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Pathophysiology of avian intestinal ion transport

  • M. NIGHOT (a1) and P. NIGHOT (a1)

The gut has great importance for the commercial success of poultry production. Numerous ion transporters, exchangers, and channels are present on both the apical and the basolateral membrane of intestinal epithelial cells, and their differential expression along the crypt-villus axis within the various intestinal segments ensures efficient intestinal absorption and effective barrier function. Recent studies have shown that intensive production systems, microbial exposure, and nutritional management significantly affect intestinal physiology and intestinal ion transport. Dysregulation of normal intestinal ion transport is manifested as diarrhoea, malabsorption, and intestinal inflammation resulting into poor production efficiency. This review discusses the basic mechanisms involved in avian intestinal ion transport and the impact of development during growth, nutritional and environmental alterations, and intestinal microbial infections on it. The effect of intestinal microbial infections on avian intestinal ion transport depends on factors such as host immunity, pathogen virulence, and the mucosal organisation of the particular intestinal segment.

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AL-BATSHAN, H.A., SCHEIDELER, S.E., BLACK, B.L., GARLICH, J.D. and ANDERSON, K.E. (1994) Duodenal calcium uptake, femur ash, and eggshell quality decline with age and increase following molt. Poultry Science 73: 1590-1596.
ASHRAF, S., ZANEB, H., YOUSAF, M.S., IJAZ, A., SOHAIL, M.U., MUTI, S., USMAN, M.M., IJAZ, S. and REHMAN, H. (2013) Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. Journal of Animal Physiology and Animal Nutrition 97 Suppl 1: 68-73.
AWAD, W.A., ASCHENBACH, J.R., KHAYAL, B., HESS, C. and HESS, M. (2012) Intestinal epithelial responses to salmonella enterica serovar enteritidis: Effects on intestinal permeability and ion transport. Poultry Science 91: 2949-2957.
AWAD, W.A., ASCHENBACH, J.R., SETYABUDI, F.M., RAZZAZI-FAZELI, E., BOHM, J. and ZENTEK, J. (2007) In vitro effects of deoxynivalenol on small intestinal d-glucose uptake and absorption of deoxynivalenol across the isolated jejunal epithelium of laying hens. Poultry Science 86: 15-20.
AWAD, W.A., BOHM, J., RAZZAZI-FAZELI, E., HULAN, H.W. and ZENTEK, J. (2004) Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poultry Science 83: 1964-1972.
AWAD, W.A., GHAREEB, K. and BOHM, J. (2010) Effect of addition of a probiotic micro-organism to broiler diet on intestinal mucosal architecture and electrophysiological parameters. Journal of Animal Physiology and Animal Nutrition 94: 486-494.
AWAD, W.A., HESS, C., KHAYAL, B., ASCHENBACH, J.R. and HESS, M. (2014) In vitro exposure to Escherichia coli decreases ion conductance in the jejunal epithelium of broiler chickens. PloS one 9: e92156.
AWAD, W.A., MOLNAR, A., ASCHENBACH, J.R., GHAREEB, K., KHAYAL, B., HESS, C., LIEBHART, D., DUBLECZ, K. and HESS, M. (2015) Campylobacter infection in chickens modulates the intestinal epithelial barrier function. Innate Immunity 21: 151-160.
AWAD, W.A., RAZZAZI-FAZELI, E., BOHM, J. and ZENTEK, J. (2008) Effects of b-trichothecenes on luminal glucose transport across the isolated jejunal epithelium of broiler chickens. Journal of Animal Physiology and Animal Nutrition 92: 225-230.
AWAD, W.A., REHMAN, H., BOHM, J., RAZZAZI-FAZELI, E. and ZENTEK, J. (2005) Effects of luminal deoxynivalenol and l-proline on electrophysiological parameters in the jejunums of laying hens. Poultry Science 84: 928-932.
BAI, S.P., WU, A.M., DING, X.M., LEI, Y., BAI, J., ZHANG, K.Y. and CHIO, J.S. (2013) Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poultry Science 92: 663-670.
BAXENDALE, W. and MEBATSION, T. (2004) The isolation and characterisation of astroviruses from chickens. Avian Pathology 33: 364-370.
BERRY, W. and BRAKE, J. (1991) Modulation of calbindin-d28k in avian egg shell gland and duodenum. Poultry Science 70: 655-657.
BERTELSEN, L.S., PAESOLD, G., ECKMANN, L. and BARRETT, K.E. (2003) Salmonella infection induces a hypersecretory phenotype in human intestinal xenografts by inducing cyclooxygenase 2. Infection and Immunity 71: 2102-2109.
