Thromb Haemost 2005; 93(04): 751-760
DOI: 10.1160/TH04-09-0573
Cellular Proteolysis and Oncology
Schattauer GmbH

Dietary polyphenols and regulation of gelatinase expression and activity

Mario Dell’Agli
1   Department of Pharmacological Sciences, University of Milan, Milan, Italy
,
Monica Canavesi
1   Department of Pharmacological Sciences, University of Milan, Milan, Italy
,
Germana Galli
1   Department of Pharmacological Sciences, University of Milan, Milan, Italy
,
Stefano Bellosta
1   Department of Pharmacological Sciences, University of Milan, Milan, Italy
› Author Affiliations
Partly presented at the Second Chianti Meeting on Proteases held in Tuscany, Italy, from May 16–20, 2004
Further Information

Publication History

Received 08 September 2004

Accepted after resubmission 16 March 2004

Publication Date:
14 December 2017 (online)

Summary

The interaction of cells with the extracellular matrix (ECM) is critical for the normal development and function of organisms. The matrix metalloproteinases (MMPs) are a family of Zn++ and Ca++ dependent endopeptidases, which are key mediators of ECM remodelling. The turnover and remodelling of ECM must be tightly regulated, since uncontrolled proteolysis would contribute to abnormal development and to the generation of many pathological conditions characterized by either excessive degradation, or lack of degradation of ECM components. In particular, the gelatinases (MMP-2 and –9) are abundantly expressed in various malignant tumors, play an active role in angiogenesis, and may also influence the process of atherosclerotic lesion formation. In recent years, much consideration has been given to the role of diet in preventing degenerative diseases, such as cancer and cardiovascular diseases. Polyphenols are abundant components/micronutrients of the human diet that have been shown in vitro to profoundly affect ECM turnover by regulating gelatinases expression and activity, acting at both the pre- and post-transcriptional level. Therefore, they could have a beneficial effect in many pathological conditions implicated in connective tissue destruction and remodelling associated with degenerative diseases.

 
  • References

  • 1 Chakraborti T, Das S, Mandal M. et al. Role of Ca2+-dependent metalloprotease-2 in stimulating Ca2+ ATPase activity under peroxynitrite treatment in bovine pulmonary artery smooth muscle membrane. IUBMB Life 2002; 53: 167-73.
  • 2 Massova I, Kotra LP, Fridman R. et al. Matrix metalloproteinases: structures, evolution, and diversification. Faseb J 1998; 12: 1075-95.
  • 3 Birkedal-Hansen H, Moore WG, Bodden MK. et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993; 4: 197-250.
  • 4 Beaudeux JL, Giral P, Bruckert E. et al. Matrix metalloproteinases, inflammation and atherosclerosis: therapeutic perspectives. Clin Chem Lab Med 2004; 42: 121-31.
  • 5 Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92: 827-39.
  • 6 Mandal M, Mandal A, Das S. et al. Clinical implications of matrix metalloproteinases. Mol Cell Biochem 2003; 252: 305-29.
  • 7 Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4: 617-29.
  • 8 Fini ME, Girard MT. Expression of collagenolytic/ gelatinolytic metalloproteinases by normal cornea. Invest Ophthalmol Vis Sci 1990; 31: 1779-88.
  • 9 Girard MT, Matsubara M, Kublin C. et al. Stromal fibroblasts synthesize collagenase and stromelysin during long-term tissue remodeling. J Cell Sci 1993; 104 (Pt 4) 1001-11.
  • 10 Dollery CM, McEwan JR, Henney AM. Matrix metalloproteinases and cardiovascular disease. Circ Res 1995; 77: 863-8.
  • 11 Johansson N, Ahonen M, Kahari VM. Matrix metalloproteinases in tumor invasion. Cell Mol Life Sci 2000; 57: 5-15.
  • 12 Westermarck J, Kahari VM. Regulation of matrix metalloproteinase expression in tumor invasion. Faseb J 1999; 13: 781-92.
  • 13 Sato H, Takino T, Okada Y. et al A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994; 370: 61-65.
  • 14 Johansson N, Vaalamo M, Grenman S. et al. Collagenase- 3 (MMP-13) is expressed by tumor cells in invasive vulvar squamous cell carcinomas. Am J Pathol 1999; 154: 469-80.
