Adrenal and thyroid morphogenesis during prenatal development in red Sokoto goats (Capra hircus)

Contenido principal del artículo

Anietie Francis Udoumoh
Innocent Chima Nwaogu
Offordile Udu Elom

Resumen

The morphological development of the adrenal and thyroid glands was evaluated in fetuses of Red Sokoto goats (Capra hircus) using anatomical techniques. Forty apparently healthy pregnant goats were grouped into first term (0–50 days), early second term (51–75 days), late second term (76–100 days), and third term (101–150 days). The oval, light-pink, paired adrenal glands showed poorly formed parenchymal zones by fetal day (FD) 57. By FD 69, the cortex and medulla were formed, and their thickness increased steadily with age. At FD 102, the adrenal cortex exhibited thin outer, middle, and inner layers, while the adrenal medulla changed from naive cords of cells in the early second term to pale-staining cords bounded by wide sinusoidal spaces towards full term. Thyroid follicle diameter increased linearly with age, with widening lumina filled with colloid. Follicular epithelium consisted mostly of follicular cells; later in the third term, parafollicular cells appeared singly or in clusters within interfollicular connective tissue. These structural changes suggest that the adrenal gland is prepared for adult function, and the thyroid assumes adult morphology early in fetal life, essential for normal physiology in fetuses and postnatally.

Palabras clave:
Fetal adrenal gland development, Thyroid gland morphogenesis, Prenatal development in goats, Red Sokoto goats, Fetal histomorphology, Capra hircus embryology

Detalles del artículo

Citas

Xing Y, Lerario AM, Rainey W, Hammer GD. Development of adrenal cortex zonation. Endocrinology and Metabolism Clinics of North America. 2015;44(2):243–274. doi.org/10.1016/j.ecl.2015.02.001. DOI: https://doi.org/10.1016/j.ecl.2015.02.001

Brant WE. Adrenal glands. In: WR Webb, WE Brant, NM Major, editors. Fundamentals of body CT. 3rd edition. Philadelphia, US: WB Saunders; 2006. pp. 303–318. doi.org/10.1016/B978-1-4160-0030-3.00016-0. DOI: https://doi.org/10.1016/B978-1-4160-0030-3.00016-0

Harbuz MS. Neuroendocrine function and chronic inflammatory stress. Experimental Physiology. 2002;87(5):519–525. doi.org/10.1113/eph8702411. DOI: https://doi.org/10.1113/eph8702411

Hoeflich A, Bielohuby M. Mechanisms of adrenal gland growth: signal integration by extracellular signal regulated kinases1/2. Journal of Molecular Endocrinology. 2009;42(3):191–203. doi.org/10.1677/JME-08-0160. DOI: https://doi.org/10.1677/JME-08-0160

Kim J, Choi MH. Embryonic development and adult regeneration of the adrenal gland. Endocrinology and Metabolism. 2020;35(4):765–773. doi.org/10.3803/EnM.2020.403. DOI: https://doi.org/10.3803/EnM.2020.403

Burford NG, Webster NA, Cruz-Topete D. Hypothalamic-Pituitary-Adrenal Axis modulation of glucocorticoids in the cardiovascular system. International Journal of Molecular Sciences. 2017;18(10):2150. doi.org/10.3390/ijms18102150. DOI: https://doi.org/10.3390/ijms18102150

Pignatti E, du Toit T, Flück CE. Development and function of the fetal adrenal. Reviews in Endocrine and Metabolic Disorders. 2023;24(1):5–21. doi.org/10.1007/s11154-022-09756-3. DOI: https://doi.org/10.1007/s11154-022-09756-3

Rosen RD, Sapra A. Embryology, thyroid. Treasure Island, FL, US: StatPearls Publishing; 2023. https://www.ncbi.nlm.nih.gov/books/NBK551611/

Hossam HA, Mohammad MA, Mona SZ, Gamal FM. Effect of seasonal temperature changes on thyroid structure and hormones secretion of white grouper (Epinephelus aeneus) in Suez Gulf. Life Science Journal. 2012;9(2):700–705.