BORGAN, M.A., MORI, Y., ITO, N., SUGIYAMA, M. and MINAMOTO, N. (2003) Antigenic analysis of nonstructural protein (nsp) 4 of group a avian rotavirus strain po-13. Microbiology and Immunology 47: 661-668.
CALONGE, M.L. and ILUNDAIN, A.A. (1998) Hco3(-)-dependent ion transport systems and intracellular ph regulation in colonocytes from the chick. Biochimica et Biophysica Acta 1371: 232-240.
CAO, G.T., ZENG, X.F., CHEN, A.G., ZHOU, L., ZHANG, L., XIAO, Y.P. and YANG, C.M. (2013) Effects of a probiotic, enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with escherichia coli k88. Poultry Science 92: 2949-2955.
CHANG, E.B., MUSCH, M.W. and MAYER, L. (1990) Interleukins 1 and 3 stimulate anion secretion in chicken intestine. Gastroenterology 98: 1518-1524.
CHEN, C.L., SANGIAH, S., CHEN, H., RODER, J.D. and SHEN, Y. (1994) Effects of heat stress on na+,k(+)-atpase, mg(2+)-activated atpase, and na(+)-atpase activities of broiler chickens vital organs. Journal of Toxicology and Environmental Health 41: 345-356.
CHOU, S.H., CHUNG, T.K. and YU, B. (2009) Effects of supplemental 25-hydroxycholecalciferol on growth performance, small intestinal morphology, and immune response of broiler chickens. Poultry Science 88: 2333-2341.
CIRAK, V.Y., KOWALIK, S., BURGER, H.J., ZAHNER, H. and CLAUSS, W. (2004) Effects of eimeria separata infections on na+ and cl- transport in the rat large intestine. Parasitology Research 92: 490-495.
CLARKE, L.L. (2009) A guide to ussing chamber studies of mouse intestine. American Journal of Physiology-Gastrointestinal and Liver Physiology 296: G1151-G1166.
DAY, J.M., SPACKMAN, E. and PANTIN-JACKWOOD, M. (2007) A multiplex rt-pcr test for the differential identification of turkey astrovirus type 1, turkey astrovirus type 2, chicken astrovirus, avian nephritis virus, and avian rotavirus. Avian Diseases 51: 681-684.
DE LA HORRA, M.C., CALONGE, M.L. and ILUNDAIN, A.A. (1998) Effect of dehydration on apical na+-h+ exchange activity and na+-dependent sugar transport in brush-border membrane vesicles isolated from chick intestine. Pflugers Archiv: European Journal of Physiology 436: 112-116.
DE LA HORRA, M.C., CANO, M., PERAL, M.J., CALONGE, M.L. and ILUNDAIN, A.A. (2001) Hormonal regulation of chicken intestinal nhe and sglt-1 activities. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 280: R655-660.
DONOWITZ, M., DE LA HORRA, C., CALONGE, M.L., WOOD, I.S., DYER, J., GRIBBLE, S.M., DE MEDINA, F.S., TSE, C.M., SHIRAZI-BEECHEY, S.P. and ILUNDAIN, A.A. (1998) In birds, nhe2 is major brush-border na+/h+ exchanger in colon and is increased by a low-nacl diet. The American Journal of Physiology 274: R1659-1669.
ECKMANN, L., RUDOLF, M.T., PTASZNIK, A., SCHULTZ, C., JIANG, T., WOLFSON, N., TSIEN, R., FIERER, J., SHEARS, S.B., KAGNOFF, M.F. and TRAYNOR-KAPLAN, A.E. (1997) D-myo-inositol 1,4,5,6-tetrakisphosphate produced in human intestinal epithelial cells in response to salmonella invasion inhibits phosphoinositide 3-kinase signaling pathways. Proceedings of the National Academy of Sciences of the United States of America 94: 14456-14460.
ELBROND, V.S., JONES, C.J. and SKADHAUGE, E. (2004) Localisation, morphology and function of the mitochondria-rich cells in relation to transepithelial na(+)-transport in chicken lower intestine (coprodeum). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 137: 683-696.
FIELD, M. (2003) Intestinal ion transport and the pathophysiology of diarrhea. The Journal of Clinical Investigation 111: 931-943.
GAL-GARBER, O., MABJEESH, S.J., SKLAN, D. and UNI, Z. (2003) Nutrient transport in the small intestine: Na+,k+-atpase expression and activity in the small intestine of the chicken as influenced by dietary sodium. Poultry Science 82: 1127-1133.
