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Iodine supplementation of the pregnant dam alters intestinal gene expression and immunoglobulin uptake in the newborn lamb

Published online by Cambridge University Press:  20 November 2015

F. M. McGovern
Affiliation:
UCD, School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
D. A. Magee
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
J. A. Browne
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
D. E. MacHugh
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland
T. M. Boland*
Affiliation:
UCD, School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
*
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Abstract

Excess iodine intake by the pregnant dam reduces lamb serum antibody concentration, specifically immunoglobulin G (IgG). An experiment was conducted to investigate the mechanisms under pinning the reduced serum IgG concentration at 24 h postpartum in the progeny of iodine supplemented dams. Forty-five mature twin bearing ewes (n=15/treatment) were allocated to one of three dietary treatments as follows: basal diet (Control); basal diet plus 26.6 mg of iodine per ewe per day as calcium iodate (CaIO3); or potassium iodide (KI). Ewes were individually housed and fed from d 119 of gestation until parturition. All lambs received colostrum at 1, 10 and 18 h postpartum via stomach tube. At 1 h postpartum lambs from the control and an iodine supplemented treatment (n=10 per treatment from control and CaIO3) were euthanised before colostrum consumption and ileal segments isolated to determine the gene expression profile of a panel of genes identified as having a role in antibody transfer. Preceding euthanasia, lambs were blood sampled for determination of serum IgG, total thyroxine and free tri-iodothyronine concentrations. Progeny of CaIO3 supplemented dams had lower tri-iodothyronine concentrations (P<0.01) at 1 h postpartum and lower serum IgG concentrations (P<0.001) at 24 h postpartum when compared with the progeny of control dams. Iodine (CaIO3) supplementation of the dam increased the relative expression (P<0.05) of the B2M, PIGR and MYC genes in the ileum of the lamb, before colostrum consumption; while the expression of THRB declined when compared with the progeny of C dams (P<0.01). In conclusion, the results of this study show that it is the actual inclusion of excess iodine in the diet of the ewe, regardless of the carrier element, that negatively affects passive transfer in the newborn lamb. This study presents novel data describing the relationship between maternal iodine nutrition and its effect on the thyroid hormone status and subsequent gene expression in the newborn lamb; which results in a failure of passive transfer and a decline in serum IgG concentration.

