Abstract
Brewer’s spent yeast (BSY) is a prevalent by-product of the brewing industry currently used in animal feed as a cheap source of protein. In this study, chemical composition of BSY from two different beer production (American IPA, BSY1, and Imperial Stout, BSY2) was characterized, aiming for potential use as nutraceutical sources. Cytotoxicity of BSY extracts was also tested in freshly isolated peripheral blood mononuclear cells (PBMCs) and in tumoral (pancreatic cancer tumor cells, PANC-1, and colorectal adenocarcinoma tumor cells, CACO-2) and non-tumoral (umbilical vein endothelial cells, HUVEC) cell lineages. BSY samples showed similar lipid and ash content, but slight differences in the content of reducing sugars, total proteins, moisture and total proteins. BSY2 sample presented higher glucans and phenolic compound concentrations than BSY1. Main phenolic compounds identified were xanthohumol, ferulic acid, p-coumaric acid (BSY1 and BSY2), and gallic acid (BSY2). BSY1 and BSY2 extracts showed similar antioxidant capacity. Neither BSY1 nor BSY2 were cytotoxic to PBMCs, HUVEC and CACO-2, but were cytotoxic to PANC-1 cells, in a concentration-dependent manner. Our findings revealed that the residue of brewery can be a value-added functional food product with an adjuvant role against PANC-1 cell lines.
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Data availability
The data that support the findings of this study are available from the corresponding author, P.A. Horn, upon request.
References
Ferreira IMPLVO, Pinho O, Vieira E, Tavarela JG (2010) Brewer's Saccharomyces yeast biomass: characteristics and potential applications. Trends Food Sci Technol. https://doi.org/10.1016/j.tifs.2009.10.008
Jaeger A, Arendt EK, Zannini E, Sahin AW (2020) Brewer’s spent yeast (BSY), an underutilized brewing by-product. Fermentation 6(4):123. https://doi.org/10.3390/fermentation6040123
Rasmeni ZZ, Madyira DM, Matheri A (2022) Comprehensive analysis of BSY as a biomass for potential energy resource recovery. Energy Rep 8:804–810. https://doi.org/10.1016/j.egyr.2022.10.272
Garcia-Garcia G, Stone J, Rahimefard S (2019) Opportunities for waste valorization in the food industry e A case study with four UK food manufacturers. J Cleaner Prod 211:1339–1356
Vélez-Erazo EM, Saturno RP, Marson GV, Hubinger MD (2021) Spent brewer’s yeast proteins and cell debris as innovative emulsifiers and carrier materials for edible oil microencapsulation. Food Res Int 140:109853. https://doi.org/10.1016/j.foodres.2020.109853
dos Santos TRM, de Mello PPM, Sérvulo EFC (2014) Solid wastes in brewing process: a review. J Brew Distilling 5:1–19. https://doi.org/10.5897/JBD2014.0043
Marson GV, de Castro RJS, Belleville MP, Hubinger MD (2020) Spent brewer’s yeast as a source of high added value molecules: a systematic review on its characteristics, processing and potential applications. World J Microbiol Biotechnol 36:1–22
Karlović A, Jurić A, Ćorić N, Habschied K, Krstanović V, Mastanjević K (2020) By-products in the malting and brewing industries—re-usage possibilities. Fermentation 6:82. https://doi.org/10.3390/fermentation6030082
Podpora B, Świderski F, Sadowska A, Rakowska R, Wasiak-Zyz G (2016) Spent brewer’s yeast extracts as a new component of functional food Czech. J Food Sci 34:544–563. https://doi.org/10.17221/419/2015-CJFS
Jacob FF, Striegel L, Rychlik M, Hutzler M, Methner FJ (2019) Spent yeast from brewing processes: a biodiverse starting material for yeast extract production. Fermentation 5:51. https://doi.org/10.3390/fermentation5020051
