Mus musculus: an experimental model for Deiodinase (DIO3) and Transthyretin (TTR) expression during placental development
DOI:
https://doi.org/10.18041/1900-3803/entramado.1.6538Keywords:
Animal Models, iodothyronine deiodinase type III, Placenta, Prealbumin, Pregnancy, Thyroid HormonesAbstract
Introduction: Correct functioning of hypothalamic-pituitary-thyroid axis is essential for embryonic-fetal growth and development, as it is involved in tissue differentiation, brain and somatic development, bone maturation and metabolic regulation. Maternal thyroid hormones passage to the fetus through the placenta depends on transmembrane transporters, deiodinase enzymes (DIO2 and DIO3) and carrier proteins (TTR). Objective: Identify DIO3 and TTR expression within placental layers of Mus musculus E10.5, E12.5 and E14.5. Methods: Placental structure, DIO3 and TTR expression were evaluated using histochemistry and immunofluorescence techniques. Results: We found that the three placental layers, labyrinth zone, junctional zone, and decidua were present since E10.5. At E12.5 placental final conformation was observed. DIO3 and TTR were detected in the three stages with a predominance in the labyrinth. Conclusion: DIO3 and TTR are expressed throughout the establishment and maturation of mouse placenta. Mice are a useful tool for studying how thyroid hormones are transported from maternal to fetal circulation at the placenta.
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BARBER, Katharine J; FRANKLYN, Jayne A.; MCCABE, Christopher J.; KHANIM, FL.; BULMER, J.N.; WHITLEY, G.S.J.; KILBY, M.D. The in vitro effects of triiodothyronine on epidermal growth factor-induced trophoblast function. In: Journal of Clinical Endocrinology and Metabolism. March 2005. vol. 90, no. 3, p.1655–1661. https://doi.org/10.1210/jc.2004-0785
BERNASCONI, Sergio; SARTORI, C.; MERLI, S.; LAZZERONI, P.; CESARI, S.; STREET, M. E. Thyroid hormones in Fetal Development. In: Thyroid Diseases in Childhood: Recent Advances from Basic Science to Clinical Practice. January 2015. In Thyroid Diseases in Childhood: Recent Advances from Basic Science to Clinical Practice (pp. 15–26). Springer International Publishing. https://doi.org/10.1007/978-3-319-19213-0_2
BIANCO, Antonio C.; DUMITRESCU, Alexandra; GEREBEN, Balázs; RIBEIRO, Miriam O.; FONSECA, Tatiana L.; FERNANDES, Gustavo W.; BOCCO, Barbara M. L. C. Paradigms of Dynamic Control of Thyroid Hormone Signaling. In: Endocrine Reviews. 2019. vol. 40, no. 4, p.1000–1047. https://doi.org/10.1210/er.2018-00275
BOLON, Brad. Protocols for placental histology. In: Croy A, Yamada AT, Lee Adamson S (eds) The guide to investigation of mouse pregnancy. Elsevier, London. p. 537–544. ISBN: 978-0-12-394445-0 https://doi.org/10.1016/B978-0-12-394445-0.00045-X
BURNUM, Kristin E.; TRANGUCH, Susanne; MI, Deming; DAIKOKU, Takiko; DEY, S. K.; CAPRIOLI, Richard M. Imaging mass spectrometry reveals unique protein profiles during embryo implantation. In: Endocrinology. 2008. vol. 149, no. 7, p.3274 –3278. https://doi.org/10.1210/en.2008-0309
CHAN, Shiao; KACHILELE, Stivelia; HOBBS, Emilie; BULMER, Judith N.; BOELAERT, Kristien; MCCABE, Christopher J.; DRIVER, Patricia M.; BRADWELL, Arthur R.; KESTER, Monica; VISSER, Theo J.; FRANKLYN, Jayne A; KILBY, Mark D. Placental Iodothyronine Deiodinase Expression in Normal and Growth-Restricted Human Pregnancies. In: The Journal of Clinical Endocrinology & Metabolism. 1 September 2003. Vol. 88, no. 9. p. 4488–4495. https://doi.org/10.1210/jc.2003-030228