  • 15 Heppner KJ, Matrisian LM, Jensen RA. et al. Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am J Pathol 1996; 149: 273-82.
  • 16 Bergers G, Brekken R, McMahon G. et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-44.
  • 17 Fang J, Shing Y, Wiederschain D. et al. Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model. Proc Natl Acad Sci U S A 2000; 97: 3884-9.
  • 18 Itoh T, Tanioka M, Yoshida H. et al. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res 1998; 58: 1048-51.
  • 19 Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation 1995; 92: 657-71.
  • 20 Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-74.
  • 21 Johnson C, Galis ZS. Matrix metalloproteinase-2 and –9 differentially regulate smooth muscle cell migration and cell-mediated collagen organization. Arterioscler Thromb Vasc Biol 2004; 24: 54-60.
  • 22 Kuzuya M, Kanda S, Sasaki T. et al. Deficiency of gelatinase a suppresses smooth muscle cell invasion and development of experimental intimal hyperplasia. Circulation 2003; 108: 1375-81.
  • 23 Galis ZS, Johnson C, Godin D. et al. Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ Res 2002; 91: 852-9.
  • 24 Silence J, Collen D, Lijnen HR. Reduced atherosclerotic plaque but enhanced aneurysm formation in mice with inactivation of the tissue inhibitor of metalloproteinase- 1 (TIMP-1) gene. Circ Res 2002; 90: 897-903.
  • 25 Lemaitre V, O'Byrne TK, Borczuk AC. et al. ApoE knockout mice expressing human matrix metalloproteinase- 1 in macrophages have less advanced atherosclerosis. J Clin Invest 2001; 107: 1227-34.
  • 26 Brown DL, Hibbs MS, Kearney M. et al. Identification of 92-kD gelatinase in human coronary atherosclerotic lesions. Association of active enzyme synthesis with unstable angina. Circulation 1995; 91: 2125-31.
  • 27 Galis ZS, Sukhova GK, Lark MW. et al. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 1994; 94: 2493-503.
  • 28 Galis ZS, Muszynski M, Sukhova GK. et al. Cytokine- stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ Res 1994; 75: 181-9.
  • 29 Aikawa M, Rabkin E, Okada Y. et al. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation 1998; 97: 2433-44.
  • 30 Bellosta S, Via D, Canavesi M. et al. HMG-CoA reductase inhibitors reduce MMP-9 secretion by macrophages. Arterioscler Thromb Vasc Biol 1998; 18: 1671-8.
  • 31 Zhuge Y, Xu J. Rac1 mediates type I collagen-dependent MMP-2 activation. role in cell invasion across collagen barrier. J Biol Chem 2001; 276: 16248-56.
  • 32 Wong B, Lumma WC, Smith AM. et al. Statins suppress THP-1 cell migration and secretion of matrix J Leukoc Biol 2001; 69: 959-962
  • 33 Bellosta S, Canavesi M, Favari E. et al. Lacidipine [correction of Lalsoacidipine] modulates the secretion of matrix metalloproteinase-9 by human macrophages. J Pharmacol Exp Ther 2001; 296: 736-43.
  • 34 Dragsted LO. Antioxidant actions of polyphenols in humans. Int J Vitam Nutr Res 2003; 73: 112-9.
  • 35 Manach C, Scalbert A, Morand C. et al. Polyphenols: food sources and bioavailability. Am J Clin Nutr 2004; 79: 727-47.
  • 36 Santos-Buelga C, Scalbert A. Proanthocyanidins and tannin-like compounds – nature, occurrence, dietary intake and effects on nutrition and health. J Sci Food Agric 2000; 80: 1094-117.
  • 37 Dell'Agli M, Busciala A, Bosisio E. Vascular effects of wine polyphenols. Cardiovasc Res 2004; 63: 593-602.
  • 38 Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr 2002; 22: 19-34.
  • 39 Beecher GR. Overview of dietary flavonoids: nomenclature, occurrence and intake. J Nutr 2003; 133: 3248-3254
  • 40 Bhat KPL, Kosmeder JW, Pezzuto JM. Biological effects of resveratrol. Antioxid Redox Signal 2001; 3: 1041-64.
