Computational and Experimental Progress on the Structure and Chemical Reactivity of Procyanidins: Their Potential as Metalloproteinases Inhibitors

Author(s): Ana María Mendoza-Wilson*, René Renato Balandrán-Quintana.

Journal Name: Current Organic Chemistry

Volume 23 , Issue 13 , 2019

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Graphical Abstract:


Matrix metalloproteinases (MMPs) are enzymes involved in various physiological processes essential for living beings, but the loss of the regulatory control by endogenous inhibitors of MMPs, leads to the development of serious diseases such as cardiovascular system affections, cancer, and metastasis. For these reasons, exogenous inhibitors are required for these enzymes, which are able to control the proteolytic activity and are selective towards the different MMPs, besides properties which, from the pharmacological point of view, are necessary to be effective under physiological conditions. Based on these expectations, some bioactive compounds that are abundant in the human diet, like procyanidins (PCs) have emerged as potential exogenous inhibitors of MMPs. This review presents the advances of experimental and computational investigations carried out to date on the structure and chemical reactivity of PCs, to support the basis of their potential use as MMP inhibitors. For such purpose, specific sites among MMPs identified for a selective inhibition, the role of PCs in the regulation of MMPs by posttranscriptional mechanisms at the level of microRNAs, modulation of reactive oxygen species (ROS), effects on tissue inhibitors of MMPs (TIMPs), the crosslinking of PCs with the extracellular matrix proteins, as well as direct interaction between PCs and MMPs, are discussed. Methods for isolation and synthesis of PCs, as well as hydrophilicity properties, bioavailability, and susceptibility to be metabolized in oral intake, are also addressed. The information gathered in this review could additionally help to visualize future research related to this topic.

Keywords: Metalloproteinases, procyanidins, inhibitors, computational, chemical reactivity, structure.

Nagase, H.; Visse, R.; Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res., 2006, 69(3), 562-573.
[] [PMID: 16405877]
Ammazzalorso, A.; De Filippis, B.; Campestre, C.; Laghezza, A.; Marrone, A.; Amoroso, R.; Tortorella, P.; Agamennone, M. Seeking for non-zinc-binding MMP-2 inhibitors: Synthesis, biological evaluation and molecular modelling studies. Int. J. Mol. Sci., 2016, 17(10), 1768.
[] [PMID: 27782083]
Li, L.; Li, H. Role of microRNA-mediated MMP regulation in the treatment and diagnosis of malignant tumors. Cancer Biol. Ther., 2013, 14(9), 796-805.
[] [PMID: 23917402]
Johnson, L.L.; Pavlovsky, A.G.; Johnson, A.R.; Janowicz, J.A.; Man, C.F.; Ortwine, D.F.; Purchase, C.F., II; White, A.D.; Hupe, D.J. A rationalization of the acidic pH dependence for stromelysin-1 (Matrix metalloproteinase-3) catalysis and inhibition. J. Biol. Chem., 2000, 275(15), 11026-11033.
[] [PMID: 10753905]
Singh, T.; Adekoya, O.A.; Jayaram, B. Understanding the binding of inhibitors of matrix metalloproteinases by molecular docking, quantum mechanical calculations, molecular dynamics simulations, and a MMGBSA/MMBappl study. Mol. Biosyst., 2015, 11(4), 1041-1051.
[] [PMID: 25611160]
Yamamoto, K.; Higashi, S.; Kioi, M.; Tsunezumi, J.; Honke, K.; Miyazaki, K. Binding of active matrilysin to cell surface cholesterol sulfate is essential for its membrane-associated proteolytic action and induction of homotypic cell adhesion. J. Biol. Chem., 2006, 281(14), 9170-9180.
[] [PMID: 16476739]
Jacobsen, J.A.; Major Jourden, J.L.; Miller, M.T.; Cohen, S.M. To bind zinc or not to bind zinc: An examination of innovative approaches to improved metalloproteinase inhibition. Biochim. Biophys. Acta, 2010, 1803(1), 72-94.
[] [PMID: 19712708]
Wang, Y.; Chung, S-J.; Song, W.O.; Chun, O.K. Estimation of daily proanthocyanidin intake and major food sources in the U.S. diet. J. Nutr., 2011, 141(3), 447-452.
[] [PMID: 21270367]
Ou, K.; Gu, L. Absorption and metabolism of proanthocyanidins. J. Funct. Foods, 2014, 7(Suppl. C), 43-53.
Gu, L.; Kelm, M.A.; Hammerstone, J.F.; Beecher, G.; Holden, J.; Haytowitz, D.; Prior, R.L. Screening of foods containing proanthocyanidins and their structural characterization using LC-MS/MS and thiolytic degradation. J. Agric. Food Chem., 2003, 51(25), 7513-7521.
[] [PMID: 14640607]
Szewczyk, K.; Lewandowska, U.; Owczarek, K.; Sosnowska, D.; Gorlach, S.; Koziołkiewicz, M.; Hrabec, Z.; Hrabec, E. Influence of polyphenol extract from evening primrose (oenothera paradoxa) seeds on proliferation of Caco-2 cells and on expression, synthesis and activity of matrix metalloproteinases and their inhibitors. Pol. J. Food Nutr. Sci., 2014, 64(3), 181-191.
Miyake, T.; Yasukawa, K.; Inouye, K. Analysis of the mechanism of inhibition of human matrix metalloproteinase 7 (MMP-7) activity by green tea catechins. Biosci. Biotechnol. Biochem., 2011, 75(8), 1564-1569.
