Activation of extracellular signal-regulated protein kinase is associated with colorectal distension-induced spinal and supraspinal neuronal response and neonatal maternal separation-induced visceral hyperalgesia in rats

Journal of Molecular Neuroscience

Volumn 37, Issue 3, 2009, Pages 274-287

  Zhang, X J ^a   Li, Z ^a   Chung, E K Y ^a   Zhang, H Q ^a   Xu, H X ^b   Sung, J J Y ^c   Bian, Z X ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

C fos; ERK; Neonatal maternal separation; Visceral hyperalgesia

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CINGULATE GYRUS; COLON DILATATION; CONTROLLED STUDY; HYPERALGESIA; IMMUNOBLOTTING; MALE; MATERNAL DEPRIVATION; NERVE POTENTIAL; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; COLON; CYTOLOGY; ENZYME ACTIVATION; FEMALE; LESIONS AND DEFECTS; METABOLISM; NERVE CELL; PAIN; PATHOLOGY; PHYSIOLOGY; PREGNANCY; RANDOMIZATION; RECTUM; SPINAL CORD; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; COLON; DILATATION, PATHOLOGIC; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HYPERALGESIA; MALE; MATERNAL DEPRIVATION; NEURONS; PAIN; PREGNANCY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECTUM; SPINAL CORD;

EID: 62149111152     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-008-9134-y     Document Type: Article

References (54)

