Naringin inhibits matrix metalloproteinase-9 expression and AKT phosphorylation in tumor necrosis factor-α-induced vascular smooth muscle cells

Molecular Nutrition and Food Research

Volumn 53, Issue 12, 2009, Pages 1582-1591

  Lee, Eo Jin ^a   Kim, Dong Il ^a   Kim, Wun Jae ^b   Moon, Sung Kwon ^a  

^a Chungju National University   (South Korea)

^b Chungbuk National University College of Medicine   (South Korea)

Author keywords

MMP 9; Naringin; PI3K AKT mTOR p70S6K pathway; TNF ; Vascular smooth muscle cell

Indexed keywords

AURANTIIN; FLAVANONE DERIVATIVE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN DERIVATIVE; MAMMALIAN TARGET OF RAPAMYCIN; NARINGENIN; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; S6 KINASE; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; PROMOTER REGION; RAT; SECRETION; SMOOTH MUSCLE FIBER; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; INTERLEUKINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MATRIX METALLOPROTEINASE 9; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NF-KAPPA B; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TRANSCRIPTION FACTOR AP-1; TUMOR NECROSIS FACTOR-ALPHA;

CITRUS;

EID: 71149104926     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200800210     Document Type: Article

References (44)

1. Ross, R., The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993, 362, 801-809.
2. Visse, R., Nagase, H., Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92, 827-839.
3. Newby, A. C., Zaltsman, A. B., Molecular mechanisms in intimal hyperplasia. J. Pathol. 2000, 190, 300-309.
4. Galis, Z. S., Muszynski, M., Sukhova, G. K., Simon-Morrissey, E. et al., Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ. Res. 1994, 75, 181-189.
5. Fabunmi, R. P., Baker, A. H., Murray, E. J., Booth, R. F. G., Newby, A. C., Divergent regulation by growth factors and cytokines of 95 kDa and 72 kDa gelatinases and tissue inhibitors or metalloproteinases-1, -2, and -3 in rabbit aortic smooth muscle cells. Biochem. J. 1996, 315, 335-342.
6. Cho, A., Graves, J., Reidy, M. A., Mitogen-activated protein kinases mediate matrix metalloproteinase-9 expression in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2000, 20, 2527-2532.
7. Bendeck, M. P., Zempo, N., Clowes, A. W., Galardy, R. E., Reidy, M. A., Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ. Res. 1994, 75, 539-545.
8. Cho, A., Reidy, M. A., Matrix metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ. Res. 2002, 91, 845-851.
9. Abedi, H., Zachary, I., Signalling mechanisms in the regulation of vascular cell migration. Cardiovasc. Res. 1995, 30, 544-556.
10. Jovinge, S., Hultgardh-Nilsson, A., Regnstrom, J., Nilsson, J., TNF-a activates smooth muscle cell migration in culture and is expressed in the balloon-injured rat aorta. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 490-497.
11. Tipping, P. G., Hancock, W. W., Production of tumor necrosis factor and interleukin-1 by macrophages from human atherosclerotic plaques. Am. J. Pathol. 1993, 142, 1721-1728.
12. Clausell, N., De Lima, V. C., Molossi, S., Expression of tumor necrosis factor-a and accumulation of fibronectin in coronary artery restenotic lesions retrieved by atherectomy. Br. Heart J. 1995, 73, 534-539.
13. Bond, M., Rosalind, P., Fabunmi, P., Baker, A. H., Newby, A. C., Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett. 1998,435,29-34.
14. Sato, H., Kita, M., Seiki, M., v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements, A mechanism regulating gene expression independent of that by inflammatory cytokines. J. Biol. Chem. 1993,268,23460-23468.
15. Farina, A. R., Tacconelli, A., Vacca, A., Maroder, M. et al., Transcriptional up-regulation of matrix metalloproteinase-9 expression during spontaneous epithelial to neuroblast phenotype conversion by SK-N-SH neuroblastoma cells, involved in enhanced invasivity, depends upon GT-Box and nuclear factor NF-kB elements. Cell Growth Differ. 1999, 10, 353-367.
16. Moon, S. K., Cha, B. Y., Kim, C. H., ERK1/2 mediates TNF-alpha-induced matrix metalloproteinase-9 expression in human vascular smooth muscle cells via the regulation of NF-kappaB and AP-1: involvement of the ras dependent pathway. J. Cell. Physiol. 2004, 198, 417-427.
17. Lee, C. W., Lin, C. C., Lin, W. N., Liang, K. C. et al., TNF-alpha induces MMP-9 expression via activation of Src/EGFR, PDGFR/PI3K/Akt cascade and promotion of NF-kappaB/p300 binding in human tracheal smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292, L799-L812.
18. Jin, U. H., Suh, S. J., Chang, H. W., Son, J. K. et al., Tanshinone IIA from Salvia miltiorrhiza BUNGE inhibits human aortic smooth muscle cell migration and MMP-9 activity through AKT signaling pathway. J. Cell. Biochem. 2008, 104, 15-26.
19. Le Marchand, L., Murphy, S. P., Hankin, J. H., Wilkens, L. R., Kolonel, L. N., Intake of flavonoids and lung cancer. J. Natl. Cancer Inst. 2000, 92, 154-160.
