Generic placeholder image

Current Protein & Peptide Science

Author(s): Xiao-Pei Peng, Cunxi Nie, Wen-Yi Guan, Li-Dong Qiao, Lin Lu* and Shou-Jun Cao*

DOI: 10.2174/1389203720666191111112941

DownloadDownload PDF Flyer Cite As
Regulation of Probiotics on Metabolism of Dietary Protein in Intestine

Page: [766 - 771] Pages: 6

  • * (Excluding Mailing and Handling)

Abstract

Proteins are indispensable components of living organisms, which are derived mainly from diet through metabolism. Dietary proteins are degraded by endogenous digestive enzymes to di- or tripeptides and free amino acids (AAs) in the small intestine lumen and then absorbed into blood and lymph through intestinal epithelial cells via diverse transporters. Microorganisms are involved not only in the proteins’ catabolism, but also the AAs, especially essential AAs, anabolism. Probiotics regulate these processes by providing exogenous proteases and AAs and peptide transporters, and reducing hazardous substances in the food and feed. But the core mechanism is modulating of the composition of intestinal microorganisms through their colonization and exclusion of pathogens. The other effects of probiotics are associated with normal intestinal morphology, which implies that the enterocytes secrete more enzymes to decompose dietary proteins and absorb more nutrients.

Keywords: Regulation, probiotics, dietary protein, amino acids (AAs), metabolism, intestinal flora, intestinal epithelial cells (IECs).

