{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,24]],"date-time":"2026-04-24T10:28:26Z","timestamp":1777026506628,"version":"3.51.4"},"reference-count":55,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,9,30]],"date-time":"2022-09-30T00:00:00Z","timestamp":1664496000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,9,30]],"date-time":"2022-09-30T00:00:00Z","timestamp":1664496000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100010787","name":"Genome Alberta","doi-asserted-by":"crossref","award":["ALGP47"],"award-info":[{"award-number":["ALGP47"]}],"id":[{"id":"10.13039\/501100010787","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Vet Res"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Porcine reproductive and respiratory syndrome virus (PRRSV) in late gestation causes a profound suppression of circulating maternal and fetal thyroid hormone during a critical window of development. To understand this relationship, we evaluated thyroid hormone metabolism at the maternal\u2013fetal interface and within fetal tissues, along with hormone metabolite levels in serum. Fetuses were classified using an established model based on viral load in serum and thymus, and preservation status, including uninfected (UNIF), high-viral load viable (HV-VIA), and high-viral load meconium-stained (HV-MEC), with additional controls from sham-inoculated gilts (CON). Expression of three iodothyronine deiodinases, five sulfotransferases, sulfatase, and two solute carriers known to transport thyroid hormone were evaluated in maternal endometrium and fetal placenta, liver, and kidney. Serum thyroxin (T4), reverse triiodothyronine (rT3), and diiodothyronine (T2) were evaluated via liquid chromatography tandem mass spectrometry. Significant changes in gene expression were observed in all four tissues, with the liver being the most severely impacted. We observed local and fetal specific regulation of maternal tissues through significant upregulation of DIO2 and DIO3 expression in the endometrium corresponding to infected but viable fetuses relative to uninfected and control fetuses. Expression levels of DIO2 and DIO3 were significantly higher in the resilient (HV-VIA) fetuses relative to the susceptible (HV-MEC) fetuses. A substantial decrease in serum T4 was confirmed, with no corresponding increase in rT3 or T2. Collectively, these results show that thyroid hormone metabolism is altered at the maternal\u2013fetal interface and within the PRRSV infected fetus and is associated with fetal viability.<\/jats:p>","DOI":"10.1186\/s13567-022-01092-3","type":"journal-article","created":{"date-parts":[[2022,9,29]],"date-time":"2022-09-29T23:04:02Z","timestamp":1664492642000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Effects of porcine reproductive and respiratory syndrome virus (PRRSV) on thyroid hormone metabolism in the late gestation fetus"],"prefix":"10.1186","volume":"53","author":[{"given":"Erin K.","family":"Ison","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amber S.","family":"Hopf-Jannasch","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John C. S.","family":"Harding","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8596-3057","authenticated-orcid":false,"given":"J.","family":"Alex Pasternak","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,9,30]]},"reference":[{"key":"1092_CR1","doi-asserted-by":"crossref","first-page":"72","DOI":"10.54846\/jshap\/754","volume":"21","author":"DJ Holtkamp","year":"2013","unstructured":"Holtkamp DJ (2013) Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J Swine Health Prod 21:72\u201384","journal-title":"J Swine Health Prod"},{"key":"1092_CR2","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/S0378-1135(98)00176-X","volume":"61","author":"S Kranker","year":"1998","unstructured":"Kranker S, Nielsen J, Bille-Hansen V, B\u00f8tner A (1998) Experimental inoculation of swine at various stages of gestation with a Danish isolate of porcine reproductive and respiratory syndrome virus (PRRSV). Vet Microbiol 61:21\u201331","journal-title":"Vet Microbiol"},{"key":"1092_CR3","doi-asserted-by":"publisher","first-page":"154883","DOI":"10.1016\/j.cyto.2019.154883","volume":"126","author":"JA Pasternak","year":"2020","unstructured":"Pasternak JA, MacPhee DJ, Harding JCS (2020) Fetal cytokine response to porcine reproductive and respiratory syndrome virus-2 infection. Cytokine 126:154883","journal-title":"Cytokine"},{"key":"1092_CR4","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1016\/j.virusres.2010.09.001","volume":"154","author":"RRR Rowland","year":"2010","unstructured":"Rowland RRR (2010) The interaction between PRRSV and the late gestation pig fetus. Virus Res 154:114\u2013122","journal-title":"Virus Res"},{"key":"1092_CR5","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1186\/s12864-020-07154-0","volume":"21","author":"A Van Goor","year":"2020","unstructured":"Van Goor A, Pasternak A, Walker K, Hong L, Malgarin C, MacPhee DJ, Harding JCS, Lunney JK (2020) Differential responses in placenta and fetal thymus at 12 days post infection elucidate mechanisms of viral level and fetal compromise following PRRSV2 infection. BMC Genom 21:763","journal-title":"BMC Genom"},{"key":"1092_CR6","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s13567-022-01030-3","volume":"53","author":"MK Mulligan","year":"2022","unstructured":"Mulligan MK, Kleiman JE, Caldemeyer AC, Harding JCS, Pasternak JA (2022) Porcine reproductive and respiratory virus 2 infection of the fetus results in multi-organ cell cycle suppression. Vet Res 53:13","journal-title":"Vet Res"},{"key":"1092_CR7","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1186\/s13567-020-00772-2","volume":"51","author":"JA Pasternak","year":"2020","unstructured":"Pasternak JA, MacPhee DJ, Harding JCS (2020) Maternal and fetal thyroid dysfunction following porcine reproductive and respiratory syndrome virus2 infection. Vet Res 51:47","journal-title":"Vet Res"},{"key":"1092_CR8","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.virusres.2018.12.002","volume":"260","author":"CM Malgarin","year":"2019","unstructured":"Malgarin CM, Nosach R, Novakovic P, Suleman M, Ladinig A, Detmer SE, MacPhee DJ, Harding JCS (2019) Classification of fetal resilience to porcine reproductive and respiratory syndrome (PRRS) based on temporal viral load in late gestation maternal tissues and fetuses. Virus Res 260:151\u2013162","journal-title":"Virus Res"},{"key":"1092_CR9","doi-asserted-by":"publisher","first-page":"e96104","DOI":"10.1371\/journal.pone.0096104","volume":"9","author":"A Ladinig","year":"2014","unstructured":"Ladinig A, Wilkinson J, Ashley C, Detmer SE, Lunney JK, Plastow G, Harding JCS (2014) Variation in fetal outcome, viral load and ORF5 sequence mutations in a large scale study of phenotypic responses to late gestation exposure to type 2 porcine reproductive and respiratory syndrome virus. PLoS One 9:e96104","journal-title":"PLoS ONE"},{"key":"1092_CR10","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.mce.2017.01.038","volume":"458","author":"DP Carvalho","year":"2017","unstructured":"Carvalho DP, Dupuy C (2017) Thyroid hormone biosynthesis and release. Mol Cell Endocrinol 458:6\u201315","journal-title":"Mol Cell Endocrinol"},{"key":"1092_CR11","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1530\/JOE-12-0204","volume":"215","author":"VM Darras","year":"2012","unstructured":"Darras VM, Van Herck SLJ (2012) Iodothyronine deiodinase structure and function: from ascidians to humans. J Endocrinol 215:189\u2013206","journal-title":"J Endocrinol"},{"key":"1092_CR12","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1210\/en.2013-1800","volume":"155","author":"J M\u00fcller","year":"2014","unstructured":"M\u00fcller J, Mayerl S, Visser TJ, Darras VM, Boelen A, Frappart L, Mariotta L, Verrey F, Heuer H (2014) Tissue-specific alterations in thyroid hormone homeostasis in combined Mct10 and Mct8 deficiency. Endocrinology 155:315\u2013325","journal-title":"Endocrinology"},{"key":"1092_CR13","doi-asserted-by":"publisher","first-page":"R87","DOI":"10.1530\/JOE-14-0025","volume":"221","author":"AJ Forhead","year":"2014","unstructured":"Forhead AJ, Fowden AL (2014) Thyroid hormones in fetal growth and prepartum maturation. J Endocrinol 221:R87\u2013R103","journal-title":"J Endocrinol"},{"key":"1092_CR14","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.beem.2007.08.006","volume":"22","author":"J Kratzsch","year":"2008","unstructured":"Kratzsch J, Pulzer F (2008) Thyroid gland development and defects. Best Pract Res Clin Endocrinol