VEGFC/VEGFR3 Signaling Regulates Mouse Spermatogonial Cell Proliferation via the Activation of AKT/MAPK and Cyclin D1 Pathway and Mediates the Apoptosis by affecting Caspase 3/9 and Bcl-2

Cell Cycle. 2018;17(2):225-239. doi: 10.1080/15384101.2017.1407891. Epub 2018 Jan 2.

Abstract

We have previously shown that the transcript levels of Vegfc and its receptor Vegfr3 were high in spermatogonia and extremely low in spermatocytes and spermatids. However, it remains unknown about the functions and the mechanisms of VEGFC/VEGFR3 signaling in regulating the fate determinations of spermatogonia. To this end, here we explored the role and signaling pathways of VEGFC/VEGFR3 by using a cell line derived from immortalized mouse spermatogonia retaining markers of mitotic germ cells, namely GC-1 cells. VEGFR3 was expressed in mouse primary spermatogonia and GC-1 cells. VEGFC stimulated the proliferation and DNA synthesis of GC-1 cells and enhanced the phosphorylation of PI3K-AKT and MAPK, whereas LY294002 (an inhibitor for AKT) and CI-1040 (an inhibitor for MAPK) blocked the effect of VEGFC on GC-1 cell proliferation. Furthermore, VEGFC increased the transcripts of c-fos and Egr1 and protein levels of cyclin D1, PCNA and Bcl-2. Conversely, the blocking of VEGFC/VEGFR3 signaling by VEGFR3 knockdown reduced the phosphorylation of AKT/MAPK and decreased the levels of cyclin D1 and PCNA. Additionally, VEGFR3 knockdown not only resulted in more apoptosis of GC-1 cells but also led to a decrease of Bcl-2 and promoted the cleavage of Caspase-3/9 and PARP. Collectively, these data suggested that VEGFC/VEGFR3 signaling promotes the proliferation of GC-1 cells via the AKT /MAPK and cyclin D1 pathway and it inhibits the cell apoptosis through Caspase-3/9, PARP and Bcl-2. Thus, this study sheds a novel insight to the molecular mechanisms underlying the fate decisions of mammalian spermatogonia.

Keywords: AKT; GC-1 cells; MAPK; VEGFC/VEGFR3; apoptosis; proliferation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Caspase 3 / metabolism
  • Caspase 9 / metabolism
  • Cell Line
  • Cell Proliferation*
  • Cyclin D1 / metabolism
  • Early Growth Response Protein 1 / biosynthesis
  • Early Growth Response Protein 1 / genetics
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Indoles / pharmacology
  • Male
  • Mice
  • Mice, Inbred ICR
  • Naphthalenes / pharmacology
  • Phosphatidylinositol 3-Kinase / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Proto-Oncogene Proteins c-fos / biosynthesis
  • Proto-Oncogene Proteins c-fos / genetics
  • Signal Transduction*
  • Spermatogonia / cytology
  • Spermatogonia / drug effects
  • Spermatogonia / enzymology
  • Spermatogonia / metabolism*
  • Vascular Endothelial Growth Factor C / genetics
  • Vascular Endothelial Growth Factor C / metabolism
  • Vascular Endothelial Growth Factor C / physiology*
  • Vascular Endothelial Growth Factor Receptor-3 / antagonists & inhibitors
  • Vascular Endothelial Growth Factor Receptor-3 / genetics
  • Vascular Endothelial Growth Factor Receptor-3 / metabolism*
  • Vascular Endothelial Growth Factor Receptor-3 / physiology

Substances

  • 3-(4-dimethylamino-naphthalen-1-ylmethylene)-1,3-dihydro-indol-2-one
  • Ccnd1 protein, mouse
  • Early Growth Response Protein 1
  • Egr1 protein, mouse
  • Indoles
  • Naphthalenes
  • Proto-Oncogene Proteins c-bcl-2
  • Proto-Oncogene Proteins c-fos
  • Vascular Endothelial Growth Factor C
  • vascular endothelial growth factor C, mouse
  • Bcl2 protein, mouse
  • Cyclin D1
  • Phosphatidylinositol 3-Kinase
  • Vascular Endothelial Growth Factor Receptor-3
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • Caspase 3
  • Caspase 9