[] [PMID: 21821933]
Mendoza-Wilson, A.; Balandrán-Quintana, R. Prediction of the interactions of distinct procyanidin oligomers with the catalytic domain of the matrix metalloproteinase-7: A molecular modeling study. J. Theor. Comput. Chem., 2017. Under review
Yanagida, A.; Murao, H.; Ohnishi-Kameyama, M.; Yamakawa, Y.; Shoji, A.; Tagashira, M.; Kanda, T.; Shindo, H.; Shibusawa, Y. Retention behavior of oligomeric proanthocyanidins in hydrophilic interaction chromatography. J. Chromatogr. A, 2007, 1143(1-2), 153-161.
[] [PMID: 17223120]
Mendoza-Wilson, A.M.; Carmelo-Luna, F.J.; Astiazarán-García, H.; Pacheco-Moreno, B.I.; Anduro-Corona, I.; Rascón-Durán, M.L. DFT study of the physicochemical properties of A- and B-type procyanidin oligomers. J. Theor. Comput. Chem., 2016, 15(08)1650069
Ardévol, A.; Bladé, C.; Salvadó, M.J.; Arola, L. Changes in lipolysis and hormone-sensitive lipase expression caused by procyanidins in 3T3-L1 adipocytes. Int. J. Obes. Relat. Metab. Disord., 2000, 24(3), 319-324.
[] [PMID: 10757625]
Ugartondo, V.; Mitjans, M.; Touriño, S.; Torres, J.L.; Vinardell, M.P. Comparative antioxidant and cytotoxic effect of procyanidin fractions from grape and pine. Chem. Res. Toxicol., 2007, 20(10), 1543-1548.
[] [PMID: 17824666]
Zhai, W-Y.; Jia, C-P.; Zhao, H.; Xu, Y-S. Procyanidins inhibit tumor angiogenesis by crosslinking extracellular matrix. Chin. J. Cancer Res., 2011, 23(2), 99-106.
[] [PMID: 23483060]
Chen, L.; Yang, Y.; Yuan, P.; Yang, Y.; Chen, K.; Jia, Q.; Li, Y. Immunosuppressive effects of A-type procyanidin oligomers from Cinnamomum tamala. Evid. Based Complement. Alternat. Med., 2014, 2014365258
[] [PMID: 25530780]
Mendoza-Wilson, A.M.; Carmelo-Luna, F.J.; Astiazarán-García, H.; Mata-Haro, V.; Espinosa-Plascencia, A.; Bermúdez-Almada, M.D.C.; Rascón-Durán, M.L. Absorption of dimers, trimers and tetramers of procyanidins present in apple skin by IEC-18 cell monolayers. J. Funct. Foods, 2016, 27(Suppl. C), 386-391.
García-Ramírez, B.; Fernández-Larrea, J.; Salvadó, M.J.; Ardèvol, A.; Arola, L.; Bladé, C. Tetramethylated dimeric procyanidins are detected in rat plasma and liver early after oral administration of synthetic oligomeric procyanidins. J. Agric. Food Chem., 2006, 54(7), 2543-2551.
[] [PMID: 16569041]
Arola-Arnal, A.; Bladé, C. Proanthocyanidins modulate microRNA expression in human HepG2 cells. PLoS One, 2011, 6(10)e25982
[] [PMID: 21998738]
Castell-Auví, A.; Cedó, L.; Movassat, J.; Portha, B.; Sánchez-Cabo, F.; Pallarès, V.; Blay, M.; Pinent, M.; Ardévol, A. Procyanidins modulate microRNA expression in pancreatic islets. J. Agric. Food Chem., 2013, 61(2), 355-363.
[] [PMID: 23215023]
Gonthier, M-P.; Donovan, J.L.; Texier, O.; Felgines, C.; Remesy, C.; Scalbert, A. Metabolism of dietary procyanidins in rats. Free Radic. Biol. Med., 2003, 35(8), 837-844.
[] [PMID: 14556848]
Van’t Slot, G.; Mattern, W.; Rzeppa, S.; Grewe, D.; Humpf, H-U. Complex flavonoids in cocoa: synthesis and degradation by intestinal microbiota. J. Agric. Food Chem., 2010, 58(15), 8879-8886.
[] [PMID: 20614902]
Overall, C.M. Molecular determinants of metalloproteinase substrate specificity: Matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol., 2002, 22(1), 51-86.
[] [PMID: 12353914]
Coronato, S.; Laguens, G.; Di Girolamo, V. [Role of metalloproteinases and their inhibitors in tumors Medicina (B. Aires), 2012, 72(6), 495-502.
[PMID: 23241294]
Pelmenschikov, V.; Siegbahn, P.E. Catalytic mechanism of matrix metalloproteinases: Two-layered ONIOM study. Inorg. Chem., 2002, 41(22), 5659-5666.
[] [PMID: 12401069]
Maskos, K. Crystal structures of MMPs in complex with physiological and pharmacological inhibitors. Biochimie, 2005, 87(3-4), 249-263.
[] [PMID: 15781312]
Gomis-Rüth, F.X.; Botelho, T.O.; Bode, W. A standard orientation for metallopeptidases. Biochim. Biophys. Acta, 2012, 1824(1), 157-163.
[] [PMID: 21558023]
Nicolotti, O.; Miscioscia, T.F.; Leonetti, F.; Muncipinto, G.; Carotti, A. Screening of matrix metalloproteinases available from the protein data bank: insights into biological functions, domain organization, and zinc binding groups. J. Chem. Inf. Model., 2007, 47(6), 2439-2448.
[] [PMID: 17958346]
Velasco, G.; Pendás, A.M.; Fueyo, A.; Knäuper, V.; Murphy, G.; López-Otín, C. Cloning and characterization of human MMP-23, a new matrix metalloproteinase predominantly expressed in reproductive tissues and lacking conserved domains in other family members. J. Biol. Chem., 1999, 274(8), 4570-4576.
