Transcriptional profile of native CD271+ multipotential stromal cells: evidence for multiple fates, with prominent osteogenic and Wnt pathway signaling activity

Arthritis Rheum. 2012 Aug;64(8):2632-43. doi: 10.1002/art.34434.

Abstract

Objective: Controversy surrounds the identity and functionality of rare bone marrow-derived multipotential stromal cells (BM-MSCs), including their differentiation capabilities, their relationship to pericytes and hematopoiesis-supporting stromal cells, and the relevance of their culture-expanded progeny in studies of skeletal biology and development of cell-based therapies. The aim of this study was to clarify the nature of candidate BM-MSCs by profiling transcripts that reflect different aspects of their putative functions in vivo.

Methods: Rare, sorted BM-derived CD45(-/low) CD271(bright) (CD271) cells were analyzed using 96-gene expression arrays focused on transcripts relevant to mesenchymal-lineage differentiation (toward bone, cartilage, fat, or muscle), hematopoietic and stromal support, and molecules critical to skeletal homeostasis. These cells were compared to matched CD45+ CD271- hematopoietic-lineage cells, culture-expanded MSCs, and skin fibroblasts. When feasible, transcription was validated using flow cytometry.

Results: CD271 cells had a transcriptional profile consistent with the multiple fates of in vivo MSCs, evident from the observed simultaneous expression of osteogenic, adipogenic, pericytic, and hematopoiesis-supporting genes (e.g., SP7 [osterix], FABP4 [fatty acid binding protein 4], ANGPT1 [angiopoietin 1], and CXCL12 [stromal cell-derived factor 1], respectively). Compared to culture-expanded MSCs and fibroblasts, CD271 cells exhibited greater transcriptional activity, particularly with respect to Wnt-related genes (>1,000-fold increased expression of FRZB [secreted frizzled-related protein 3] and WIF1 [Wnt inhibitory factor 1]). A number of transcripts were identified as novel markers of MSCs.

Conclusion: The native, BM-derived in vivo MSC population is endowed with a gene signature that is compatible with multiple functions, reflecting the topographic bone niche of these cells, and their signature is significantly different from that of culture-expanded MSCs. This indicates that studies of the biologic functions of MSCs in musculoskeletal diseases, including osteoporosis and osteoarthritis, should focus on in vivo MSCs, rather than their culture-adapted progeny.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Angiopoietin-1 / metabolism
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / metabolism*
  • Cell Differentiation / physiology*
  • Cells, Cultured
  • Chemokine CXCL12 / metabolism
  • Child
  • Child, Preschool
  • Fatty Acid-Binding Proteins / metabolism
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Humans
  • Leukocyte Common Antigens / metabolism
  • Middle Aged
  • Multipotent Stem Cells / cytology
  • Multipotent Stem Cells / metabolism*
  • Nerve Tissue Proteins / metabolism*
  • Osteogenesis / physiology*
  • Receptors, Nerve Growth Factor / metabolism*
  • Skin / cytology
  • Sp7 Transcription Factor
  • Stromal Cells / cytology
  • Stromal Cells / metabolism*
  • Transcription Factors / metabolism
  • Transcriptome*
  • Wnt Signaling Pathway / physiology*
  • Young Adult

Substances

  • ANGPT1 protein, human
  • Angiopoietin-1
  • CXCL12 protein, human
  • Chemokine CXCL12
  • FABP4 protein, human
  • Fatty Acid-Binding Proteins
  • NGFR protein, human
  • Nerve Tissue Proteins
  • Receptors, Nerve Growth Factor
  • Sp7 Transcription Factor
  • SP7 protein, human
  • Transcription Factors
  • Leukocyte Common Antigens
  • PTPRC protein, human