Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-15T23:25:27.516Z Has data issue: false hasContentIssue false
  • English
  • Français

Gut immunity: its development and reasons and opportunities for modulation in monogastric production animals

Published online by Cambridge University Press:  29 April 2018

Leon J. Broom  and
Michael H. Kogut
Leon J. Broom*
Affiliation:
Gut Health Consultancy, Exeter, Devon, UK Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
Michael H. Kogut
Affiliation:
Southern Plains Agricultural Research Center, USDA-ARS, College Station, TX 77845, USA
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The intestine performs the critical roles of nutrient acquisition, tolerance of innocuous and beneficial microorganisms, while retaining the ability to respond appropriately to undesirable microbes or microbial products and preventing their translocation to more sterile body compartments. Various components contribute to antimicrobial defenses in the intestine. The mucus layer(s), antimicrobial peptides and IgA provide the first line of defense, and seek to trap and facilitate the removal of invading microbes. If breached, invading microbes next encounter a single layer of epithelial cells and, below this, the lamina propria with its associated immune cells. The gut immune system has developmental stages, and studies from different species demonstrate that innate capability develops earlier than acquired. In addition, various factors may influence the developmental process; for example, the composition and activity of the gut microbiota, antimicrobials, maternally derived antibodies, host genetics, and various stressors (e.g. feed deprivation). Therefore, it is clear that particularly younger (meat-producing) animals are reliant on innate immune responses (as well as passive immunity) for a considerable period of their productive life, and thus focusing on modulating appropriate innate responses should be an intervention priority. The gut microbiota is probably the most influential factor for immune development and capability. Interventions (e.g. probiotics, prebiotics, antibodies, etc.) that appropriately modulate the composition or activity of the intestinal microbiota can play an important role in shaping the desired functionality of the innate (and acquired) response. In addition, innate immune mediators, such as toll-like receptor agonists, cytokines, etc., may provide more specific ways to suitably modulate the response. A better understanding of mucosal immunology, signaling pathways, and processes, etc., will provide even more precise methods in the future to boost innate immune capability and minimize any associated (e.g. nutrient) costs. This will provide the livestock industry with more effective options to promote robust and efficient productivity.

