Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Dietary Protein and Gut Microbiota Composition and Function

Author(s): Jianfei Zhao, Xiaoya Zhang, Hongbin Liu, Michael A. Brown and Shiyan Qiao*

Volume 20, Issue 2, 2019

Page: [145 - 154] Pages: 10

DOI: 10.2174/1389203719666180514145437

Price: $65

Abstract

Dietary protein and its metabolites, amino acids, are essential nutrients for humans and animals. Accumulated research has revealed that the gut microbiota mediate the crosstalk between protein metabolism and host immune response. Gut microbes are involved in the digestion, absorption, metabolism and transformation process of dietary protein in the gastrointestinal tract. Amino acids can be metabolized into numerous microbial metabolites, and these metabolites participate in various physiological functions related to host health and diseases. The components of dietary protein impact the gut microbiota composition and microbial metabolites. The source, concentration, and amino acid balance of dietary protein are primary factors which contribute to the composition, structure and function of gut microbes. A suitable ratio between protein and carbohydrate or even a low protein diet is recommended over a diet with protein in excess of requirements. Greater levels and undigested protein lead to an increase of pathogenic microorganism with associated higher risk of metabolic diseases. Herein, the crosstalk between dietary protein and gut microbiota composition and function is summarized, which will help to reveal the potential mechanism of gut microbes on the gastrointestinal tract health.

Keywords: Dietary protein metabolism, gut microbiota, metabolites, amino acid transporter, mucosal barrier, host health.

Graphical Abstract
[1]
Davila, A.M.; Blachier, F.; Gotteland, M.; Andriamihaja, M.; Benetti, P.H.; Sanz, Y.; Tome, D. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacol. Res., 2013, 68, 95-107.
[2]
Bishu, S. Sensing of nutrients and microbes in the gut. Curr. Opin. Gastroenterol., 2016, 32, 86-95.
[3]
Hughes, R.; Magee, E.A.; Bingham, S. Protein degradation in the large intestine: Relevance to colorectal cancer. Curr. Issues Intest. Microbiol., 2000, 1, 51-58.
[4]
Wikoff, W.R.; Anfora, A.T.; Liu, J.; Schultz, P.G.; Lesley, S.A.; Peters, E.C.; Siuzdak, G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA, 2009, 106, 3698-3703.
[5]
Fan, P.; Li, L.; Rezaei, A.; Eslamfam, S.; Che, D.; Ma, X. Metabolites of dietary protein and peptides by intestinal microbes and their impacts on gut. Curr. Protein Pept. Sci., 2015, 16, 646-654.
[6]
Shanahan, M.T.; Carroll, I.M.; Gulati, A.S. Critical design aspects involved in the study of Paneth cells and the intestinal microbiota. Gut Microbes, 2014, 5, 208-214.
[7]
Fan, P.; Liu, P.; Song, P.; Chen, X.; Ma, X. Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model. Sci. Rep., 2017, 7, 43412.
[8]
Macfarlane, G.T.; Allison, C.; Gibson, S.A.; Cummings, J.H. Contribution of the microflora to proteolysis in the human large intestine. J. Appl. Bacteriol., 1988, 64, 37-46.
[9]
He, L.; Han, M.; Qiao, S.; He, P.; Li, D.; Li, N.; Ma, X. Soybean antigen proteins and their intestinal sensitization activities. Curr. Protein Pept. Sci., 2015, 16, 613-621.
[10]
Libao-Mercado, A.J.; Zhu, C.L.; Cant, J.P.; Lapierre, H.; Thibault, J.N.; Seve, B.; Fuller, M.F.; de Lange, C.F. Dietary and endogenous amino acids are the main contributors to microbial protein in the upper gut of normally nourished pigs. J. Nutr., 2009, 139, 1088-1094.
[11]
Laparra, J.M.; Sanz, Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol. Res., 2010, 61, 219-225.
[12]
Cani, P.D.; Everard, A.; Duparc, T. Gut microbiota, enteroendocrine functions and metabolism. Curr. Opin. Pharmacol., 2013, 13, 935-940.