1. E. D. Al-Chaer Y. Feng W. D. Willis 1998 A role for the dorsal column in nociceptive visceral input into the thalamus of primates Journal of Neurophysiology 79 3143 3150 9636114 1:STN:280:DyaK1czgtFGitw%3D%3D
2. F. Barreau L. Ferrier J. Fioramonti L. Bueno 2007 New insights in the etiology and pathophysiology of irritable bowel syndrome: contribution of neonatal stress models Pediatric Research 62 240 245 17622962 10.1203/PDR.0b013e3180db2949 (Pubitemid 47301468)
3. T. Bast 2007 Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior Reviews in the Neurosciences 18 253 281 18019609
4. E. Bullitt 1990 Expression of c-fos-like protein as a marker for neuronal-activity following noxious-stimulation in the rat The Journal of Comparative Neurology 296 517 530 2113539 10.1002/cne.902960402 1:STN:280:By%2BB1Mzit1w%3D (Pubitemid 20191460)
5. A. Chaouch J. M. Besson 1986 Peripheral and spinal mechanisms of nociception Revue Neurologique 142 173 200 3099361 1:STN:280:BiiD1MzmvF0%3D
6. E. K. Y. Chung X. J. Zhang Z. Li H. Q. Zhang H. X. Xu Z. X. Bian 2007 Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat Brain Research 1153 68 77 17434464 10.1016/j.brainres.2007.03. 047 1:CAS:528:DC%2BD2sXlvVyisLk%3D (Pubitemid 46802528)
7. E. K. Chung X. J. Zhang H. X. Xu J. J. Sung Z. X. Bian 2007 Visceral hyperalgesia induced by neonatal maternal separation is associated with nerve growth factor-mediated central neuronal plasticity in rat spinal cord Neuroscience 149 685 695 17913374 10.1016/j.neuroscience.2007.07.055 1:CAS:528:DC%2BD2sXht1ahu7bN (Pubitemid 47633020)
8. R. E. Coggeshall 2005 Fos, nociception and the dorsal horn Progress in Neurobiology 77 299 352 16356622 1:CAS:528:DC%2BD2MXhtlCrtr7N
9. S. V. Coutinho P. M. Plotsky M. Sablad J. C. Miller H. Zhou A. I. Bayati, et al. 2002 Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat American Journal of Physiology. Gastrointestinal and Liver Physiology 282 G307 G316 11804852 1:CAS:528:DC%2BD38XhtFGiurc%3D
10. S. V. Coutinho M. R. Sablad J. C. Miller H. Zhou A. Lam A. I. Bayati, et al. 2000 Neonatal maternal separation results in stress-induced visceral hyperalgesia in adult rats: a new model for IBS Gastroenterology 118 A637
11. C. D. Cruz D. Ferreira S. B. McMahon F. Cruz 2007 The activation of the ERK pathway contributes to the spinal c-fos expression observed after noxious bladder stimulation Somatosensory & Motor Research 24 15 20 10.1080/08990220601143265 (Pubitemid 47250623)
12. Y. Dai K. Iwata T. Fukuoka E. Kondo A. Tokunaga H. Yamanaka, et al. 2002 Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization The Journal of Neuroscience 22 7737 7745 12196597 1:CAS:528:DC%2BD38XmvFCmtL0%3D
13. L. Daulhac C. Mallet C. Courteix M. Etienne E. Duroux A. M. Privat, et al. 2006 Diabetes-induced mechanical hyperalgesia involves spinal mitogen-activated protein kinase activation in neurons and microglia via N-methyl-d-aspartate-dependent mechanisms Molecular Pharmacology 70 1246 1254 16868181 10.1124/mol.106.025478 1:CAS:528:DC%2BD28XhtVOjt7bL (Pubitemid 44435976)
14. G. Dent D. C. Choi J. P. Herman S. Levine 2007 GABAergic circuits and the stress hyporesponsive period in the rat: ontogeny of glutamic acid decarboxylase (GAD) 67 mRNA expression in limbic-hypothalamic stress pathways Brain Research 1138 1 9 17276416 10.1016/j.brainres.2006.04.082 1:CAS:528:DC%2BD2sXit1Kjtbc%3D (Pubitemid 46281879)
15. V. Duric K. E. McCarson 2006 Persistent pain produces stress-like alterations in hippocampal neurogenesis and gene expression Journal of Pain 7 544 555 16885011 10.1016/j.jpain.2006.01.458 (Pubitemid 44119288)
16. A. Galan F. Cervero J. M. Laird 2003 Extracellular signaling-regulated kinase-1 and -2 (ERK 1/2) mediate referred hyperalgesia in a murine model of visceral pain Brain Research. Molecular Brain Research 116 126 134 12941468 10.1016/S0169-328X(03)00284-5 1:CAS:528:DC%2BD3sXms1ylt7o%3D (Pubitemid 36993703)
17. M. G. Gareau J. Jury P. C. Yang G. MacQueen M. H. Perdue 2006 Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance Pediatric Research 59 83 88 16326990 10.1203/01.pdr.0000190577. 62426.45 (Pubitemid 43754460)
18. M. Gioia S. Galbiati L. Rigamonti C. Moscheni N. Gagliano 2001 Extracellular signal-regulated kinases 1 and 2 phosphorylated neurons in the tele- and diencephalon of rat after visceral pain stimulation: an immunocytochemical study Neuroscience Letters 308 177 180 11479017 10.1016/S0304-3940(01)02008-0 1:CAS:528:DC%2BD3MXls1eisLg%3D (Pubitemid 32710152)