Chua JY, Lu Y, Liu SQ (2017) Biotransformation of soy whey into soy alcoholic beverage by four commercial strains of Saccharomyces cerevisiae. Int J Food Microbiol 262:14–22. https://doi.org/10.1016/j.ijfoodmicro.2017.09.007
Padilla B, Frau F, Ruiz-Matute AI, Montilla A, Belloch C, Manzanares P, Corzo N (2015) Production of lactulose oligosaccharides by isomerisation of transgalactosylated cheese whey permeate obtained by β-galactosidases from dairy Kluyveromyces. J Dairy Res 82:356–364
Rai AK, Jeyaram K (2017) Role of yeasts in food fermentation. Yeast diversity in human welfare, pp 83–113
León-González ME, Gómez-Mejía E, Rosales-Conrado N, Madrid-Albarrán Y (2017) Residual brewing yeast as a source of polyphenols: extraction, identification, and quantification by chromatographic and chemometric tools. Food Chem. https://doi.org/10.1016/j.foodchem.2017.06.141
Horn PA, Pedron NB, Junges LH, Rebelo AM, da Silva Filho HH, Zeni ALB (2021) Antioxidant profile at the different stages of craft beers production: the role of phenolic compounds. Eur Food Res Technol 247:439–452. https://doi.org/10.1007/s00217-020-03637-2
Puligundla P, Mok C, Park S (2020) Advances in the valorization of spent brewer’s yeast Innovative. Food Sci Emerg Technol 62:102350. https://doi.org/10.1016/j.ifset.2020.102350
Avramia I, Amariei S (2021) Spent brewer’s yeast as a source of insoluble β-glucans Int. J Mol Sci 22:825. https://doi.org/10.3390/ijms22020825
Caruso A, Piermaria JA, Abraham AG, Micaela M (2022) β-Glucans obtained from beer spent yeasts as functional food grade additive: focus on biological activity. Food Hydrocoll. https://doi.org/10.1016/j.foodhyd.2022.107963
Del Cornò M, Gessani S, Conti L (2020) Shaping the innate immune response by dietary glucans: any role in the control of cancer? Cancers 8:155. https://doi.org/10.3390/cancers12010155
Laroche C, Michaud P (2007) New developments and prospective applications for β (1, 3) Glucans. Recent Pat Biotechnol 1:59–73. https://doi.org/10.2174/187220807779813938
Wasziewicz-Robak B (2011) Spent brewer’s yeast and beta-glucans isolated from them as diet components modifying blood lipid metabolism disturbed by an atherogenic diet. IntechOpen. https://www.intechopen.com/chapters/42112. Accessed 20 Sept 2020
Choromanska A, Kulbacka J, Harasym J, Oledzki R, Szewczyk A, Saczko J (2018) High-and low-molecular weight oat beta-glucan reveals antitumor activity in human epithelial lung cancer. Pathol Oncol Res 25:583–592
Sima P, Richter J, Vetvicka V (2019) Glucans as new anticancer agents. Anticancer Res 39:3373–3378 https://doi.org/10.21873/anticanres.13480
Stier H, Ebbeskotte V, Gruenwald J (2014) Immune-modulatory effects of dietary yeast Beta-1, 3/1, 6-d-glucan. Nutr J 28:13–38. https://doi.org/10.1186/1475-2891-13-38
Bacha U, Nasir M, Iqbal S, Anjum AA (2017) Nutraceutical, anti-inflammatory, and immune modulatory effects of β-glucan isolated from yeast. Biomed Res Int. https://doi.org/10.1155/2017/8972678
León-González ME, Gómez-Mejía E, Rosales-Conrado N, Madrid-Albarrán Y (2018) Residual brewing yeast as a source of polyphenols: extraction, identification, and quantification by chromatographic and chemometric tools. Food Chem 267:246–254. https://doi.org/10.1016/j.foodchem.2017.06.141
Tatullo M, Simoe GM, Tarullo F, Irlandese G, de Vito D, Marrelli M, Santacroce L, Cocco T, Ballini A, Scacco S (2016) Antioxidant and antitumor activity of a bioactive polyphenolic fraction isolated from the brewing process. Sci Rep 6:1–7. https://doi.org/10.1038/srep36042
