Biopeptides from vegetable proteins: new scientific evidences

Biopeptides from vegetable proteins: new scientific evidences

Available online at www.sciencedirect.com ScienceDirect Biopeptides from vegetable proteins: new scientific evidences Domenico Montesano1,3, Monica G...

327KB Sizes 0 Downloads 24 Views

Available online at www.sciencedirect.com

ScienceDirect Biopeptides from vegetable proteins: new scientific evidences Domenico Montesano1,3, Monica Gallo2,3, Francesca Blasi1 and Lina Cossignani1 In the last few decades, the search for new bioactive compounds able to fight several chronic degenerative diseases has increased. In this context, natural sources are especially appealing. Among these new products, peptides are included, for the promising bioactivities and potential applications. In fact, bioactive peptides represent specific sequences of amino acids with numerous health effects so they can be used for the formulation of new drugs, nutraceuticals and ingredients for functional foods. They can be obtained from different protein sources both of animal (milk, derivatives and eggs, meat, fish and even insects) and of vegetable origin (soy, wheat, corn, rice, barley, potatoes, algae). In particular, here it is shown an overview of recent data on some bioactive peptides of plant origin. Addresses 1 Department of Pharmaceutical Sciences, Section of Food Science and Nutrition, University of Perugia, via San Costanzo 1, 06126 Perugia, Italy 2 Department of Molecular Medicine and Medical Biotechnology, University of Naples Federico II, via Pansini 5, 80131 Naples, Italy Corresponding author: Gallo, Monica ([email protected]) These authors contributed equally to this work.

3

Current Opinion in Food Science 2020, 31:31–37 This review comes from a themed issue on Food bioprocessing Edited by Gabriele Rocchetti

https://doi.org/10.1016/j.cofs.2019.10.008 2214-7993/ã 2019 Elsevier Ltd. All rights reserved.

Introduction The relationship between diet and diseases is the subject of great attention by researchers, as confirmed by several studies published every year on the most authoritative scientific journals. In this context, a research field of great interest concerns food proteins and their nutritional quality [1]. Obtaining bioactive compounds, such as biopeptides, requires extraction from the matrix in which they are contained and their subsequent analysis. On the other hand, there is no valid extraction and/or analysis method for all the compounds, but the choice depends on the objectives of the study, the samples and the target compounds. Currently, traditional extraction methods such as the maceration and extraction of Soxhlet are accompanied by more modern www.sciencedirect.com

methods, such as microwave-assisted extraction (MAE), ultrasound-assisted extraction (UAE), supercritical fluid extraction (SFE) and rapid solid-liquid dynamic extraction (RSLDE) [2], in which the various advances aim to increase the yield, to reduce the costs and the environmental impact. Furthermore, modifications to the extraction and analysis methods are continuously developed [3]. As is known, the biological value of proteins is defined by the type of amino acids contained in them. In this regards, foods of animal origin such as meat, fish, eggs and dairy products are considered a source of high quality proteins, even if also some plant foods stand out for the content of essential amino acids, such as amaranth, quinoa, buckwheat [4]. On the other hand, an important factor determining the nutritional quality of food proteins is the potential regulatory activity of the bioactive peptides contained in the amino acid sequence. In fact, recent studies have shown that some peptides contained within the primary sequence of proteins, released by in vitro enzymatic hydrolysis during food production processes or during in vivo digestion, can exert important biological functions [5,6], as they can bind to receptors belonging to cells implicated in specific metabolic processes. Depending on the sequence of amino acids, these peptides can exhibit immunomodulatory, antimicrobial, antioxidant, antithrombotic, hypocholesterolemic, and antihypertensive actions [7]. The numerous evidences on the beneficial effects of bioactive peptides have greatly increased the interest in these molecules in recent years; not only their bioavailability and the biological effects are studied, but their applicability and large-scale production in the food industry are also assessed [8]. In fact, the integration of these components into foods could lead to significant advances in the production of so-called ‘functional foods’, that have a beneficial influence on one or more functions of the organism [9]. As shown by recent literature, vegetable sources of bioactive peptides are increasingly considered and now represent an important starting point for obtaining these precious compounds [10,11]. Moreover, the need to implement efficient and economically viable strategies for production on an industrial scale must be taken into Current Opinion in Food Science 2020, 31:31–37

32 Food bioprocessing

account. In this review, alternative protein sources for the production of bioactive peptides are considered, as well as the relative biological and pharmacological effects also with a view to using these peptides as new nutraceutical products. In particular, a section is dedicated to alternative lowcost sources, for example derived from by-products and waste of agro-industrial processing related to plant foods. On the other hand, bioactive peptides were found in many plant-based foods, such as potato, soy, hempseeds, cereals, pseudocereals, algae and others, as the consequence of fermentation and enzymatic hydrolysis [11]. Following are several examples of peptides obtained from the main plant sources with their specific biological properties, as reported in recent literature and a preliminary section dedicates to current strategies for the release of peptides from protein precursors.