20. So, F. V., Guthrie, N., Chambers, A. F., Moussa, M., Carroll, K. K., Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr. Cancer 1996, 26, 167-181.
21. Kanno, S., Tomizawa, A., Hiura, T., Osanai, Y. et al., Inhibitory effects of naringenin on tumor growth in human cancer cell lines and sarcoma S-180-implanted mice. Biol. Pharm. Bull. 2005, 28, 527-530.
22. Ng, T. B., Liu, F., Wang, Z. T., Antioxidative activity of natural products from plants. Life Sci. 2000, 66, 709-723.
23. Lee, C. H., Jeong, T. S., Choi, Y. K., Hyun, B. H. et al., Antiatherogenic effect of citrus flavonoids, naringin and naringenin, associated with hepatic ACAT and aortic VCAM-1 and MCP-1 in high cholesterol-fed rabbits. Biochem. Biophys. Res. Commun. 2001, 284, 681-688.
24. Moon, S. K., Jung, S. Y., Choi, Y. H., Lee, Y. C. et al., PDTC, metal chelating compound, induces G1 phase cell cycle arrest in vascular smooth muscle cells through inducing p21Cip1 expression: involvement of p38 mitogen activated protein kinase. J. Cell. Physiol. 2004, 198, 310-323.
25. Oak, M. H., El Bedoui, J., Anglard, P., Schini-Kerth, V. B., Red wine polyphenolic compounds strongly inhibit pro-matrix metalloproteinase-2 expression and its activation in response to thrombin via direct inhibition of membrane type 1-matrix metalloproteinase in vascular smooth muscle cells. Circulation 2004, 110, 1861-1867.
26. Moon, S. K., Cho, G. O., Jung, S. Y., Gal, S. W. et al., Quercetin exerts multiple inhibitory effects on vascular smooth muscle cells: role of ERK1/2, cell-cycle regulation, and matrix metalloproteinase-9. Biochem. Biophys. Res. Commun. 2003, 301, 1069-1078.
27. Bok, S. H., Lee, S. H., Park, Y. B., Bae, K. H. et al., Plasma and hepatic cholesterol and hepatic activities of 3-hydroxy-3-methyl-glutaryl-CoA reductase and acyl CoA: cholesterol transferase are lower in rats fed citrus peel extract or a mixture of citrus bioflavonoids. J. Nutr. 1999, 129, 1182-1185.
28. Choe, S. C., Kim, H. S., Jeong, T. S., Bok, S. H., Park, Y. B., Naringin has an antiatherogenic effect with the inhibition of intercellular adhesion molecule-1 in hypercholesterolemic rabbits. J. Cardiovasc. Pharmacol. 2001, 38, 947-955.
29. Wang, Z., Castresana, M. R., Newman, W. H., NF-kappaB is required for TNF-alpha-directed smooth muscle cell migration. FEBS Lett. 2001, 508, 360-364.
30. Baeuerle, P. A., Henkel, T., Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 1994, 12,141-179.
31. Dell'Agli, M., Canavesi, M., Galli, G., Bellosta, S., Dietary polyphenols and regulation of gelatinase expression and activity. Thromb. Haemost. 2005, 93, 751-760.
32. Brown, D. L., Hibbs, M. S., Kearney, M., Loushin, C., Isner, J. M., Identification of 92-kD gelatinase in human coronary atherosclerotic lesions. Association of active enzyme synthesis with unstable angina. Circulation 1995, 91, 2125-2131.
33. Galis, Z. S., Sukhova, G. K., Lark, M. W., Libby, P., Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human athero-sclerotic plaques. J. Clin. Invest. 1994, 94, 2493-2503.
34. Bellosta, S., Baetta, R., Canavesi, M., Comparato, C. et al., Raloxifene inhibits matrix metalloproteinases expression and activity in macrophages and smooth muscle cells. Pharmacol. Res. 2007, 56, 160-167.
35. Galis, Z. S., Khatri, J. J., Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res. 2002, 90, 251-262.
36. Galis, Z. S., Johnson, C., Godin, D., Magid, R. et al., Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ. Res. 2002, 91, 852-859.
37. Stoclet, J. C., Chataigneau, T., Ndiaye, M., Oak, M. H. et al., Vascular protection by dietary polyphenols. Eur. J. Pharmacol. 2004, 500, 299-313.
38. Bachmeier, B. E., Iancu, C. M., Jochum, M., Nerlich, A. G., Matrix metalloproteinases in cancer: comparison of known and novel aspects of their inhibition as a therapeutic approach. Expert Rev. Anticancer Ther. 2005, 5, 149-163.
39. Kim, D. I., Lee, S. J., Lee, S. B., Park, K. et al., Requirement for Ras/Raf/ERK pathway in naringin-induced G1-cell cycle arrest via p21WAF1 expression. Carcinogenesis 2008, 29, 1701-1709.
40. Ameer, B., Weintraub, R. A., Johnson, J. V., Yost, R. A., Rouseff, R. L., Flavanone absorption after naringin, hesperidin, and citrus administration. Clin. Pharmacol. Ther. 1996, 60, 34-40.
41. Morikawa, K., Nonaka, M., Mochizuki, H., Handa, K. et al., Naringenin and hesperetin induce growth arrest, apoptosis, and cytoplasmic fat deposit in human preadipocytes. J. Agric. Food Chem. 2007, 56, 11030-11037.
42. 0-OH flavanone inhibit metastasis of lung cancer cells via down-regulation of proteinases activities and MAPK pathway. Chem. Biol. Interact. 2007, 167, 193-206.
43. Park, J. H., Jin, C. Y., Lee, B. K., Kim, G. Y. et al., Naringenin induces apoptosis through downregulation of Akt and caspase-3 activation in human leukemia THP-1 cells. Food Chem. Toxicol. 2008, 46, 3684-3690.
44. Erlund, I., Meririnne, E., Alfthan, G., Aro, A., Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J. Nutr. 2001, 131, 235-241.