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Beaumont M, Lencina C, Painteaux L, et al. A mix of functional amino acids and grape polyphenols promotes the growth of piglets, modulates the gut microbiota in vivo and regulates epithelial homeostasis in intestinal organoids. Amino Acids. 2021;doi: 10.1007/s00726-021-03082-9.
Beaumont, M., Lencina, C., Painteaux, L., Viémon-Desplanque, J., Phornlaphat, O., Lambert, W., & Chalvon-Demersay, T. (2021). A mix of functional amino acids and grape polyphenols promotes the growth of piglets, modulates the gut microbiota in vivo and regulates epithelial homeostasis in intestinal organoids. Amino acids, . https://doi.org/10.1007/s00726-021-03082-9
Beaumont, Martin, et al. "A mix of functional amino acids and grape polyphenols promotes the growth of piglets, modulates the gut microbiota in vivo and regulates epithelial homeostasis in intestinal organoids." Amino acids vol. (2021). doi: https://doi.org/10.1007/s00726-021-03082-9
Beaumont M, Lencina C, Painteaux L, Viémon-Desplanque J, Phornlaphat O, Lambert W, Chalvon-Demersay T. A mix of functional amino acids and grape polyphenols promotes the growth of piglets, modulates the gut microbiota in vivo and regulates epithelial homeostasis in intestinal organoids. Amino Acids. 2021 Oct 12; doi: 10.1007/s00726-021-03082-9. Epub 2021 Oct 12. PMID: 34642825.
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Amino Acids. 2021 Oct 12; doi: 10.1007/s00726-021-03082-9. Epub 2021 Oct 12.

A mix of functional amino acids and grape polyphenols promotes the growth of piglets, modulates the gut microbiota in vivo and regulates epithelial homeostasis in intestinal organoids.

Amino acids

Martin Beaumont, Corinne Lencina, Louise Painteaux, Joffrey Viémon-Desplanque, Orasin Phornlaphat, William Lambert, Tristan Chalvon-Demersay

Affiliations

  1. GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet-Tolosan, France. [email protected].
  2. GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet-Tolosan, France.
  3. BARC, Bangkok Animal Research Center Co., Ltd, 74/4 Mu 7 Tambon Naiklong Bangplakod, Phrasamutjedi,, Samut Prakan, 10290, Thailand.
  4. METEX NOOVISTAGO, 32 rue Guersant, 75017, Paris, France.

PMID: 34642825 DOI: 10.1007/s00726-021-03082-9

Abstract

Weaning is a challenging period for gut health in piglets. Previous studies showed that dietary supplementations with either amino acids or polyphenols promote piglet growth and intestinal functions, when administered separately. Thus, we hypothesized that a combination of amino acids and polyphenols could facilitate the weaning transition. Piglets received during the first two weeks after weaning a diet supplemented or not with a mix of a low dose (0.1%) of functional amino acids (L-arginine, L-leucine, L-valine, L-isoleucine, L-cystine) and 100 ppm of a polyphenol-rich extract from grape seeds and skins. The mix of amino acids and polyphenols improved growth and feed efficiency. These beneficial effects were associated with a lower microbiota diversity and a bloom of Lactobacillaceae in the jejunum content while the abundance of Proteobacteria was reduced in the caecum content. The mix of amino acids and polyphenols also increased the production by the caecum microbiota of short-chain fatty acids (butyrate, propionate) and of metabolites derived from amino acids (branched-chain fatty acids, valerate, putrescine) and from polyphenols (3-phenylpropionate). Experiments in piglet jejunum organoids revealed that the mix of amino acids and polyphenols upregulated the gene expression of epithelial differentiation markers while it reduced the gene expression of proliferation and innate immunity markers. In conclusion, the supplementation of a mix of amino acids and polyphenols is a promising nutritional strategy to manage gut health in piglets through the modulation of the gut microbiota and of the epithelial barrier.

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.