Current strategies for the release of peptides from protein precursors Various methods for obtaining bioactive peptides have been considered: some techniques involve the use of hydrolytic enzymes, such as trypsin, pepsin, alkalase, others use microbial fermentation that allows the proteolytic enzymes of lactic flora and finally through synthesis techniques [12]. The main techniques used for the synthesis of bioactive peptides are: chemical synthesis, synthesis by recombinant DNA technology and enzymatic synthesis. Currently, enzymatic hydrolysis represents the main process for the recovery of these molecules from both animal and plant sources. Most commercial enzymatic preparations frequently used are from animal and microbial sources. Although the use of plant proteases is still relatively limited to papain and bromelain from papaya and pineapple, respectively, the application of new plant proteases is increasing. A recent review by Mazorra-Manzano et al. [13] shows the latest knowledge in the use and diversity of plant proteases for bioactive peptides release from food proteins including both available commercial plant proteases as well as new potential plant sources. In addition, this work described the properties of peptides released by plant proteases and health benefits associated in the control of disorders such as hypertension, diabetes, obesity, and cancer. In alternative to enzymatic methods, in several studies the potential effects of bacterial strains in the production of bioactive peptides were evaluated. Fermentation techniques, depending on the type of fermenting microorganism and the desired peptide product, can last from a few hours to several days [14]. However, nowadays the use of enzymes to produce bioactive peptides is the most widespread method, in fact this method is faster and the reactions are more easily controlled than those using microorganisms. To this aspect contributes the remarkable specificity of substrate that allows the development of protein hydrolysates with both well-defined chemical and nutritional characteristics. Moreover, even for the aspect of food safety, enzymatic reactions are more Current Opinion in Food Science 2020, 31:31–37

suitable as they do not leave residues of organic solvents or other potentially toxic products for human health [15].

Bioactive peptides from cereals and legumes Cereals and legumes are the main sources of the vegetable-derived peptides, being both rich sources of proteins with a complementary spectrum of amino acids. Antioxidant properties and potential mechanisms of hydrolyzed proteins and peptides from cereals have been recently reviewed [16]. Karami et al. reported the antioxidant, anticancer and angiotensin converting enzyme (ACE)inhibitory activities of bioactive peptides from wheat germ protein hydrolysates, identified using nano-LC– MS/MS analysis [17]. Peptides with high antioxidant activity were obtained after the hydrolysis of rice bran protein under in vitro gastrointestinal digestion and the successive fractionation [18]. Also bioactive peptides from legume proteins have interesting biological activities and potential nutraceutical applications. It was reported that some lupine biopeptides, with molecular profile determined by molecular exclusion chromatography, exert anti-inflammatory effects and improve the immune and antioxidant status in human peripheral lymphocytes [19]. It was recently reported the antioxidant and ACE-inhibitory activities of protein hydrolysates from Mung bean, characterized by UV, circular dichroism (CD) spectroscopy and Fourier transform infrared (FTIR) spectroscopy [20]. A review article by Gonza´lez-Montoya et al. [21] is focused on the antiproliferative properties of the bioactive peptides from the main legumes: soybean, peas, chickpeas, common beans, fava beans, lentils, lupins.

Dietary peptides from soy Soy protein is the major plant source that produces peptides with biological/pharmacological properties, that exhibit antihypertensive, anticholesterol, and antioxidant activities, and seem to prevent cancer [22]. The processing of soy protein into peptides in the gastrointestinal tract greatly increases their healthful effects by exposing active groups within the amino acid chain. Some soy peptides like lunasin and soymorphins possess several properties and play a role in the prevention of multiple chronic diseases [23]. A work by Wang et al. [24] reports the preparation of bioactive peptides from soy proteins with antidiabetic, antihypertensive, antioxidant and identification of peptides inhibiting a-glucosidase. The results obtained allow to consider the hydrolysed peptides from soy proteins as promising natural ingredients for nutraceutical and/or functional food formulation. Cannabis sativa as new source of biopeptides

