Skip to main content

Advertisement

SpringerLink
Log in

Transcriptomic Profiling of Reproductive Age Marmoset Monkey Ovaries

  • Reproductive Biology: Original Article
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

The decline in ovarian reserve and the aging of the ovaries is a significant concern for women, particularly in the context of delayed reproduction. However, there are ethical limitations and challenges associated with conducting long-term studies to understand and manipulate the mechanisms that regulate ovarian aging in human. The marmoset monkey offers several advantages as a reproductive model, including a shorter gestation period and similar reproductive physiology to that of human. Additionally, they have a relatively long lifespan compared to other mammals, making them suitable for long-term studies. In this study, we focused on analyzing the structural characteristics of the marmoset ovary and studying the mRNA expression of 244 genes associated with ovarian aging. We obtained ovaries from marmosets at three different reproductive stages: pre-pubertal (1.5 months), reproductive (82 months), and menopausal (106 months) ovaries. The structural analyses revealed the presence of numerous mitochondria and lipid droplets in the marmoset ovaries. Many of the genes expressed in the ovaries were involved in multicellular organism development and transcriptional regulation. Additionally, we identified the expression of protein-binding genes. Within the expressed genes, VEGFA and MMP9 were found to be critical for regulating ovarian reserve. An intriguing finding of the study was the strong correlation between genes associated with female infertility and genes related to fibrosis and wound healing. The authors suggest that this correlation might be a result of the repeated rupture and subsequent healing processes occurring in the ovary due to the menstrual cycle, potentially leading to the indirect onset of fibrosis. The expression profile of ovarian aging-related gene set in the marmoset monkey ovaries highlight the need for further studies to explore the relationship between fibrosis, wound healing, and ovarian aging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

Data Availability

Not applicable

Code Availability

Not applicable

References

  1. Cho E, et al. A new possibility in fertility preservation: the artificial ovary. J Tissue Eng Regen Med. 2019;13(8):1294–315.

    Article  CAS  PubMed  Google Scholar 

  2. Dong MH, Kim YY, Ku SY. Identification of stem cell-like cells in the ovary. Tissue Eng Regen Med. 2022;19(4):675–85.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kim YJ, et al. Effects of estradiol on the paracrine regulator expression of in vitro maturated murine ovarian follicles. Tissue Eng Regenerat Med. 2017;14(1):31–8.

    Article  CAS  Google Scholar 

  4. Espey LL. The distribution of collagenous connective tissue in rat ovarian follicles. Biol Reprod. 1976;14(4):502–6.

    Article  CAS  PubMed  Google Scholar 

  5. Espey LL, Coons PJ. Factors which influence ovulatory regradation of rabbit ovarian follicles. Biol Reprod. 1976;14(3):233–45.

    Article  CAS  PubMed  Google Scholar 

  6. Kim YJ, et al. Proliferation Profile of uterine endometrial stromal cells during in vitro culture with gonadotropins: recombinant versus urinary follicle stimulating hormone. Tissue Eng Regen Med. 2019;16(2):131–9.

    Article  CAS  PubMed  Google Scholar 

  7. Spencer TE, Dunlap KA, Filant J. Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption. Mol Cell Endocrinol. 2012;354(1-2):34–53.

    Article  CAS  PubMed  Google Scholar 

  8. Yun JW, et al. Use of nonhuman primates for the development of bioengineered female reproductive organs. Tissue Eng Regen Med. 2016;13(4):323–34.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kim YY, et al. Gonadotropin ratio affects the in vitro growth of rhesus ovarian preantral follicles. J Investig Med. 2016;64(4):888–93.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lin ZYC, et al. Molecular signatures to define spermatogenic cells in common marmoset (Callithrix jacchus). Reprod. 2012;143(5):597–609.

    Article  CAS  Google Scholar 

  11. Fereydouni B, et al. The neonatal marmoset monkey ovary is very primitive exhibiting many oogonia. Reprod. 2014;148(2):237–47.

    Article  CAS  Google Scholar 

  12. Wolfe LG, et al. Reproduction of wild-caught and laboratory-born marmoset species used in biomedical research (Saguinus sp, Callithrix jacchus). Lab Anim Sci. 1975;25(6):802–13.

    CAS  PubMed  Google Scholar 

  13. Han HJ, Powers SJ, Gabrielson KL. The common marmoset-biomedical research animal model applications and common spontaneous diseases. Toxicol Pathol. 2022;50(5):628–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Abbott DH, et al. Aspects of common marmoset basic biology and life history important for biomedical research. Comp Med. 2003;53(4):339–50.

    CAS  PubMed  Google Scholar 

  15. Burgess DJ. Dissecting the genetics of ovarian ageing. Nat Rev Genet. 2021;22(10):623.

    Article  CAS  PubMed  Google Scholar 

  16. Campos FA, et al. Female reproductive aging in seven primate species: Patterns and consequences. Proc Natl Acad Sci U S A. 2022;119(20):e2117669119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang S, et al. Deciphering primate retinal aging at single-cell resolution. Protein Cell. 2021;12(11):889–98.

    Article  PubMed  Google Scholar 

  18. Metsis A, et al. Whole-genome expression profiling through fragment display and combinatorial gene identification. Nucleic Acids Res. 2004;32(16):e127.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Okano H, et al. The common marmoset as a novel animal model system for biomedical and neuroscience research applications. Semin Fetal Neonatal Med. 2012;17(6):336–40.

    Article  PubMed  Google Scholar 

  20. Montardy Q, et al. Mapping the neural circuitry of predator fear in the nonhuman primate. Brain Struct Funct. 2021;226(1):195–205.