19. M. Gioia C. Moscheni S. Galbiati N. Gagliano 2003 Immunocytochemical localization of extracellular signal-regulated kinases 1 and 2 phosphorylated neurons in the brainstem of rat following visceral noxious stimulation Neuroscience Letters 349 167 170 12951195 10.1016/S0304-3940(03)00821-8 1:CAS:528:DC%2BD3sXmvVyit7w%3D (Pubitemid 37297804)
20. S. W. Guo M. G. Liu Y. L. Long L. Y. Ren Z. M. Lu H. Y. Yu, et al. 2007 Region- or state-related differences in expression and activation of extracellular signal-regulated kinases (ERKs) in naive and pain-experiencing rats BMC Neuroscience 8 53 17650295 10.1186/1471-2202-8-53 1:CAS:528: DC%2BD2sXmt12ksro%3D (Pubitemid 47288069)
21. T. G. Heffner J. A. Hartman L. S. Seiden 1980 A rapid method for the regional dissection of the rat brain Pharmacology, Biochemistry, and Behavior 13 453 456 7422701 10.1016/0091-3057(80)90254-3 1:STN:280:Bi6D3s3mtlQ%3D (Pubitemid 10008987)
22. R. L. Huot K. V. Thrivikraman M. J. Meaney P. M. Plotsky 2001 Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment Psychopharmacology 158 366 373 11797057 10.1007/s002130100701 1:CAS:528:DC%2BD38XnsVKqtg%3D%3D (Pubitemid 33141312)
23. R. Ikeda Y. Takahashi K. Inoue F. Kato 2007 NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain Pain 127 161 172 17055162 10.1016/j.pain.2006.09.003 1:CAS:528: DC%2BD2sXht1ertg%3D%3D (Pubitemid 44959439)
24. A. Ikoma R. Rukwied S. Stander M. Steinhoff Y. Miyachi M. Schmelz 2003 Neuronal sensitization for histamine-induced itch in lesional skin of patients with atopic dermatitis Archives of Dermatology 139 1455 1458 14623705 10.1001/archderm.139.11.1455 (Pubitemid 37433135)
25. H. Imbe S. Murakami K. Okamoto Y. Iwai-Liao E. Senba 2004 The effects of acute and chronic restraint stress on activation of ERK in the rostral ventromedial medulla and locus coeruleus Pain 112 361 371 15561392 10.1016/j.pain.2004.09.015 (Pubitemid 39550737)
26. R. R. Ji C. J. Woolf 2001 Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain Neurobiology of Disease 8 1 10 11162235 10.1006/nbdi.2000.0360 1:CAS:528:DC%2BD3MXpvVSrtQ%3D%3D (Pubitemid 32171813)
27. Y. Kawasaki T. Kohno Z. Y. Zhuang G. J. Brenner H. Wang M. C. Van Der, et al. 2004 Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization The Journal of Neuroscience 24 8310 8321 15385614 10.1523/JNEUROSCI.2396-04.2004 1:CAS:528:DC%2BD2cXotVyntL0%3D (Pubitemid 39280810)
28. R. J. Kelleher A. Govindarajan H. Y. Jung H. J. Kang S. Tonegawa 2004 Translational control by MAPK signaling in long-term synaptic plasticity and memory Cell 116 467 479 15016380 10.1016/S0092-8674(04)00115-1 1:CAS:528:DC%2BD2cXhsFagt78%3D (Pubitemid 38366322)
29. Y. Kominato T. Tachibana Y. Dai H. Tsujino S. Maruo K. Noguchi 2003 Changes in phosphorylation of ERK and Fos expression in dorsal horn neurons following noxious stimulation in a rat model of neuritis of the nerve root Brain Research 967 89 97 12650969 10.1016/S0006-8993(02)04229-4 1:CAS:528: DC%2BD3sXitV2gsbw%3D (Pubitemid 36324291)
30. V. Martinez L. X. Wang Y. Tache 2006 Proximal colon distension induces Fos expression in the brain and inhibits gastric emptying through capsaicin-sensitive pathways in conscious rats Brain Research 1086 168 180 16626641 10.1016/j.brainres.2006.02.063 1:CAS:528:DC%2BD28XksVCqt7s%3D
31. H. Mertz 2003 Review article: visceral hypersensitivity Alimentary Pharmacology & Therapeutics 17 623 633 10.1046/j.1365-2036.2003.01447.x 1:CAS:528:DC%2BD3sXjt1ejs7Y%3D (Pubitemid 36418885)
32. M. J. Millan 1999 The induction of pain: an integrative review Progress in Neurobiology 57 1 164 9987804 10.1016/S0301-0082(98)00048-3 1:CAS:528:DyaK1MXitVOjsA%3D%3D (Pubitemid 28551764)
33. M. Million L. Wang Y. Wang D. W. Adelson P. Q. Yuan C. Maillot, et al. 2006 CRF2 receptor activation prevents colorectal distension induced visceral pain and spinal ERK1/2 phosphorylation in rats Gut 55 172 181 15985561 10.1136/gut.2004.051391 1:CAS:528:DC%2BD28XhsFaqs7c%3D (Pubitemid 43117273)
34. H. Monnikes J. Ruter M. Konig C. Grote P. Kobelt B. F. Klapp, et al. 2003 Differential induction of c-fos expression in brain nuclei by noxious and non-noxious colonic distension: role of afferent C-fibers and 5-HT3 receptors Brain Research 966 253 264 12618348 10.1016/S0006-8993(02)04197-5 1:CAS:528:DC%2BD3sXhs1ags7c%3D (Pubitemid 36255588)
35. K. Obata K. Noguchi 2004 MAPK activation in nociceptive neurons and pain hypersensitivity Life Sciences 74 2643 2653 15041446 10.1016/j.lfs.2004.01.007 1:CAS:528:DC%2BD2cXisVemtro%3D (Pubitemid 38369361)
36. K. Obata H. Yamanaka K. Kobayashi Y. Dai T. Mizushima H. Katsura, et al. 2004 Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation The Journal of Neuroscience 24 10211 10222 15537893 10.1523/JNEUROSCI.3388-04.2004 1:CAS:528:DC%2BD2cXhtVeqtb7F (Pubitemid 39492048)