Keywords: Arginine; Cystine; Enteroids; Isoleucine; Leucine; Metabolites; Tannins; Valine; Weaning

References

  1. Adamczyk B, Simon J, Kitunen V et al (2017) Tannins and their complex interaction with different organic nitrogen compounds and enzymes: old paradigms versus recent advances. ChemistryOpen 6:610–614. https://doi.org/10.1002/open.201700113 - PubMed
  2. Allaire JM, Crowley SM, Law HT et al (2018) The intestinal epithelium: central coordinator of mucosal immunity. Trends Immunol 39:677–696. https://doi.org/10.1016/j.it.2018.04.002 - PubMed
  3. Andersen-Civil AIS, Arora P, Williams AR (2021) Regulation of enteric infection and immunity by dietary proanthocyanidins. Front Immunol. https://doi.org/10.3389/fimmu.2021.637603 - PubMed
  4. Beaumont M, Blachier F (2020) Amino acids in intestinal physiology and health. Adv Exp Med Biol 1265:1–20. https://doi.org/10.1007/978-3-030-45328-2_1 - PubMed
  5. Beaumont M, Blanc F, Cherbuy C et al (2021a) Intestinal organoids in farm animals. Vet Res 52:33. https://doi.org/10.1186/s13567-021-00909-x - PubMed
  6. Beaumont M, Cauquil L, Bertide A et al (2021b) Gut microbiota-derived metabolite signature in suckling and weaned piglets. J Proteome Res 20:982–994. https://doi.org/10.1021/acs.jproteome.0c00745 - PubMed
  7. Bian G, Ma S, Zhu Z et al (2016) Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross-fostering model: gut bacterial succession in piglets. Environ Microbiol 18:1566–1577. https://doi.org/10.1111/1462-2920.13272 - PubMed
  8. Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276 - PubMed
  9. Bonetti A, Tugnoli B, Piva A, Grilli E (2021) Towards zero zinc oxide: feeding strategies to manage post-weaning diarrhea in piglets. Animals (basel). https://doi.org/10.3390/ani11030642 - PubMed
  10. Boudry G, Jamin A, Chatelais L et al (2013) Dietary protein excess during neonatal life alters colonic microbiota and mucosal response to inflammatory mediators later in life in female pigs. J Nutr 143:1225–1232. https://doi.org/10.3945/jn.113.175828 - PubMed
  11. Brenes A, Viveros A, Chamorro S, Arija I (2016) Use of polyphenol-rich grape by-products in monogastric nutrition. A review. Anim Feed Sci Technol 211:1–17. https://doi.org/10.1016/j.anifeedsci.2015.09.016 - PubMed
  12. Burgueño JF, Abreu MT (2020) Epithelial toll-like receptors and their role in gut homeostasis and disease. Nat Rev Gastroenterol Hepatol. https://doi.org/10.1038/s41575-019-0261-4 - PubMed
  13. Campbell JM, Crenshaw JD, Polo J (2013) The biological stress of early weaned piglets. J Anim Sci Biotechnol 4:19. https://doi.org/10.1186/2049-1891-4-19 - PubMed
  14. Casanova-Martí À, González-Abuín N, Serrano J et al (2020) Long term exposure to a grape seed proanthocyanidin extract enhances L-cell differentiation in intestinal organoids. Mol Nutr Food Res 64:2000303. https://doi.org/10.1002/mnfr.202000303 - PubMed
  15. Chalvon-Demersay T, Luise D, Le Floch N et al (2021) Functional amino acids in pigs and chickens: implication for gut health. Front Vet Sci. https://doi.org/10.3389/fvets.2021.663727 - PubMed
  16. Choy YY, Quifer-Rada P, Holstege DM et al (2014) Phenolic metabolites and substantial microbiome changes in pig feces by ingesting grape seed proanthocyanidins. Food Funct 5:2298–2308. https://doi.org/10.1039/C4FO00325J - PubMed
  17. Cires MJ, Wong X, Carrasco-Pozo C, Gotteland M (2017) The gastrointestinal tract as a key target organ for the health-promoting effects of dietary proanthocyanidins. Front Nutr. https://doi.org/10.3389/fnut.2016.00057 - PubMed