Amorim MM, Pereira JO, Monteiro KM, Ruiz AL, Carvalho JE, Pinheiro H, Pintado M (2016) Antiulcer and antiproliferative properties of spent brewer’s yeast peptide extracts for incorporation into foods. Food Funct 7:2331–2337. https://doi.org/10.1039/C6FO00030D
Vieira E, Brandão T, Ferreira IM (2013) Evaluation of brewer’s spent yeast to produce flavor enhancer nucleotides: influence of serial repitching. J Agric Food Chem 61:8724–8729. https://doi.org/10.1021/jf4021619
AOAC G (2016) Official methods of analysis of AOAC International. Rockville, MD: AOAC International. ISBN: 978-0-935584-87-5
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Vasconcelos NM, Pinto GAS, de Aragão FAS (2013) Determinação de açúcares redutores pelo ácido 3,5-dinitrosalicílico: histórico do desenvolvimento do método e estabelecimento de um protocolo para o laboratório de bioprocessos. Embrapa Agroindústria Tropical-Boletim de Pesquisa e Desenvolvimento (INFOTECA-E). https://ainfo.cnptia.embrapa.br/digital/bitstream/item/103342/1/BPD13017.pdf. Accessed 01 Sept 2022
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
Zeni ALB, Albuquerque CACD, Gonçalves F, Latini A, Tasca CI, Podestá R, Pagliosa CM, Duarte FS, de Lima TCM, Maraschin M (2013) Phytochemical profile, toxicity and antioxidant activity of Aloysia gratissima (Verbenaceae). Quim Nova 36:69–73. https://doi.org/10.1590/S0100-40422013000100013
Schulz M, Borges GDSC, Gonzaga LV, Seraglio SKT, Olivo IS, Azevedo MS, Nehring P, de Gois JS, de Almeida TD, Vitali L, Spudeit DA, Micke GA, Borges DLG, Fett R (2015) Chemical composition, bioactive compounds and antioxidant capacity of juçara fruit (Euterpe edulis Martius) during ripening. Food Res Int 77:125–131. https://doi.org/10.1016/j.foodres.2015.08.006
da Silva LR, Ferreira SRS, Vitali L, Block JM (2019) May the superfruit red guava and its processing waste be a potential ingredient in functional foods? Food Res Int 115:451–459. https://doi.org/10.1016/j.foodres.2018.10.053
Rudke AR, Mazzutti S, Andrade KS, Vitali L, Ferreira SRS (2019) Optimization of green PLE method applied for the recovery of antioxidant compounds from buriti (Mauritia flexuosa L.) shell. Food Chem 298:125061. https://doi.org/10.1016/j.foodchem.2019.125061
Urrea-Victoria V, Pires JS, Torres PB, Chow F, dos Santos DAC (2016) Ensaio antioxidante em microplaca do poder de redução do ferro (FRAP) para extratos de algas. Inst Biociências USP. https://doi.org/10.13140/RG.2.2.24094.64322
Brand-Williams W, Cuvelier MEBC (1995) Use of free radical methods to evaluate antioxidant activity. J Food Sci Technol 28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Van de Loosdrecht AA, Beelen RHJ, Ossenkoppele GJ, Broekhoven MG, Langenhujsen MMAC (1994) A tetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. J Immunol Methods 174:311–320. https://doi.org/10.1016/0022-1759(94)90034-5
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. https://doi.org/10.1016/0022-1759(83)90303-4
Fotakis G, Timbrell JA (2006) In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol Lett 15:153–161. https://doi.org/10.1016/j.toxlet.2005.07.001
Borenfreund E, Buerner JA (1985) A simple quantitative procedure using monolayer culture for toxicity assays (HTR/NR90). J Tissue Culture Methods 9:7–9
Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131–138. https://doi.org/10.1016/0003-2697(82)90118-x
Borra RC, Lotufo MA, Gagioti SM, Barros FM, Andrade PM (2009) A simple method to measure cell viability in proliferation and cytotoxicity assays. Braz Oral Res 23:255–262. https://doi.org/10.1590/S1806-83242009000300006
