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

Volumn 50, Issue 2, 2011, Pages 159-170

  Wu, Un In ^a   Mai, Fu Der ^b   Sheu, Ji Nan ^c   Chen, Li You ^d   Liu, Yu Ting ^d   Huang, Hai Cheng ^d   Chang, Hung Ming ^c,d  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

apoptosis; bacterial meningitis; interleukins; melatonin; microglia; quantitative molecular imaging analysis; tumor necrosis factor

Indexed keywords

CYTOCHROME C OXIDASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOLECTIN B4; MELATONIN; TUMOR NECROSIS FACTOR ALPHA;

ACUTE KLEBSIELLA PNEUMONIAE MENINGITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BACTERIAL MENINGITIS; BRAIN CELL; CELL ACTIVATION; CEREBROSPINAL FLUID; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOKINE RELEASE; HIPPOCAMPUS; HISTOCHEMISTRY; IMMUNOMODULATION; INOCULATION; KLEBSIELLA PNEUMONIAE INFECTION; MALE; MICROGLIA; NICK END LABELING; NONHUMAN; RAT; SURVIVAL; TIME OF FLIGHT MASS SPECTROMETRY;

ANIMALS; CYTOKINES; HIPPOCAMPUS; IN SITU NICK-END LABELING; KLEBSIELLA PNEUMONIAE; MALE; MASS SPECTROMETRY; MELATONIN; MENINGITIS; MICROGLIA; NEURONS; RATS; RATS, WISTAR;

EID: 79951662424     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2010.00825.x     Document Type: Article

References (81)