[13]
Metges, C.C. Contribution of microbial amino acids to amino acid homeostasis of the host. J. Nutr., 2000, 130, 1857S-1864S.
[14]
Torrallardona, D.; Harris, C.I.; Fuller, M.F. Microbial amino acid synthesis and utilization in rats: The role of coprophagy. Br. J. Nutr., 1996, 76, 701-709.
[15]
Grohmann, U.; Bronte, V. Control of immune response by amino acid metabolism. Immunol. Rev., 2010, 236, 243-264.
[16]
Stoll, B.; Henry, J.; Reeds, P.J.; Yu, H.; Jahoor, F.; Burrin, D.G. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. J. Nutr., 1998, 128, 606-614.
[17]
Pridmore, R.D.; Berger, B.; Desiere, F.; Vilanova, D.; Barretto, C.; Pittet, A.C.; Zwahlen, M.C.; Rouvet, M.; Altermann, E.; Barrangou, R.; Mollet, B.; Mercenier, A.; Klaenhammer, T.; Arigoni, F.; Schell, M.A. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc. Natl. Acad. Sci. USA, 2004, 101, 2512-2517.
[18]
Riepe, S.P.; Goldstein, J.; Alpers, D.H. Effect of secreted Bacteroides proteases on human intestinal brush border hydrolases. J. Clin. Invest., 1980, 66, 314-322.
[19]
Baglieri, A.; Mahe, S.; Zidi, S.; Huneau, J.F.; Thuillier, F.; Marteau, P.; Tome, D. Gastro-jejunal digestion of soya-bean-milk protein in humans. Br. J. Nutr., 1994, 72, 519-532.
[20]
Gaudichon, C.; Mahe, S.; Benamouzig, R.; Luengo, C.; Fouillet, H.; Dare, S.; Van Oycke, M.; Ferriere, F.; Rautureau, J.; Tome, D. Net postprandial utilization of [15N]-labeled milk protein nitrogen is influenced by diet composition in humans. J. Nutr., 1999, 129, 890-895.
[21]
Bos, C.; Juillet, B.; Fouillet, H.; Turlan, L.; Dare, S.; Luengo, C.; N’Tounda, R.; Benamouzig, R.; Gausseres, N.; Tome, D.; Gaudichon, C. Postprandial metabolic utilization of wheat protein in humans. Am. J. Clin. Nutr., 2005, 81, 87-94.
[22]
Evenepoel, P.; Claus, D.; Geypens, B.; Hiele, M.; Geboes, K.; Rutgeerts, P.; Ghoos, Y. Amount and fate of egg protein escaping assimilation in the small intestine of humans. Am. J. Physiol., 1999, 277, G935-G943.
[23]
Blachier, F.; Mariotti, F.; Huneau, J.F.; Tome, D. Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids, 2007, 33, 547-562.
[24]
Barker, H.A. Amino acid degradation by anaerobic bacteria. Annu. Rev. Biochem., 1981, 50, 23-40.
[25]
Macfarlane, S.; Macfarlane, G.T. Regulation of short-chain fatty acid production. Proc. Nutr. Soc., 2003, 62, 67-72.
[26]
Maslowski, K.M.; Vieira, A.T.; Ng, A.; Kranich, J.; Sierro, F.; Yu, D.; Schilter, H.C.; Rolph, M.S.; Mackay, F.; Artis, D.; Xavier, R.J.; Teixeira, M.M.; Mackay, C.R. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature, 2009, 461, 1282-1286.
[27]
den Besten, G.; van Eunen, K.; Groen, A.K.; Venema, K.; Reijngoud, D.J.; Bakker, B.M. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res., 2013, 54, 2325-2340.
[28]
Tolhurst, G.; Heffron, H.; Lam, Y.S.; Parker, H.E.; Habib, A.M.; Diakogiannaki, E.; Cameron, J.; Grosse, J.; Reimann, F.; Gribble, F.M. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes, 2012, 61, 364-371.
[29]
Chen, J.; Li, Y.; Tian, Y.; Huang, C.; Li, D.; Zhong, Q.; Ma, X. Interaction between microbes and host intestinal health: Modulation by dietary nutrients and gut-brain-endocrine-immune axis. Curr. Protein Pept. Sci., 2015, 16, 592-603.
