Effects of voluntary exercise on testicular histopathological changes in the offspring of hypothyroid rats

authors:

avatar Jafar Amirsadat , avatar Manouchehr Safari , avatar Abbas Ali Vafaei , avatar Behpour Yousefi , avatar A. li Rashidy Pour , avatar Hamid Reza Sameni ORCID , *

Koomesh: Vol.20, issue 3; 575-581
published online: September 01, 2018
article type: Research Article
received: March 09, 2017
accepted: December 01, 2017

how to cite: Amirsadat J, Safari M, Vafaei A A, Yousefi B, Rashidy Pour A L, et al. Effects of voluntary exercise on testicular histopathological changes in the offspring of hypothyroid rats. koomesh. 2018;20(3):e152996. 

Abstract

Introduction: Thyroid  hormones  play a  key  role  in  the  evolution  of  various  body systems. Relatively, maternal hypothyroidism results in structural and functional changes in the testis by decreasing thyroid hormones. Exercise can potentially improve these changes by increasing thyroid hormones. The purpose of this study was to investigate the effect of voluntary exercise on histopathological changes in testies in children of hypothyroid rats. Materials and Methods: In this experimental study 40 female Wistar rats were randomly divided into four groups by age 30 days: control-sedentary, control-voluntary exercise, hypothyroidism-sedentary, and hyperthyroidism - voluntary exercise. The total experiments started of the day 30 after birth and ended the day 44 after birth. Hypothyroidism was created using anti-thyroid drug 6-propyl 2-thiouracil from day 6 of pregnancy to day 21 after birth with the addition of the drinking water. At the end of testing, 5 micrometer sections were prepared from the testicle using a microscope equipped with software to analyze the images of tissue were histomorphometry. Results: Hypothyroidism reduces number of spermatogonia cells, primary spermatocytes cells, leydig cells, and as well as increased sertoli cells in testis.  Hypothyroidism also reduces basement membrane diameter and seminiferous epithelium thickness.  Exercise increases the number spermatogonia cells, primary spermatocytes cells, leydig cells, and as well as reduced sertoli cells in testes. Exercise also increases basement membrane diameter and seminiferous epithelium thickness. Conclusion: This study showed that exercise is likely to substantially prevent the testis from structural and functional changes due to hypothyroidism.

References

  • 1.

    Calvo RM, Jauniaux E, Gulbis B, Asuncion M, Gervy C, Contempre B, Morreale de Escobar G. Fetal tissues are exposed to biologically relevant free thyroxine concentrations during early phases of development. J Clin Endocrinol Metab 2002; 87: 1768-1777.

  • 2.

    Glinoer D. The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 1997; 18: 404-433.

  • 3.

    de Escobar GM, Obregn MJ, del Rey FE. Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab 2004; 18: 225-248.

  • 4.

    Wajner SM, Wagner MS, Maia AL. Clinical implications of altered thyroid status in male testicular function. Arq Bras Endocrinol Metabol 2009; 53: 976-982.

  • 5.

    Roberts CG, Ladenson PW. Hypothyroidism. Lancet 2004; 363: 793-803.

  • 6.

    Morganti S, Ceda GP, Saccani M, Milli B, Ugolotti D, Prampolini R, Maggio M, Valenti G, Ceresini G. Thyroid disease in the elderly: sex-related differences in clinical expression. J Endocrinol Invest 2005; 28: 101-104.

  • 7.

    Lazarus J, Premawardhana L. Best practice NO 184 Screening for thyroid disease in pregnancy. J Clin Pathol 2005; 58: 449-452.

  • 8.

    Wagner MS, Wajner SM, Maia AL. The role of thyroid hormone in testicular development and function. J Endocrinol 2008; 199: 351-365.

  • 9.

    Silva D, Lizama C, Tapia V, Moreno RD. Propylthiouracil-induced hypothyroidism delays apoptosis during the first wave of spermatogenesis. Biol Res 2011; 44: 181-188.

  • 10.

    Holsberger DR, Jirawatnotai S, Kiyokawa H, Cooke PS. Thyroid hormone regulates the cell cycle inhibitor p27Kip1 in postnatal murine Sertoli cells. Endocrinology 2003; 144: 3732-3738.

  • 11.

    Yang Y, Huang H, Ba Y, Cheng XM, Cui LX. Effect of oxidative stress on fluoride-induced apoptosis in primary cultured Sertoli cells of rats. Int J Environ Health Res 2015; 25: 1-9.

  • 12.

    Kumar A, Shekhar S, Dhole B. Thyroid and male reproduction. Indian J Endocrinol Metab 2014; 18: 23-31.

