Essential role of the RNA-binding protein HuR in progenitor cell survival in mice

J Clin Invest. 2009 Dec;119(12):3530-43. doi: 10.1172/JCI38263. Epub 2009 Nov 2.

Abstract

The RNA-binding protein HuR (also known as ELAV1) binds to the 3'-untranslated region of mRNAs and regulates transcript stability and translation. However, the in vivo functions of HuR are not well understood. Here, we report that murine HuR is essential for life; postnatal global deletion of Elavl1 induced atrophy of hematopoietic organs, extensive loss of intestinal villi, obstructive enterocolitis, and lethality within 10 days. Upon Elavl1 deletion, progenitor cells in the BM, thymus, and intestine underwent apoptosis, whereas quiescent stem cells and differentiated cells were unaffected. The survival defect of hematopoietic progenitor cells was cell intrinsic, as transplant of Elavl1-/- BM led to compromised hematopoietic reconstitution but did not cause lethality. Expression of p53 and its downstream effectors critical for cell death were induced in progenitor cells as HuR levels declined. In mouse embryonic fibroblasts, HuR bound to and stabilized the mRNA for Mdm2, a critical negative regulator of p53. Furthermore, cell survival was restored by expression of Mdm2 in Elavl1-/- cells, suggesting that HuR keeps p53 levels in check in progenitor cells and thereby promotes cell survival. This regulation of cell stress response by HuR in progenitor cells, which we believe to be novel, could potentially be exploited in cytotoxic anticancer therapies as well as stem cell transplant therapy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, Surface / genetics
  • Antigens, Surface / metabolism*
  • Apoptosis
  • Cell Differentiation
  • Cell Survival / genetics
  • Cell Survival / physiology
  • ELAV Proteins
  • ELAV-Like Protein 1
  • Female
  • Gastrointestinal Tract / cytology
  • Gastrointestinal Tract / drug effects
  • Gastrointestinal Tract / metabolism
  • Gene Deletion
  • Hematopoiesis / drug effects
  • Hematopoiesis / genetics
  • Hematopoiesis / physiology
  • Hematopoietic Stem Cells / cytology*
  • Hematopoietic Stem Cells / drug effects
  • Hematopoietic Stem Cells / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Models, Biological
  • Proto-Oncogene Proteins c-mdm2 / genetics
  • Proto-Oncogene Proteins c-mdm2 / metabolism
  • RNA Stability
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Radiation Tolerance
  • Tamoxifen / toxicity
  • Transplantation Chimera
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Antigens, Surface
  • ELAV Proteins
  • ELAV-Like Protein 1
  • ELAVL1 protein, human
  • RNA, Messenger
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • Tamoxifen
  • Mdm2 protein, mouse
  • Proto-Oncogene Proteins c-mdm2