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Mannan rich fraction from yeast modulates inflammatory responses in intestinal cells (HT-29) exposed to Escherichia coli

Published online by Cambridge University Press:  18 June 2019

Niall Browne Open the ORCID record for Niall Browne [Opens in a new window] ,
Aimee Traynor  and
Karina A. Horgan
Niall Browne*
Affiliation:
Alltech Biotechnology Centre, Sarney, Summerhill road, Dunboyne, Co. Meath, Ireland.
Aimee Traynor
Affiliation:
Alltech Biotechnology Centre, Sarney, Summerhill road, Dunboyne, Co. Meath, Ireland.
Karina A. Horgan
Affiliation:
Alltech Biotechnology Centre, Sarney, Summerhill road, Dunboyne, Co. Meath, Ireland.
*
*Corresponding author: nbrowne@Alltech.com
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Abstract

Mannan from yeast has been demonstrated to limit infection in animals susceptible to gastrointestinal infection, including pigs, poultry and cows, by blocking the mechanism by which gram-negative bacteria adhere to and invade the intestines. Enterotoxigenic Escherichia coli (ETEC) cause post weaning diarrhoea (PWD) which results in poor weight gain and potential death at great economic cost to the farmer. A mannan rich fraction (MRF) was assessed in vitro for its impact on ETEC infection of HT-29 intestinal cell line. Gene expression markers for inflammation (TNFα and IL-1β) and TLR4 (TICAM-1 and LY96) associated recognition of bacteria were significantly elevated following exposure to E. coli alone, but not in combination with MRF compared to the control. HT-29 cells exposed to MRF alone demonstrated significantly reduced expression of immune signalling genes IRAK1, IRF7 and JUN when compared to the control. HT-29 cell protein abundance for TNFα and TLR4 associated proteins were significantly increased in response to E. coli exposure alone while no significant change was observed for MRF treatment with E. coli infection. E. coli adhesion to HT-29 cells was significantly decreased with addition of MRF compared to E. coli infection alone. The action of MRF demonstrated its potential capacity to limit infection on an in vitro level through blocking bacterial interaction with the intestines that leads to infection as marked by a reduction in proinflammatory responses. MRF on its own demonstrated potential anti-inflammatory effects on intestinal cells with the reduction of proinflammatory responses observed.

Keywords

Enterotoxigenic Escherichia coliHT-29Post weaning diarrheaMannan rich fractionInflammatory
Type
Original Research
Information
Journal of Applied Animal Nutrition , Volume 7 , 2019 , e5
Copyright
Copyright © Cambridge University Press and Journal of Applied Animal Nutrition Ltd. 2019 