CARTER, Anthony Michael. Animal models of human placentation--a review. In: Placenta. Apr , 2007. vol. 28 Suppl A:S41-7. Epub 2006 Dec 27. PMID: 17196252. https://doi.org/10.1016/j.placenta.2006.11.002
CORNETT, Bridget; SNOWBALL, John; VARISCO, Brian M.; LANG, Richard; WHITSETT Jeffrey; SINNER, Debora. Wntless is required for peripheral lung differentiation and pulmonary vascular development. In: Developmental Biology. Jul, 2013. vol. 1 no. 379(1). p. 38-52. PMID: 23523683; PMCID: PMC3699333. https://doi.org/10.1016/j.ydbio.2013.03.010
CHOURPILIADI, Charikleia; PAPARODIS, Rodis. Physiology, Pituitary Issues During Pregnancy. In: StatPearls. 2020. In T. Island (Ed.), StatPearls. StatPearls Publishing. http://www.ncbi.nlm.nih.gov/pubmed/31869188
DARRAS, Veerle M.; HUME, Robert; VISSER, Theo J. Regulation of thyroid hormone metabolism during fetal development. In: Molecular and Cellular Endocrinology. 1999. vol. 151, p.37–47.
DENTICE, Monica; SALVATORE, Domenico. Local impact of thyroid hormone inactivation. In: Journal of Endocrinology. June 2011. vol. 209, no. 3, p.273–282. https://doi.org/10.1530/JOE-11-0002
DIAO, Honglu; XIAO, Shuo; CUI, Juan; CHUN, Jerold; XU, Ying; YE, Xiaoqin. Progesterone receptor-mediated up-regulation of transthyretin in preimplantation mouse uterus. In: Fertility and Sterility. May 2010. vol. 93, no. 8, p.2750–2753. https://doi.org/10.1016/j.fertnstert.2010.01.009
EERDEKENS, An; VERHAEGHE, Johan; DARRAS, Veerle; NAULAERS, Gunnar; DEN BERGHE, Greet; LANGOUCHE, Lies; VANHOLE, Christine. The placenta in fetal thyroid hormone delivery: from normal physiology to adaptive mechanisms in complicated pregnancies. In: The Journal of Maternal-Fetal & Neonatal Medicine. March 2019. vol. 14, p.1–10. https://doi.org/10.1080/14767058.2019.1586875
FELDING, Peter; FEX, Goran. Cellular Origin of Prealbumin in the Rat. In: Biochimica et Biophysica A Cta. 1982. vol. 716, no. 3, p.446–449. https://doi.org/10.1016/0304-4165(82)90040-X
FELDT-RASMUSSEN, Ulla; MATHIESEN, Elisabeth R. Endocrine disorders in pregnancy: Physiological and hormonal aspects of pregnancy. In: Best Practice and Research: Clinical Endocrinology and Metabolism. 2011. vol. 25, no. 6, p.875–884. https://doi.org/10.1016/j.beem.2011.07.004
FORHEAD, AJ.; FOWDEN, AL. Thyroid hormones in fetal growth and prepartum maturation. In: Journal of Endocrinology. 2014. vol. 221, no. 3, p.R87- 103. https://doi.org/10.1530/joe-14-0025
GALTON, Valerie A.; MARTÍNEZ, Elena; HERNÁNDEZ, Arturo; GERMAIN, Emily AS.; BATES, Joanne M.; GERMAIN, Donald L. S. Pregnant rat uterus expresses high levels of the type 3 iodothyronine deiodinase. In: Journal of Clinical Investigation. 1999. vol. 103, no. 7, p.979–987. https://doi.org/10.1172/JCI6073
GERHARDT Bradley; LEESMAN Lauren; BURRA Kaulini; John SNOWBALL; ROSENZWEIG Rachel; GUZMAN Natalie; AMBALAVANAN Manoj; SINNER Debora. Notum attenuates Wnt/β–catenin signaling to promote tracheal cartilagepatterning. In: Developmental Biology. Febrero 2018. no. 436 p. 14-27 https://doi.org/10.1016/j.ydbio.2018.02.002
