antihypertension; gastrointestinal digestion; ACE inhibitory peptides; gut dysbiosis; microbiota modification
Abstract :
[en] Despite the well-established role of quinoa protein as the source of antihypertensive
peptides through in vitro enzymolysis, there is little evidence supporting the in vivo antihypertensive effect of intact quinoa protein. In this study, in vivo study on spontaneously hypertensive rats (SHRs) was conducted by administering quinoa protein for five weeks. Gastrointestinal content identification indicated that many promising precursors of bioactive peptides were released from quinoa protein under gastrointestinal processing. Quinoa protein administration on SHRs resulted in a significant decrease in blood pressure, a significant increase in alpha diversity, and microbial structure alternation towards that in non-hypertension rats. Furthermore, blood pressure was highly negatively correlated with the elevated abundance of genera in quinoa protein-treated SHRs, such as Turicibacter and Allobaculum. Interestingly, the fecal microbiota in quinoa protein-treated SHRs shared more features in the composition of genera with non-hypertension rats than that of the captopril-treated group. These results indicate that quinoa protein may serve as a potential candidate to lower blood pressure and ameliorate hypertension-related gut dysbiosis.
Disciplines :
Agriculture & agronomy
Author, co-author :
Guo, Huimin ; Université de Liège - ULiège > TERRA Research Centre
Hao, Yuqiong
Fan, Xin
Richel, Aurore ; Université de Liège - ULiège > Département GxABT > SMARTECH
Everaert, Nadia ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition
Yang, Xiushi
Ren, Guixing
Language :
English
Title :
Administration with Quinoa Protein Reduces the Blood Pressure in Spontaneously Hypertensive Rats and Modifies the Fecal Microbiota
Alternative titles :
[en] 比利时
Publication date :
2021
Journal title :
Nutrients
ISSN :
2072-6643
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
Williams, B.; Mancia, G.; Spiering, W.; Agabiti Rosei, E.; Azizi, M.; Burnier, M.; Clement, D.L.; Coca, A.; de Simone, G.; Dominiczak, A.; et al. ESC/ESH guidelines for the management of arterial hypertension. Eur. Heart J. 2018, 39, 3021–3104. [CrossRef]
Ait-Yahia, D.; Madani, S.; Savelli, J.L.; Prost, J.; Bouchenak, M.; Belleville, J. Dietary fish protein lowers blood pressure and alters tissue polyunsaturated fatty acid composition in spontaneously hypertensive rats. Nutrition 2003, 19, 342–346. [CrossRef]
Pal, S.; Ellis, V. The chronic effects of whey proteins on blood pressure, vascular function, and inflammatory markers in overweight individuals. Obesity 2010, 18, 1354–1359. [CrossRef]
de Oliveira, M.R.; Silva, T.J.; Barros, E.; Guimarães, V.M.; Baracat-Pereira, M.C.; Eller, M.R.; Reis Coimbra, J.S.; de Oliveira, E.B. Anti-Hypertensive Peptides Derived from Caseins: Mechanism of Physiological Action, Production Bioprocesses, and Challenges for Food Applications. Appl. Biochem. Biotechnol. 2018, 185, 884–908. [CrossRef]
Rai, A.K.; Sanjukta, S.; Jeyaram, K. Production of angiotensin I converting enzyme inhibitory (ACE-I) peptides during milk fermentation and their role in reducing hypertension. Crit. Rev. Food Sci. 2017, 57, 2789–2800. [CrossRef] [PubMed]
Richter, C.K.; Skulas-Ray, A.C.; Champagne, C.M.; Kris-Etherton, P.M. Plant protein and animal proteins: Do they differentially affect cardiovascular disease risk? Adv. Nutr. 2015, 6, 712–728. [CrossRef] [PubMed]
Norris, R.; FitzGerald, R.J. Antihypertensive peptides from food proteins. In Bioactive Food Peptides in Health and Disease; Hernandez-Ledesma, B., Hsieh, C.C., Eds.; InTech Publishers: London, UK, 2013; pp. 45–72.