Keywords

immunityinnateintestinepoultryswine
Type
Review Article
Information
Animal Health Research Reviews , Volume 19 , Issue 1 , June 2018 , pp. 46 - 52
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Assmann, N and Finlay, DK (2016). Metabolic regulation of immune responses; therapeutic opportunities. Journal of Clinical Investigation 126: 2031–2039.Google Scholar
Bar-Shira, E and Friedman, A (2006). Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Developmental and Comparative Immunology 30: 930–941.Google Scholar
Bar-Shira, E, Sklan, D and Friedman, A (2003). Establishment of immune competence in the avian GALT during the immediate post-hatch period. Developmental and Comparative Immunology 27: 147–157.Google Scholar
Bar-Shira, E, Sklan, D and Friedman, A (2005). Impaired immune responses in broiler hatchling hindgut following delayed access to feed. Veterinary Immunology and Immunopathology 105: 33–45.Google Scholar
Broom, LJ (2017). The sub-inhibitory theory for antibiotic growth promoters. Poultry Science 96: 3104–3108.Google Scholar
Broom, LJ and Kogut, MH (2017). Inflammation: friend or foe for animal production? Poultry Science 96: pex314.Google Scholar
Carpenter, S and O'Neill, LAJ (2007). How important are toll-like receptors for antimicrobial responses? Cellular Microbiology 9: 1891–1901.Google Scholar
Castanon, JIR (2007). History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science 86: 2466–2471.Google Scholar
Gadde, U, Kim, WH, Oh, ST and Lillehoj, HS (2017). Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Animal Health Research Reviews 18: 26–45.Google Scholar
Garg, D, Nowis, D, Golab, J, Vandenabeele, P, Krysko, DV and Agostinis, P (2010). Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Bioenergetics 1805: 53–71.Google Scholar
Gupta, SK, Deb, R, Dey, S and Chellappa, MM (2014). Toll-like receptor-based adjuvants: enhancing the immune response to vaccines against infectious diseases of chicken. Expert Review of Vaccines 13: 909–925.Google Scholar
He, H, MacKinnon, KM, Genovese, KJ and Kogut, MH (2011). Cpg oligodeoxynucleotide and double-stranded RNA synergize to enhance nitric oxide production and mRNA expression of inducible nitric oxide synthase, pro-inflammatory cytokines and chemokines in chicken monocytes. Innate Immunity 17: 137–144.Google Scholar
Hodgins, DC, Kang, SY, deArriba, L, Parreño, V, Ward, LA, Yuan, L, To, T and Saif, LJ (1999). Effects of maternal antibodies on protection and development of antibody responses to human rotavirus in gnotobiotic pigs. Journal of Virology 73: 186–197.Google Scholar
Honda, K and Littman, DR (2012). The microbiome in infectious disease and inflammation. Annual Review of Immunology 30: 759–795.Google Scholar
Hooper, LV, Littman, DR and Macpherson, AJ (2012). Interactions between the microbiota and the immune system. Science 336: 1268–1273.Google Scholar
Inman, CF, Haverson, K, Konstantinov, SR, Jones, PH, Harris, C, Smidt, H, Miller, B, Bailey, M and Stokes, C (2010). Rearing environment affects development of the immune system in neonates. Clinical and Experimental Immunology 160: 431–439.Google Scholar
Janeway, CA and Medzhitov, R (2002). Innate immune recognition. Annual Reviews of Immunology 20: 197–216.Google Scholar
Kagnoff, MF (1993). Immunology of the intestinal tract. Gastroenterology 105: 1275–1280.Google Scholar
Karpala, AJ, Stewart, C, McKay, J, Lowenthal, JW and Bean, AG (2011). Characterization of chicken Mda5 activity: regulation of IFN- β in the absence of RIG-I functionality. The Journal of Immunology 186: 5397–5405.Google Scholar
Kawai, T and Akira, S (2009). The roles of TLRs, RLRs and NLRs in pathogen recognition. International Immunology 21: 317–337.Google Scholar
Keestra, AM, de Zoete, MR, Bouwman, LI, Vaezirad, MM and van Putten, JP (2013). Unique features of chicken toll-like receptors. Developmental and Comparative Immunology 41: 316–323.Google Scholar
Khoruts, A, Mondino, A, Pape, KA, Reiner, SL and Jenkins, MK (1998). A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL)-2-independent mechanism. Journal of Experimental Medicine 187: 225–236.Google Scholar
Kogut, MH (2000). Cytokines and prevention of infectious diseases in poultry: a review. Avian Pathology 29: 395–404.Google Scholar
Kogut, MH (2017). Issues and consequences of using nutrition to modulate the avian immune response. Journal of Applied Poultry Research 26: 605–612.Google Scholar
Kogut, MH, Yin, X, Yuan, J and Broom, LJ (2017). Gut health in poultry. CAB Reviews 12: 31.Google Scholar
Krysko, DV, Agostinis, P, Krysko, O, Garg, AD, Bachert, C, Lambrecht, BN and Vandenabeele, P (2011). Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends in Immunology 32: 157–164.Google Scholar
Lackey, DE and Olefsky, JM (2016). Regulation of metabolism by the innate immune system. Nature Reviews Endocrinology 12: 15–28.Google Scholar
Lammers, A, Wieland, WH, Kruijt, L, Jansma, A, Straetemans, T, Schots, A, den Hartog, G and Parmentier, HK (2010). Successive immunoglobulin and cytokine expression in the small intestine of juvenile chicken. Developmental and Comparative Immunology 34: 1254–1262.Google Scholar
Le Bourgot, C, Ferret-Bernard, S, Le Normand, L, Savary, G, Menendez-Aparicio, E, Blat, S, Appert-Bossard, E, Respondek, F and Le Huerou-Luron, I (2014). Maternal short-chain fructooligosaccharide supplementation influences intestinal immune system maturation in piglets. PLoS ONE 9: e107508.Google Scholar
Lee, MS and Kim, YJ (2007). Signalling pathways downstream of pattern-recognition receptors and their cross talk. Annual Review of Biochemistry 76: 447–480.Google Scholar
Lee, KW, Lillehoj, HS, Lee, SH, Jang, SI, Park, MS, Bautista, DA, Ritter, GD, Hong, YH, Siragusa, GR and Lillehoj, EP (2012). Effect of dietary antimicrobials on immune status in broiler chickens. Asian-Australasian Journal of Animal Science 25: 382–392.Google Scholar
