Involvement of protein kinase ζ in the maintenance of hippocampal long-term potentiation in rats with chronic visceral hypersensitivity

Journal of Neurophysiology

Volumn 113, Issue 9, 2015, Pages 3047-3055

  Chen, Aiqin ^a   Bao, Chengjia ^a   Tang, Ying ^a   Luo, Xiaoqing ^a   Guo, Lixia ^a   Liu, Bin ^a   Lin, Chun ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Chronic visceral pain; Hippocampus; Long term potentiation; Neonatal maternal separation; Protein kinase M

Indexed keywords

PROTEIN KINASE; PROTEIN KINASE M DELTA; UNCLASSIFIED DRUG; LIPOPEPTIDE; MYRISTOYLATED ZETA-PSEUDOSUBSTRATE INHIBITORY PEPTIDE; PROTEIN KINASE C; PROTEIN KINASE C ZETA;

ABDOMINAL WALL MUSCULATURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAM; HIPPOCAMPUS; LEARNING; LOCOMOTION; LONG TERM POTENTIATION; MALE; MATERNAL DEPRIVATION; MORRIS WATER MAZE TEST; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VISCERAL PAIN; WESTERN BLOTTING; ANALYSIS OF VARIANCE; ANIMAL; COLON; DISEASE MODEL; DRUG EFFECTS; ELECTROMYOGRAPHY; ELECTROSTIMULATION; ENZYMOLOGY; EXPLORATORY BEHAVIOR; IN VITRO STUDY; MAZE TEST; METABOLISM; NEWBORN; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; COLON; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; IN VITRO TECHNIQUES; LIPOPEPTIDES; LONG-TERM POTENTIATION; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; VISCERAL PAIN;

EID: 84930842196     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00929.2014     Document Type: Article

References (47)

