Impact of in vitro gastrointestinal digestion and transepithelial transport on antioxidant and ACE-inhibitory activities of Brewer's spent yeast autolysate

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 39, 2016, Pages 7335-7341

  Vieira, Elsa F ^a   Das Neves, José ^b,c,d   Vitorino, Rui ^e,f   Dias Da Silva, Diana ^a   Carmo, Helena ^a   Ferreira, Isabel M P L V O ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^d UNIVERSITY INSTITUTE OF HEALTH SCIENCES IUCS   (Portugal)

^e UNIVERSITY OF AVEIRO   (Portugal)

^f University of Porto   (Portugal)

Author keywords

ACE inhibitory activity; antioxidant activity; Brewer's spent yeast; gastrointestinal digestion; transepithelial transport

Indexed keywords

CELLS; CYTOLOGY; CYTOTOXICITY; MONOLAYERS; PEPTIDES; YEAST;

ACE-INHIBITORY ACTIVITY; ANTI-OXIDANT ACTIVITIES; BIOACTIVE COMPOUNDS; CONCENTRATION RANGES; CYTOTOXIC EFFECTS; GASTROINTESTINAL; GASTROINTESTINAL DIGESTION; TRANSEPITHELIAL TRANSPORT;

ANTIOXIDANTS;

ANTIOXIDANT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; FUNGAL PROTEIN; PEPTIDE; PROTEIN HYDROLYSATE;

CACO-2 CELL LINE; CELL SURVIVAL; CHEMISTRY; COCULTURE; DIGESTION; GASTROINTESTINAL ABSORPTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; PERMEABILITY; SACCHAROMYCES CEREVISIAE; TRANSPORT AT THE CELLULAR LEVEL;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTIOXIDANTS; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COCULTURE TECHNIQUES; DIGESTION; FUNGAL PROTEINS; GASTROINTESTINAL ABSORPTION; HUMANS; PEPTIDES; PERMEABILITY; PROTEIN HYDROLYSATES; SACCHAROMYCES CEREVISIAE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84990038900     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b02719     Document Type: Article

References (33)

