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A Perivascular Origin for Mesenchymal Stem Cells in Multiple Human Organs
Open accessAbstract
Mesenchymal stem cells (MSCs), the archetypal multipotent progenitor cells derived in cultures of developed organs, are of unknown identity and native distribution. We have prospectively identified perivascular cells, principally pericytes, in multiple human organs including skeletal muscle, pancreas, adipose tissue, and placenta, on CD146, NG2, and PDGF-Rbeta expression and absence of hematopoietic, endothelial, and myogenic cell markers. Perivascular cells purified from skeletal muscle or nonmuscle tissues were myogenic in culture and in vivo. Irrespective of their tissue origin, long-term cultured perivascular cells retained myogenicity; exhibited at the clonal level osteogenic, chondrogenic, and adipogenic potentials; expressed MSC markers; and migrated in a culture model of chemotaxis. Expression of MSC markers was also detected at the surface of native, noncultured perivascular cells. Thus, blood vessel walls harbor a reserve of progenitor cells that may be integral to the origin of the elusive MSCs and other related adult stem cells.
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“MSCs can function as perivascular-like support cells, physically associating with endothelial networks and promoting their architecture through direct contact mechanisms (Au et al., 2008; Crisan et al., 2008).”
From APOE3-Christchurch variant enhances neurovascular support functions of iPSC-derived mesenchymal stromal cells (2026) · cites this paper as Crisan et al., 2008
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“Subsequent studies have shown that peri-vascular cells, pericytes and fibroblasts from different tissues closely resemble the surface phenotype of MSCs, exhibit similar genome-wide expression profiles based on cluster analysis of microarray data and share similar functional properties based on qualitative in vitro ass…”
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“Multipotent adult stem cells have been isolated from all layers of blood vessel wall in skeletalmuscle and various other organs: intima contains endothelial progenitor cells (MECs), media of small blood vessels contains pericytes, and in large vessels smooth muscle cell progenitors (SMPCs), and the outermost layer con…”
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“The pro-SP-C /CD90þ cell was a pericyte in the alveolar wall (arrow).(47,48) (b) A”
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Rossini, A., Frati, C., Lagrasta, C. A., Graiani, G., Scopece, A., Cavalli, S., Musso, E., Baccarin, M., Segni, M. D., Fagnoni, F. F., et al. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq290 · Cited by 122
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BackgroundMesenchymal stem cells: The roles and functions in cutaneous wound healing and tumor growth
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“Although expressed by cardiac fibroblasts, this receptor is also expressed by immune cells [19], lymphatic endothelium [20], and pericytes [21], making its use limited, at least for immunohistological examination of fibroblasts.”
BackgroundThe secretome of mesenchymal stem cells: Potential implications for neuroregeneration
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“A population of mesenchymal stem cells (P-MSCs) was identified in the normal human and mouse pancreas [8,9]; however, whether MSCs are present in pancreatic carcinoma and what their function might be during carcinogenesis remained unclear.”
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“1): platelet-derived growth factor receptor β (PDGFRβ): receptor with tyrosin kinase activity, involved in pericytes proliferation and recruitment [11]; nerve-glial antigen-2 (NG2): membrane chondroitin sulfate proteoglycan involved in pericyte recruitment to tumor vasculature [12]; CD146: transmembrane glycoprotein t…”
BackgroundFOXO3-Engineered Human ESC-Derived Vascular Cells Promote Vascular Protection and Regeneration
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“MSCs are thought to have a perivascular origin, and can be derived from multiple human organs including bone marrow, skeletal muscle, placenta, pancreas, and adipose tissue [32].”
BackgroundThe effect of mesenchymal stem cell shape on the maintenance of multipotency
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“Recent evidence suggests MSCs are a subset of perivascular cells [18,19], reside around sinusoids [20], remain in a quiescent state [21], and maintain a niche for hematopoietic stem cells [22e24].”
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“Recent investigations suggest that MSCs are found as perivascular cells or pericytes (Crisan et al., 2008; Caplan, 2009).”
BackgroundMesenchymal Stem Cells Derived from Human Limbal Niche Cells
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Self-citationRegenerative Therapeutic Potential of Adipose Stromal Cells in Early Stage Diabetic Retinopathy
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“ASC are multipotential mesenchymal progenitor cells that we and others have recently demonstrated to have functional and phenotypic overlap with pericytes closely encircling microvessels in multiple human organs including adipose tissue [18,41,42].”