[] [PMID: 9988691]
Minond, D.; Lauer-Fields, J.L.; Cudic, M.; Overall, C.M.; Pei, D.; Brew, K.; Visse, R.; Nagase, H.; Fields, G.B. The roles of substrate thermal stability and P2 and P1′ subsite identity on matrix metalloproteinase triple-helical peptidase activity and collagen specificity. J. Biol. Chem., 2006, 281(50), 38302-38313.
[] [PMID: 17065155]
Terp, G.E.; Cruciani, G.; Christensen, I.T.; Jørgensen, F.S. Structural differences of matrix metalloproteinases with potential implications for inhibitor selectivity examined by the GRID/CPCA approach. J. Med. Chem., 2002, 45(13), 2675-2684.
[] [PMID: 12061871]
Whittaker, M.; Floyd, C.D.; Brown, P.; Gearing, A.J. Design and therapeutic application of matrix metalloproteinase inhibitors. Chem. Rev., 1999, 99(9), 2735-2776.
[] [PMID: 11749499]
Matziari, M.; Beau, F.; Cuniasse, P.; Dive, V.; Yiotakis, A. Evaluation of P1′-diversified phosphinic peptides leads to the development of highly selective inhibitors of MMP-11. J. Med. Chem., 2004, 47(2), 325-336.
[] [PMID: 14711305]
Rao, B.G. Recent developments in the design of specific Matrix Metalloproteinase inhibitors aided by structural and computational studies. Curr. Pharm. Des., 2005, 11(3), 295-322.
[] [PMID: 15723627]
Rowsell, S.; Hawtin, P.; Minshull, C.A.; Jepson, H.; Brockbank, S.M.; Barratt, D.G.; Slater, A.M.; McPheat, W.L.; Waterson, D.; Henney, A.M.; Pauptit, R.A. Crystal structure of human MMP9 in complex with a reverse hydroxamate inhibitor. J. Mol. Biol., 2002, 319(1), 173-181.
[] [PMID: 12051944]
Higashi, S.; Oeda, M.; Yamamoto, K.; Miyazaki, K. Identification of amino acid residues of matrix metalloproteinase-7 essential for binding to cholesterol sulfate. J. Biol. Chem., 2008, 283(51), 35735-35744.
[] [PMID: 18955490]
Arnold, L.H.; Butt, L.E.; Prior, S.H.; Read, C.M.; Fields, G.B.; Pickford, A.R. The interface between catalytic and hemopexin domains in matrix metalloproteinase-1 conceals a collagen binding exosite. J. Biol. Chem., 2011, 286(52), 45073-45082.
[] [PMID: 22030392]
Tsukada, H.; Pourmotabbed, T. Unexpected crucial role of residue 272 in substrate specificity of fibroblast collagenase. J. Biol. Chem., 2002, 277(30), 27378-27384.
[] [PMID: 12011042]
Collier, I.E.; Krasnov, P.A.; Strongin, A.Y.; Birkedal-Hansen, H.; Goldberg, G.I. Alanine scanning mutagenesis and functional analysis of the fibronectin-like collagen-binding domain from human 92-kDa type IV collagenase. J. Biol. Chem., 1992, 267(10), 6776-6781.
[PMID: 1313021]
Labarbe, B.; Cheynier, V.; Brossaud, F.; Souquet, J-M.; Moutounet, M. Quantitative fractionation of grape proanthocyanidins according to their degree of polymerization. J. Agric. Food Chem., 1999, 47(7), 2719-2723.
[] [PMID: 10552552]
Saucier, C.; Mirabel, M.; Daviaud, F.; Longieras, A.; Glories, Y. Rapid fractionation of grape seed proanthocyanidins. J. Agric. Food Chem., 2001, 49(12), 5732-5735.
[] [PMID: 11743755]
Boukharta, M.; Girardin, M.; Metche, M. Procyanidines galloylées du sarment de vigne (Vitis vinifera): Séparation et identification par chromatographie liquide haute performance et chromatographie en phase gazeuse. J. Chromatogr. A, 1988, 455, 406-409.
Ohnishi-Kameyama, M.; Yanagida, A.; Kanda, T.; Nagata, T. Identification of catechin oligomers from apple (Malus pumila cv. Fuji) in matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and fast-atom bombardment mass spectrometry. Rapid Commun. Mass Spectrom., 1997, 11(1), 31-36.
[<31:AID-RCM784>3.0.CO;2-T] [PMID: 9050260]
Sun, B.; Leandro, C.; Ricardo da Silva, J.M.; Spranger, I. Separation of grape and wine proanthocyanidins according to their degree of polymerization. J. Agric. Food Chem., 1998, 46(4), 1390-1396.
Yanagida, A.; Kanda, T.; Shoji, T. OhnishiKameyama, M.; Nagata, T. Fractionation of apple procyanidins by size-exclusion chromatography. J. Chromatogr. A, 1999, 855(1), 181-190.
[] [PMID: 10514983]
Kraus, G.A.; Geraskin, I.M. Rapid assembly of the procyanidin a skeleton. Tetrahedron Lett., 2017, 58(49), 4609-4611.
Higashino, Y.; Okamoto, T.; Mori, K.; Kawasaki, T.; Hamada, M.; Nakajima, N.; Saito, A. Regioselective synthesis of procyanidin B6, a 4-6-condensed (+)-catechin dimer, by intramolecular condensation. Molecules, 2018, 23(1), 205.
