open access

Vol 79, No 3 (2020)
Original article
Submitted: 2019-06-28
Accepted: 2019-08-27
Published online: 2019-09-03
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Aging changes of the testis in albino rat: light, electron microscopic, morphometric, immunohistochemical and biochemical study

S. M. Hussein1, A. B. El-Fadaly1, A. G. Metawea1, B. E. A. Khaled12
·
Pubmed: 31489605
·
Folia Morphol 2020;79(3):503-515.
Affiliations
  1. Department of Anatomy and Embryology, Faculty of Medicine, Cairo University, Cairo, Egypt
  2. Department of Anatomy, College of Medicine, Jouf University, Skaka, AlJouf, Saudi Arabia

open access

Vol 79, No 3 (2020)
ORIGINAL ARTICLES
Submitted: 2019-06-28
Accepted: 2019-08-27
Published online: 2019-09-03

Abstract

Background: Aging has a deleterious effect on the morphology of the male reproductive system which might, in turn, lead to changes in spermatogenesis and consequently, decrease in both quality and quantity of spermatozoa.

Materials and methods: The present study elucidated the histological and ultrastructural changes of testes of adult albino rats during aging and applied morphometric measures to obtain quantitative data for these changes. The oxidative and antioxidative markers of aged testes were also assessed.

Results: The results documented the presence of age-related regressive structural changes of the testis accompanied with an increase in the apoptosis and a decrease in the proliferative capacity.

Conclusions: The biochemical results gave evidence of an imbalance between the oxidative damage and the antioxidant defence indicating increased oxidative stress of aged testis.

Abstract

Background: Aging has a deleterious effect on the morphology of the male reproductive system which might, in turn, lead to changes in spermatogenesis and consequently, decrease in both quality and quantity of spermatozoa.

Materials and methods: The present study elucidated the histological and ultrastructural changes of testes of adult albino rats during aging and applied morphometric measures to obtain quantitative data for these changes. The oxidative and antioxidative markers of aged testes were also assessed.

Results: The results documented the presence of age-related regressive structural changes of the testis accompanied with an increase in the apoptosis and a decrease in the proliferative capacity.

Conclusions: The biochemical results gave evidence of an imbalance between the oxidative damage and the antioxidant defence indicating increased oxidative stress of aged testis.

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Keywords

aging, testis, morphological changes; oxidative markers; ultrastructure; proliferative cell nuclear antigen (PCNA); apoptosis (caspase-3)

About this article
Title

Aging changes of the testis in albino rat: light, electron microscopic, morphometric, immunohistochemical and biochemical study

Journal

Folia Morphologica

Issue

Vol 79, No 3 (2020)

Article type

Original article

Pages

503-515

Published online

2019-09-03

Page views

1680

Article views/downloads

1482

DOI

10.5603/FM.a2019.0102

Pubmed

31489605

Bibliographic record

Folia Morphol 2020;79(3):503-515.

Keywords

aging
testis
morphological changes
oxidative markers
ultrastructure
proliferative cell nuclear antigen (PCNA)
apoptosis (caspase-3)