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“…2006; Malinowski et al., 2008), visceral and PVAT have been associated with angiogenesis (Rhoads et al., 2009), mesenchymal stem cell recruitment (Crisan et al., 2008), vascular smooth muscle cell (VSMC) growth (Wang et al., 2009), cardiomyocyte electrical activity (Kourliouros et al., 2010) and…”
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“Pericytes in organs are thought to possess multipotent progenitor cell characteristics (Crisan et al., 2008) and we next determined whether pericytes potentially present in the genetically labeled fibroblast pool could have contributed to calcification.”
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“However, mesenchymal stromal cells are located in the perivascular niche [32–35] and they secrete an array of cytokines and chemokines, including angiopoietin-1 [34].”
BackgroundGasperini, P., Espígol‐Frigolé, G., McCormick, P. J., Salvucci, O., Maric, D., Uldrick, T. S., Polizzotto, M. N., Yarchoan, R., & Tosato, G. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3067 · Cited by 115
“Because CD146 is also expressed in the vascular endothelium (21), we used CD31 costaining to distinguish between these cell types.”
BackgroundMethodInfluentialLin, R., Moreno‐Luna, R., Zhou, B., Pu, W. T., & Melero‐Martin, J. M. (2012) · Angiogenesis · doi:10.1007/s10456-012-9272-2 · Cited by 115
“Additionally, the presence of MSCs in the stromal vascular fraction of several adult tissues has been recently recognized [6, 7].”
BackgroundInfluentialMesenchymal Stem Cells in Tissue Growth and Repair
Kalinina, N., Sysoeva, V., Rubina, K. A., Parfenova, Y. V., & Va, T. (2011) · Acta Naturae · doi:10.32607/20758251-2011-3-4-30-37 · Cited by 116
Origin and function of tumor stroma fibroblasts
Xouri, G., & Christian, S. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.11.017 · Cited by 125
Human Dermis Harbors Distinct Mesenchymal Stromal Cell Subsets
Vaculik, C., Schuster, C., Bauer, W. M., Iram, N., Pfisterer, K., Kramer, G., Reinisch, A., Strunk, D., & Elbe‐Bürger, A. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.355 · Cited by 114
“CD146 is expressed on pericytes (Crisan et al., 2008) and all types of human endothelial cells (Bardin et al., 2001).”
BackgroundMesenchymal stromal/stem cells markers in the human bone marrow
Rasini, V., Dominici, M., Kluba, T., Siegel, G., Lusenti, G., Northoff, H., Horwitz, E. M., & Schäfer, R. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2012.11.009 · Cited by 114
Buxboim, A., Irianto, J., Swift, J., Athirasala, A., Shin, J., Rehfeldt, F., & Discher, D. E. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-06-0393 · Cited by 114
“Although all tissues are now understood to harbor MSCs as perivascular cells with a highly plastic phenotype (Crisan et al., 2008), it is surprising that a single stem cell type in culture, the MSC, shows the same four components with the same trend in variation, that is, SYNE2 > SYNE1 > LMNA > LBR.”
BackgroundNew Era of Cell-Based Orthopedic Therapies
Caplan, A. I. (2009) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2008.0515 · Cited by 114
“In some cases, the MSCs call up sentinels from other deposits 55 or we systemically supply additional contributors.”
Characterization of adipocyte differentiation from human mesenchymal stem cells in bone marrow
Qian, S.-W., Li, X., Zhang, Y.-Y., Huang, H.-Y., Liu, Y., Sun, X., & Tang, Q.-Q. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-47 · Cited by 114
“Recent studies indicate that pericytes in blood vessel walls have adipogenic potential, express mesenchymal stem cell (MSC) markers and are multipotent [4].”
BackgroundTang, Y., & Weiss, S. J. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1280643 · Cited by 114
The Fibrotic Scar in Neurological Disorders
Fernández‐Klett, F., & Priller, J. (2014) · Brain Pathology · doi:10.1111/bpa.12162 · Cited by 113
“Pericytes in many organs, including the brain, have also been identified as multipotent mesenchymal stromal cells (MSCs) that can differentiate into various tissues such as muscle, bone, cartilage and adipose tissue (12).”
BackgroundTissue-resident mesenchymal stromal cells: Implications for tissue-specific antifibrotic therapies
Lemos, D. R., & Duffield, J. S. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aan5174 · Cited by 115
Biologic Scaffold Remodeling in a Dog Model of Complex Musculoskeletal Injury
Turner, N. J., Badylak, J. S., Weber, D. J., & Badylak, S. F. (2011) · Journal of Surgical Research · doi:10.1016/j.jss.2011.11.1029 · Cited by 113
Self-citationStem Cells in Skin Wound Healing: Are We There Yet?