Hemp (Cannabis sativa L.) is a source of nutritious seeds that have been used as human food for thousands of years [25]. In particular, hemp seed cake, a by-product of cold oil processing, represents a food waste material of high www.sciencedirect.com

New scientific advances on vegetable biopeptides Montesano et al. 33

nutritional value. In a recent research by Hadnapev et al., it was used as starting raw material for bioactive peptides production [26]. Alkali extraction followed by isoelectric precipitation was employed for hemp protein isolation. Subsequently, the influence of different enzymes (alcalase and pancreatin), as well as the degree of hydrolysis on the kinetics of different molecular weights peptides production and their antioxidant potential was investigated. The obtained results showed that the peptides characterized by the highest degree of hydrolysis exhibited the strongest antioxidant activity. Moreover, the properties of the obtained hydrolysates were dependent on the type and specificity of the employed protease, as well as the hydrolysis time. Another study by Nongonierma and FitzGerald [27] demonstrated the potential benefit of hydrolysing plant protein substrates before oral ingestion with the view of releasing dipeptidyl peptidase IV (DPP-IV) inhibitory peptides. In this research, four plant protein isolates from hemp, pea, rice and soy were hydrolysed with three enzyme preparations. The results obtained showed that food protein hydrolysates contained peptide sequences with DPP-IV inhibitory properties which may find use to improve serum glucose regulation in type 2 diabetics.

Biopeptides from marine organisms Marine organisms are rich sources of structurally diverse bioactive compounds with various biological activities. Therefore, seafood has an essential role in the human diet and is not only a reliable source of protein, but it also has a nutritional impact due to its lipids, vitamin and mineral constituents. A book by Abbas et al. [28] reported the various functional compounds of seafood focusing on their potential use and health benefits. Among the various types of seafood containing functional compounds with beneficial health effects, spirulina (Arthrospira platensis), an unicellular blue algae, known for its high protein content and therapeutic properties, can be mentioned. Several studies in vivo and in vitro show its effectiveness in treatments of anemia, hepatotoxicity, cardiovascular diseases, hyperglycemia, hyperlipidemia, immunodeficiency, inflammatory processes, and enhancement of immune resistance in several types of cancer, reduction of cholesterol, HIV, and other viral diseases. Consequently, it has been considered as a generally recognized as safe (GRAS) ingredient since 2003 and defined as food of the future. These attributes, combined with its disseminated cultivation techniques, sustainable production, and commercial popularity, make Spirulina an attractive source for exploration and production of bioactive peptides [29]. In another paper, Alzahrani et al. [30] reported interesting data on Nitzschia laevis, a common pennate marine diatom, as compared to spirulina and chlorella, another well-known microalga, concluding that the hydrolysates obtained from their protein fraction showed strong in vitro antioxidant activities. www.sciencedirect.com

Bioactive peptides from other vegetable sources Garlic (Allium sativum L.)

This plant has been known since ancient times and historically represents a significant antioxidant potential also used in folk medicine and for the treatment of ageing-related disorders. In the literature there are many studies on the antiglicative properties of bioactive peptides extracted from aged garlic compared to the fresh one. This is because aged garlic has a greater concentration of organosulfur compounds, which are potent antioxidants and free radical scavengers. A study by Shi et al. [31] has investigated the antiglycative effect of active peptides in fresh garlic extract by electron spin resonance (ESR) spectroscopy. The results of this study showed that the water-soluble active peptides with small side chains of fresh garlic had a high inhibitory effect on glycation in aqueous systems, when compared with hydrophobic ones with long side chains.

Quinoa (Chenopodium quinoa L.)

The cereals and flour of the quinoa pseudocereal represent a food with an high nutritional value, in fact they contain an elevated quantity of proteins, minerals and vitamins. In particular, quinoa proteins are rich in amino acids such as lysine, threonine and methionine, commonly lacking in cereals, and are close to the ideal protein balance recommended by FAO [32,33]. The authors evaluated the antioxidant potential of quinoa flour, after fermentation with autochthonous and selected lactic bacteria. Specifically, biopeptides were identified, characterized and evaluated for antioxidant properties in vitro, also using human keratinocytes NCTC 2544. The autochthonous lactic acid bacteria, therefore, were shown to promote the release of antioxidant peptides by means of proteolysis of native proteins. It is possible to state that the fermentation process applied to quinoa flour with a selected starter can be used to produce a functional food ingredient, a food supplement or pharmaceutical preparations.