    Article  PubMed  Google Scholar 

  21. Chongtham MC, et al. Transcriptome response and spatial pattern of gene expression in the primate subventricular zone neurogenic niche after cerebral ischemia. Front Cell Dev Biol. 2020;8:584314.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kim YY, et al. Expression of transcripts in marmoset oocytes retrieved during follicle isolation without gonadotropin induction. Int J Mol Sci. 2019;20(5).

  23. Kim YY, et al. Synergistic promoting effects of x-linked inhibitor of apoptosis protein and matrix on the in vitro follicular maturation of marmoset follicles. Tissue Eng Regenerat Med. 2022;19(1):93–103.

    Article  CAS  Google Scholar 

  24. Tardif SD, Jaquish CE. The common marmoset as a model for nutritional impacts upon reproduction. Ann N Y Acad Sci. 1994;709:214–5.

    Article  CAS  PubMed  Google Scholar 

  25. Hodges JK, Hearn JP. Effects of immunisation against luteinising hormone releasing hormone on reproduction of the marmoset monkey Callithrixjacchus. Nature. 1977;265(5596):746–8.

    Article  CAS  PubMed  Google Scholar 

  26. Li J, et al. A single-cell transcriptomic atlas of primate pancreatic islet aging. Natl Sci Rev. 2021;8(2):nwaa127.27.

    Article  Google Scholar 

  27. Zhang W, et al. A single-cell transcriptomic landscape of primate arterial aging. Nat Commun. 2020;11(1):2202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Motohashi HH, Ishibashi H. Cryopreservation of ovaries from neonatal marmoset monkeys. Exp Anim. 2016;65(3):189–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ishida-Yamamoto A, et al. Epidermal lamellar granules transport different cargoes as distinct aggregates. J Investig Dermatol. 2004;122(5):1137–44.

    Article  PubMed  Google Scholar 

  30. Rossi LF, Solari AJ. Large lamellar bodies and their role in the growing oocytes of the armadillo Chaetophractus villosus. J Morphol. 2021;282(9):1330–8.

    Article  CAS  PubMed  Google Scholar 

  31. Fraser HM, et al. GnRH receptor mRNA expression by in-situ hybridization in the primate pituitary and ovary. Mol Hum Reprod. 1996;2(2):117–21.

    Article  CAS  PubMed  Google Scholar 

  32. Fraser HM, Duncan WC. Vascular morphogenesis in the primate ovary. Angiogen. 2005;8(2):101–16.

    Article  Google Scholar 

  33. Fraser HM, Wulff C. Angiogenesis in the primate ovary. Reprod Fertil Dev. 2001;13(7-8):557–66.

    Article  CAS  PubMed  Google Scholar 

  34. Chaffin CL, et al. Estrogen receptor and aromatic hydrocarbon receptor in the primate ovary. Endocrine. 1996;5(3):315–21.

    Article  CAS  PubMed  Google Scholar 

  35. diZerega GS, Hodgen GD. Fluorescence localization of luteinizing hormone/human chorionic gonadotropin uptake in the primate ovary. II. Changing distribution during selection of the dominant follicle. J Clin Endocrinol Metab. 1980;51(4):903–7.

    Article  CAS  PubMed  Google Scholar 

  36. Goodman AL, Hodgen GD. Between-ovary interaction in the regulation of follicle growth, corpus luteum function, and gonadotropin secretion in the primate ovarian cycle. II. Effects of luteectomy and hemiovariectomy during the luteal phase in cynomolgus monkeys. Endocrinology. 1979;104(5):1310–6.

    Article  CAS  PubMed  Google Scholar 

  37. Umehara T, et al. Female reproductive life span is extended by targeted removal of fibrotic collagen from the mouse ovary. Sci Adv. 2022;8(24).

  38. Briley SM, et al. Reproductive age-associated fibrosis in the stroma of the mammalian ovary. Reprod. 2016;152(3):245–60.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors appreciated the technical assistance of Jina Kwak, Jiyeon Kim, and Jinho Choi.

Funding

This study was supported by the grants of Ministry of ICT grants and the Ministry of Education, Republic of Korea (2020R1A2C1010293 and 2022R1A2B5B01002541).

Author information

Author notes

  1. Yoon Young Kim and Sung Woo Kim equally contributed to this study.

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Seoul National University Hospital, Daehak-ro 101, Jongno-gu, Seoul, 03080, South Korea

    Yoon Young Kim, Sung Woo Kim, Eunjin Kim & Seung-Yup Ku

  2. Institute of Reproductive Medicine and Population, Medical Research Center, Seoul National University, Seoul, South Korea

    Yoon Young Kim & Seung-Yup Ku

  3. Department of Obstetrics and Gynecology, Korea University College of Medicine, Seoul, South Korea

    Yong Jin Kim

  4. Department of Medicine, Seoul National University College of Medicine, Seoul, South Korea

    Byeong-Cheol Kang

Authors
  1. Yoon Young Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sung Woo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eunjin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yong Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Byeong-Cheol Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seung-Yup Ku
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seung-Yup Ku.

Ethics declarations

Ethics Approval

The experimental and retrospective study was approved by the IACUC of Seoul National University Hospital (SNUH-IACUC No. 20-0131-S1A1(1)).

Consent to Participate

Not applicable

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, Y.Y., Kim, S.W., Kim, E. et al. Transcriptomic Profiling of Reproductive Age Marmoset Monkey Ovaries. Reprod. Sci. 31, 81–95 (2024). https://doi.org/10.1007/s43032-023-01342-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43032-023-01342-5

Keywords

Search

Navigation