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Pleiotropic Effects of Isoflavones in Inflammation and Chronic

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Pleiotropic Effects of Isoflavones in Inflammation and Chronic International Journal of Molecular Sciences Review Pleiotropic Effects of Isoflavones in Inflammation and Chronic Degenerative Diseases Jurga Bernatoniene 1,2,* , Jurga Andreja Kazlauskaite 2 and Dalia Marija Kopustinskiene 2 1 Department of Drug Technology and Social Pharmacy, Faculty of Pharmacy, Medical Academy, Lithuanian University of Health Sciences, Sukileliu pr. 13, LT-50161 Kaunas, Lithuania 2 Institute of Pharmaceutical Technologies, Faculty of Pharmacy, Medical Academy, Lithuanian University of Health Sciences, Sukileliu pr. 13, LT-50161 Kaunas, Lithuania; [email protected] (J.A.K.); [email protected] (D.M.K.) * Correspondence: [email protected] Abstract: Isoflavones are phytoestrogens of plant origin, mostly found in the members of the Fabaceae family, that exert beneficial effects in various degenerative disorders. Having high similarity to 17-b- estradiol, isoflavones can bind estrogen receptors, scavenge reactive oxygen species, activate various cellular signal transduction pathways and modulate growth and transcription factors, activities of enzymes, cytokines, and genes regulating cell proliferation and apoptosis. Due to their pleiotropic activities isoflavones might be considered as a natural alternative for the treatment of estrogen decrease-related conditions during menopause. This review will focus on the effects of isoflavones on inflammation and chronic degenerative diseases including cancer, metabolic, cardiovascular, neurodegenerative diseases, rheumatoid arthritis and adverse postmenopausal symptoms. Keywords: isoflavones; genistein; daidzein; inflammation; cancer; degenerative diseases Citation: Bernatoniene, J.; Kazlauskaite, J.A.; Kopustinskiene, D.M. Pleiotropic Effects of Isoflavones in Inflammation and Chronic Degenerative Diseases. Int. J. Mol. Sci. 1. Introduction 2021, 22, 5656. https://doi.org/ Isoflavones are polyphenolic plant-derived compounds acting as phytoestrogens due 10.3390/ijms22115656 to their structural similarity to 17-b-estradiol [1]. They are found as secondary plant metabolites in a conjugated form mainly in the members of the Fabaceae family, such as Academic Editors: Tullia Maraldi, soybeans (Glycine max (L.) Merr.), red clover (Trifolium pratense L.), white clover (Trifolium Cristina Angeloni and Cecilia Prata repens L.), alfalfa (Medicago sativa L.), various lupin (Lupinus) species and beans (Phaseolus vulgaris L.). Depending on the endocrine levels of estrogen in an organism, isoflavones can Received: 28 April 2021 act as estrogen agonists (at low concentrations) or antagonists (at high concentrations) [2–4]. Accepted: 25 May 2021 Isoflavones can interact with both estrogen receptors a and b, with a much higher affinity Published: 26 May 2021 for the latter [5], and mimic the action of estrogens on target organs, thereby exerting many health benefits when used in some hormone-dependent diseases [3,5–8]. Publisher’s Note: MDPI stays neutral Isoflavones can alleviate many pathological conditions including cancer, metabolic, with regard to jurisdictional claims in cardiovascular, neurodegenerative diseases, rheumatoid arthritis and adverse menopause published maps and institutional affil- symptoms (Figure1). Recently, various aspects of isoflavones have been overviewed in iations. detail in the following reviews [3,9–13]. Two mechanisms are implicated to be respon- sible for the beneficial effects of isoflavones—the estrogen receptor-mediated signaling pathway [2,7,8] and the modulation of other intracellular signaling pathways, e.g., phos- pholipase C, protein tyrosine kinase and mitogen-activated protein kinase [3,7,14,15]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Int. J. Mol. Sci. 2021, 22, 5656. https://doi.org/10.3390/ijms22115656 https://www.mdpi.com/journal/ijms Int. J. J. Mol. Mol. Sci. Sci. 20212021,, 2222,, xx 5656 FORFOR PEERPEER REVIEWREVIEW 2 of 18 Figure 1. BiologicalBiological activity activity of isoflavones. isoflavones. VEGF VEGF-vascular-vascular endothelial growth factor. 2.2. Chemical Chemical Properties Properties and and Bioavailability Bioavailability of Isoflavones Isoflavones IsoflavonesIsoflavones form form a a group group of of distinct distinct secondary secondary metabolites metabolites produced produced predominately predominately inin leguminous leguminous plants. plants. These These secondary secondary metabolites metabolites are are formed formed by by symbiotic symbiotic relationship relationship with the Rhizobia bacteria and t thehe defense responses of leguminous plant [[16]16]... IsoflavonesIsoflavones Isoflavones areare synthesized as as part part of of the the phenylpropanoid phenylpropanoid pathway, pathway, the same biosynthetic pathway ofof flavonoid flavonoid biosynthesis biosynthesis [17] [17..]