[] [PMID: 29346322]
Pomilio, A.; Otto, M.; Gerhard, S.; Klaus, W. Zur kenntnis der proanthocyanidine, xxii. Über die konstitution der kondensationsprodukte von phenolen mit flavyliumsalzen. Justus Liebigs Ann. Chem., 1977, 1977(4), 597-601.
He, F.; Pan, Q-H.; Shi, Y.; Duan, C-Q. Chemical synthesis of proanthocyanidins in vitro and their reactions in aging wines. Molecules, 2008, 13(12), 3007-3032.
[] [PMID: 19052525]
Alejo-Armijo, A.; Glibota, N.; Frías, M.P.; Altarejos, J.; Gálvez, A.; Salido, S.; Ortega-Morente, E. Synthesis and evaluation of antimicrobial and antibiofilm properties of A-type procyanidin analogues against resistant bacteria in food. J. Agric. Food Chem., 2018, 66(9), 2151-2158.
[] [PMID: 29464945]
Izzotti, A.; Cartiglia, C.; Steele, V.E.; De Flora, S. MicroRNAs as targets for dietary and pharmacological inhibitors of mutagenesis and carcinogenesis. Mutat. Res., 2012, 751(2), 287-303.
[] [PMID: 22683846]
Fanjul-Fernández, M.; Folgueras, A.R.; Cabrera, S.; López-Otín, C. Matrix metalloproteinases: Evolution, gene regulation and functional analysis in mouse models. Biochim. Biophys. Acta, 2010, 1803(1), 3-19.
[] [PMID: 19631700]
Sun, Q.; Prasad, R.; Rosenthal, E.; Katiyar, S.K. Grape seed proanthocyanidins inhibit the invasiveness of human HNSCC cells by targeting EGFR and reversing the epithelial-to-mesenchymal transition. PLoS One, 2012, 7(1)e31093
[] [PMID: 22299051]
Sternlicht, M.D.; Werb, Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol., 2001, 17, 463-516.
[] [PMID: 11687497]
Kresty, L.A.; Clarke, J.; Ezell, K.; Exum, A.; Howell, A.B.; Guettouche, T. MicroRNA alterations in Barrett’s esophagus, esophageal adenocarcinoma, and esophageal adenocarcinoma cell lines following cranberry extract treatment: Insights for chemoprevention. J. Carcinog., 2011, 10, 34.
[] [PMID: 22279419]
Ma, J.; Fang, B.; Ma, C.; Pang, H.; Zeng, F.; Xia, J. [Proanthocyanidins inhibit pancreatic cancer AsPC-1 cell growth and migration through up-regulation of let-7a Nan Fang Yi Ke Da Xue Xue Bao, 2015, 35(8), 1110-1115.
[PMID: 26277505]
Hoffman, A.; Qadri, B.; Frant, J.; Katz, Y.; Bhusare, S.R.; Breuer, E.; Hadar, R.; Reich, R. Carbamoylphosphonate matrix metalloproteinase inhibitors 6: Cis-2-aminocyclohexylcarbamoylphosphonic acid, a novel orally active antimetastatic matrix metalloproteinase-2 selective inhibitor--synthesis and pharmacodynamic and pharmacokinetic analysis. J. Med. Chem., 2008, 51(5), 1406-1414.
[] [PMID: 18257543]
Bansode, R.R.; Khatiwada, J.R.; Losso, J.N.; Williams, L.L. Targeting microrna in cancer using plant-based proanthocyanidins. Diseases, 2016, 4(2), 21.
[] [PMID: 28933401]
Sela-Passwell, N.; Rosenblum, G.; Shoham, T.; Sagi, I. Structural and functional bases for allosteric control of MMP activities: Can it pave the path for selective inhibition? Biochim. Biophys. Acta, 2010, 1803(1), 29-38.
[] [PMID: 19406173]
Osorio, C.; Cavalla, F.; Paula-Lima, A.; Díaz-Araya, G.; Vernal, R.; Ahumada, P.; Gamonal, J.; Hernández, M.H. 2 O2 activates matrix metalloproteinases through the nuclear factor kappa B pathway and Ca2+ signals in human periodontal fibroblasts. J. Periodontal Res., 2015, 50(6), 798-806.
[] [PMID: 25824649]
Lovett, D.H.; Mahimkar, R.; Raffai, R.L.; Cape, L.; Maklashina, E.; Cecchini, G.; Karliner, J.S. A novel intracellular isoform of matrix metalloproteinase-2 induced by oxidative stress activates innate immunity. PLoS One, 2012, 7(4)e34177
[] [PMID: 22509276]
Deem, T.L.; Cook-Mills, J.M. Vascular cell adhesion molecule 1 (VCAM-1) activation of endothelial cell matrix metalloproteinases: Role of reactive oxygen species. Blood, 2004, 104(8), 2385-2393.
[] [PMID: 15265790]
Rajagopalan, S.; Meng, X.P.; Ramasamy, S.; Harrison, D.G.; Galis, Z.S. 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(11), 2572-2579.
[] [PMID: 8958220]
Henrotin, Y.E.; Bruckner, P.; Pujol, J.P.L. The role of reactive oxygen species in homeostasis and degradation of cartilage. Osteoarthritis Cartilage, 2003, 11(10), 747-755.
[] [PMID: 13129694]
Cheynier, V.; Rigaud, J.; da Silva, J.M.R. Structure of procyanidin oligomers isolated from grape seeds in relation to some of their chemical properties.In: Plant Polyphenols. Basic Life Sciences; Hemingway, R.W., Ed.; Springer: Boston, MA, 1992, Vol. 59, pp. 281-294.