Martinez-Gomez A, Caballero I, Blanco CA (2020) Phenols and melanoidins as natural antioxidants in beer. Structure, Reactivity and Antioxidant Activity. Biomolecules 10:1–9. https://doi.org/10.3390/biom10030400
Olivares-Galván S, Marina ML, García MC (2022) Extraction of valuable compounds from brewing residues: malt rootlets, spent hops, and spent yeast. Trends Food Sci. https://doi.org/10.1016/j.tifs.2022.06.002
Zhu L, Wang J, Feng Y, Yin H, Lai H, Xiao R, He S, Yang Z, He Y (2022) Process optimization, amino acid composition, and antioxidant activities of protein and polypeptide extracted from waste beer yeast. Molecules 27:6825. https://doi.org/10.3390/molecules27206825
Yamada EA, Alvim ID, Santucci MCC, Sgarbieri VC (2003) Composição centesimal e valor protéico de levedura residual da fermentação etanólica e de seus derivados. Rev Nutr 16:423–432. https://doi.org/10.1590/S1415-52732003000400006
Bertolo AP, Biz AP, Kempka AP, Rigo E, Cavalheiro D (2019) Yeast (Saccharomyces cerevisiae): evaluation of cellular disruption processes, chemical composition, functional properties and digestibility. J Food Sci Technol 56:3697–3706. https://doi.org/10.1007/s13197-019-03833-3
Lynch KM, Steffen EJ, Arendt EK (2016) Brewers’ spent grain: a review with an emphasis on food and health. J Inst Brew 122:553–568. https://doi.org/10.1002/jib.363
Mathias TRDS, Alexandre VMF, Cammarota MC, de Mello PPM, Sérvulo EFC (2015) Characterization and determination of brewer’s solid wastes composition. J Inst Brew 121:400–404. https://doi.org/10.1002/jib.229
de Araújo VBS, de Melo ANF, Costa AG, Castro-Gomez RH, Madruga MS, de Souza EL, Magnani M (2014) Followed extraction of β-glucan and mannoprotein from spent brewer’s yeast (Saccharomyces uvarum) and application of the obtained mannoprotein as a stabilizer in mayonnaise. Innov Food Sci Emerg Technol 23:164–170. https://doi.org/10.1016/j.ifset.2013.12.013
Vieira EF, Carvalho J, Pinto E, Cunha S, Almeida AA, Ferreira IM (2016) Nutritive value, antioxidant activity and phenolic compounds profile of brewer’s spent yeast extract. J Food Compost Anal 52:44–51. https://doi.org/10.1016/j.jfca.2016.07.006
Carvalho DO, Curto AF, Guido LF (2015) Determination of phenolic content in different barley varieties and corresponding malts by liquid chromatography-diode array detection-electrospray ionization tandem mass spectrometry. Antioxidants 4:563–576. https://doi.org/10.3390/antiox4030563
Maillard MN, Soum MH, Boivin P, Berset C (1996) Antioxidant activity of barley and malt: relationship with phenolic content. LWT Food Sci Technol 29:238–244. https://doi.org/10.1006/fstl.1996.0035
McCarthy AL, O’Callaghan YC, Neugart S, Piggott CO, Connolly A, Jansen MA, Krumbein A, Schreiner M, FitzGerald JR, O’Brien NM (2013) The hydroxycinnamic acid content of barley and brewers’ spent grain (BSG) and the potential to incorporate phenolic extracts of BSG as antioxidants into fruit beverages. Food Chem 141:2567–2574. https://doi.org/10.1016/j.foodchem.2013.05.048
Becker D, Stegmüller S, Richling E (2022) Characterization of brewer's spent grain extracts by tandem mass spectrometry and HPLC‐DAD: Ferulic acid dehydrodimers, phenolamides, and oxylipins. Food Sci Nutr. https://doi.org/10.1002/fsn3.3178
Boronat A, Soldevila-Domenech N, Rodríguez-Morató J, Martínez-Huélamo M, Lamuela-Raventós RM, De la Torre R (2020) Beer phenolic composition of simple phenols, prenylated flavonoids and alkylresorcinols. Molecules 25:2582. https://doi.org/10.3390/molecules25112582
Stewart GG (2017) Harvesting and cropping yeast: flocculation and centrifugation. Brewing and distilling yeasts, pp 259–308