Lian, L, Ciraci, C, Chang, G, Hu, J and Lamont, SJ (2012). NLRC5 knockdown in chicken macrophages alters response to LPS and poly (I:C) stimulation. BMC Veterinary Research 8: 23.Google Scholar
Madej, JP and Bednarczyk, M (2016). Effect of in ovo-delivered prebiotics and synbiotics on the morphology and specific immune cell composition in the gut-associated lymphoid tissue. Poultry Science 95: 19–29.Google Scholar
Magor, KE, Miranzo Navarro, D, Barber, MR, Petkau, K, Fleming-Canepa, X, Blyth, GA and Blaine, AH (2013). Defense genes missing from the flight division. Developmental and Comparative Immunology 41: 377–388.Google Scholar
Majidi-Mosleh, A, Sadeghi, AA, Mousavi, SN, Chamani, M and Zarei, A (2017). Ileal MUC2 gene expression and microbial population, but not growth performance and immune response, are influenced by in ovo injection of probiotics in broiler chickens. British Poultry Science 58: 40–45.Google Scholar
McGettrick, AF and O'Neill, LAJ (2013). How metabolism generates signals during innate immunity and inflammation. The Journal of Biological Chemistry 288: 22893–22898.Google Scholar
McLamb, BL, Gibson, AJ, Overman, EL, Stahl, C and Moeser, AJ (2013). Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease. PLoS ONE 8: e59838.Google Scholar
Niewold, TA (2007). The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poultry Science 86: 605–609.Google Scholar
Nurmi, E and Rantala, M (1973). New aspects of Salmonella infection in broiler production. Nature 241: 210–211.Google Scholar
Owusu-Asiedu, A, Nyachoti, CM and Marquardt, RR (2003). Response of early-weaned pigs to an enterotoxigenic Esherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid or antibiotic. Journal of Animal Science 81: 1790–1798.Google Scholar
Pender, CM, Kim, S, Potter, TD, Ritzi, MM, Young, M and Dalloul, RA (2017). In ovo supplementation of probiotics and its effects on performance and immune-related gene expression in broiler chicks. Poultry Science 96: 1052–1062.Google Scholar
Peng, ZX, Wang, AR, Xie, LQ, Song, WP, Wang, J, Yin, Z, Zhou, DS and Li, FQ (2016). Use of recombinant porcine beta-defensin 2 as a medicated feed additive for weaned piglets. Scientific Reports 6: 26790.Google Scholar
Pourabedin, M and Zhao, X (2015). Prebiotics and gut microbiota in chickens. FEMS Microbiology Letters 362: fnv122.Google Scholar
Quinteiro-Filho, WM, Rodrigues, MV, Ribeiro, A, Ferraz-de-Paula, V, Pinheiro, ML, Sa, LRM, Ferreira, AJP and Palermo-Neto, J (2012). Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation. Journal of Animal Science 90: 1986–1994.Google Scholar
Russler-Germain, EV, Rengarajan, S and Hsieh, CS (2017). Antigen-specific regulatory T-cell responses to intestinal microbiota. Mucosal Immunology 10: 1375–1386.Google Scholar
Sandell, MI, Tobler, M and Hasselquist, D (2009). Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula). The Journal of Experimental Biology 212: 815–822.Google Scholar
Schokker, D, Veninga, G, Vastenhouw, SA, Bossers, A, de Bree, FM, Kaal-Lansbergen, LMTE, Rebel, JMJ and Smits, MA (2015). Early life microbial colonization of the gut and intestinal development differ between genetically divergent broiler lines. BMC Genomics 16: 418.Google Scholar
St Paul, M, Brisbin, JT, Abdul-Careem, MF and Sharif, S (2013). Immunostimulatory properties of Toll-like receptor ligands in chickens. Veterinary Immunology and Immunopathology 152: 191–199.Google Scholar
Sterzl, J, Rejnek, J and Trávnícek, J (1966). Impermeability of pig placenta for antibodies. Folia Microbiologica 11: 7–10.Google Scholar
Stokes, CR (2017). The development and role of microbial host interactions in gut mucosal immune development. Journal of Animal Science and Biotechnology 8: 12.Google Scholar
Stokes, CR, Bailey, M, Haverson, K, Harris, C, Jones, P, Inman, C, Pie, S, Oswald, IP, Williamson, BA, Akkermans, ADL, Sowa, E, Rothkotter, HJ and Miller, BG (2004). Postnatal development of intestinal immune system in piglets: implications for the process of weaning. Animal Research 53: 325–334.Google Scholar
Swaggerty, CL, Pevzner, IY and Kogut, MH (2014). Selection for pro-inflammatory mediators yields chickens with increased resistance against Salmonella enterica serovar Enteritidis. Poultry Science 93: 535–544.Google Scholar
Swaggerty, CL, Pevzner, IY and Kogut, MH (2015). Selection for pro-inflammatory mediators produces chickens more resistant to Eimeria tenella. Poultry Science 94: 37–42.Google Scholar
Swaggerty, CL, McReynolds, JL, Byrd, JA, Pevzner, IY, Duke, SE, Genovese, KJ, He, H and Kogut, MH (2016). Selection for pro-inflammatory mediators produces chickens more resistant to Clostridium perfringens-induced necrotic enteritis. Poultry Science 95: 370–374.Google Scholar
Takeuchi, O and Akira, S (2010). Pattern recognition receptors and inflammation. Cell 140: 805–820.Google Scholar
Tannahill, GM, Curtis, AM, Adamik, J, Palsson-McDermott, EM, McGettrick, AF, Goel, G, Frezza, C, Bernard, NJ, Kelly, B, Foley, NH, Zheng, L, Gardet, A, Tong, Z, Jany, SS, Corr, SC, Haneklaus, M, Caffrey, BE, Pierce, K, Walmsley, S, Beasley, FC, Cummins, E, Nizet, V, Whyte, M, Taylor, CT, Lin, H, Masters, SL, Gottlieb, E, Kelly, VP, Clish, C, Auron, PE, Xavier, RJ, O'Neill, LA (2013). Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 496: 238–242.Google Scholar
Umar, S, Arif, M, Shah, MAA, Munir, MT, Yaqoob, M, Ahmed, S, Khan, MI, Younus, M and Shahzad, M (2015). Application of avian cytokines as immuno-modulating agents. Worlds Poultry Science Journal 71: 643–653.Google Scholar
Vega-Lopez, MA, Bailey, M, Telemo, E and Stokes, CR (1995). Effect of early weaning on the development of immune cells in the pig small-intestine. Veterinary Immunology and Immunopathology 44: 319–327.Google Scholar