  • 13.

    Sahoo D. Increased germ cell apoptosis during testicular development and maturation by experimentally induced transient and persistent hypothyroidism. http://www.webmedcentral.com 2013; 1-14.

  • 14.

    Yang Y, Huang H, Yuan W, Feng D, Wang Z, Cheng X, Ba Y, Cui L. [Effects of fluoride on oxidative stress and apoptosis in primary culture of rat sertoli cells]. Wei Sheng Yan Jiu 2013; 42: 1004-1007.

  • 15.

    Sahoo DK, Chainy G. Tissue specific response of antioxidant defence systems of rat to experimentally-induced hyperthyroidism. Nat Acad Sci Lett 2007; 30: 247-250.

  • 16.

    Pamplona R, Portero-Otn M, Ruiz C, Bellmunt MJ, Requena JR, Thorpe SR, et al. Thyroid status modulates glycoxidative and lipoxidative modification of tissue proteins. Free Radic Biol Med 1999; 27: 901-910.

  • 17.

    Hamadouche NA, Slimani M, Merad-Boudia B, Zaoui C. Reproductive toxicity of lead acetate in adult male rats. Am J Sci Res 2009; 3: 38-50.

  • 18.

    Reglero MM, Taggart MA, Castellanos P, Mateo R. Reduced sperm quality in relation to oxidative stress in red deer from a lead mining area. Environ Pollut 2009; 157: 2209-2215.

  • 19.

    Iemitsu M, Miyauchi T, Maeda S, Tanabe T, Takanashi M, Matsuda M, Yamaguchi I. Exercise training improves cardiac function-related gene levels through thyroid hormone receptor signaling in aged rats. Am J Physiol Heart Circ Physiol 2004; 286: 1696-1705.

  • 20.

    Ciloglu F, Peker I, Pehlivan A, Karacabey K, Ilhan N, Saygin O, Ozmerdivenli R. Exercise intensity and its effects on thyroid hormones. Neuro Endocrinol Lett 2005; 26: 830-834.

  • 21.

    Karkoulias K, Habeos I, Charokopos N, Tsiamita M, Mazarakis A, Pouli A, Spiropoulos K. Hormonal responses to marathon running in non-elite athletes. Eur J Int Med 2008; 19: 598-601.

  • 22.

    Bogaard JM, Busch HF, Scholte HR, Stam H, Versprille A. Exercise responses in patients with an enzyme deficiency in the mitochondrial respiratory chain. Eur Respir J 1988; 1: 445-452.

  • 23.

    Hajizadeh Maleki B, Tartibian B, Eghbali M, AsriRezaei S. Comparison of seminal oxidants and antioxidants in subjects with different levels of physical fitness. Andrology 2013; 1: 607-614.

  • 24.

    Tartibian B, Maleki BH. Correlation between seminal oxidative stress biomarkers and antioxidants with sperm DNA damage in elite athletes and recreationally active men. Clin J Sport Med 2012; 22: 132-139.

  • 25.

    Rosety MA, Daz AJ, Rosety JM, Pery MT, Brenes-Martn F, Bernardi M, et all. Exercise improved semen quality and reproductive hormone levels in sedentary obese adults. Nutr Hosp 2017; 34: 608-612.

  • 26.

    Hill K, Geist R, Goldstein RS, Lacasse Y. Anxiety and depression in end-stage COPD. Eur Resp J 2008; 31: 667-77.

  • 27.

    Fox JH, Hammack SE, Falls WA. Exercise is associated with reduction in the anxiogenic effect of mCPP on acoustic startle. Behav Neurosci 2008; 122: 943-948.

  • 28.

    Duman CH, Schlesinger L, Russell DS, Duman RS. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 2008; 1199: 148-158.

  • 29.

    Manna I, Jana K, Samanta P. Effect of intensive exerciseinduced testicular gametogenic and steroidogenic disorders in mature male Wistar strain rats: a correlative approach to oxidative stress. Acta Physiol Scand 2003; 178: 33-40.

  • 30.

    du Plessis SS, Kashou A, Vaamonde D, Agarwal A. Is there a link between exercise and male factor infertility. Open Reprod Sci J 2011; 3: 105-113.

  • 31.

    Atalay M, Laaksonen DE. Diabetes, Oxidative Stress and Physical Exercise. J Sport Sci Med 2002; 1: 1-14.

  • 32.

    Adlard PA, Perreau VM, Cotman CW. The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol Aging 2005; 26: 511-520.

  • 33.