Miscellaneous

In addition to these reviewed products, there are many other plant-derived products that are able to provide bioactive peptides by different hydrolysis methods. In the Table 1 are summarized the main sources of bioactive peptides with the relative biological properties.

Recovery of bioactive peptides from byproduct and processing waste Waste generated by agro-industries [43] can be a rich source of valuable compounds, among which proteins, and therefore could become a sustainable alternative to reduce malnutrition and hunger in developing countries [44]. Current Opinion in Food Science 2020, 31:31–37

34 Food bioprocessing

Table 1 Sources of bioactive peptides with the relative biological properties Source

Biological properties

Reference

Potato Rapeseed Lupine Cowpea

Antioxidant ACE inhibitory and antihypertensive Anti-inflammatory Anti-inflammatory, benefits against cancer, diabetes, and cardiovascular disease Antioxidant and ACE-inhibitory Anti-inflammatory Prevention of chronic diseases ACE-inhibitory Antioxidant and ACE-inhibitory

[34] [35] [36] [37]

Wheat Pyropia yezoensis Amaranth Walnut Cocoa

Currently, a large amount of by-products and various waste is produced annually from the processing of microalgae, soybean meal, olive, cherry, rapeseed flour, and so on. Generally these by-products contain significant amounts of proteins, peptides and amino acids. Bioactive peptides production from waste and by-products does not significantly differ from the production from food vegetables, and enzymes are commonly used to hydrolyse proteins [45]. A review by Lemes et al. [46] describes recent advances in bioactive peptide technology, such as: new strategies for transforming bioactive peptides from residual waste into added-value products; nanotechnology for the encapsulation, protection and release of controlled peptides, use of techniques of large-scale recovery and purification of peptides aiming at future applications in pharmaceutical and food industries. Table 2 reports the summary of some bioactive peptides obtained from byproducts and agro-industrial waste mainly by enzymatic hydrolysis. Recent examples in this field include the production of bioactive peptides from date seeds, that constitute a waste or can be used as animal feed. Different enzymes were used for the hydrolysis of date seed proteins by individual or sequential treatment and several bioactivities were investigated with positive results [47]. Garcia et al. [48] reported that waste material derived from the processing of cherry represented a starting point to obtain peptides showing antioxidant and antihypertensive properties. Peach seeds contain more than 40% of

[38] [39] [40] [41] [42]

proteins and can constitute a cheap source of bioactive peptides. They were investigated for the production of antioxidant peptides using different enzymes, with the best bioactivity produced by hydrolysis with thermolysin [49]. Tomato seed contains proteins of high nutritional value and nutraceutical properties, so they can be recovered for application as food additives. Mechmeche et al. [50,51], in some studies have developed a simple and inexpensive method to produce bioactive peptides from tomato seed meal isolate using Lactobacillus plantarum and their antioxidant activity was also evaluated. In another paper, Esteve et al. [52] proposed a new strategy for the revalorization of olive waste material using proteases to obtain bioactive peptides. A flour with about 22% protein, hydrolysed with specific enzymes, provided hydrolysates with antioxidant and antihypertensive capacity. Brewers’ spent grain is the most abundant by-product generated in the beer-brewing process and, due to its high content of protein, it represents an attractive compound in human nutrition. A proteinenriched isolate from brewers’ spent grain was hydrolysed using some enzymes and six ACE inhibitory peptides were identified [53]. The proteins from the potato starch industry byproduct is a promising source, as several health benefits may be associated with their hydrolysates. Waglay et al. [54] investigated the efficiency of some selected proteases and characterized the

Table 2 Peptides and their biological properties from agro-industrial plant-based waste or by-products Source

By-product/waste

Biological properties

Reference

Date Cherry Peach Tomato Olive Barley Potato

Seeds Seeds Seeds Seeds Flour Brewers’ spent grain Potato starch industry by-product

[47] [48] [49] [50,51] [52] [53] [54]

Cauliflower Palmaria palmata

Cauliflower by-products Red alga

Antioxidant and ACE inhibitory Antioxidant and antihypertensive Antioxidant Antioxidant Antioxidant and antihypertensive ACE inhibitory ACE inhibitory, antioxidant, lipolysis stimulating, anti-cholesterol ACE inhibitory ACE inhibitory

Current Opinion in Food Science 2020, 31:31–37

[55] [56]

www.sciencedirect.com

New scientific advances on vegetable biopeptides Montesano et al. 35

hydrolysate properties. Cauliflower by-products are a potential source of value-added compounds. Chiozzi et al. [55] developed an analytical strategy for the production of purified bioactive peptides from cauliflower waste proteins, by testing two different extraction protocols and screening different enzymes for protein hydrolysis, in this way, they identified three novel ACE-inhibitory peptides. Palmaria palmate is a red alga which is rarely eaten and is usually discarded in the production of kombu (Saccharina japonica), although it is becoming popular as a foodstuff. Some authors reported that thermolysin digestion produces two peptides with ACE inhibitor activity, that can be considered as one more example of revalorization of waste [56].

