open access

Vol 81, No 2 (2022)
Original article
Submitted: 2021-03-01
Accepted: 2021-04-22
Published online: 2021-05-06
Get Citation

Histological analysis of spermatogenesis and the germ cell seasonal development within the testis of domesticated tree shrews (Tupaia belangeri chinensis)

J. Tang12, G. He13, Y. Yang1, Q. Li1, Y. He1, C. Yu1, L. Luo1
·
Pubmed: 33997948
·
Folia Morphol 2022;81(2):412-420.
Affiliations
  1. School of Basic Medical Sciences, Kunming Medical University, Kunming, China
  2. Department of Medical Genetics and Prenatal Diagnosis, Kunming Maternity and Child Health Hospital, Kunming, China
  3. Clinical Laboratory, Yunnan Maternal and Child Health Care Hospital, Kunming, China

open access

Vol 81, No 2 (2022)
ORIGINAL ARTICLES
Submitted: 2021-03-01
Accepted: 2021-04-22
Published online: 2021-05-06

Abstract

Background: This study aimed to address the lack of information on the male germ cell seasonal development of domesticated tree shrews (Tupaia belangeri chinensis).
Materials and methods: Testicular tissues were collected from 60 tree shrews (n = 5 per month). The ultrastructures of the testes and spermatids were examined via transmission electron microscopy. Apoptosis of spermatogenic cells was measured through terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL) staining. The expression of proliferation factors, namely, proliferating cell nuclear antigen (PCNA) and Ki67, in testicular tissues was assayed through
immunohistochemistry.
Results: Spermatid ultrastructure showed seasonal differences, and spermatogenesis was relatively active in June and July and relatively stagnant from October to November. The percentage of TUNEL-positive germ cells was less during October and November, while greater in July than other phases. The number of PCNA-nucleus-positive germ cells was most in June and July, but with cytoplasm staining from October to November. Ki67 presented positive expression in the testes from April to September, with highest expression in June, but with no expression from October to March.
Conclusions: In summary, there are seasonal differences in tissue morphology related to spermatogenesis in domesticated tree shrews. PCNA expression and Ki67 expression are good indicators of seasonal differences in male germ cells.

Abstract

Background: This study aimed to address the lack of information on the male germ cell seasonal development of domesticated tree shrews (Tupaia belangeri chinensis).
Materials and methods: Testicular tissues were collected from 60 tree shrews (n = 5 per month). The ultrastructures of the testes and spermatids were examined via transmission electron microscopy. Apoptosis of spermatogenic cells was measured through terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL) staining. The expression of proliferation factors, namely, proliferating cell nuclear antigen (PCNA) and Ki67, in testicular tissues was assayed through
immunohistochemistry.
Results: Spermatid ultrastructure showed seasonal differences, and spermatogenesis was relatively active in June and July and relatively stagnant from October to November. The percentage of TUNEL-positive germ cells was less during October and November, while greater in July than other phases. The number of PCNA-nucleus-positive germ cells was most in June and July, but with cytoplasm staining from October to November. Ki67 presented positive expression in the testes from April to September, with highest expression in June, but with no expression from October to March.
Conclusions: In summary, there are seasonal differences in tissue morphology related to spermatogenesis in domesticated tree shrews. PCNA expression and Ki67 expression are good indicators of seasonal differences in male germ cells.

Get Citation

Keywords

tree shrew, spermatogenic cell, seasonal differences, testis

About this article
Title

Histological analysis of spermatogenesis and the germ cell seasonal development within the testis of domesticated tree shrews (Tupaia belangeri chinensis)

Journal

Folia Morphologica

Issue

Vol 81, No 2 (2022)

Article type

Original article

Pages

412-420

Published online

2021-05-06

Page views

5297

Article views/downloads

1063

DOI

10.5603/FM.a2021.0048

Pubmed

33997948

Bibliographic record

Folia Morphol 2022;81(2):412-420.