  18. Dowarah R, Verma AK, Agarwal N (2017) The use of Lactobacillus as an alternative of antibiotic growth promoters in pigs: a review. Anim Nutr 3:1–6. https://doi.org/10.1016/j.aninu.2016.11.002 - PubMed
  19. Escudié F, Auer L, Bernard M et al (2018) FROGS: find, rapidly, OTUs with galaxy solution. Bioinformatics 34:1287–1294. https://doi.org/10.1093/bioinformatics/btx791 - PubMed
  20. Gardiner GE, Metzler-Zebeli BU, Lawlor PG (2020) Impact of intestinal microbiota on growth and feed efficiency in pigs: a review. Microorganisms. https://doi.org/10.3390/microorganisms8121886 - PubMed
  21. Ghosh S, Whitley CS, Haribabu B, Jala VR (2021) Regulation of intestinal barrier function by microbial metabolites. Cell Mol Gastroenterol Hepatol 11:1463–1482. https://doi.org/10.1016/j.jcmgh.2021.02.007 - PubMed
  22. Giacomoni F, Le Corguillé G, Monsoor M et al (2015) Workflow4Metabolomics: a collaborative research infrastructure for computational metabolomics. Bioinformatics 31:1493–1495. https://doi.org/10.1093/bioinformatics/btu813 - PubMed
  23. Girard M, Bee G (2020) Invited review: Tannins as a potential alternative to antibiotics to prevent coliform diarrhea in weaned pigs. Animal 14:95–107. https://doi.org/10.1017/S1751731119002143 - PubMed
  24. Gresse R, Chaucheyras-Durand F, Fleury MA et al (2017) Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health. Trends Microbiol 25:851–873. https://doi.org/10.1016/j.tim.2017.05.004 - PubMed
  25. Grosu IA, Pistol GC, Taranu I, Marin DE (2019) The impact of dietary grape seed meal on healthy and aflatoxin B1 afflicted microbiota of pigs after weaning. Toxins 11:25. https://doi.org/10.3390/toxins11010025 - PubMed
  26. Han M, Song P, Huang C et al (2016) Dietary grape seed proanthocyanidins (GSPs) improve weaned intestinal microbiota and mucosal barrier using a piglet model. Oncotarget 7:80313–80326. https://doi.org/10.18632/oncotarget.13450 - PubMed
  27. Hao R, Li Q, Zhao J et al (2015) Effects of grape seed procyanidins on growth performance, immune function and antioxidant capacity in weaned piglets. Livest Sci 178:237–242. https://doi.org/10.1016/j.livsci.2015.06.004 - PubMed
  28. Hou Q, Dong Y, Huang J et al (2020) Exogenous L-arginine increases intestinal stem cell function through CD90+ stromal cells producing mTORC1-induced Wnt2b. Commun Biol 3:1–16. https://doi.org/10.1038/s42003-020-01347-9 - PubMed
  29. Kafantaris I, Stagos D, Kotsampasi B et al (2018) Grape pomace improves performance, antioxidant status, fecal microbiota and meat quality of piglets. Animal 12:246–255. https://doi.org/10.1017/S1751731117001604 - PubMed
  30. Kamada N, Chen GY, Inohara N, Núñez G (2013) Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 14:685–690. https://doi.org/10.1038/ni.2608 - PubMed
  31. Kim CJ, Kovacs-Nolan J, Yang C et al (2009) L-cysteine supplementation attenuates local inflammation and restores gut homeostasis in a porcine model of colitis. Biochim Biophys Acta 1790:1161–1169. https://doi.org/10.1016/j.bbagen.2009.05.018 - PubMed
  32. Lallès J-P, Bosi P, Smidt H, Stokes CR (2007) Weaning—a challenge to gut physiologists. Livest Sci 108:82–93. https://doi.org/10.1016/j.livsci.2007.01.091 - PubMed
  33. Lan J, Dou X, Li J et al (2020) l-arginine ameliorates lipopolysaccharide-induced intestinal inflammation through inhibiting the TLR4/NF-κB and MAPK pathways and stimulating β-defensin expression in vivo and in vitro. J Agric Food Chem 68:2648–2663. https://doi.org/10.1021/acs.jafc.9b07611 - PubMed
