IL-10 plays a pivotal role in anti-inflammatory effects of resveratrol in activated microglia cells

International Immunopharmacology

Volumn 24, Issue 2, 2015, Pages 369-376

  Cianciulli, Antonia ^a   Dragone, Teresa ^a   Calvello, Rosa ^a   Porro, Chiara ^b   Trotta, Teresa ^b   Lofrumento, Dario Domenico ^c   Panaro, Maria Antonietta ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF FOGGIA   (Italy)

^c UNIVERSITY OF SALENTO   (Italy)

Author keywords

IL 10; Inflammation; Microglia; Neurological diseases; Resveratrol

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE 1; JANUS KINASE 2; LIPOPOLYSACCHARIDE; MESSENGER RNA; RESVERATROL; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; CYTOKINE; JAK1 PROTEIN, MOUSE; SOCS3 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; STILBENE DERIVATIVE; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; MICROGLIA; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; CYTOKINES; JANUS KINASE 1; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; STILBENES; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84920733364     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2014.12.035     Document Type: Article

References (64)

1. C. Colton, and D.M. Wilcock Assessing activation states in microglia CNS Neurol Disord Drug Targets 9 2010 174 191
2. C.D. Mills M1 and M2 macrophages: oracles of health and disease Crit Rev Immunol 32 2012 463 488
3. S. Gordon, and P.R. Taylor Monocyte and macrophage heterogeneity Nat Rev Immunol 5 2005 953 964
4. X. Hu, R.K. Leak, Y. Shi, J. Suenaga, Y. Gao, and P. Zheng Microglial and macrophage polarization - new prospects for brain repair Nat Rev Neurol 11 2015 56 64
5. P.J. Murray, J.E. Allen, S.K. Biswas, E.A. Fisher, D.W. Gilroy, and S. Goerdt Macrophage activation and polarization: nomenclature and experimental guidelines Immunity 41 2014 14 20
6. J.D. Cherry, J.A. Olschowka, and M.K. O'Banion Neuroinflammation and M2 microglia: the good, the bad, and the inflamed J Neuroinflammation 11 2014 98
7. M.M. Varnum, and T. Ikezu The classification of microglial activation phenotypes on neurodegeneration and regeneration in Alzheimer's disease brain Arch Immunol Ther Exp (Warsz) 60 2012 251 266
8. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat Neurosci 10 2007 1387 1394
9. M.L. Block, and J.S. Hong Chronic microglial activation and progressive dopaminergic neurotoxicity Biochem Soc Trans 35 2007 1127 1132
10. C.K. Glass, K. Saijo, B. Winner, M.C. Marchetto, and F.H. Gage Mechanisms underlying inflammation in neurodegeneration Cell 140 2010 918 934
11. M.B. Graeber, and W.J. Streit Microglia: biology and pathology Acta Neuropathol 119 2010 89 105
12. M.A. Panaro, and A. Cianciulli Current opinions and perspectives on the role of immune system in the pathogenesis of Parkinson's disease Curr Pharm Des 18 2012 200 208
13. W. Kim, and S. De Vellis Microglia in health and disease J Neurosci Res 81 2005 302 313
14. F. Aloisi Immune function of microglia Glia 36 2001 165 179
15. D.K. Choi, S. Koppula, and K. Suk Inhibitors of microglial neurotoxicity: focus on natural products Molecules 16 2011 1021 1043
16. C. Cunningham, D.C. Wilcockson, S. Campion, K. Lunnon, and V.H. Perry Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration J Neurosci 25 2005 9275 9284
17. S. Lund, K.V. Christensen, M. Hedtjarn, A.L. Mortensen, H. Hagberg, and J. Falsig The dynamics of the LPS triggered inflammatory response of murine microglia under different culture and in vivo conditions J Neuroimmunol 180 2006 71 87
18. D.D. Lofrumento, G. Nicolardi, A. Cianciulli, F. De Nuccio, V. La Pesa, and V. Carofiglio Neuroprotective effects of resveratrol in an MPTP mouse model of Parkinson's-like disease: possible role of SOCS-1 in reducing pro-inflammatory responses Innate Immun 20 2014 249 260
19. F. Zhang, J. Liu, and J.S. Shi Anti-inflammatory activities of resveratrol in the brain: role of resveratrol in microglial activation Eur J Pharmacol 636 2010 1 7