Arteel, G.E.; Sies, H. Protection against peroxynitrite by cocoa polyphenol oligomers. FEBS Lett., 1999, 462(1-2), 167-170.
[] [PMID: 10580113]
Vayalil, P.K.; Mittal, A.; Hara, Y.; Elmets, C.A.; Katiyar, S.K. Green tea polyphenols prevent ultraviolet light-induced oxidative damage and matrix metalloproteinases expression in mouse skin. J. Invest. Dermatol., 2004, 122(6), 1480-1487.
[] [PMID: 15175040]
Woo, Y.J.; Joo, Y.B.; Jung, Y.O.; Ju, J.H.; Cho, M.L.; Oh, H.J.; Jhun, J.Y.; Park, M.K.; Park, J.S.; Kang, C.M.; Sung, M.S.; Park, S.H.; Kim, H.Y.; Min, J.K. Grape seed proanthocyanidin extract ameliorates monosodium iodoacetate-induced osteoarthritis. Exp. Mol. Med., 2011, 43(10), 561-570.
[] [PMID: 21795829]
Edwards, D.R. The Tissue Inhibitors of Metalloproteinases (Timps). In: In: Matrix Metalloproteinase Inhibitors in Cancer Therapy; Clendeninn NA, K., Eds.; Humana: Totowa, NJ. , 2001; p. p. 67-84.
Matchett, M.D.; MacKinnon, S.L.; Sweeney, M.I.; Gottschall-Pass, K.T.; Hurta, R.A. Inhibition of matrix metalloproteinase activity in DU145 human prostate cancer cells by flavonoids from lowbush blueberry (Vaccinium angustifolium): Possible roles for protein kinase C and mitogen-activated protein-kinase-mediated events. J. Nutr. Biochem., 2006, 17(2), 117-125.
[] [PMID: 16111875]
Lewandowska, U.; Owczarek, K.; Szewczyk, K.; Sosnowska, D.; Koziołkiewicz, M.; Hrabec, E. Differentiated impact of procyanidins from evening primrose on human breast cancer cells. Cent. Eur. J. Biol., 2014, 9(6), 647-658.
Iravani, S.; Zolfaghari, B. Pharmaceutical and nutraceutical effects of Pinus pinaster bark extract. Res. Pharm. Sci., 2011, 6(1), 1-11.
[PMID: 22049273]
Fini, L.; Piazzi, G.; Daoud, Y.; Selgrad, M.; Maegawa, S.; Garcia, M.; Fogliano, V.; Romano, M.; Graziani, G.; Vitaglione, P.; Carmack, S.W.; Gasbarrini, A.; Genta, R.M.; Issa, J-P.; Boland, C.R.; Ricciardiello, L. Chemoprevention of intestinal polyps in ApcMin/+ mice fed with western or balanced diets by drinking annurca apple polyphenol extract. Cancer Prev. Res. (Phila.), 2011, 4(6), 907-915.
[] [PMID: 21383028]
Zhai, W.; Chang, J.; Lin, K.; Wang, J.; Zhao, Q.; Sun, X. Crosslinking of decellularized porcine heart valve matrix by procyanidins. Biomaterials, 2006, 27(19), 3684-3690.
[] [PMID: 16513164]
Grimm, T.; Schäfer, A.; Högger, P. Antioxidant activity and inhibition of matrix metalloproteinases by metabolites of maritime pine bark extract (pycnogenol). Free Radic. Biol. Med., 2004, 36(6), 811-822.
[] [PMID: 14990359]
Fini, M.; Cook, J.; Mohan, R.; Brinckerhoff, C. Regulation of Matrix Metalloproteinase Gene Expression.In: Matrix Metalloproteinases; Parks, W.M.R.P., Ed.; Academic: New York, 1998, pp. 299-356.
Sternlicht, M.; Werb, Z. Ecm Proteinases.In: Guidebook To The Extracellular Matrix, Anchor And Adhesion Proteins; Kreis, T.V.R., Ed.; Oxford Univ. Press: Oxford, UK, 1999, pp. 503-562.
Uría, J.A.; Jiménez, M.G.; Balbín, M.; Freije, J.M.P.; López-Otín, C. Differential effects of transforming growth factor-β on the expression of collagenase-1 and collagenase-3 in human fibroblasts. J. Biol. Chem., 1998, 273(16), 9769-9777.
[] [PMID: 9545314]
Mudgett, J.S.; Hutchinson, N.I.; Chartrain, N.A.; Forsyth, A.J.; McDonnell, J.; Singer, I.I.; Bayne, E.K.; Flanagan, J.; Kawka, D.; Shen, C.F.; Stevens, K.; Chen, H.; Trumbauer, M.; Visco, D.M. Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis Rheum., 1998, 41(1), 110-121.
[<110:AID-ART14>3.0.CO;2-G] [PMID: 9433876]
Hamano, Y.; Zeisberg, M.; Sugimoto, H.; Lively, J.C.; Maeshima, Y.; Yang, C.; Hynes, R.O.; Werb, Z.; Sudhakar, A.; Kalluri, R. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell, 2003, 3(6), 589-601.
[] [PMID: 12842087]
Demeule, M.; Brossard, M.; Pagé, M.; Gingras, D.; Béliveau, R. Matrix metalloproteinase inhibition by green tea catechins. Biochim. Biophys. Acta, 2000, 1478(1), 51-60.
[] [PMID: 10719174]
La, V.D.; Howell, A.B.; Grenier, D. Cranberry proanthocyanidins inhibit MMP production and activity. J. Dent. Res., 2009, 88(7), 627-632.