Choksi NY, Jahnke GD, St. Hilaire C, Shelby M. Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Research Part B: Developmental and Reproductive Toxicology. 2003;68(6):479–491. doi.org/10.1002/bdrb.10045. DOI: https://doi.org/10.1002/bdrb.10045

Jara EL, Muñoz-Durango N, Llanos C, Fardella C, González PA, Bueno SM, et al. Modulating the function of the immune system by thyroid hormones and thyrotropin. Immunology Letters. 2017;184:76–83. doi.org/10.1016/j.imlet.2017.02.010. DOI: https://doi.org/10.1016/j.imlet.2017.02.010

Yamakawa H, Kato TS, Noh JY, Yuasa S, Kawamura A, Fukuda K, et al. Thyroid hormone plays an important role in cardiac function: from bench to bedside. Frontiers in Physiology. 2021;12:606931. doi.org/10.3389/fphys.2021.606931h. DOI: https://doi.org/10.3389/fphys.2021.606931

Buffenstein R, Woodley R, Thomadakis C, Daly TJ, Gray DA. Cold-induced changes in thyroid function in a poikilothermic mammal, the naked mole-rat. American Journal of Physiology-Regulatory Integrative and Comparative Physiology. 2001;280(1):R149–R155. doi.org/10.1152/ajpregu.2001.280.1.R149. DOI: https://doi.org/10.1152/ajpregu.2001.280.1.R149

Rosol TJ, DeLellis RA, Philip W, Harvey PW, Sutcliffe C. Endocrine system. In: WM Haschek, CG Rousseaux, MA Wallig, editors. Haschek and Rousseaux’s Handbook of Toxicologic Pathology. 3rd edition. San Diego, California, US: Academic Press; 2013. pp. 2391–2492. doi.org/10.1016/B978-0-12-415759-0.00058-3. DOI: https://doi.org/10.1016/B978-0-12-415759-0.00058-3

Missero C, Cobellis G, de Felice M, Lauro R. Molecular events involved in differentiation of thyroid follicular cells. Molecular and Cellular Endocrinology. 1998;140(1–2):37–43. doi.org/10.1016/S0303-7207(98)00027-6. DOI: https://doi.org/10.1016/S0303-7207(98)00027-6

Morillo-Bernal J, Fernández-Santos JM, Utrilla JC, de Miguel M, García-Marín R, Martín-Lacave I. Functional expression of the thyrotropin receptor in C cells: new insights into their involvement in the hypothalamic-pituitary-thyroid axis. Journal of Anatomy. 2009;215(2):150–158. doi.org/10.1111/j.1469-7580.2009.01095.x. DOI: https://doi.org/10.1111/j.1469-7580.2009.01095.x

Ali SA, El-Sayed SA, Goda NIA, Beheiry RR. Morphological characteristics of the goat thyroid glands among summer and winter seasons. Advances in Animal and Veterinary Sciences. 2020;8(3):252–259. doi.org/10.17582/journal.aavs/2020/8.3.252.259. DOI: https://doi.org/10.17582/journal.aavs/2020/8.3.252.259

Egwu OC, Samuel UC, Philip BD, Okekeaji U, Eze CC. Evaluation of microbial loads, parasites and antinutrient factors in Talinum triangulare grown on sewage dump site in University of Nigeria, Nsukka Nigeria. IOSR Journal of Environmental Science, Toxicology and Food Technology. 2019;13(5):51–58.

