Trans-Resveratrol Attenuates High Fatty Acid-Induced P2X7 Receptor Expression and IL-6 Release in PC12 Cells: Possible Role of P38 MAPK Pathway

Inflammation

Volumn 38, Issue 1, 2015, Pages 327-337

  Xu, Hong ^a   Xiong, Chaopeng ^b   He, Luling ^a   Wu, Bing ^a   Peng, Lulu ^a   Cheng, Yajun ^a   Jiang, Fuqing ^a   Tan, Liping ^a   Tang, Lan ^a   Tu, Yunming ^b   Yang, Yuping ^b   Liu, Changle ^a   Gao, Yun ^a   Li, Guilin ^a   Zhang, Chunping ^a   Liu, Shuangmei ^a   Xu, Changshui ^a   Wu, Hong ^a   Li, Guodong ^a,c   Liang, Shangdong ^a,b  

^a JIANGXI MEDICAL COLLEGE   (China)

^b NANCHANG UNIVERSITY   (China)

^c SINGAPORE GENERAL HOSPITAL   (Singapore)

Author keywords

high fatty acids; IL 6; P2X7 receptor; P38; resveratrol

Indexed keywords

3' O (4 BENZOYLBENZOYL)ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; FATTY ACID; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PURINERGIC P2X7 RECEPTOR; RESVERATROL; THREONINE; PROTEIN BINDING; STILBENE DERIVATIVE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; HYDROGEN BOND; MOLECULAR DOCKING; NEUROPROTECTION; NONHUMAN; PC12 CELL LINE; PROTEIN EXPRESSION; RAT; SENSITIZATION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SECRETION (PROCESS);

ANIMALS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS, NONESTERIFIED; INTERLEUKIN-6; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PC12 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, PURINERGIC P2X7; STILBENES;

EID: 84925513391     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-014-0036-6     Document Type: Article

References (47)