[] [PMID: 19641150]
Moon, H-I.; Kim, T-I.; Cho, H-S.; Kim, E.K. Identification of potential and selective collagenase, gelatinase inhibitors from Crataegus pinnatifida. Bioorg. Med. Chem. Lett., 2010, 20(3), 991-993.
[] [PMID: 20053563]
Strek, M.; Gorlach, S.; Podsedek, A.; Sosnowska, D.; Koziolkiewicz, M.; Hrabec, Z.; Hrabec, E. Procyanidin oligomers from Japanese quince (Chaenomeles japonica) fruit inhibit activity of MMP-2 and MMP-9 metalloproteinases. J. Agric. Food Chem., 2007, 55(16), 6447-6452.
[] [PMID: 17616210]
Matchett, M.D.; MacKinnon, S.L.; Sweeney, M.I.; Gottschall-Pass, K.T.; Hurta, R.A.R. Blueberry flavonoids inhibit matrix metalloproteinase activity in DU145 human prostate cancer cells. Biochem. Cell Biol., 2005, 83(5), 637-643.
[] [PMID: 16234852]
Lee, K.W.; Kang, N.J.; Oak, M.H.; Hwang, M.K.; Kim, J.H.; Schini-Kerth, V.B.; Lee, H.J. Cocoa procyanidins inhibit expression and activation of MMP-2 in vascular smooth muscle cells by direct inhibition of MEK and MT1-MMP activities. Cardiovasc. Res., 2008, 79(1), 34-41.
[] [PMID: 18310679]
Atale, N. Effect of Syzygium Cumini in Glucose Induced Cardiac Stress, PhD Thesis, Jaypee Institute of Information Technology: Noida, India. 2016.
Scafuri, B.; Marabotti, A.; Carbone, V.; Minasi, P.; Dotolo, S.; Facchiano, A. A theoretical study on predicted protein targets of apple polyphenols and possible mechanisms of chemoprevention in colorectal cancer. Sci. Rep., 2016, 6, 32516.
[] [PMID: 27587238]
Domínguez-Rosas, E. Estudio computacional de interacciones moleculares de la procianidina B1 con las metaloproteinasas de matriz MMP-1, MMP-2 y MMP-7;, MSc Thesis, Centro de Investigación en Alimentación y Desarrollo, A.C.: Hermosillo, Son., México. 2017.
Achurra, P. Investigating Protein-Polymer Interactions On A Microfluidic Platform, PhD, Stanford University: Stanford. 2006.
Verstraeten, S.V.; Jaggers, G.K.; Fraga, C.G.; Oteiza, P.I. Procyanidins can interact with Caco-2 cell membrane lipid rafts: Involvement of cholesterol. Biochim. Biophys. Acta, 2013, 1828(11), 2646-2653.
[] [PMID: 23899501]
Fraga, C.G.; Galleano, M.; Verstraeten, S.V.; Oteiza, P.I. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol. Aspects Med., 2010, 31(6), 435-445.
[] [PMID: 20854840]
Soares, S.; Brandao, E.; Mateus, N.; de Freitas, V. Interaction between red wine procyanidins and salivary proteins: Effect of stomach digestion on the resulting complexes. RSC Advances, 2015, 5(17), 12664-12670.
Ginjom, I. Health Aspects of Wine Antioxidants: Composition and In Vitro Bioavailability; PhD, The University of Queensland: Brisbane. , 2009.
Freitas, V.D.; Mateus, N. Nephelometric study of salivary protein–tannin aggregates. J. Sci. Food Agric., 2002, 82(1), 113-119.
Baba, S.; Osakabe, N.; Natsume, M.; Terao, J. Absorption and urinary excretion of procyanidin B2 [epicatechin-(4β-8)-epicatechin] in rats. Free Radic. Biol. Med., 2002, 33(1), 142-148.
[] [PMID: 12086692]
Rios, L.Y.; Bennett, R.N.; Lazarus, S.A.; Rémésy, C.; Scalbert, A.; Williamson, G. Cocoa procyanidins are stable during gastric transit in humans. Am. J. Clin. Nutr., 2002, 76(5), 1106-1110.
[] [PMID: 12399286]
Ottaviani, J.I.; Kwik-Uribe, C.; Keen, C.L.; Schroeter, H. Intake of dietary procyanidins does not contribute to the pool of circulating flavanols in humans. Am. J. Clin. Nutr., 2012, 95(4), 851-858.
[] [PMID: 22378733]
Gu, L.; House, S.E.; Rooney, L.; Prior, R.L. Sorghum bran in the diet dose dependently increased the excretion of catechins and microbial-derived phenolic acids in female rats. J. Agric. Food Chem., 2007, 55(13), 5326-5334.
[] [PMID: 17536823]
Tsang, C.; Auger, C.; Mullen, W.; Bornet, A.; Rouanet, J-M.; Crozier, A.; Teissedre, P-L. The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br. J. Nutr., 2005, 94(2), 170-181.
[] [PMID: 16115350]
Deprez, S.; Mila, I.; Huneau, J-F.; Tome, D.; Scalbert, A. Transport of proanthocyanidin dimer, trimer, and polymer across monolayers of human intestinal epithelial Caco-2 cells. Antioxid. Redox Signal., 2001, 3(6), 957-967.
[] [PMID: 11813991]
Appeldoorn, M.M.; Vincken, J-P.; Gruppen, H.; Hollman, P.C.H. Procyanidin dimers A1, A2, and B2 are absorbed without conjugation or methylation from the small intestine of rats. J. Nutr., 2009, 139(8), 1469-1473.
[] [PMID: 19494022]
Ou, K.; Percival, S.S.; Zou, T.; Khoo, C.; Gu, L. Transport of cranberry A-type procyanidin dimers, trimers, and tetramers across monolayers of human intestinal epithelial Caco-2 cells. J. Agric. Food Chem., 2012, 60(6), 1390-1396.
