Rapamycin promotes the osteoblastic differentiation of human embryonic stem cells by blocking the mTOR pathway and stimulating the BMP/Smad pathway

Stem Cells Dev. 2010 Apr;19(4):557-68. doi: 10.1089/scd.2009.0147.

Abstract

Studies revealed that PI3K/AKT/mTOR signaling is important in the regulation of human embryonic stem cell (hESC) self-renewal and differentiation. However, its action on osteogenic differentiation of hESCs is poorly understood. We tested the effects of pharmacological PI3K/AKT/mTOR inhibitors on their potential to induce osteogenic differentiation of hESCs. Under feeder-free culture conditions, rapamycin (an mTOR inhibitor) potently inhibited the activities of mTOR and p70S6K in undifferentiated hESCs; however, LY294002 (a PI3K inhibitor) and an AKT inhibitor had no effects. Treatment with any of these inhibitors down-regulated the hESC markers Oct4 and Nanog, but only rapamycin induced the up-regulation of the early osteogenic markers BMP2 and Runx2. We also observed that hESCs differentiated when treated with FK506, a structural analog of rapamycin, but did not exhibit an osteogenic phenotype. Increases in Smad1/5/8 phosphorylation and Id1-4 mRNA expression indicated that rapamycin significantly stimulated BMP/Smad signaling. After inducing both hESCs and human embryoid bodies (hEBs) for 2-3 weeks with rapamycin, osteoblastic differentiation was further characterized by the expression of osteoblastic marker mRNAs and/or proteins (osterix, osteocalcin, osteoprotegerin, osteonectin, and bone sialoprotein), alkaline phosphatase activity, and alizarin red S staining for mineralized bone nodule formation. No significant differences in the osteogenic phenotypes of rapamycin-differentiated hESCs and hEBs were detected. Our results suggest that, among these 3 inhibitors, only rapamycin functions as a potent stimulator of osteoblastic differentiation of hESCs, and it does so by modulating rapamycin-sensitive mTOR and BMP/Smad signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biomarkers
  • Bone Morphogenetic Protein Receptors / genetics
  • Bone Morphogenetic Protein Receptors / metabolism
  • Cell Differentiation / drug effects*
  • Cell Line
  • Chromones / pharmacology
  • Core Binding Factor Alpha 1 Subunit / genetics
  • Embryonic Stem Cells / cytology*
  • Embryonic Stem Cells / drug effects
  • Embryonic Stem Cells / metabolism
  • Enzyme Inhibitors / pharmacology
  • Homeodomain Proteins / genetics
  • Humans
  • Immunosuppressive Agents / pharmacology
  • Inhibitor of Differentiation Protein 1 / genetics
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Morpholines / pharmacology
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3 / genetics
  • Osteoblasts* / cytology
  • Osteoblasts* / metabolism
  • Osteogenesis* / drug effects
  • Osteogenesis* / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Signal Transduction / drug effects
  • Sirolimus / pharmacology*
  • Smad Proteins / metabolism
  • TOR Serine-Threonine Kinases
  • Tacrolimus / pharmacology

Substances

  • Biomarkers
  • Chromones
  • Core Binding Factor Alpha 1 Subunit
  • Enzyme Inhibitors
  • Homeodomain Proteins
  • ID1 protein, human
  • Immunosuppressive Agents
  • Inhibitor of Differentiation Protein 1
  • Intracellular Signaling Peptides and Proteins
  • Morpholines
  • NANOG protein, human
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3
  • POU5F1 protein, human
  • Phosphoinositide-3 Kinase Inhibitors
  • RNA, Messenger
  • Smad Proteins
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • MTOR protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Ribosomal Protein S6 Kinases, 70-kDa
  • TOR Serine-Threonine Kinases
  • Bone Morphogenetic Protein Receptors
  • Sirolimus
  • Tacrolimus