1. Ferreira, I. M. P. L. V. O.; Pinho, O.; Vieira, E.; Tavarela, J. G. Brewer's Saccharomyces yeast biomass: characteristics and potential applications Trends Food Sci. Technol. 2010, 21, 77-84 10.1016/j.tifs.2009.10.008
2. Mussatto, S. I. Biotechnological potential of brewing industry by-products. In Biotechnology for agro-industrial residues utilisation; Springer: 2009; pp 313-326.
3. Thammakiti, S.; Suphantharika, M.; Phaesuwan, T.; Verduyn, C. Preparation of spent brewer's yeast β-glucans for potential applications in the food industry Int. J. Food Sci. Technol. 2004, 39, 21-29 10.1111/j.1365-2621.2004.00742.x
4. Vieira, E.; Brandão, T.; Ferreira, I. M. P. L. V. O. Evaluation of Brewer's spent yeast to produce flavor enhancer nucleotides: Influence of serial repitching J. Agric. Food Chem. 2013, 61, 8724-8729 10.1021/jf4021619
5. Tanguler, H.; Erten, H. Utilisation of spent brewer's yeast for yeast extract production by autolysis: The effect of temperature Food Bioprod. Process. 2008, 86, 317-321 10.1016/j.fbp.2007.10.015
6. Boonyeun, P.; Shotipruk, A.; Prommuak, C.; Suphantharika, M.; Muangnapoh, C. Enhancement of amino acid production by two-step autolysis of spent brewer's yeast Chem. Eng. Commun. 2011, 198, 1594-1602 10.1080/00986445.2011.560219
7. Estevez, P. M. M. Process for obtaining bioactive peptide and polysaccharide extracts from spent brewers yeast and uses thereof. Patent WO2014102757A1. 2014.
8. Vieira, E.; Teixeira, J.; Ferreira, I. M. Valorization of brewers' spent grain and spent yeast through protein hydrolysates with antioxidant properties Eur. Food Res. Technol. 2016, 1-10 10.1007/s00217-016-2696-y
9. Lea, T., Caco-2 Cell Line. In The impact of food bioactives on health, in vitro and ex vivo models; Verhoeckx, K.; Cotter, P.; López-Expósito, I.; Kleiveland, C.; Lea, T.; Mackie, A.; Requena, T.; Swiatecka, D.; Wichers, H., Eds.; Springer International Publishing: 2015; pp 103-111.
10. Antunes, F.; Andrade, F.; Araujo, F.; Ferreira, D.; Sarmento, B. Establishment of a triple co-culture in vitro cell models to study intestinal absorption of peptide drugs Eur. J. Pharm. Biopharm. 2013, 83, 427-35 10.1016/j.ejpb.2012.10.003
11. Gallego, M.; Grootaert, C.; Mora, L.; Aristoy, M. C.; Van Camp, J.; Toldrá, F. Transepithelial transport of dry-cured ham peptides with ACE inhibitory activity through a Caco-2 cell monolayer J. Funct. Foods 2016, 21, 388-395 10.1016/j.jff.2015.11.046
12. Musatti, A.; Devesa, V.; Calatayud, M.; Vélez, D.; Manzoni, M.; Rollini, M. Glutathione-enriched baker's yeast: production, bioaccessibility and intestinal transport assays J. Appl. Microbiol. 2014, 116, 304-313 10.1111/jam.12363
13. Cinq-Mars, C. D.; Hu, C.; Kitts, D. D.; Li-Chan, E. C. Investigations into inhibitor type and mode, simulated gastrointestinal digestion, and cell transport of the angiotensin I-converting enzyme-inhibitory peptides in Pacific hake (Merluccius productus) fillet hydrolysate J. Agric. Food Chem. 2008, 56, 410-9 10.1021/jf072277p
14. Calatayud, M.; Vazquez, M.; Devesa, V.; Velez, D. In vitro study of intestinal transport of inorganic and methylated arsenic species by Caco-2/HT29-MTX cocultures Chem. Res. Toxicol. 2012, 25, 2654-62 10.1021/tx300295n
15. Kosińska, A.; Andlauer, W. Modulation of tight junction integrity by food components Food Res. Int. 2013, 54, 951-960 10.1016/j.foodres.2012.12.038
16. Kleiveland, C. R. Co-cultivation of Caco-2 and HT-29MTX. In The impact of food bioactives on health, in vitro and ex vivo models; Verhoeckx, K.; Cotter, P.; López-Expósito, I.; Kleiveland, C.; Lea, T.; Mackie, A.; Requena, T.; Swiatecka, D.; Wichers, H., Eds.; Springer International Publishing: 2015; pp 135-140.
17. Bradford Protein Assay. Bio-protocol Bio101: e45. http://www.bio-protocol.org/e45. 2011.