[] [PMID: 22263899]
Shoji, T.; Masumoto, S.; Moriichi, N.; Akiyama, H.; Kanda, T.; Ohtake, Y.; Goda, Y. Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. J. Agric. Food Chem., 2006, 54(3), 884-892.
[] [PMID: 16448199]
Zumdick, S.; Deters, A.; Hensel, A. In vitro intestinal transport of oligomeric procyanidins (DP 2 to 4) across monolayers of Caco-2 cells. Fitoterapia, 2012, 83(7), 1210-1217.
[] [PMID: 22776719]
Galleano, M.; Verstraeten, S.V.; Oteiza, P.I.; Fraga, C.G. Antioxidant actions of flavonoids: Thermodynamic and kinetic analysis. Arch. Biochem. Biophys., 2010, 501(1), 23-30.
[] [PMID: 20388486]
Lu, H.; Meng, X.; Li, C.; Sang, S.; Patten, C.; Sheng, S.; Hong, J.; Bai, N.; Winnik, B.; Ho, C-T.; Yang, C.S. Glucuronides of tea catechins: Enzymology of biosynthesis and biological activities. Drug Metab. Dispos., 2003, 31(4), 452-461.
[] [PMID: 12642472]
Epriliati, I.; Ginjom, I.R. Bioavailability of Phytochemicals.Phytochemicals - A Global Perspective of Their Role in Nutrition and Health; Rao, Janeza Trdine: Rijeka, Croatia, 2012.
Spencer, J.P.E.; Schroeter, H.; Shenoy, B.; Srai, S.K.; Debnam, E.S.; Rice-Evans, C. Epicatechin is the primary bioavailable form of the procyanidin dimers B2 and B5 after transfer across the small intestine. Biochem. Biophys. Res. Commun, 2001, 285(3), 588-593.
[] [PMID: 11453632]
Serra, A.; Macià, A.; Romero, M-P.; Valls, J.; Bladé, C.; Arola, L.; Motilva, M-J. Bioavailability of procyanidin dimers and trimers and matrix food effects in in vitro and in vivo models. Br. J. Nutr, 2010, 103(7), 944-952.
[] [PMID: 20003617]
Holt, R.R.; Lazarus, S.A.; Sullards, M.C.; Zhu, Q.Y.; Schramm, D.D.; Hammerstone, J.F.; Fraga, C.G.; Schmitz, H.H.; Keen, C.L. Procyanidin dimer B2 [epicatechin-(4β-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am. J. Clin. Nutr, 2002, 76(4), 798-804.
[] [PMID: 12324293]
Sano, A.; Yamakoshi, J.; Tokutake, S.; Tobe, K.; Kubota, Y.; Kikuchi, M. Procyanidin B1 is detected in human serum after intake of proanthocyanidinrich grape seed extract. Biosci. Biotechnol. Biochem, 2003, 67(5), 1140- 1143.
[] [PMID: 12834296]
Déprez, S.; Brezillon, C.; Rabot, S.; Philippe, C.; Mila, I.; Lapierre, C.; Scalbert, A. Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J. Nutr., 2000, 130(11), 2733-2738.
[] [PMID: 11053514]
Stoupi, S.; Williamson, G.; Viton, F.; Barron, D.; King, L.J.; Brown, J.E.; Clifford, M.N. In vivo bioavailability, absorption, excretion, and pharmacokinetics of [14C]procyanidin B2 in male rats. Drug Metab. Dispos., 2010, 38(2), 287-291.
[] [PMID: 19910517]
Baselga-Escudero, L.; Blade, C.; Ribas-Latre, A.; Casanova, E.; Suárez, M.; Torres, J.L.; Salvadó, M.J.; Arola, L.; Arola-Arnal, A. Resveratrol and EGCG bind directly and distinctively to miR-33a and miR-122 and modulate divergently their levels in hepatic cells. Nucleic Acids Res., 2014, 42(2), 882-892.
[] [PMID: 24165878]
Abba, M.; Patil, N.; Allgayer, H. Micrornas in the regulation of mmps and metastasis. Cancers (Basel), 2014, 6(2), 625-645.
[] [PMID: 24670365]
Tyrakowska, B.; Lemańska, K.; Szymusiak, H.; Borkowski, T.; Rietjens, I.M.C.M. Modified TEAC test for determination of the antioxidant properties of dietary polyphenolic compounds over a wide pH range. Pol. J. Food Nutr. Sci, 2003, 12/53(SI 2), 141-148.
Leopoldini, M.; Marino, T.; Russo, N.; Toscano, M. Antioxidant properties of phenolic compounds: H-atom versus electron transfer mechanism. J. Phys. Chem. A, 2004, 108(22), 4916-4922.
Amić, D.; Lucić, B. Reliability of bond dissociation enthalpy calculated by the PM6 method and experimental TEAC values in antiradical QSAR of flavonoids. Bioorg. Med. Chem., 2010, 18(1), 28-35.
[] [PMID: 19944611]
Mendoza-Wilson, A.M.; Sotelo-Mundo, R.R.; Balandrán-Quintana, R.R.; Glossman-Mitnik, D.; Sántiz-Gómez, M.A.; García-Orozco, K.D. Exploration of the kinetic and thermochemical abilities for the free radical scavenging of two quercetin conformers. J. Mol. Struct., 2010, 981(1), 187-193.
Saint-Cricq De Gaulejac, N.; Provost, C.; Vivas, N. Comparative study of polyphenol scavenging activities assessed by different methods. J. Agric. Food Chem., 1999, 47(2), 425-431.