  • 41 Fremont L. Biological effects of resveratrol. Life Sci 2000; 66: 663-73.
  • 42 Waterhouse AL. Wine phenolics. Ann N Y Acad Sci 2002; 957: 21-36.
  • 43 Vuorinen H, Maatta K, Torronen R. Content of the flavonols myricetin, quercetin, and kaempferol in finnish berry wines. J Agric Food Chem 2000; 48: 2675-80.
  • 44 Osman HE, Maalej N, Shanmuganayagam D. et al. Grape juice but not orange or grapefruit juice inhibits platelet activity in dogs and monkeys. J Nutr 1998; 128: 2307-12.
  • 45 Ruidavets J, Teissedre P, Ferrieres J. et al. Catechin in the Mediterranean diet: vegetable, fruit or wine?. Atherosclerosis 2000; 153: 107-17.
  • 46 Ahmad N, Mukhtar H. Green tea polyphenols and cancer: biologic mechanisms and practical implications. Nutr Rev 1999; 57: 78-83.
  • 47 Mukhtar H, Ahmad N. Green tea in chemoprevention of cancer. Toxicol Sci 1999; 52: 111-7.
  • 48 Graham HN. Green tea composition, consumption, and polyphenol chemistry. Prev Med 1992; 21: 334-50.
  • 49 Yang CS, Wang ZY. Tea and cancer. J Natl Cancer Inst 1993; 85: 1038-49.
  • 50 Bavaresco L, Fregoni C. Molecular biology and biotechnology of the grapevine. Roubelakis-Angelakis K A. 2001; 153-82.
  • 51 Bavaresco L, Fregoni C, Cantu E. et al. Stilbene compounds: from the grapevine to wine. Drugs Exp Clin Res 1999; 25: 57-63.
  • 52 Ferrigni NR, McLaughlin JL, Powell RG. et al. Use of potato disc and brine shrimp bioassays to detect activity and isolate piceatannol as the antileukemic principle from the seeds of Euphorbia lagascae. J Nat Prod 1984; 47: 347-52.
  • 53 Cantos E, Espin JC, Fernandez MJ. et al. Postharvest UV-C-irradiated grapes as a potential source for producing stilbene-enriched red wines. J Agric Food Chem 2003; 51: 1208-14.
  • 54 Cantos E, Espin JC, Tomas-Barberan FA. Postharvest stilbene-enrichment of red and white table grape varieties using UV-C irradiation pulses. J Agric Food Chem 2002; 50: 6322-9.
  • 55 Helm RF, Zhentian L, Ranatunga T. et al. Toward understanding monomeric ellagitannin biosynthesis. New York. Kluwer Academic/Plenum. Gross GG, Hemingway RW, Yoshida T. 1999
  • 56 Lee JH, Talcott ST. Ellagic acid and ellagitannins affect on sedimentation in muscadine juice and wine. J Agric Food Chem 2002; 50: 3971-6.
  • 57 Olsson ME, Ekvall J, Gustavsson KE. et al. Antioxidants, low molecular weight carbohydrates, and total antioxidant capacity in strawberries (Fragaria x ananassa): effects of cultivar, ripening, and storage. J Agric Food Chem 2004; 52: 2490-8.
  • 58 Bombardelli E, Morazzoni P. Vitis vinifera L. Fitoterapia 1995; 66: 291-317.
  • 59 Cao Y, Cao R. Angiogenesis inhibited by drinking tea. Nature 1999; 398: 381
  • 60 Fujiki H, Suganuma M, Okabe S. et al. Cancer inhibition by green tea. Mutat Res 1998; 402: 307-10.
  • 61 Tachibana H, Koga K, Fujimura Y. et al. A receptor for green tea polyphenol EGCG. Nat Struct Mol Biol 2004; 11: 380-1.
  • 62 Maeda K, Kuzuya M, Cheng XW. et al. Green tea catechins inhibit the cultured smooth muscle cell invasion through the basement barrier. Atherosclerosis 2003; 166: 23-30.
  • 63 Maeda-Yamamoto M, Kawahara H, Tahara N. et al. Effects of tea polyphenols on the invasion and matrix metalloproteinases activities of human fibrosarcoma HT1080 cells. J Agric Food Chem 1999; 47: 2350-4.