Metab 22:57\u201375","journal-title":"Best Pract Res Clin Endocrinol Metab"},{"key":"1092_CR15","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1556\/avet.52.2004.4.1","volume":"52","author":"E Brzezi\u0144ska-Slebodzi\u0144ska","year":"2004","unstructured":"Brzezi\u0144ska-Slebodzi\u0144ska E, Slebodzi\u0144ski AB (2004) Changes in thyroxine, 3,3\u2032,5-triiodothyronine and 3,3\u20325\u2032-triiodothyronine content in the thyroid gland and in serum to thyroid tissue iodothyronine ratios during ontogenesis in the fetal pig. Acta Vet Hung 52:379\u2013387","journal-title":"Acta Vet Hung"},{"key":"1092_CR16","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1677\/joe.0.1550295","volume":"155","author":"E Krysin","year":"1997","unstructured":"Krysin E, Brzezi\u0144ska-Slebodzi\u0144ska E, Slebodzi\u0144ski AB (1997) Divergent deiodination of thyroid hormones in the separated parts of the fetal and maternal placenta in pigs. J Endocrinol 155:295\u2013303","journal-title":"J Endocrinol"},{"key":"1092_CR17","doi-asserted-by":"publisher","first-page":"163","DOI":"10.3389\/fendo.2017.00163","volume":"8","author":"A Chatzitomaris","year":"2017","unstructured":"Chatzitomaris A, Hoermann R, Midgley JE, Hering S, Urban A, Dietrich B, Abood A, Klein HH, Dietrich JW (2017) Thyroid allostasis\u2013adaptive responses of thyrotropic feedback control to conditions of strain, stress, and developmental programming. Front Endocrinol 8:163","journal-title":"Front Endocrinol"},{"key":"1092_CR18","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.neuroscience.2015.09.070","volume":"342","author":"NK Moog","year":"2017","unstructured":"Moog NK, Entringer S, Heim C, Wadhwa PD, Kathmann N, Buss C (2017) Influence of maternal thyroid hormones during gestation on fetal brain development. Neuroscience 342:68","journal-title":"Neuroscience"},{"key":"1092_CR19","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1038\/s41574-019-0218-2","volume":"15","author":"C Luongo","year":"2019","unstructured":"Luongo C, Dentice M, Salvatore D (2019) Deiodinases and their intricate role in thyroid hormone homeostasis. Nat Rev Endocrinol 15:479\u2013488","journal-title":"Nat Rev Endocrinol"},{"key":"1092_CR20","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1016\/1043-2760(90)90055-8","volume":"1","author":"TJ Visser","year":"1990","unstructured":"Visser TJ, van Buuren JC, Rutgers M, Eelkman Rooda SJ, de Herder WW (1990) The role of sulfation in thyroid hormone metabolism. Trends Endocrinol Metab 1:211\u2013218","journal-title":"Trends Endocrinol Metab"},{"key":"1092_CR21","first-page":"2734","volume":"86","author":"K Richard","year":"2001","unstructured":"Richard K, Hume R, Kaptein E, Stanley EL, Visser TJ, Coughtrie MW (2001) Sulfation of thyroid hormone and dopamine during human development: ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain. J Clin Endocrinol Metab 86:2734\u20132742","journal-title":"J Clin Endocrinol Metab"},{"key":"1092_CR22","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/S0303-7207(99)00088-X","volume":"151","author":"VM Darras","year":"1999","unstructured":"Darras VM, Hume R, Visser TJ (1999) Regulation of thyroid hormone metabolism during fetal development. Mol Cell Endocrinol 151:37\u201347","journal-title":"Mol Cell Endocrinol"},{"key":"1092_CR23","doi-asserted-by":"publisher","first-page":"104800","DOI":"10.1016\/j.livsci.2021.104800","volume":"255","author":"H Ko","year":"2022","unstructured":"Ko H, Sammons J, Pasternak JA, Hamonic G, Starrak G, MacPhee DJ, Detmer SE, Plastow GS, Harding JCS (2022) Phenotypic effect of a single nucleotide polymorphism on SSC7 on fetal outcomes in PRRSV-2 infected gilts. Livest Sci 255:104800","journal-title":"Livest Sci"},{"key":"1092_CR24","doi-asserted-by":"publisher","first-page":"skab325","DOI":"10.1093\/jas\/skab325","volume":"99","author":"JA Pasternak","year":"2021","unstructured":"Pasternak JA, MacPhee DJ, Lunney JK, Rowland RRR, Dyck MK, Fortin F, Dekkers JCM, Plastow GS, Harding JCS, PigGen C (2021) Thyroid hormone suppression in feeder pigs following polymicrobial or porcine reproductive and respiratory syndrome virus-2 challenge. J Anim Sci 99:skab325","journal-title":"J Anim Sci"},{"key":"1092_CR25","first-page":"443","volume":"43","author":"E Krysin","year":"1995","unstructured":"Krysin