[30]
Yano, J.M.; Yu, K.; Donaldson, G.P.; Shastri, G.G.; Ann, P.; Ma, L.; Nagler, C.R.; Ismagilov, R.F.; Mazmanian, S.K.; Hsiao, E.Y. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell, 2015, 161, 264-276.
[31]
Hamer, H.M.; Jonkers, D.; Venema, K.; Vanhoutvin, S.; Troost, F.J.; Brummer, R.J. Review article: The role of butyrate on colonic function. Aliment. Pharmacol. Ther., 2008, 27, 104-119.
[32]
Thibault, R.; Blachier, F.; Darcy-Vrillon, B.; de Coppet, P.; Bourreille, A.; Segain, J.P. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: A transport deficiency. Inflamm. Bowel Dis., 2010, 16, 684-695.
[33]
Morrison, D.J.; Preston, T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes, 2016, 7, 189-200.
[34]
Brim, H.; Kumar, K.; Nazarian, J.; Hathout, Y.; Jafarian, A.; Lee, E.; Green, W.; Smoot, D.; Park, J.; Nouraie, M.; Ashktorab, H. SLC5A8 gene, a transporter of butyrate: A gut flora metabolite, is frequently methylated in African American colon adenomas. PLoS One, 2011, 6, e20216.
[35]
Ganapathy, V.; Gopal, E.; Miyauchi, S.; Prasad, P.D. Biological functions of SLC5A8, a candidate tumour suppressor. Biochem. Soc. Trans., 2005, 33, 237-240.
[36]
Liu, H.; Wang, J.; He, T.; Becker, S.; Zhang, G.; Li, D.; Ma, X. Butyrate: A double-edged sword for health? Adv. Nutr., 2018, 9(1), 21-29.
[37]
Sunkara, L.T.; Achanta, M.; Schreiber, N.B.; Bommineni, Y.R.; Dai, G.; Jiang, W.; Lamont, S.; Lillehoj, H.S.; Beker, A.; Teeter, R.G.; Zhang, G. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS One, 2011, 6, e27225.
[38]
Mouille, B.; Robert, V.; Blachier, F. Adaptative increase of ornithine production and decrease of ammonia metabolism in rat colonocytes after hyperproteic diet ingestion. Am. J. Physiol. Gastrointest. Liver Physiol., 2004, 287, G344-G351.
[39]
Eklou-Lawson, M.; Bernard, F.; Neveux, N.; Chaumontet, C.; Bos, C.; Davila-Gay, A.M.; Tome, D.; Cynober, L.; Blachier, F. Colonic luminal ammonia and portal blood L-glutamine and L-arginine concentrations: A possible link between colon mucosa and liver ureagenesis. Amino Acids, 2009, 37, 751-760.
[40]
Handlogten, M.E.; Hong, S.P.; Zhang, L.; Vander, A.W.; Steinbaum, M.L.; Campbell-Thompson, M.; Weiner, I.D. Expression of the ammonia transporter proteins Rh B glycoprotein and Rh C glycoprotein in the intestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol., 2005, 288, G1036-G1047.
[41]
Ma, N.; Wu, Y.; Xie, F.; Du, K.; Wang, Y.; Shi, L.; Ji, L.; Liu, T.; Ma, X. Dimethyl fumarate reduces the risk of mycotoxins via improving intestinal barrier and microbiota. Oncotarget, 2017, 8, 44625-44638.
[42]
Fan, P.; Song, P.; Li, L.; Huang, C.; Chen, J.; Yang, W.; Qiao, S.; Wu, G.; Zhang, G.; Ma, X. Roles of biogenic amines in intestinal signaling. Curr. Protein Pept. Sci., 2017, 18, 532-540.
[43]
Awano, N.; Wada, M.; Mori, H.; Nakamori, S.; Takagi, H. Identification and functional analysis of Escherichia coli cysteine desulfhydrases. Appl. Environ. Microbiol., 2005, 71, 4149-4152.