Authors

S. M. Hussein
A. B. El-Fadaly
A. G. Metawea
B. E. A. Khaled

References (49)
  1. Beattie MC, Chen H, Fan J, et al. Aging and luteinizing hormone effects on reactive oxygen species production and DNA damage in rat Leydig cells. Biol Reprod. 2013; 88(4): 100.
  2. Buege J, Aust S. [30] Microsomal lipid peroxidation. Methods Enzymol. 1978: 302–310.
  3. Chen H, Zirkin BR. Long-term suppression of Leydig cell steroidogenesis prevents Leydig cell aging. Proc Natl Acad Sci U S A. 1999; 96(26): 14877–14881.
  4. Creasy D, Bube A, de Rijk E, et al. Proliferative and nonproliferative lesions of the rat and mouse male reproductive system. Toxicol Pathol. 2012; 40(6 Suppl): 40S–40121S.
  5. Crowley C, Gillham B, Thorn M. A direct enzymic method for the determination of reduced glutathione in blood and other tissues. Biochem Med. 1975; 13(3): 287–292.
  6. Dakouane M, Bicchieray L, Bergere M, et al. A histomorphometric and cytogenetic study of testis from men 29-102 years old. Fertil Steril. 2005; 83(4): 923–928.
  7. Desai N, Sabanegh E, Kim T, et al. Free radical theory of aging: implications in male infertility. Urology. 2010; 75(1): 14–19.
  8. Drew B, Leeuwenburgh C. Aging and the role of reactive nitrogen species. Ann N Y Acad Sci. 2002; 959: 66–81.
  9. Foley JF, Dietrich DR, Swenberg JA, et al. Detection and evaluation of proliferating cell nuclear antigen (PCNA) in rat tissue by an improved immunohistochemical procedure. J Histotechnol. 1991; 14(4): 237–241.
  10. Frungieri MB, Calandra RS, Bartke A, et al. Ageing and inflammation in the male reproductive tract. Andrologia. 2018; 50(11): e13034.
  11. Fu L, Chen YH, Xu S, et al. Vitamin D deficiency impairs testicular development and spermatogenesis in mice. Reprod Toxicol. 2017; 73: 241–249.
  12. Goedken MJ, Kerlin RL, Morton D. Spontaneous and age-related testicular findings in beagle dogs. Toxicol Pathol. 2008; 36(3): 465–471.
  13. Gofur MR, Khan M, Karim MR, et al. Histomorphology and histochemistry of testis of indigenous bull (Bos indicus) of Bangladesh. Bangladesh J Vet Med. 1970; 6(1): 67–74.
  14. Golalipour MJ, Azarhoush R, Ghafari S, et al. Formaldehyde exposure induces histopathological and morphometric changes in the rat testis. Folia Morphol. 2007; 66(3): 167–171.
  15. Green L, Wagner D, Glogowski J, et al. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem. 1982; 126(1): 131–138.
  16. Gunes S, Hekim GN, Arslan MA, et al. Effects of aging on the male reproductive system. J Assist Reprod Genet. 2016; 33(4): 441–454.
  17. Hikim AP, Vera Y, Vernet D, et al. Involvement of nitric oxide-mediated intrinsic pathway signaling in age-related increase in germ cell apoptosis in male Brown-Norway rats. J Gerontol A Biol Sci Med Sci. 2005; 60(6): 702–708.
  18. Horn R, Pastor LM, Moreno E. Morphological and morphometric study of early changes in the ageing golden hamster testis. J Anat. 1996; 188(1): 109–117.
  19. Jiang H, Zhu WJ, Li J, et al. Quantitative histological analysis and ultrastructure of the aging human testis. Int Urol Nephrol. 2014; 46(5): 879–885.
  20. Johnson L, Petty CS, Neaves WB. Influence of age on sperm production and testicular weights in men. J Reprod Fertil. 1984; 70(1): 211–218.
  21. Kim JM, Ghosh SR, Weil AC, et al. Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinology. 2001; 142(9): 3809–3816.
  22. Kühnert B, Nieschlag E. Reproductive functions of the ageing male. Hum Reprod Update. 2004; 10(4): 327–339.
  23. Lee JD, Lee TH, Cheng WH, et al. Involved intrinsic apoptotic pathway of testicular tissues in varicocele-induced rats. World J Urol. 2009; 27(4): 527–532.
  24. Levy S, Serre V, Hermo L. The effects of aging on the seminiferous epithelium and the blood — testis barrier of the Brown Norway rat. J Androl. 1999; 20(3): 356–365.
  25. Lobo V, Patil A, Phatak A, et al. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev. 2010; 4(8): 118–126.