E (1995) Differences in the thyroxine, triiodothyronine and reverse triiodothyronine contents of fetal pig tissues relative to gestational age. Acta Vet Hung 43:443\u2013451","journal-title":"Acta Vet Hung"},{"key":"1092_CR26","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1186\/s12917-021-02883-0","volume":"17","author":"CM Malgarin","year":"2021","unstructured":"Malgarin CM, Moser F, Pasternak JA, Hamonic G, Detmer SE, MacPhee DJ, Harding JCS (2021) Fetal hypoxia and apoptosis following maternal porcine reproductive and respiratory syndrome virus (PRRSV) infection. BMC Vet Res 17:182","journal-title":"BMC Vet Res"},{"key":"1092_CR27","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1373\/clinchem.2008.112797","volume":"55","author":"SA Bustin","year":"2009","unstructured":"Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611\u2013622","journal-title":"Clin Chem"},{"key":"1092_CR28","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1071\/RD11013","volume":"23","author":"G Oliver","year":"2011","unstructured":"Oliver G, Novak S, Patterson JL, Pasternak JA, Paradis F, Norrby M, Oxtoby K, Dyck MK, Dixon WT, Foxcroft GR (2011) Restricted feed intake in lactating primiparous sows. II. Effects on subsequent litter sex ratio and embryonic gene expression. Reprod Fertil Dev 23:899\u2013911","journal-title":"Reprod Fertil Dev"},{"key":"1092_CR29","doi-asserted-by":"publisher","first-page":"7556","DOI":"10.3168\/jds.2019-16294","volume":"102","author":"C Kent-Dennis","year":"2019","unstructured":"Kent-Dennis C, Pasternak A, Plaizier JC, Penner GB (2019) Potential for a localized immune response by the ruminal epithelium in nonpregnant heifers following a short-term subacute ruminal acidosis challenge. J Dairy Sci 102:7556\u20137569","journal-title":"J Dairy Sci"},{"key":"1092_CR30","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/j.vetimm.2015.06.003","volume":"166","author":"T K\u00e4ser","year":"2015","unstructured":"K\u00e4ser T, Cnudde T, Hamonic G, Rieder M, Pasternak JA, Lai K, Tikoo SK, Wilson HL, Meurens F (2015) Porcine retinal cell line VIDO R1 and Chlamydia suis to modelize ocular chlamydiosis. Vet Immunol Immunopathol 166:95\u2013107","journal-title":"Vet Immunol Immunopathol"},{"key":"1092_CR31","doi-asserted-by":"publisher","first-page":"e7399","DOI":"10.1371\/journal.pone.0007399","volume":"4","author":"JN Fleming-Waddell","year":"2009","unstructured":"Fleming-Waddell JN, Olbricht GR, Taxis TM, White JD, Vuocolo T, Craig BA, Tellam RL, Neary MK, Cockett NE, Bidwell CA (2009) Effect of DLK1 and RTL1 but not MEG3 or MEG8 on muscle gene expression in Callipyge lambs. PLoS One 4:e7399","journal-title":"PLoS ONE"},{"key":"1092_CR32","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1186\/s12864-018-4682-1","volume":"19","author":"H Yu","year":"2018","unstructured":"Yu H, Waddell JN, Kuang S, Tellam RL, Cockett NE, Bidwell CA (2018) Identification of genes directly responding to DLK1 signaling in Callipyge sheep. BMC Genom 19:283","journal-title":"BMC Genom"},{"key":"1092_CR33","doi-asserted-by":"publisher","first-page":"1831","DOI":"10.1007\/s00216-010-3705-9","volume":"397","author":"D Wang","year":"2010","unstructured":"Wang D, Stapleton HM (2010) Analysis of thyroid hormones in serum by liquid chromatography\u2013tandem mass spectrometry. Anal Bioanal Chem 397:1831\u20131839","journal-title":"Anal Bioanal Chem"},{"key":"1092_CR34","volume-title":"R: a language and environment for statistical computing","author":"Team RC","year":"2018","unstructured":"Team RC (2018) R: a language and environment for statistical computing. Austria, Vienna"},{"key":"1092_CR35","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/S0960-0760(03)00025-6","volume":"84","author":"MW Pfaffl","year":"2003","unstructured":"Pfaffl MW, Lange IG, Meyer HHD (2003) The gastrointestinal tract as target of steroid hormone action: quantification of steroid receptor mRNA expression (AR, ER\u03b1, ER\u03b2 and PR) in 10 bovine gastrointestinal tract compartments by kinetic RT-PCR. J Steroid Biochem Mol Biol 84:159\u2013166","journal-title":"J Steroid Biochem Mol Biol"},{"key":"1092_CR36","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-24277-4","volume-title":"ggplot2: elegant graphics for data analysis","author":"H