SPECIAL COLUMN:RESEARCH PROGRESS ON FEED NUTRITION

Research Progress of Mechanism of Intestinal Inflammation and Its Nutritional Regulation

  • WEI Hongkui ,
  • WU Xiaoyu ,
  • CUI Chenbin ,
  • PENG Jian
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  • 1. College of Animal Science and Technology, Huazhong Agricultural University, Wuhan 430070, China;
    2. Cooperative Innovation Center for Sustainable Pig Production, Wuhan 430070, China

Received date: 2022-08-01

  Online published: 2022-10-17

Abstract

The normal structure and function of intestinal epithelial barrier is the basis for maintaining production performance of pigs. However, in pig production, a variety of infectious or non-infectious factors may induce excessive intestinal inflammation, damage the intestinal epithelium and repair progress, thus seriously affecting the health and performance of pigs. For the intestinal excessive inflammatory response caused by different factors, the common feature is that the initiated inflammatory response will be amplified to produce a large number of inflammatory cytokines. Recent studies have found that programmed cell death (PCD) plays an important role in the occurrence and development of intestinal inflammation. This review will focus on the role of PCD in intestinal inflammation and the effects of dietary components on the regulation of intestinal cell PCD and intestinal inflammatory response.

Cite this article

WEI Hongkui , WU Xiaoyu , CUI Chenbin , PENG Jian . Research Progress of Mechanism of Intestinal Inflammation and Its Nutritional Regulation[J]. Chinese Journal of Animal Nutrition, 2022 , 34(10) : 6358 -6370 . DOI: 10.3969/j.issn.1006-267x.2022.10.029

References

[1] WEISS U.Intestinal networks in health and disease[J].Nature,2011,474(7351):297.
[2] ADEWOLE D I,KIM I H,NYACHOTI C M.Gut health of pigs:challenge models and response criteria with a critical analysis of the effectiveness of selected feed additives-a review[J].Asian-Australasian Journal of Animal Sciences,2016,29(7):909-924.
[3] TANG F,WANG J F,LI D Z,et al.Comparative genomic analysis of 127 Escherichia coli strains isolated from domestic animals with diarrhea in China[J].BMC Genomics,2019,20(1):212.
[4] ZHANG H L,HAN F F,YAN X G,et al.Prevalence and phylogenetic analysis of spike gene of porcine epidemic diarrhea virus in Henan province,China in 2015-2019[J].Infection,Genetics and Evolution,2021,88:104709.
[5] YANG C K,CHENG Y H,TSAI W T,et al.Prevalence of mycotoxins in feed and feed ingredients between 2015 and 2017 in Taiwan[J].Environmental Science and Pollution Research International,2019,26(23):23798-23806.  
[6] LEBERT D C,HUTTENLOCHER A.Inflammation and wound repair[J].Seminars in Immunology,2014,26(4):315-320.  
[7] SOMMER K,WIENDL M,MVLLER T M,et al.Intestinal mucosal wound healing and barrier integrity in IBD-crosstalk and trafficking of cellular players[J].Frontiers in Medicine,2021,8:643973.
[8] XUE X,FALCON D M.The role of immune cells and cytokines in intestinal wound healing[J].International Journal of Molecular Sciences,2019,20(23):6097.
[9] JUNG K,SAIF L J,WANG Q H.Porcine epidemic diarrhea virus (PEDV):an update on etiology,transmission,pathogenesis,and prevention and control[J].Virus Research,2020,286:198045.
[10] PARDO-CAMACHO C,GONZÁLEZ-CASTRO A M,RODIÑO-JANEIRO B K,et al.Epithelial immunity:priming defensive responses in the intestinal mucosa[J].American Journal of Physiology.Gastrointestinal and Liver Physiology,2018,314(2):G247-G255.
[11] ALLAIRE J M,CROWLEY S M,LAW H T,et al.The intestinal epithelium:central coordinator of mucosal immunity[J].Trends in Immunology,2018,39(9):677-696.  