GARRIGA, C., HUNTER, R.R., AMAT, C., PLANAS, J.M., MITCHELL, M.A. and MORETO, M. (2006) Heat stress increases apical glucose transport in the chicken jejunum. American Journal of Physiology.Regulatory, Integrative and Comparative Physiology 290: R195-201.
GILBERT, E.R., LI, H., EMMERSON, D.A., WEBB, K.E. (Jr) and WONG, E.A. (2010) Dietary protein composition influences abundance of peptide and amino acid transporter messenger ribonucleic acid in the small intestine of 2 lines of broiler chicks. Poultry Science 89: 1663-1676.
GLASS, R.I., NOEL, J., MITCHELL, D., HERRMANN, J.E., BLACKLOW, N.R., PICKERING, L.K., DENNEHY, P., RUIZ-PALACIOS, G., DE GUERRERO, M.L. and MONROE, S.S. (1996) The changing epidemiology of astrovirus-associated gastroenteritis: A review. Archives of Virology. Supplementum 12: 287-300.
GROHMANN, G.S., GLASS, R.I., PEREIRA, H.G., MONROE, S.S., HIGHTOWER, A.W., WEBER, R. and BRYAN, R.T. (1993) Enteric viruses and diarrhea in hiv-infected patients. Enteric opportunistic infections working group. The New England Journal of Medicine 329: 14-20.
GRUBB, B.R. (1991a) Avian cecum: Role of glucose and volatile fatty acids in transepithelial ion transport. The American Journal of Physiology 260: G703-710.
GRUBB, B.R. (1991b) Ion transport across the chick ileum: A good model for transport studies. Comparative Biochemistry and Physiology. A, Comparative Physiology 100: 753-757.
HAYASHI, H., SZASZI, K., COADY-OSBERG, N., FURUYA, W., BRETSCHER, A.P., ORLOWSKI, J. and GRINSTEIN, S. (2004) Inhibition and redistribution of nhe3, the apical na+/h+ exchanger, by clostridium difficile toxin b. The Journal of General Physiology 123: 491-504.
HODGES, K. and GILL, R. (2010) Infectious diarrhea: Cellular and molecular mechanisms. Gut Microbes 1: 4-21.
HOQUE, K.M., RAJENDRAN, V.M. and BINDER, H.J. (2005) Zinc inhibits camp-stimulated cl secretion via basolateral k-channel blockade in rat ileum. American Journal of Physiology. Gastrointestinal and Liver Physiology 288: G956-963.
HOWE, K., GAULDIE, J. and MCKAY, D.M. (2002) Tgf-beta effects on epithelial ion transport and barrier: Reduced cl- secretion blocked by a p38 mapk inhibitor. American Journal of Physiology. Cell Physiology 283: C1667-1674.
HU, X.F., GUO, Y.M., HUANG, B.Y., BUN, S., ZHANG, L.B., LI, J.H., LIU, D., LONG, F.Y., YANG, X. and JIAO, P. (2010) The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poultry Science 89: 1967-1974.
KAPEL, N., HUNEAU, J.F., MAGNE, D., TOME, D. and GOBERT, J.G. (1997) Cryptosporidiosis-induced impairment of ion transport and na+-glucose absorption in adult immunocompromised mice. The Journal of Infectious Diseases 176: 834-837.
KOCI, M.D., MOSER, L.A., KELLEY, L.A., LARSEN, D., BROWN, C.C. and SCHULTZ-CHERRY, S. (2003) Astrovirus induces diarrhea in the absence of inflammation and cell death. Journal of Virology 77: 11798-11808.
KURAZONO, H., HOSOKAWA, M., MATSUDA, H. and SAKAGUCHI, G. (1987) Fluid accumulation in the ligated intestinal loop and histopathological changes of the intestinal mucosa caused by clostridium botulinum c2 toxin in the pheasant and chicken. Research in Veterinary Science 42: 349-353.
LARMONIER, C.B., LAUBITZ, D., HILL, F.M., SHEHAB, K.W., LIPINSKI, L., MIDURA-KIELA, M.T., MCFADDEN, R.M., RAMALINGAM, R., HASSAN, K.A., GOLEBIEWSKI, M., BESSELSEN, D.G., GHISHAN, F.K. and KIELA, P.R. (2013) Reduced colonic microbial diversity is associated with colitis in nhe3-deficient mice. American Journal of Physiology. Gastrointestinal and Liver Physiology 305: G667-677.
LAVERTY, G., ANTTILA, A., CARTY, J., REDDY, V., YUM, J. and ARNASON, S.S. (2012) Cftr mediated chloride secretion in the avian renal proximal tubule. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 161: 53-60.