  34. Larrosa M, Luceri C, Vivoli E et al (2009) Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models. Mol Nutr Food Res 53:1044–1054. https://doi.org/10.1002/mnfr.200800446 - PubMed
  35. Le Floch N, Wessels A, Corrent E et al (2018) The relevance of functional amino acids to support the health of growing pigs. Anim Feed Sci Technol 245:104–116. https://doi.org/10.1016/j.anifeedsci.2018.09.007 - PubMed
  36. Leonard W, Zhang P, Ying D, Fang Z (2021) Hydroxycinnamic acids on gut microbiota and health. Compr Rev Food Sci Food Saf 20:710–737. https://doi.org/10.1111/1541-4337.12663 - PubMed
  37. Mao X, Liu M, Tang J et al (2015) Dietary leucine supplementation improves the mucin production in the jejunal mucosa of the weaned pigs challenged by porcine rotavirus. PLoS ONE 10:e0137380. https://doi.org/10.1371/journal.pone.0137380 - PubMed
  38. Marín L, Miguélez EM, Villar CJ, Lombó F (2015) Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int 2015:e905215. https://doi.org/10.1155/2015/905215 - PubMed
  39. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217 - PubMed
  40. Modina SC, Polito U, Rossi R et al (2019) Nutritional regulation of gut barrier integrity in weaning piglets. Animals 9:1045. https://doi.org/10.3390/ani9121045 - PubMed
  41. Monagas M, Gómez-Cordovés C, Bartolomé B et al (2003) Monomeric, oligomeric, and polymeric flavan-3-ol composition of wines and grapes from Vitis vinifera L. Cv. Graciano, Tempranillo, and Cabernet Sauvignon. J Agric Food Chem 51:6475–6481. https://doi.org/10.1021/jf030325+ - PubMed
  42. Nallathambi R, Poulev A, Zuk JB, Raskin I (2020) Proanthocyanidin-rich grape seed extract reduces inflammation and oxidative stress and restores tight junction barrier function in Caco-2 colon cells. Nutrients 12:1623. https://doi.org/10.3390/nu12061623 - PubMed
  43. Noda T, Iwakiri R, Fujimoto K et al (2002) Exogenous cysteine and cystine promote cell proliferation in CaCo-2 cells. Cell Prolif 35:117–129. https://doi.org/10.1046/j.1365-2184.2002.00229.x - PubMed
  44. Odenwald MA, Turner JR (2017) The intestinal epithelial barrier: a therapeutic target? Nat Rev Gastroenterol Hepatol 14:9–21. https://doi.org/10.1038/nrgastro.2016.169 - PubMed
  45. Portune KJ, Beaumont M, Davila A-M et al (2016) Gut microbiota role in dietary protein metabolism and health-related outcomes: the two sides of the coin. Trends Food Sci Technol 57:213–232. https://doi.org/10.1016/j.tifs.2016.08.011 - PubMed
  46. Prates JAM, Freire JPB, de Almeida AM et al (2021) Influence of dietary supplementation with an amino acid mixture on inflammatory markers, immune status and serum proteome in LPS-challenged weaned piglets. Animals 11:1143. https://doi.org/10.3390/ani11041143 - PubMed
  47. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590-596. https://doi.org/10.1093/nar/gks1219 - PubMed
  48. Ren W, Chen S, Yin J et al (2014) Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity. J Nutr 144:988–995. https://doi.org/10.3945/jn.114.192120 - PubMed
  49. Ren M, Cai S, Zhou T et al (2019) Isoleucine attenuates infection induced by E. coli challenge through the modulation of intestinal endogenous antimicrobial peptide expression and the inhibition of the increase in plasma endotoxin and IL-6 in weaned pigs. Food Funct 10:3535–3542. https://doi.org/10.1039/c9fo00218a - PubMed
  50. Rohart F, Gautier B, Singh A, Cao K-AL (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13:e1005752. https://doi.org/10.1371/journal.pcbi.1005752 - PubMed
