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Natural history of mesenchymal stem cells, from vessel walls to culture vessels

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Abstract

Mesenchymal stem/stromal cells (MSCs) can regenerate tissues by direct differentiation or indirectly by stimulating angiogenesis, limiting inflammation, and recruiting tissue-specific progenitor cells. MSCs emerge and multiply in long-term cultures of total cells from the bone marrow or multiple other organs. Such a derivation in vitro is simple and convenient, hence popular, but has long precluded understanding of the native identity, tissue distribution, frequency, and natural role of MSCs, which have been defined and validated exclusively in terms of surface marker expression and developmental potential in culture into bone, cartilage, and fat. Such simple, widely accepted criteria uniformly typify MSCs, even though some differences in potential exist, depending on tissue sources. Combined immunohistochemistry, flow cytometry, and cell culture have allowed tracking the artifactual cultured mesenchymal stem/stromal cells back to perivascular anatomical regions. Presently, both pericytes enveloping microvessels and adventitial cells surrounding larger arteries and veins have been described as possible MSC forerunners. While such a vascular association would explain why MSCs have been isolated from virtually all tissues tested, the origin of the MSCs grown from umbilical cord blood remains unknown. In fact, most aspects of the biology of perivascular MSCs are still obscure, from the emergence of these cells in the embryo to the molecular control of their activity in adult tissues. Such dark areas have not compromised intents to use these cells in clinical settings though, in which purified perivascular cells already exhibit decisive advantages over conventional MSCs, including purity, thorough characterization and, principally, total independence from in vitro culture. A growing body of experimental data is currently paving the way to the medical usage of autologous sorted perivascular cells for indications in which MSCs have been previously contemplated or actually used, such as bone regeneration and cardiovascular tissue repair.

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Abbreviations

AGM:

Aorta-gonad-mesonephros

BGP:

β-glycerophosphate

BM:

Bone marrow

BMP:

Bone morphogenetic protein

CB:

Cord blood

CD:

Cluster of differentiation

CFU:

Colony-forming unit

CPD:

Cumulative population doubling

CSC:

Cardiac stem cell

DLK-1:

Delta-like 1

ECM:

Extracellular matrix

EPC:

Endothelial progenitor cell

FACS:

Fluorescence-activated cell sorting

FDA:

Food and Drug Administration

HGF:

Hepatocyte growth factor

HLADR:

Human leukocyte antigen-DR

HSC:

Hematopoietic stem cell

IBMX:

3-isobutyl-1-methylxanthine

IGF:

Insulin-like growth factor

ISCT:

International Society for Cellular Therapy

Lep-R:

Leptin receptor

mAbs:

Monoclonal antibodies

MAPC:

Multipotent adult progenitor cell

MASC:

Multipotent adult stem cell

MCAM:

Melanoma cell adhesion molecule

MI:

Myocardial infarction

MIAMI:

Marrow-isolated adult multilineage inducible cell

MLPC:

Multilineage progenitor cell

MSC:

Mesenchymal stem cell

NELL1:

Nel-like molecule 1

OVX:

Ovariectomized

PDGFRβ:

Platelet-derived growth factor receptor β

PSC:

Perivascular stem cell

SCF:

Stem cell factor

SVF:

Stromal vascular fraction

SVP:

Saphenous vein pericyte

USSC:

Unrestricted somatic stem cell

VCAM:

Vascular cell adhesion molecule

VEGF:

Vascular endothelial growth factor

VESL:

Very small embryonic-like stem cell

vWF:

von Willebrand factor

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Disclosure

B.P., and C.S. are inventors of perivascular stem cell-related patents filed from UCLA. Dr C.S. is a founder of Scarless Laboratories Inc. which sublicenses perivascular stem cell-related patents from the UC Regents, and who also hold equity in the company. Dr C.S. is also an officer of Scarless Laboratories, Inc. This work was supported by the CIRM Early Translational II Research Award TR2-01821.

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Authors and Affiliations

  1. MRC Center for Regenerative Medicine, University of Edinburgh, Edinburgh, UK

    Iain R. Murray, Christopher C. West, Tulyapruek Tawonsawatruk & Bruno Péault

  2. BHF Center for Cardiovascular Science, Queens Medical Research Institute, University of Edinburgh, Edinburgh, UK

    Iain R. Murray, Christopher C. West, Tulyapruek Tawonsawatruk & Bruno Péault

  3. Orthopedic Hospital Research Center and Broad Stem Cell Center, David Geffen School of Medicine, University of California, Los Angeles, USA

    Iain R. Murray, Winters R. Hardy & Bruno Péault

  4. Indiana Center for Vascular Biology and Medicine, Indianapolis, USA

    Winters R. Hardy

  5. Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los Angeles, USA

    Aaron W. James & Alan Nguyen

  6. Institute for Cell Engineering, Johns Hopkins School of Medicine, Baltimore, USA

    Tea Soon Park

  7. Cell Factory, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy

    Lorenza Lazzari

  8. Division of Plastic and Reconstructive Surgery, Departments of Surgery and Orthopedic Surgery, David Geffen School of Medicine, University of California, Los Angeles, USA

    Chia Soo

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  1. Iain R. Murray
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  2. Christopher C. West
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  3. Winters R. Hardy
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  5. Tea Soon Park
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  6. Alan Nguyen
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  7. Tulyapruek Tawonsawatruk
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  8. Lorenza Lazzari
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  9. Chia Soo
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  10. Bruno Péault
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Corresponding author

Correspondence to Bruno Péault.

Additional information

C. C. West, W. R. Hardy, A. W. James, and T. S. Park contributed equally to this work.

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Murray, I.R., West, C.C., Hardy, W.R. et al. Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell. Mol. Life Sci. 71, 1353–1374 (2014). https://doi.org/10.1007/s00018-013-1462-6

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  • DOI: https://doi.org/10.1007/s00018-013-1462-6

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