l-Glutamine and l-arginine protect against enterotoxigenic Escherichia coli infection via intestinal innate immunity in mice

Amino Acids

Volumn 49, Issue 12, 2017, Pages 1945-1954

  Liu, Gang ^a   Ren, Wenkai ^a   Fang, Jun ^b   Hu, Chien An Andy ^c   Guan, Guiping ^b   Al Dhabi, Naif Abdullah ^d   Yin, Jie ^a   Duraipandiyan, Veeramuthu ^d   Chen, Shuai ^a   Peng, Yuanyi ^e   Yin, Yulong ^a,f,g  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b HUNAN AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e SOUTHWEST UNIVERSITY   (China)

^f HUNAN NORMAL UNIVERSITY   (China)

^g SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arginine; Enterotoxigenic E. coli; Glutamine; Innate immunity; Paneth cell

Indexed keywords

ANTIBODY; ARGININE; CRYPTDIN RELATED SEQUENCE 1C; GLUTAMINE; MESSENGER RNA; MUCIN; REG3 GAMMA; SECRETORY COMPONENT; SECRETORY IMMUNOGLOBULIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; PROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; CONTROLLED STUDY; DIET SUPPLEMENTATION; DUODENUM; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI INFECTION; FEMALE; GENE EXPRESSION; ILEUM; INNATE IMMUNITY; JEJUNUM; MORTALITY; MOUSE; MURINE MODEL; NONHUMAN; PRIORITY JOURNAL; ANIMAL; DIETARY SUPPLEMENT; DRUG EFFECT; GENE EXPRESSION REGULATION; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFECTIVE AGENTS; ARGININE; BACTERIAL LOAD; DIETARY SUPPLEMENTS; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION REGULATION; GLUTAMINE; ILEUM; IMMUNITY, INNATE; INTESTINAL MUCOSA; JEJUNUM; MICE; PROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 85015204806     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-017-2410-9     Document Type: Article

References (44)

1. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801. doi:10.1016/j.cell.2006.02.015
2. Bevins CL, Salzman NH (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9(5):356–368. doi:10.1038/nrmicro2546
3. Fleckenstein JM, Hardwidge PR, Munson GP, Rasko DA, Sommerfelt H, Steinsland H (2010) Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect/Inst Pasteur 12(2):89–98. doi:10.1016/j.micinf.2009.10.002
4. Gao X, Wan F, Mateo K, Callegari E, Wang D, Deng W, Puente J, Li F, Chaussee MS, Finlay BB, Lenardo MJ, Hardwidge PR (2009) Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog 5(12):e1000708. doi:10.1371/journal.ppat.1000708
5. Gao X, Wang X, Pham TH, Feuerbacher LA, Lubos ML, Huang M, Olsen R, Mushegian A, Slawson C, Hardwidge PR (2013) NleB, a bacterial effector with glycosyltransferase activity, targets GAPDH function to inhibit NF-kappaB activation. Cell Host Microbe 13(1):87–99. doi:10.1016/j.chom.2012.11.010
6. Heim G, Sweeney T, O’Shea CJ, Doyle DN, O’Doherty JV (2014) Effect of maternal supplementation with seaweed extracts on growth performance and aspects of gastrointestinal health of newly weaned piglets after challenge with enterotoxigenic Escherichia coli K88. Br J Nutr 112(12):1955–1965. doi:10.1017/S0007114514003171
7. Kreisberg RB, Harper J, Strauman MC, Marohn M, Clements JD, Nataro JP (2011) Induction of increased permeability of polarized enterocyte monolayers by enterotoxigenic Escherichia coli heat-labile enterotoxin. Am J Trop Med Hyg 84(3):451–455. doi:10.4269/ajtmh.2011.10-0445
8. Leocadio PC, Antunes MM, Teixeira LG, Leonel AJ, Alvarez-Leite JI, Machado DC, Generoso SV, Cardoso VN, Correia MI (2015) l-Arginine pretreatment reduces intestinal mucositis as induced by 5-FU in mice. Nutr Cancer 67(3):486–493. doi:10.1080/01635581.2015.1004730
9. Li N, Neu J (2009) Glutamine deprivation alters intestinal tight junctions via a PI3-K/Akt mediated pathway in Caco-2 cells. J Nutr 139(4):710–714. doi:10.3945/jn.108.101485
10. Loos M, Geens M, Schauvliege S, Gasthuys F, van der Meulen J, Dubreuil JD, Goddeeris BM, Niewold T, Cox E (2012) Role of heat-stable enterotoxins in the induction of early immune responses in piglets after infection with enterotoxigenic Escherichia coli. PLoS One 7(7):e41041. doi:10.1371/journal.pone.0041041
11. Nakashima R, Kamata Y, Nishikawa Y (2013) Effects of Escherichia coli heat-stable enterotoxin and guanylin on the barrier integrity of intestinal epithelial T84 cells. Vet Immunol Immunopathol 152(1–2):78–81. doi:10.1016/j.vetimm.2012.09.026
12. Nassour H, Dubreuil JD (2014) Escherichia coli STb enterotoxin dislodges claudin-1 from epithelial tight junctions. PLoS One 9(11):e113273. doi:10.1371/journal.pone.0113273
13. Ngendahayo Mukiza C, Dubreuil JD (2013) Escherichia coli heat-stable toxin b impairs intestinal epithelial barrier function by altering tight junction proteins. Infect Immun 81(8):2819–2827. doi:10.1128/IAI.00455-13
14. Ren W, Yin Y, Liu G, Yu X, Li Y, Yang G, Li T, Wu G (2012) Effect of dietary arginine supplementation on reproductive performance of mice with porcine circovirus type 2 infection. Amino Acids 42(6):2089–2094. doi:10.1007/s00726-011-0942-y
15. Ren W, Li Y, Yu X, Luo W, Liu G, Shao H, Yin Y (2013a) Glutamine modifies immune responses of mice infected with porcine circovirus type 2. Br J Nutr 110(6):1053–1060. doi:10.1017/S0007114512006101
16. Ren W, Liu S, Chen S, Zhang F, Li N, Yin J, Peng Y, Wu L, Liu G, Yin Y, Wu G (2013b) Dietary l-glutamine supplementation increases Pasteurella multocida burden and the expression of its major virulence factors in mice. Amino Acids 45(4):947–955. doi:10.1007/s00726-013-1551-8
17. Ren W, Luo W, Wu M, Liu G, Yu X, Fang J, Li T, Yin Y, Wu G (2013c) Dietary l-glutamine supplementation improves pregnancy outcome in mice infected with type-2 porcine circovirus. Amino Acids 45(3):479–488. doi:10.1007/s00726-011-1134-5
18. Ren W, Zou L, Li N, Wang Y, Liu G, Peng Y, Ding J, Cai L, Yin Y, Wu G (2013d) Dietary arginine supplementation enhances immune responses to inactivated Pasteurella multocida vaccination in mice. Br J Nutr 109(5):867–872. doi:10.1017/S0007114512002681
19. Ren W, Chen S, Yin J, Duan J, Li T, Liu G, Feng Z, Tan B, Yin Y, Wu G (2014a) Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity. J Nutr 144(6):988–995. doi:10.3945/jn.114.192120
20. Ren W, Duan J, Yin J, Liu G, Cao Z, Xiong X, Chen S, Li T, Yin Y, Hou Y, Wu G (2014b) Dietary l-glutamine supplementation modulates microbial community and activates innate immunity in the mouse intestine. Amino Acids 46(10):2403–2413. doi:10.1007/s00726-014-1793-0
21. Ren W, Yin J, Duan J, Liu G, Zhu X, Chen S, Li T, Wang S, Tang Y, Hardwidge PR (2014c) Mouse intestinal innate immune responses altered by enterotoxigenic Escherichia coli (ETEC) infection. Microbes Infect/Inst Pasteur 16(11):954–961. doi:10.1016/j.micinf.2014.09.005
