Melatonin inhibits matrix metalloproteinase-9 (MMP-9) activation in the lipopolysaccharide (LPS)-stimulated RAW 264.7 and BV2 cells and a mouse model of meningitis

Journal of Pineal Research

Volumn 53, Issue 2, 2012, Pages 188-197

  Chang, Che Chao ^a   Tien, Chih Hao ^a   Lee, E Jian ^a   Juan, Wei Sheng ^a   Chen, Ying Hsin ^a   Hung, Yu Chang ^a   Chen, Tsung Ying ^a,b   Chen, Hung Yi ^a,c   Wu, Tian Shung ^c,d  

^a NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^b BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

lipopolysaccharide; matrix metalloproteinase 9; melatonin; neuroinflammation; nuclear factor kappa B

Indexed keywords

ANTIINFLAMMATORY AGENT; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MELATONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GEL MOBILITY SHIFT ASSAY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MENINGITIS; MOUSE; NONHUMAN; PROTEIN BINDING; ZYMOGRAPHY;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME ACTIVATION; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MENINGITIS; MICE; NF-KAPPA B;

EID: 84864975206     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2012.00986.x     Document Type: Article

References (54)

1. Stamenkovic I,. Matrix metalloproteinases in tumor invasion and metastasis. Semin Cancer Biol 2000; 10: 415-433.
2. Vu TH, Werb Z,. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000; 14: 2123-2133.
3. Ganguly K, Maity P, Reiter RJ, et al., Effect of melatonin on secreted and induced matrix metalloproteinase-9 and -2 activity during prevention of indomethacin-induced gastric ulcer. J Pineal Res 2005; 39: 307-315.
4. Swarnakar S, Mishra A, Ganguly K, et al., Matrix metalloproteinase-9 activity and expression is reduced by melatonin during prevention of ethanol-induced gastric ulcer in mice. J Pineal Res 2007; 43: 56-64.
5. Gill SE, Parks WC,. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 2008; 40: 1334-1347.
6. Hung YC, Chen TY, Lee EJ, et al., Melatonin decreases matrix metalloproteinase-9 activation and expression and attenuates reperfusion-induced hemorrhage following transient focal cerebral ischemia in rats. J Pineal Res 2008; 45: 459-461.
7. Tai SH, Chen HY, Lee EJ, et al., Meatonin inhibits postischemic matrix metalloproteinase-9 (MMP-9) activation via dual modulation of plasminogen/plasmin system and endogenous MMP inhibitor in mice subjected to transient focal cerebral ischemia. J Pineal Res 2010; 49: 332-341.
8. Swarnakar S, Paul S, Singh LP, Reiter RJ,. Matrix metalloproteinases in health and disease: regulation by melatonin. J Pineal Res 2011; 50: 8-20.
9. Griendling KK, Sorescu D, Lassegue B, et al., Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 2000; 20: 2175-2183.
10. Chen TY, Lee MY, Chen HY, et al., Melatonin attenuates the postischemic increase in blood-brain barrier permeability and decreases hemorrhagic transformation of tissue-plasminogen activator therapy following ischemic stroke in mice. J Pineal Res 2006; 40: 242-250.
11. Zhao BQ, Ikeda Y, Ihara H, et al., Essential role of endogenous tissue plasminogen activator through matrix metalloproteinase 9 induction and expression on heparin-produced cerebral hemorrhage after cerebral ischemia in mice. Blood 2004; 103: 2610-2616.
12. Gasche Y, Copin JC, Sugawara T, et al., Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2001; 21: 1393-1400.
13. Chen HY, Chen TY, Lee MY, et al., Melatonin decreases neurovascular oxidative/nitrosative damage and protects against early increases in the blood-brain barrier permeability after transient focal cerebral ischemia in mice. J Pineal Res 2006; 41: 175-182.