Final considerations and recommendations The interest for health-promoting functional foods, dietary supplements and pharmaceutical preparations containing bioactive peptides is markedly increasing. A focal point is represented by the fact that the sequences that show the same bioactivity can be released from both animal and plant native proteins. More recently, the scientific community investigated the possibility to obtain bioactive peptides from plants. Several researches showed that plant-derived peptides display a myriad of activities ranging from antimicrobial, anticancer, anticholesterol to beneficial effects for cardiovascular health. In addition, studies in humans have established the effects of identified plant peptides on cancer, cell proliferation, and their use as preventative control agents for diseases such as diabetes and high blood pressure. The peptides reviewed generally have shown excellent health-promoting properties and potentially prevent many diseases by making them extremely suitable for nutraceutical applications. However, more studies are required to further identify their target organs, and elucidate their biological mechanisms of action in order to be potentially used as functional foods or even therapeutics for the prevention or treatment of chronic diseases. In particular, further clinical studies are needed to better understand the gastrointestinal stability, bioavailability and safety of these peptides for their use as drugs, nutraceuticals or functional foods. Moreover, industrial scale-up technologies are required to ensure cost of production of these bioactives remains feasible. Finally, from the last paragraph it seems relevant the effort of the scientific community to derive high valueadded products from waste from agro-industrial processing, in accordance with the concepts of circular economy and sustainability, fundamental to guarantee respect for the ecosystem.

Conflict of interest statement Nothing declared. www.sciencedirect.com

Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-forprofit sectors.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1. 

Fernandes SS, Coelho MS, de las Mercedes Salas-Mellado M: Bioactive compounds as ingredients of functional foods: polyphenols, carotenoids, peptides from animal and plant sources new. Bioactive Compounds. Woodhead Publishing; 2019:129-142 Bioactive ingredients provide some physiological benefits, which direct the food industry to focus its research on products of this nature. Peptides are among the most studied bioactive compounds for their beneficial effects. In this chapter, the authors provide on the use of bioactive compounds, in order to improve health and quality of life. 2.

Naviglio D, Scarano P, Ciaravolo M, Gallo M: Rapid solid-liquid dynamic extraction (RSLDE): a powerful and greener alternative to the latest solid-liquid extraction techniques. Foods 2019, 8:245.

3. 

Piovesana S, Capriotti AL, Cavaliere C, La Barbera G, Montone CM, Chiozzi RZ, Lagana` A: Recent trends and analytical challenges in plant bioactive peptide separation, identification and validation. Anal Bioanal Chem 2018, 410:3425-3444 This review provides an overview of developments on the isolation and separation of biopeptides, using single or multiple chromatographic techniques. Furthermore, the most recent applications in biopeptide investigations for plant foods and by-products are discussed.

4. 

Hayes M, Bleakley S: Peptides from plants and their applications. Peptide Applications in Biomedicine, Biotechnology and Bioengineering. Woodhead Publishing; 2018:603-622 Several studies report that bioactive peptides derived from plants are a source of compounds to improve health particularly when consumed as part of a healthy and balanced diet. This chapter describes bioactive peptides of plant origin including cereals and legumes and their use as functional foods. Furthermore, it provides examples of products derived from vegetable peptides currently on the market. 5.

Sa´nchez A, Va´zquez A: Bioactive peptides: a review. Food Qual Saf 2017, 1:29-46.

6.

Toldra´ F, Reig M, Aristoy MC, Mora L: Generation of bioactive peptides during food processing. Food Chem 2018, 267:395404.

7.

Mohanty DP, Mohapatra S, Misra S, Sahu PS: Milk derived bioactive peptides and their impact on human health–a review. Saudi J Biol Sci 2016, 23:577-583.

8.

Hajfathalian M, Ghelichi S, Garcı´a-Moreno PJ, Moltke Sørensen AD, Jacobsen C: Peptides: Production, bioactivity, functionality, and applications. Crit Rev Food Sci Nutr 2018, 58:3097-3129.

9.

