Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-05T02:54:10.868Z Has data issue: false hasContentIssue false

Whole-transcriptome profiling of sheep fed with a high iodine-supplemented diet

Published online by Cambridge University Press:  23 October 2019

M. Iannaccone
Affiliation:
Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via R. Balzarini 1, 64100Teramo, Italy
R. Elgendy
Affiliation:
Department of Comparative Biomedicine and Food Science, University of Padua, Viale dell’Università 16, 35020Legnaro, Italy
A. Ianni
Affiliation:
Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via R. Balzarini 1, 64100Teramo, Italy
C. Martino
Affiliation:
Specialist Diagnostic Department, Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “G. Caporale”, Via Campo Boario, 64100 Teramo (TE), Italy
F. Palazzo
Affiliation:
Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via R. Balzarini 1, 64100Teramo, Italy
M. Giantin
Affiliation:
Department of Comparative Biomedicine and Food Science, University of Padua, Viale dell’Università 16, 35020Legnaro, Italy
L. Grotta
Affiliation:
Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via R. Balzarini 1, 64100Teramo, Italy
M. Dacasto
Affiliation:
Department of Comparative Biomedicine and Food Science, University of Padua, Viale dell’Università 16, 35020Legnaro, Italy
G. Martino*
Affiliation:
Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via R. Balzarini 1, 64100Teramo, Italy
*
Get access

Abstract

Iodine (I) is a micronutrient that mammals need for proper functionality of thyroid gland since it is the main component of thyroid hormones. Besides studies that have investigated the role of I in livestock nutrition, it is also important to know the transcriptomics changes in small ruminants following I supplementation. Therefore, the aim of this study was to investigate the effects of I on the whole blood transcriptome in sheep. Fifteen lactating cross-bred ewes (3 to 4-year-old, 55 to 65 kg BW) at their late lactation period were enrolled in this study. At the beginning, all the animals had a 2-week acclimation period where they were fed with a basal diet which includes an adequate level of I (2 mg I/animal per day) in the form of calcium iodate (CaI2O6). Then, the ewes were randomly divided into two groups and fed in individual troughs: the control group (n = 5) was maintained on basal diet and the experimental group (I, n = 10) was fed for 40 days with a diet containing a high I supplementation (equivalent to 30 mg I/animal per day), in the form of potassium iodide. Whole blood and milk were collected individually at the beginning (T0) and after the 40 days of supplementation (T40). Iodine quantification was assessed in serum and milk sample. Microarray gene expression analysis was performed on whole blood and, filtering data using a fold change >2 with an adjusted P < 0.05, we identified 250 differentially expressed genes (DEGs) in the I group (T40 v. T0). Looking for biological processes associated with our DEGs, we found significant association with cell growth regulation. Thus, our study unveils the role of I supplementation on gene expression in sheep improving the knowledge about micronutrients in animal nutrition.

Type
Research Article
Copyright
© The Animal Consortium 2019 

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.)

Footnotes

*

These authors contributed equally to this work.

a

Present address: Department of Immunology, Genetics and Pathology, Uppsala University, 75185 Uppsala, Sweden