GEORGIADES, P.; FERGYSON-SMITH, AC.; BURTON, GJ. Comparative developmental anatomy of the murine and human definitive placentae. In: Placenta. 2002. vol. 23, no. 1, p.3–19. https://doi.org/10.1053/plac.2001.0738
HEMBERGER, Myriam; HANNA, Courtney W.; DEAN, Wendy. Mechanisms of early placental development in mouse and humans. In: Nature Reviews Genetics. 2020. vol. 21, no. 1, p.27–43. https://doi.org/10.1038/s41576-019-0169-4
HERNÁNDEZ, Arturo; MARTINEZ, M. Elena; FIERING, Steven; GALTON, Valerie A.; ST. GERMAIN, Donald. Type 3 deiodinase is critical for the maturation and function of the thyroid axis. In: Journal of Clinical Investigation. February 2006. vol. 116, no. 2, p.476–484. https://doi.org/10.1172/JCI26240
HADDOW, James E.; KNIGHT, George J.; PALOMAKI, Glenn E.; MCCLAIN, Monica R.; PULKKINEN, Andrea J. The reference range and within-person variability of thyroid stimulating hormone during the first and second trimesters of pregnancy. In: J Med Screen. 2004. vol. 11, no. 4. p. 170-174. https://doi.org/10.1258/0969141042467340
HUANG, Stephen A.; DORFMAN, David M.; GENEST, David R.; SALVATORE, Domenico; LARSEN, P. Reed. Type 3 iodothyronine deiodinase is highly expressed in the human uteroplacental unit and in fetal epithelium. In: Journal of Clinical Endocrinology and Metabolism. March 2003. vol. 88, no. 3, p.1384–1388. https://doi.org/10.1210/jc.2002-021291
HUANG, Tien-Shang; CHOPRA, Inder J.; BOADO, Ruben; SOLOMON, David H.; TECO, Guadalupe NC. Thyroxine Inner Ring Monodeiodinating Activity in Fetal Tissues of the Rat. In: Pediatric Research. 1988. vol. 23, no. 2, p.196–199. https://www.nature.com/articles/pr1988240
HUANG, Tien Shang; BEREDO, Angelita; SOLOMON, David H.; CHOPRA, Inder J. The inner ring (5-) monodeiodination of thyroxine (T4) in cerebral cortex during fetal, neonatal, and adult life. In: Metabolism. 1986. vol. 35, no. 3, p.272–277. https://doi.org/10.1016/0026-0495(86)90213-1
HUANG, Tien S.; CHOPRA, Inder J.; BEREDO, Angelita; SOLOMON, David H.; CHUA TECO, Chua N. Skin is an active site for the inner ring monodeiodination of thyroxine to 3, 3′, 5′-triiodothyronine. In: Endocrinology. 1985. vol. 117, no. 5, p.2106–2113. https://doi.org/10.1210/endo-117-5-2106
KALKUNTE, Satyan S.; NEUBECK, Stefan; NORRIS, Wendy E.; CHENG, Shi B; KOSTADINOV, Stefan; VU HOANG, Dang; AHMED, Aftab; VON EGGELING, Ferdinand; SHAIKH, Zahir; PADBURY, James; BERG, Gogran; OLOFSSON, Anders; MARKERT, Udo R.; SHARMA, Surendra. Transthyretin is dysregulated in preeclampsia, and its native form prevents the onset of disease in a preclinical mouse model. In: American Journal of Pathology. November 2013. vol. 183, no. 5, p.1425–1436. https://doi.org/10.1016/j.ajpath.2013.07.022
KNÖFLER, Martin; HAIDER, Sandra; SALEH, Leila; POLLHEIMER, Jurgen; GAMAGE, Teena K. J. B.; JAMES, Joanna. Human placenta and trophoblast development: key molecular mechanisms and model systems. In: Cellular and Molecular Life Sciences. September 2019. vol. 76, no. 18, p.3479–3496. https://doi.org/10.1007/s00018-019-03104-6
KOOPDONK-KOOL, Jolanda M.; DE VIJLDER, Jan JM.; VEENBOER, Geertruda JM.; RIS-STALPERS, Carrie; KOK, Joke H.; WLSMA, Thomas; BOER, Kees; VISSER, Theo J.; VULSMA, Thomas. Type II and Type III Deiodinase Activity in Human Placenta as a Function of Gestational Age. In: The Journal of Clinical Endocrinology and Metabolism. 1996. vol. 81, no. 6, p.2154–2158.