Miralles, B.; Amigo, L.; Recio, I. Critical review and perspectives on food derived antihypertensive peptides. J. Agric. Food Chem. 2018, 66, 9384–9390. [CrossRef] [PubMed]
Lee, S.Y.; Hur, S.J. Antihypertensive peptides from animal products, marine organisms, and plants. Food Chem. 2017, 228, 506–517. [CrossRef] [PubMed]
Adnan, S.; Nelson, J.W.; Ajami, N.J.; Venna, V.R.; Petrosino, J.F.; Bryan, R.M., Jr.; Durgan, D.J. Alterations in the gut microbiota can elicit hypertension in rats. Physiol. Genom. 2017, 49, 96–104. [CrossRef]
Marques, F.Z.; Mackay, C.R.; Kaye, D.M. Beyond gut feelings: How the gut microbiota regulates blood pressure. Nat. Rev. Cardiol. 2018, 15, 20–32. [CrossRef]
Tain, Y.L.; Lee, W.C.; Wu, K.L.H.; Leu, S.; Chan, J.Y.H. Resveratrol prevents the development of hypertension programmed by maternal plus post-weaning high-fructose consumption through modulation of oxidative stress, nutrient-sensing signals, and gut microbiota. Mol. Nutr. Food Res. 2018, 62, 1800066. [CrossRef]
Yang, T.; Aquino, V.; Lobaton, G.O.; Li, H.B.; Colon-Perez, L.; Goel, R.; Qi, Y.F.; Zubcevic, J.; Febo, M.; Richards, E.M.; et al. Sustained captopril-induced reduction in blood pressure is associated with alterations in gut-brain axis in the spontaneously hypertensive rat. J. Am. Heart Assoc. 2019, 8, e010721. [CrossRef]
Jama, H.A.; Beale, A.; Shihata, W.A.; Marques, F.Z. The effect of diet on hypertensive pathology: Is there a link via gut microbiota-driven immunometabolism? Cardiovasc. Res. 2019, 115, 1435–1447. [CrossRef]
Wu, G.D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y.Y.; Keilbaugh, S.A.; Bewtra, M.; Knights, D.; Walters, W.A.; Knight, R.; et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011, 334, 105–108. [CrossRef]
Aluko, R.E.; Monu, E. Functional and bioactive properties of quinoa seed protein hydrolysates. J. Food Sci. 2003, 68, 1254–1258. [CrossRef]
Mudgil, P.; Kilari, B.P.; Kamal, H.; Olalere, O.A.; FitzGerald, R.J.; Gan, C.H.; Maqsood, S. Multifunctional bioactive peptides derived from quinoa protein hydrolysates: Inhibition of α-glucosidase, dipeptidyl peptidase-IV and angiotensin I converting enzymes. J. Cereal Sci. 2020, 96, 103130. [CrossRef]
Ujiroghene, O.J.; Liu, L.; Zhang, S.W.; Lu, J.; Pang, X.Y.; Lv, J.P. α-Glucosidase and ACE dual inhibitory protein hydrolysates and peptide fractions of sprouted quinoa yoghurt beverages inoculated with Lactobacillus casei. Food Chem. 2019, 299, 124985.
Zheng, Y.J.; Wang, X.; Zhuang, Y.L.; Li, Y.; Tian, H.L.; Shi, P.Q.; Li, G.F. Isolation of novel ACE-inhibitory and antioxidant peptides from quinoa bran albumin assisted with an in silico approach: Characterization, in vivo antihypertension, and molecular docking. Molecules 2019, 24, 4562. [CrossRef]
Guo, H.M.; Hao, Y.Q.; Richel, A.; Everaert, N.; Chen, Y.H.; Liu, M.J.; Yang, X.S.; Ren, G.X. Antihypertensive effect of quinoa protein under simulated gastrointestinal digestion and peptide characterization. J. Sci. Food Agric. 2020, 100, 5569–5576. [CrossRef]
Guo, H.M.; Richel, A.; Hao, Y.Q.; Everaert, N.; Yang, X.S.; Ren, G.X. Novel dipeptidyl peptidase-IV and angiotensin-I-converting enzyme inhibitory peptides released from quinoa protein by in silico proteolysis. Food Sci. Nutr. 2020, 8, 1415–1422. [CrossRef]
Fritz, M.; Rinaldi, G. Blood pressure measurement with the tail-cuff method in Wistar and spontaneously hypertensive rats: Influence of adrenergic-and nitric oxide-mediated vasomotion. J. Pharmacol. Toxicol. Methods 2008, 58, 215–221. [CrossRef] [PubMed]
Boutrou, R.; Gaudichon, C.; Dupont, D.; Jardin, J.; Airinei, G.; Marsset-Baglieri, A.; Benamouzig, R.; Tome, D.; Leonil, J. Sequential release of milk protein-derived bioactive peptides in the jejunum in healthy humans. Am. J. Clin. Nutr. 2013, 97, 1314–1323. [CrossRef]
Boutrou, R.; Henry, G.; Sanchez-Rivera, L. On the trail of milk bioactive peptides in human and animal intestinal tracts during digestion: A review. Dairy Sci. Technol. 2015, 95, 815–829. [CrossRef]
Portune, K.J.; Beaumont, M.; Davila, A.M.; Tomé, D.; Blachier, F.; Sanz, Y. Gut microbiota role in dietary protein metabolism and health-related outcomes: The two sides of the coin. Trends Food Sci. Technol. 2016, 57, 213–232. [CrossRef]
Davila, A.M.; Blachier, F.; Gotteland, M.; Andriamihaja, M.; Benetti, P.H.; Sanz, Y.; Tomé, D. Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host. Pharmacol. Res. 2013, 68, 95–107. [CrossRef]
Barbe, F.; Le Feunteun, S.; Remond, D.; Ménard, O.; Jardin, J.; Henry, G.; Laroche, B.; Dupont, D. Tracking the in vivo release of bioactive peptides in the gut during digestion: Mass spectrometry peptidomic characterization of effluents collected in the gut of dairy matrix. Food Res. Int. 2014, 63, 147–156. [CrossRef]
Volpe, M.; Gallo, G.; Tocci, G. Is early and fast blood pressure control important in hypertension management? Int. J. Cardiol. 2018, 254, 328–332. [CrossRef]
Gupta, R.; Guptha, S. Strategies for initial management of hypertension. Indian J. Med. Res. 2010, 132, 531–542.