1. Bird CM, Burgess N. The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9: 182–194, 2008.
2. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39, 1993.
3. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol 6: 71–80, 2014.
4. Chen Y, Chen AQ, Luo XQ, Guo LX, Tang Y, Bao CJ, Lin L, Lin C. Hippocampal NR2B-containing NMDA receptors enhance long-term potentiation in rats with chronic visceral pain. Brain Res 1570: 43–53, 2014.
5. Chen Y, Yuanxiang P, Knopfel T, Thomas U, Behnisch T. Hippocampal LTP triggers proteasome-mediated SPAR degradation in CA1 neurons. Synapse 66: 142–150, 2012.
6. Choi DS, Choi DY, Whittington RA, Nedeljkovic SS. Sudden amnesia resulting in pain relief: the relationship between memory and pain. Pain 132: 206–210, 2007.
7. Coutinho SV, Plotsky PM, Sablad M, Miller JC, Zhou H, Bayati AI, McRoberts JA, Mayer EA. Neonatal maternal separation alters stressinduced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282: G307–G316, 2002.
8. Gerlai R. Hippocampal LTP and memory in mouse strains: is there evidence for a causal relationship? Hippocampus 12: 657–666, 2002.
9. Hu S, Xu W, Miao X, Gao Y, Zhu L, Zhou Y, Xiao Y, Xu GY. Sensitization of sodium channels by cystathionine beta-synthetase activation in colon sensory neurons in adult rats with neonatal maternal deprivation. Exp Neurol 248: 275–285, 2013.
10. Jaffard R, Meunier M. Role of the hippocampal formation in learning and memory. Hippocampus 3 Spec No: 203–217, 1993.
11. Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26: 696–705, 2003.
12. Kannampalli P, Pochiraju S, Chichlowski M, Berg BM, Rudolph C, Bruckert M, Miranda A, Sengupta JN. Probiotic Lactobacillus rhamnosus GG (LGG) and prebiotic prevent neonatal inflammation-induced visceral hypersensitivity in adult rats. Neurogastroenterol Motil 26: 1694– 1704, 2014.
13. King T, Qu C, Okun A, Melemedjian OK, Mandell EK, Maskaykina IY, Navratilova E, Dussor GO, Ghosh S, Price TJ, Porreca F. Contribution of PKMzeta-dependent and independent amplification to components of experimental neuropathic pain. Pain 153: 1263–1273, 2012.
14. Li XY, Ko HG, Chen T, Collingridge GL, Kaang BK, Zhuo M. Erasing injury-related cortical synaptic potentiation as a new treatment for chronic pain. J Mol Med 89: 847–855, 2011.
15. 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. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 330: 1400–1404, 2010.
16. Ling DS, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, Sacktor TC. Protein kinase Mzeta is necessary and sufficient for LTP maintenance. Nat Neurosci 5: 295–296, 2002.
17. Liu MG, Chen J. Roles of the hippocampal formation in pain information processing. Neurosci Bull 25: 237–266, 2009.
18. Liu MG, Lu D, Wang Y, Chen XF, Li Z, Xu Y, Jin JH, Wang RR, Chen J. Counteracting roles of metabotropic glutamate receptor subtypes 1 and 5 in regulation of pain-related spatial and temporal synaptic plasticity in rat entorhinal-hippocampal pathways. Neurosci Lett 507: 38–42, 2012.
19. Liu MG, Wang RR, Chen XF, Zhang FK, Cui XY, Chen J. Differential roles of ERK, JNK and p38 MAPK in pain-related spatial and temporal enhancement of synaptic responses in the hippocampal formation of rats: multi-electrode array recordings. Brain Res 1382: 57–69, 2011.
20. Luo XQ, Cai QY, Chen Y, Guo LX, Chen AQ, Wu ZQ, Lin C. Tyrosine phosphorylation of the NR2B subunit of the NMDA receptor in the spinal cord contributes to chronic visceral pain in rats. Brain Res 1542: 167–175, 2014.
21. Lyu D, Yu W, Tang N, Wang R, Zhao Z, Xie F, He Y, Du H, Chen J. The mTOR signaling pathway regulates pain-related synaptic plasticity in rat entorhinal-hippocampal pathways. Mol Pain 9: 64, 2013.
22. Madronal N, Gruart A, Sacktor TC, Delgado-Garcia JM. PKMzeta inhibition reverses learning-induced increases in hippocampal synaptic strength and memory during trace eyeblink conditioning. PLoS One 5: e10400, 2010.
23. Marchand F, D’Mello R, Yip PK, Calvo M, Muller E, Pezet S, Dickenson AH, McMahon SB. Specific involvement of atypical PKCzeta/PKMzeta in spinal persistent nociceptive processing following peripheral inflammation in rat. Mol Pain 7: 86, 2011.
24. Mayer EA, Naliboff BD, Chang L, Coutinho SV. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 280: G519–G524, 2001.
25. Noel M, Chambers CT, McGrath PJ, Klein RM, Stewart SH. The influence of children’s pain memories on subsequent pain experience. Pain 153: 1563–1572, 2012.
26. Ohnami S, Kato A, Ogawa K, Shinohara S, Ono H, Tanabe M. Effects of milnacipran, a 5-HT and noradrenaline reuptake inhibitor, on C-fibreevoked field potentials in spinal long-term potentiation and neuropathic pain. Br J Pharmacol 167: 537–547, 2012.
27. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC. Storage of spatial information by the maintenance mechanism of LTP. Science 313: 1141–1144, 2006.
28. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (4th ed.). San Diego, CA: Academic, 1998.
29. Price DD, Zhou Q, Moshiree B, Robinson ME, Verne GN. Peripheral and central contributions to hyperalgesia in irritable bowel syndrome. J Pain 7: 529–535, 2006.
30. Ren SQ, Yan JZ, Zhang XY, Bu YF, Pan WW, Yao W, Tian T, Lu W. PKClambda is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP. EMBO J 32: 1365–1380, 2013.
31. Ren TH, Wu J, Yew D, Ziea E, Lao L, Leung WK, Berman B, Hu PJ, Sung JJ. Effects of neonatal maternal separation on neurochemical and sensory response to colonic distension in a rat model of irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 292: G849–G856, 2007.
32. Rutten JM, Benninga MA, Vlieger AM. IBS and FAPS in children: a comparison of psychological and clinical characteristics. J Pediatr Gastroenterol Nutr 59: 493–499, 2014.
33. Saab CY, Wang J, Gu C, Garner KN, Al-Chaer ED. Microglia: a newly discovered role in visceral hypersensitivity? Neuron Glia Biol 2: 271–277, 2006.
34. Sacktor TC. Memory maintenance by PKMzeta—an evolutionary perspective. Mol Brain 5: 31, 2012.
35. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E. Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci USA 90: 8342–8346, 1993.
36. Sanchez CA. Working through the pain: working memory capacity and differences in processing and storage under pain. Memory 19: 226–232, 2011.
37. Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, Alberini C, Kelley AE, Maren S, Rudy JW, Yin JC, Sacktor TC, Fenton AA. PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6: 2698–2706, 2008.
38. Serrano P, Yao Y, Sacktor TC. Persistent phosphorylation by protein kinase Mzeta maintains late-phase long-term potentiation. J Neurosci 25: 1979–1984, 2005.
39. Shema R, Hazvi S, Sacktor TC, Dudai Y. Boundary conditions for the maintenance of memory by PKMzeta in neocortex. Learn Mem 16: 122–128, 2009.
40. Song C, Detert JA, Sehgal M, Moyer JR. Trace fear conditioning enhances synaptic and intrinsic plasticity in rat hippocampus. J Neurophysiol 107: 3397–3408, 2012.
41. Sousa VC, Vital J, Costenla AR, Batalha VL, Sebastiao AM, Ribeiro JA, Lopes LV. Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats. Neurobiol Aging 35: 1680–1685, 2014.
42. Volk LJ, Bachman JL, Johnson R, Yu Y, Huganir RL. PKM-zeta is not required for hippocampal synaptic plasticity, learning and memory. Nature 493: 420–423, 2013.
43. Wei F, Xu ZC, Qu Z, Milbrandt J, Zhuo M. Role of EGR1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation. J Cell Biol 149: 1325–1334, 2000.
44. Yang HW, Hu XD, Zhang HM, Xin WJ, Li MT, Zhang T, Zhou LJ, Liu XG. Roles of CaMKII, PKA, and PKC in the induction and maintenance of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. J Neurophysiol 91: 1122–1133, 2004.
45. Yang JM, Xian YF, Ip PS, Wu JC, Lao L, Fong HH, Sung JJ, Berman B, Yeung JH, Che CT. Schisandra chinensis reverses visceral hypersensitivity in a neonatal-maternal separated rat model. Phytomedicine 19: 402–408, 2012.
46. Yi M, Zhang H. Nociceptive memory in the brain: cortical mechanisms of chronic pain. J Neurosci 31: 13343–13345, 2011.
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109–110, 1983.