References

Boland, T, Callan, J, Brophy, P, Quinn, P and Crosby, T 2006. Lamb serum vitamin E and immunoglobulin G concentrations in response to various maternal mineral and iodine supplementation regimens. Animal Science 82, 319325.CrossRefGoogle Scholar
Boland, T, Guinan, M, Brophy, P, Callan, J, Quinn, P, Nowakowski, P and Crosby, T 2005. 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.CrossRefGoogle Scholar
Brent, GA 2012. Mechanisms of thyroid hormone action. Journal of Clinical Investigation 122, 30353043.CrossRefGoogle ScholarPubMed
Comandini, P, Cerretani, L, Rinaldi, M, Cichelli, A and Chiavaro, E 2013. Stability of iodine during cooking: investigation on biofortified and not fortified vegetables International Journal of Food Sciences and Nutrition 64, 857861.CrossRefGoogle Scholar
Conneely, M, Berry, DP, Sayers, R, Murphy, JP, Doherty, ML, Lorenz, I and Kennedy, E 2014. Does iodine supplementation of the prepartum dairy cow diet affect serum immunoglobulin G concentration, iodine, and health status of the calf? Journal of Dairy Science 97, 111.CrossRefGoogle ScholarPubMed
Elgendy, R, Giantin, M, Castellani, F, Grotta, L, Palazzo, F, Dacasto, M and Martino, G 2016. Transcriptomic signature of high dietary organic selenium supplementation in sheep: a nutrigenomic insight using a custom microarray platform and gene set enrichment analysis. Journal of Animal Science 94, 31693184.CrossRefGoogle ScholarPubMed
Elgendy, R, Palazzo, F, Castellani, F, Giantin, M, Grotta, L, Cerretani, L, Dacasto, M and Martino, G 2017. Transcriptome profiling and functional analysis of sheep fed with high zinc-supplemented diet: a nutrigenomic approach. Animal Feed Science and Technology 234, 195204.CrossRefGoogle Scholar
EU Commission 2005. Commission Regulation (EC) No 1459/2005 amending the conditions for authorization of a number of feed additives belonging to the group of trace elements. Off. J. Eur. Union.Google Scholar
European Food Safety Authority 2005. Opinion of the scientific panel on additives and products or substances used in animal feed on the request from the commission on the use of iodine in feedingstuffs. EFSA-Q-2003-058. The EFSA Journal 168, 142.Google Scholar
European Union (EU) Commission Implementing Regulation 2015/861 of 3 June 2015 concerning the authorisation of potassium iodide, calcium iodate anhydrous and coated granulated calcium iodate anhydrous as feed additives for all animal species. Off. J. Eur. Union.Google Scholar
Fecher, P, Goldmann, I and Nagengast, A 1998. Determination of iodine in food samples by inductively coupled plasma mass spectrometry after alkaline extraction. Journal of Analytical Atomic Spectrometry 13, 977982.CrossRefGoogle Scholar
FAO (Food and Agriculture Organization of the United Nations) 2015. Statistical pocketbook: World food and agriculture, 2015. Rome, Food and Agriculture Organization of the United Nations.Google Scholar
Fox, C, Pencina, M, D’agostino, R, Murabito, J, Seely, E, Pearce, E and Vasan, R 2008. Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Archives of Internal Medicine 168, 587592.CrossRefGoogle Scholar
Henao-Velásquez, AF, Múnera-Bedoya, OD, Herrera, AC, Agudelo-Trujillo, JHand Cerón-Muñoz, MF and 2014. Lactose and milk urea nitrogen: fluctuations during lactation in Holstein cows. Revista Brasileira de Zootecnia 43, 479484.CrossRefGoogle Scholar
Huang, D, Sherman, BT and Lempicki, RA 2009a. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37, 113.CrossRefGoogle Scholar
Huang, D, Sherman, BT and Lempicki, RA 2009b. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocol 4, 4457.CrossRefGoogle Scholar
Hwa, V, Oh, Y and Rosenfeld, RG 1999. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocrinology Review 20, 761787.Google ScholarPubMed
Iannaccone, M, Elgendy, R, Giantin, M, Martino, C, Giansante, D, Ianni, A, Dacasto, M and Martino, G 2018. RNA sequencing-based whole-transcriptome analysis of Friesian cattle fed with grape pomace-supplemented diet. Animals 8, 188.CrossRefGoogle ScholarPubMed
Iannaccone, M, Ianni, A, Ramazzotti, S, Grotta, L, Marone, E, Cichelli, A and Martino, G. 2019. Whole blood transcriptome analysis reveals positive effects of dried olive pomace-supplemented diet on inflammation and cholesterol in laying hens. Animals 9, 427.CrossRefGoogle ScholarPubMed
McCauley, EH, Linn, JG and Goodrich, RD 1973. Experimentally induced iodide toxicosis in lambs. American Journal of Veterinary Research 34, 6570.Google ScholarPubMed
McDowell, LR 2003. Minerals in animal and human nutrition (No. Ed. 2). Elsevier Science BV.Google Scholar
Metsalu, T and Vilo, J 2015. ClustVis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Research 43, W566570.CrossRefGoogle ScholarPubMed
Meyer, U, Weigel, K, Schöne, F, Leiterer, M and Flachowsky, G 2008. Effect of dietary iodine on growth and iodine status of growing fattening bulls. Livestock Science 115, 219225.CrossRefGoogle Scholar
National Research Council (NRC) 2007. Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids. US National Academies Press, Washington, DC, USA.Google Scholar
Norouzian, MA, Valizadeh, R, Azizi, F, Hedayati, M, Naserian, AA and Shahroodi, FE 2009. The effect of feeding different levels of potassium iodide on performance, T3 and T4 concentrations and iodine excretion in Holstein dairy cows. Journal of Animal and Veterinary Advances 8, 111114.Google Scholar
Ritchie, ME, Phipson, B, Wu, D, Hu, Y, Law, CW, Shi, W and Smyth, GK 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research 43, e47.CrossRefGoogle ScholarPubMed
Rose, MT, Wolf, B 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 44, 315320.CrossRefGoogle Scholar
Schone, F, Leiterer, M, Lebzien, P, Bemmann, D, Spolders, M and Flachowsky, G 2009. Iodine concentration of milk in a dose – response study with dairy cows and implications for consumer iodine intake. Journal of Trace Elements in Medicine and Biology 23, 8492.CrossRefGoogle Scholar
Schone, F and Rajendram, R (ed. Preedy, VR, Burrow, GN and Watson, R 2009. Iodine in farm animals. In Comprehensive handbook of iodine (ed. ), pp. 151170. Elsevier, Amsterdam, the Netherlands.CrossRefGoogle Scholar
Tusher, VG, Tibshirani, R and Chu, G 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 98, 51165121.CrossRefGoogle ScholarPubMed
Yao, X, Sa, R, Ye, C, Zhang, D, Zhang, S, Xia, H, Wang, Y, Jiang, J, Yin, H and Ying, H 2015. Effects of thyroid hormone status on metabolic pathways of arachidonic acid in mice and humans: a targeted metabolomic approach. Prostaglandins & Other Lipid Mediators 118–119, 1118.CrossRefGoogle ScholarPubMed
Zimmermann, MB 2009. Iodine deficiency. Endocrinology Review 30, 376408.CrossRefGoogle ScholarPubMed
Zimmermann, MB, Jooste, PL, Mabapa, NS, Mbhenyane, X, Schoeman, S, Biebinger, R, Chaouki, N, Bozo, M, Grimci, L and Bridson, J 2007. Treatment of iodine deficiency in school-age children increases insulin-like growth factor (IGF)-I and IGF binding protein-3 concentrations and improves somatic growth. The Journal of Clinical Endocrinology and Metabolism 92, 437442.CrossRefGoogle ScholarPubMed
Supplementary material: File

Iannaccone et al. supplementary material

Table S1 and Figure S1

Download Iannaccone et al. supplementary material(File)
File 160.3 KB