  26. Matzkin ME, Miquet JG, Fang Y, et al. Alterations in oxidative, inflammatory and apoptotic events in short-lived and long-lived mice testes. Aging (Albany NY). 2016; 8(1): 95–110.
  27. Merendino RA, Salvo F, Saija A, et al. Malondialdehyde in benign prostate hypertrophy: a useful marker? Mediators Inflamm. 2003; 12(2): 127–128.
  28. Morales E, Horn R, Pastor LM, et al. Involution of seminiferous tubules in aged hamsters: an ultrastructural, immunohistochemical and quantitative morphological study. Histol Histopathol. 2004; 19(2): 445–456.
  29. Neuman SL, Lin TL, Heste PY. The effect of dietary carnitine on semen traits of white Leghorn roosters. Poult Sci. 2002; 81(4): 495–503.
  30. Paniagua R, Martinez-Onsurbe P, Santamaria L, et al. Quantitative and ultrastructural alterations in the lamina propria and Sertoli cells in human cryptorchid testes. Int J Androl. 1990; 13(6): 470–487.
  31. Paniagua R, Nistal M, Sáez FJ, et al. Ultrastructure of the aging human testis. J Electron Microsc Tech. 1991; 19(2): 241–260.
  32. Pastor LM, Zuasti A, Ferrer C, et al. Proliferation and apoptosis in aged and photoregressed mammalian seminiferous epithelium, with particular attention to rodents and humans. Reprod Domest Anim. 2011; 46(1): 155–164.
  33. Paulson RJ, Milligan RC, Sokol RZ. The lack of influence of age on male fertility. Am J Obstet Gynecol. 2001; 184(5): 818–22; discussion 822.
  34. Perheentupa A, Huhtaniemi I. Aging of the human ovary and testis. Mol Cell Endocrinol. 2009; 299(1): 2–13.
  35. Pop OT, Cotoi CG, Plesea IE. Histological and ultrastructural analysis of the seminiferous tubule wall in ageing testis. Rom J Morphol Embryol. 2011; 52(1): 241–248.
  36. Pop OT, Cotoi CO, Plesea IE. Correlations between intralobular interstitial morphological changes and epithelial changes in ageing testis. Rom J Morphol Emryol. 2011; 52(1): 339–347.
  37. Russell L, Ettlin R, Hikim A, et al. Histological and histopathological evaluation of the testis. Int J Androl. 1993; 16(1): 83–83.
  38. Russell LD, Hikim AP, Overbeek PA, et al. Testis structure in the sys (symplastic spermatids) mouse. Am J Anat. 1991; 192(2): 169–182.
  39. Santiago J, Silva JV, Alves MG, et al. Testicular aging: an overview of ultrastructural, cellular, and molecular alterations. J Gerontol A Biol Sci Med Sci. 2019; 74(6): 860–871.
  40. Schoenfeld HA, Hall SJ, Boekelheide K. Continuously proliferative stem germ cells partially repopulate the aged, atrophic rat testis after gonadotropin-releasing hormone agonist therapy. Biol Reprod. 2001; 64(4): 1273–1282.
  41. Sengupta P. A scientific review of age determination for a laboratory rat: how old is it in comparison with human age? Biomed Int. 2015; 2(2): 81–89.
  42. Sinha Hikim AP, Wang C, Lue Y, et al. Spontaneous germ cell apoptosis in humans: evidence for ethnic differences in the susceptibility of germ cells to programmed cell death. J Clin Endocrinol Metab. 1998; 83(1): 152–156.
  43. Standring S, Ariana L, Alan J. Abdomen and Pelvis: Male reproductive system. In: Gray’s anatomy, the anatomical basis of clinical practice, 41th ed. Churchill Livingstone Elsevier, London 2015: 1272–1286.
  44. Syntin P, Robaire B. Sperm structural and motility changes during aging in the Brown Norway rat. J Androl. 2001; 22(2): 235–244.
  45. Turner TT, Lysiak JJ. Oxidative stress: a common factor in testicular dysfunction. J Androl. 2008; 29(5): 488–498.
  46. Wyrobek AJ, Eskenazi B, Young S, et al. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci U S A. 2006; 103(25): 9601–9606.
  47. Xu YC, Jing LI, Liang WB. evaluation on changes of testicular histology in aging men. J Reprod Contracept. 2013; 24(4): 199–204.
  48. Yip BH, Pawitan Y, Czene K. Parental age and risk of childhood cancers: a population-based cohort study from Sweden. Int J Epidemiol. 2006; 35(6): 1495–1503.
  49. Zhu JL, Madsen KM, Vestergaard M, et al. Paternal age and congenital malformations. Hum Reprod. 2005; 20(11): 3173–3177.

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