1. Lelkes, E., B.R. Unsworth, and P.I. Lelkes. 2001. Reactive oxygen species, apoptosis and altered NGF-induced signaling in PC12 pheochromocytoma cells cultured in elevated glucose: an in vitro cellular model for diabetic neuropathy. Neurotox Res 3: 189–203.
2. Negi, G., A. Kumar, and S.S. Sharma. 2011. Nrf2 and NF-kappaB modulation by sulforaphane counteracts multiple manifestations of diabetic neuropathy in rats and high glucose-induced changes. Curr Neurovasc Res 8: 294–304.
3. Imrie, H., A. Abbas, and M. Kearney. 2010. Insulin resistance, lipotoxicity and endothelial dysfunction. Biochim Biophys Acta 1801: 320–326.
4. Savary, S., D. Trompier, P. Andreoletti, F. Le Borgne, J. Demarquoy, and G. Lizard. 2012. Fatty acids-induced lipotoxicity and inflammation. Curr Drug Metab 13: 1358–70.
5. Diakogiannaki, E., H.J. Welters, and N.G. Morgan. 2008. Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J Endocrinol 197: 553–563.
6. Sabin, M.A., C.E. Stewart, E.C. Crowne, S.J. Turner, L.P. Hunt, G.I. Welsh, M.J. Grohmann, J.M. Holly, and J.P. Shield. 2007. Fatty acid-induced defects in insulin signalling, in myotubes derived from children, are related to ceramide production from palmitate rather than the accumulation of intramyocellular lipid. J Cell Physiol 211: 244–252.
7. Unger, R. H. 1995. Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 44: 863–870
8. Boden, G., X. Chen, J. Ruiz, J.V. White, and L. Rossetti. 1994. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest 93: 2438–2446.
9. Smith, A.G., and J.R. Singleton. 2012. Diabetic neuropathy. Continuum (Minneap Minn) 18: 60–84.
10. Vincent, A.M., J.M. Hayes, L.L. McLean, A. Vivekanandan-Giri, S. Pennathur, and E.L. Feldman. 2009. Dyslipidemia-induced neuropathy in mice: the role of oxLDL/LOX-1. Diabetes 58: 2376–2385.
11. Xu, H., B. Wu, F. Jiang, S. Xiong, B. Zhang, G. Li, S. Liu, Y. Gao, C. Xu, G. Tu, H. Peng, S. Liang, and H. Xiong. 2013. High fatty acids modulate P2X(7) expression and IL-6 release via the p38 MAPK pathway in PC12 cells. Brain Res Bull 94: 63–70.
12. Loddick, S.A., A.V. Turnbull, and N.J. Rothwell. 1998. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 18: 176–179.
13. Klein, M.A., J.C. Moller, L.L. Jones, H. Bluethmann, G.W. Kreutzberg, and G. Raivich. 1997. Impaired neuroglial activation in interleukin-6 deficient mice. Glia 19: 227–233.
14. Nakamachi, T., M. Tsuchida, N. Kagami, S. Yofu, Y. Wada, M. Hori, D. Tsuchikawa, A. Yoshikawa, N. Imai, K. Nakamura, S. Arata, and S. Shioda. 2012. IL-6 and PACAP receptor expression and localization after global brain ischemia in mice. J Mol Neurosci 48: 518–525.
15. Murphy, P.G., J. Grondin, M. Altares, and P.M. Richardson. 1995. Induction of interleukin-6 in axotomized sensory neurons. J Neurosci 15: 5130–5138.
16. Song, D.K., Y.B. Im, J.S. Jung, H.W. Suh, S.O. Huh, J.H. Song, and Y.H. Kim. 1999. Central injection of nicotine increases hepatic and splenic interleukin 6 (IL-6) mRNA expression and plasma IL-6 levels in mice: involvement of the peripheral sympathetic nervous system. FASEB J 13: 1259–1267.
17. Orellana, D.I., R.A. Quintanilla, C. Gonzalez-Billault, and R.B. Maccioni. 2005. Role of the JAKs/STATs pathway in the intracellular calcium changes induced by interleukin-6 in hippocampal neurons. Neurotox Res 8: 295–304.
18. Campbell, I.L., C.R. Abraham, E. Masliah, P. Kemper, J.D. Inglis, M.B. Oldstone, and L. Mucke. 1993. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A 90: 10061–10065.
19. Nelson, T.E., E.A. Olde, R. Hernandez, A. Puro, S. Huitron-Resendiz, C. Hao, P.N. De Graan, and D.L. Gruol. 2012. Altered synaptic transmission in the hippocampus of transgenic mice with enhanced central nervous systems expression of interleukin-6. Brain Behav Immun 26: 959–971.
20. Zhu, J., X.F. Bai, E. Mix, and H. Link. 1997. Cytokine dichotomy in peripheral nervous system influences the outcome of experimental allergic neuritis: dynamics of mRNA expression for IL-1 beta, IL-6, IL-10, IL-12, TNF-alpha, TNF-beta, and cytolysin. Clin Immunol Immunopathol 84: 85–94.
21. Sugiyama, T. 2014. Role of P2X7 receptors in the development of diabetic retinopathy. World J Diabetes 5: 141–145.
22. Alves, L.A., R.J. Bezerra, R.X. Faria, L.G. Ferreira, and S.F.V. Da. 2013. Physiological roles and potential therapeutic applications of the P2X7 receptor in inflammation and pain. Molecules 18: 10953–10972.
23. Lister, M.F., J. Sharkey, D.A. Sawatzky, J.P. Hodgkiss, D.J. Davidson, A.G. Rossi, and K. Finlayson. 2007. The role of the purinergic P2X7 receptor in inflammation. J Inflamm (Lond) 4: 5.
