Cell-lineage specificity of primary cilia during postnatal epididymal development.
Abstract: Where are primary cilia (PC) organelles located during postnatal epididymal development? Our findings unveil the existence of PC sensory organelles in different epididymal cell types according to postnatal development stage. Primary cilia are sensory organelles that orchestrate major signaling pathways during organ development and homeostasis. Epididymal PC have been detected in the horses, donkey and mules but their cell-lineage specificity has never been investigated in this organ. A longitudinal study was performed by examining tissue from n = 3 to n = 10 transgenic mice at different times of postnatal development. Tissues were fixed by intracardiac perfusion and the epididymides collected. Transmission electron microscopy and confocal microscopy/3D reconstruction were used on a double transgenic mouse model expressing endogenous fluorescence in PC and centrioles (Arl13b-mCherry/Centrin2-GFP). Several PC parameters (i.e. length, orientation relative to the lumen) were quantified by using an image-processing pipeline. Epididymal tissues and serum-free cultures of DC2 immortalized epididymal principal murine cell lines were used to identify primary ciliary signaling components. We report here a constitutive localization of PC in peritubular myoid cells and a dynamic profiling in epithelial cells throughout postnatal epididymal development. While PC are present at the apical pole of the undifferentiated epithelial cells from birth to puberty, they are absent from the apical pole of the epithelium in adults, where they appear exclusively associated with cytokeratin 5-positive basal cells. We determined that PC from epididymal cells are associated with polycystin 1 (PC1), polycystin 2 (PC2), and Gli-3 Hedgehog signaling transcription factor. No inter-individual variability was observed within each age group. As our present study is descriptive and performed exclusively in the mouse, future functional studies will be required to unravel the contribution of these organelles in the control of reproductive functions. Acknowledging the important roles played by PC sensory organelles in organ homeostasis and development in humans, our work opens new avenues of research concerning the cellular control of epididymal functions, which are essential to male fertility. Study funded by an NSERC operating grant to CB (RGPIN-2015-109194). No competing interest to declare.
Publication Date: 2018-09-22 PubMed ID: 30239723DOI: 10.1093/humrep/dey276Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research explores the presence and function of primary cilia, a type of sensory organ, in different types of cells within the epididymis during postnatal development. The study also identifies signals associated with primary cilia in the epididymis, thus shedding new light on the role primary cilia may play in organ development and reproductive functions.
Methodology
- The study was conducted using transgenic mice, with tissue samples taken at various stages of postnatal development.
- Primary cilia were visualized through a combination of transmission electron microscopy and confocal microscopy/3D reconstruction and they were identified by their inherent fluorescence that was observable in this double transgenic mouse model.
- The research methodology included quantification of various parameters of primary cilia, like length, and orientation in relation to the lumen, assisted by the use of image-processing pipeline.
- Additionally, tissue cultures of DC2 (an epididymal principal murine cell line), were used to identify the signaling components linked with primary cilia.
Findings
- Researchers observed that primary cilia are consistently located in peritubular myoid cells and exhibit dynamic profiling in epithelial cells as the epididymis develops after birth.
- At initial stages of development – from birth to puberty – primary cilia are found at the apical pole of undifferentiated epithelial cells. However, in adults, they are absent from the apical pole and appear exclusively associated with cytokeratin 5-positive basal cells.
- The examination revealed that primary cilia in epididymal cells are connected with several signaling components: polycystin 1 (PC1), polycystin 2 (PC2), and Gli-3 Hedgehog signaling transcription factor.
- No significant differences in these observations were found within each age group, indicating that these findings are consistent across individuals.
Implications and Further Research
- The findings of the study are fundamental yet descriptive, adding to the understanding of the roles and location of primary cilia during organ development. It does not, however, draw conclusions about the function of these cilia in the control of reproductive functions.
- The study concludes that more expansive, functional studies will be required in the future to comprehend fully the role these organelles might play in reproductive function control.
- Considering the crucial role of primary cilia in organ homeostasis and development in humans, this research lays the groundwork for further investigation into the cellular control of epididymal functions – a key to understanding male fertility.