Wickham","year":"2016","unstructured":"Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York"},{"key":"1092_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0378-1135(01)00450-3","volume":"84","author":"J Nielsen","year":"2002","unstructured":"Nielsen J, Botner A, Bille-Hansen V, Oleksiewicz MB, Storgaard T (2002) Experimental inoculation of late term pregnant sows with a field isolate of porcine reproductive and respiratory syndrome vaccine-derived virus. Vet Microbiol 84:1\u201313","journal-title":"Vet Microbiol"},{"key":"1092_CR38","doi-asserted-by":"publisher","first-page":"2534","DOI":"10.2527\/2004.8292534x","volume":"82","author":"RL McPherson","year":"2004","unstructured":"McPherson RL, Ji F, Wu G, Blanton JR, Kim SW (2004) Growth and compositional changes of fetal tissues in pigs. J Anim Sci 82:2534\u20132540","journal-title":"J Anim Sci"},{"key":"1092_CR39","first-page":"2868","volume":"83","author":"K Richard","year":"1998","unstructured":"Richard K, Hume R, Kaptein E, Sanders JP, van Toor H, de Herder WW, den Hollander JC, Krenning EP, Visser TJ (1998) Ontogeny of iodothyronine deiodinases in human liver. J Clin Endocrinol Metab 83:2868\u20132874","journal-title":"J Clin Endocrinol Metab"},{"key":"1092_CR40","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1056\/NEJM199410203311608","volume":"331","author":"FH Epstein","year":"1994","unstructured":"Epstein FH, Burrow GN, Fisher DA, Larsen PR (1994) Maternal and fetal thyroid function. N Engl J Med 331:1072\u20131078","journal-title":"N Engl J Med"},{"key":"1092_CR41","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1016\/0304-4165(87)90008-0","volume":"923","author":"R Iglesias","year":"1987","unstructured":"Iglesias R, Fernandez JA, Mampel T, Obreg\u00f3n MJ, Villarroya F (1987) Iodothyronine 5\u2032-deiodinase activity in rat brown adipose tissue during development. Biochim Biophys Acta 923:233\u2013240","journal-title":"Biochim Biophys Acta"},{"key":"1092_CR42","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1210\/endo.140.2.6537","volume":"140","author":"JM Bates","year":"1999","unstructured":"Bates JM, St. Germain DL, Galton VA (1999) Expression profiles of the three iodothyronine deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 140:844\u2013851","journal-title":"Endocrinology"},{"key":"1092_CR43","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1172\/JCI26240","volume":"116","author":"A Hernandez","year":"2006","unstructured":"Hernandez A, Martinez ME, Fiering S, Galton VA, St. Germain D (2006) Type 3 deiodinase is critical for the maturation and function of the thyroid axis. J Clin Invest 116:476\u2013484","journal-title":"J Clin Invest"},{"key":"1092_CR44","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1210\/endo-111-3-959","volume":"111","author":"E Roti","year":"1982","unstructured":"Roti E, Braverman LE, Fang SL, Alex S, Emerson CH (1982) Ontogenesis of placental inner ring thyroxine deiodinase and amniotic fluid 3,3\u2032,5\u2032-triiodothyronine concentration in the rat. Endocrinology 111:959\u2013963","journal-title":"Endocrinology"},{"key":"1092_CR45","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1210\/jcem-53-3-498","volume":"53","author":"E Roti","year":"1981","unstructured":"Roti E, Fang SL, Green K, Emerson CH, Braverman LE (1981) Human placenta is an active site of thyroxine and 3,3\u20325-triiodothyronine tyrosyl ring deiodination. J Clin Endocrinol Metab 53:498\u2013501","journal-title":"J Clin Endocrinol Metab"},{"key":"1092_CR46","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1007\/s00018-007-7396-0","volume":"65","author":"B Gereben","year":"2008","unstructured":"Gereben B, Ze\u00f6ld A, Dentice M, Salvatore D, Bianco AC (2008) Activation and inactivation of thyroid hormone by deiodinases: local action with general consequences. Cell Mol Life Sci 65:570\u2013590","journal-title":"Cell Mol Life Sci"},{"key":"1092_CR47","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1172\/JCI111471","volume":"74","author":"JE Silva","year":"1984","unstructured":"Silva JE, Matthews PS (1984) Production rates and turnover of triiodothyronine in rat-developing cerebral cortex and cerebellum. Responses to hypothyroidism. J Clin Invest 74:1035\u20131049","journal-title":"J Clin