Li-Chan EC: Bioactive peptides and protein hydrolysates: research trends and challenges for application as nutraceuticals and functional food ingredients. Curr Opin Food Sci 2015, 1:28-37.

10. Daliri E, Oh D, Lee B: Bioactive peptides. Foods 2017, 6:32. 11. Salas CE, Badillo-Corona JA, Ramı´rez-Sotelo G, OliverSalvador C: Biologically active and antimicrobial peptides from plants. BioMed Res Int 2015:102129. 11 pages. 12. Chew LY, Toh GT, Ismail A: Application of proteases for the  production of bioactive peptides. Enzymes in Food Biotechnology. Academic Press; 2019:247-261 In recent years, the use of enzymatic preparation in food processing has increased greatly because it is considered a green technology. This chapter describes the proteases used in food preparation, as well as Current Opinion in Food Science 2020, 31:31–37

36 Food bioprocessing

discussing the feasibility and possible challenges of the industrial application of proteases for the production of bioactive peptides.

Sources. Edited by Nadathur SR, Wanasundara JPD, Scanlin L. Academic Press; 2017:121-132.

13. Mazorra-Manzano MA, Ramı´rez-Suarez JC, Yada RY: Plant  proteases for bioactive peptides release: a review. Crit Rev Food Sci Nutr 2018, 58:2147-2163 Enzymatic hydrolysis is the most commonly used process for the production of bioactive peptides. This review describes the use of plant proteases for the release of bioactive peptides from dietary proteins. Furthermore, the properties of peptides released by plant proteases and health benefits are reviewed.

-Hadnapev T, Jovanov P, cevic 26. Hadnapev M, Dizdar M, Dap9 Misˇan A, Saka9 c M: Hydrolyzed hemp seed proteins as bioactive peptides. J Process Energy Agric 2018, 22:90-94.

14. Rizzello CG, Tagliazucchi D, Babini E, Rutella GS, Saa DLT,  Gianotti A: Bioactive peptides from vegetable food matrices: research trends and novel biotechnologies for synthesis and recovery. J Funct Foods 2016, 27:549-569 Recently, the scientific community is studying the possibility of obtaining bioactive peptides from plant sources, also discovering new functional characteristics. In this article, several functional effects of plant-derived peptides are described. Furthermore, modern technologies for their recovery, purification and analysis are reported.

28. Abbas M, Saeed F, Suleria HAR: Marine bioactive compounds: Innovative trends in food and medicine. Plant-and Marinebased Phytochemicals for Human Health: Attributes, Potential, and Use. CRC Press; 2018.

15. Chakrabarti S, Guha S, Majumder K: Food-derived bioactive  peptides in human health: challenges and opportunities. Nutrients 2018, 10:1738-1755 In the last decades a wide range of food-derived bioactive peptide sequences has been identified, with multiple health-beneficial activities. This review describes the current techniques for producing bioactive peptides, the gastrointestinal bioavailability of these food-derived biopeptides and the general regulatory environment. 16. Esfandi R, Walters ME, Tsopmo A: Antioxidant properties and potential mechanisms of hydrolyzed proteins and peptides from cereals. Heliyon 2019, 5:e01538. 17. Karami Z, Peighambardoust SH, Hesari J, Akbari-Adergani B, Andreu D: Antioxidant, anticancer and ACE-inhibitory activities of bioactive peptides from wheat germ protein hydrolysates. Food Biosci 2019, 32:100450. 18. Phongthai S, D’Amico S, Schoenlechner R, Homthawornchoo W, Rawdkuen S: Fractionation and antioxidant properties of rice bran protein hydrolysates stimulated by in vitro gastrointestinal digestion. Food Chem 2018, 240:156-164. 19. Cruz-Chamorro I, A´lvarez-Sa´nchez N, Milla´n-Linares MC, Yust MM, Pedroche J, Milla´n F, Lardone PJ, Carrera-Sa´nchez C, Guerrero JM, Carrillo-Vico A: Lupine protein hydrolysates decrease the inflammatory response and improve the oxidative status in human peripheral lymphocytes. Food Res Int 2019, 126:108585. 20. Xie J, Du M, Shen M, Wu T, Lin L: Physico-chemical properties, antioxidant activities and angiotensin-I converting enzyme inhibitory of protein hydrolysates from Mung bean (Vigna radiate). Food Chem 2019, 270:243-250. 21. Gonza´lez-Montoya M, Cano-Sampedro E, Mora-Escobedo R: Bioactive peptides from legumes as anticancer therapeutic agents. Int J Cancer Clin Res 2017, 4:1-10. 22. Singh BP, Yadav D, Vij S: Soybean bioactive molecules: current trend and future prospective. In Bioactive Molecules in Food. Edited by Me’rillon J-M, Ramawat KG. Springer International Publishing; 2017:1-29. 23. Ferna´ndez-Tome´ S, Herna´ndez-Ledesma B: Current state of art after twenty years of the discovery of bioactive peptide lunasin. Food Res Int 2019, 116:71-78. 24. Wang R, Zthao H, Pan X, Orfila C, Lu W, Ma Y: Preparation of  bioactive peptides with anidiabetic, antihypertensive, and antioxidant activities and identification of a-glucosidase inhibitory peptides from soy protein. Food Sci Nutr 2019, 7:1848-1856 Bioactive peptides have a wide range of functional properties, including antimicrobial, antihypertension, hypoglycemic activity, immunomodulation, and antioxidative functions. In this study, the peptides of soy protein obtained by enzymatic digestion with proteases were analyzed for their antidiabetic, antihypertensive, and antioxidant activities. 25. Aluko RE: Hemp seed (Cannabis sativa L.) proteins: composition, structure, enzymatic modification, and functional or bioactive properties. In Sustainable Protein Current Opinion in Food Science 2020, 31:31–37