20. K.T. Lu, R.Y. Chiou, L.G. Chen, M.H. Chen, W.T. Tseng, and H.T. Hsieh Neuroprotective effects of resveratrol on cerebral ischemia-induced neuron loss mediated by free radical scavenging and cerebral blood flow elevation J Agric Food Chem 54 2006 3126 3131
21. Q. Wang, J. Xu, G.E. Rottinghaus, A. Simonyi, D. Lubahn, and G.Y. Sun Resveratrol protects against global cerebral ischemic injury in gerbils Brain Res 958 2002 439 447
22. M. Mokni, S. Elkahoui, F. Limam, M. Amri, and E. Aouani Effect of resveratrol on antioxidant enzyme activities in the brain of healthy rat Neurochem Res 32 2007 981 987
23. M. Okawara, H. Katsuki, E. Kurimoto, H. Shibata, T. Kume, and A. Akaike Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults Biochem Pharmacol 73 2007 550 560
24. T.S. Anekonda Resveratrol - a boon for treating Alzheimer's disease? Brain Res Rev 52 2006 316 326
25. J. Chen, Y. Zhou, S. Mueller-Steiner, L.F. Chen, H. Kwon, and S. Yi SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling J Biol Chem 280 2005 40364 40374
26. J.A. Parker, M. Arango, S. Abderrahmane, E. Lambert, C. Tourette, and H. Catoire Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons Nat Genet 37 2005 349 350
27. A. Ledeboer, J.J.P. Breve', S. Poole, F.J.H. Tilders, and A.M. Van Dam Interleukin-10, interleukin-4, and transforming growth factor-b differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells Glia 30 2000 134 142
28. F. Molina-Holgado, R. Grencis, and N.J. Rothwell Actions of exogenous and endogenous IL-10 on glial responses to bacterial LPS/cytokines Glia 33 2001 97 106
29. A.M. Szczepanik, S. Funes, W. Petko, and G.E. Ringheim IL-4, IL-10 and IL-13 modulate Ab(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line J Neuroimmunol 113 2001 49 62
30. J. Mikita, N. Dubourdieu-Cassagno, M.S. Deloire, A. Vekris, M. Biran, and G. Raffard Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration Mult Scler 17 2011 2 15
31. M. Wu, J.C. Nissen, E.I. Chen, and S.E. Tsirka Tuftsin promotes an anti-inflammatory switch and attenuates symptoms in experimental autoimmune encephalomyelitis PLoS One 7 2012 e34933
32. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 2004 677 686
33. M.J. Carson, J. Crane, and A.X. Xie Modeling CNS microglia: the quest to identify predictive models Drug Discov Today Dis Models 5 2008 19 25
34. C.A. de la Lastra, and I. Villegas Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications Mol Nutr Food Res 49 2005 405 430
35. F. Bianchini, and H. Vainio Wine and resveratrol: mechanisms of cancer prevention? Eur J Cancer Prev 12 2003 417 425
36. M.A. Panaro, V. Carofiglio, A. Acquafredda, P. Cavallo, and A. Cianciulli Anti-inflammatory effects of resveratrol occur via inhibition of lipopolysaccharide-induced NF-κB activation in Caco-2 and SW480 human colon cancer cells Br J Nutr 108 2012 1623 1632
37. T. Dragone, A. Cianciulli, R. Calvello, C. Porro, T. Trotta, and M.A. Panaro Resveratrol counteracts lipopolysaccharide-mediated microglial inflammation by modulating a SOCS-1 dependent signaling pathway Toxicol In Vitro 28 2014 1126 1135
38. K.C. Park, S.Y. Kim, and D.S. Kim Experimental photodynamic therapy for liver cancer cell-implanted nude mice by an indole-3-acetic acid and intense pulsed light combination Biol Pharm Bull 32 2009 1609 1613
39. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
40. X. Gao, Y.X. Xu, N. Janakiraman, R.A. Chapman, and S.C. Gautam Immunomodulatory activity of resveratrol: suppression of lymphocyte proliferation, development of cell-mediated cytotoxicity, and cytokine production Biochem Pharmacol 62 2001 1299 1308
41. M. Zhong, G.F. Cheng, W.J. Wang, Y. Guo, X.Y. Zhu, and J.T. Zhang Inhibitory effect of resveratrol on interleukin 6 release by stimulated peritoneal macrophages of mice Phytomedicine 6 1999 79 84
42. S.V. Culpitt, D.F. Rogers, P.S. Fenwick, P. Shah, C. De Matos, and R.E. Russell Inhibition by red wine extract, resveratrol, of cytokine release by alveolar macrophages in COPD Thorax 58 2003 942 946