Graphical Abstract

[1]
Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; Calder, P.C.; Sanders, M.E. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol., 2014, 11(8), 506-514.
[http://dx.doi.org/10.1038/nrgastro.2014.66] [PMID: 24912386]
[2]
Plaza-Diaz, J.; Ruiz-Ojeda, F.J.; Gil-Campos, M.; Gil, A. Mechanisms of Action of Probiotics. Adv. Nutr., 2019, 10(suppl_1), S49-S66.,
[http://dx.doi.org/10.1093/advances/nmy063] [PMID: 30721959]
[3]
Arnoldini, M.; Cremer, J.; Hwa, T. Bacterial growth, flow, and mixing shape human gut microbiota density and composition. Gut Microbes, 2018, 9(6), 559-566.
[http://dx.doi.org/10.1080/19490976.2018.1448741] [PMID: 29533125]
[4]
Han, X.; Lee, A.; Huang, S.; Gao, J.; Spence, J.R.; Owyang, C. Lactobacillus rhamnosus GG prevents epithelial barrier dysfunction induced by interferon-gamma and fecal supernatants from irritable bowel syndrome patients in human intestinal enteroids and colonoids. Gut Microbes, 2019, 10(1), 59-76.
[http://dx.doi.org/10.1080/19490976.2018.1479625] [PMID: 30040527]
[5]
Bagga, D.; Reichert, J.L.; Koschutnig, K.; Aigner, C.S.; Holzer, P.; Koskinen, K.; Moissl-Eichinger, C.; Schöpf, V. Probiotics drive gut microbiome triggering emotional brain signatures. Gut Microbes, 2018, 9(6), 486-496.
[http://dx.doi.org/10.1080/19490976.2018.1460015] [PMID: 29723105]
[6]
Ma, X. Editorial: Signal proteins involved in glucose and lipid metabolism regulation. Curr. Protein Pept. Sci., 2017, 18(6), 524.
[http://dx.doi.org/10.2174/138920371806170418222704] [PMID: 29336244]
[7]
Ma, X. Editorial: Bioavailability and turnover of proteins in mammals. Curr. Protein Pept. Sci., 2019, 20(2), 114.
[http://dx.doi.org/10.2174/138920372002181113112335] [PMID: 30516103]
[8]
Ma, N.; Ma, X. Dietary amino acids and the gut-microbiome-immune axis: Physiological metabolism and therapeutic Prospects. Compr. Rev. Food Sci. Food Saf., 2019, 18, 221-242.
[http://dx.doi.org/10.1111/1541-4337.12401]
[9]
Nie, C.; He, T.; Zhang, W.; Zhang, G.; Ma, X. Branched chain amino acids: Beyond nutrition metabolism. Int. J. Mol. Sci., 2018, 19(4)E954
[http://dx.doi.org/10.3390/ijms19040954] [PMID: 29570613]
[10]
Hu, S.; Han, M.; Rezaei, A.; Li, D.; Wu, G.; Ma, X. L-Arginine modulates glucose and lipid metabolism in obesity and diabetes. Curr. Protein Pept. Sci., 2017, 18(6), 599-608.
[http://dx.doi.org/10.2174/1389203717666160627074017] [PMID: 27356939]
[11]
Ma, X.; Han, M.; Li, D.; Hu, S.; Gilbreath, K.R.; Bazer, F.W.; Wu, G. L-Arginine promotes protein synthesis and cell growth in brown adipocyte precursor cells via the mTOR signal pathway. Amino Acids, 2017, 49(5), 957-964.
[http://dx.doi.org/10.1007/s00726-017-2399-0] [PMID: 28260165]
[12]
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(7), 646-654.
[http://dx.doi.org/10.2174/1389203716666150630133657] [PMID: 26122784]
[13]
Nie, C.; Xie, F.; Ma, N.; Bai, Y.; Zhang, W.; Ma, X. Nutrients mediate bioavailability and turnover of proteins in mammals. Curr. Protein Pept. Sci., 2019, 20(7), 661-665.
[http://dx.doi.org/10.2174/1389203720666190125111235] [PMID: 30678625]
[14]
Dai, Z.L.; Li, X.L.; Xi, P.B.; Zhang, J.; Wu, G.; Zhu, W.Y. Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids, 2012, 42(5), 1597-1608.
[http://dx.doi.org/10.1007/s00726-011-0846-x] [PMID: 21344175]
[15]
Metges, C.C.; Eberhard, M.; Petzke, K.J. Synthesis and absorption of intestinal microbial lysine in humans and non-ruminant animals and impact on human estimated average requirement of dietary lysine. Curr. Opin. Clin. Nutr. Metab. Care, 2006, 9(1), 37-41.
[http://dx.doi.org/10.1097/01.mco.0000196142.72985.d3] [PMID: 16444817]
[16]
Cammack, K.M.; Austin, K.J.; Lamberson, W.R.; Conant, G.C.; Cunningham, H.C. RUMINNAT NUTRITION SYMPOSIUM: Tiny but mighty: the role of the rumen microbes in livestock production. J. Anim. Sci., 2018, 96, 752-770.