27. Nongonierma AB, FitzGerald RJ: Investigation of the potential of hemp, pea, rice and soy protein hydrolysates as a source of dipeptidyl peptidase IV (DPP-IV) inhibitory peptides. Food Digest: Res Curr Opin 2015, 6:19-29.

29. Ovando CA, Carvalho JCD, Vinı´cius de Melo Pereira G, Jacques P, Soccol VT, Soccol CR: Functional properties and health benefits of bioactive peptides derived from Spirulina: a review. Food Rev Int 2018, 34:34-51. 30. Alzahrani MAJ, Perera CO, Hemar Y: Production of bioactive proteins and peptides from the diatom Nitzschia laevis and comparison of their in vitro antioxidant activities with those from Spirulina platensis and Chlorella vulgaris. Int J Food Sci Technol 2018, 53:676-682. 31. Shi F, Bai B, Ma S, Ji S, Liu L: The inhibitory effects of g-glutamylcysteine derivatives from fresh garlic on glycation radical formation. Food Chem 2016, 194:538-544. 32. Rizzello CG, Lorusso A, Montemurro M, Gobbetti M: Use of sourdough made with quinoa (Chenopodium quinoa) flour and autochthonous selected lactic acid bacteria for enhancing the nutritional, textural and sensory features of white bread. Food Microbiol 2016, 56:1-13. 33. Rizzello CG, Lorusso A, Russo V, Pinto D, Marzani B, Gobbetti M: Improving the antioxidant properties of quinoa flour through fermentation with selected autochthonous lactic acid bacteria. Int J Food Microbiol 2017, 241:252-261. 34. Udenigwe CC, Udechukwu MC, Yiridoe C, Gibson A, Gong M: Antioxidant mechanism of potato protein hydrolysates against in vitro oxidation of reduced glutathione. J Funct Foods 2016, 20:195-203. 35. He R, Girgih AT, Rozoy E, Bazinet L, Ju XR, Aluko RE: Selective separation and concentration of antihypertensive peptides from rapeseed protein hydrolysate by electrodialysis with ultrafiltration membranes. Food Chem 2016, 197:1008-1014. 36. Cruz-Chamorro I, A´lvarez-Sa´nchez N, del Carmen Milla´nLinares M, del Mar Yust M, Pedroche J, Milla´n F et al.: Lupine protein hydrolysates decrease the inflammatory response and improve the oxidative status in human peripheral lymphocytes. Food Res Int 2019, 126:108585. 37. Awika JM, Duodu KG: Bioactive polyphenols and peptides in cowpea (Vigna unguiculata) and their health promoting properties: a review. J Funct Foods 2017, 38:686-697. 38. Cian RE, Vioque J, Drago SR: Structure–mechanism relationship of antioxidant and ACE I inhibitory peptides from wheat gluten hydrolysate fractionated by pH. Food Res Int 2015, 69:216-223. 39. Lee HA, Kim IH, Nam TJ: Bioactive peptide from Pyropia yezoensis and its anti-inflammatory activities. Int J Mol Med 2015, 36:1701-1706. 40. Montoya-Rodrı´guez A, Go´mez-Favela MA, Reyes-Moreno C, Mila´n-Carrillo J, Gonza´lez de Mejı´a E: Identification of bioactive peptide sequences from amaranth (Amaranthus hypochondriacus) seed proteins and their potential role in the prevention of chronic diseases. Compr Rev Food Sci Food Saf 2015, 14:139-158. 41. Wang C, Tu M, Wu D, Chen H, Chen C, Wang Z, Jiang L: Identification of an ACE-inhibitory peptide from walnut protein and its evaluation of the inhibitory mechanism. Int J Mol Sci 2018, 19:1156. 42. Marseglia A, Dellafiora L, Prandi B, Lolli V, Sforza S, Cozzini P et al.: Simulated gastrointestinal digestion of cocoa: detection of www.sciencedirect.com