Gołąbczak J, Gendaszewska-Darmach E (2010) Ksantohumol i inne prenyloflawonoidy szyszek chmielu–aspekty biologiczne i technologiczne. Biotechnologia 88:75–89
Stevens JF, Taylor AW, Deinzer ML (1999) Quantitative analysis of xanthohumol and related prenylflavonoids in hops and beer by liquid chromatography-tandem mass spectrometry. J Chromatogr A. https://doi.org/10.1016/s0021-9673(98)01001-2
Girisa S, Saikia Q, Bordoloi D, Banik K, Monisha J, Daimary UD, Verma E, Ahn KS, Kunnumakkara AB (2021) Xanthohumol from Hop: Hope for cancer prevention and treatment. IUBMB Life. https://doi.org/10.1002/iub.2522
Paszkot J, Kawa-Rygielska J, Anioł M (2021) Properties of dry hopped dark beers with high xanthohumol content. Antioxidants 10:763. https://doi.org/10.3390/antiox10050763
Mirzaei M, Mirdamadi S, Ehsani MR, Aminlari M, Hosseini E (2015) Purification and identification of antioxidant and ACE-inhibitory peptide from Saccharomyces cerevisiae protein hydrolysate. J Funct Foods 19:259–268. https://doi.org/10.1016/j.jff.2015.09.031
Hu SQ, Wang XZ, Guo SS, Li L, Hou Y (2014) Preparation and properties of bioactive peptides from yeast protein. Focus Modern Food Ind 3:52–58. https://doi.org/10.14355/fmfi.2014.03.007
Habschied K, Lončarić A, Mastanjević K (2020) Screening of polyphenols and antioxidative activity in industrial beers. Foods 9:238. https://doi.org/10.3390/foods9020238
Oliveira AS, Ferreira C, Pereira JO, Pintado ME, Carvalho AP (2022) Spent brewer's yeast (Saccharomyces cerevisiae) as a potential source of bioactive peptides: an overview. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2022.03.094
Zhang XL, Zhang YD, Wang T, Guo HY, Liu QM, Su HX (2014) Evaluation on antioxidant effect of xanthohumol by different antioxidant capacity analytical methods. J Chem. https://doi.org/10.1155/2014/249485
Żołnierczyk AK, Baczyńska D, Potaniec B, Kozłowska J, Grabarczyk M, Woźniak E, Anioł M (2017) Antiproliferative and antioxidant activity of xanthohumol acyl derivatives. Med Chem Res 26:1764–1771
Gąsior J, Kawa-Rygielska J, Kucharska AZ (2020) Carbohydrates profile, polyphenols content and antioxidative properties of beer worts produced with different dark malts varieties or roasted barley grains. Molecules 25:3882. https://doi.org/10.3390/molecules25173882
Rai Y, Pathak R, Kumari N, Sah DK, Pandey S, Kalra N, Soni R, Dwarakanath BS, Bhatt AN (2018) Mitochondrial biogenesis and metabolic hyperactivation limits the application of MTT assay in the estimation of radiation induced growth inhibition. Sci Rep. https://doi.org/10.1038/s41598-018-19930-w
Stuehr DJ (2004) Enzymes of the L-arginine to nitric oxide pathway. J Nutr. https://doi.org/10.1093/jn/134.10.2748S
Huang J, de Paulis T, May JM (2004) Antioxidant effects of dihydrocaffeic acid in human EA. hy926 endothelial cells. J Nutr Biochem. https://doi.org/10.1016/j.jnutbio.2004.07.002
Chen S, Yin DK, Yao WB, Wang YD, Zhang YR, Gao XD (2009) Macrophage receptors of polysaccharide isolated from a marine filamentous fungus Phoma herbarum YS4108. Acta Pharmacol Sin. https://doi.org/10.1038/aps.2009.93
Jung EY, Lee HS, Chang UJ, Bae SH, Kwon KH, Suh HJ (2010) Acute and subacute toxicity of yeast hydrolysate from Saccharomyces cerevisiae. Food Chem Toxicol. https://doi.org/10.1016/j.fct.2010.03.04448(6)
Vannucci L, Krizan J, Sima P, Stakheev D, Caja F, Rajsiglova L, Saieh M (2013) Immunostimulatory properties and antitumor activities of glucans. Int J Onc. https://doi.org/10.3892/ijo.2013.1974
Mantovani MS, Bellini MF, Angeli JPF, Oliveira RJ, Silva AF, Ribeiro LR (2008) β-Glucans in promoting health: prevention against mutation and cancer. Mutat Res. https://doi.org/10.1016/j.mrrev.2007.07.002