[http://dx.doi.org/10.1093/jas/sky331] [PMID: 29385535]
[17]
Gomes, A.C.; Hoffmann, C.; Mota, J.F. The human gut microbiota: Metabolism and perspective in obesity. Gut Microbes, 2018, 9(4), 308-325.
[http://dx.doi.org/10.1080/19490976.2018.1465157] [PMID: 29667480]
[18]
Burns, M.B.; Blekhman, R. Integrating tumor genomics into studies of the microbiome in colorectal cancer. Gut Microbes, 2019, 10(4), 547-552.
[http://dx.doi.org/10.1080/19490976.2018.1549421] [PMID: 30556775]
[19]
Elhenawy, W.; Oberc, A.; Coombes, B.K. A polymicrobial view of disease potential in Crohn’s-associated adherent-invasive E. coli. Gut Microbes, 2018, 9(2), 166-174.
[http://dx.doi.org/10.1080/19490976.2017.1378291] [PMID: 28914579]
[20]
Florin, T.; Movva, R.; Begun, J.; Duley, J.; Oancea, I.; Cuív, P.O. Colonic thioguanine pro-drug: Investigation of microbiome and novel host metabolism. Gut Microbes, 2018, 9(2), 175-178.
[http://dx.doi.org/10.1080/19490976.2017.1387343] [PMID: 28976243]
[21]
Gomez-Arango, L.F.; Barrett, H.L.; Wilkinson, S.A.; Callaway, L.K.; McIntyre, H.D.; Morrison, M.; Dekker Nitert, M. Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women. Gut Microbes, 2018, 9(3), 189-201.
[http://dx.doi.org/10.1080/19490976.2017.1406584] [PMID: 29144833]
[22]
Huang, Y.Y.; Martínez-Del Campo, A.; Balskus, E.P. Anaerobic 4-hydroxyproline utilization: Discovery of a new glycyl radical enzyme in the human gut microbiome uncovers a widespread microbial metabolic activity. Gut Microbes, 2018, 9(5), 437-451.
[http://dx.doi.org/10.1080/19490976.2018.1435244] [PMID: 29405826]
[23]
Kiely, C.J.; Pavli, P.; O’Brien, C.L. The role of inflammation in temporal shifts in the inflammatory bowel disease mucosal microbiome. Gut Microbes, 2018, 9(6), 477-485.
[http://dx.doi.org/10.1080/19490976.2018.1448742] [PMID: 29543557]
[24]
Le Roy, C.I.; Beaumont, M.; Jackson, M.A.; Steves, C.J.; Spector, T.D.; Bell, J.T. Heritable components of the human fecal microbiome are associated with visceral fat. Gut Microbes, 2018, 9(1), 61-67.
[http://dx.doi.org/10.1080/19490976.2017.1356556] [PMID: 28767316]
[25]
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(8), 795-808.
[http://dx.doi.org/10.2174/1389203718666170216153505] [PMID: 28215168]
[26]
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(7), 592-603.
[http://dx.doi.org/10.2174/1389203716666150630135720] [PMID: 26122779]
[27]
Demeyer, D.; Fievez, V. Is the synthesis of rumen bacterial protein limited by the availability of pre-formed amino acids and/or peptides? Br. J. Nutr., 2004, 91(2), 175-176.
[http://dx.doi.org/10.1079/BJN20031073] [PMID: 14756901]
[28]
Libao-Mercado, A.J.; Zhu, C.L.; Cant, J.P.; Lapierre, H.; Thibault, J.N.; Sève, 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(6), 1088-1094.
[http://dx.doi.org/10.3945/jn.108.103267] [PMID: 19403708]
[29]
Chen, X.; Song, P.; Fan, P.; He, T.; Jacobs, D.; Levesque, C.L.; Johnston, L.J.; Ji, L.; Ma, N.; Chen, Y.; Zhang, J.; Zhao, J.; Ma, X. Moderate dietary protein restriction optimized gut microbiota and mucosal barrier in growing pig model. Front. Cell. Infect. Microbiol., 2018, 8, 246.
[http://dx.doi.org/10.3389/fcimb.2018.00246] [PMID: 30073151]
[30]
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.
[http://dx.doi.org/10.1038/srep43412] [PMID: 28252026]
[31]
Wang, W.; Yang, Q.; Sun, Z.; Chen, X.; Yang, C.; Ma, X. Advance of interactions between exogenous natural bioactive peptides and intestinal barrier and immune responses. Curr. Protein Pept. Sci., 2015, 16(7), 574-575.
[http://dx.doi.org/10.2174/138920371607150810124927] [PMID: 26283417]
[32]
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(7), 592-603.
[http://dx.doi.org/10.2174/1389203716666150630135720] [PMID: 26122779]
[33]