1. Lu CH, Chang WN, Chang HW,. Klebsiella meningitis in adults: clinical features, prognostic factors and therapeutic outcomes. J Clin Neurosci 2002; 9: 533-538.
2. Ko WC, Paterson DL, Sagnimeni AJ, et al. Community-acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg Infect Dis 2002; 8: 160-166. (Pubitemid 34202438)
3. Tang LM, Chen ST, Hsu WC, et al. Acute bacterial meningitis in adults: a hospital-based epidemiological study. QJM 1999; 92: 719-725.
4. Fang CT, Chen YC, Chang SC, et al. Klebsiella pneumoniae meningitis: timing of antimicrobial therapy and prognosis. QJM 2000; 93: 45-53.
5. Tunkel AR, Scheld WM,. Pathogenesis and pathophysiology of bacterial meningitis. Clin Microbiol Rev 1993; 6: 118-136.
6. Pfister HW, Scheld WM,. Brain injury in bacterial meningitis. Curr Opin Neurol 1997; 10: 254-259.
7. Nau R, Brück W,. Neuronal injury in bacterial meningitis: mechanisms and implications for therapy. Trends Neurosci 2002; 25: 38-45. (Pubitemid 34093784)
8. Scheld WM, Koedel U, Nathan B, et al. Pathophysiology of bacterial meningitis: mechanisms of neuronal injury. J Infect Dis 2002; 186 (Suppl. 2): S225-S233. (Pubitemid 35370486)
9. Wen LL, Chiu CT, Huang YN, et al. Rapid glia expression and release of pro-inflammatory cytokines in experimental Klebsiella pneumoniae meningoencephalitis. Exp Neurol 2007; 205: 270-278.
10. Färber K, Kettenmann H,. Functional role of calcium signals for microglial function. Glia 2006; 54: 656-665. (Pubitemid 44629629)
11. Hoffmann A, Kann O, Ohlemeyer C, et al. 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. J Neurosci 2003; 23: 4410-4419. (Pubitemid 36706171)
12. Täuber MG, Moser B,. Cytokines and chemokines in meningeal inflammation: biology and clinical implications. Clin Infect Dis 1999; 28: 1-12. (Pubitemid 29246115)
13. Van Der Flier M, Geelen SPM, Kimpen JLL, et al. Reprogramming the host response in bacterial meningitis: how best to improve outcome? Clin Microbiol Rev 2003; 16: 415-429. (Pubitemid 36871314)
14. Tan DX, Chen LD, Poeggeler B, et al. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
15. Tan DX, Manchester LC, Terron MP, et al. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007; 42: 28-42. (Pubitemid 44924323)
16. Reiter RJ, Tan DX, Manchester LC, et al. Melatonin and reproduction revisited. Biol Reprod 2009; 81: 445-456.
17. Dominguez-Rodriguez A, Abreu-Gonzalez P, Sanchez-Sanchez JJ, et al. Melatonin and circadian biology in human cardiovascular disease. J Pineal Res 2010; 49: 14-22.
18. Reiter RJ, Calvo JR, Karbownik M, et al. Melatonin and its relation to the immune system and inflammation. Ann N Y Acad Sci 2000; 917: 376-386.
19. Cuzzocrea S, Reiter RJ,. Pharmacological actions of melatonin in acute and chronic inflammation. Curr Top Med Chem 2002; 2: 153-165.
20. Carrillo-Vico A, Guerrero JM, Lardone PJ, et al. A review of the multiple actions of melatonin on the immune system. Endocrine 2005; 27: 189-200. (Pubitemid 41558451)
21. Carrillo-Vico A, Reiter RJ, Lardone PJ, et al. The modulatory role of melatonin on immune responsiveness. Curr Opin Investig Drugs 2006; 7: 423-431. (Pubitemid 43772981)
22. Giannoulia-Karantana A, Vlachou A, Polychronopoulou S, et al. Melatonin and immunomodulation: connections and potential clinical applications. Neuroimmunomodulation 2006; 13: 133-144. (Pubitemid 46187689)
23. Szczepanik M,. Melatonin and its influence on immune system. J Physiol Pharmacol 2007; 58 (Suppl. 6): 115-124.
24. Rosales-Corral S, Reiter RJ, Tan DX, et al. Functional aspects of redox control during neuroinflammation. Antioxid Redox Signal 2010; 13: 193-247.
25. Rosales-Corral S, Tan DX, Reiter RJ, et al. Orally administered melatonin reduces oxidative stress and proinflammatory cytokines induced by amyloid-beta peptide in rat brain: a comparative, in vivo study versus vitamin C and E. J Pineal Res 2003; 35: 80-84. (Pubitemid 36960345)
26. Xu DX, Wang H, Ning H, et al. Maternally administered melatonin differentially regulates lipopolysaccharide-induced proinflammatory and anti-inflammatory cytokines in maternal serum, amniotic fluid, fetal liver, and fetal brain. J Pineal Res 2007; 43: 74-79. (Pubitemid 47035224)
27. Fang Q, Chen G, Zhu W, et al. Influence of melatonin on cerebrovascular proinflammatory mediators expression and oxidative stress s following subarachnoid hemorrhage in rabbits. Mediators Inflamm 2009; 2009: 426346 (article ID).
28. Li ZQ, Liang GB, Xue YX, et al. Effects of combination treatment of dexamethasone and melatonin on brain injury in intracerebral hemorrhage model in rats. Brain Res 2009; 1264: 98-103.
