Activation of Notch1 signalling promotes multi-lineage differentiation of c-Kit(POS)/NKX2.5(POS) bone marrow stem cells: implication in stem cell translational medicine

Stem Cell Res Ther. 2015 May 9;6(1):91. doi: 10.1186/s13287-015-0085-2.

Abstract

Introduction: Transplantation of bone marrow mesenchymal stem cells (BMSCs) can repair injured hearts. However, whether BMSC populations contain cells with cardiac stem cell characteristics is ill-defined. We report here that Notch signalling can promote differentiation of c-Kit(POS)/NKX2.5(POS) BMSCs into cardiomyocyte-like cells.

Methods: Total BMSCs were isolated from Sprague-Dawley rat femurs and c-Kit(POS) cells were purified. c-Kit(POS)/NKX2.5(POS) cells were isolated by single-cell cloning, and the presence of cardiomyocyte, smooth muscle cell (SMC), and endothelial cell differentiation markers assessed by immunofluorescence staining and semi-quantitative reverse-transcription polymerase chain reaction (RT-PCR) analysis. Levels of c-Kit and Notch1-4 in total BMSCs and c-Kit(POS)/NKX2.5(POS) BMSCs were quantitated by flow cytometry. Following infection with an adenovirus over-expressing Notch1 intracellular domain (NICD), total BMSCs and c-Kit(POS)/NKX2.5(POS) cells were assessed for differentiation to cardiomyocyte, SMC, and endothelial cell lineages by immunofluorescence staining and real-time quantitative RT-PCR. Total BMSCs and c-Kit(POS)/NKX2.5(POS) cells were treated with the Notch1 ligand Jagged1 and markers of cardiomyocyte, SMC, and endothelial cell differentiation were examined by immunofluorescence staining and real-time quantitative RT-PCR analysis.

Results: c-Kit(POS)/NKX2.5(POS) cells were present among total BMSC populations, and these cells did not express markers of adult cardiomyocyte, SMC, or endothelial cell lineages. c-Kit(POS)/NKX2.5(POS) BMSCs exhibited a multi-lineage differentiation potential similar to total BMSCs. Following sorting, the c-Kit level in c-Kit(POS)/NKX2.5(POS) BMSCs was 84.4%. Flow cytometry revealed that Notch1 was the predominant Notch receptor present in total BMSCs and c-Kit(POS)/NKX2.5(POS) BMSCs. Total BMSCs and c-Kit(POS)/NKX2.5(POS) BMSCs overexpressing NICD had active Notch1 signalling accompanied by differentiation into cardiomyocyte, SMC, and endothelial cell lineages. Treatment of total BMSCs and c-Kit(POS)/NKX2.5(POS) BMSCs with exogenous Jagged1 activated Notch1 signalling and drove multi-lineage differentiation, with a tendency towards cardiac lineage differentiation in c-Kit(POS)/NKX2.5(POS) BMSCs.

Conclusions: c-Kit(POS)/NKX2.5(POS) cells exist in total BMSC pools. Activation of Notch1 signalling contributed to multi-lineage differentiation of c-Kit(POS)/NKX2.5(POS) BMSCs, favouring differentiation into cardiomyocytes. These findings suggest that modulation of Notch1 signalling may have potential utility in stem cell translational medicine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / cytology*
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Cell Differentiation
  • Cell Lineage
  • Cells, Cultured
  • Endothelial Cells / cytology
  • Homeobox Protein Nkx-2.5
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Jagged-1 Protein
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism*
  • Microfilament Proteins / metabolism
  • Microscopy, Fluorescence
  • Muscle Proteins / metabolism
  • Myocytes, Cardiac / cytology
  • Myocytes, Smooth Muscle / cytology
  • Proto-Oncogene Proteins c-kit / genetics
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Notch1 / chemistry
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism*
  • Serrate-Jagged Proteins
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Troponin T / genetics
  • Troponin T / metabolism
  • von Willebrand Factor / genetics
  • von Willebrand Factor / metabolism

Substances

  • Calcium-Binding Proteins
  • Homeobox Protein Nkx-2.5
  • Homeodomain Proteins
  • Intercellular Signaling Peptides and Proteins
  • Jag1 protein, rat
  • Jagged-1 Protein
  • Membrane Proteins
  • Microfilament Proteins
  • Muscle Proteins
  • Nkx2-5 protein, rat
  • Notch1 protein, rat
  • Receptor, Notch1
  • Serrate-Jagged Proteins
  • Transcription Factors
  • Troponin T
  • Von Willebrand antigen
  • transgelin
  • von Willebrand Factor
  • Proto-Oncogene Proteins c-kit