[12] PLUSKE J R,TURPIN D L,KIM J C.Gastrointestinal tract (gut) health in the young pig[J].Animal Nutrition,2018,4(2):187-196.  
[13] YANG Q L,WANG Y X,JIA A N,et al.The crosstalk between gut bacteria and host immunity in intestinal inflammation[J].Journal of Cellular Physiology,2021,236(4):2239-2254.  
[14] LEONARDI I,LI X,ILIEV I D.Macrophage interactions with fungi and bacteria in inflammatory bowel disease[J].Current Opinion in Gastroenterology,2018,34(6):392-397.  
[15] UENISHI H,SHINKAI H.Porcine Toll-like receptors:the front line of pathogen monitoring and possible implications for disease resistance[J].Developmental and Comparative Immunology,2009,33(3):353-361.  
[16] BRYAN N,AHSWIN H,SMART N,et al.Reactive oxygen species (ROS)-a family of fate deciding molecules pivotal in constructive inflammation and wound healing[J].European Cells&Materials,2012,24:249-265.
[17] KRATOFIL R M,KUBES P,DENISET J F.Monocyte conversion during inflammation and injury[J].Arteriosclerosis,Thrombosis,and Vascular Biology,2017,37(1):35-42.  
[18] PATANKAR J V,BECKER C.Cell death in the gut epithelium and implications for chronic inflammation[J].Nature Reviews:Gastroenterology&Hepatology,2020,17(9):543-556.  
[19] LIU Y L.Fatty acids,inflammation and intestinal health in pigs[J].Journal of Animal Science and Biotechnology,2015,6(1):41.
[20] SHIRKEY T W,SIGGERS R H,GOLDADE B G,et al.Effects of commensal bacteria on intestinal morphology and expression of proinflammatory cytokines in the gnotobiotic pig[J].Experimental Biology and Medicine,2006,231(8):1333-1345.  
[21] CHENG C S,XIA M,ZHANG X M,et al.Supplementing oregano essential oil in a reduced-protein diet improves growth performance and nutrient digestibility by modulating intestinal bacteria,intestinal morphology,and antioxidative capacity of growing-finishing pigs[J].Animals,2018,8(9):159.
[22] LUO Y H,LIU L,CHEN D W,et al.Dietary supplementation of fructo-oligosaccharides alleviates enterotoxigenic E. coli-induced disruption of intestinal epithelium in a weaned piglet model[J/OL].British Journal of Nutrition:1-9[2022-07-15].https://doi.org/10.1017/S0007114521004451.DOI:10.1017/S0007114521004451.
[23] CAPRARA G,ALLAVENA P,ERRENI M.Intestinal macrophages at the crossroad between diet,inflammation,and cancer[J].International Journal of Molecular Sciences,2020,21(14):4825.
[24] ADOLPH T E,TOMCZAK M F,NIEDERREITER L,et al.Paneth cells as a site of origin for intestinal inflammation[J].Nature,2013,503(7475):272-276.  
[25] CUI C B,LIU Q,DUAN B B,et al.Bioactive triple peptide inhibits inflammasome activation to alleviate Salmonella-induced intestinal inflammation in mice via modulation of host defense and bacterial virulence[J].Food&Function,2022,13(6):3512-3525.  
[26] BOATRIGHT K M,SALVESEN G S.Mechanisms of caspase activation[J].Current Opinion in Cell Biology,2003,15(6):725-731.  
[27] SHI Y G.Caspase activation:revisiting the induced proximity model[J].Cell,2004,117(7):855-858.  
[28] 李若楠,康瑞芬,沈丹,等.谷氨酰胺对呕吐毒素诱导IPEC-J2细胞凋亡和炎症的影响[J].南京农业大学学报,2020,43(4):740-747. LI R N,KANG R F,SHEN D,et al.Effects of glutamine on deoxynivalenol induced apoptosis and inflammation of IPEC-J2 cells[J].Journal of Nanjing Agricultural University,2020,43(4):740-747.(in Chinese)
[29] 廖美芳,孟英才,詹济华,等.呕吐毒素对IPEC-J2细胞凋亡的影响[J].动物营养学报,2018,30(3):1027-1034. LIAO M F,MENG Y C,ZHAN J H,et al.Effects of deoxynivalenol on apoptosis of IPEC-J2 cells[J].Chinese Journal of Animal Nutrition,2018,30(3):1027-1034.(in Chinese)
[30] XIAO K,LIU C C,QIN Q,et al.EPA and DHA attenuate deoxynivalenol-induced intestinal porcine epithelial cell injury and protect barrier function integrity by inhibiting necroptosis signaling pathway[J].The FASEB Journal,2020,34(2):2483-2496.  
[31] XIA P P,WU Y P,LIAN S Q,et al.Deletion of FaeG alleviated enterotoxigenic Escherichia coli F4ac-induced apoptosis in the intestine[J].AMB Express,2021,11(1):44.
[32] KUMAR P,JAGTAP Y A,PATWA S M,et al.Autophagy based cellular physiological strategies target oncogenic progression[J].Journal of Cellular Physiology,2022,237(1):258-277.  
[33] BEDOUI S,HEROLD M J,STRASSER A.Emerging connectivity of programmed cell death pathways and its physiological implications[J].Nature Reviews Molecular Cell Biology,2020,21(11):678-695.  
[34] KROEMER G,LEVINE B.Autophagic cell death:the story of a misnomer[J].Nature Reviews:Molecular Cell Biology,2008,9(12):1004-1010.  
[35] CAO Z,GAO J S,HUANG W Y,et al.Curcumin mitigates deoxynivalenol-induced intestinal epithelial barrier disruption by regulating Nrf2/p53 and NF-κB/MLCK signaling in mice[J].Food and Chemical Toxicology,2022,167:113281.
[36] LIU S P,KANG W L,MAO X R,et al.Low dose of arsenic exacerbates toxicity to mice and IPEC-J2 cells exposed with deoxynivalenol:aryl hydrocarbon receptor and autophagy might be novel therapeutic targets[J].Science of the Total Environment,2022,832:155027.
[37] GE L,LIU D D,MAO X R,et al.Low dose of deoxynivalenol aggravates intestinal inflammation and barrier dysfunction induced by enterotoxigenic Escherichia coli infection through activating macroautophagy/NLRP3 inflammasomes[J].Journal of Agricultural and Food Chemistry,2022,70(9):3009-3022.  
[38] YAMOTO M,LEE C,CHUSILP S,et al.The role of autophagy in intestinal epithelial injury[J].Pediatric Surgery International,2019,35(12):1389-1394.  
[39] TENEV T,BIANCHI K,DARDING M,et al.The ripoptosome,a signaling platform that assembles in response to genotoxic stress and loss of IAPs[J].Molecular Cell,2011,43(3):432-448.  
[40] HILDEBRAND J M,TANZER M C,LUCET I S,et al.Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death[J].Proceedings of the National Academy of Sciences of the United States of America,2014,111(42):15072-15077.  
[41] MARTENS S,BRIDELANCE J,ROELANDT R,et al.MLKL in cancer:more than a necroptosis regulator[J].Cell Death and Differentiation,2021,28(6):1757-1772.  
[42] LIU Y L,XU Q,WANG Y,et al.Necroptosis is active and contributes to intestinal injury in a piglet model with lipopolysaccharide challenge[J].Cell Death&Disease,2021,12(1):62.
[43] ZHANG Y,ZHANG J L,BAO J,et al.Selenium deficiency induced necroptosis,Th1/Th2 imbalance,and inflammatory responses in swine ileum[J].Journal of Cellular Physiology,2021,236(1):222-234.  
[44] CHEN X M,BI M Y,YANG J,et al.Cadmium exposure triggers oxidative stress,necroptosis,Th1/Th2 imbalance and promotes inflammation through the TNF-α/NF-κB pathway in swine small intestine[J].Journal of Hazardous Materials,2022,421:126704.
[45] XIAO K,XU Q,LIU C C,et al.Docosahexaenoic acid alleviates cell injury and improves barrier function by suppressing necroptosis signaling in TNF-α-challenged porcine intestinal epithelial cells[J].Innate Immunity,2020,26(8):653-665.  
[46] RAUCH I,DEETS K A,JI D X,et al.NAIP-NLRC4 inflammasomes coordinate intestinal epithelial cell expulsion with eicosanoid and IL-18 release via activation of caspase-1 and-8[J].Immunity,2017,46(4):649-659.  
[47] KAYAGAKI N,WONG M T,STOWE I B,et al.Noncanonical inflammasome activation by intracellular LPS independent of TLR4[J].Science,2013,341(6151):1246-1249.  
[48] KERN M,ASCHENBACH J R,TEDIN K,et al.Characterization of inflammasome components in pig intestine and analysis of the influence of probiotic Enterococcus faecium during an Escherichia coli challenge[J].Immunological Investigations,2017,46(7):742-757.  
[49] LIU Y,YAO W X,XU J,et al.The anti-inflammatory effects of acetaminophen and N-acetylcysteine through suppression of the NLRP3 inflammasome pathway in LPS-challenged piglet mononuclear phagocytes[J].Innate Immunity,2015,21(6):587-597.  
[50] SAKUMA C,TOKI D,SHINKAI H,et al.Pig lacks functional NLRC4 and NAIP genes[J].Immunogenetics,2017,69(2):125-130.  
[51] WU G Y.Functional amino acids in growth,reproduction,and health[J].Advances in Nutrition,2010,1(1):31-37.  
[52] KIM S W,MATEO R D,YIN Y L,et al.Functional amino acids and fatty acids for enhancing production performance of sows and piglets[J].Asian-Australasian Journal of Animal Sciences,2007,20(2):295-306.
[53] LIU Y L,HUANG J J,HOU Y Q,et al.Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs[J].British Journal of Nutrition,2008,100(3):552-560.  
[54] ZHOU X H,ZHANG Y M,WU X,et al.Effects of dietary serine supplementation on intestinal integrity,inflammation and oxidative status in early-weaned piglets[J].Cellular Physiology and Biochemistry,2018,48(3):993-1002.  
[55] ZHU L H,CAI X,GUO Q,et al.Effect of N-acetyl cysteine on enterocyte apoptosis and intracellular signaling pathways'response to oxidative stress in weaned piglets[J].British Journal of Nutrition,2013,110(11):1938-1947.  
[56] ZHANG Y C,MU T Q,JIA H,et al.Protective effects of glycine against lipopolysaccharide-induced intestinal apoptosis and inflammation[J].Amino Acids,2022,54(3):353-364.  
[57] LIU G M,TAO J Y,LU J J,et al.Dietary tryptophan supplementation improves antioxidant status and alleviates inflammation,endoplasmic reticulum stress,apoptosis,and pyroptosis in the intestine of piglets after lipopolysaccharide challenge[J].Antioxidants,2022,11(5):872.
[58] YANG Y,LI W,SUN Y L,et al.Amino acid deprivation disrupts barrier function and induces protective autophagy in intestinal porcine epithelial cells[J].Amino Acids,2015,47(10):2177-2184.  
[59] ZHU Y H,LIN G,DAI Z L,et al.L-glutamine deprivation induces autophagy and alters the mTOR and MAPK signaling pathways in porcine intestinal epithelial cells[J].Amino Acids,2015,47(10):2185-2197.  
[60] ZHANG H,MA Y,WANG M Z,et al.Dietary supplementation of L-arginine and N-carbamylglutamate enhances duodenal barrier and mitochondrial functions and suppresses duodenal inflammation and mitophagy in suckling lambs suffering from intrauterine-growth-restriction[J].Food&Function,2020,11(5):4456-4470.  
[61] WANG H Y,LI C C,PENG M,et al.N-acetylcysteine improves intestinal function and attenuates intestinal autophagy in piglets challenged with β-conglycinin[J].Scientific Reports,2021,11(1):1261.
[62] ZIMMERMAN M A,SINGH N,MARTIN P M,et al.Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells[J].American Journal of Physiology.Gastrointestinal and Liver Physiology,2012,302(12):G1405-G1415.
[63] ZHOU C,LI L Z,LI T M,et al.SCFAs induce autophagy in intestinal epithelial cells and relieve colitis by stabilizing HIF-1α[J].Journal of Molecular Medicine,2020,98(8):1189-1202.  
[64] LI X,WANG C C,ZHU J,et al.Sodium butyrate ameliorates oxidative stress-induced intestinal epithelium barrier injury and mitochondrial damage through AMPK-mitophagy pathway[J].Oxidative Medicine and Cellular Longevity,2022,2022:3745135.
[65] WANG C C,CAO S T,ZHANG Q H,et al.Dietary tributyrin attenuates intestinal inflammation,enhances mitochondrial function,and induces mitophagy in piglets challenged with diquat[J].Journal of Agricultural and Food Chemistry,2019,67(5):1409-1417.  
[66] CHU B X,ZHU Y H,SU J H,et al.Butyrate-mediated autophagy inhibition limits cytosolic Salmonella infantis replication in the colon of pigs treated with a mixture of Lactobacillus and Bacillus[J].Veterinary Research,2020,51(1):99.
[67] FENG Y H,WANG Y,WANG P,et al.Short-chain fatty acids manifest stimulative and protective effects on intestinal barrier function through the inhibition of NLRP3 inflammasome and autophagy[J].Cellular Physiology and Biochemistry,2018,49(1):190-205.  
[68] XIAO K,YANG Y,ZHANG Y,et al.Long-chain PUFA ameliorate enterotoxigenic Escherichia coli-induced intestinal inflammation and cell injury by modulating pyroptosis and necroptosis signaling pathways in porcine intestinal epithelial cells[J].British Journal of Nutrition,2022,128(5):835-850.  
[69] 王晓杰,黄立新,张彩虹,等.植物提取物饲料添加剂的研究进展[J].生物质化学工程,2018,52(3):50-58. WANG X J,HUANG L X,ZHANG C H,et al.Research development of botanical extract as feed additive in poultry[J].Biomass Chemical Engineering,2018,52(3):50-58.(in Chinese)
[70] MOHAMMADI GHEISAR M,KIM I H.Phytobiotics in poultry and swine nutrition-a review[J].Italian Journal of Animal Science,2018,17(1):92-99.  
[71] WAN J,ZHANG J,CHEN D W,et al.Alginate oligosaccharide-induced intestinal morphology,barrier function and epithelium apoptosis modifications have beneficial effects on the growth performance of weaned pigs[J].Journal of Animal Science and Biotechnology,2018,9:58.
[72] CHEN J L,XIE H M,CHEN D W,et al.Chlorogenic acid improves intestinal development via suppressing mucosa inflammation and cell apoptosis in weaned pigs[J].ACS Omega,2018,3(2):2211-2219.  
[73] XU X X,YAN G R,CHANG J,et al.Astilbin ameliorates deoxynivalenol-induced oxidative stress and apoptosis in intestinal porcine epithelial cells (IPEC-J2)[J].Journal of Applied Toxicology,2020,40(10):1362-1372.  
[74] JIN Y H,ZHAI Z A,JIA H,et al.Kaempferol attenuates diquat-induced oxidative damage and apoptosis in intestinal porcine epithelial cells[J].Food&Function,2021,12(15):6889-6899.  
[75] CHEN Z G,YUAN Q L,XU G R,et al.Effects of quercetin on proliferation and H2O2-induced apoptosis of intestinal porcine enterocyte cells[J].Molecules,2018,23(8):2012.
[76] LI L,WAN G W,HAN B,et al.Echinacoside alleviated LPS-induced cell apoptosis and inflammation in rat intestine epithelial cells by inhibiting the mTOR/STAT3 pathway[J].Biomedicine&Pharmacotherapy,2018,104:622-628.
[77] LOGANES C,LEGA S,BRAMUZZO M,et al.Curcumin anti-apoptotic action in a model of intestinal epithelial inflammatory damage[J].Nutrients,2017,9(6):578.
[78] ZHAO J,SUN Y,SHI P L,et al.Celastrol ameliorates experimental colitis in IL-10 deficient mice via the up-regulation of autophagy[J].International Immunopharmacology,2015,26(1):221-228.  
[79] FAN X D,WANG J,HOU J C,et al.Berberine alleviates ox-LDL induced inflammatory factors by up-regulation of autophagy via AMPK/mTOR signaling pathway[J].Journal of Translational Medicine,2015,13:92.
[80] CAO S T,SHEN Z J,WANG C C,et al.Resveratrol improves intestinal barrier function,alleviates mitochondrial dysfunction and induces mitophagy in diquat challenged piglets[J].Food&Function,2019,10(1):344-354.  
[81] GUO W J,LIU W,JIN B,et al.Asiatic acid ameliorates dextran sulfate sodium-induced murine experimental colitis via suppressing mitochondria-mediated NLRP3 inflammasome activation[J].International Immunopharmacology,2015,24(2):232-238.  
[82] WANG K,LV Q,MIAO Y M,et al.Cardamonin,a natural flavone,alleviates inflammatory bowel disease by the inhibition of NLRP3 inflammasome activation via an AhR/Nrf2/NQO1 pathway[J].Biochemical Pharmacology,2018,155:494-509.
[83] LI X D,WU X,WANG Q,et al.Sanguinarine ameliorates DSS induced ulcerative colitis by inhibiting NLRP3 inflammasome activation and modulating intestinal microbiota in C57BL/6 mice[J].Phytomedicine,2022,104:154321.
[84] 佚名.农业农村部办公厅关于印发《直接饲喂微生物和发酵制品生产菌株鉴定及其安全性评价指南》的通知(农办牧
[2021] 43号)[J].中华人民共和国农业农村部公报,2021(11):97-111. Anon.Circular of the General Office of the Ministry of Agriculture and Rural Affairs on printing and distributing the guidelines on identification and safety evaluation of direct-fed microbials and fermented-food-derived bacterial strains (
[2021] 43)[J].Gazette of the Ministry of Agriculture and Affairs of the People's Republic of China,2021(11):97-111.(in Chinese)
[85] BUNTYN J O,SCHMIDT T B,NISBET D J,et al.The role of direct-fed microbials in conventional livestock production[J].Annual Review of Animal Biosciences,2016,4:335-355.
[86] GARCÍA G R,PAYROS D,PINTON P,et al.Intestinal toxicity of deoxynivalenol is limited by Lactobacillus rhamnosus RC007 in pig jejunum explants[J].Archives of Toxicology,2018,92(2):983-993.  
[87] YANG X,LIANG S S,GUO F S,et al.Gut microbiota mediates the protective role of Lactobacillus plantarum in ameliorating deoxynivalenol-induced apoptosis and intestinal inflammation of broiler chickens[J].Poultry Science,2020,99(5):2395-2406.  
[88] GAO Q X,QI L L,WU T X,et al.Ability of Clostridium butyricum to inhibit Escherichia coli-induced apoptosis in chicken embryo intestinal cells[J].Veterinary Microbiology,2012,160(3/4):395-402.
[89] XIAO Z P,LIU L J,TAO W J,et al.Clostridium tyrobutyricum protect intestinal barrier function from LPS-induced apoptosis via P38/JNK signaling pathway in IPEC-J2 cells[J].Cellular Physiology and Biochemistry,2018,46(5):1779-1792.  
[90] TANG L,ZENG Z H,ZHOU Y H,et al.Bacillus amyloliquefaciens SC06 induced AKT-FOXO signaling pathway-mediated autophagy to alleviate oxidative stress in IPEC-J2 cells[J].Antioxidants,2021,10(10):1545.
[91] KHAILOVA L,MOUNT PATRICK S K,ARGANBRIGHT K M,et al.Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis[J].American Journal of Physiology:Gastrointestinal and Liver Physiology,2010,299(5):G1118-G1127.
[92] LI H H,LI Y P,ZHU Q,et al.Dietary supplementation with Clostridium butyricum helps to improve the intestinal barrier function of weaned piglets challenged with enterotoxigenic Escherichia coli K88[J].Journal of Applied Microbiology,2018,125(4):964-975.  
[93] XIA B,YU J,HE T,et al.Lactobacillus johnsonii L531 ameliorates enteritis via elimination of damaged mitochondria and suppression of SQSTM1-dependent mitophagy in a Salmonella infantis model of piglet diarrhea[J].The FASEB Journal,2020,34(2):2821-2839.  
[94] YU J,ZHU Y H,YANG G Y,et al.Anti-inflammatory capacity of Lactobacillus rhamnosus GG in monophasic variant Salmonella infected piglets is correlated with impeding NLRP6-mediated host inflammatory responses[J].Veterinary Microbiology,2017,210:91-100.
[95] SUZUKI H,YAMAZAKI T,OHSHIO K,et al.A specific strain of lactic acid bacteria,Lactobacillus paracasei,inhibits inflammasome activation in vitro and prevents inflammation-related disorders[J].Journal of Immunology,2020,205(3):811-821.  
[96] CHEN S Y,LI Y N,CHU B X,et al.Lactobacillus johnsonii L531 alleviates the damage caused by Salmonella typhimurium via inhibiting TLR4,NF-κB,and NLRP3 inflammasome signaling pathways[J].Microorganisms,2021,9(9):1983.
[97] HAN C Q,DING Z,SHI H Y,et al.The role of probiotics in lipopolysaccharide-induced autophagy in intestinal epithelial cells[J].Cellular Physiology and Biochemistry,2016,38(6):2464-2478.  
[98] YAN S Q,QIAO L,DOU X N,et al.Biogenic selenium nanoparticles by Lactobacillus casei ATCC 393 alleviate the intestinal permeability,mitochondrial dysfunction and mitophagy induced by oxidative stress[J].Food&Function,2021,12(15):7068-7080.  
[99] CUI Y J,LIU L,DOU X X,et al.Lactobacillus reuteri ZJ617 maintains intestinal integrity via regulating tight junction,autophagy and apoptosis in mice challenged with lipopolysaccharide[J].Oncotarget,2017,8(44):77489-77499.  
[100] ZHANG W,ZHU Y H,YANG G Y,et al.Lactobacillus rhamnosus GG affects microbiota and suppresses autophagy in the intestines of pigs challenged with Salmonella infantis[J].Frontiers in Microbiology,2018,8:2705.
[101] KORHONEN H,PIHLANTO A.Food-derived bioactive peptides-opportunities for designing future foods[J].Current Pharmaceutical Design,2003,9(16):1297-1308.  
[102] GIANFRANCESCHI G L,GIANFRANCESCHI G,QUASSINTI L,et al.Biochemical requirements of bioactive peptides for nutraceutical efficacy[J].Journal of Functional Foods,2018,47:252-263.
[103] BECHAUX J,GATELLIER P,LE PAGE J F,et al.A comprehensive review of bioactive peptides obtained from animal byproducts and their applications[J].Food&Function,2019,10(10):6244-6266.  
[104] DALIRI E B M,LEE B H,OH D H.Current trends and perspectives of bioactive peptides[J].Critical Reviews in Food Science and Nutrition,2018,58(13):2273-2284.  
[105] DENG Z,NI J J,WU X Y,et al.GPA peptide inhibits NLRP3 inflammasome activation to ameliorate colitis through AMPK pathway[J].Aging,2020,12(18):18522-18544.  
[106] DENG Z,LIU Q,WANG M M,et al.GPA peptide-induced Nur77 localization at mitochondria inhibits inflammation and oxidative stress through activating autophagy in the intestine[J].Oxidative Medicine and Cellular Longevity,2020,2020:4964202.
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