37. J. Palecek 2004 The role of dorsal columns pathway in visceral pain Physiological Research 53 S125 S130 15119943
38. J. Palecek V. Paleckova W. D. Willis 2003 Fos expression in spinothalamic and postsynaptic dorsal column neurons following noxious visceral and cutaneous stimuli Pain 104 249 257 12855335 10.1016/S0304-3959(03)00013-7 1:CAS:528:DC%2BD3sXltF2gu7c%3D (Pubitemid 36835894)
39. C. Pihoker M. J. Owens C. M. Kuhn S. M. Schanberg C. B. Nemeroff 1993 Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis-a putative role for corticotropin-releasing factor Psychoneuroendocrinology 18 485 493 8265736 10.1016/0306-4530(93)90042-J 1:CAS:528:DyaK2cXht1Ggt7Y%3D (Pubitemid 23289034)
40. E. Polgar A. D. Campbell L. M. MacIntyre M. Watanabe A. J. Todd 2007 Phosphorylation of ERK in neurokinin 1 receptor-expressing neurons in laminae III and IV of the rat spinal dorsal horn following noxious stimulation Molecular Pain 3 4 17309799 10.1186/1744-8069-3-4 (Pubitemid 46351584)
41. T. H. Ren J. Wu D. Yew E. Ziea L. Lao W. K. Leung, et al. 2007 Effects of neonatal maternal separation on neurochemical and sensory response to colonic distension in a rat model of irritable bowel syndrome American Journal of Physiology. Gastrointestinal and Liver Physiology 292 G849 G856 17110521 10.1152/ajpgi.00400.2006 1:CAS:528:DC%2BD2sXjsFequ78%3D (Pubitemid 46440389)
42. S. M. Sagar F. R. Sharp T. Curran 1988 Expression of c-fos protein in brain: metabolic mapping at the cellular-level Science 240 1328 1331 3131879 10.1126/science.3131879 1:CAS:528:DyaL1cXkt1SlsLY%3D
43. X. S. Song J. L. Cao Y. B. Xu J. H. He L. C. Zhang Y. M. Zeng 2005 Activation of ERK/CREB pathway in spinal cord contributes to chronic constrictive injury-induced neuropathic pain in rats Acta Pharmacologica Sinica 26 789 798 15960884 10.1111/j.1745-7254.2005.00123.x 1:CAS:528: DC%2BD2MXmtlChsbw%3D (Pubitemid 40978759)
44. D. Spani M. Arras B. Konig T. Rulicke 2003 Higher heart rate of laboratory mice housed individually vs in pairs Laboratory Animals 37 54 62 12626072 10.1258/002367703762226692 1:STN:280:DC%2BD3s7htlOqsA%3D%3D (Pubitemid 36143328)
45. C. I. Svensson M. Marsala A. Westerlund N. A. Calcutt W. M. Campana J. D. Freshwater, et al. 2003 Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing Journal of Neurochemistry 86 1534 1544 12950462 10.1046/j.1471-4159. 2003.01969.x 1:CAS:528:DC%2BD3sXnsV2iurs%3D (Pubitemid 37174270)
46. J. D. Sweatt 2004 Mitogen-activated protein kinases in synaptic plasticity and memory Current Opinion in Neurobiology 14 311 317 15194111 10.1016/j.conb.2004.04.001 1:CAS:528:DC%2BD2cXkvV2nsr0%3D (Pubitemid 38759861)
47. A. Trentani S. D. Kuipers G. J. Ter Horst J. A. Den Boer 2002 Selective chronic stress-induced in vivo ERK1/2 hyperphosphorylation in medial prefrontocortical dendrites: implications for stress-related cortical pathology? The European Journal of Neuroscience 15 1681 1691 12059976 10.1046/j.1460-9568. 2002.02000.x 1:STN:280:DC%2BD38zhslCktg%3D%3D (Pubitemid 35471924)
48. E. Valjent J. Caboche P. Vanhoutte 2001 Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain-a molecular substrate for learning and memory? Molecular Neurobiology 23 83 99 11817219 10.1385/MN:23:2-3:083 1:CAS:528:DC%2BD3MXpt1Wrtr0%3D
49. A. Vicentic D. Francis M. Moffett A. Lakatos G. Rogge G. W. Hubert, et al. 2006 Maternal separation alters serotonergic transporter densities and serotonergic 1A receptors in rat brain Neuroscience 140 355 365 16530973 10.1016/j.neuroscience.2006.02.008 1:CAS:528:DC%2BD28XksVGisL0%3D (Pubitemid 43668442)
50. H. C. Wang S. C. Chai Y. S. Wu C. C. Wang 2007 Does the medial thalamus play a role in the negative affective component of visceral pain in rats? Neuroscience Letters 420 80 84 17512660 10.1016/j.neulet.2007.04.064 1:CAS:528:DC%2BD2sXlvVyiu7k%3D (Pubitemid 46777111)
51. C. J. Woolf M. W. Salter 2000 Neuronal plasticity: increasing the gain in pain Science 288 1765 1768 10846153 10.1126/science.288.5472.1765 1:CAS:528:DC%2BD3cXjvFCisr8%3D (Pubitemid 30399008)
52. X. J. Zhang Z. Li W. M. Leung L. Liu H. X. Xu Z. X. Bian 2008 The analgesic effect of paeoniflorin on neonatal maternal separation-induced visceral hyperalgesia in rats Journal of Pain 9 497 505 18387856 10.1016/j.jpain.2007.12.009 1:CAS:528:DC%2BD1cXmsFyqs7g%3D
53. M. Zhuo 2006 Molecular mechanisms of pain in the anterior cingulate cortex Journal of Neuroscience Research 84 927 933 16862566 10.1002/jnr.21003 1:CAS:528:DC%2BD28XhtV2htrjN (Pubitemid 44521036)
54. M. Zimmermann 1983 Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 109 110 6877845 10.1016/0304-3959(83)90201-4 1:STN:280:BiyB2s3lvFc%3D