29. Olcese JM, Cao C, Mori T, et al. Protection against cognitive deficits and markers of neurodegeneration by long-term oral administration of melatonin in a transgenic model of Alzheimer disease. J Pineal Res 2009; 47: 82-96.
30. Chung SY, Han SH,. Melatonin attenuates kainic acid-induced hippocampal neurodegeneration and oxidative stress through microglial inhibition. J Pineal Res 2003; 34: 95-102.
31. Shen Y, Zhang G, Liu L, et al. Suppressive effects of melatonin on amyloid-beta-induced glial activation in rat hippocampus. Arch Med Res 2007; 38: 284-290. (Pubitemid 46366081)
32. Kaur C, Ling EA,. Effects of melatonin on macrophages/microglia in postnatal rat brain. J Pineal Res 1999; 26: 158-168. (Pubitemid 29183119)
33. Peters JL, Earnest BJ, Tjalkens RB, et al. Modulation of intercellular calcium signaling by melatonin in avian and mammalian astrocytes is brain region-specific. J Comp Neurol 2005; 493: 370-380. (Pubitemid 41677468)
34. Tocharus J, Chongthammakun S, Govitrapong P,. Melatonin inhibits amphetamine- induced nitric oxide synthase mRNA overexpression in microglial cell lines. Neurosci Lett 2008; 439: 134-137.
35. Zhou J, Zhang S, Zhao X, et al. Melatonin impairs NADPH oxidase assembly and decreases superoxide anion production in microglia exposed to amyloid-beta1-42. J Pineal Res 2008; 45: 157-165.
36. Tocharus J, Khonthun C, Chongthammakun S, et al. Melatonin attenuates methamphetamine-induced overexpression of pro-inflammatory cytokines in microglial cell lines. J Pineal Res 2010; 48: 347-352.
37. Grandgirard D, Leib SL,. Strategies to prevent neuronal damage in pediatric bacterial meningitis. Curr Opin Pediatr 2006; 18: 112-118.
38. Belu AM, Graham DJ, Castner DG,. Time-of-flight secondary ion mass spectrometry: techniques and applications for the characterization of biomaterial surfaces. Biomaterials 2003; 24: 3635-3653. (Pubitemid 36773600)
39. Wu CH, Shieh JY, Wen CY, et al. 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. In: Topical Issues of Microglia Research, Ling EA, Tan CK, Tan CBC, eds., Singapore Neuroscience Association, Singapore, 1996; pp. 83-104.
40. Hulse RE, Kunkler PE, Fedynyshyn JP, et al. Optimization of multiplexed bead-based cytokine immunoassays for rat serum and brain tissue. J Neurosci Methods 2004; 136: 87-98. (Pubitemid 38569875)
41. Wong-Riley MTT,. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 1989; 12: 94-101. (Pubitemid 19067056)
42. Sharma M, Gupta YK,. Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment. Life Sci 2001; 68: 1021-1029. (Pubitemid 32168054)
43. Chang HM, Mai FD, Chen BJ, et al. Sleep deprivation predisposes liver to oxidative stress and phospholipid damage: a quantitative molecular imaging study. J Anat 2008; 212: 295-305.
44. Mai FD, Chen LY, Ling YC, et al. Molecular imaging of in vivo calcium ion expression in area postrema of total sleep deprived rats: implications for cardiovascular regulation by TOF-SIMS analysis. Appl Surf Sci 2010; 256: 4456-4461.
45. Chang HM, Ling EA, Chen CF, et al. Melatonin attenuates the neuronal NADPH-d/NOS expression in the nodose ganglion of acute hypoxic rats. J Pineal Res 2002; 32: 65-73.
46. Chang HM, Tseng CY, Wei IH, et al. Melatonin restores the cytochrome oxidase reactivity in the nodose ganglia of acute hypoxic rats. J Pineal Res 2005; 39: 206-214.
47. Chang HM, Wu UI, Lan CT,. Melatonin preserves longevity protein (sirtuin 1) expression in the hippocampus of total sleep-deprived rats. J Pineal Res 2009; 47: 211-220.
48. Smolen AJ,. Image analytic techniques for quantification of immuno-histochemical staining in the nervous system. In: Quantitative and Qualitative Microscopy, Vol. 3, Conn PM, ed., Academic Press, San Diego, 1990; pp. 208-229.
49. Dinarello CA,. Pro-inflammatory cytokines. Chest 2000; 118: 503-508.
50. Weissenböck H, Hornig M, Hickey WF, et al. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats. Brain Pathol 2000; 10: 260-272. (Pubitemid 30181094)
51. Nakai Y, Itoh M, Mizuguchi M, et al. Apoptosis and microglial activation in influenza encephalopathy. Acta Neuropathol 2003; 105: 233-239. (Pubitemid 36798814)
52. 2+ disturbance in microglia activation-mediated dopaminergic cell degeneration. Mech Ageing Dev 2005; 126: 1241-1254. (Pubitemid 41572241)
53. Bessis A, Béchade C, Bernard D, et al. Microglial control of neuronal death and synaptic properties. Glia 2007; 55: 233-238. (Pubitemid 46225955)
54. Barone FC, Parsons AA,. Therapeutic potential of anti-inflammatory drugs in focal stroke. Expert Opin Investig Drugs 2000; 9: 2281-2306.
55. Lloyd E, Somera-Molina K, Van Eldik LJ, et al. Suppression of acute proinflammatory 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. J Neuroinflammation 2008; 5: 28 (article ID).