New scientific advances on vegetable biopeptides Montesano et al. 37

resistant peptides and in silico/in vitro prediction of their ace inhibitory activity. Nutrients 2019, 11:985. 43. Yates M, Gomez MR, Martin-Luengo MA, Iban˜ez VZ, Serrano AMM: Multivalorization of apple pomace towards materials and chemicals. Waste to wealth. J Clean Prod 2017, 143:847-853. 44. Torres-Leon C, Ramirez N, London˜o L, Martinez G, Diaz R, Navarro V et al.: Food waste and byproducts: an opportunity to minimize malnutrition and hunger in developing countries. Front Sustain Food Syst 2018, 2:52. 45. Banerjee J, Singh R, Vijayaraghavan R, MacFarlane D, Patti AF, Arora A: Bioactives from fruit processing wastes: green approaches to valuable chemicals. Food Chem 2017, 225:10-22.

50. Mechmeche M, Kachouri F, Chouabi M, Ksontini H, Setti K, Hamdi M: Optimization of extraction parameters of protein isolate from tomato seed using response surface methodology. Food Anal Methods 2017, 10:809-819. 51. Mechmeche M, Kachouri F, Ksontini H, Chouabi M, Hamdi M: Production of bioactive peptides from tomato seed isolate by Lactobacillus plantarum fermentation and enhancement of antioxidant activity. Food Biotechnol 2017, 31:94-113. 52. Esteve C, Marina ML, Garcı´a MC: Novel strategy for the revalorization of olive (Olea europaea) residues based on the extraction of bioactive peptides. Food Chem 2015, 167:272-280.

46. Lemes A, Sala L, Ores J, Braga A, Egea M, Fernandes K: A review of the latest advances in encrypted bioactive peptides from protein-rich waste. Int J Mol Sci 2016, 17:950.

53. Connolly A, O’Keeffe MB, Piggott CO, Nongonierma AB, FitzGerald RJ: Generation and identification of angiotensin converting enzyme (ACE) inhibitory peptides from a brewers’spent grain protein isolate. Food Chem 2015, 176:64-71.

47. Ambigaipalan P, Al-Khalifa AS, Shahidi F: Antioxidant and angiotensin I converting enzyme (ACE) inhibitory activities of date seed protein hydrolysates prepared using Alcalase, Flavourzyme and Thermolysin. J Funct Foods 2015, 18:1125-1137.

54. Waglay A, Karboune S: Enzymatic generation of peptides from potato proteins by selected proteases and characterization of their structural properties. Biotechnol Prog 2016, 32:420-429.

48. Garcia MC, Endermann J, Gonzalez-Garcia E, Marina ML: HPLCQ-TOF-MS identification of antioxidant and antihypertensive peptides recovered from cherry (Prunus cerasus L.) subproducts. J Agric Food Chem 2015, 63:1514-1520.

55. Chiozzi RZ, Capriotti AL, Cavaliere C, La Barbera G, Piovesana S, Lagana` A: Identification of three novel angiotensin-converting enzyme inhibitory peptides derived from cauliflower byproducts by multidimensional liquid chromatography and bioinformatics. J Funct Foods 2016, 27:262-273.

49. Va´squez-Villanueva R, Marina ML, Garcı´a MC: Identification by hydrophilic interaction and reversed-phase liquid chromatography–tandem mass spectrometry of peptides with antioxidant capacity in food residues. J Chromatogr A 2016, 1428:185-192.

www.sciencedirect.com

56. Furuta T, Miyabe Y, Yasui H, Kinoshita Y, Kishimura H: Angiotensin I converting enzyme inhibitory peptides derived from phycobiliproteins of dulse Palmaria palmata. Marine Drugs 2016, 14:32.

Current Opinion in Food Science 2020, 31:31–37