[] [PMID: 10563911]
Mendoza-Wilson, A.M.; Armenta-Vázquez, M.E.; Castro-Arredondo, S.I.; Espinosa-Plascencia, A.; Robles-Burgueño, M.D.R.; González-Ríos, H.; González-León, A.; Balandrán-Quintana, R.R. Potential of polyphenols from an aqueous extract of apple peel as inhibitors of free radicals: An experimental and computational study. J. Mol. Struct., 2013, 1035(Suppl. C), 61-68.
Mendoza-Wilson, A.M.; Castro-Arredondo, S.I.; Balandrán-Quintana, R.R. Computational study of the structure-free radical scavenging relationship of procyanidins. Food Chem., 2014, 161(Suppl. C), 155-161.
[] [PMID: 24837934]
Vennat, B.; Bos, M.A.; Pourrat, A.; Bastide, P. Procyanidins from tormentil: Fractionation and study of the anti-radical activity towards superoxide anion. Biol. Pharm. Bull., 1994, 17(12), 1613-1615.
[] [PMID: 7735205]
Appeldoorn, M.M. Dietary a-and b-type procyanidins: Characterization and biofunctional potential of an abundant and diverse group of phenolics, PhD Thesis, Wageningen Universiteit. 2009.
Da Silva, J.M.R.; Darmon, N.; Fernandez, Y.; Mitjavila, S. Oxygen free radical scavenger capacity in aqueous models of different procyanidins from grape seeds. J. Agric. Food Chem., 1991, 39(9), 1549-1552.
Glories, Y.; Laguerre, M.; Laguerre, M.; de Freitas, V.A. Incidence of molecular structure in oxidation of grape seed procyanidins. J. Agric. Food Chem., 1998, 46(2), 376-382.
[] [PMID: 10554249]
Mendoza-Wilson, A.M.; Balandrán-Quintana, R.R. Effect of constituent units, type of interflavan bond, and conformation on the antioxidant properties of procyanidin dimers: A computational outlook. J. Chem. (Hindawi. Online), 2017, 2017, 11.
Tarascou, I.; Ducasse, M-A.; Dufourc, E.J.; Moskau, D.; Fouquet, E.; Laguerre, M.; Pianet, I. Structural and conformational analysis of two native procyanidin trimers. Magn. Reson. Chem., 2007, 45(2), 157-166.
[] [PMID: 17167811]
Lobayan, R.M.; Bentz, E.N.; Jubert, A.H.; Pomilio, A.B. Charge delocalization in Z-isomers of (4α→6″, 2α→o→1″)-phenylflavans with R=H, OH and OCH3. Effects on bond dissociation enthalpies and ionization potentials. Comput. Theor. Chem., 2013, 1006, 37-46.
Bentz, E.N.; Pomilio, A.B.; Lobayan, R.M. Structure and electronic properties of (+)-catechin: Aqueous solvent effects. J. Mol. Model., 2014, 20(2), 2105.
[] [PMID: 24526380]
Bentz, E.N.; Pomilio, A.B.; Lobayan, R.M. Donor-acceptor interactions as descriptors of the free radical scavenging ability of flavans and catechin. Comput. Theor. Chem., 2017, 1110, 14-24.
Mercader, A.G.; Pomilio, A.B. (Iso)flav(an)ones, chalcones, catechins, and theaflavins as anticarcinogens: Mechanisms, anti-multidrug resistance and QSAR studies. Curr. Med. Chem., 2012, 19(25), 4324-4347.
[] [PMID: 22830339]
Pomilio, A.B.; Mercader, A.G. Natural Acylated Anthocyanins and Other Related Flavonoids: Structure Elucidation of Ipomoea Cairica Compounds and QSAR Studies Including Multidrug Resistance In: In: Studies in Natural Products Chemistry; Atta ur R., Ed.; Elsevier. , 2018; p. 55, p. 293-322.
Manka, S.W.; Carafoli, F.; Visse, R.; Bihan, D.; Raynal, N.; Farndale, R.W.; Murphy, G.; Enghild, J.J.; Hohenester, E.; Nagase, H. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Natl. Acad. Sci. USA, 2012, 109(31), 12461-12466.
[] [PMID: 22761315]
Tallant, C.; Marrero, A.; Gomis-Rüth, F.X. Matrix metalloproteinases: Fold and function of their catalytic domains. Biochim. Biophys. Acta, 2010, 1803(1), 20-28.
[] [PMID: 19374923]
Tauro, M.; Laghezza, A.; Loiodice, F.; Piemontese, L.; Caradonna, A.; Capelli, D.; Montanari, R.; Pochetti, G.; Di Pizio, A.; Agamennone, M.; Campestre, C.; Tortorella, P. Catechol-based matrix metalloproteinase inhibitors with additional antioxidative activity. J. Enzyme Inhib. Med. Chem, 2016, 31(sup4), 25-37.
Johnson, A.R.; Pavlovsky, A.G.; Ortwine, D.F.; Prior, F.; Man, C-F.; Bornemeier, D.A.; Banotai, C.A.; Mueller, W.T.; McConnell, P.; Yan, C.; Baragi, V.; Lesch, C.; Roark, W.H.; Wilson, M.; Datta, K.; Guzman, R.; Han, H-K.; Dyer, R.D. Discovery and characterization of a novel inhibitor of matrix metalloprotease-13 that reduces cartilage damage in vivo without joint fibroplasia side effects. J. Biol. Chem., 2007, 282(38), 27781-27791.
[] [PMID: 17623656]

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Year: 2019
Page: [1403 - 1420]
Pages: 18
DOI: 10.2174/1385272822666180828114021
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