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References

Al Naiemi, N., Heddema, E., Bart, A., de Jonge, E., Vandenbroucke-Grauls, C., Savelkoul, P. and Duim, B. (2006). Emergence of multidrug-resistant Gram-negative bacteria during selective decontamination of the digestive tract on an intensive care unit. J Antimicrob Chemother 58: 853–856.Google Scholar
Amezcua, R., Friendship, R. M., Dewey, C. E., Gyles, C. and Fairbrother, J. M. (2002). Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns. Can J Vet Res 66: 73–78.Google Scholar
Anadón, A., Martínez-Larrañaga, M. and Aranzazu Martínez, M. (2006). Probiotics for animal nutrition in the European Union. Regulation and safety assessment. Reg Toxicol Pharmacol 45(1): 91–95.Google Scholar
Betis, F., Brest, P., Hofman, V., Guignot, J., Kansau, I., Rossi, B., Servin, A. and Hofman, P. (2003). Afa/Dr diffusely adhering Escherichia coli infection in T84 cell monolayers induces increased neutrophil transepithelial migration, which in turn promotes cytokine-dependent upregulation of decay-accelerating factor (CD55), the receptor for Afa/Dr adhesins. Infect Immun 71: 1774–1783.Google Scholar
Biggs, P., Parsons, C. M. and Fahey, G. C. (2007). The effects of several oligosaccharides on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. Poult Sci 86(11):2327–2336.Google Scholar
Boisen, S. and Fernández, J. A. (1997). Prediction of the total tract digestibility of energy in feedstuffs and pig diets by in vitro analyses. Anim Feed Sci Tech 68(3): 277–286.Google Scholar
Brady, M. J., Radhakrishnan, P., Liu, H., Magoun, L., Murphy, K. C., Mukherjee, J., Donohue-Rolfe, A., Tzipori, S. and Leong, J. M. (2011). Enhanced Actin Pedestal Formation by Enterohemorrhagic Escherichia coli O157:H7 Adapted to the Mammalian Host. Front Microbiol 2: 226.Google Scholar
Brennan, K. M., Graugnard, D. E., Xiao, R., Spry, M. L., Pierce, J. L., Lumpkins, B. and Mathis, G. F. (2013). Comparison of gene expression profiles of the jejunum of broilers supplemented with a yeast cell wall-derived mannan oligosaccharide versus bacitractin methylene disalicylate. Br Poult Sci 54(2): 238–246.Google Scholar
Brosnahan, A. J. and Brown, D. R. (2012). Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations. Vet Microbiol 156 (3–4):229–37.Google Scholar
Burkey, T. E., Dritz, S. S., Nietfeld, J. C., Johnson, B. J. and Minton, J. E. (2004). Effect of dietary mannanoligosaccharide and sodium chlorate on the growth performance, acute-phase response, and bacterial shedding of weaned pigs challenged with Salmonella enterica serotype Typhimurium. J Anim Sci 82: 397–404.Google Scholar
Cane, G., Ginouves, A., Marchetti, S., Busca, R., Pouyssegur, J., Berra, E., Hofman, P. and Vouret-Craviari, V. (2010). HIF-1alpha mediates the induction of IL-8 and VEGF expression on infection with Afa/Dr diffusely adhering E. coli and promotes EMT-like behaviour. Cell Microbiol. 12: 640–653.Google Scholar
Castillo, M., Martin-Orue, S., Taylor-Pickard, J., Perez, J. and Gasa, J. (2008). Use of mannanoligosaccharides and zinc chelate as growth promoters and diarrhea preventative in weaning pigs: Effects on microbiota and gut function. J Anim Sci. 86: 94–101.Google Scholar
Cervantes, H. M. (2015). Antibiotic-free poultry production: Is it sustainable? J Appl Poult Res 24(1): 91–97.Google Scholar
Che, T. M., Song, M., Liu, Y., Johnson, R., Kelley, K., Van Alstine, W., Dawson, K. and Pettigrew, J. E. (2012). Mannan oligosaccharide increases serum concentrations of antibodies and inflammatory mediators in weanling pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J Anim Sci 90: 2784–2793.Google Scholar
Coffman, J. R., Augsburg, J., Beran, G. W., Colten, H. R., Greig, C., Halloran, J., Hayes, D., Kaneene, J. B., MacDonald, A., McNutt, K., Meeker, D. L., Nickerson, S. C. and Seay, T. (1999). Committee on Drug Use in Food Animals.Google Scholar
Cromwell, G. L. (2002). Why and how antibiotics are used in swine production. Anim Biotechnol 13: 7–27.Google Scholar
Duan, X. D., Chen, D. W., Zheng, P., Tian, G., Wang, J. P., Mao, X. B., Yu, J., He, J., Li, B., Huang, Z. Q., Ao, Z. G. and Yu, B. (2016). Effects of dietary mannan oligosaccharide supplementation on performance and immune response of sows and their offspring. Anim Feed Sci Tech 218: 17–25.Google Scholar
European-Commission (2005). Ban on antibiotics as growth promoters in animal feed enters into effect. EUROPAGoogle Scholar
Fairbrother, J. M., Nadeau, E. and Gyles, C. L. (2005). Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev 6: 17–39.Google Scholar
