Resveratrol suppresses calcium-mediated microglial activation and rescues hippocampal neurons of adult rats following acute bacterial meningitis

Comparative Immunology, Microbiology and Infectious Diseases

Volumn 36, Issue 2, 2013, Pages 137-148

  Sheu, Ji Nan ^a   Liao, Wen Chieh ^a   Wu, Un In ^b   Shyu, Ling Yuh ^a   Mai, Fu Der ^c   Chen, Li You ^a   Chen, Mei Jung ^d   Youn, Su Chung ^a   Chang, Hung Ming ^c  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d MING CHUAN UNIVERSITY   (Taiwan)

Author keywords

Klebsiella pneumoniae; Microglia; Oxidative stress; Pro inflammatory cytokines; Resveratrol; TOF SIMS

Indexed keywords

ADAPTOR PROTEIN; CALCIUM; INTERLEUKIN 1BETA; INTERLEUKIN 6; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; ISOLECTIN B4; MALONALDEHYDE; NITRIC OXIDE SYNTHASE; RESVERATROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; BRAIN NERVE CELL; CALCIUM SIGNALING; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; QUANTITATIVE ANALYSIS; RAT; TIME OF FLIGHT MASS SPECTROMETRY;

ANIMALS; CALCIUM; CEREBROSPINAL FLUID; CYTOKINES; HIPPOCAMPUS; INFLAMMATION MEDIATORS; MALE; MENINGITIS, BACTERIAL; MICROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; RATS; STILBENES;

BACTERIA (MICROORGANISMS); GRIFFONIA SIMPLICIFOLIA; KLEBSIELLA PNEUMONIAE; RATTUS;

EID: 84875250287     PISSN: 01479571     EISSN: 18781667     Source Type: Journal    
DOI: 10.1016/j.cimid.2012.11.002     Document Type: Article

References (53)

