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Overview of the Anticancer Profile of Avenanthramides From International Journal of Molecular Sciences Review Overview of the Anticancer Profile of Avenanthramides from Oat Eleonora Turrini , Francesca Maffei, Andrea Milelli , Cinzia Calcabrini and Carmela Fimognari * Department for Life Quality Studies, Alma Mater Studiorum-Università di Bologna, Corso d’Augusto 237, 47921 Rimini, Italy; [email protected] (E.T.); francesca.maff[email protected] (F.M.); [email protected] (A.M.); [email protected] (C.C.) * Correspondence: carmela.fi[email protected]; Tel.: +39-0541-434-658 Received: 12 August 2019; Accepted: 10 September 2019; Published: 13 September 2019 Abstract: Cancer represents one of the leading causes of death worldwide. Progresses in treatment of cancer have continued at a rapid pace. However, undesirable side effects and drug resistance remain major challenges for therapeutic success. Natural products represent a valuable starting point to develop new anticancer strategies. Polyphenols, well-known as antioxidant, exert anticancer effects through the modulation of multiple pathways and mechanisms. Oat (Avena sativa L., Poaceae) is a unique source of avenanthramides (AVAs), a group of polyphenolic alkaloids, considered as its signature compounds. The present review aims to offer a comprehensive and critical perspective on the chemopreventive and chemotherapeutic potential of AVAs. AVAs prevent cancer mainly by blocking reactive species. Moreover, they exhibit potential therapeutic activity through the modulation of different pathways including the activation of apoptosis and senescence, the block of cell proliferation, and the inhibition of epithelial mesenchymal transition and metastatization. AVAs are promising chemopreventive and anticancer phytochemicals, which need further clinical trials and toxicological studies to define their efficacy in preventing and reducing the burden of cancer diseases. Keywords: oat; avenanthramides; cancer therapy; cancer chemoprevention; anticancer mechanisms; pharmacokinetics; toxicological profile 1. Introduction Fiber-rich and unrefined food has been found to decrease the risk of several chronic diseases, including cancer [1,2]. Cancer is the second cause of mortality all over the world [3]. Although the availability of many chemotherapeutic agents, toxicity and chemoresistance are common problems compromising their clinical effectiveness [4]. Natural products represent a valuable starting point to develop new anticancer strategies [5–7]. The ability of natural products to synergistically interact with multiple cellular targets can help counteracting the complexity of cancer pathogenesis. Moreover, natural compounds are usually characterized by a better safety profile, compared to traditional chemotherapeutic drugs [8]. Oat (Avena sativa L., Poaceae) is an annual 1.5-m-high grass widely cultivated in cool and moist region of Northern Europe and North America [9]. After removal of the inedible outer hull, the remaining oat groats are processed to obtain oatmeal, naturally containing oat bran. Oat is mainly eaten as porridge, breakfast cereals, and baked goods (oatcakes, oat cookies, and oat bread). Initially, the interest in whole grain oat was mainly due to its advantageous macronutrient composition including lipids with a high degree of unsaturation and fibers with high content of β-glucans [10]. Then, scientific evidence has shown that oat contains other important bioactive compounds, such as polyphenols, which share with fibers a protective effect against the development of chronic degenerative diseases, including cancer [11]. In particular, besides phenolic acids and flavonoids, oat is a unique source of Int. J. Mol. Sci. 2019, 20, 4536; doi:10.3390/ijms20184536 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 26 degenerative diseases, including cancer [11]. In particular, besides phenolic acids and flavonoids, oat is a unique source of avenanthramides (AVAs), a group of phenolic alkaloids considered its signature Int. J. Mol. Sci. 2019, 20, 4536 2 of 23 compounds. AVAs were firstly isolated by Collins and colleagues [12] and represent the major alcohol-soluble phenolic antioxidants in oat. In the plant, they act as key phytoalexins against plant avenanthramidespathogens. AVAs (AVAs),are constitutively a group of expressed phenolic alkaloidsin the hulls, considered groats, bran, its signature and outer compounds. layers of the AVAs oat werekernel firstly [12,13]. isolated by Collins and colleagues [12] and represent the major alcohol-soluble phenolic antioxidantsAVAs modulate in oat. In multiple the plant, biological they act events, as key phytoalexinsresulting in anti-inflammatory, against plant pathogens. anti-itching, AVAs and are constitutivelyimmunomodulatory expressed effects in