LANDERS, KA.; MORTIMER, RH.; RICHARD, K. Transthyretin and the human placenta. In: Placenta. July 2013. vol. 34, no. 7, p.513–517. https://doi.org/10.1016/j.placenta.2013.04.013
LANDERS, Kelly A.; LI, Huika; MORTIMER, Robin H.; MCLEOD, Donald S. A.; D’EMDEN, Michael C.; RICHARD, Kerry. Transthyretin uptake in placental cells is regulated by the high-density lipoprotein receptor, scavenger receptor class B member 1. In: Molecular and Cellular Endocrinology. 2018. vol. 474, p.89–96. https://doi.org/10.1016/j.mce.2018.02.014
LIU, Ai-Xia; JIN, Fan; ZHANG, Wu-Wen; ZHOU, Tian-Hua; ZHOU, Cai-Yun; YAO, Wei-Miao; QIAN, Yu-Li; HUANG, He-Feng. Proteomic Analysis on the Alteration of Protein Expression in the Placental Villous Tissue of Early Pregnancy Loss. In: Biology of Reproduction. September 2006. vol. 75, no. 3, p.414–420. https://doi.org/10.1095/biolreprod.105.049379
LIU, Yan Y.; BRENT, Gregory A. Thyroid hormone and the brain: Mechanisms of action in development and role in protection and promotion of recovery after brain injury. In: Pharmacology and Therapeutics. June 2018. vol. 186, p.176–185. https://doi.org/10.1016/j.pharmthera.2018.01.007
LOUBIÈRE, Laurence S.; VASILOPOULOU, Elisavet; GLAZIER, Jocelyn D.; TAYLOR, Prter M.; FRANKLYN, Jayne A.; KILBY, Mark D.; CHAN, Shiao Y. Expression and Function of Thyroid Hormone Transporters in the Microvillous Plasma Membrane of Human Term Placental Syncytiotrophoblast. In: Endocrinology. December 2012. vol. 153, no. 12, 1. p. 6126-6135 https://doi.org/10.1210/en.2012-1753
MA, Xiao-Peng; LIU, Chong-Dong; CAO, Guang-Ming; ZHANG, Zhen-Yu. Transthyretin increases migration and invasion of ratplacental trophoblast cells. In: FEBS Open Bio. June, 2020. vol. 10, no. 8. p. 1568–1576 https://doi.org/10.1002/2211-5463.12911
MALTEPE, Emin; BAKARDJIEV, Anna I.; FISHER, Susan J. The placenta: transcriptional, epigenetic, and physiological integration during development. In: The Journal of Clinical Investigation. April, 2010.vol. 120, no.4. p. 1016-1025. https://doi.org/10.1172/JCI41211
MALASSINÉ, André; FRENDO, Jean Louis; EVAIN-BRION, Danièle. A comparison of placental development and endocrine functions between the human and mouse model. In: Human Reproduction Update. November 2003. vol. 9, no 6. p. 531 539. https://doi.org/10.1093/humupd/dmg043
MARUO, Takeshi. Progesterone, thyroid hormone and relaxin in the regulation of the invasive potential of extravillous trophoblasts in early placental development. In: Gynecological Endocrinology. September 2010. vol. 26, no. 9, p.629–630. https://doi.org/10.3109/09513590.2010.492966
MCKINNON, Brett; LI, Huika; RICHARD, Kerry; MORTIMER, Robin. Synthesis of thyroid hormone binding proteins transthyretin and albumin by human trophoblast. In: Journal of Clinical Endocrinology and Metabolism. 2005. vol. 90, no. 12, p.6714–6720. https://doi.org/10.1210/jc.2005-0696