  51. Song ZH, Tong G, Xiao K, et al (2016) L-cysteine protects intestinal integrity, attenuates intestinal inflammation and oxidant stress, and modulates NF-κB and Nrf2 pathways in weaned piglets after LPS challenge. Innate Immun 22:152–161. https://doi.org/10.1177/1753425916632303 - PubMed
  52. Sun Y, Wu Z, Li W et al (2015) Dietary L-leucine supplementation enhances intestinal development in suckling piglets. Amino Acids 47:1517–1525. https://doi.org/10.1007/s00726-015-1985-2 - PubMed
  53. Toden S, Ravindranathan P, Gu J et al (2018) Oligomeric proanthocyanidins (OPCs) target cancer stem-like cells and suppress tumor organoid formation in colorectal cancer. Sci Rep 8:3335. https://doi.org/10.1038/s41598-018-21478-8 - PubMed
  54. Tsang C, Auger C, Mullen W et al (2005) The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br J Nutr 94:170–181. https://doi.org/10.1079/bjn20051480 - PubMed
  55. Valeriano VDV, Balolong MP, Kang D-K (2017) Probiotic roles of Lactobacillus sp. in swine: insights from gut microbiota. J Appl Microbiol 122:554–567. https://doi.org/10.1111/jam.13364 - PubMed
  56. van der Hee B, Wells JM (2021) Microbial regulation of host physiology by short-chain fatty acids. Trends Microbiol. https://doi.org/10.1016/j.tim.2021.02.001 - PubMed
  57. Verhelst R, Schroyen M, Buys N, Niewold T (2014) Dietary polyphenols reduce diarrhea in enterotoxigenic Escherichia coli (ETEC) infected post-weaning piglets. Livest Sci 160:138–140. https://doi.org/10.1016/j.livsci.2013.11.026 - PubMed
  58. Verschuren LMG, Calus MPL, Jansman AJM et al (2018) Fecal microbial composition associated with variation in feed efficiency in pigs depends on diet and sex. J Anim Sci 96:1405–1418. https://doi.org/10.1093/jas/sky060 - PubMed
  59. Vreugdenhil ACE, Dentener MA, Snoek AMP et al (1999) Lipopolysaccharide binding protein and serum amyloid a secretion by human intestinal epithelial cells during the acute phase response. J Immunol 163:2792–2798 - PubMed
  60. Wu G (2010) Functional amino acids in growth, reproduction, and health. Adv Nutr 1:31–37. https://doi.org/10.3945/an.110.1008 - PubMed
  61. Wu H, Luo T, Li YM et al (2018) Granny Smith apple procyanidin extract upregulates tight junction protein expression and modulates oxidative stress and inflammation in lipopolysaccharide-induced Caco-2 cells. Food Funct 9:3321–3329. https://doi.org/10.1039/C8FO00525G - PubMed
  62. Wu Y, Ma N, Song P et al (2019) Grape seed proanthocyanidin affects lipid metabolism via changing gut microflora and enhancing propionate production in weaned pigs. J Nutr 149:1523–1532. https://doi.org/10.1093/jn/nxz102 - PubMed
  63. Yang Z, Liao SF (2019) Physiological effects of dietary amino acids on gut health and functions of swine. Front Vet Sci. https://doi.org/10.3389/fvets.2019.00169 - PubMed
  64. Yang Z, Huang S, Zou D et al (2016) Metabolic shifts and structural changes in the gut microbiota upon branched-chain amino acid supplementation in middle-aged mice. Amino Acids 48:2731–2745. https://doi.org/10.1007/s00726-016-2308-y - PubMed
  65. Yang G, Bibi S, Du M et al (2017) Regulation of the intestinal tight junction by natural polyphenols: a mechanistic perspective. Crit Rev Food Sci Nutr 57:3830–3839. https://doi.org/10.1080/10408398.2016.1152230 - PubMed
  66. Zhou H, Yu B, Gao J et al (2018) Regulation of intestinal health by branched-chain amino acids. Anim Sci J 89:3–11. https://doi.org/10.1111/asj.12937 - PubMed

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