LAVERTY, G., BJARNADOTTIR, S., ELBROND, V.S. and ARNASON, S.S. (2001) Aldosterone suppresses expression of an avian colonic sodium-glucose cotransporter. American Journal of Physiology.Regulatory, Integrative and Comparative Physiology 281: R1041-1050.
LAVERTY, G., ELBROND, V.S., ARNASON, S.S. and SKADHAUGE, E. (2006) Endocrine regulation of ion transport in the avian lower intestine. General and Comparative Endocrinology 147: 70-77.
LEESON, S., NAMKUNG, H., ANTONGIOVANNI, M. and LEE, E.H. (2005) Effect of butyric acid on the performance and carcass yield of broiler chickens. Poultry Science 84: 1418-1422.
LEI, K., LI, Y.L., YU, D.Y., RAJPUT, I.R. and LI, W.F. (2013) Influence of dietary inclusion of bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poultry Science 92: 2389-2395.
LILLEHOJ, H.S. and LEE, K.W. (2012) Immune modulation of innate immunity as alternatives-to-antibiotics strategies to mitigate the use of drugs in poultry production. Poultry Science 91: 1286-1291.
LIU, N., RU, Y.J., LI, F.D. and COWIESON, A.J. (2008) Journal of Animal Science 86: 3432-3439.
LLOYD, S., IRVINE, K.L., EVES, S.M. and GIBSON, J.S. (2005) Fluid absorption in the small intestine of healthy game birds and those infected with spironucleus spp. Avian Pathology 34: 252-257.
MA, T., THIAGARAJAH, J.R., YANG, H., SONAWANE, N.D., FOLLI, C., GALIETTA, L.J. and VERKMAN, A.S. (2002) Thiazolidinone cftr inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. The Journal of Clinical Investigation 110: 1651-1658.
MCNULTY, M.S., ALLAN, G.M. and STUART, J.C. (1978) Rotavirus infection in avian species. The Veterinary Record 103: 319-320.
MITCHELL, M.A. and CARLISLE, A.J. (1992) The effects of chronic exposure to elevated environmental temperature on intestinal morphology and nutrient absorption in the domestic fowl (gallus domesticus). Comparative Biochemistry and Physiology. A, Comparative Physiology 101: 137-142.
MORI, Y., BORGAN, M.A., ITO, N., SUGIYAMA, M. and MINAMOTO, N. (2002) Diarrhea-inducing activity of avian rotavirus nsp4 glycoproteins, which differ greatly from mammalian rotavirus nsp4 glycoproteins in deduced amino acid sequence in suckling mice. Journal of Virology 76: 5829-5834.
NAKPHAICHIT, M., THANOMWONGWATTANA, S., PHRAEPHAISARN, C., SAKAMOTO, N., KEAWSOMPONG, S., NAKAYAMA, J. and NITISINPRASERT, S. (2011) The effect of including lactobacillus reuteri kub-ac5 during post-hatch feeding on the growth and ileum microbiota of broiler chickens. Poultry Science 90: 2753-2765.
NASRIN, M., SIDDIQI, M., MASUM, M. and WARES, M. (2012) Gross and histological studies of digestive tract of broilers during postnatal growth and development. Journal of the Bangladesh Agricultural University 10: 69-77.
NIGHOT, P.K., MOESER, A., ALI, R.A., BLIKSLAGER, A.T. and KOCI, M.D. (2010) Astrovirus infection induces sodium malabsorption and redistributes sodium hydrogen exchanger expression. Virology 401: 146-154.
NILE, C.J., TOWNES, C.L., MICHAILIDIS, G., HIRST, B.H. and HALL, J. (2004) Identification of chicken lysozyme g2 and its expression in the intestine. Cellular and Molecular Life Sciences: CMLS 61: 2760-2766.
NORKINA, O., BURNETT, T.G. and DE LISLE, R.C. (2004) Bacterial overgrowth in the cystic fibrosis transmembrane conductance regulator null mouse small intestine. Infection and Immunity 72: 6040-6049.
NORRIS, F.A., WILSON, M.P., WALLIS, T.S., GALYOV, E.E. and MAJERUS, P.W. (1998) Sopb, a protein required for virulence of salmonella dublin, is an inositol phosphate phosphatase. Proceedings of the National Academy of Sciences of the United States of America 95: 14057-14059.
PANDA, A.K., RAMA RAO, S.V., RAJU, M.V. and SHYAM SUNDER, G. (2009) Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Sciences 22: 1026.