the [14]. hulls, Different groats, bran,studies and indicate outer layers that AVAs of the oatalso kernel exert [antioxidant12,13]. and antiproliferativeAVAs modulate effects, multiple which help biological preventing events, or resultingtreating cancer in anti-inflammatory, [10,15]. anti-itching, and immunomodulatoryThe aim of the present effects [review14]. Di isff erentto provide studies a cr indicateitical overview that AVAs of the also cancer exert chemopreventive antioxidant and antiproliferativeand chemotherapeutic effects, activity which helpof AVAs, preventing as single or treatingmolecules cancer or oat [10 preparations.,15]. Emphasis is placed on theThe mechanisms aim of the present triggered review by these is to provide phytochemicals a critical overviewto counteract of the cancer cancer pathogenesis. chemopreventive Besides, and chemotherapeuticthe review highlights activity the ofepidemiological AVAs, as single studies molecules investigating or oat preparations. the preventive Emphasis role of is oat placed dietary on theintake mechanisms on cancer triggeredrisk. by these phytochemicals to counteract cancer pathogenesis. Besides, the review highlights the epidemiological studies investigating the preventive role of oat dietary intake on cancer2. Chemical risk. Structure of AVAs and Their Derivatives 2. ChemicalStructurally, Structure AVAs of are AVAs substituted and Their N-cinnamoyl Derivatives anthranilic acids composed of the combination of two fragments: the left side of the molecule derives from anthranilic acid and the right side derives fromStructurally, cinnamic acid AVAs (Figure are substituted1A). Based onN-cinnamoyl this particular anthranilic structure acids and composedon the substitution of the combination patterns, a ofsystematic two fragments: nomenclature the left has side been of thedeveloped molecule asso derivesciating from letters anthranilic and numbers acid to and each the substituent right side derives[16,17]. The from three cinnamic main acidcinnamic (Figure acid1A). derivatives Based on are this caffeic particular acid, structureindicated andwithon the the letter substitution (c), ferulic patterns,acid (f), and a systematic p-coumaric nomenclature acid (p) (Figure has been1B). The developed five differently associating substituted letters and anthranilic numbers acids to each are substituentanthranilic [acid,16,17 indicated]. The three as main(1), 5-hydroxyanthran cinnamic acid derivativesilic acid (2), are 5-hydroxy-4-methoxyanthranic caffeic acid, indicated with the letter acid (c),(3), ferulic4-hydroxyanthranic acid (f), and p-coumaric acid (4), 4,5-dihydroxyanthranic acid (p) (Figure1B). The fiveacid di (5)ff erently(Figure substituted1B). anthranilic acids are anthranilicAmong the acid, 25 AVAs indicated congeners as (1), 5-hydroxyanthranilicfound in oat, 2c, 2f and acid 2p (2), (Figure 5-hydroxy-4-methoxyanthranic 1C) are the most abundant acidand (3),better 4-hydroxyanthranic characterized for their acid (4),biological 4,5-dihydroxyanthranic profiles. acid (5) (Figure1B). FigureFigure 1.1.( A(A) General) General structure structure of avenanthramides of avenanthramides (AVAs). (AVAs). (B) Derivatives (B) Derivatives of cinnamic of andcinnamic anthranilic and acidsanthranilic find in acids AVAs find and in respective AVAs and nomenclature. respective nomenclature. (C) Most abundant (C) Most AVAs. abundant AVAs. AmongConsidering the 25 the AVAs wide congeners range of foundpotential in oat, therapeu 2c, 2f andtic applications 2p (Figure1C) of areAVAs, the mostgenetic abundant engineering and betterstrategies characterized as alternative for theirto conventional biologicalprofiles. chemical synthesis were developed to help AVAs production on anConsidering industrial scale. the wide [18]. range For ofinstance, potential AVAs therapeutic can be applicationsproduced through of AVAs, genetically genetic engineering engineered strategies as alternative to conventional chemical synthesis were developed to help AVAs production on an industrial scale. [18]. For instance, AVAs can be produced through genetically Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 3 of 26 microorganisms, including Saccharomyces cerevisiae and Escherichia coli. Two novel yeast-derived Int. J. Mol. Sci. 2019, 20, 4536 3 of 23 recombinantInt. J. Mol. Sci. 2019 AVAs, 20, x [i.e.,FOR PEERN-(4 ′REVIEW-hydroxycinnamoyl)-3-hydroxyanthranilic acid (YAvn I) and N-(33 of′-4 26′- dihydroxycinnamoyl)-3-hydroxyanthranilic acid (YAvn II)] have been produced by introducing two microorganisms, including Saccharomyces cerevisiae and Escherichia coli. Two novel yeast-derived engineeredplant genes, microorganisms,4cl-2 from tobacco including and hct fromSaccharomyces globe artichoke, cerevisiae in Saccharomycesand Escherichia cerevisiae
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