  • 64 Maeda-Yamamoto M, Suzuki N, Sawai Y. et al. Association of suppression of extracellular signalregulated kinase phosphorylation by epigallocatechin gallate with the reduction of matrix metalloproteinase activities in human fibrosarcoma HT1080 cells. J Agric Food Chem 2003; 51: 1858-63.
  • 65 Kim HS, Kim MH, Jeong M. et al. EGCG blocks tumor promoter-induced MMP-9 expression via suppression of MAPK and AP-1 activation in human gastric AGS cells. Anticancer Res 2004; 24: 747-53.
  • 66 Ho LL, Chen WJ, Lin-Shiau SY. et al. Penta- O-galloyl-beta-D-glucose inhibits the invasion of mouse melanoma by suppressing metalloproteinase-9 through down-regulation of activator protein-1. Eur J Pharmacol 2002; 453: 149-58.
  • 67 Bellosta S, Dell'Agli M, Canavesi M. et al. Inhibition of metalloproteinase-9 activity and gene expression by polyphenolic compounds isolated from the bark of Tristaniopsis calobuxus (Myrtaceae). Cell Mol Life Sci 2003; 60: 1440-8.
  • 68 Demeule M, Brossard M, Page M. et al. Matrix metalloproteinase inhibition by green tea catechins. Biochim Biophys Acta 2000; 1478: 51-60.
  • 69 Annabi B, Lachambre MP, Bousquet-Gagnon N. et al. Green tea polyphenol (-)-epigallocatechin 3-gallate inhibits MMP-2 secretion and MT1-MMP-driven migration in glioblastoma cells. Biochim Biophys Acta 2002; 1542: 209-20.
  • 70 Garbisa S, Sartor L, Biggin S. et al. Tumor gelatinases and invasion inhibited by the green tea flavanol epigallocatechin-3-gallate. Cancer 2001; 91: 822-32.
  • 71 Morgunova E, Tuuttila A, Bergmann U. et al. Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 1999; 284: 1667-70.
  • 72 Cheng XW, Kuzuya M, Kanda S. et al. Epigallocatechin- 3-gallate binding to MMP-2 inhibits gelatinolytic activity without influencing the attachment to extracellular matrix proteins but enhances MMP-2 binding to TIMP-2. Arch Biochem Biophys 2003; 415: 126-32.
  • 73 Cheng XW, Kuzuya M, Sasaki T. et al. Green tea catechins inhibit neointimal hyperplasia in a rat carotid arterial injury model by TIMP-2 overexpression. Cardiovasc Res 2004; 62: 594-602.
  • 74 Holmes-McNary M, Baldwin , Jr AS. Chemopreventive properties of trans-resveratrol are associated with inhibition of activation of the IkappaB kinase. Cancer Res 2000; 60: 3477-83.
  • 75 Manna SK, Mukhopadhyay A, Aggarwal BB. Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J Immunol 2000; 164: 6509-19.
  • 76 Banerjee S, Bueso-Ramos C, Aggarwal BB. Suppression of 7,12-dimethylbenz(a)anthracene-induced mammary carcinogenesis in rats by resveratrol: role of nuclear factor-kappaB, cyclooxygenase 2, and matrix metalloprotease 9. Cancer Res 2002; 62: 4945-54.
  • 77 Woo JH, Lim JH, Kim YH. et al. Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase- 9 expression by inhibiting JNK and PKC delta signal transduction. Oncogene 2004; 23: 1845-53.
  • 78 Godichaud S, Krisa S, Couronne B. et al. Deactivation of cultured human liver myofibroblasts by transresveratrol, a grapevine-derived polyphenol. Hepatology 2000; 31: 922-31.
  • 79 Iijima K, Yoshizumi M, Hashimoto M. et al. Red wine polyphenols inhibit vascular smooth muscle cell migration through two distinct signaling pathways. Circulation 2002; 105: 2404-10.
  • 80 Ashikawa K, Majumdar S, Banerjee S. et al. Piceatannol inhibits TNF-induced NF-kappaB activation and NF-kappaB-mediated gene expression through suppression of IkappaBalpha kinase and p65 phosphorylation. J Immunol 2002; 169: 6490-7.