Fakruddin M, Hossain MN, Ahmed MM (2017) Antimicrobial and antioxidant activities of Saccharomyces cerevisiae IFST062013, a potential probiotic. BMC complement Altern Med. https://doi.org/10.1186/s12906-017-1591-9
Caetano JM, Parames MT, Babo MJ, Santos A, Ferreira AB, Freitas AA, Coelho MR, Mateus AM (1986) Immunopharmacological effects of Saccharomyces boulardii in healthy human volunteers. Int J immunopharmacol. https://doi.org/10.1016/0192-0561(86)90106-2
Su LJ, Zhang JH, Gomez H, Murugan R, Hong X, Xu D, Jiang F, Peng ZY (2019) Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxi Med Cell Long. https://doi.org/10.1155/2019/5080843
Scott MB, Styring AK, McCullagh JS (2022) Polyphenols: bioavailability, microbiome interactions and cellular effects on health in humans and animals. Pathogens 11:770
Cardona F, Andrés-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuño MI (2013) Benefits of polyphenols on gut microbiota and implications in human health. J Nutrit Biochem. https://doi.org/10.1016/j.jnutbio.2013.05.001
Manach C, Williamson G, Morand C, Scalbert A, Rémésy C (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr. https://doi.org/10.1093/ajcn/81.1.230S
Ruskovska T, Maksimova V, Milenkovic D (2020) Polyphenols in human nutrition: from the in vitro antioxidant capacity to the beneficial effects on cardiometabolic health and related inter-individual variability—an overview and perspective. Br J Nutr. https://doi.org/10.1017/S0007114519002733
Del Rio D, Rodriguez-Mateos A, Spencer JP, Tognolini M, Borges G, Crozier A (2013) Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal. https://doi.org/10.1089/ars.2012.4581
Vieira EF, da Silva DD, Carmo H, Ferreira IM (2017) Protective ability against oxidative stress of brewers’ spent grain protein hydrolysates. Food Chem. https://doi.org/10.1016/j.foodchem.2017.02.050
Zlotek U, Lewicki S, Markiewwicz A, Szymanowska U, Jakubczyk A (2021) Effects of drying methods on antioxidant, anti-inflammatory, and anticancer potentials of phenolic acids in lovage elicited by jasmonic acid and yeast extract. Antioxidants. https://doi.org/10.3390/antiox10050662
Machado JJC, Faria MA, MeloA, Martins ZE, Ferreira IM (2019) Modeling of α-acids and xanthohumol extraction in dry-hopped beers. Food Chem. https://doi.org/10.1016/j.foodchem.2018.11.050
Liu M, Hansen PE, Wang G, Qiu L, Dong J, Yin H, Qian Z, Yang M, Miao J (2015) Pharmacological profile of xanthohumol, a prenylated flavonoid from hops (Humulus lupulus). Molecules 20:754–779. https://doi.org/10.3390/molecules20010754
Delmulle L, Bellahcene A, Dhooge W, Comhaire F, Roelens F, Huvaere K, Heyerick A, Castronovo V, De Keukeleire D (2006) Anti-proliferative properties of prenylated flavonoids from hops (Humulus lupulus L.) in human prostate cancer cell lines. Phytomedicine 13:732–734. https://doi.org/10.1016/j.phymed.2006.01.001
Monteghirfo S, Tosetti F, Ambrosini C, Stigliani S, Pozzi S, Frassoni F, Fassina G, Soverini S, Albini A, Ferrari N (2008) Antileukemia effects of xanthohumol in Bcr/Abl-transformed cells involve nuclear factor-κB and p53 modulation. Mol Cancer Ther 7:2692–2702. https://doi.org/10.1158/1535-7163.MCT-08-0132
Harikumar KB, Kunnumakkara AB, Ahn KS, Anand P, Krishnan S, Guha S, Aggarwal BB (2009) Modification of the cysteine residues in IκBα kinase and NF-κB (p65) by xanthohumol leads to suppression of NF-κB-regulated gene products and potentiation of apoptosis in leukemia cells. Blood J Am Soc Hematol 113:2003–2013. https://doi.org/10.1182/blood-2008-04-151944