[44]
Smith, E.A.; Macfarlane, G.T. Dissimilatory amino Acid metabolism in human colonic bacteria. Anaerobe, 1997, 3, 327-337.
[45]
Mouille, B.; Morel, E.; Robert, V.; Guihot-Joubrel, G.; Blachier, F. Metabolic capacity for L-citrulline synthesis from ammonia in rat isolated colonocytes. Biochim. Biophys. Acta, 1999, 1427, 401-407.
[46]
Fan, P.; Tan, Y.; Jin, K.; Lin, C.; Xia, S.; Han, B.; Zhang, F.; Wu, L.; Ma, X. Supplemental lipoic acid relieves post-weaning diarrhoea by decreasing intestinal permeability in rats. J. Anim. Physiol. Anim. Nutr. (Berl.), 2017, 101, 136-146.
[47]
Noack, J.; Dongowski, G.; Hartmann, L.; Blaut, M. The human gut bacteria Bacteroides thetaiotaomicron and Fusobacterium varium produce putrescine and spermidine in cecum of pectin-fed gnotobiotic rats. J. Nutr., 2000, 130, 1225-1231.
[48]
Nowak, A.; Libudzisz, Z. Influence of phenol, p-cresol and indole on growth and survival of intestinal lactic acid bacteria. Anaerobe, 2006, 12, 80-84.
[49]
Smith, E.A.; Macfarlane, G.T. Formation of phenolic and indolic compounds by anaerobic bacteria in the human large intestine. Microb. Ecol., 1997, 33, 180-188.
[50]
Macfarlane, G.T.; Macfarlane, S. Human colonic microbiota: Ecology, physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. Suppl., 1997, 222, 3-9.
[51]
Windey, K.; De Preter, V.; Verbeke, K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res., 2012, 56, 184-196.
[52]
Hughes, R.; Kurth, M.J.; McGilligan, V.; McGlynn, H.; Rowland, I. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutr. Cancer, 2008, 60, 259-266.
[53]
Pedersen, G.; Brynskov, J.; Saermark, T. Phenol toxicity and conjugation in human colonic epithelial cells. Scand. J. Gastroenterol., 2002, 37, 74-79.
[54]
Klose, V.; Bayer, K.; Bruckbeck, R.; Schatzmayr, G.; Loibner, A.P. In vitro antagonistic activities of animal intestinal strains against swine-associated pathogens. Vet. Microbiol., 2010, 144, 515-521.
[55]
Sørensen, M.T.; Vestergaard, E.; Jensen, S.K.; Lauridsen, C.; Højsgaard, S. Performance and diarrhoea in piglets following weaning at seven weeks of age: Challenge with E. coli O 149 and effect of dietary factors. Livestock Science, 2009, 123, 314-321.
[56]
Espeche, T.M.; de Moreno, D.L.A.; Perdigon, G.; Savoy, D.G.G.; Hebert, E.M. beta-Casein hydrolysate generated by the cell envelope-associated proteinase of Lactobacillus delbrueckii ssp. Lactis CRL 581 protects against trinitrobenzene sulfonic acid-induced colitis in mice. J. Dairy Sci., 2012, 95, 1108-1118.
[57]
Farooq, S.; Hussain, I.; Mir, M.A.; Bhat, M.A.; Wani, S.A. Isolation of atypical enteropathogenic Escherichia coli and Shiga toxin 1 and 2f-producing Escherichia coli from avian species in India. Lett. Appl. Microbiol., 2009, 48, 692-697.
[58]
Peng, M.; Bitsko, E.; Biswas, D. Functional properties of peanut fractions on the growth of probiotics and foodborne bacterial pathogens. J. Food Sci., 2015, 80, M635-M641.
[59]
Lozupone, C.A.; Stombaugh, J.I.; Gordon, J.I.; Jansson, J.K.; Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature, 2012, 489, 220-230.
[60]
Tremaroli, V.; Bäckhed, F. Functional interactions between the gut microbiota and host metabolism. Nature, 2012, 489, 242-249.
[61]
Deplancke, B.; Gaskins, H.R. Microbial modulation of innate defense: Goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr., 2001, 73, 1131S-1141S.
