Pigmented Maize (Zea Mays L.) Contains Anthocyanins with Potential Therapeutic Action Against Oxidative Stress – a Review

Pol. J. Food Nutr. Sci., 2020, Vol. 70, No. 2, pp. 85–99 DOI: 10.31883/pjfns/113272 http://journal.pan.olsztyn.pl Review article Section: Food Quality and Functionality Pigmented Maize (Zea mays L.) Contains Anthocyanins with Potential Therapeutic Action Against Oxidative Stress – A Review Jesús Miguel Magaña-Cerino1, Héctor Arturo Peniche-Pavía2, Axel Tiessen2,3, Carmen Magdalena Gurrola-Díaz1* 1Instituto de Investigación en Enfermedades Crónico Degenerativas, Instituto Transdisciplinar de Investigación e Innovación en Salud, Departamento de Biología Molecular y Genómica, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, C. Sierra Mojada 950, Col. Independencia, C. P. 44350, Guadalajara, Jalisco, México 2Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional Unidad Irapuato, Libramiento Norte Km. 9.6, C. P. 36824, Irapuato Guanajuato, México 3Laboratorio Nacional PlanTECC, Libramiento Norte Km 9.6, C. P. 36824 Irapuato, Guanajuato, México Key words: Zea mays L., anthocyanins, oxidative stress, antioxidant, in vivo and in vitro effect Different maize (Zea mays L.) varieties have been used for thousands of years as a healthy food source in Mesoamerica including pigmented maize. Maize ingestion could contribute to the reduction in the rate of non-communicable diseases and, in turn, to its function as an adjuvant in their management. These diseases are mainly associated with oxidative stress, which is characterized by a redox cell imbalance produced due to pro-oxidant molecules accumulation, inducing irreversible damages. Although the endogenous antioxidant defense system is effi cient, exogenous antioxidants are necessary to help to prevent this damage. Bioactive compounds, like anthocyanins, contained in dietary plants exert a major activity against oxidative stress. Could the maize anthocyanins play a curative, preventive or complementary role in the treatment of chronic diseases? Here, we describe the occurrence of anthocyanins from pigmented maize and their chemical structures. Furthermore, the biosynthesis, bioavailability, and stability are also summarized. Finally, many in vitro and in vivo studies of maize anthocyanins are discussed that demonstrated their nutraceutical potential, antioxidant capacity, and other biological effects. Given the importance of the biological properties of maize anthocyanins, it is necessary to understand the current knowledge and propose further research or clinical studies which allows us to better elucidate the biological mechanism of maize anthocyanins deriva- tives of several varieties and processes of cooking and combination with other ingredients to enhance their nutritional and health benefi ts. INTRODUCTION membranes and tissues), and deoxyribonucleic acid (DNA) [Birben et al., 2012]. Oxidative stress is a condition that begins when the redox Although the endogenous antioxidant defense system balance of living organisms is altered by an excessive forma- is effi cient, sometimes it is overwhelmed and needs exogenous tion of radical molecules, which exceeds the endogenous an- antioxidants. Plant and animal reducing compounds such as tioxidant capacity [Lobo et al., 2010]. Usually, the electron vitamin C, vitamin E, carotenoids (xanthophylls and caro- transport chains in the mitochondria utilize oxygen to convert tenes), anthocyanins, chalcones, isofl avones, tannins, fl avan- nutrients into adenosine triphosphate (ATP) and through this diols, and fl avonols can restore the oxidative balance [Kasote process generate radicals, which are used to carry out cellular et al., 2015]. Several epidemiological studies have demon- signaling processes. However, various environmental, physi- strated that individuals who consumed fruits, vegetables, cal, and chemical factors can cause the excessive generation and whole grains with anthocyanins, were at a lower risk to of these radicals, resulting in the chemical imbalance of bio- develop chronic diseases such as cancer, diabetes, and car- molecules and cellular stress [McCord, 2000]. diovascular disease (CVD) [Pandey & Rizvi, 2009]. Most The main feature of this condition is an increase in free of these benefi cial health effects are attributed to exogenous radicals and reactive species such as hydrogen peroxide antioxidant compounds ingested from plant sources at dif- − − (H2O2), superoxide (O2 ), hydroxyl radical (HO ), singlet ox- ferent concentrations. Anthocyanins are among the bioactive 1 • ygen ( O2), alkoxy radical (RO), and peroxyl radical (ROO ). compounds that stand out for their benefi cial properties [He These compounds cause necrosis, apoptosis, damage, & Giusti, 2010]. and cell death due to modifi cation in the structure and func- Maize is widely distributed and consumed around tion of macromolecules such as lipids, proteins (in biological the world, especially in developing countries. Because of this, some researchers have focused their efforts on the generation of new varieties of pigmented maize through cross-hy- * Corresponding Author: Tel. +52 (33) 10585200 Ext. 33930 E-mail: [email protected] (C.M. Gurrola-Díaz) bridization to obtain new varieties of grains with a greater © Copyright by Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences © 2020 Author(s). This is an open access article licensed under the Creative Commons Attribution-NonCommercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/3.0/). 