22. Ren W, Yin J, Wu M, Liu G, Yang G, Xion Y, Su D, Wu L, Li T, Chen S, Duan J, Yin Y, Wu G (2014d) Serum amino acids profile and the beneficial effects of l-arginine or l-glutamine supplementation in dextran sulfate sodium colitis. PLoS One 9(2):e88335. doi:10.1371/journal.pone.0088335
23. Ren WK, Yin J, Gao W, Chen S, Duan JL, Liu G, Li TJ, Li NZ, Peng YY, Yin YL (2015) Metabolomics study of metabolic variations in enterotoxigenic Escherichia coli-infected piglets. Rsc Adv 5(73):59550–59555. doi:10.1039/c5ra09513a
24. Ren W, Yin J, Chen S, Duan J, Liu G, Li T, Li N, Peng Y, Tan B, Yin Y (2016a) Proteome analysis for the global proteins in the jejunum tissues of enterotoxigenic Escherichia coli-infected piglets. Sci Rep 6:25640. doi:10.1038/srep25640
25. Ren W, Wang K, Yin J, Chen S, Liu G, Tan B, Wu G, Bazer FW, Peng Y, Yin Y (2016b) Glutamine-induced secretion of intestinal secretory immunoglobulin A: a mechanistic perspective. Front Immunol 7:503. doi:10.3389/fimmu.2016.00503
26. Ren W, Yin J, Duan J, Liu G, Tan B, Yang G, Wu G, Bazer FW, Peng Y, Yin Y (2016c) mTORC1 signaling and IL-17 expression: Defining pathways and possible therapeutic targets. Eur J Immunol 46(2):291–299
27. Ren W, Yin J, Xiao H, Chen S, Liu G, Tan B, Li N, Peng Y, Li T, Zeng B, Li W, Wei H, Yin Z, Wu G, Hardwidge PR, Yin Y (2017a) Intestinal microbiota-derived GABA mediates interleukin-17 expression during enterotoxigenic Escherichia coli infection. Front Immunol 7
28. Ren W, Liu G, Yin J, Tan B, Wu G, Bazer FW, Peng Y, Yin Y (2017b) Amino-acid transporters in T-cell activation and differentiation. Cell Death Dis 8(3):e2655
29. Rowe B, Taylor J, Bettelheim KA (1970) An investigation of traveller’s diarrhoea. Lancet 1(7636):1–5
30. Schroder K, Tschopp J (2010) The inflammasomes. Cell 140(6):821–832. doi:10.1016/j.cell.2010.01.040
31. Sears CL, Kaper JB (1996) Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol Rev 60(1):167–215
32. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820. doi:10.1016/j.cell.2010.01.022
33. Tan B, Xiao H, Xiong X, Wang J, Li G, Yin Y, Huang B, Hou Y, Wu G (2015) l-Arginine improves DNA synthesis in LPS-challenged enterocytes. Frontiers Biosci 20:989–1003
34. Tang Y, Li F, Tan B, Liu G, Kong X, Hardwidge PR, Yin Y (2014) Enterotoxigenic Escherichia coli infection induces intestinal epithelial cell autophagy. Vet Microbiol 171(1–2):160–164. doi:10.1016/j.vetmic.2014.03.025
35. Vereecke L, Beyaert R, van Loo G (2011) Enterocyte death and intestinal barrier maintenance in homeostasis and disease. Trends Mol Med 17(10):584–593. doi:10.1016/j.molmed.2011.05.011
36. Wan F, Weaver A, Gao X, Bern M, Hardwidge PR, Lenardo MJ (2011) IKKbeta phosphorylation regulates RPS3 nuclear translocation and NF-kappaB function during infection with Escherichia coli strain O157:H7. Nat Immunol 12(4):335–343. doi:10.1038/ni.2007
37. Wang X, Hardwidge PR (2012) Enterotoxigenic Escherichia coli prevents host NF-kappaB activation by targeting IkappaBalpha polyubiquitination. Infect Immun 80(12):4417–4425. doi:10.1128/IAI.00809-12
38. Wang X, Gao X, Hardwidge PR (2012) Heat-labile enterotoxin-induced activation of NF-kappaB and MAPK pathways in intestinal epithelial cells impacts enterotoxigenic Escherichia coli (ETEC) adherence. Cell Microbiol 14(8):1231–1241. doi:10.1111/j.1462-5822.2012.01793.x
39. Wang B, Wu Z, Ji Y, Sun K, Dai Z, Wu G (2016) l-Glutamine enhances tight junction integrity by activating CaMK kinase 2-AMP-activated protein kinase signaling in intestinal porcine epithelial cells. J Nutr 146(3):501–508. doi:10.3945/jn.115.224857
40. Wu L, Liao P, He L, Feng Z, Ren W, Yin J, Duan J, Li T, Yin Y (2015) Dietary l-arginine supplementation protects weanling pigs from deoxynivalenol-induced toxicity. Toxins 7(4):1341–1354. doi:10.3390/toxins7041341
41. Wu M, Xiao H, Liu G, Chen S, Tan B, Ren W, Bazer FW, Wu G, Yin Y (2016) Glutamine promotes intestinal SIgA secretion through intestinal microbiota and IL-13. Mol Nutr Food Res 60(7):1637–1648. doi:10.1002/mnfr.201600026
42. Xiao D, Wang Y, Liu G, He J, Qiu W, Hu X, Feng Z, Ran M, Nyachoti CM, Kim SW, Tang Z, Yin Y (2014) Effects of chitosan on intestinal inflammation in weaned pigs challenged by enterotoxigenic Escherichia coli. PLoS One 9(8):e104192. doi:10.1371/journal.pone.0104192
43. Xiao DF, Ren WK, Bin P, Chen S, Yin J, Gao W, Liu G, Nan Z, Hu XG, He JH (2016) Chitosan lowers body weight through intestinal microbiota and reduces IL-17 expression via mTOR signalling. J Funct Foods 22:166–176. doi:10.1016/j.jff.2016.01.009
44. Zhang L, Zhang L, Zhan X, Zeng X, Zhou L, Cao G, Chen A, Yang C (2016) Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J Anim Sci Biotechnol 7:3. doi:10.1186/s40104-016-0061-4