Research Article
BibTex RIS Cite

Expression pattern and subcellular localization of p62/SQSTM 1 during mouse oocyte maturation

Year 2023, Volume: 9 Issue: 2, 236 - 244, 31.05.2023
https://doi.org/10.19127/mbsjohs.1221058

Abstract

Objective: Autophagy is a survival mechanism, and it is initiated by several factors such as oxidative stress. Cells give autophagy response against oxidative stress through Nrf2-Keap1-p62 pathway. p62 or Sequestosome 1 (SQSTM 1) which takes place during autophagy, and it is showed that p62 plays critical role during primordial follicle formation. During oocyte maturation, Germinal Vesicle (GV) oocytes resume meiosis with the beginning of puberty and progress through Metaphase I and Metaphase II stages. Metaphase II (MII) oocytes are ready to be fertilized and until fertilization they are arrested at metaphase II stages. It is known that oxidative stress is increasing during oocyte maturation. However, it is not shown that spatial and temporal expression of p62 throughout oocyte maturation. Thus, the aim of the study was to reveal expression pattern and the subcellular localization of the p62 protein in mouse GV, MI and MII oocytes.

Methods: GV oocytes were received from female Balb/C mice at 4 weeks aged and GV oocytes were cultured for 8h to develop into MI oocytes and for 14h to mature into MII oocytes. Then, expression of p62 protein was observed in oocytes at GV, MI and MII maturation stages by using immunofluorescence method.

Results: Our results showed that there is a significant increasing p62 expression when GV oocytes are compared to MI and MII oocytes, but there is no difference between MI and MII oocytes. Moreover, we revealed that p62 is localized in cytoplasm of GV oocytes, while it is localized around chromosomes in MI and MII oocytes.

Conclusion: In conclusion, our results indicate that further study is mandatory to understand the participation of p62 during meiosis, and the impact of p62 during oocyte maturation.

Supporting Institution

The Scientific and Technological Research Council of Turkey (TUBITAK)

Project Number

220S736

Thanks

We would like to thank all authors who provided published data.

References

  • 1. Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 2015;22(3):377-88.
  • 2. Kim KH, Lee MS. Autophagy--a key player in cellular and body metabolism. Nat Rev Endocrinol. 2014;10(6):322-37.
  • 3. Bhardwaj JK, Paliwal A, Saraf P, Sachdeva SN. Role of autophagy in follicular development and maintenance of primordial follicular pool in the ovary. J Cell Physiol. 2022;237(2):1157-70.
  • 4. Katsuragi Y, Ichimura Y, Komatsu M. p62/SQSTM1 functions as a signaling hub and an autophagy adaptor. Febs j. 2015;282(24):4672-8.
  • 5. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282(33):24131-45.
  • 6. Liu WJ, Ye L, Huang WF, Guo LJ, Xu ZG, Wu HL, et al. p62 links the autophagy pathway and the ubiqutin-proteasome system upon ubiquitinated protein degradation. Cell Mol Biol Lett. 2016;21:29.
  • 7. Yoshinobu I, Waguri S., Sou Y. et all Phosphorylation of p62 Activates the Keap1-Nrf2 Pathway during Selective Autophagy. Molecular Cell 2013.
  • 8. Zhihan T, Xinyi M, Qingying L, Rufei G, Yan Z, Xuemei C, et al. Autophagy participates in cyst breakdown and primordial folliculogenesis by reducing reactive oxygen species levels in perinatal mouse ovaries. J Cell Physiol. 2019;234(5):6125-35.
  • 9. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213-23.
  • 10. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, et al. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell. 2013;51(5):618-31.
  • 11. Jiang T, Harder B, Rojo de la Vega M, Wong PK, Chapman E, Zhang DD. p62 links autophagy and Nrf2 signaling. Free Radic Biol Med. 2015;88(Pt B):199-204.
  • 12. Rimon-Dahari N, Yerushalmi-Heinemann L, Alyagor L, Dekel N. Ovarian Folliculogenesis. Results Probl Cell Differ. 2016;58:167-90.
  • 13. Filatov M, Khramova Y, Semenova M. Molecular Mechanisms of Prophase I Meiotic Arrest Maintenance and Meiotic Resumption in Mammalian Oocytes. Reprod Sci. 2019;26(11):1519-37.
  • 14. Li J, Qian WP, Sun QY. Cyclins regulating oocyte meiotic cell cycle progression†. Biol Reprod. 2019;101(5):878-81.
  • 15. Kala M, Shaikh MV, Nivsarkar M. Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol. 2017;16(1):28-35.
  • 16. Gao Q. Oxidative Stress and Autophagy. Adv Exp Med Biol. 2019;1206:179-98.
  • 17. Xu J, Zhang D, Ju S, Sun L, Zhang S, Wu C, et al. Mitophagy is involved in the mitochondrial dysfunction of vitrified porcine oocytes. Mol Reprod Dev. 2021;88(6):427-36.
  • 18. He M, Zhang T, Zhu Z, Qin S, Wang H, Zhao L, et al. LSD1 contributes to programmed oocyte death by regulating the transcription of autophagy adaptor SQSTM1/p62. Aging Cell. 2020;19(3):e13102.
  • 19. Lin FH, Zhang WL, Li H, Tian XD, Zhang J, Li X, et al. Role of autophagy in modulating post-maturation aging of mouse oocytes. Cell Death Dis. 2018;9(3):308.
  • 20. Uyar A, Torrealday S, Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil Steril. 2013;99(4):979-97.
  • 21. He H, Wang J, Mou X, Liu X, Li Q, Zhong M, et al. Selective autophagic degradation of ACLY (ATP citrate lyase) maintains citrate homeostasis and promotes oocyte maturation. Autophagy. 2022:1-17.
  • 22. Ye X, Sloboda RD. Molecular characterization of p62, a mitotic apparatus protein required for mitotic progression. J Biol Chem. 1997;272(6):3606-14.
  • 23. Yun HR, Jo YH, Kim J, Shin Y, Kim SS, Choi TG. Roles of Autophagy in Oxidative Stress. Int J Mol Sci. 2020;21(9).
  • 24. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol. 2005;3:28.
Year 2023, Volume: 9 Issue: 2, 236 - 244, 31.05.2023
https://doi.org/10.19127/mbsjohs.1221058