1. Kim K.S. Acute bacterial meningitis in infants and children. Lancet Infectious Diseases 2010, 10:32-42.
2. Khwannimit B., Chayakul P., Geater A. Acute bacterial meningitis in adults: a 20 year review. Southeast Asian Journal of Tropical Medicine and Public Health 2004, 35:886-892.
3. Brouwer M.C., Tunkel A.R., van de Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clinical Microbiology Reviews 2010, 23:467-492.
4. Singhi P., Bansal A., Geeta P., Singhi S. Predictors of long term neurological outcome in bacterial meningitis. Indian Journal of Pediatrics 2007, 74:369-374.
5. Tunkel A.R., Scheld W.M. Pathogenesis and pathophysiology of bacterial meningitis. Clinical Microbiology Reviews 1993, 6:118-136.
6. Pfister H.W., Scheld W.M. Brain injury in bacterial meningitis. Current Opinion in Neurology 1997, 10:254-259.
7. Scheld W.M., Koedel U., Nathan B., Pfister H.W. Pathophysiology of bacterial meningitis: mechanisms of neuronal injury. Journal of Infectious Diseases 2002, 186:S225-S233.
8. Nau R., Brück W. Neuronal injury in bacterial meningitis: mechanisms and implications for therapy. Trends in Neurosciences 2002, 25:38-45.
9. Barichello T., Lemos J.C., Generoso J.S., Cipriano A.L., Milioli G.L., Marcelino D.M., et al. Oxidative stress, cytokine/chemokine and disruption of blood-brain barrier in neonate rats after meningitis by Streptococcus agalactiae. Neurochemical Research 2011, 36:1922-1930.
10. Färber K., Kettenmann H. Functional role of calcium signals for microglial function. Glia 2006, 54:656-665.
11. Hoffmann A., Kann O., Ohlemeyer C., Hanisch U.K., Kettenmann H. Elevation of basal intracellular calcium as central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. Journal of Neuroscience 2003, 23:4410-4419.
12. Das S., Das D.K. Anti-inflammatory responses of resveratrol. Inflammation & Allergy - Drug Targets 2007, 6:168-173.
13. de la Lastra C.A., Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochemical Society Transactions 2007, 35:1156-1160.
14. Juhasz B., Varga B., Gesztelyi R., Kemeny-Beke A., Zsuga J., Tosaki A. Resveratrol: a multifunctional cytoprotective molecule. Current Pharmaceutical Biotechnology 2010, 11:810-818.
15. Shukla Y., Singh R. Resveratrol and cellular mechanisms of cancer prevention. Annals of the New York Academy of Sciences 2011, 1215:1-8.
16. Zhang F., Liu J., Shi J.S. Anti-inflammatory activities of resveratrol in the bra role of resveratrol in microglial activation. European Journal of Pharmacology 2010, 636:1-7.
17. Meng X.L., Yang J.Y., Chen G.L., Wang L.H., Zhang L.J., Wang S., et al. Effects of resveratrol and its derivatives on lipopolysaccharide-induced microglial activation and their structure-activity relationships. Chemico-Biological Interactions 2008, 174:51-59.
18. Lu X., Ma L., Ruan L., Kong Y., Mou H., Zhang Z., et al. Resveratrol differentially modulates inflammatory responses of microglia and astrocytes. Journal of Neuroinflammation 2010, 7(46.). (article ID).
19. Zhang F., Shi J.S., Zhou H., Wilson B., Hong J.S., Gao H.M. Resveratrol protects dopamine neurons against lipopolysaccharide-induced neurotoxicity through its anti-inflammatory actions. Molecular Pharmacology 2010, 78:466-477.
20. Wang Q., Xu J., Rottinghaus G.E., Simonyi A., Lubahn D., Sun G.Y., et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Research 2002, 958:439-447.
21. Bi X.L., Yang J.Y., Dong Y.X., Wang J.M., Cui Y.H., Ikeshima T., et al. Resveratrol inhibits nitric oxide and TNF-α production by lipopolysaccharide-activated microglia. International Immunopharmacology 2005, 5:185-193.
22. Bureau G., Longpré F., Martinoli M.G. Resveratrol and quercetin, two natural polyphenols, reduce apoptotic neuronal cell death induced by neuroinflammation. Journal of Neuroscience Research 2008, 86:403-410.
23. Patel K.R., Scott E., Brown V.A., Gescher A.J., Steward W.P., Brown K. Clinical trials of resveratrol. Annals of the New York Academy of Sciences 2011, 1215:161-169.
24. Bifrare Y.D., Gianinazzi C., Imboden H., Leib S.L., Täuber M.G. Bacterial meningitis causes two distinct forms of cellular damage in the hippocampal dentate gyrus in infant rats. Hippocampus 2003, 13:481-488.
25. Hofer S., Grandgirard D., Burri D., Fröhlich T.K., Leib S.L. Bacterial meningitis impairs hippocampal neurogenesis. Journal of Neuropathology and Experimental Neurology 2011, 70:890-899.
26. Wu C.H., Shieh J.Y., Wen C.Y., Ling E.A. Use of lectin as a tool for the study of microglial cells: expression and regulation of lectin receptors in normal development and under experimental conditions. Topical issues of microglia research 1996, 83-104. Singapore Neuroscience Association, Singapore. E.A. Ling, C.K. Tan, C.B.C. Tan (Eds.).
27. Ito D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Research: Molecular Brain Research 1998, 57:1-9.
28. Wen L.L., Chiu C.T., Huang Y.N., Chang C.F., Wang J.Y. Rapid glia expression and release of pro-inflammatory cytokines in experimental Klebsiella pneumoniae meningoencephalitis. Experimental Neurology 2007, 205:270-278.