  • 81 Cho A, Reidy MA. Matrix metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ Res 2002; 91: 845-51.
  • 82 Moon SK, Cho GO, Jung SY. 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: 1069-78.
  • 83 Zhang XM, Huang SP, Xu Q. Quercetin inhibits the invasion of murine melanoma B16-BL6 cells by decreasing pro-MMP-9 via the PKC pathway. Cancer Chemother Pharmacol 2004; 53: 82-8.
  • 84 Morrow DM, Fitzsimmons PE, Chopra M. et al. Dietary supplementation with the anti-tumour promoter quercetin: its effects on matrix metalloproteinase gene regulation. Mutat Res 2001; 480 (481) 269-276
  • 85 Vayalil PK, Mittal A, Katiyar SK. Proanthocyanidins from grape seeds inhibit expression of matrix metalloproteinases in human prostate carcinoma cells, which is associated with the inhibition of activation of MAPK and NF kappa B. Carcinogenesis 2004; 25: 987-95.
  • 86 Sartor L, Pezzato E, Dell'Aica I. et al. Inhibition of matrix-proteases by polyphenols: chemical insights for anti-inflammatory and anti-invasion drug design. Biochem Pharmacol 2002; 64: 229-37.
  • 87 Francis FJ. Food colorants: anthocyanins. Crit Rev Food Sci Nutr 1989; 28: 273-314.
  • 88 Saller R, Meier R, Brignoli R. The use of silymarin in the treatment of liver diseases. Drugs 2001; 61: 2035-63.
  • 89 Agarwal C, Singh RP, Dhanalakshmi S. et al. Silibinin upregulates the expression of cyclin-dependent kinase inhibitors and causes cell cycle arrest and apoptosis in human colon carcinoma HT-29 cells. Oncogene 2003; 22: 8271-82.
  • 90 Singh RP, Sharma G, Dhanalakshmi S. et al. Suppression of advanced human prostate tumor growth in athymic mice by silibinin feeding is associated with re- duced cell proliferation, increased apoptosis, and inhibition of angiogenesis. Cancer Epidemiol Biomarkers Prev 2003; 12: 933-9.
  • 91 Singh RP, Agarwal R. Prostate cancer prevention by silibinin. Curr Cancer Drug Targets 2004; 4: 1-11.
  • 92 Jiang C, Agarwal R, Lu J. Anti-angiogenic potential of a cancer chemopreventive flavonoid antioxidant, silymarin: inhibition of key attributes of vascular endothelial cells and angiogenic cytokine secretion by cancer epithelial cells. Biochem Biophys Res Commun 2000; 276: 371-8.
  • 93 Chu SC, Chiou HL, Chen PN. et al. Silibinin inhibits the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Mol Carcinog 2004; 40: 143-9.
  • 94 Dhanalakshmi S, Singh RP, Agarwal C. et al. Silibinin inhibits constitutive and TNFalpha-induced activation of NF-kappaB and sensitizes human prostate carcinoma DU145 cells to TNFalpha-induced apoptosis. Oncogene 2002; 21: 1759-67.
  • 95 Messina MJ, Persky V, Setchell KD. et al. Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutr Cancer 1994; 21: 113-31.
  • 96 Fotsis T, Pepper M, Adlercreutz H. et al. Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J Nutr 1995; 125: 790-797
  • 97 Huang YT, Hwang JJ, Lee PP. et al. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis-associated properties in A431 cells overexpressing epidermal growth factor receptor. Br J Pharmacol 1999; 128: 999-1010.
  • 98 Myoung H, Hong SP, Yun PY. et al. Anti-cancer effect of genistein in oral squamous cell carcinoma with respect to angiogenesis and in vitro invasion. Cancer Sci 2003; 94: 215-20.
  • 99 Kim MH. Flavonoids inhibit VEGF/bFGF-induced angiogenesis in vitro by inhibiting the matrix-degrading proteases. J Cell Biochem 2003; 89: 529-38.
  • 100 Huang TS, Kuo ML, Lin JK. et al. A labile hyperphosphorylated c-Fos protein is induced in mouse fibroblast cells treated with a combination of phorbol ester and anti-tumor promoter curcumin. Cancer Lett 1995; 96: 1-7.
