Antagonism between JAK/STAT downstream targets controls stem cell proliferation, cell fate conversion and tumorigenesis

Development. 2025 Nov 1;152(21):dev204701. doi: 10.1242/dev.204701. Epub 2025 Oct 31.

Abstract

Proper proliferation and differentiation of adult stem cells maintains tissue homeostasis. However, how cell proliferation and fate conversion are regulated by niche signals remains poorly understood. Here, we systemically identify JAK/STAT downstream targets in adult Drosophila testis using multi-omics approaches. ubr5, encoding an HECT type E3 ligase, is identified as a putative JAK/STAT target. Depletion of ubr5 in somatic cyst cells affects the proliferation and differentiation of cyst stem cells (CySCs) and germline stem cells (GSCs). Importantly, ubr5-defective CySC-like cells adopt the fate of a group of quiescent somatic cells. Mechanistically, UBR5 interacts with Drumstick (Drm), another putative JAK/STAT target, through its UBR domain and mediates Drm poly-ubiquitination for proteolysis. Ectopic expression of drm mimics that in ubr5-depleted testes and further removal of drm significantly suppresses the defects observed in ubr5-depleted testes. Finally, the function of UBR5 in stem cell regulation is evolutionarily conserved. Collectively, antagonism between JAK/STAT targets controls JAK/STAT signaling duration, stem cell proliferation and/or differentiation, and cell fate conversion within the testicular niche. Thus, our study uncovers the mechanism underlying the proper control of stem cell proliferation and fate conversion during tissue homeostasis and tumorigenesis.

Keywords: Cyst stem cell; Drm; E3 ligase; Hyd; Testis; UBR5.

MeSH terms

  • Animals
  • Carcinogenesis* / genetics
  • Carcinogenesis* / metabolism
  • Carcinogenesis* / pathology
  • Cell Differentiation / genetics
  • Cell Proliferation / genetics
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Janus Kinases* / metabolism
  • Male
  • STAT Transcription Factors* / metabolism
  • Signal Transduction
  • Stem Cells* / cytology
  • Stem Cells* / metabolism
  • Testis / cytology
  • Testis / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism
  • Ubiquitination

Substances

  • Drosophila Proteins
  • STAT Transcription Factors
  • Janus Kinases
  • Ubiquitin-Protein Ligases