[62]
Hooper, L.V.; Littman, D.R.; Macpherson, A.J. Interactions between the microbiota and the immune system. Science, 2012, 336, 1268-1273.
[63]
Liu, H.; Zhang, J.; Zhang, S.; Yang, F.; Thacker, P.A.; Zhang, G.; Qiao, S.; Ma, X. Oral administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. J. Agric. Food Chem., 2014, 62, 860-866.
[64]
Ma, X.; He, P.; Sun, P.; Han, P. Lipoic acid: An immunomodulator that attenuates glycinin-induced anaphylactic reactions in a rat model. J. Agric. Food Chem., 2010, 58, 5086-5092.
[65]
Hu, S.; Liu, H.; Qiao, S.; He, P.; Ma, X.; Lu, W. Development of immunoaffinity chromatographic method for isolating glycinin (11S) from soybean proteins. J. Agric. Food Chem., 2013, 61, 4406-4410.
[66]
Putignani, L.; Dallapiccola, B. Foodomics as part of the host-microbiota-exposome interplay. J. Proteomics, 2016, 147, 3-20.
[67]
Pluske, J.R.; Pethick, D.W.; Hopwood, D.E.; Hampson, D.J. Nutritional influences on some major enteric bacterial diseases of pig. Nutr. Res. Rev., 2002, 15, 333-371.
[68]
Morita, T.; Kasaoka, S.; Kiriyama, S. Physiological functions of resistant proteins: Proteins and peptides regulating large bowel fermentation of indigestible polysaccharide. J. AOAC Int., 2004, 87, 792-796.
[69]
Hancock, R.E.; Haney, E.F.; Gill, E.E. The immunology of host defence peptides: beyond antimicrobial activity. Nat. Rev. Immunol., 2016, 16, 321-334.
[70]
Faith, J.J.; McNulty, N.P.; Rey, F.E.; Gordon, J.I. Predicting a human gut microbiota’s response to diet in gnotobiotic mice. Science, 2011, 333, 101-104.
[71]
Neis, E.P.; Dejong, C.H.; Rensen, S.S. The role of microbial amino acid metabolism in host metabolism. Nutrients, 2015, 7, 2930-2946.
[72]
Tilg, H.; Moschen, A.R. Food, immunity, and the microbiome. Gastroenterology, 2015, 148, 1107-1119.
[73]
Kau, A.L.; Ahern, P.P.; Griffin, N.W.; Goodman, A.L.; Gordon, J.I. Human nutrition, the gut microbiome and the immune system. Nature, 2011, 474, 327-336.
[74]
Gensollen, T.; Iyer, S.S.; Kasper, D.L.; Blumberg, R.S. How colonization by microbiota in early life shapes the immune system. Science, 2016, 352(6285), 539-544.
[75]
Zitvogel, L.; Ayyoub, M.; Routy, B.; Kroemer, G. Microbiome and anticancer immunosurveillance. Cell, 2016, 165, 276-287.
[76]
Sokol, H.; Pigneur, B.; Watterlot, L.; Lakhdari, O.; Bermudez-Humaran, L.G.; Gratadoux, J.J.; Blugeon, S.; Bridonneau, C.; Furet, J.P.; Corthier, G.; Grangette, C.; Vasquez, N.; Pochart, P.; Trugnan, G.; Thomas, G.; Blottiere, H.M.; Dore, J.; Marteau, P.; Seksik, P.; Langella, P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA, 2008, 105, 16731-16736.
[77]
Louis, P.; Hold, G.L.; Flint, H.J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol., 2014, 12, 661-672.
[78]
Sandrini, S.; Aldriwesh, M.; Alruways, M.; Freestone, P. Microbial endocrinology: Host-bacteria communication within the gut microbiome. J. Endocrinol., 2015, 225, R21-R34.
[79]
Jalanka, J.; Salonen, A.; Fuentes, S.; de Vos, W.M. Microbial signatures in post-infectious irritable bowel syndrome--toward patient stratification for improved diagnostics and treatment. Gut Microbes, 2015, 6, 364-369.