  • 101 Singh S, Aggarwal BB. Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane) [corrected]. J Biol Chem 1995; 270: 24995-5000.
  • 102 Yokoo T, Kitamura M. Dual regulation of IL-1 beta-mediated matrix metalloproteinase-9 expression in mesangial cells by NF-kappa B and AP-1. Am J Physiol 1996; 270: F123-130.
  • 103 Lin I L, Ke YF, Ko YC. et al. Curcumin inhibits SK-Hep-1 hepatocellular carcinoma cell invasion in vitro and suppresses matrix metalloproteinase-9 secretion. Oncology 1998; 55: 349-53.
  • 104 Mohan R, Sivak J, Ashton P. et al. Curcuminoids inhibit the angiogenic response stimulated by fibroblast growth factor-2, including expression of matrix metalloproteinase gelatinase B. J Biol Chem 2000; 275: 10405-12.
  • 105 Takada Y, Aggarwal BB. Flavopiridol inhibits NFkappaB activation induced by various carcinogens and inflammatory agents through inhibition of IkappaBalpha kinase and p65 phosphorylation: abrogation of cyclin D1, cyclooxygenase-2, and matrix metalloprotease-9. J Biol Chem 2004; 279: 4750-9.
  • 106 Reddy KB, Krueger JS, Kondapaka SB. et al. Mitogen- activated protein kinase (MAPK) regulates the expression of progelatinase B (MMP-9) in breast epithelial cells. Int J Cancer 1999; 82: 268-73.
  • 107 Lindenmeyer F, Li H, Menashi S. et al. Apigenin acts on the tumor cell invasion process and regulates protease production. Nutr Cancer 2001; 39: 139-47.
  • 108 Banerji A, Chakrabarti J, Mitra A. et al. Effect of curcumin on gelatinase A (MMP-2) activity in B16F10 melanoma cells. Cancer Lett 2004; 211: 235-42.
  • 109 Philip S, Kundu GC. Osteopontin induces nuclear factor kappa B-mediated promatrix metalloproteinase- 2 activation through I kappa B alpha /IKK signaling pathways, and curcumin (diferulolylmethane) down-regulates these pathways. J Biol Chem 2003; 278: 14487-97.
  • 110 Tate P, God J, Bibb R. et al. Inhibition of metalloproteinase activity by fruit extracts. Cancer Lett 2004; 212: 153-8.
  • 111 Puricelli L, Dell'Aica I, Sartor L. et al. Preliminary evaluation of inhibition of matrix-metalloprotease MMP-2 and MMP-9 by Passiflora edulis and P foetida aqueous extracts. Fitoterapia 2003; 74: 302-4.
  • 112 Peterson JT. Matrix metalloproteinase inhibitor development and the remodeling of drug discovery. Heart Fail Rev 2004; 9: 63-79.
  • 113 Renkiewicz R, Qiu L, Lesch C. et al. Broad-spectrum matrix metalloproteinase inhibitor marimastat-induced musculoskeletal side effects in rats. Arthritis Rheum 2003; 48: 1742-9.
  • 114 Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002; 295: 2387-92.
  • 115 Hishikawa K, Nakaki T, Fujita T. Oral flavonoid supplementation attenuates atherosclerosis development in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 1-5
  • 116 Chyu K-Y, Babbidge SM, Zhao X. et al. Differential effects of green tea-derived catechin on developing versus established atherosclerosis in apolipoprotein E-null mice. Circulation 2004; 109: 2448-53.
  • 117 Mukamal KJ, Maclure M, Muller JE. et al. Tea consumption and mortality after acute myocardial infarction. Circulation 2002; 105: 2476-81.
  • 118 Geleijnse JM, Launer LJ, Hofman A. et al. Tea flavonoids may protect against atherosclerosis: the Rotterdam Study. Arch Intern Med 1999; 159: 2170-4.
  • 119 Rajagopalan S, Meng XP, Ramasamy S. et al. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 1996; 98: 2572-9.
  • 120 Galis ZS, Asanuma K, Godin D. et al. N-acetylcysteine decreases the matrix-degrading capacity of macrophage-derived foam cells: new target for antioxidant therapy?. Circulation 1998; 97: 2445-53.
  • 121 Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003; 3: 768-80.