86 Anthocyanins in Pigmented Maize Against Oxidative Stress antioxidant capacity [Tiessen et al., 2017]. Therefore, such dale, 2014], and bean (Phaseolus) [Takeoka et al., 1997]. improved maize varieties could function as bioactive agents These foods (seeds, fruits, and vegetables) are the main and potential candidates to be included in the prevention source of natural pigments, which providing them unique col- and integral management of chronic degenerative diseases, ors and fl avors and make them attractive for consumption, and in reducing their incidence [Chander et al., 2008]. This and eventually may serve in a complementary natural treat- review aimed to collect data on the effect of anthocyanins ment of chronic diseases. In maize, they accumulate in struc- present in pigmented maize. They were considered regarding tures such as stem, pod, leaves and infl orescences; in the cob, their metabolism, as well as their intervention in the antioxi- they are found in bracts, rachis, and kernels [Cui et al., 2012]. dant and modulating capacity of several cellular processes Chemically, the anthocyanins are polyhydroxy/polymethoxy involved in oxidative stress such as cell growth, cell prolifera- glycosides derived from the anthocyanidins. They are formed tion and cell death. by an anthocyanidin molecule, that is the aglycone, to which a sugar moiety is bound by a β-glycosidic bond or, in some OCCURRENCE OF ANTHOCYANINS AND THEIR cases, by α-glycosidic bond. There are approximately 20 types CHEMICAL STRUCTURES of anthocyanidins in nature, but only six: pelargonidin (Pl), cyanidin (Cy), peonidin (Peo), delphinidin (Dp), petunidin Anthocyanins are responsible for many colors (blue, (Pt) and malvidin (Mv), are widely distributed [Tsuda, 2012]. blue-black, red, and purple) of leaves, fl owers, fruits, seeds, The name of these compounds is derived from the plant roots, and stems. In cereal grain (a kind of single-seed fruit), source from which they were fi rst isolated. The basic chemical the anthocyanins are localized mainly in the cells of pericarp, structure of aglycones is the fl avylium ion, also called 2-phe- testa, and aleurone layer, which depends on many structural nyl-1-benzopyrylium (2-phenylchromenyl; IUPAC). It con- and regulatory genes [Fan et al., 2016; Li et al., 2018]. Several sists of a 15-carbon skeleton (C6-C3-C6) organized into two plant foods contain different concentrations of anthocyanins aromatic groups: benzopyrylium/chromenium, and phenolic including: berries (Morus and Rubus gender), grapes (Vitis), (also known as hydroxycinnamoyl) (see Figure 1). Because plums and cherries (Prunus), red pear (Pyrus), red apple (Ma- of the trivalent character of oxygen, fl avylium typically func- lus), pomegranate (Punica), blackcurrants (Ribes), raspberry tions as a cation (oxonium ion) or fl avylium salt [De Rosso (Rubus), strawberries (Fragaria), chili (Capsicum) [Aza-Gon- et al., 2008]. zalez & Ochoa-Alejo, 2012], camu-camu (Myrciaria dubia) The monosaccharides commonly bound by O-glyco- [Langley et al., 2015], açaí (Euterpe oleracea) [Peixoto et al., sylation to the anthocyanidins, are glucose and rhamnose 2016], cacao (Theobroma) [Chavez-Rivera & Ordoñez-Go- followed by galactose, xylose, arabinose, and occasionally, mez, 2013], and calyces of Hibiscus sabdariffa L. (Jamaica) gentiobiose and raffi nose [Horbowicz et al., 2008; Yonekura- [Gurrola-Diaz et al., 2010], as well as such red radishes, red -Sakakibara et al., 2012; Fang, 2014]. All of them bind to an- peppers, tomatoes, red onions, purple and red-fl eshed po- thocyanidin primarily by the hydroxyl group at the 3-position tatoes (Solanum Tuberosum L.) [Jansen & Flamme, 2006], and secondarily at the 5 or 7-position but can also be found purple cabbage (Brassica oleracea var. capitate), and eggplant at positions 3’, 5’, or 6’, but rarely at the 4’ position. When (Solanum melongena L.) [Sadilova et al., 2006]. Anthocya- two sugars are present in the same molecule, they are located nins are also present in grains such as in the color-varieties in

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