Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis

Cosimo De Bari, F. Dell'Accio, J. Vanlauwe, J. Eyckmans, I. M. Khan, C. W. Archer, E. A. Jones, D. Mcgonagle, T. A. Mitsiadis, C. Pitzalis, F. P. Luyten

Research output: Contribution to journalArticle

283 Citations (Scopus)

Abstract

Objective. To investigate whether periosteal cells from adult humans have features of multipotent mesenchymal stem cells (MSCs) at the single-cell level.

Methods. Cell populations were enzymatically released from the periosteum of the proximal tibia obtained from adult human donors and then expanded in monolayer. Single-cell-derived clonal populations were obtained by limiting dilution. Culture-expanded periosteal cell populations were tested for their growth potential and for expression of conventional markers of MSCs and were subjected to in vitro assays to investigate their multilineage potential. To assess their multipotency in vivo, periosteal cells were injected into a regenerating mouse tibialis anterior muscle for skeletal myogenesis or were either seeded into an osteoinductive matrix and implanted subcutaneously into nude mice for osteogenesis or implanted in a joint surface defect under a periosteal nap into goats for chondrogenesis. Cell phengtypes were analyzed by histochemistry and immunohistochemistry and by reverse transcription-polymerase chain reaction for the expression of lineagerelated marker genes.

Results. Regardless of donor age, periosteal cells were clonogenic and could be expanded extensively in monolayer, maintaining linear growth curves over at least 30 population doublings. They displayed long telomeres and expressed markers of MSCs. Under specific conditions, both parental and single-cell-derived clonal cell populations differentiated to the chondrocyte, osteoblast, adipocyte, and skeletal myocyte lineages in vitro and in vivo.

Conclusion. Our study demonstrates that, regardless of donor age, the adult human periosteum contains cells that, upon enzymatic release and culture expansion, are multipotent MSCs at the single-cell level.

Original languageEnglish
Pages (from-to)1209-1221
Number of pages12
JournalArthritis & Rheumatism
Volume54
Issue number4
DOIs
Publication statusPublished - Apr 2006

Keywords

  • human articular-cartilage
  • tissue-engineered bone
  • marrow stromal cells
  • stem-cells
  • progenitor cells
  • osteochondrogenic differentiation
  • morphogenetic proteins
  • phenotypic stability
  • synovial-membrane
  • adipose-tissue

Cite this

De Bari, C., Dell'Accio, F., Vanlauwe, J., Eyckmans, J., Khan, I. M., Archer, C. W., ... Luyten, F. P. (2006). Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis & Rheumatism, 54(4), 1209-1221. https://doi.org/10.1002/ART.21753

Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. / De Bari, Cosimo; Dell'Accio, F.; Vanlauwe, J.; Eyckmans, J.; Khan, I. M.; Archer, C. W.; Jones, E. A.; Mcgonagle, D.; Mitsiadis, T. A.; Pitzalis, C.; Luyten, F. P.

In: Arthritis & Rheumatism, Vol. 54, No. 4, 04.2006, p. 1209-1221.

Research output: Contribution to journalArticle

De Bari, C, Dell'Accio, F, Vanlauwe, J, Eyckmans, J, Khan, IM, Archer, CW, Jones, EA, Mcgonagle, D, Mitsiadis, TA, Pitzalis, C & Luyten, FP 2006, 'Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis' Arthritis & Rheumatism, vol. 54, no. 4, pp. 1209-1221. https://doi.org/10.1002/ART.21753
De Bari, Cosimo ; Dell'Accio, F. ; Vanlauwe, J. ; Eyckmans, J. ; Khan, I. M. ; Archer, C. W. ; Jones, E. A. ; Mcgonagle, D. ; Mitsiadis, T. A. ; Pitzalis, C. ; Luyten, F. P. / Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. In: Arthritis & Rheumatism. 2006 ; Vol. 54, No. 4. pp. 1209-1221.
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abstract = "Objective. To investigate whether periosteal cells from adult humans have features of multipotent mesenchymal stem cells (MSCs) at the single-cell level.Methods. Cell populations were enzymatically released from the periosteum of the proximal tibia obtained from adult human donors and then expanded in monolayer. Single-cell-derived clonal populations were obtained by limiting dilution. Culture-expanded periosteal cell populations were tested for their growth potential and for expression of conventional markers of MSCs and were subjected to in vitro assays to investigate their multilineage potential. To assess their multipotency in vivo, periosteal cells were injected into a regenerating mouse tibialis anterior muscle for skeletal myogenesis or were either seeded into an osteoinductive matrix and implanted subcutaneously into nude mice for osteogenesis or implanted in a joint surface defect under a periosteal nap into goats for chondrogenesis. Cell phengtypes were analyzed by histochemistry and immunohistochemistry and by reverse transcription-polymerase chain reaction for the expression of lineagerelated marker genes.Results. Regardless of donor age, periosteal cells were clonogenic and could be expanded extensively in monolayer, maintaining linear growth curves over at least 30 population doublings. They displayed long telomeres and expressed markers of MSCs. Under specific conditions, both parental and single-cell-derived clonal cell populations differentiated to the chondrocyte, osteoblast, adipocyte, and skeletal myocyte lineages in vitro and in vivo.Conclusion. Our study demonstrates that, regardless of donor age, the adult human periosteum contains cells that, upon enzymatic release and culture expansion, are multipotent MSCs at the single-cell level.",
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T1 - Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis

AU - De Bari, Cosimo

AU - Dell'Accio, F.

AU - Vanlauwe, J.

AU - Eyckmans, J.

AU - Khan, I. M.

AU - Archer, C. W.

AU - Jones, E. A.

AU - Mcgonagle, D.

AU - Mitsiadis, T. A.

AU - Pitzalis, C.

AU - Luyten, F. P.

PY - 2006/4

Y1 - 2006/4

N2 - Objective. To investigate whether periosteal cells from adult humans have features of multipotent mesenchymal stem cells (MSCs) at the single-cell level.Methods. Cell populations were enzymatically released from the periosteum of the proximal tibia obtained from adult human donors and then expanded in monolayer. Single-cell-derived clonal populations were obtained by limiting dilution. Culture-expanded periosteal cell populations were tested for their growth potential and for expression of conventional markers of MSCs and were subjected to in vitro assays to investigate their multilineage potential. To assess their multipotency in vivo, periosteal cells were injected into a regenerating mouse tibialis anterior muscle for skeletal myogenesis or were either seeded into an osteoinductive matrix and implanted subcutaneously into nude mice for osteogenesis or implanted in a joint surface defect under a periosteal nap into goats for chondrogenesis. Cell phengtypes were analyzed by histochemistry and immunohistochemistry and by reverse transcription-polymerase chain reaction for the expression of lineagerelated marker genes.Results. Regardless of donor age, periosteal cells were clonogenic and could be expanded extensively in monolayer, maintaining linear growth curves over at least 30 population doublings. They displayed long telomeres and expressed markers of MSCs. Under specific conditions, both parental and single-cell-derived clonal cell populations differentiated to the chondrocyte, osteoblast, adipocyte, and skeletal myocyte lineages in vitro and in vivo.Conclusion. Our study demonstrates that, regardless of donor age, the adult human periosteum contains cells that, upon enzymatic release and culture expansion, are multipotent MSCs at the single-cell level.

AB - Objective. To investigate whether periosteal cells from adult humans have features of multipotent mesenchymal stem cells (MSCs) at the single-cell level.Methods. Cell populations were enzymatically released from the periosteum of the proximal tibia obtained from adult human donors and then expanded in monolayer. Single-cell-derived clonal populations were obtained by limiting dilution. Culture-expanded periosteal cell populations were tested for their growth potential and for expression of conventional markers of MSCs and were subjected to in vitro assays to investigate their multilineage potential. To assess their multipotency in vivo, periosteal cells were injected into a regenerating mouse tibialis anterior muscle for skeletal myogenesis or were either seeded into an osteoinductive matrix and implanted subcutaneously into nude mice for osteogenesis or implanted in a joint surface defect under a periosteal nap into goats for chondrogenesis. Cell phengtypes were analyzed by histochemistry and immunohistochemistry and by reverse transcription-polymerase chain reaction for the expression of lineagerelated marker genes.Results. Regardless of donor age, periosteal cells were clonogenic and could be expanded extensively in monolayer, maintaining linear growth curves over at least 30 population doublings. They displayed long telomeres and expressed markers of MSCs. Under specific conditions, both parental and single-cell-derived clonal cell populations differentiated to the chondrocyte, osteoblast, adipocyte, and skeletal myocyte lineages in vitro and in vivo.Conclusion. Our study demonstrates that, regardless of donor age, the adult human periosteum contains cells that, upon enzymatic release and culture expansion, are multipotent MSCs at the single-cell level.

KW - human articular-cartilage

KW - tissue-engineered bone

KW - marrow stromal cells

KW - stem-cells

KW - progenitor cells

KW - osteochondrogenic differentiation

KW - morphogenetic proteins

KW - phenotypic stability

KW - synovial-membrane

KW - adipose-tissue

U2 - 10.1002/ART.21753

DO - 10.1002/ART.21753

M3 - Article

VL - 54

SP - 1209

EP - 1221

JO - Arthritis & Rheumatism

JF - Arthritis & Rheumatism

SN - 0004-3591

IS - 4

ER -