Ma, N.; Guo, P.; Zhang, J.; He, T.; Kim, S.W.; Zhang, G.; Ma, X. Nutrients mediate intestinal bacteria-mucosal immune crosstalk. Front. Immunol., 2018, 9, 5.
[http://dx.doi.org/10.3389/fimmu.2018.00005] [PMID: 29416535]
[34]
Kandasamy, P.; Gyimesi, G.; Kanai, Y.; Hediger, M.A. Amino acid transporters revisited: New views in health and disease. Trends Biochem. Sci., 2018, 43(10), 752-789.
[http://dx.doi.org/10.1016/j.tibs.2018.05.003] [PMID: 30177408]
[35]
Fan, M.Z.; Matthews, J.C.; Etienne, N.M.; Stoll, B.; Lackeyram, D.; Burrin, D.G. Expression of apical membrane L-glutamate transporters in neonatal porcine epithelial cells along the small intestinal crypt-villus axis. Am. J. Physiol. Gastrointest. Liver Physiol., 2004, 287(2), G385-G398.
[http://dx.doi.org/10.1152/ajpgi.00232.2003] [PMID: 15044176]
[36]
Bauch, C.; Forster, N.; Loffing-Cueni, D.; Summa, V.; Verrey, F. Functional cooperation of epithelial heteromeric amino acid transporters expressed in madin-darby canine kidney cells. J. Biol. Chem., 2003, 278(2), 1316-1322.
[http://dx.doi.org/10.1074/jbc.M210449200] [PMID: 12417581]
[37]
Bröer, A.; Klingel, K.; Kowalczuk, S.; Rasko, J.E.; Cavanaugh, J.; Bröer, S. Molecular cloning of mouse amino acid transport system B0, a neutral amino acid transporter related to Hartnup disorder. J. Biol. Chem., 2004, 279(23), 24467-24476.
[http://dx.doi.org/10.1074/jbc.M400904200] [PMID: 15044460]
[38]
Fan, M.Z.; Adeola, O.; McBurney, M.I.; Cheeseman, C.I. Kinetic analysis of L-glutamine transport into porcine jejunal enterocyte brush-border membrane vesicles. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 1998, 121(4), 411-422.
[http://dx.doi.org/10.1016/S1095-6433(98)10152-6] [PMID: 10048191]
[39]
Wu, G.; Bazer, F.W.; Dai, Z.; Li, D.; Wang, J.; Wu, Z. Amino acid nutrition in animals: protein synthesis and beyond. Annu. Rev. Anim. Biosci., 2014, 2, 387-417.
[http://dx.doi.org/10.1146/annurev-animal-022513-114113] [PMID: 25384149]
[40]
Chen, L.; Li, P.; Wang, J.; Li, X.; Gao, H.; Yin, Y.; Hou, Y.; Wu, G. Catabolism of nutritionally essential amino acids in developing porcine enterocytes. Amino Acids, 2009, 37(1), 143-152.
[http://dx.doi.org/10.1007/s00726-009-0268-1] [PMID: 19291365]
[41]
Bauchart-Thevret, C.; Cottrell, J.; Stoll, B.; Burrin, D.G. First-pass splanchnic metabolism of dietary cysteine in weanling pigs. J. Anim. Sci., 2011, 89(12), 4093-4099.
[http://dx.doi.org/10.2527/jas.2011-3944] [PMID: 21821812]
[42]
Cui, Y.; Xu, T.; Qu, X.; Hu, T.; Jiang, X.; Zhao, C. New insights into various production characteristics of Streptococcus thermophilus strains. Int. J. Mol. Sci., 2016, 17(10)E1701
[http://dx.doi.org/10.3390/ijms17101701] [PMID: 27754312]
[43]
Delorme, C.; Bartholini, C.; Bolotine, A.; Ehrlich, S.D.; Renault, P. Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl. Environ. Microbiol., 2010, 76(2), 451-460.
[http://dx.doi.org/10.1128/AEM.01018-09] [PMID: 19915034]
[44]
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(18), 4406-4410.
[http://dx.doi.org/10.1021/jf400009g] [PMID: 23594133]
[45]
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(7), 613-621.
[http://dx.doi.org/10.2174/1389203716666150630134602] [PMID: 26122781]
[46]
Yang, A.; Zuo, L.; Cheng, Y.; Wu, Z.; Li, X.; Tong, P.; Chen, H. Degradation of major allergens and allergenicity reduction of soybean meal through solid-state fermentation with microorganisms. Food Funct., 2018, 9(3), 1899-1909.
[http://dx.doi.org/10.1039/C7FO01824J] [PMID: 29536997]
[47]
Huang, C.; Song, P.; Fan, P.; Hou, C.; Thacker, P.; Ma, X. Dietary sodium butyrate decreased postweaning diarrhea by modulating intestinal permeability and changing the bacterial community in weaned piglets. J. Nutr., 2015, 145(12), 2774-2780.
[http://dx.doi.org/10.3945/jn.115.217406] [PMID: 26491121]
[48]
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(49), 80313-80326.