    Khanna S, Atalay M, Laaksonen DE, Gul M, Roy S, Sen CK. A-lipoic acid supplementation: tissue glutathione homeostasis at rest and after exercise. J Appl Physiol 1999; 86: 1191-1196.

  • 34.

    Shafiee SM, Vafaei AA, Rashidy-Pour A. Effects of maternal hypothyroidism during pregnancy on learning, memory and hippocampal BDNF in rat pups: Beneficial effects of exercise. Neuroscience. 2016 Aug 4;329:151-61.

  • 35.

    Ghaffari Z, Vafaei AA, Rashidy-Pour A, Hadjzadeh MA, Hosseini SM. Effects of maternal hypothroidism during preganacy on anxiety-like behaviors in adulthood rats: Impact of moderate treadmill exercise. koomesh. 2016 Mar 8:707-17.

  • 36.

    Mokhtari-Zaer A, Ghodrati-Jaldbakhan S, Vafaei AA, Miladi-Gorji H, Akhavan MM, Bandegi AR, Rashidy-Pour A. Effects of voluntary and treadmill exercise on spontaneous withdrawal signs, cognitive deficits and alterations in apoptosis-associated proteins in morphine-dependent rats. Behavioural brain research. 2014 Sep 1;271:160-70.

  • 37.

    Akhavan MM, Miladi-Gorji H, Emami-Abarghoie M, Safari M, Sadighi-Moghaddam B, Vafaei AA, Rashidy-Pour A. Maternal voluntary exercise during pregnancy enhances the spatial learning acquisition but not the retention of memory in rat pups via a TrkB-mediated mechanism: the role of hippocampal BDNF Expression. Iranian journal of basic medical sciences. 2013 Sep;16(9):955-961.

  • 38.

    Pabst DA, Rommel S, Mclellan WA, Williams T, Rowles T. Thermoregulation of the intra-abdominal testes of the bottlenose dolphin (Tursiops truncatus) during exercise. J Exp Biol 1995; 198: 221-226.

  • 39.

    Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat Rev Urol 2010; 7: 153-161.

  • 40.

    de Paula Ramos S, Goessler KF, Ruiz RJ, Ferrari O, Polito MD, Salles MJS. Exercise protects rat testis from cyclophosphamide-induced damage-doi: 10.4025/actascibiolsci. v35i1. 12475. Acta Scient Biol Sci 2012; 35: 105-113.

  • 41.

    Braga AF, Halpern G, Rita de Cssia SF, Setti AS, Iaconelli A, Borges E. Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomes. Fertil Steril 2012; 97: 53-59.

  • 42.

    Hammoud AO, Meikle AW, Reis LO, Gibson M, Peterson CM, Carrell DT. Obesity and male infertility: a practical approach. Semin Reprod Med 2012; 30: 486-495.

  • 43.

    Hkonsen LB, Thulstrup AM, Aggerholm AS, Olsen J, Bonde JP, Andersen CY, Bungum M, et all. Does weight loss improve semen quality and reproductive hormones? Results from a cohort of severely obese men. Reprod Health 2011; 8: 24.

  • 44.

    Freitas KMd, Natali AJ, Lunz W, Costa KLC, Leite RP, Dolder H, Matta SLPd. Colon cancer and swimming exercise: effect on wistar rat testes. Brazil Arch Biol Technol 2013; 56: 557-566.

  • 45.

    Foletto MP, da Costa CEM, Ferrari F, Franzi-de-Moraes SM, Segatelli TM. Effect of the nandrolone decanoate on the efficiency of spermatogenesis of sedentary rats and rats subjected to physical training-DOI: 10.4025/actascihealthsci. v32i1. 5741. Acta Scient Health Sci 2009; 32: 17-22.

  • 46.

    Aiyun LA. An Experimental Study of Endurance Training and Apoptosis in CNS [J]. Sport Sci 2003; 5: 019.

  • 47.

    Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Adv Exp Med Biol 2008; 636: 154-171.

  • 48.

    Joseph AM, Nguyen LD, Welter A, Dominguez II J, Behnke B, Adhihetty P. Mitochondrial adaptations evoked with exercise are associated with a reduction in age-induced testicular atrophy in Fischer-344 rats. Biogerontology 2014; 15: 517-534.

  • 49.

    Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007; 30: 464-472.

  • 50.

    Sahoo DK, Roy A. Compromised Rat Testicular Antioxidant Defence System by Hypothyroidism before Puberty. Int J Endocrinol 2012; 2012: 1-11.

  • 51.

    Mendis-Handagama SM, Ariyaratne HB. Effects of thyroid hormones on Leydig cells in the postnatal testis. Histol Histopathol 2004; 19: 985-997.##.