. TheThe The structuresstructures structures ofof ofthethe the mainmain main isoflavonesisoflavones isoflavones areareare presentedpresented presented inin in FiFiguregure 22.. FigureFigure 2. MainMain isoflavones isoflavones and and their structural similarity to 17 βb--estradiol.estradiol. Isoflavones contain 12 different isoforms that are divided into four chemical forms Isoflavones contain 12 different isoforms that are divided into four chemical forms (Figure3 and Table1): aglycones, 7- O-glucosides, 6”-O-acetyl-7-O-glucosides and 6”-O- (Figure 3 and Table 1): aglycones, 7-O-glucosides, 6″-O-acetyl-7-O-glucosides and 6″-O- Int. J. Mol. Sci. 2021, 22, 5656 3 of 18 Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 3 of 18 malonyl-7-malonyl-7-OO-glucosides-glucosides [[18]18].. ItIt isis alsoalso possiblepossible forfor anyany conjugatedconjugated isoflavoneisoflavone toto generategenerate thethe aglyconeaglycone formform byby cleavagecleavage ofof thethe glycosidicglycosidic bond.bond. FigureFigure 3.3. Chemical structurestructure ofof isoflavonesisoflavones from from Fabaceae Fabaceae family family plants plants (alfalfa, (alfalfa, red red clover clover and and soy). soy). Some glycosides, including malonyl- and acetyl-isoflavones, are particularly unstable (TableSome1). The glycosides, use of drastic includi temperatures,ng malonyl- pressure and acetyl conditions-isoflavones, and are long particularly extraction timesunsta- may cause the degradation of isoflavonoids conjugates, changing the isoflavone profile. In ble (Table 1). The use of drastic temperatures, pressure conditions and long extraction addition, chemical hydrolysis leads to a marked increase in the concentration of aglycones times may cause the degradation of isoflavonoids conjugates, changing the isoflavone present in the sample at the expense of the glucosides and hence augment the available profile. In addition, chemical hydrolysis leads to a marked increase in the concentration amount of aglycones to be extracted [19,20]. of aglycones present in the sample at the expense of the glucosides and hence augment the available amount of aglycones to be extracted [19,20]. Table 1. Main isoflavone aglycones (genistein, daidzein, glycitein) and their isoforms. Table 1. Main isoflavone aglycones (genistein, daidzein, glycitein) and their isoforms. Compound R1 R2 R3 R4 CompoundGenistein R1 HR H2 OHR3 R H4 GenisteinGenistin CH6O 5H11 HH OHOH H Acetyl-genistin C6O5H11 + COCH3 H OH H Genistin C6O5H11 H OH H Malonyl-genistin C6O5H11 + COCH2COOH H OH H AcetylDaidzein-genistin C6O5H11 + C HOCH3 H H OH H H MalonylDaidzin-genistin C6O5H11 + C COCH6O5H211COOH HHHH OH H Acetyl-daidzinDaidzein C6O5HH11 + COCH3 HHHH H H Malonyl-daidzin C6O5H11 + COCH2COOH H H H Daidzin C6O5H11 H H H Glycitein H OCH3 HH Acetyl-daidzin C6O5H11 + COCH3 H H H Glycitin C6O5H11 OCH3 HH MalonylAcetyl-glycitin-daidzin C6O5H C116 O+ C5HOCH11 + COCH2COOH3 OCHH 3 HHH H Malonyl-glycitinGlycitein C6O5H11 H+ COCH2COOHOCH OCH3 3 HHH H Glycitin C6O5H11 OCH3 H H AcetylIsoflavones-glycitin in glycosideC6O5 formH11 + areCOCH poorly3 absorbedOCH in3 the small intestine,H due toH their higherMalonyl molecular-glycitin weight C6O and5H11hydrophilicity. + COCH2COOH However, OCH gut3 microfloraH plays an importantH role in the bioconversion of isoflavones. Bacteria, mainly Bifidobacterium and Lactobacillus strainsIsoflavones present in in the glycoside gastrointestinal form aretract poorly hydrolyze absorbed isoflavones in the small to intestine, their corresponding due to their bioactivehigher molecular aglycone weight forms and [21, hydrophilicity.22]. Once hydrolyzed, However, aglycone gut microflora forms are plays absorbed an important in the upperrole in gastrointestinalthe bioconversion tract of byisoflavones. a passive diffusionBacteria, [mainly21]. Bifidobacterium and Lactobacillus strainsGenistein present and in the daidzein gastrointestinal (aglycones) tract can hydrolyze be produced isoflavones from their to glucosides their corresponding or from the precursorsbioactive aglycone biochanin forms A and [21,22] formononetin. Once hydrolyzed, by intestinal aglyconeb-glucosidase, forms are these absorbed compounds in the areupper extensively gastrointestinal metabolized tract by in thea passive intestine diffusion and liver [21] [23. ]. After ingestion and hydrolysis, aglyconesGenistein are absorbedand daidzei in then (aglycones) small intestine can be completely produced in from part their or further glucosides metabolized or from intothe precursors other metabolites biochanin (sulfonic A and or
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