[http://dx.doi.org/10.18632/oncotarget.13450] [PMID: 27880936]
[49]
He, L.; Zang, J.; Liu, P.; Fan, P.; Song, P.; Chen, J.; Ma, Y.; Ding, W.; Ma, X. Supplementation of milky flavors improves the reproductive performance and gut function using sow model. Protein Pept. Lett., 2017, 24(5), 449-455.
[http://dx.doi.org/10.2174/0929866524666170223144728] [PMID: 28240159]
[50]
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(4), 860-866.
[http://dx.doi.org/10.1021/jf403288r] [PMID: 24404892]
[51]
Zhang, J.; Chen, X.; Liu, P.; Zhao, J.; Sun, J.; Guan, W.; Johnston, L.J.; Levesque, C.L.; Fan, P.; He, T.; Zhang, G.; Ma, X. Dietary Clostridium Butyricum induces a phased shift in fecal microbiota structure and increases the acetic acid-producing bacteria in a weaned piglet model. J. Agric. Food Chem., 2018, 66(20), 5157-5166.
[http://dx.doi.org/10.1021/acs.jafc.8b01253] [PMID: 29683328]
[52]
Liu, P.; Zhao, J.; Guo, P.; Lu, W.; Geng, Z.; Levesque, C.L.; Johnston, L.J.; Wang, C.; Liu, L.; Zhang, J.; Ma, N.; Qiao, S.; Ma, X. Dietary corn bran fermented by bacillus subtilisma139 decreased gut cellulolytic bacteria and microbiota diversity in finishing pigs. Front. Cell. Infect. Microbiol., 2017, 7, 526.
[http://dx.doi.org/10.3389/fcimb.2017.00526] [PMID: 29312900]
[53]
Bazanella, M.; Maier, T.V.; Clavel, T.; Lagkouvardos, I.; Lucio, M.; Maldonado-Gòmez, M.X.; Autran, C.; Walter, J.; Bode, L.; Schmitt-Kopplin, P.; Haller, D. Randomized controlled trial on the impact of early-life intervention with bifidobacteria on the healthy infant fecal microbiota and metabolome. Am. J. Clin. Nutr., 2017, 106(5), 1274-1286.
[http://dx.doi.org/10.3945/ajcn.117.157529] [PMID: 28877893]
[54]
Hascoët, J.M.; Hubert, C.; Rochat, F.; Legagneur, H.; Gaga, S.; Emady-Azar, S.; Steenhout, P.G. Effect of formula composition on the development of infant gut microbiota. J. Pediatr. Gastroenterol. Nutr., 2011, 52(6), 756-762.
[http://dx.doi.org/10.1097/MPG.0b013e3182105850] [PMID: 21593648]
[55]
Bermudez-Brito, M.; Plaza-Díaz, J.; Muñoz-Quezada, S.; Gómez-Llorente, C.; Gil, A. Probiotic mechanisms of action. Ann. Nutr. Metab., 2012, 61(2), 160-174.
[http://dx.doi.org/10.1159/000342079] [PMID: 23037511]
[56]
Olivares, M.; Díaz-Ropero, M.A.; Gómez, N.; Lara-Villoslada, F.; Sierra, S.; Maldonado, J.A.; Martín, R.; López-Huertas, E.; Rodríguez, J.M.; Xaus, J. Oral administration of two probiotic strains, Lactobacillus gasseri CECT5714 and Lactobacillus coryniformis CECT5711, enhances the intestinal function of healthy adults. Int. J. Food Microbiol., 2006, 107(2), 104-111.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2005.08.019] [PMID: 16271414]
[57]
Cotter, P.D.; Ross, R.P.; Hill, C. Bacteriocins - a viable alternative to antibiotics? Nat. Rev. Microbiol., 2013, 11(2), 95-105.
[http://dx.doi.org/10.1038/nrmicro2937] [PMID: 23268227]
[58]
Renye, J.A.; Jr Somkuti, G.A.; Steinberg, D.H. Thermophilin 109 is a naturally produced broad spectrum bacteriocin encoded within cthe blp gene cluster of Streptococcus thermophilus. Biotechnol. Lett., 2019, 41, 283-292.
[http://dx.doi.org/10.1007/s10529-018-02637-3] [PMID: 30564999]
[59]
Zhu, J.; Gao, M.; Zhang, R.; Sun, Z.; Wang, C.; Yang, F.; Huang, T.; Qu, S.; Zhao, L.; Li, Y.; Hao, Z. Effects of soybean meal fermented by L. plantarum, B. subtilis and S. cerevisieae on growth, immune function and intestinal morphology in weaned piglets. Microb. Cell Fact., 2017, 16(1), 191-200.
[http://dx.doi.org/10.1186/s12934-017-0809-3] [PMID: 29121938]
[60]
Chen, H.Q.; Shen, T.Y.; Zhou, Y.K.; Zhang, M.; Chu, Z.X.; Hang, X.M.; Qin, H.L. Lactobacillus plantarum consumption increases PepT1-mediated amino acid absorption by enhancing protein kinase C activity in spontaneously colitic mice. J. Nutr., 2010, 140(12), 2201-2206.
[http://dx.doi.org/10.3945/jn.110.123265] [PMID: 20980636]