Mell, B.; Jala, V.R.; Mathew, A.V.; Byun, J.; Waghulde, H.; Zhang, Y.; Haribabu, B.; Vijay-Kumar, M.; Pennathur, S.; Joe, B. Evidence for a link between gut microbiota and hypertension in the Dahl rat. Physiol. Genom. 2015, 47, 187–197. [CrossRef] [PubMed]
Durgan, D.J.; Ganesh, B.P.; Cope, J.L.; Ajami, N.J.; Phillips, S.C.; Petrosino, J.F.; Hollister, E.B.; Bryan, R.M. Role of the gut microbiome in obstructive sleep apnea-induced hypertension. Hypertension 2016, 67, 469–474. [CrossRef] [PubMed]
Yang, T.; Santisteban, M.M.; Rodriguez, V.; Li, E.; Ahmari, N.; Marulanda Carvajal, J.; Zadeh, M.; Gong, M.; Qi, Y.; Zubcevic, J.; et al. Gut dysbiosis is linked to hypertension. Hypertension 2015, 65, 1331–1340. [CrossRef] [PubMed]
Hoffman, J.D.; Parikh, I.; Green, S.J.; Chlipala, G.; Mohney, R.P.; Keaton, M.; Bauer, B.; Hartz, A.M.S.; Lin, A.L. Age drives distortion of brain metabolic, vascular and cognitive functions, and the gut microbiome. Front. Aging Neurosci. 2017, 9, 298. [CrossRef] [PubMed]
Badal, V.D.; Vaccariello, E.D.; Murray, E.R.; Yu, K.E.; Knight, R.; Jeste, D.V.; Nguyen, T.T. The gut microbiome, aging, and longevity: A systematic review. Nutrients 2020, 12, 3759. [CrossRef]
Lopetuso, L.R.; Quagliariello, A.; Schiavoni, M.; Petito, V.; Russo, A.; Reddel, S.; Chierico, F.D.; Ianiro, G.; Scaldaferri, F.; Neri, M.; et al. Towards a disease-associated common trait of gut microbiota dysbiosis: The pivotal role of Akkermansia muciniphila. Digest. Liver Dis. 2020, 52, 1002–1010. [CrossRef] [PubMed]
Liu, G.; Bei, J.; Liang, L.; Yu, G.; Li, L.; Li, Q. Stachyose improves inflammation through modulating gut microbiota of high-fat diet/streptozotocin-induced type 2 diabetes in rats. Mol. Nutr. Food Res. 2018, 62, 1700954. [CrossRef]
Gu, Z.; Zhu, Y.; Jiang, S.; Xia, G.; Li, C.; Zhang, X.; Zhang, J.; Shen, X. Tilapia head glycolipids reduce inflammation by regulating the gut microbiota in dextran sulphate sodium-induced colitis mice. Food Funct. 2020, 11, 3245–3255. [CrossRef]
Presley, L.L.; Wei, B.; Braun, J.; Borneman, J. Bacteria associated with immunoregulatory cells in mice. Appl. Environ. Microbiol. 2010, 76, 936–941. [CrossRef]
Zhong, Y.; Nyman, M.; Fak, F. Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barley malt. Mol. Nutr. Food Res. 2015, 59, 2066–2076. [CrossRef] [PubMed]
Naqvi, S.; Asar, T.O.; Kumar, V.; Al-Abbasi, F.A.; Alhayyani, S.; Kamal, M.A.; Anwar, F. A cross-talk between gut microbiome, salt and hypertension. Biomed. Pharmacother. 2021, 134, 111156. [CrossRef] [PubMed]
Metzler-Zebeli, B.U.; Mann, E.; Schmitz-Esser, S.; Wagner, M.; Ritzmann, M.; Zebelib, Q. Changing dietary calcium-phosphorus level and cereal source selectively alters abundance of bacteria and metabolites in the upper gastrointestinal tracts of weaned pigs. Appl. Environ. Microbiol. 2013, 79, 7264–7272. [CrossRef] [PubMed]
Al Khodor, S.; Reichert, B.; Shatat, I.F. The microbiome and blood pressure: Can microbes regulate our blood pressure? Front. Pediatr. 2017, 5, 138. [CrossRef] [PubMed]
Zhang, L.S.; Davies, S.S. Microbial metabolism of dietary components to bioactive metabolites: Opportunities for new therapeutic interventions. Genome Med. 2016, 8, 46. [CrossRef] [PubMed]