Fein, J. E. (1981). Screening of uropathogenic Escherichia coli for expression of mannose-selective adhesins: importance of culture conditions. J Clin Microbiol 13(6): 1088–1095.Google Scholar
Geens, M. M. and Niewold, T. A. (2011). Optimizing culture conditions of a porcine epithelial cell line IPEC-J2 through a histological and physiological characterization. Cytotech 63: 415–423.Google Scholar
Goutard, F.L., Bordier, M., Calba, C., Erlacher-Vindel, E., Góchez, D., de Balogh, K., Benigno, C., Kalpravidh, W., Roger, F. and Vong, S.. (2017) Antimicrobial policy interventions in food animal production in South East Asia. BMJ, 358, 36–41.Google Scholar
Guani-Guerra, E., Santos-Mendoza, T., Lugo-Reyes, S. O. and Teran, L. M. (2010). Antimicrobial peptides: general overview and clinical implications in human health and disease. Clin Immunol 135(1): 1–11.Google Scholar
Halas, V. and Nochta, I. (2012). Mannan Oligosaccharides in Nursery Pig Nutrition and Their Potential Mode of Action. Anim (Basel) 2: 261–274.Google Scholar
Hartmann, M., Papavlassopoulos, H., Chandrasekaran, V., Grabosch, C., Beiroth, F., Lindhorst, T. K. and Röhl, C. (2012). Inhibition of bacterial adhesion to live human cells: activity and cytotoxicity of synthetic mannosides. FEBS Lett 21(10): 1459–1465.Google Scholar
Hermes, R. G., Manzanilla, E. G., Martin Orue, S. M., Perez, J. and Klasing, K. C. (2011). Influence of dietary ingredients on in vitro inflammatory response of intestinal porcine epithelial cells challenged by an enterotoxigenic Escherichia coli (K88). Comp Immunol Microbiol Infect Dis 34(6): 479–488.Google Scholar
Hooge, D. M. (2004). Meta-analysis of broiler chicken pen trials evaluating dietary mannan oligosaccharide, 1993–2003. Int. J. Poult. Sci 3(3): 163–174.Google Scholar
Horgan, K., Madden, G. and Jacques, K. (2018). Yeast cell wall mannan rich fraction reduces the ability of Enterotoxigenic E. coli (ETEC) to attach to porcine intestinal cells in vitro. J Anim Sci. 96: 114.Google Scholar
Kennan, R. and Monckton, R. (1990). Adhesive Fimbriae Associated with Porcine Enterotoxigenic Escherichia coli of the 0141 Serotype. Amer Soc Microbiol. 28: 2006–2011.Google Scholar
Kuzmich, N. N., Sivak, K. V., Chubarev, V. N., Porozov, Y. B., Savateeva Lyubimova, T. N. and Peri, F. (2017). TLR4 Signaling Pathway Modulators as Potential Therapeutics in Inflammation and Sepsis. Vac 5(4), 34.Google Scholar
Leonard, B., Affolter, V. and Bevins, B. (2012). Antimicrobial peptides: agents of border protection for companion animals. Vet Dermatol 23(3): 177–e136.Google Scholar
Li, J. (2017). Current status and prospects for in-feed antibiotics in the different stages of pork production - A review. Asian-Australas J Anim Sci 30(12): 1667–1673.Google Scholar
Liu, P., Piao, X., Kim, S., Wang, L., Shen, Y., Lee, H. and Li, S. Y. (2008). Effects of chito-oligosaccharide supplementation on the growth performance, nutrient digestibility, intestinal morphology, and fecal shedding of Escherichia coli and Lactobacillus in weaning pigs. J Anim Sci 86: 2609–2618.Google Scholar
Luquetti, B. C., Furlan, R. L., Alarcon, M. F. F. and Macari, M. (2012). Saccharomyces Cerevisiae Cell Wall Dietary Supplementation on the Performance and Intestinal Mucosa Development and Integrity of Broiler Chickens Vaccinated Against Coccidiosis. Braz J Poultry Sci 14(2): 89–95.Google Scholar
Meunier, J. P., Manzanilla, E. G., Anguita, M., Denis, S., Pérez, J. F., Gasa, J., Cardot, J. M., Garcia, F., Moll, X. and Alric, M. (2008). Evaluation of a dynamic in vitro model to simulate the porcine ileal digestion of diets differing in carbohydrate composition1. J Anim Sci 86(5): 1156–1163.Google Scholar
Meurens, F., Summerfield, A., Nauwynck, H., Saif, L. and Gerdts, V. (2011). The pig: a model for human infect dis. Trends Microbiol 20: 50–57.Google Scholar
Miller, E. and Ullrey, D. E. (1987). The pig as a model for human nutrition. Annu Rev Nutr 7: 361–382.Google Scholar
Monira, S., Shabnam, S. A., Ali, S. I., Sadique, A., Johura, F.-T., Rahman, K. Z., Alam, N. H., Watanabe, H. and Alam, M. (2017). Multi-drug resistant pathogenic bacteria in the gut of young children in Bangladesh. Gut patho 9(1): 19.Google Scholar
Munyaka, P. M., E. H, , Yitbarek, A., Camelo Jaimes, G., Sharif, S., Guenter, W., House, J. D. and Rodriguez-Lecompte, J. C. (2012). Local and systemic innate immunity in broiler chickens supplemented with yeast-derived carbohydrates. Poult Sci 91: 2164–2172.Google Scholar
Nedrud, J. G. (1999). Animal models for gastric Helicobacter immunology and vaccine studies. FEMS Immunology & Med Microbiol 24(2): 243–250.Google Scholar