Invest"},{"key":"1092_CR48","first-page":"2154","volume":"81","author":"JM Koopdonk-Kool","year":"1996","unstructured":"Koopdonk-Kool JM, de Vijlder JJ, Veenboer GJ, Ris-Stalpers C, Kok JH, Vulsma T, Boer K, Visser TJ (1996) Type II and type III deiodinase activity in human placenta as a function of gestational age. J Clin Endocrinol Metab 81:2154\u20132158","journal-title":"J Clin Endocrinol Metab"},{"key":"1092_CR49","doi-asserted-by":"publisher","first-page":"4420","DOI":"10.1210\/en.2007-0505","volume":"148","author":"MM Joyce","year":"2007","unstructured":"Joyce MM, Burghardt RC, Geisert RD, Burghardt JR, Hooper RN, Ross JW, Ashworth MD, Johnson GA (2007) Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. Endocrinology 148:4420\u20134431","journal-title":"Endocrinology"},{"key":"1092_CR50","first-page":"1357","volume":"84","author":"MHA Kester","year":"1999","unstructured":"Kester MHA, Kaptein E, Roest TJ, van Dijk CH, Tibboel D, Meinl W, Glatt H, Coughtrie MWH, Visser TJ (1999) Characterization of human iodothyronine sulfotransferases1. J Clin Endocrinol Metab 84:1357\u20131364","journal-title":"J Clin Endocrinol Metab"},{"key":"1092_CR51","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1016\/j.mce.2005.06.003","volume":"240","author":"EL Stanley","year":"2005","unstructured":"Stanley EL, Hume R, Coughtrie MWH (2005) Expression profiling of human fetal cytosolic sulfotransferases involved in steroid and thyroid hormone metabolism and in detoxification. Mol Cell Endocrinol 240:32\u201342","journal-title":"Mol Cell Endocrinol"},{"key":"1092_CR52","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1203\/00006450-200012000-00024","volume":"48","author":"S-Y Wu","year":"2000","unstructured":"Wu S-Y, Huang W-S, Fisher DA, Florsheim WH, Galton VA (2000) Iodothyronine sulfotransferase activity in rat uterus during gestation. Pediatr Res 48:847\u2013851","journal-title":"Pediatr Res"},{"key":"1092_CR53","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1089\/thy.1996.6.255","volume":"6","author":"IJ Chopra","year":"1996","unstructured":"Chopra IJ, Nguyen D (1996) Demonstration of thyromimetic effects of 3,5,3\u2032-triiodothyronine sulfate (T3S) in euthyroid rats. Thyroid 6:229\u2013232","journal-title":"Thyroid"},{"key":"1092_CR54","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1210\/endo.133.1.8319558","volume":"133","author":"F Santini","year":"1993","unstructured":"Santini F, Hurd RE, Lee B, Chopra IJ (1993) Thyromimetic effects of 3,5,3\u2032-triiodothyronine sulfate in hypothyroid rats. Endocrinology 133:105\u2013110","journal-title":"Endocrinology"},{"key":"1092_CR55","first-page":"E115","volume":"265","author":"SY Wu","year":"1993","unstructured":"Wu SY, Polk DH, Huang WS, Reviczky A, Wang K, Fisher DA (1993) Sulfate conjugates of iodothyronines in developing sheep: effect of fetal hypothyroidism. Am J Physiol 265:E115\u2013E120","journal-title":"Am J Physiol"}],"container-title":["Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13567-022-01092-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13567-022-01092-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13567-022-01092-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,4]],"date-time":"2024-10-04T23:44:59Z","timestamp":1728085499000},"score":1,"resource":{"primary":{"URL":"https:\/\/veterinaryresearch.biomedcentral.com\/articles\/10.1186\/s13567-022-01092-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,30]]},"references-count":55,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["1092"],"URL":"https:\/\/doi.org\/10.1186\/s13567-022-01092-3","relation":{},"ISSN":["1297-9716"],"issn-type":[{"value":"1297-9716","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,30]]},"assertion":[{"value":"11 July 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 August 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 September 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Animal work was conducted in strict accordance with the guidelines of the Canadian Council of Animal Care and with approval of the University of Saskatchewan\u2019s Animal Research Ethics Board (Exp. Protocol #20180071).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"The authors declare that they have no competing interest.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"74"}}