Stromal cell-derived factor 1 regulates in vitro sperm migration towards the cumulus-oocyte complex in cattle

PLoS One. 2020 Apr 30;15(4):e0232536. doi: 10.1371/journal.pone.0232536. eCollection 2020.

Abstract

Sperm migration towards an oocyte in the female reproductive tract is an important step for successful fertilization. Although several sperm-chemotactic factors have been identified in mammals, it is unclear whether these chemoattractants contribute to sperm migration towards an oocyte that is the final destination for sperm. Furthermore, chemoattractants for bovine sperm are still undiscovered even though the follicular fluid attracts sperm in cattle. Here, we demonstrated that a single bovine cumulus-oocyte complex (COC) had the ability to attract sperm, suggesting that the COC secreted sperm chemoattractants. We identified stromal cell-derived factor 1 (SDF1), which was expressed in COCs, and its receptor CXCR4 in sperm, as a candidate. Our results showed that bovine sperm preferentially migrated to the area with a high SDF1 concentration and occasionally showed turn movements by asymmetric flagellar bends during the migration. We also demonstrated that increasing the intracellular Ca2+ concentration via Ca2+ channels was related to SDF1-induced sperm chemotaxis. Finally, a CXCR4 inhibitor significantly suppressed the in vitro bovine sperm migration towards a COC. Taken together, we propose that SDF1 is a chemotactic factor for bovine sperm to regulate their migration towards an oocyte via the CXCR4 receptor.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Animals
  • Cattle
  • Chemokine CXCL12 / metabolism*
  • Chemotaxis / physiology*
  • Cumulus Cells / metabolism
  • Female
  • Fertilization in Vitro / veterinary
  • Intravital Microscopy
  • Male
  • Oocytes / metabolism
  • Receptors, CXCR4 / metabolism*
  • Sperm Motility / physiology*
  • Spermatozoa / physiology

Substances

  • Chemokine CXCL12
  • Receptors, CXCR4

Grants and funding

This work was supported by a Grant-in-Aid for JSPS Fellows (grant No. JP17J02431, K. U.), and MEXT KAKENHI (grant No. JP19H05237, K. H.). Miyagi Agricultural Development Corporation provided support in the form of salaries for author T. N., but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of this author are articulated in the ‘author contributions’ section.