Cite This Article
APA
Bernet A, Bastien A, Soulet D, Jerczynski O, Roy C, Bianchi Rodrigues Alves M, Lecours C, Tremblay MÈ, Bailey JL, Robert C, Belleannée C.
(2018).
Cell-lineage specificity of primary cilia during postnatal epididymal development.
Hum Reprod, 33(10), 1829-1838.
https://doi.org/10.1093/humrep/dey276 Publication
Researcher Affiliations
- Université Laval, Department of Obstetrics, Gynecology and Reproduction, CHU de Q Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Animal Sciences, Q City, Q, Canada.
- Université Laval, Faculty of Pharmacy, CHU de Québec Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Obstetrics, Gynecology and Reproduction, CHU de Q Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Obstetrics, Gynecology and Reproduction, CHU de Q Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Obstetrics, Gynecology and Reproduction, CHU de Q Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Faculty of Pharmacy, CHU de Québec Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Molecular Medicine, CHU de Québec Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Molecular Medicine, CHU de Québec Research Center (CHUL), Q City, Q, Canada.
- Université Laval, Department of Animal Sciences, Q City, Q, Canada.
- Université Laval, Department of Animal Sciences, Q City, Q, Canada.
- Université Laval, Department of Obstetrics, Gynecology and Reproduction, CHU de Q Research Center (CHUL), Q City, Q, Canada.
MeSH Terms
- Animals
- Cell Lineage
- Cilia / metabolism
- Disease Models, Animal
- Epididymis / metabolism
- Humans
- Infertility, Male / metabolism
- Longitudinal Studies
- Male
- Mice
- Mice, Inbred C57BL
Citations
This article has been cited 11 times.- Girardet L, Cyr DG, Belleannée C. Arl13b controls basal cell stemness properties and Hedgehog signaling in the mouse epididymis. Cell Mol Life Sci 2022 Oct 19;79(11):556.
- Sterpka A, Yang J, Strobel M, Zhou Y, Pauplis C, Chen X. Diverged morphology changes of astrocytic and neuronal primary cilia under reactive insults. Mol Brain 2020 Mar 2;13(1):28.
- Yuan Y, Liu R, Huang H. [Research progress on the roles of primary cilia in fertility]. Zhejiang Da Xue Xue Bao Yi Xue Ban 2025 Dec 25;54(6):764-771.
- Zhang BL, Liu BY, Cao S, Shi S, Shum W. Extracellular Vesicles, Nutrient Balance, and Redox Metabolism During Epididymal Sperm Maturation: A Perspective on the Complexity of Intercellular Interplay. Adv Anat Embryol Cell Biol 2026;241:1-87.
- Long AB, Wilson IM, Terry TT, Van Sciver RE, Caspary T. ARL13B-Cerulean rescues Arl13b-null mouse from embryonic lethality and reveals a role for ARL13B in spermatogenesis. J Cell Sci 2025 Oct 15;138(20).
- Liu Y, Fang Y, Dhikhirullahi O, Zhang L, Zhang Z. Intraflagellar Transport (IFT) and Sperm Formation. Adv Exp Med Biol 2025;1469:395-409.
- Long AB, Wilson IM, Terry TT, Van Sciver RE, Caspary T. ARL13B-Cerulean rescues Arl13b-null mouse from embryonic lethality and reveals a role for ARL13B in spermatogenesis. bioRxiv 2025 Aug 18;.
- Fakhari S, Campolina-Silva G, Asayesh F, Girardet L, Scott-Boyer MP, Droit A, Soulet D, Greener J, Belleannée C. Shear stress effects on epididymal epithelial cell via primary cilia mechanosensory signaling. J Cell Physiol 2025 Jan;240(1):e31475.
- Vinay L, Hess RA, Belleannée C. Human efferent ductules and epididymis display unique cell lineages with motile and primary cilia. Andrology 2025 May;13(4):894-910.
- Long X, Chen L, Xiao X, Min X, Wu Y, Yang Z, Wen X. Structure, function, and research progress of primary cilia in reproductive physiology and reproductive diseases. Front Cell Dev Biol 2024;12:1418928.
- Lee V, Hinton BT, Hirashima T. Collective cell dynamics and luminal fluid flow in the epididymis: A mechanobiological perspective. Andrology 2024 Jul;12(5):939-948.
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