Ofek, I., Mirelman, D. and Sharon, N. (1977). Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature 265: 623–625.Google Scholar
Pang, X., Hua, X., Yang, Q., Ding, D., Che, C., Cui, L., Jia, W., Bucheli, P. and Zhao, L. (2017). Inter-species transplantation of gut microbiota from human to pigs. Vac (Basel) 5.Google Scholar
Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C., Jones, R., Nightingale, C., Preston, R. and Waddell, J. (2003). Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother 53(1): 28–52.Google Scholar
Rajaiah, R., Perkins, D. J., Ireland, D. D. C. and Vogel, S. N. (2015). CD14 dependence of TLR4 endocytosis and TRIF signaling displays ligand specificity and is dissociable in endotoxin tolerance. Proc Nati Acad Sci USA 112(27): 8391–8396.Google Scholar
Rhouma, M., Fairbrother, J. M., Beaudry, F. and Letellier, A. (2017). Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Veterinaria Scandinavica 59(1): 31.Google Scholar
Ricke, S. C. (2015). Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems. Poult Sci 94: 1411–1418.Google Scholar
Rosen, G. D. (2004). Optimizing the replacement of pronutrient antibiotics in poultry nutrition. Lexington, Kentucky, U.S.A., Proc. of Alltech's 20th Annual International Symposium 20: 93–101Google Scholar
Samuel, R. S. and Brennan, K. M. (2012). Effect of Actigen™ supplementation in gestation and lactation on sow and piglet performance, colostrum Ig level and milk composition. J Anim Sci. 90 391.Google Scholar
Sandegren, L. (2014). Selection of antibiotic resistance at very low antibiotic concentrations. Ups J Med Sci 119(2): 103–107.Google Scholar
Smith, D. L., Harris, A. D., Johnson, J. A., Silbergeld, E. K. and Morris, J. G. (2002). Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Nati Acad Sci USA 99(9): 6434–6439.Google Scholar
Slaughter, L. (2017) H.R.1587. Preservation of Antibiotics for Medical Treatment Act. Congress. 115.Google Scholar
Spring, P., Wenk, C., Connolly, A. and Kiers, A. (2015). A review of 733 published trials on Bio-Mos®, a mannan oligosaccharide, and Actigen®, a second generation mannose rich fraction, on farm and companion animals. J Appl Anim Nutri 3: e8.Google Scholar
Steele, J., Feng, H., Parry, N. and Tzipori, S. (2010). Piglet Models for Acute or Chronic Clostridium difficile Illness (CDI). J infect dis 201(3): 428–434.Google Scholar
Thacker, P. A. (2013). Alternatives to antibiotics as growth promoters for use in swine production: a review. J Anim Sci Biotechnol 4(1): 35.Google Scholar
Thornberry, N. A., Hg, B., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Aunins, J., Aunins and, J. et al. (1992). A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356: 768–774.Google Scholar
Verstegen, M. W. and Williams, B. A. (2002). Alternatives to the use of antibiotics as growth promoters for monogastric animals. Anim Biotechnol 13(1): 113–127.Google Scholar
Vitovec, J. and Koudela, B. (1992). Pathogenesis of intestinal cryptosporidiosis in conventional and gnotobiotic piglets. Vet Parasitol 43: 25–36.Google Scholar
Wang, H., Czura, C. J. and Tracey, K. J. (2003). CHAPTER 35 - Tumor necrosis factor A2 - Thomson, Angus W. Cytokine Handbook (Fourth Edition). Lotze, M. T.. London, Academic Press: 837–860.Google Scholar
White, L. A., Newman, M. C., Cromwell, G. L. and Lindemann, M. D. (2002). Brewers dried yeast as a source of mannan oligosaccharides for weanling pigs1,2. J Anim Sci 80(10): 2619–2628.Google Scholar
Wong Fok Lung, T., Pearson, J., Schuelein, R. and Hartland, E. L. (2014). The cell death response to enteropathogenic Escherichia coli infection. Cell Microbiol 16(12): 1736–1745.Google Scholar
Xiao, R., Power, R. F., Mallonee, D., Crowdus, C., Ao, T., Pierce, J. L. and Dawson, K. A. (2010). Transcriptional signatures associated with biological functions of Bio-Mos® and Actigen® in broilers. Atlanta, GA, USA, Proc IPSF 76.Google Scholar
Yuan, L., Ward, L., Rosen, B., To, T. and Saif, L. (1996). Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J. Virol 70(5): 5 3075–3083.Google Scholar
Zhang, Q., Widmer, G. and Tzipori, S. (2013). A pig model of the human gastrointestinal tract. Gut Microbe 4(3): 193–200.Google Scholar
Zhao, H., Li, C., Beck, B. H., Zhang, R., Thongda, W., Davis, D. A. and Peatman, E. (2015). Impact of feed additives on surface mucosal health and columnaris susceptibility in channel catfish fingerlings, Ictalurus punctatus. Fish Shellfish Immunol 46(2): 624–637.Google Scholar
Zhao, P., Jung, J. and Kim, I. (2012). Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. J Anim Sci 90(3): 2011–3921.Google Scholar