Gall CF, Stier CH, Frahm K. Age estimation of goat fetus. Small Ruminant Research. 1994;14(1):91–94. doi.org/10.1016/0921-4488(94)90016-7. DOI: https://doi.org/10.1016/0921-4488(94)90016-7

Pathak SK, Farooqui MM, Kumar P, Prakash A, Pathak A, Singh D. Gross anatomical studies on the adrenal gland in prenatal goat (Capra hircus). International Journal of Morphology. 2014;32(1):131–135. doi.org/10.4067/S0717-95022014000100023. DOI: https://doi.org/10.4067/S0717-95022014000100022

Kumar V, Sharma A. Gross morphometric study on postnatal development of adrenal gland in Gohilwadi goat (Capra hircus). The Indian Journal of Veterinary Sciences & Biotechnology. 2017;12(3):96–98. DOI: https://doi.org/10.21887/ijvsbt.v12i3.7105

Suri S, Kour G, Sasan JS. Histomorphology and histochemistry of adrenal cortex of adult Bakerwali goat of Jammu region. Journal of Livestock Science. 2022;13(2):80–87. doi.org/10.33259/JLivestSci.2022.80-87. DOI: https://doi.org/10.33259/JLivestSci.2022.80-87

Paul B, Sarkar S, Islam MN, Das R. Morphological and histological investigations on the adrenal glands in black Bengal goat (Capra hircus). Journal of Sylhet Agricultural University. 2016;3(2):181–187.

Özgüner G, Sulak O, Koyuncu E. A morphometric study of suprarenal gland development in the fetal period. Surgical and Radiologic Anatomy. 2012;34(7):581–587. doi.org/10.1007/s00276-012-0959-2. DOI: https://doi.org/10.1007/s00276-012-0959-2

Bechmann N, Berger I, Bornstein SR, Steenblock C. Adrenal medulla development and medullary-cortical interactions. Molecular and Cellular Endocrinology. 2021;528:111258. doi.org/10.1016/j.mce.2021.111258. DOI: https://doi.org/10.1016/j.mce.2021.111258

Saxena R, Yang Y, Gu HF. Asymmetries of left and right adrenal glands in neural innervation and glucocorticoids production. International Journal of Molecular Sciences. 2023;24(24):17456. doi.org/10.3390/ijms242417456. DOI: https://doi.org/10.3390/ijms242417456

Einer-Jensen N, Carter AM. Local transfer of hormones between blood vessels within the adrenal gland may explain the functional interaction between the adrenal cortex and medulla. Medical Hypotheses. 1995;44(6):471–474. doi.org/10.1016/0306-9877(95)90508-1. DOI: https://doi.org/10.1016/0306-9877(95)90508-1

Nicolaides NC, Willenberg HS, Bornstein SR, Chrousos GP. Adrenal cortex: embryonic development, anatomy, histology and physiology. In: KR Feingold, MR Anawalt B, Blackman, A Boyce, G Chrousos, E Corpas, et al., editors. Endotext. South Dartmouth, MA: MDText.com, Inc.; 2023. https://www.ncbi.nlm.nih.gov/books/NBK278928/

Hoermann H, van Faassen M, Roeper M, Hagenbeck C, Herebian D, Müller Kobold AC, et al. Association of fetal catecholamines with neonatal hypoglycemia. JAMA Pediatrics. 2024;178(6):577–585. doi.org/10.1001/jamapediatrics.2024.0304. DOI: https://doi.org/10.1001/jamapediatrics.2024.0304

Copper RL, Goldenberg RL. Catecholamine secretion in fetal adaptation to stress. Journal of Obstetric, Gynecologic & Neonatal Nursing. 1990;19(3):223–226. doi.org/10.1111/j.1552-6909.1990.tb01641.x. DOI: https://doi.org/10.1111/j.1552-6909.1990.tb01640.x

Rakers F, Bischoff S, Schiffner R, Haase M, Rupprecht S, Kiehntopf M, et al. Role of catecholamines in maternal-fetal stress transfer in sheep. American Journal of Obstetrics and Gynecology. 2015;213(5):684.e1–684.e9. doi.org/10.1016/j.ajog.2015.07.020. DOI: https://doi.org/10.1016/j.ajog.2015.07.020