MIRANDA, Alexandra; SOUSA, Nuno. Maternal hormonal milieu influence on fetal brain development. In: Brain and Behavior. February 2018. vol. 8, no. 2, p.1–23. https://doi.org/10.1002/brb3.920
MOLETI, Mariacarla; DI MAURO, Maria; STURNIOLO, Giacomo; RUSSO, Marco; VERMIGLIO, Francesco. Hyperthyroidism in the pregnant woman: Maternal and fetal aspects. In: Journal of Clinical and Translational Endocrinology. June 2019. vol. 16, p.2–7. https://doi.org/10.1016/j.jcte.2019.100190
MOOG, Nora K.; ENTRINGER, Sonja; HEIM, Christine; WADHWA, Pathik D.; KATHMANN, Norbert; BUSS, Claudia. Influence of maternal thyroid hormones during gestation on fetal brain development. In: Neuroscience. February 2017. vol. 342, p.68–100. https://doi.org/10.1016/j.neuroscience.2015.09.070
PATEL, Jatin; LANDERS, Kelly A.; LI, Huika; MORTIMER, Robin H.; RICHARD, Kerry. Ontogenic changes in placental transthyretin. In: Placenta. November 2011a. vol. 32, no. 11, p.817–822. https://doi.org/10.1016/j.placenta.2011.09.007
PATEL, Jatin; LANDERS, Kelly; LI, Huika; MORTIMER, Robin H.; RICHARD, Kerry. Delivery of maternal thyroid hormones to the fetus. In: Trends in Endocrinology and Metabolism. May 2011b. In Trends in Endocrinology and Metabolism vol. 22, no. 5, p. 164–170. https://doi.org/10.1016/j.tem.2011.02.002
PENG, Shiqiao; LI, Chenyan; XIE, Xiaochen; ZHANG, Xiaomei; WANG, Danyang; LU, Xixuan; SUN, Manni; MENG, Tao; WANG, Shiwei; JIANG Yaqiu; SHAN, Zhongyan; TENG, Weiping. Divergence of Iodine and Thyroid Hormones in the Fetal and Maternal Parts of Human-Term Placenta. In: Biol Trace Elem Res. May, 2020 vol. 195. p. 27-38. https://doi.org/10.1007/s12011-019-01834-z
SONCIN, Francesa; KHATER, Marwa; TO, Cuong; PIZZO, Donald; FARAH, Omar; WAKELAND, Anna; RAJAN, Kanaga AN.; NELSON, Katharine K. ; CHANG, Ching W. ; MORETTO-ZITA, Matteo; NATALE, David R.; LAURENT, Louise C.; PARAST, Mana M. Comparative analysis of mouse and human placentae across gestation reveals species-specific regulators of placental development. In: Development. 2018. vol. 145, no. 2, p.1–13. https://doi.org/10.1242/dev.156273
TONG, Mancy; CHENG, Shi B.; CHEN, Qi; DESOUSA, Joana; STONE, Peter R.; JAMES, Joanna L.; CHAMLEY, Lawrence W.; SHARMA, Surendra. Aggregated transthyretin is specifically packaged into placental nano-vesicles in preeclampsia. In: Scientific Reports. 2017. vol. 7, no. 1, p.1–9. https://doi.org/10.1038/s41598-017-07017-x
WATSON, Erica D.; CROSS, James C. Development of structures and transport functions in the mouse placenta. In: Physiology. June 2005. vol. 20, no. 3, p.180–193. https://doi.org/10.1152/physiol.00001.2005
ZIEGELMÜLLER, Brigitte; VATTAI, Aurelia; KOST, Bernd; KUHN, Christina; HOFMANN, Simone; BAYER, Birgit; TOTH, Bettina; JESCHKE, Udo; DITSCH, Nina. Expression of Thyroid Hormone Receptors in Villous Trophoblasts and Decidual Tissue at Protein and mRNA Levels Is Downregulated in Spontaneous and Recurrent Miscarriages. March, 2015. vol. 63, no.7. p. 511-523 https://doi.org/10.1369/0022155415582052
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