Drenzek JG, Seiler NL, Jaskula-Sztul R, Rausch MM, Rose SL (2011) Xanthohumol decreases Notch1 expression and cell growth by cell cycle arrest and induction of apoptosis in epithelial ovarian cancer cell lines. Gynecol Oncol 122:396–401. https://doi.org/10.1016/j.ygyno.2011.04.027
Ho YC, Liu C H, Chen CN, Duan KJ, Lin MT (2008) Inhibitory effects of xanthohumol from hops (Humulus lupulus L.) on human hepatocellular carcinoma cell lines. Phytother Res Int J Devoted Pharmacol Toxicol Eval Nat Prod Derivat 22:1465–1468. https://doi.org/10.1002/ptr.2481
Chen CJ, Song BA, Yang S, Xu GF, Bhadury PS, Jin LH, Hu H, Li QZ, Liu F, Xue W, Lu P, Chen Z (2007) Synthesis and antifungal activities of 5-(3,4,5-trimethoxyphenyl)-2-sulfonyl-1,3,4-thiadiazole and 5-(3,4,5-trimethoxyphenyl)-2-sulfonyl-1,3,4-oxadiazole derivatives. Bioorg Med Chem 15:3981–3989. https://doi.org/10.1016/j.bmc.2007.04.014
Festa M, Capasso A, D’Acunto CW, Masullo M, Rossi AG, Pizza C, Piacente S (2011) Xanthohumol induces apoptosis in human malignant glioblastoma cells by increasing reactive oxygen species and activating MAPK pathways. J Nat Prod 74:2505–2513. https://doi.org/10.1021/np200390x
Zajc I, Filipič M, Lah TT (2012) Xanthohumol induces different cytotoxicity and apoptotic pathways in malignant and normal astrocytes. Phytother Res 26:1709–1713. https://doi.org/10.1002/ptr.4636
Carpenter KC, Breslin WL, Davidson T, Adams A, McFarlin BK (2013) Baker's yeast β-glucan supplementation increases monocytes and cytokines post-exercise: implications for infection risk? Br J Nutr. https://doi.org/10.1017/S0007114512001407
Rahar S, Swami G, Nagpal N, Nagpal MA, Singh GS (2011) Preparation, characterization, and biological properties of β-glucans. J Adv Pharm Technol Res. https://doi.org/10.4103/2231-4040.82953
Barsanti L, Passarelli V, Evangelista V, Frassanito AM, Gualtieri P (2011) Chemistry, physico-chemistry and applications linked to biological activities of β-glucans. Nat Prod Rep. https://doi.org/10.1039/c0np00018c
Isoda N, Eguchi Y, Nukaya H, Hosho K, Suga Y, Suga T, Suga SN, Sugano K (2009) Clinical efficacy of superfine dispersed lentinan (beta-1,3-glucan) in patients with hepatocellular carcinoma. Hepatogastroenterology 56:437–441
Shimizu K, Watanabe S, Matsuda K, Suga T, Nakazawa S, Shiratori K (2009) Efficacy of oral administered superfine dispersed lentinan for advanced pancreatic cancer. Hepatogastroenterology 56:240–244
Nakashima A, Yamada K, Iwata O, Sugimoto R, Atsuji K, Ogawa T, Ishibashi-Ohgo N, Suzuki K (2018) β-Glucan in foods and its physiological functions. J Nut Sci Vitaminol. https://doi.org/10.3177/jnsv.64.8
Atila F, Owaid MN, Shariati MA (2021) The nutritional and medical benefits of Agaricus bisporus: a review. J Microbiol Biotechnol Food Sci 2021:281–286. https://doi.org/10.15414/jmbfs.2017/18.7.3.281-286
Acknowledgements
This work has the financial support of the “Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq” (424660/2018-02) and “Coordenação De Aperfeiçoamento de Pessoal de Nível Superior, CAPES” (001). E.A. Almeida is a recipient of productivity fellowship by CNPq (307390/2017-9). The authors declare no competing financial interest.
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Horn, P.A., Zeni, A.L.B., Cavichioli, N. et al. Chemical profile of craft brewer’s spent yeast and its antioxidant and antiproliferative activities. Eur Food Res Technol 249, 2001–2015 (2023). https://doi.org/10.1007/s00217-023-04268-z
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DOI: https://doi.org/10.1007/s00217-023-04268-z