HFM1 is Essential for the Germ Cell Intercellular Bridge Transport in Primordial Follicle Formation in Mice

Overview

Journal Cell Mol Life Sci

Publisher Springer

Specialty Biology

Date 2024 Dec 26

PMID 39725823

Authors

Yuheng He

Huiyuan Wang

Tongtong Hong

Luanqian Hu

Chao Gao

Li Gao

Yugui Cui

Rongrong Tan

Danhua Pu

Jie Wu

Affiliations

Soon will be listed here.

Abstract

The reproductive lifespan of female mammals is determined by the size of the primordial follicle pool, which comprises oocytes enclosed by a layer of flattened pre-granulosa cells. Oocyte differentiation needs acquiring organelles and cytoplasm from sister germ cells in cysts, but the mechanisms regulating this process remain unknown. Previously helicase for meiosis 1 (HFM1) is reported to be related to the development of premature ovarian insufficiency. Here, it is found that HFM1 is involved in oocyte differentiation through organelle enrichment from sister germ cells. Further study indicates that HFM1 is involved in intercellular directional transport through intercellular bridges via the RAC1/ANLN/E-cad signaling pathway, which is indispensable for oocyte differentiation and primordial follicle formation. These findings shed light on the critical role of HFM1 in intercellular bridge transport, which is essential for the establishment of the primordial follicle pool and presenting new horizons for female fertility protection.

References

Umeno K, Sasaki A, Kimura N . The impact of oocyte death on mouse primordial follicle formation and ovarian reserve. Reprod Med Biol. 2022; 21(1):e12489. PMC: 9623396. DOI: 10.1002/rmb2.12489. View

Webber L, Davies M, Anderson R, Bartlett J, Braat D, Cartwright B . ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod. 2016; 31(5):926-37. DOI: 10.1093/humrep/dew027. View

Kechad A, Jananji S, Ruella Y, Hickson G . Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr Biol. 2012; 22(3):197-203. PMC: 3698874. DOI: 10.1016/j.cub.2011.11.062. View

Tingen C, Kim A, Woodruff T . The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod. 2009; 15(12):795-803. PMC: 2776475. DOI: 10.1093/molehr/gap073. View

Ikami K, Nuzhat N, Lei L . Organelle transport during mouse oocyte differentiation in germline cysts. Curr Opin Cell Biol. 2016; 44:14-19. DOI: 10.1016/j.ceb.2016.12.002. View

Pepling M, Wilhelm J, OHara A, Gephardt G, Spradling A . Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc Natl Acad Sci U S A. 2006; 104(1):187-92. PMC: 1765432. DOI: 10.1073/pnas.0609923104. View

He Y, Chen Q, Dai J, Cui Y, Zhang C, Wen X . Single-cell RNA-Seq reveals a highly coordinated transcriptional program in mouse germ cells during primordial follicle formation. Aging Cell. 2021; 20(7):e13424. PMC: 8282241. DOI: 10.1111/acel.13424. View

Li X, Feng Q, Yang H, Ruan J, Kang Y, Yu Z . p120 regulates E-cadherin expression in nasal epithelial cells in chronic rhinosinusitis. Rhinology. 2022; 60(4):270-281. DOI: 10.4193/Rhin21.276. View

Pepling M, Spradling A . Female mouse germ cells form synchronously dividing cysts. Development. 1998; 125(17):3323-8. DOI: 10.1242/dev.125.17.3323. View

10.

Panay N, Anderson R, Nappi R, Vincent A, Vujovic S, Webber L . Premature ovarian insufficiency: an International Menopause Society White Paper. Climacteric. 2020; 23(5):426-446. DOI: 10.1080/13697137.2020.1804547. View

11.

Lei L, Spradling A . Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science. 2016; 352(6281):95-9. PMC: 6910648. DOI: 10.1126/science.aad2156. View

12.

Tian D, Diao M, Jiang Y, Sun L, Zhang Y, Chen Z . Anillin Regulates Neuronal Migration and Neurite Growth by Linking RhoG to the Actin Cytoskeleton. Curr Biol. 2015; 25(9):1135-45. DOI: 10.1016/j.cub.2015.02.072. View

13.

Spradling A, Niu W, Yin Q, Pathak M, Maurya B . Conservation of oocyte development in germline cysts from to mouse. Elife. 2022; 11. PMC: 9708067. DOI: 10.7554/eLife.83230. View

14.

Huhtaniemi I, Hovatta O, La Marca A, Livera G, Monniaux D, Persani L . Advances in the Molecular Pathophysiology, Genetics, and Treatment of Primary Ovarian Insufficiency. Trends Endocrinol Metab. 2018; 29(6):400-419. DOI: 10.1016/j.tem.2018.03.010. View

15.

Fukuda K, Muraoka M, Kato Y, Saga Y . Decoding the transcriptome of pre-granulosa cells during the formation of primordial follicles in the mouse†. Biol Reprod. 2021; 105(1):179-191. DOI: 10.1093/biolre/ioab065. View

16.

Lei L, Spradling A . Mouse primordial germ cells produce cysts that partially fragment prior to meiosis. Development. 2013; 140(10):2075-81. PMC: 3640216. DOI: 10.1242/dev.093864. View

17.

Sun L, Guan R, Lee I, Liu Y, Chen M, Wang J . Mechanistic insights into the anchorage of the contractile ring by anillin and Mid1. Dev Cell. 2015; 33(4):413-26. PMC: 4449299. DOI: 10.1016/j.devcel.2015.03.003. View

18.

Greenbaum M, Iwamori T, Buchold G, Matzuk M . Germ cell intercellular bridges. Cold Spring Harb Perspect Biol. 2011; 3(8):a005850. PMC: 3140685. DOI: 10.1101/cshperspect.a005850. View

19.

Greenbaum M, Iwamori N, Agno J, Matzuk M . Mouse TEX14 is required for embryonic germ cell intercellular bridges but not female fertility. Biol Reprod. 2008; 80(3):449-57. PMC: 2805395. DOI: 10.1095/biolreprod.108.070649. View

20.

Kim H, Yoon J, Matsuura A, Na J, Lee W, Kim H . Structural and biochemical insights into the role of testis-expressed gene 14 (TEX14) in forming the stable intercellular bridges of germ cells. Proc Natl Acad Sci U S A. 2015; 112(40):12372-7. PMC: 4603477. DOI: 10.1073/pnas.1418606112. View