18. Samaranayaka, A. G.; Kitts, D. D.; Li-Chan, E. C. Antioxidative and angiotensin-I-converting enzyme inhibitory potential of a Pacific Hake (Merluccius productus) fish protein hydrolysate subjected to simulated gastrointestinal digestion and Caco-2 cell permeation J. Agric. Food Chem. 2010, 58, 1535-42 10.1021/jf9033199
19. Jansen, E.; Ruskovska, T. Comparative analysis of serum (anti)oxidative status parameters in healthy persons Int. J. Mol. Sci. 2013, 14, 6106-6115 10.3390/ijms14036106
20. Sentandreu, M. á.; Toldrá, F. A rapid, simple and sensitive fluorescence method for the assay of angiotensin-I converting enzyme Food Chem. 2006, 97, 546-554 10.1016/j.foodchem.2005.06.006
21. Quiros, A.; del Mar Contreras, M.; Ramos, M.; Amigo, L.; Recio, I. Stability to gastrointestinal enzymes and structure-activity relationship of beta-casein-peptides with antihypertensive properties Peptides 2009, 30, 1848-53 10.1016/j.peptides.2009.06.031
22. Béduneau, A.; Tempesta, C.; Fimbel, S.; Pellequer, Y.; Jannin, V.; Demarne, F.; Lamprecht, A. A tunable Caco-2/HT29-MTX co-culture model mimicking variable permeabilities of the human intestine obtained by an original seeding procedure Eur. J. Pharm. Biopharm. 2014, 87, 290-298 10.1016/j.ejpb.2014.03.017
23. Laitinen, L. A.; Galkin, A.; Vuorela, H. J.; Marvola, M. L.; Vuorela, P. M. Effects of extracts of commonly consumed food supplements and food fractions on the permeability of drugs across Caco-2 cell monolayers Pharm. Res. 2004, 21, 1904-1916 10.1023/B:PHAM.0000045246.94064.ab
24. da Silva, D. D.; Silva, E.; Carmo, H. Combination effects of amphetamines under hyperthermia-the role played by oxidative stress J. Appl. Toxicol. 2014, 34, 637-50 10.1002/jat.2889
25. Ferraro, V.; Ferreira Jorge, R.; Cruz, I. B.; Antunes, F.; Sarmento, B.; Castro, P. M. L.; Pintado, M. E. In vitro intestinal absorption of amino acid mixtures extracted from codfish (Gadus morhua L.) salting wastewater Int. J. Food Sci. Technol. 2014, 49, 27-33 10.1111/ijfs.12269
26. Ferreira, I. M. P. L. V. O.; Eça, R.; Pinho, O.; Tavares, P.; Pereira, A.; Cecília Roque, A. Development and validation of an HPLC/UV method for quantification of bioactive peptides in fermented milks J. Liq. Chromatogr. Relat. Technol. 2007, 30, 2139-2147 10.1080/10826070701435145
27. Putnam, K. P.; Bombick, D. W.; Doolittle, D. J. Evaluation of eight in vitro assays for assessing the cytotoxicity of cigarette smoke condensate Toxicol. In Vitro 2002, 16, 599-607 10.1016/S0887-2333(02)00050-4
28. Ward, M. W.; Huber, H. J.; Weisova, P.; Dussmann, H.; Nicholls, D. G.; Prehn, J. H. Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance J. Neurosci. 2007, 27, 8238-49 10.1523/JNEUROSCI.1984-07.2007
29. Ding, L.; Wang, L.; Zhang, Y.; Liu, J. Transport of antihypertensive peptide RVPSL, ovotransferrin 328-332, in human intestinal Caco-2 Cell monolayers J. Agric. Food Chem. 2015, 63, 8143-8150 10.1021/acs.jafc.5b01824
30. Yee, S. In vitro permeability across Caco-2 cells (colonic) can predict in vivo (small intestinal) absorption in man-fact or myth Pharm. Res. 1997, 14, 763-766 10.1023/A:1012102522787
31. Araujo, F.; Sarmento, B. Towards the characterization of an in vitro triple co-culture intestine cell model for permeability studies Int. J. Pharm. 2013, 458, 128-34 10.1016/j.ijpharm.2013.10.003
32. Jin, Y.; Song, Y.; Zhu, X.; Zhou, D.; Chen, C.; Zhang, Z.; Huang, Y. Goblet cell-targeting nanoparticles for oral insulin delivery and the influence of mucus on insulin transport Biomaterials 2012, 33, 1573-82 10.1016/j.biomaterials.2011.10.075
33. Escudero, E.; Mora, L.; Toldrá, F. Stability of ACE inhibitory ham peptides against heat treatment and in vitro digestion Food Chem. 2014, 161, 305-311 10.1016/j.foodchem.2014.03.117