43. A. Foey, S. Parry, L. Williams, M. Feldmann, B. Foxwell, and F. Brennan Regulation of monocyte IL-10 synthesis by endogenous IL-1 and TNF-alpha: role of the p38 and p42/44 mitogen-activated protein kinases J Immunol 160 1998 920 928
44. S. Sánchez-Fidalgo, A. Cárdeno, I. Villegas, E. Talero, and C.A. de la Lastra Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice Eur J Pharmacol 633 2010 78 84
45. P. Orsu, B.V. Murthy, and A. Akula Cerebroprotective potential of resveratrol through anti-oxidant and anti-inflammatory mechanisms in rats J Neural Transm 120 2013 1217 1223
46. S. Bereswill, M. Muñoz, A. Fischer, R. Plickert, L.M. Haag, and B. Otto Anti-inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation PLoS One 5 2010 e15099
47. Malefyt R. de Waal, J. Abrams, B. Bennett, C.G. Figdor, and J.E. de Vries Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes J Exp Med 174 1991 1209 1220
48. D.F. Fiorentino, A. Zlotnik, T.R. Mosmann, M. Howard, and A. O'Garra IL-10 inhibits cytokine production by activated macrophages J Immunol 147 1991 3815 3822
49. J.F. Frøen, B.H. Munkeby, B. Stray-Pedersen, and O.D. Saugstad Interleukin-10 reverses acute detrimental effects of endotoxin-induced inflammation on perinatal cerebral hypoxia-ischemia Brain Res 942 2002 87 94
50. B. Mesples, F. Plaisant, and P. Gressens Effects of interleukin-10 on neonatal excitotoxic brain lesions in mice Brain Res Dev Brain Res 141 2003 25 32
51. F. Pousset, S. Cremona, R. Dantzer, K.W. Kelley, and P. Parnet IL-10 and IL-4 regulate type-I and type-II IL-1 receptors expression on IL-1 beta-activated mouse primary astrocytes J Neurochem 79 2001 726 736
52. Y.B. Lee, A. Nagai, and S.U. Kim Cytokines, chemokines, and cytokine receptors in human microglia J Neurosci Res 69 2002 94 103
53. D.A. Joyce, D.P. Gibbons, P. Green, J.H. Steer, M. Feldmann, and F.M. Brennan Two inhibitors of pro-inflammatory cytokine release, interleukin-10 and interleukin-4, have contrasting effects on release of soluble p75 tumor necrosis factor receptor by cultured monocytes Eur J Immunol 24 1994 2699 2705
54. D.A. Joyce, and J.H. Steer IL-4, IL-10 and IFN-gamma have distinct, but interacting, effects on differentiation-induced changes in TNF-alpha and TNF receptor release by cultured human monocytes Cytokine 8 1996 49 57
55. A.M. Lynch, C. Walsh, A. Delaney, Y. Nolan, V.A. Campbell, and M.A. Lynch Lipopolysaccharide-induced increase in signalling in hippocampus is abrogated by IL-10 - a role for IL-1 beta? J Neurochem 88 2004 635 646
56. M. Sawada, A. Suzumura, H. Hosoya, T. Marunouchi, and T. Nagatsu Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia J Neurochem 72 1999 1466 1471
57. K.W. Moore, M.R. de Waal, R.L. Coffman, and A. O'Garra Interleukin-10 and the interleukin-10 receptor Annu Rev Immunol 19 2001 683 765
58. K. Takeda, B.E. Clausen, and T. Kaisho Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils Immunity 10 1999 9 49
59. J.K. Riley, K. Takeda, S. Akira, and R.D. Schreiber Interleukin-10 receptor signaling through the JAK-STAT pathway. Requirement for two distinct receptor-derived signals for anti-inflammatory action J Biol Chem 274 1999 16513 16521
60. S.J. Rodig, M.A. Meraz, J.M. White, P.A. Lampe, J.K. Riley, and C.D. Arthur Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses Cell 93 1998 373 383
61. R. Lang, D. Patel, J.J. Morris, R.L. Rutschman, and P.J. Murray Shaping gene expression in activated and resting primary macrophages by IL-10 J Immunol 169 2002 2253 2263
62. L. Williams, L. Bradley, A. Smith, and B. Foxwell Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages J Immunol 172 2004 567 576
63. P.J. Murray The JAK-STAT signaling pathway: input and output integration J Immunol 178 2007 2623 2629
64. R. Starr, T.A. Willson, E.M. Viney, L.J.L. Murray, J.R. Rayner, and B.J. Jenkins A family of cytokine-inducible inhibitors of signalling Nature 387 1997 917 921