Type
Research Article
Copyright
© The Animal Consortium 2015 

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References

Agricultural and Food Research Council (AFRC) 1993. Energy and protein requirements of ruminants. An advisory manual prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Oxford, UK.Google Scholar
Barry, T, Duncan, S, Sadler, W, Millar, K and Sheppard, A 1983. Iodine metabolism and thyroid hormone relationships in growing sheep fed on kale (Brassica oleracea) and ryegrass (Lolium perenne)–clover (Trifolium repens) fresh-forage diets. British Journal of Nutrition 49, 241253.Google Scholar
Baumrucker, CR and Bruckmaier, RM 2014. Colostrogenesis: IgG1 transcytosis mechanisms. Journal of Mammary Gland Biology and Neoplasia 19, 103117.Google Scholar
Boland, TM, Brophy, PO, Callan, JJ, Quinn, PJ, Nowakowski, P and Crosby, TF 2004. Effects of mineral-block components when offered to ewes in late pregnancy on colostrum yield and immunoglobulin G absorption in their lambs. Animal Science 79, 293302.CrossRefGoogle Scholar
Boland, TM, Guinan, M, Brophy, PO, Callan, JJ, Quinn, PJ, Nowakowski, P and Crosby, TF 2005a. The effect of varying levels of mineral and iodine supplementation to ewes during late pregnancy on serum immunoglobulin G concentrations in their progeny. Animal Science 80, 209218.Google Scholar
Boland, TM, Keane, N, Nowakowski, P, Brophy, PO and Crosby, TF 2005b. High mineral and vitamin E intake by pregnant ewes lowers colostral immunoglobulin G absorption by the lamb. Journal of Animal Science 83, 871878.Google Scholar
Boland, TM, Brophy, PO, Callan, JJ, Quinn, PJ, Nowakowski, P and Crosby, TF 2005c. The effects of mineral supplementation to ewes in late pregnancy on colostrum yield and immunoglobulin G absorption in their lambs. Livestock Production Science 97, 141150.Google Scholar
Boland, TM, Callan, JJ, Brophy, PO, Quinn, PJ and Crosby, TF 2006. Lamb serum vitamin E and immunoglobulin G concentrations in response to various maternal mineral and iodine supplementation regimens. Animal Science 82, 319325.Google Scholar
Boland, TM, Hayes, L, Sweeney, T, Callan, JJ, Baird, AW, Keely, S and Crosby, TF 2008. The effects of cobalt and iodine supplementation of the pregnant ewe diet on immunoglobulin G, vitamin E, T3 and T4 levels in the progeny. Animal 2, 197206.Google Scholar
Brambell, FWR 1970. The transmission of passive immunity from mother to young. In The transmission of passive immunity from mother to young (ed. A Neuberger and EL Tatum), pp. 20–41. North Holland Publishing Co, Amsterdam, The Netherlands.Google Scholar
Bruno, ME, West, RB, Schneeman, TA, Bresnick, EH and Kaetzel, CS 2004. Upstream stimulatory factor but not c-Myc enhances transcription of the human polymeric immunoglobulin receptor gene. Molecular Immunology 40, 695708.Google Scholar
Cabello, G and Levieux, D 1982. Absorption and half-life of bovine, caprine and ovine IgG1 in the newborn lamb. Effect of experimental prematurity and endocrine factors. Annales de Recherches Vé té rinaires 12, 421429.Google Scholar
Camacho, LE, Meyer, AM, Neville, TL, Hammer, CJ, Redmer, DA, Reynolds, LP, Caton, JS and Vonnahme, KA 2012. Neonatal hormone changes and growth in lambs born to dams receiving differing nutritional intakes and selenium supplementation during gestation. Reproduction 144, 2335.Google Scholar
Cervenak, J and Kacskovics, I 2009. The neonatal Fc receptor plays a crucial role in the metabolism of IgG in livestock animals. Veterinary Immunology and Immunopathology 128, 171177.Google Scholar
Choksi, NY, Jahnke, GD, St Hilaire, C and Shelby, M 2003. Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Research Part B: Developmental and Reproductive Toxicology 68, 479491.CrossRefGoogle ScholarPubMed
Crosby, TF, Boland, TM, Brophy, PO, Quinn, PJ, Callan, JJ and Joyce, D 2004. Effects of offering mineral blocks to ewes pre-mating and in late pregnancy on block intake, pregnant ewe performance and immunoglobulin status of the progeny. Animal Science 79, 493504.CrossRefGoogle Scholar
Doney, J, Peart, J, Smith, W and Louda, F 1979. A consideration of the techniques for estimation of milk yield by suckled sheep and a comparison of estimates obtained by two methods in relation to the effect of breed, level of production and stage of lactation. Journal Agricultural Science 92, 123132.Google Scholar
European Communities (Amendment of Cruelty to Animals Act 1876) Regulations, 2002. Retrieved November 20, 2011, from http://www.irishstatutebook.ie/eli/2003/si/30/made/en/print Google Scholar
Forhead, AJ and Fowden, AL 2014. Thyroid hormones in fetal growth and prepartum maturation. Journal of Endocrinology 221, R87R103.CrossRefGoogle ScholarPubMed
Fowden, AL, Li, J and Forhead, AJ 1998. Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proceedings of the Nutrition Society 57, 113122.CrossRefGoogle ScholarPubMed
Gauthier, K, Chassande, O, Plateroti, M, Roux, JP, Legrand, C, Pain, B, Rousset, B, Weiss, R, Trouillas, J and Samarut, J 1999. Different functions for the thyroid hormone receptors TRα and TRβ in the control of thyroid hormone production and post‐natal development. The EMBO Journal 18, 623631.Google Scholar