29. Chang H.M., Mai F.D., Chen B.J., Wu U.I., Huang Y.L., Lan C.T., et al. Sleep deprivation predisposes liver to oxidative stress and phospholipid damage: a quantitative molecular imaging study. Journal of Anatomy 2008, 212:295-305.
30. Chang H.M., Mai F.D., Lei S.L., Ling Y.C. Impaired sodium levels in the suprachiasmatic nucleus are associated with the formation of cardiovascular efficiency in sleep-deprived rats. Journal of Anatomy 2010, 217:694-704.
31. Hulse R.E., Kunkler P.E., Fedynyshyn J.P., Kraig R.P. Optimization of multiplexed bead-based cytokine immunoassays for rat serum and brain tissue. Journal of Neuroscience Methods 2004, 136:87-98.
32. 2+-independent NOS activity. Journal of Neuroscience Methods 2004, 138:73-79.
33. Gluck M.R., Moy L.Y., Jayatilleke E., Hogan K.A., Manzino L., Sonsalla P.K. Parallel increases in lipid and protein oxidative markers in several mouse brain regions after methamphetamine treatment. Journal of Neurochemistry 2001, 79:152-160.
34. Silva R.H., Abilio V.C., Takatsu A.L., Kameda S.R., Grassl C., Chehin A.B., et al. Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 2004, 46:895-903.
35. Chang H.M., Ling E.A., Chen C.F., Lue J.H., Wen C.Y., Shieh J.Y. Melatonin attenuates the neuronal NADPH-d/NOS expression in the nodose ganglion of acute hypoxic rats. Journal of Pineal Research 2002, 32:65-73.
36. Lu C.H., Chang W.N., Chang H.W. Klebsiella meningitis in adults: clinical features, prognostic factors and therapeutic outcomes. Journal of Clinical Neuroscience 2002, 9:533-538.
37. Buster B.L., Weintrob A.C., Townsend G.C., Scheld W.M. Potential role of nitric oxide in the pathophysiology of experimental bacterial meningitis in rats. Infection and Immunity 1995, 63:3835-3839.
38. Dinarello C.A. Pro-inflammatory cytokines. Chest 2000, 118:503-508.
39. Barone F.C., Parsons A.A. Therapeutic potential of anti-inflammatory drugs in focal stroke. Expert Opinion on Investigational Drugs 2000, 9:2281-2306.
40. Lloyd E., Somera-Molina K., van Eldik L.J., Watterson D.M., Wainwright MS Suppression of acute pro-inflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. Journal of Neuroinflammation 2008, 5:28. (article ID).
41. McCarty M.F. Down-regulation of microglial activation may represent a practical strategy for combating neurodegenerative disorders. Medical Hypotheses 2006, 67:251-269.
42. Li Y., Hu X., Liu Y., Bao Y., An L. Nimodipine protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. Neuropharmacology 2009, 56:580-589.
43. Leonard S.S., Xia C., Jiang B.H., Stinefelt B., Klandorf H., Harris G.K., et al. Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochemical and Biophysical Research Communications 2003, 309:1017-1026.
44. Holthoff J.H., Woodling K.A., Doerge D.R., Burns S.T., Hinson J.A., Mayeux P.R. Resveratrol a dietary polyphenolic phytoalexin, is a functional scavenger of peroxynitrite. Biochemical Pharmacology 2010, 80:1260-1265.
45. Fulda S., Debatin K.M. Resveratrol modulation of signal transduction in apoptosis and cell survival: a mini-review. Cancer Detection and Prevention 2006, 30:217-223.
46. Wang L., Ma Q., Chen X., Sha H., Ma Z. Effects of resveratrol on calcium regulation in rats with severe acute pancreatitis. European Journal of Pharmacology 2008, 580:271-276.
47. 2+ mobilization in rats in vivo and in vitro. Endocrinology 2011, 152:2090-2099.
48. Tsuda Y., Nakahara T., Mori A., Sakamoto K., Ishii K. Resveratrol prevents bradykinin-induced contraction of rat urinary bladders by decreasing prostaglandin production and calcium influx. European Journal of Pharmacology 2011, 666:189-195.
49. Ye Y., Huang X., Zhang Y., Lai X., Wu X., Zeng X., et al. Calcium influx blocked by SK&F 96365 modulates the LPS plus IFN-γ-induced inflammatory response in murine peritoneal macrophages. International Immunopharmacology 2012, 12:384-393.
50. Williams L.D., Burdock G.A., Edwards J.A., Beck M., Bausch J. Safety studies conducted on high-purity trans-resveratrol in experimental animals. Food and Chemical Toxicology 2009, 49:2170-2221.
51. la Porte C., Voduc N., Zhang G., Seguin I., Tardiff D., Singhal N., et al. Steady-state pharmacokinetics and tolerability of trans-resveratrol 2000mg trice daily with food, quercetin and alcohol (ethanol) in healthy human subjects. Clinical Pharmacokinetics 2010, 49:449-454.
52. Larrosa M., Azorín-Ortuño M., Yañez-Gascón M.J., García-Conesa M.T., Tomás-Barberán F., Espín J.C. Lack of effect of oral administration of resveratrol in LPS-induced systemic inflammation. European Journal of Nutrition 2011, 50:673-680.
53. Wu U.I., Mai F.D., Sheu J.N., Chen L.Y., Liu Y.T., Huang H.C., et al. Melatonin inhibits microglial activation, reduces pro-inflammatory cytokine levels, and rescues hippocampal neurons of adult rats with acute Klebsiella pneumoniae meningitis. Journal of Pineal Research 2011, 50:159-170.