Jevtić P, Edens LJ, Vuković LD, Levy DL. Sizing and shaping the nucleus: mechanisms and significance. Current Opinion in Cell Biology. 2014;28:16–27. doi.org/10.1016/j.ceb.2014.01.003ht. DOI: https://doi.org/10.1016/j.ceb.2014.01.003

Naaman Répérant E, Durand P. The development of the ovine fetal adrenal gland and its regulation. Reproduction Nutrition Development. 1997;37(1):81–95. doi.org/10.1051/rnd:19970109. DOI: https://doi.org/10.1051/rnd:19970109

Auchus RJ. Adrenal gland. In: MJ Aminoff, RB Daroff, editors. Encyclopedia of the Neurological Sciences. 2nd edition. San Diego, California, US: Academic Press; 2014. pp. 61–64. DOI: https://doi.org/10.1016/B978-0-12-385157-4.01205-7

Huang CC, Kang Y. The transient cortical zone in the adrenal gland: the mystery of the adrenal X-zone. Journal of Endocrinology. 2019;241(1):R51–R63. doi.org/10.1530/JOE-18-0632. DOI: https://doi.org/10.1530/JOE-18-0632

La Perle KMD, Dintzis SM. Endocrine system. In: PM Treuting, SM Dintzis, KS Montine, editors. Comparative Anatomy and Histology. 2nd edition. San Diego, California, US: Academic Press; 2018. pp. 251–273. doi.org/10.1016/B978-0-12-802900-8.00015-4. DOI: https://doi.org/10.1016/B978-0-12-802900-8.00015-4

Soliman SM, Nabil TM, El-Kerdawy AZ, El-Bayomy AM. Development of the thyroid gland of New-Zealand white rabbit. Beni-Suef Veterinary Medical Journal. 2005;15(2):1–8. DOI: https://doi.org/10.21608/jvmr.2005.77924

Obregon MJ, Calvo RM, del Rey FE, de Escobar GM. Ontogenesis of thyroid function and interactions with maternal function. Endocrine Development. 2007;10:86–98. doi.org/10.1159/000106821. DOI: https://doi.org/10.1159/000106821

Patel J, Landers K, Li H, Mortimer RH, Richard K. Thyroid hormones and fetal neurological development. Journal of Endocrinology. 2011;209(1):1–8. doi.org/10.1530/JOE-10-0444. DOI: https://doi.org/10.1530/JOE-10-0444

Moog NK, Entringer S, Heim C, Wadhwa PD, Kathmann N, Buss C. Influence of maternal thyroid hormones during gestation on fetal brain development. Neuroscience. 2017;342:68–100. doi.org/10.1016/j.neuroscience.2015.09.070. DOI: https://doi.org/10.1016/j.neuroscience.2015.09.070

Krause WJ, Cutts JH. Post-natal development of the thyroid gland in the opossum (Didelphis virginiana). Acta Anatomica. 1983;116(4):322–338. doi.org/10.1159/000145760. DOI: https://doi.org/10.1159/000145757

Das SS, Mishra S, Kaul JM. Development of parafollicular cells and their relationship with developing thyroid follicles in human foetuses. Journal of Clinical and Diagnostic Research. 2017;11(7):AC01–AC04. doi.org/10.7860/JCDR/2017/26211.10225. DOI: https://doi.org/10.7860/JCDR/2017/26211.10225

White CP. Calcium metabolism in pregnancy and lactation. Obstetric Medicine. 2009;2(1):2–5. doi.org/10.1258/om.2008.080013. DOI: https://doi.org/10.1258/om.2008.080013

Kiriakopoulos A, Giannakis P, Menenakos E. Calcitonin: current concepts and differential diagnosis. Therapeutic Advances in Endocrinology and Metabolism. 2022;13:20420188221099344. doi.org/10.1177/20420188221099344. DOI: https://doi.org/10.1177/20420188221099344