14. Lee MY, Kuan YH, Chen HY, et al., Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J Pineal Res 2007; 42: 297-309.
15. Fu X, Kao JLF, Bergt C, et al., Oxidative cross-linking of tryptophan to glycine restrains matrix metalloproteinase activity: specific structural motifs control protein oxidation. J Biol Chem 2004; 279: 6209-6212.
16. Pustovrh MC, Jawerbaum A, Capobianco E, et al., Oxidative stress promotes the increase of matrix metalloproteinases-2 and -9 activities in the feto-placental unit of diabetic rats. Free Radic Res 2005; 39: 1285-1293.
17. Rees MD, Kennett EC, Whitelock JM, et al., Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic Biol Med 2008; 44: 1973-2001.
18. Nelson KK, Subbaram S, Connor KM, et al., Redox-dependent matrix metalloproteinase-1 expression is regulated by JNK through Ets and AP-1 promoter motifs. J Biol Chem 2006; 281: 14100-1410.
19. Chetsawang B, Putthaprasart C, Phansuwan-Pujito P, et al., Melatonin protects against hydrogen peroxide-induced cell death signaling in SH-SY5Y cultured cells: involvement of nuclear factor kappa B, Bax and Bcl-2. J Pineal Res 2006; 41: 116-123.
20. Van den Steen PE, Dubois B, Nelissen I, et al., Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002; 37: 375-536.
21. Esposito E, Genovese T, Caminiti R, Bramanti P, Meli R, Cuzzocrea S,. Melatonin regulates matrix metalloproteinases after traumatic experimental spinal cord injury. J Pineal Res 2008; 45: 149-156.
22. Paul S, Sharma AV, Mahapatra PD, Bhattacharya P, Reiter RJ, Swarnakar S,. Role of melatonin in regulating matrix metalloproteinase-9 via tissue inhibitors of metalloproteinase-1 during protection against endometriosis. J Pineal Res 2008; 44: 439-449.
23. Esposito E, Mazzon E, Riccardi L, Caminiti R, Meli R, Cuzzocrea S,. Matrix metalloproteinase-9 and metalloproteinase-2 activity and expression is reduced by melatonin during experimental colitis. J Pineal Res 2008; 45: 166-173.
24. Ganguly K, Swarnakar S,. Induction of matrix metalloproteinase-9 and -3 in nonsteroidal anti-inflammatory drug-induced acute gastric ulcers in mice: regulation by melatonin. J Pineal Res 2009; 47: 43-55.
25. Mishra A, Paul S, Swarnakar S,. Downregulation of matrix metalloproteinase-9 by melatonin during prevention of alcohol-induced liver injury in mice. Biochimie 2011; 93: 854-866.
26. 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.
27. Hardeland R, Tan DX, Reiter RJ,. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009; 47: 109-126.
28. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
29. Natarajan M, Sadeghi K, Reiter RJ, et al., The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-kappa B. Biochem Mol Biol Int 1995; 37: 1063-1070.
30. Chuang JI, Natarajan M, Meltz ML, et al., Effect of melatonin on NF-kappa-B DNA-binding activity in the rat spleen. Cell Biol Int 1996; 20: 687-692.
31. Li N, Karin M,. Is NF-kappaB the sensor of oxidative stress? FASEB J 1999; 13: 1137-1143.
32. Beni SM, Kohen R, Reiter RJ, Tan DX, Shohami E,. Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-kappaB and AP-1. FASEB J 2004; 18: 149-151.
33. Esposito E, Iacono A, Muiá C, et al., Signal transduction pathways involved in protective effects of melatonin in C6 glioma cells. J Pineal Res 2008; 44: 78-87.
34. Trachootham D, Alexandre J, Huang P,. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009; 8: 579-591.