56. Mccarty MF,. Down-regulation of microglial activation may represent a practical strategy for combating neurodegenerative disorders. Med Hypotheses 2006; 67: 251-269. (Pubitemid 43825600)
57. Li Y, Hu X, Liu Y, et al. Nimodipine protects dopaminergic neurons against inflammation- mediated degeneration through inhibition of microglial activation. Neuropharmacology 2009; 56: 580-589.
58. Mirrione MM, Konomos DK, Gravanis I, et al. Microglial ablation and lipopolysaccharide preconditioning affects pilocarpine-induced seizures in mice. Neurobiol Dis 2010; 39: 85-97.
59. Bonilla E, Valero N, Chacín-Bonilla L, et al. Melatonin and viral infections. J Pineal Res 2004; 36: 73-79. (Pubitemid 38250876)
60. Gerber J, Lotz M, Ebert S, et al. Melatonin is neuroprotective in experimental Streptococcus pneumoniae meningitis. J Infect Dis 2005; 191: 783-790. (Pubitemid 40271070)
61. Santello FH, Frare EO, Dos Santos CD, et al. Melatonin treatment reduces the severity of experimental Trypanosoma cruzi infection. J Pineal Res 2007; 42: 359-363. (Pubitemid 46581660)
62. Srinivasan V, Warren Spence D, Moscovitch A, et al. Malaria: therapeutic implications of melatonin. J Pineal Res 2010; 48: 1-8.
63. El-Sokkary GH, Omar HM, Hassanein AF, et al. Melatonin reduces oxidative damage and increases survival of mice infected with Schistosoma mansoni. Free Radic Biol Med 2002; 32: 319-332. (Pubitemid 34159086)
64. Tekbas OF, Ogur R, Korkmaz A, et al. Melatonin as an antibiotic: new insights into the actions of this ubiquitous molecule. J Pineal Res 2008; 44: 222-226. (Pubitemid 351255501)
65. Guha M, Maity P, Choubey V, et al. Melatonin inhibits free radical-mediated mitochondrial- dependent hepatocyte apoptosis and liver damage induced during malarial infection. J Pineal Res 2007; 43: 372-381. (Pubitemid 47512269)
66. Huang SH, Cao XJ, Liu W, et al. Inhibitory effect of melatonin on lung oxidative stress induced by respiratory syncytial virus infection in mice. J Pineal Res 2010; 48: 109-116.
67. Escames G, Leõn J, Macías M, et al. Melatonin counteracts lipopolysaccharide-induced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J 2003; 17: 932-934.
68. Moncada S, Bolaños JP,. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 2006; 97: 1676-1689. (Pubitemid 43873660)
69. Zhang J, Dawson VL, Dawson TM, et al. Nitric oxide activation of poly (ADP-ribose) synthetase in neurotoxicity. Science 1994; 263: 687-689. (Pubitemid 24076297)
70. Kim YH, Koh JY,. The role of NADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp Neurol 2002; 177: 407-418.
71. Williams BL, Hornig M, Yaddanapudi K, et al. Hippocampal poly(ADP-Ribose) polymerase 1 and caspase 3 activation in neonatal bornavirus infection. J Virol 2008; 82: 1748-1758. (Pubitemid 351206925)
72. Dugo L, Serraino I, Fulia F, et al. Effect of melatonin on cellular energy depletion mediated by peroxynitrite and poly (ADP-ribose) synthetase activation in an acute model of inflammation. J Pineal Res 2001; 31: 76-84. (Pubitemid 32626049)
73. Carrillo-Vico A, Lardone PJ, Naji L, et al. Beneficial pleiotropic actions of melatonin in an experimental model of septic shock in mice: regulation of pro-/anti-inflammatory cytokine network, protection against oxidative damage and anti-apoptotic effects. J Pineal Res 2005; 39: 400-408.
74. Das A, Belagodu A, Reiter RJ, et al. Cytoprotective effects of melatonin on C6 astroglial cells exposed to glutamate excitotoxicity and oxidative stress. J Pineal Res 2008; 45: 117-124.
75. Olivier P, Fontaine RH, Loron G, et al. Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats. PLoS ONE 2009; 4: e7128.
76. Reiter RJ, Tan DX, Qi W, et al. Pharmacology and physiology of melatonin in the reduction of oxidative stress in vivo. Biol Signals Recept 2000; 9: 160-171. (Pubitemid 30481269)
77. Reiter RJ,. Oxidative processes and anti-oxidative defense mechanisms in the aging brain. FASEB J 1995; 9: 526-533.
78. Havter CL, Bishop GM, Robinson SR,. Pharmacological but not physiological concentrations of melatonin reduce iron-induced neuronal death in rat cerebral cortex. Neurosci Lett 2004; 362: 182-184. (Pubitemid 38648936)
79. Chang HM, Ling EA, Lue JH, et al. Melatonin attenuates neuronal NADPH-d/NOS expression in the hypoglossal nucleus of adult rats following peripheral nerve injury. Brain Res 2000; 873: 243-251.
80. Chang HM, Huang YL, Lan CT, et al. Melatonin preserves superoxide dismutase activity in hypoglossal motoneurons of adult rats following peripheral nerve injury. J Pineal Res 2008; 44: 172-180.
81. Spreer A, Gerber J, Baake D, et al. Anti-inflammatory but no neuroprotective effects of melatonin under clinical treatment conditions in rabbit models of bacterial meningitis. J Neurosci Res 2006; 84: 1575-1579. (Pubitemid 44683150)