely unchanged in male mice with tissue or nerve injury-induced mechanical hypersensitivity. Urban R, Scherrer G, Goulding EH, Tecott LH, Basbaum AI, Pain 2011 152 990 1000
69. Microbiota, disease, and back to health: a metastable journey. Blumberg R, Powrie F, Sci Transl Med 2012 4 137rv137
70. Gut microbiota: Intestinal bacteria influence brain activity in healthy humans. Collins SM, Bercik P, Nat Rev Gastroenterol Hepatol 2013 10 326 327
71. The interplay between the intestinal microbiota and the brain. Collins SM, Surette M, Bercik P, Nat Rev Microbiol 2012 10 735 742
72. Cortical plasticity as a new endpoint measurement for chronic pain. Zhuo M, Mol Pain 2011 7 54
73. Dissociating anxiety from pain: mapping the neuronal marker N-acetyl aspartate to perception distinguishes closely interrelated characteristics of chronic pain. Grachev ID, Fredickson BE, Apkarian AV, Mol Psychiatry 2001 6 256 258 (Pubitemid 32275667)
74. Mechanisms of action of gabapentin. Taylor CP, Rev Neurol (Paris) 1997 153 Suppl 1 39 S45
75. T-type calcium channels inhibitors: a patent review. Giordanetto F, Knerr L, Wallberg A, Expert Opin Ther Pat 2011 21 85 101
76. A novel mechanism of inhibition of high-voltage activated calcium channels by alpha-conotoxins contributes to relief of nerve injury-induced neuropathic pain. Klimis H, Adams DJ, Callaghan B, Nevin S, Alewood PF, Vaughan CW, Mozar CA, Christie MJ, Pain 2011 152 259 266
77. Anxiety-like behaviour in rats with mononeuropathy is reduced by the analgesic drugs morphine and gabapentin. Roeska K, Doods H, Arndt K, Treede RD, Ceci A, Pain 2008 139 349 357
78. Anxiety-like behaviour is attenuated by gabapentin, morphine and diazepam in a rodent model of HIV anti-retroviral-associated neuropathic pain. Wallace VC, Segerdahl AR, Blackbeard J, Pheby T, Rice AS, Neurosci Lett 2008 448 153 156
79. Gabapentin-induced neurologic toxicities. Bookwalter T, Gitlin M, Pharmacotherapy 2005 25 1817 1819 (Pubitemid 41790104)
80. Gabapentin-associated hepatotoxicity. Lasso-de-la-Vega MC, Zapater P, Such J, Perez-Mateo M, Horga JF, Am J Gastroenterol 2001 96 3460 3462
81. Gabapentin-induced coma in a patient with renal failure. Dogukan A, Aygen B, Berilgen MS, Dag S, Bektas S, Gunal AI, Hemodial Int 2006 10 168 169
82. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Hogg S, Pharmacol Biochem Behav 1996 54 21 30 (Pubitemid 26146661) Canada