35. Lee EJ, Wu TS, Lee MY, et al., Delayed treatment with melatonin enhances electrophysiological recovery following transient focal cerebral ischemia in rats. J Pineal Res 2004; 36: 33-42.
36. Lee EJ, Lee MY, Chen HY, et al., Melatonin attenuates gray and white matter damage in a mouse model of transient focal cerebral ischemia. J Pineal Res 2005; 38: 42-52.
37. Chen HY, Hung YC, Chen TY, et al., Melatonin improves presynaptic protein, SNAP-25, expression and dendritic spine density and enhances functional and electrophysiological recovery following transient focal cerebral ischemia in rats. J Pineal Res 2009; 47: 260-270.
38. Lee EJ, Chen HY, Hung YC, et al., Therapeutic window for cinnamophilin following oxygen-glucose deprivation and transient focal cerebral ischemia. Exp Neurol 2009; 217: 74-83.
39. Tai SH, Hung YC, Lee EJ, et al., Melatonin protects against transient focal cerebral ischemia in both reproductively active and estrogen-deficient female rats: the impact of circulating estrogen on its hormetic dose-response. J Pineal Res 2011; 50: 292-303.
40. Webster CM, Kelly S, Koike MA, et al., Inflammation and NF-kappa B activation is decreased by hypothermia following global cerebral ischemia. Neurobiol Dis 2009; 33: 301-312.
41. Romanic AM, White RF, Arleth AJ, et al., Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 1998; 29: 1020-1030.
42. Chen TY, Lin MH, Lee WT, et al., Nicotinamide inhibits nuclear factor-kappa B translocation after transient focal cerebral ischemia. Crit Care Med 2012; 40: 532-537.
43. Chen TY, Tai SH, Lee EJ, et al., Cinnamophilin offers prolonged neuroprotection against gray and white matter damage and improves functional and electrophysiological outcomes after transient focal cerebral ischemia. Crit Care Med 2011; 39: 1130-1137.
44. Tan DX, Chen LD, Poeggeler B, et al., Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
45. Rodriguez C, Mayo JC, Sainz RM, et al., Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9.
46. Kilic U, Kilic E, Reiter RJ, et al., Signal transduction pathways involved in melatonin-induced neuroprotection after focal cerebral ischemia in mice. J Pineal Res 2005; 38: 67-71.
47. Wu UI, Mai FD, Sheu JN, et al., Melatonin inhibits microglial activation, reduces pro-inflammatory cytokine levels, and rescues hippocampal neurons of adult rats with acute Klebsiella pneumoniae meningitis. J Pineal Res 2011; 50: 159-170.
48. Cuzzocrea S, Reiter RJ,. Pharmacological actions of melatonin in acute and chronic inflammation. Curr Top Med Chem 2002; 2: 153-165.
49. Esposito E, Paterniti I, Mazzon E, Bramanti P, Cuzzocrea S,. Melatonin reduces hyperalgesia associated with inflammation. J Pineal Res 2010; 49: 321-331.
50. Veneroso C, Tuñõn MJ, González-Gallego J, Collado PS,. Melatonin reduces cardiac inflammatory injury induced by acute exercise. J Pineal Res 2009; 47: 184-191.
51. Raghavendra V, Agrewala JN, Kulkarni SK,. Melatonin reversal of lipopolysacharides-induced thermal and behavioral hyperalgesia in mice. Eur J Pharmacol 2000; 395: 15-21.
52. Ganguly K, Kundu P, Banerjee A, et al., Hydrogen peroxide-mediated downregulation of matrix metalloprotease-2 in indomethacin-induced acute gastric ulceration is blocked by melatonin and other antioxidants. Free Radic Biol Med 2006; 41: 911-925.
53. Kilic E, Kilic U, Reiter RJ, et al., Tissue-plasminogen activator-induced ischemic brain injury is reversed by melatonin: role of iNOS and Akt. J Pineal Res 2005; 39: 151-155.
54. Sanchez-Barcelo EJ, Mediavilla MD, Tan DX, et al., Clinical uses of melatonin: evaluation of human trials. Curr Med Chem 2010; 17: 2070-2095.