Gilbert, R, Gaskins, C, Hillers, J, Parker, C and McGuire, T 1988. Genetic and environmental factors affecting immunoglobulin G1 concentrations in ewe colostrum and lamb serum. Journal of Animal Science 66, 855863.Google Scholar
Johansen, FE, Pekna, M, Norderhaug, IN, Haneberg, B, Hietala, MA, Krajci, P, Betsholtz, C and Brandtzaeg, P 1999. Absence of epithelial immunoglobulin a transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component–deficient mice. The Journal of Experimental Medicine 190, 915922.Google Scholar
Jones, EA and Waldmann, TA 1972. The mechanism of intestinal uptake and transcellular transport of IgG in the neonatal rat. Journal of Clinical Investigation 51, 2916.Google Scholar
Laegreid, WW, Heaton, MP, Keen, JE, Grosse, WM, Chitko-McKown, CG, Smith, TPL, Keele, JW, Bennett, GL and Besser, TE 2002. Association of bovine neonatal Fc receptor a-chain gene (FCGRT) haplotypes with serum IgG concentration in newborn calves. Mammalian Genome 13, 704710.Google Scholar
Larson, RE, Ward, A, Frederiksen, K, Ardrey, W and Frank, F 1974. Capability of lambs to absorb immunoproteins from freeze-dried bovine colostrum. American Journal of Veterinary Research 35, 10611063.Google Scholar
Mayer, B, Zolnai, A, Frenyo, LV, Jancsik, V, Szentirmay, Z, Hammarstrom, L and Kacskovics, I 2002. Redistribution of the sheep neonatal Fc receptor in the mammary gland around the time of parturition in ewes and its localization in the small intestine of neonatal lambs. Immunology 107, 288296.Google Scholar
McEwan, A, Fisher, E and Selman, I 1970. Observations on the immune globulin levels of neonatal calves and their relationship to disease. Journal of Comparative Pathology 80, 259265.Google Scholar
O’Doherty, J and Crosby, T 1997. The effect of diet in late pregnancy on colostrum production and immunoglobulin absorption in sheep. Animal Science 64, 8796.Google Scholar
Pácha, J 2000. Development of intestinal transport function in mammals. Physiological Reviews 80, 16331667.Google Scholar
Piosik, P, Van Groenigen, M, Van Doorn, J, Baas, F and De Vijlder, J 1997. Effects of maternal thyroid status on thyroid hormones and growth in congenitally hypothyroid goat fetuses during the second half of gestation 1. Endocrinology 138, 511.CrossRefGoogle Scholar
Praetor, A, Ellinger, I, Fuchs, R and Hunziker, W 2000. Transcytosis of immunoglobulin G. Protoplasma 211, 134139.Google Scholar
Quigley, JD, Hammer, CJ, Russel, LE and Polo, J 2005. Passive immunity in newborn calves. In Calf and heifer rearing (ed. PC Garnsworthy), pp. 135157. Nottingham University Press, Nottingham.Google Scholar
Rodewald, R 1976. pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. The Journal of Cell Biology 71, 666669.Google Scholar
Rojas, R and Apodaca, G 2002. Immunoglobulin transport across polarized epithelial cells. Nature Reviews Molecular Cell Biology 3, 944956.Google Scholar
Rose, MT, Wolf, BT and Haresign, W 2007. Effect of the level of iodine in the diet of pregnant ewes on the concentration of immunoglobulin G in the plasma of neonatal lambs following the consumption of colostrum. British Journal of Nutrition 97, 315320.Google Scholar
Rose, M, Pearson, S and Cratchley, T 2012. Effect of iodine, selenium and cobalt rumen boluses given to dry dairy cows on the immunoglobulin and thyroid hormone status of calves. Animal Science Journal 83, 543548.Google Scholar
Russel, A 1984. Means of assessing the adequacy of nutrition of pregnant ewes. Livestock Production Science 11, 429436.Google Scholar
Sangild, PT 2006. Gut responses to enteral nutrition in preterm infants and animals. Experimental Biology and Medicine 231, 16951711.Google Scholar
SAS 2013. SAS users guide, 9.4 Cary. SAS Institue Inc, NC.Google Scholar
Simister, NE and Rees, AR 1985. Isolation and characterization of an Fc receptor from neonatal rat small intestine. European Journal of Immunology 15, 733738.Google Scholar
Spiekermann, GM, Finn, PW, Ward, ES, Dumont, J, Dickinson, BL, Blumberg, RS and Lencer, WI 2002. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life functional expression of FcRn in the mammalian lung. The Journal of Experimental Medicine 196, 303310.Google Scholar
Underwood, EJ and Suttle, NF 1999. Iodine. In The mineral nutrition of livestock, 3rd edition (ed. S Hulbert and K Hill), pp. 343374. CABI Publishing, Oxon.Google Scholar
van der Linden, DS, Kenyon, PR, Blair, HT, Lopez-Villalobas, N, Jenkinson, CMC, Peterson, SW and Mackenzie, DDS 2009. Relationships between early postnatal growth and metabolic function of 16-month-old female offspring born to ewes exposed to different environments during pregnancy. Journal of Developmental Origins of Health and Disease 1, 5059.CrossRefGoogle Scholar
Yvon, M, Levieux, D, Valluy, MC, Pélissier, JP and Mirand, PP 1993. Colostrum protein digestion in newborn lambs. The Journal of Nutrition 123, 586596.Google Scholar
Zhu, X, Peng, J, Raychowdhury, R, Nakajima, A, Lencer, W and Blumberg, R 2002. The heavy chain of neonatal Fc receptor for IgG is sequestered in endoplasmic reticulum by forming oligomers in the absence of β2-microglobulin association. Biochemical Journal 367, 703714.Google Scholar