[80]
Bikker, P.; Dirkzwager, A.; Fledderus, J.; Trevisi, P.; le Huerou-Luron, I.; Lalles, J.P.; Awati, A. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. J. Anim. Sci., 2006, 84, 3337-3345.
[81]
Thaler, D.S. Toward a microbial Neolithic revolution in buildings. Microbiome, 2016, 4, 14.
[82]
Huang, C.; Song, P.; Fan, P.; Hou, C.; Thacker, P.; Ma, X. Dietary sodium butyrate decreases postweaning diarrhea by modulating intestinal permeability and changing the bacterial communities in weaned piglets. J. Nutr., 2015, 145, 2774-2780.
[83]
Ma, X.; Fan, P.X.; Li, L.S.; Qiao, S.Y.; Zhang, G.L.; Li, D.F. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. J. Anim. Sci., 2012, 90(Suppl. 4), 266-268.
[84]
Han, M.; Song, P.; Huang, C.; Rezaei, A.; Farrar, S.; Brown, M.A.; Ma, X. Dietary grape seed proanthocyanidins (GSPs) improve weaned intestinal microbiota and mucosal barrier using a piglet model. Oncotarget, 2016, 7, 80313-80326.
[85]
Maruyama, N.; Maruyama, Y.; Tsuruki, T.; Okuda, E.; Yoshikawa, M.; Utsumi, S. Creation of soybean beta-conglycinin beta with strong phagocytosis-stimulating activity. Biochim. Biophys. Acta, 2003, 1648, 99-104.
[86]
Maruyama, N.; Fukuda, T.; Saka, S.; Inui, N.; Kotoh, J.; Miyagawa, M.; Hayashi, M.; Sawada, M.; Moriyama, T.; Utsumi, S. Molecular and structural analysis of electrophoretic variants of soybean seed storage proteins. Phytochemistry, 2003, 64, 701-708.
[87]
Ma, X.; He, P.; Sun, P.; Han, P. Lipoic acid: an immunomodulator that attenuates glycinin-induced anaphylactic reactions in a rat model. J. Agric. Food Chem., 2010, 58, 5086-5092.
[88]
Shen, C.L.; Chen, W.H.; Zou, S.X. In vitro and in vivo effects of hydrolysates from conglycinin on intestinal microbial community of mice after Escherichia coli infection. J. Appl. Microbiol., 2007, 102, 283-289.
[89]
Rist, V.T.; Weiss, E.; Sauer, N.; Mosenthin, R.; Eklund, M. Effect of dietary protein supply originating from soybean meal or casein on the intestinal microbiota of piglets. Anaerobe, 2014, 25, 72-79.
[90]
Ma, N.; Tian, Y.; Wu, Y.; Ma, X. Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Curr. Protein Pept. Sci., 2017, 18, 795-808.
[91]
Han, P.; Ma, X.; Yin, J. The effects of lipoic acid on soybean beta-conglycinin-induced anaphylactic reactions in a rat model. Arch. Anim. Nutr., 2010, 64, 254-264.
[92]
Song, P.; Zhang, R.; Wang, X.; He, P.; Tan, L.; Ma, X. Dietary grape-seed procyanidins decreased postweaning diarrhea by modulating intestinal permeability and suppressing oxidative stress in rats. J. Agric. Food Chem., 2011, 59, 6227-6232.
[93]
Ma, X.; Sun, P.; He, P.; Han, P.; Wang, J.; Qiao, S.; Li, D. Development of monoclonal antibodies and a competitive ELISA detection method for glycinin, an allergen in soybean. Food Chem., 2010, 121, 546-551.
[94]
Weintraut, M.L.; Kim, S.; Dalloul, R.A.; Wong, E.A. Expression of small intestinal nutrient transporters in embryonic and posthatch turkeys. Poult. Sci., 2016, 95, 90-98.
[95]
Woyengo, T.A.; Weihrauch, D.; Nyachoti, C.M. Effect of dietary phytic acid on performance and nutrient uptake in the small intestine of piglets. J. Anim. Sci., 2012, 90, 543-549.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy