Gut microbiota; Immunity; Inflammatory response; Laying hen; Yeast cell wall polysaccharides; Structural Biology; Biochemistry; Molecular Biology; General Medicine
Abstract :
[en] Effects of dietary supplementation of yeast cell-wall polysaccharides (YCWP) on production performance, ileal microbial composition, immunomodulatory and anti-inflammatory effects in LPS-challenged laying hens, were evaluated. A total of 288 35-week-old Hy-Line Brown layers were randomly assigned into 4 dietary treatments: 0, 250, 500 and 1000 mg/kg YCWP, respectively. After a 12-week feeding period, a total of 32 birds were selected from the control (n = 16) and 1000 mg/kg YCWP group (n = 16). For each group, half (n = 8) received Escherichia coli LPS and half (n = 8) received PBS at 1 mg/kg body weight, intravenously. Results showed that YCWP enhanced feed efficiency and egg production linearly, with optimal laying performance notable in the 1000 mg/kg YCWP group. Dietary YCWP enhanced serum IgM and expression of ileal avian β-defensin, alleviated the LPS-induced elevated levels of serum IL-6 and IL-1β and the up-regulated expression of IL-1β, TNF-α, IFN-γ, and IL-6 in spleen and/or ileal mucosa. Furthermore, anti-inflammatory and immunomodulatory effects of YCWP were linked with its enhancement effect on microbial diversity, proliferation of Bifidobacteriaceae, Lactocillus, Candidatus_Arthromitus, Streptomyces, Bacillaceae, and Desulfovibrio, and reduced abundance of Shigella. Therefore, YCWP has the potentials to be utilized as safe prebiotics and gut enhancer in laying hens.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Zhou, Jianmin; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Fu, Yu ; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Qi, Guanghai; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Zhang, Haijun; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Wang, Jing; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China. Electronic address: wangjing@caas.cn
Wu, Shugeng; Key Laboratory of Feed Biotechnology of Ministry of Agriculture & Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Language :
English
Title :
Yeast cell-wall polysaccharides improve immunity and attenuate inflammatory response via modulating gut microbiota in LPS-challenged laying hens.
Publication date :
18 October 2022
Journal title :
International Journal of Biological Macromolecules
This work was supported by Agriculture Research System of China ( CARS-40-K12 ), and the Agricultural Science and Technology Innovation Program (ASTIP) of the Chinese Academy of Agricultural Sciences .
Nie, W., Wang, B., Gao, J., Guo, Y., Wang, Z., Effects of dietary phosphorous supplementation on laying performance, egg quality, bone health and immune responses of laying hens challenged with Escherichia coli lipopolysaccharide. J. Anim. Sci. Biotechnol., 9, 2018, 53, 10.1186/s40104-018-0271-z.
Zhen, W., Shao, Y., Wu, Y., Li, L., Pham, V.H., Abbas, W., Wan, Z., Guo, Y., Wang, Z., Dietary yeast beta-glucan supplementation improves eggshell color and fertile eggs hatchability as well as enhances immune functions in breeder laying hens. Int. J. Biol. Macromol. 159 (2020), 607–621, 10.1016/j.ijbiomac.2020.05.134.
Zhou, J., Wu, S., Qi, G., Fu, Y., Wang, W., Zhang, H., Wang, J., Dietary supplemental xylooligosaccharide modulates nutrient digestibility, intestinal morphology, and gut microbiota in laying hens. Anim. Nutr. 7 (2021), 152–162, 10.1016/j.aninu.2020.05.010.
Lillehoj, H.S., Lee, K.W., Immune modulation of innate immunity as alternatives-to-antibiotics strategies to mitigate the use of drugs in poultry production. Poult. Sci. 91 (2012), 1286–1291, 10.3382/ps.2012-02374.
Fleet, G.H., Manners, D.J., Isolation and composition of an alkali-soluble glucan from the cell walls of Saccharomyces cerevisiae. J. Gen. Microbiol. 94 (1976), 180–192, 10.1099/00221287-94-1-180.
Jawhara, S., Habib, K., Maggiotto, F., Pignede, G., Vandekerckove, P., Maes, E., Dubuquoy, L., Fontaine, T., Guerardel, Y., Poulain, D., Modulation of intestinal inflammation by yeasts and cell wall extracts: strain dependence and unexpected anti-inflammatory role of glucan fractions. PLoS One, 7, 2012, e40648, 10.1371/journal.pone.0040648.
Liu, Y., Wu, Q., Wu, X., Algharib, S.A., Gong, F., Hu, J., Luo, W., Zhou, M., Pan, Y., Yan, Y., Wang, Y., Structure, preparation, modification, and bioactivities of beta-glucan and mannan from yeast cell wall: a review. Int. J. Biol. Macromol. 173 (2021), 445–456, 10.1016/j.ijbiomac.2021.01.125.
Schwartz, B., Vetvicka, V., Review: beta-glucans as effective antibiotic alternatives in poultry. Molecules, 26, 2021, 3560, 10.3390/molecules26123560.
Ganan, M., Carrascosa, A.V., de Pascual-Teresa, S., Martinez-Rodriguez, A.J., Effect of mannoproteins on the growth, gastrointestinal viability, and adherence to Caco-2 cells of lactic acid bacteria. J. Food Sci. 77 (2012), M176–M180, 10.1111/j.1750-3841.2011.02602.x.
Chen, K.L., Weng, B.C., Chang, M.T., Liao, Y.H., Chen, T.T., Chu, C., Direct enhancement of the phagocytic and bactericidal capability of abdominal macrophage of chicks by beta-1,3–1,6-glucan. Poult. Sci. 87 (2008), 2242–2249, 10.3382/ps.2008-00147.
Chen, H.L., Li, D.F., Chang, B.Y., Gong, L.M., Piao, X.S., Yi, G.F., Zhang, J.X., Effects of lentinan on broiler splenocyte proliferation, interleukin-2 production, and signal transduction. Poult. Sci. 82 (2003), 760–766, 10.1093/ps/82.5.760.
Chuammitri, P., Redmond, S.B., Kimura, K., Andreasen, C.B., Lamont, S.J., Palić, D., Heterophil functional responses to dietary immunomodulators vary in genetically distinct chicken lines. Vet. Immunol. Immunopathol. 142 (2011), 219–227, 10.1016/j.vetimm.2011.05.019.
Chae, B.J., Lohakare, J.D., Moon, W.K., Lee, S.L., Park, Y.H., Hahn, T.W., Effects of supplementation of beta-glucan on the growth performance and immunity in broilers. Res. Vet. Sci. 80 (2006), 291–298, 10.1016/j.rvsc.2005.07.008.
Cox, C.M., Stuard, L.H., Kim, S., McElroy, A.P., Bedford, M.R., Dalloul, R.A., Performance and immune responses to dietary beta-glucan in broiler chicks. Poult. Sci. 89 (2010), 1924–1933, 10.3382/ps.2010-00865.
Xue, G.D., Wu, S.B., Choct, M., Swick, R.A., Effects of yeast cell wall on growth performance, immune responses and intestinal short chain fatty acid concentrations of broilers in an experimental necrotic enteritis model. Anim. Nutr. 3 (2017), 399–405, 10.1016/j.aninu.2017.08.002.
Lee, Y., Lee, S.H., Gadde, U.D., Oh, S.T., Lee, S.J., Lillehoj, H.S., Dietary Allium hookeri reduces inflammatory response and increases expression of intestinal tight junction proteins in LPS-induced young broiler chicken. Res. Vet. Sci. 112 (2017), 149–155, 10.1016/j.rvsc.2017.03.019.
Hu, R., He, Z., Liu, M., Tan, J., Zhang, H., Hou, D.X., He, J., Wu, S., Dietary protocatechuic acid ameliorates inflammation and up-regulates intestinal tight junction proteins by modulating gut microbiota in LPS-challenged piglets. J. Anim. Sci. Biotechnol., 11, 2020, 92, 10.1186/s40104-020-00492-9.
Gao, R., Tian, S., Wang, J., Zhu, W., Galacto-oligosaccharides improve barrier function and relieve colonic inflammation via modulating mucosa-associated microbiota composition in lipopolysaccharides-challenged piglets. J. Anim. Sci. Biotechnol., 12, 2021, 92, 10.1186/s40104-021-00612-z.
Jiang, J., Qi, L., Wei, Q., Shi, F., Maternal stevioside supplementation ameliorates intestinal mucosal damage and modulates gut microbiota in chicken offspring challenged with lipopolysaccharide. Food Funct. 12 (2021), 6014–6028, 10.1039/d0fo02871a.
Dobrovolskaia, M.A., Vogel, S.N., Toll receptors, CD14, and macrophage activation and deactivation by LPS. Microbes Infect. 4 (2002), 903–914, 10.1016/S1286-4579(02)01613-1.
Zhou, J.M., Zhang, H.J., Wu, S.G., Qiu, K., Fu, Y., Qi, G.H., Wang, J., Supplemental xylooligosaccharide modulates intestinal mucosal barrier and cecal microbiota in laying hens fed oxidized fish oil. Front. Microbiol., 12, 2021, 635333, 10.3389/fmicb.2021.635333.
Gao, S., Khan, M.I., Kalsoom, F., Liu, Z., Chen, Y., Chen, Z., Role of gene regulation and inter species interaction as a key factor in gut microbiota adaptation. Arch. Microbiol., 204, 2022, 342, 10.1007/s00203-022-02935-5.
Gao, J., Xu, K., Liu, H., Liu, G., Bai, M., Peng, C., Li, T., Yin, Y., Impact of the gut microbiota on intestinal immunity mediated by tryptophan metabolism. Front. Cell. Infect. Microbiol., 8, 2018, 13, 10.3389/fcimb.2018.00013.
Amoroso, C., Perillo, F., Strati, F., Fantini, M.C., Caprioli, F., Facciotti, F., The role of gut microbiota biomodulators on mucosal immunity and intestinal inflammation. Cells, 9, 2020, 1234, 10.3390/cells9051234.
Jiao, Y., Wu, L., Huntington, N.D., Zhang, X., Crosstalk between gut microbiota and innate immunity and its implication in autoimmune diseases. Front. Immunol., 11, 2020, 282, 10.3389/fimmu.2020.00282.
Xiang, L., Si, C., Zhao, Z.T., Meng, Z., Yi, H., Ye, X.M., Qi, A., Ouyang, K.H., Wang, W.J., Effects of polysaccharides from yingshan yunwu tea on meat quality, immune status and intestinal microflora in chickens. Int. J. Biol. Macromol. 155 (2020), 61–70, 10.1016/j.ijbiomac.2020.03.198.
Sun, Y., Zhang, C., Zhang, P., Ai, C., Song, S., Digestion characteristics of polysaccharides from Gracilaria lemaneiformis and its interaction with the human gut microbiota. Int. J. Biol. Macromol. 213 (2022), 305–316, 10.1016/j.ijbiomac.2022.05.172.
Abbott, D.W., Martens, E.C., Gilbert, H.J., Cuskin, F., Lowe, E.C., Coevolution of yeast mannan digestion: convergence of the civilized human diet, distal gut microbiome, and host immunity. Gut Microbes 6 (2015), 334–339, 10.1080/19490976.2015.1091913.
Jayachandran, M., Chen, J., Chung, S.S.M., Xu, B., A critical review on the impacts of β-glucans on gut microbiota and human health. J. Nutr. Biochem. 61 (2018), 101–110, 10.1016/j.jnutbio.2018.06.010.
Zhu, Y., Wang, X., Zhang, C., Ni, J., Luo, Q., Teng, L., Liao, S., Yang, Y., Chen, H., Chen, Y., Characterizations of glucose-rich polysaccharides from Amomum longiligulare T.L. Wu fruits and their effects on immunogenicities of infectious bursal disease virus VP2 protein. Int. J. Biol. Macromol. 183 (2021), 1574–1584, 10.1016/j.ijbiomac.2021.05.138.
Li, H., Li, J., Shi, H., Li, C., Huang, W., Zhang, M., Luo, Y., Song, L., Yu, R., Zhu, J., Structural characterization and immunoregulatory activity of a novel acidic polysaccharide from Scapharca subcrenata. Int. J. Biol. Macromol. 210 (2022), 439–454, 10.1016/j.ijbiomac.2022.04.204.
Bo, R., Ji, X., Yang, H., Liu, M., Li, J., The characterization of optimal selenized garlic polysaccharides and its immune and antioxidant activity in chickens. Int. J. Biol. Macromol. 182 (2021), 136–143, 10.1016/j.ijbiomac.2021.03.197.
Wu, Q.J., Wang, Y.Q., Qi, Y.X., The protective effect of procyanidin against LPS-induced acute gut injury by the regulations of oxidative state. Springerplus, 5, 2016, 1645, 10.1186/s40064-016-3306-y.
Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25 (2001), 402–408, 10.1006/meth.2001.1262.
Guo, W., Gu, X., Tong, Y., Wang, X., Wu, J., Chang, C., Protective effects of mannan/beta-glucans from yeast cell wall on the deoxyniyalenol-induced oxidative stress and autophagy in IPEC-J2 cells. Int. J. Biol. Macromol. 135 (2019), 619–629, 10.1016/j.ijbiomac.2019.05.180.
Zhang, L., Ma, L., Pan, Y., Zheng, X., Sun, Q., Wang, Z., Wang, Q., Qiao, H., Effect of molecular weight on the antibacterial activity of polysaccharides produced by Chaetomium globosum CGMCC 6882. Int. J. Biol. Macromol. 188 (2021), 863–869, 10.1016/j.ijbiomac.2021.08.059.
Yalcin, S., Yalcin, S., Cakin, K., Eltan, O., Dagasan, L., Effects of dietary yeast autolysate (Saccharomyces cerevisiae) on performance, egg traits, egg cholesterol content, egg yolk fatty acid composition and humoral immune response of laying hens. J. Sci. Food Agric. 90 (2010), 1695–1701, 10.1002/jsfa.4004.
Koiyama, N.T.G., Utimi, N.B.P., Santos, B.R.L., Bonato, M.A., Barbalho, R., Gameiro, A.H., Araújo, C.S.S., Araújo, L.F., Effect of yeast cell wall supplementation in laying hen feed on economic viability, egg production, and egg quality. J. Appl. Poult. Res. 27 (2018), 116–123, 10.3382/japr/pfx052.
Furuse, M., Fujita, K., Hiiragi, T., Fujimoto, K., Tsukita, S., Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141 (1998), 1539–1550, 10.1083/jcb.141.7.1539.
Kariyawasam, S., Wilkie, B.N., Hunter, D.B., Gyles, C.L., Systemic and mucosal antibody responses to selected cell surface antigens of avian pathogenic Escherichia coli in experimentally infected chickens. Avian Dis. 46 (2002), 668–678, 10.1637/0005-2086(2002)046[0668:Samart]2.0.Co;2.
Sakaguchi, S., Mikami, N., Wing, J.B., Tanaka, A., Ichiyama, K., Ohkura, N., Regulatory T cells and human disease. Annu. Rev. Immunol. 38 (2020), 541–566, 10.1146/annurev-immunol-042718-041717.
Takahashi, K., Aoki, A., Takimoto, T., Akiba, Y., Dietary supplementation of glycine modulates inflammatory response indicators in broiler chickens. Br. J. Nutr. 100 (2008), 1019–1028, 10.1017/s0007114508966125.
Al-Sadi, R.M., Ma, T.Y., IL-1 causes an increase in intestinal epithelial tight junction permeability. J. Immunol. 178 (2007), 4641–4649, 10.4049/jimmunol.178.7.4641.
Al-Sadi, R., Boivin, M., Ma, T., Mechanism of cytokine modulation of epithelial tight junction barrier. Front. Biosci. 14 (2009), 2765–2778, 10.2741/3413.
Bedirli, A., Kerem, M., Pasaoglu, H., Akyurek, N., Tezcaner, T., Elbeg, S., Memis, L., Sakrak, O., Beta-glucan attenuates inflammatory cytokine release and prevents acute lung injury in an experimental model of sepsis. Shock 27 (2007), 397–401, 10.1097/01.shk.0000245030.24235.f1.
Weaver, A.C., See, M.T., Kim, S.W., Protective effect of two yeast based feed additives on pigs chronically exposed to deoxynivalenol and zearalenone. Toxins 6 (2014), 3336–3353, 10.3390/toxins6123336.
Collier, C.T., Carroll, J.A., Ballou, M.A., Starkey, J.D., Sparks, J.C., Oral administration of Saccharomyces cerevisiae boulardii reduces mortality associated with immune and cortisol responses to Escherichia coli endotoxin in pigs. J. Anim. Sci. 89 (2011), 52–58, 10.2527/jas.2010-2944.
Li, J., Xing, J., Li, D., Wang, X., Zhao, L., Lv, S., Huang, D., Effects of beta-glucan extracted from Saccharomyces cerevisiae on humoral and cellular immunity in weaned piglets. Arch. Anim. Nutr. 59 (2005), 303–312, 10.1080/17450390500247832.
Lehrer, R.I., Ganz, T., Antimicrobial peptides in mammalian and insect host defence. Curr. Opin. Immunol. 11 (1999), 23–27, 10.1016/s0952-7915(99)80005-3.
Abdelsalam, M., Isobe, N., Yoshimura, Y., Effects of lipopolysaccharide and interleukins on the expression of avian beta-defensins in hen ovarian follicular tissue. Poult. Sci. 91 (2012), 2877–2884, 10.3382/ps.2012-02312.
Wellens, A., Garofalo, C., Nguyen, H., Van Gerven, N., Slättegård, R., Hernalsteens, J.P., Wyns, L., Oscarson, S., De Greve, H., Hultgren, S., Bouckaert, J., Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One., 3, 2008, e2040, 10.1371/journal.pone.0002040.
Janczyk, P., Halle, B., Souffrant, W.B., Microbial community composition of the crop and ceca contents of laying hens fed diets supplemented with Chlorella vulgaris. Poult. Sci. 88 (2009), 2324–2332, 10.3382/ps.2009-00250.
Han, Z., Willer, T., Li, L., Pielsticker, C., Rychlik, I., Velge, P., Kaspers, B., Rautenschlein, S., Influence of the gut microbiota composition on Campylobacter jejuni colonization in chickens. Infect. Immun., 85, 2017, e00380-00317, 10.1128/IAI.00380-17.
Carvalho, F.A., Koren, O., Goodrich, J.K., Johansson, M.E., Nalbantoglu, I., Aitken, J.D., Su, Y., Chassaing, B., Walters, W.A., Gonzalez, A., Clemente, J.C., Cullender, T.C., Barnich, N., Darfeuille-Michaud, A., Vijay-Kumar, M., Knight, R., Ley, R.E., Gewirtz, A.T., Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe 12 (2012), 139–152, 10.1016/j.chom.2012.07.004.
Tian, X., Yu, Z., Feng, P., Ye, Z., Li, R., Liu, J., Hu, J., Kakade, A., Liu, P., Li, X., Lactobacillus plantarum TW1-1 alleviates diethylhexylphthalate-induced testicular damage in mice by modulating gut microbiota and decreasing inflammation. Front. Cell. Infect. Microbiol., 9, 2019, 221, 10.3389/fcimb.2019.00221.
Dowarah, R., Verma, A.K., Agarwal, N., The use of Lactobacillus as an alternative of antibiotic growth promoters in pigs: a review. Anim. Nutr. 3 (2017), 1–6, 10.1016/j.aninu.2016.11.002.
Ashida, H., Mimuro, H., Sasakawa, C., Shigella manipulates host immune responses by delivering effector proteins with specific roles. Front. Immunol., 6, 2015, 219, 10.3389/fimmu.2015.00219.
Robino, P., Ferrocino, I., Rossi, G., Dogliero, A., Alessandria, V., Grosso, L., Galosi, L., Tramuta, C., Cocolin, L., Nebbia, P., Changes in gut bacterial communities in canaries infected by Macrorhabdus ornithogaster. Avian Pathol. 48 (2019), 111–120, 10.1080/03079457.2018.1553294.
Xiang, L., Peng, L., Du, W., Hong, W., Wang, T.T., Protective effects of Bifidobacterium on intestinal barrier function in LPS-induced enterocyte barrier injury of Caco-2 monolayers and in a rat NEC model. PLoS One, 11, 2016, e0161635, 10.1371/journal.pone.0161635.
Dong, P., Yi, Y., Wang, W.P., The role of intestinal Bifidobacteria on immune system development in young rats. Early Hum. Dev. 86 (2010), 51–58, 10.1016/j.earlhumdev.2010.01.002.
Richards, P., Fothergill, J., Bernardeau, M., Wigley, P., Development of the caecal microbiota in three broiler breeds. Front. Vet. Sci., 6, 2019, 201, 10.3389/fvets.2019.00201.
Sue, P., Sahar, M., Sally, R., Graeme, T., Susan, T., Keith, S., Lang, S., David, H., Corynebacterium species isolated from patients with mastitis. Clin. Infect. Dis. 35 (2002), 1434–1440, 10.1086/344463.
Zhang, C.C., Hsu, H.J., Li, C.M., Brevundimonas vesicularis bacteremia resistant to trimethoprim-sulfamethoxazole and ceftazidime in a tertiary hospital in southern Taiwan. J. Microbiol. Immunol. Infect. 45 (2012), 448–452, 10.1016/j.jmii.2012.01.010.
Han, Q.Q., Fu, Y., Le, J.M., Pilot, A., Cheng, S., Chen, P.Q., Wu, H., Wan, G.Q., Gu, X.F., Electroacupuncture may alleviate behavioral defects via modulation of gut microbiota in a mouse model of Parkinson's disease. Acupunct. Med. 39 (2021), 501–511, 10.1177/0964528421990658.
Wang, J., Wan, C., Shuju, Z., Yang, Z., Celi, P., Ding, X., Bai, S., Zeng, Q., Mao, X., Xu, S., Zhang, K., Li, M., Differential analysis of gut microbiota and the effect of dietary Enterococcus faecium supplementation in broiler breeders with high or low laying performance. Poult. Sci. 100 (2021), 1109–1119, 10.1016/j.psj.2020.10.024.
Lee, K.W., Lillehoj, H.S., Jang, S.I., Li, G., Lee, S.H., Lillehoj, E.P., Siragusa, G.R., Effect of bacillus-based direct-fed microbials on Eimeria maxima infection in broiler chickens. Comp. Immunol. Microbiol. Infect. Dis. 33 (2010), e105–e110, 10.1016/j.cimid.2010.06.001.
Liu, S., Li, E., Sun, Z., Fu, D., Duan, G., Jiang, M., Yu, Y., Mei, L., Yang, P., Tang, Y., Zheng, P., Altered gut microbiota and short chain fatty acids in Chinese children with autism spectrum disorder. Sci. Rep., 9, 2019, 287, 10.1038/s41598-018-36430-z.