24. Di Virgilio, F., D. Ferrari, and E. Adinolfi. 2009. P2X(7): a growth-promoting receptor—implications for cancer. Purinergic Signal 5: 251–256.
25. Adinolfi, E., M.G. Callegari, D. Ferrari, C. Bolognesi, M. Minelli, M.R. Wieckowski, P. Pinton, R. Rizzuto, and F. Di Virgilio. 2005. Basal activation of the P2X7 ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth. Mol Biol Cell 16: 3260–3272.
26. Volonte, C., S. Apolloni, S.D. Skaper, and G. Burnstock. 2012. P2X7 receptors: channels, pores and more. CNS Neurol Disord Drug Targets 11: 705–721.
27. Solini, A., P. Chiozzi, A. Morelli, E. Adinolfi, R. Rizzo, O.R. Baricordi, and F. Di Virgilio. 2004. Enhanced P2X7 activity in human fibroblasts from diabetic patients: a possible pathogenetic mechanism for vascular damage in diabetes. Arterioscler Thromb Vasc Biol 24: 1240–1245.
28. Solini, A., P. Chiozzi, S. Falzoni, A. Morelli, R. Fellin, and F. Di Virgilio. 2000. High glucose modulates P2X7 receptor-mediated function in human primary fibroblasts. Diabetologia 43: 1248–1256.
29. Vonend, O., C.M. Turner, C.M. Chan, A. Loesch, G.C. Dell’Anna, K.S. Srai, G. Burnstock, and R.J. Unwin. 2004. Glomerular expression of the ATP-sensitive P2X receptor in diabetic and hypertensive rat models. Kidney Int 66: 157–166.
30. Zhang, F., H. Wang, Q. Wu, Y. Lu, J. Nie, X. Xie, and J. Shi. 2013. Resveratrol protects cortical neurons against microglia-mediated neuroinflammation. Phytother Res 27(3): 344–349.
31. Sun, A.Y., Q. Wang, A. Simonyi, and G.Y. Sun. 2010. Resveratrol as a therapeutic agent for neurodegenerative diseases. Mol Neurobiol 41: 375–383.
32. Orsu, P., B.V. Murthy, and A. Akula. 2013. Cerebroprotective potential of resveratrol through anti-oxidant and anti-inflammatory mechanisms in rats. J Neural Transm 120: 1217–23.
33. Li, F., Q. Gong, H. Dong, and J. Shi. 2012. Resveratrol, a neuroprotective supplement for Alzheimer’s disease. Curr Pharm Des 18: 27–33.
34. Frozza, R.L., Bernardi, A., Hoppe, J.B., Meneghetti, A.B., Battastini, A.M., Pohlmann, A.R., Guterres, S.S., and Salbego, C. 2013. Lipid-core nanocapsules improve the effects of resveratrol against Abeta-induced neuroinflammation. J Biomed Nanotechnol 9: 2086–2104.
35. Hirose, H., Y.H. Lee, L.R. Inman, Y. Nagasawa, J.H. Johnson, and R.H. Unger. 1996. Defective fatty acid-mediated beta-cell compensation in Zucker diabetic fatty rats. Pathogenic implications for obesity-dependent diabetes. J Biol Chem 271: 5633–5637.
36. Tang, Y., and G.D. Li. 2004. Chronic exposure to high glucose impairs bradykinin-stimulated nitric oxide production by interfering with the phospholipase-C-implicated signalling pathway in endothelial cells: evidence for the involvement of protein kinase C. Diabetologia 47: 2093–2104.
37. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408.
38. Naim, M., S. Bhat, K.N. Rankin, S. Dennis, S.F. Chowdhury, I. Siddiqi, P. Drabik, T. Sulea, C.I. Bayly, A. Jakalian, and E.O. Purisima. 2007. Solvated interaction energy (SIE) for scoring protein-ligand binding affinities. 1. Exploring the parameter space. J Chem Inf Model 47: 122–133.
39. Chang, L., and M. Karin. 2001. Mammalian MAP kinase signalling cascades. Nature 410: 37–40.
40. Siddiqui, M.A., Kashyap, M.P., Kumar, V., Al-Khedhairy, A.A., Musarrat, J., and Pant, A.B. 2010. Protective potential of trans-resveratrol against 4-hydroxynonenal induced damage in PC12 cells. Toxicol In Vitro 24: 1592–1598.
41. North, R.A. 2002. Molecular physiology of P2X receptors. Physiol Rev 82(4): 1013–1067.
42. Zhou, H., Q. Chen, D.L. Kong, J. Guo, Q. Wang, and S.Y. Yu. 2011. Effect of resveratrol on gliotransmitter levels and p38 activities in cultured astrocytes. Neurochem Res 36: 17–26.
43. Han, Y., Jiang, C., Tang, J., Wang, C., Wu, P., Zhang, G., Liu, W., Jamangulova, N., Wu, X., and Song, X. 2014. Resveratrol reduces morphine tolerance by inhibiting microglial activation via AMPK signalling. Eur J Pain [Epub ahead of print]
44. Armstrong, J.N., T.B. Brust, R.G. Lewis, and B.A. MacVicar. 2002. Activation of presynaptic P2X7-like receptors depresses mossy fiber-CA3 synaptic transmission through p38 mitogen-activated protein kinase. J Neurosci 22: 5938–5945.
45. Friedle, S.A., V.M. Brautigam, M. Nikodemova, M.L. Wright, and J.J. Watters. 2011. The P2X7-Egr pathway regulates nucleotide-dependent inflammatory gene expression in microglia. Glia 59: 1–13.
46. Oliver, M.F., and L.H. Opie. 1994. Effects of glucose and fatty acids on myocardial ischaemia and arrhythmias. Lancet 343: 155–158.
47. Ando, R.D., and B. Sperlagh. 2013. The role of glutamate release mediated by extrasynaptic P2X7 receptors in animal models of neuropathic pain. Brain Res Bull 93: 80–85.