Abstract

Project Number

220S736

References

  • 1. Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 2015;22(3):377-88.
  • 2. Kim KH, Lee MS. Autophagy--a key player in cellular and body metabolism. Nat Rev Endocrinol. 2014;10(6):322-37.
  • 3. Bhardwaj JK, Paliwal A, Saraf P, Sachdeva SN. Role of autophagy in follicular development and maintenance of primordial follicular pool in the ovary. J Cell Physiol. 2022;237(2):1157-70.
  • 4. Katsuragi Y, Ichimura Y, Komatsu M. p62/SQSTM1 functions as a signaling hub and an autophagy adaptor. Febs j. 2015;282(24):4672-8.
  • 5. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282(33):24131-45.
  • 6. Liu WJ, Ye L, Huang WF, Guo LJ, Xu ZG, Wu HL, et al. p62 links the autophagy pathway and the ubiqutin-proteasome system upon ubiquitinated protein degradation. Cell Mol Biol Lett. 2016;21:29.
  • 7. Yoshinobu I, Waguri S., Sou Y. et all Phosphorylation of p62 Activates the Keap1-Nrf2 Pathway during Selective Autophagy. Molecular Cell 2013.
  • 8. Zhihan T, Xinyi M, Qingying L, Rufei G, Yan Z, Xuemei C, et al. Autophagy participates in cyst breakdown and primordial folliculogenesis by reducing reactive oxygen species levels in perinatal mouse ovaries. J Cell Physiol. 2019;234(5):6125-35.
  • 9. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213-23.
  • 10. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, et al. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell. 2013;51(5):618-31.
  • 11. Jiang T, Harder B, Rojo de la Vega M, Wong PK, Chapman E, Zhang DD. p62 links autophagy and Nrf2 signaling. Free Radic Biol Med. 2015;88(Pt B):199-204.
  • 12. Rimon-Dahari N, Yerushalmi-Heinemann L, Alyagor L, Dekel N. Ovarian Folliculogenesis. Results Probl Cell Differ. 2016;58:167-90.
  • 13. Filatov M, Khramova Y, Semenova M. Molecular Mechanisms of Prophase I Meiotic Arrest Maintenance and Meiotic Resumption in Mammalian Oocytes. Reprod Sci. 2019;26(11):1519-37.
  • 14. Li J, Qian WP, Sun QY. Cyclins regulating oocyte meiotic cell cycle progression†. Biol Reprod. 2019;101(5):878-81.
  • 15. Kala M, Shaikh MV, Nivsarkar M. Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol. 2017;16(1):28-35.
  • 16. Gao Q. Oxidative Stress and Autophagy. Adv Exp Med Biol. 2019;1206:179-98.
  • 17. Xu J, Zhang D, Ju S, Sun L, Zhang S, Wu C, et al. Mitophagy is involved in the mitochondrial dysfunction of vitrified porcine oocytes. Mol Reprod Dev. 2021;88(6):427-36.
  • 18. He M, Zhang T, Zhu Z, Qin S, Wang H, Zhao L, et al. LSD1 contributes to programmed oocyte death by regulating the transcription of autophagy adaptor SQSTM1/p62. Aging Cell. 2020;19(3):e13102.
  • 19. Lin FH, Zhang WL, Li H, Tian XD, Zhang J, Li X, et al. Role of autophagy in modulating post-maturation aging of mouse oocytes. Cell Death Dis. 2018;9(3):308.
  • 20. Uyar A, Torrealday S, Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil Steril. 2013;99(4):979-97.
  • 21. He H, Wang J, Mou X, Liu X, Li Q, Zhong M, et al. Selective autophagic degradation of ACLY (ATP citrate lyase) maintains citrate homeostasis and promotes oocyte maturation. Autophagy. 2022:1-17.
  • 22. Ye X, Sloboda RD. Molecular characterization of p62, a mitotic apparatus protein required for mitotic progression. J Biol Chem. 1997;272(6):3606-14.
  • 23. Yun HR, Jo YH, Kim J, Shin Y, Kim SS, Choi TG. Roles of Autophagy in Oxidative Stress. Int J Mol Sci. 2020;21(9).
  • 24. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol. 2005;3:28.
There are 24 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Research articles
Authors

Fatma Uysal 0000-0002-9176-326X

Nazlıcan Bozdemir 0000-0001-9110-4267

Özgür Çınar 0000-0003-2901-1910

Project Number 220S736
Publication Date May 31, 2023
Published in Issue Year 2023 Volume: 9 Issue: 2

Cite

Vancouver Uysal F, Bozdemir N, Çınar Ö. Expression pattern and subcellular localization of p62/SQSTM 1 during mouse oocyte maturation. Mid Blac Sea J Health Sci. 2023;9(2):236-44.

2310022108  22107  22106  22105  22103  22109 22137 22102  22110    e-ISSN 2149-7796