PANTIN-JACKWOOD, M.J., SPACKMAN, E., DAY, J.M. and RIVES, D. (2007) Periodic monitoring of commercial turkeys for enteric viruses indicates continuous presence of astrovirus and rotavirus on the farms. Avian Diseases 51: 674-680.
PATTERSON, J.A. and BURKHOLDER, K.M. (2003) Application of prebiotics and probiotics in poultry production. Poultry Science 82: 627-631.
PODOLSKY, D.K. (1997) Healing the epithelium: Solving the problem from two sides. Journal of Gastroenterology 32: 122-126.
REHMAN, H., AWAD, W.A., LINDNER, I., HESS, M. and ZENTEK, J. (2006) Clostridium perfringens alpha toxin affects electrophysiological properties of isolated jejunal mucosa of laying hens. Poultry Science 85: 1298-1302.
REYNOLDS, D.L. and SAIF, Y.M. (1986) Astrovirus: A cause of an enteric disease in turkey poults. Avian Diseases 30: 728-735.
REYNOLDS, D.L., SAIF, Y.M. and THEIL, K.W. (1987) Enteric viral infections of turkey poults: Incidence of infection. Avian Diseases 31: 272-276.
SANDLE, G.I. (2011) Infective and inflammatory diarrhoea: Mechanisms and opportunities for novel therapies. Current Opinion in Pharmacology 11: 634-639.
SINGH, U., VAN ITALLIE, C.M., MITIC, L.L., ANDERSON, J.M. and MCCLANE, B.A. (2000) Caco-2 cells treated with clostridium perfringens enterotoxin form multiple large complex species, one of which contains the tight junction protein occludin. The Journal of Biological Chemistry 275: 18407-18417.
SODRING ELBROND, V., DANTZER, V., MAYHEW, T.M. and SKADHAUGE, E. (1991) Avian lower intestine adapts to dietary salt (nacl) depletion by increasing transepithelial sodium transport and microvillous membrane surface area. Experimental Physiology 76: 733-744.
SONAWANE, N.D., ZHAO, D., ZEGARRA-MORAN, O., GALIETTA, L.J. and VERKMAN, A.S. (2007) Lectin conjugates as potent, nonabsorbable cftr inhibitors for reducing intestinal fluid secretion in cholera. Gastroenterology 132: 1234-1244.
SONODA, N., FURUSE, M., SASAKI, H., YONEMURA, S., KATAHIRA, J., HORIGUCHI, Y. and TSUKITA, S. (1999) Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier. The Journal of Cell Biology 147: 195-204.
SUN, X., ZHANG, H., SHEIKHAHMADI, A., WANG, Y., JIAO, H., LIN, H. and SONG, Z. (2015) Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (gallus gallus domesticus). International Journal of Biometeorology 59: 127-135.
THOUVENELLE, M.L., HAYNES, J.S., SELL, J.L. and REYNOLDS, D.L. (1995) Astrovirus infection in hatchling turkeys: Alterations in intestinal maltase activity. Avian Diseases 39: 343-348.
UNI, Z., GEYRA, A., BEN-HUR, H. and SKLAN, D. (2000) Small intestinal development in the young chick: Crypt formation and enterocyte proliferation and migration. British Poultry Science 41: 544-551.
UNI, Z., TAKO, E., GAL-GARBER, O. and SKLAN, D. (2003) Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo. Poultry Science 82: 1747-1754.
WALLIS, T.S. and GALYOV, E.E. (2000) Molecular basis of salmonella-induced enteritis. Molecular Microbiology 36: 997-1005.
WANG, L., LI, J., LI, J. (Jr), LI, R.X., LV, C.F., LI, S., MI, Y.L. and ZHANG, C.Q. (2016) Identification of the paneth cells in chicken small intestine. Poultry Science 95: 1631-1635.
YAN, F., ANGEL, R. and ASHWELL, C.M. (2007) Characterisation of the chicken small intestine type iib sodium phosphate cotransporter. Poultry Science 86: 67-76.
YIN, Y., LEI, F., ZHU, L., LI, S., WU, Z., ZHANG, R., GAO, G.F., ZHU, B. and WANG, X. (2010) Exposure of different bacterial inocula to newborn chicken affects gut microbiota development and ileum gene expression. The International Society for Microbial Ecology Journal 4: 367-376.
YUNUS, A.W., AWAD, W.A., KROGER, S., ZENTEK, J. and BOHM, J. (2010) In vitro aflatoxin b(1) exposure decreases response to carbamylcholine in the jejunal epithelium of broilers. Poultry Science 89: 1372-1378.
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