Keywords

tree shrew
spermatogenic cell
seasonal differences
testis

Authors

J. Tang
G. He
Y. Yang
Q. Li
Y. He
C. Yu
L. Luo

References (32)
  1. Aitken RJ, Findlay JK, Hutt KJ, et al. Apoptosis in the germ line. Reproduction. 2011; 141(2): 139–150.
  2. Ben-Rafael Z, Farhi J, Feldberg D, et al. Follicle-stimulating hormone treatment for men with idiopathic oligoteratoasthenozoospermia before in vitro fertilization: the impact on sperm microstructure and fertilization potential. Fertil Steril. 2000; 73(1): 24–30.
  3. Blottner S, Hingst O, Meyer HH. Inverse relationship between testicular proliferation and apoptosis in mammalian seasonal breeders. Theriogenology. 1995; 44(3): 321–328.
  4. Cao XM. Seasonal changes in spermatogenesis of tree shrew (Tupaia belangeri Chinensis). Zool Res. 1989; 10(1): 15–21.
  5. De Chiara A, Pederzoli-Ribeil M, Burgel PR, et al. Targeting cytosolic proliferating cell nuclear antigen in neutrophil-dominated inflammation. Front Immunol. 2012; 3: 311.
  6. Donnelly ET, Lewis SE, McNally JA, et al. In vitro fertilization and pregnancy rates: the influence of sperm motility and morphology on IVF outcome. Fertil Steril. 1998; 70(2): 305–314.
  7. DuRant S, Love AC, Belin B, et al. Captivity alters neuroendocrine regulators of stress and reproduction in the hypothalamus in response to acute stress. Gen Comp Endocrinol. 2020; 295: 113519.
  8. Fan Yu, Huang ZY, Cao CC, et al. Genome of the Chinese tree shrew. Nat Commun. 2013; 4: 1426.
  9. França LR, Avelar GF, Almeida FFL. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology. 2005; 63(2): 300–318.
  10. Hsueh AJ, Eisenhauer K, Chun SY, et al. Gonadal cell apoptosis. Recent Prog Horm Res. 1996; 51: 433–55; discussion 455.
  11. Ito J, Meguro K, Komatsu K, et al. Seasonal changes in the spermatogenesis of the large Japanese field mice (Apodemus speciosus) controlled by proliferation and apoptosis of germ cells. Anim Reprod Sci. 2020; 214: 106288.
  12. Jahnukainen K, Chrysis D, Hou Mi, et al. Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol Reprod. 2004; 70(2): 290–296.
  13. Korgun ET, Celik-Ozenci C, Acar N, et al. Location of cell cycle regulators cyclin B1, cyclin A, PCNA, Ki67 and cell cycle inhibitors p21, p27 and p57 in human first trimester placenta and deciduas. Histochem Cell Biol. 2006; 125(6): 615–624.
  14. Li B, Chen LI, Liu RW, et al. Preliminary discussions about laboratory breeding and management of tupaia belangeri chinensis. Sci Tech Info. 2008; 2008(35): 664.
  15. Liberal V, De Miguel MP, Henze M, et al. Reduced spermatogonial proliferation and decreased fertility in mice overexpressing cyclin E in spermatogonia. Cell Cycle. 2010; 9(20): 4222–4227.
  16. Maeda S, Endo H, Kimura J, et al. Classification of the cycle of the seminiferous epithelium in the common tree shrew (Tupaia glis). J Vet Med Sci. 1996; 58(5): 481–484.
  17. Müller R, Misund K, Holien T, et al. Targeting proliferating cell nuclear antigen and its protein interactions induces apoptosis in multiple myeloma cells. PLoS One. 2013; 8(7): e70430.
  18. Nikolettos N, Küpker W, Demirel C, et al. Fertilization potential of spermatozoa with abnormal morphology. Hum Reprod. 1999; 14 Suppl 1: 47–70.
  19. Ohayon D, De Chiara A, Chapuis N, et al. Cytoplasmic proliferating cell nuclear antigen connects glycolysis and cell survival in acute myeloid leukemia. Sci Rep. 2016; 6: 35561.
  20. Pereira R, Sá R, Barros A, et al. Major regulatory mechanisms involved in sperm motility. Asian J Androl. 2017; 19(1): 5–14.
  21. Romano FJ, Rossetti S, Conteduca V, et al. Role of DNA repair machinery and p53 in the testicular germ cell cancer: a review. Oncotarget. 2016; 7(51): 85641–85649.
  22. Sanada T, Tsukiyama-Kohara K, Shin-I T, et al. Construction of complete Tupaia belangeri transcriptome database by whole-genome and comprehensive RNA sequencing. Sci Rep. 2019; 9(1): 12372.
  23. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000; 182(3): 311–322, doi: 10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9.
  24. Shen P-Q, Zheng H, Liu RW. Progress and prospect in research on laboratory tree shrew in China. Dongwuxue Yanjiu. 2011; 32(1): 109–114.
  25. Steger K, Aleithe I, Behre H, et al. The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen. Mol Hum Reprod. 1998; 4(3): 227–233.
  26. Strzalka W, Ziemienowicz A. Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann Bot. 2011; 107(7): 1127–1140.
  27. Sun X, Kaufman PD. Ki-67: more than a proliferation marker. Chromosoma. 2018; 127(2): 175–186.
  28. White-Cooper H, Doggett K, Ellis R. The evolution of spermatogenesis. Sperm Biology. 2009: 151–183.
  29. Xiao-mei C. Seasonal changes in spermatogenesis of tree shrew (Tupaia belangeri Chinensis). Zool Res. 1989; 10(1): 15–21.
  30. Yao YG. Creating animal models, why not use the Chinese tree shrew (Tupaia belangeri chinensis)? Zool Res. 2017; 38(3): 118.
  31. Zhao WP, Wang HW, Liu J, et al. Positive PCNA and Ki-67 expression in the testis correlates with spermatogenesis dysfunction in fluoride-treated rats. Biol Trace Elem Res. 2018; 186(2): 489–497.
  32. Zhong S, Zhang Sy, Xing Hj, et al. Revealing histological and morphological features of female reproductive system in tree shrew (Tupaia belangeri). Zoomorphology. 2017; 137(1): 191–199.

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By VM Media Group sp. z o.o., Grupa Via Medica, Świętokrzyska 73, 80–180 Gdańsk, Poland

tel.: +48 58 320 94 94, faks: +48 58 320 94 60, e-mail: viamedica@viamedica.pl