Cerqueira, M. T., Pirraco, R. P., & Marques, A. P. (2015) · Advances in Wound Care · doi:10.1089/wound.2014.0607 · Cited by 115
“Interestingly, these findings were also associated to a pericytic phenotype of undifferentiated transplanted cells also described by others(45) and in accordance to the reports that associate MSCs with perivascular niches and close/common origin with pericytes.(50,51) Despite being able to act as building blocks, stem…”
Spiekman, M., van Dongen, J. A., Willemsen, J. C. N., Hoppe, D. L., van der Lei, B., & Harmsen, M. C. (2017) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2213 · Cited by 117
Lee, M. W., Ryu, S., Kim, D. S., Lee, J. W., Sung, K. W., Koo, H. H., & Yoo, K. H. (2019) · Leukemia · doi:10.1038/s41375-018-0373-9 · Cited by 116
High-resolution 3D imaging uncovers organ-specific vascular control of tissue aging
Chen, J., Sivan, U., Tan, S. L., Lippo, L., Angelis, J. E. D., Labella, R., Singh, A., Chatzis, A., Cheuk, S., Medhghalchi, M., et al. (2021) · Science Advances · doi:10.1126/sciadv.abd7819 · Cited by 117
Fatty pancreas: A possible risk factor for pancreatic cancer in animals and humans
Takahashi, M., Hori, M., Ishigamori, R., Mutoh, M., Imai, T., & Nakagama, H. (2018) · Cancer Science · doi:10.1111/cas.13766 · Cited by 120
“Perivascular mesenchymal stem cells were shown to differentiate into adipocytes in an adipogenic differentiation medium containing dexamethasone, 3‐isobutyl‐1‐methylxanthine, insulin and indomethacin.(43) Hyperinsulinemia in obesity/ T2DM and stress‐induced glucocorticoid production may prompt the”
BackgroundMaki, T., Maeda, M., Uemura, M. T., Lo, E. K., Terasaki, Y., Liang, A. C., Shindo, A., Choi, Y. K., Taguchi, A., Matsuyama, T., et al. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.04.047 · Cited by 113
“In addition, mesenchymal stem cells may reside in the perivascular area and exhibit certain characteristics identical to a subclass of pericytes, presumably behaving as pericyte progenitor cells [8, 27].”
BackgroundJoos, H., Wildner, A., Hogrefe, C., Reichel, H., & Brenner, R. E. (2013) · Arthritis Research & Therapy · doi:10.1186/ar4299 · Cited by 111
“Their observation is in agreement with the hypothesis that the presence of cells with characteristics of MSC in adult vascularized tissues may be based on a common perivascular origin [35].”
ResultMatrix Composition and Mechanics Direct Proangiogenic Signaling from Mesenchymal Stem Cells
Abdeen, A. A., Weiss, J. B., Lee, J., & Kilian, K. A. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2013.0661 · Cited by 111
“MSCs are postulated to exist as pericytes in the vasculature within tissues where they are present.(8,9) The mechanism behind the therapeutic efficacy of MSCs is contentious.”
Darzi, S., Werkmeister, J. A., Deane, J. A., & Gargett, C. E. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0190 · Cited by 114
Origin and differentiation trajectories of fibroblastic reticular cells in the splenic white pulp
Cheng, H., Onder, L., Novković, M., Soneson, C., Lütge, M., Pikor, N. B., Scandella, E., Robinson, M. D., Miyazaki, J., Tersteegen, A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09728-3 · Cited by 111
Adipose-Derived Stem Cells in Bone Tissue Engineering: Useful Tools with New Applications
Storti, G., Scioli, M. G., Kim, B., Orlandi, A., & Cervelli, V. (2019) · Stem Cells International · doi:10.1155/2019/3673857 · Cited by 110
Isolation and Characterization of Human Anterior Cruciate Ligament-Derived Vascular Stem Cells
Matsumoto, T., Ingham, S. M., Mifune, Y., Osawa, A., Logar, A., Ūsas, A., Kuroda, R., Kurosaka, M., Fu, F. H., & Huard, J. (2011) · Stem Cells and Development · doi:10.1089/scd.2010.0528 · Cited by 111
“Recently, blood vessels have been reported to be a richer supply of stem/progenitor cells with a characteristic of expression of CD34 and CD146 surface cell markers [25–28].”
Self-citationCharacterization of vascular mural cells during zebrafish development
Santoro, M. M., Pesce, G., & Stainier, D. Y. R. (2009) · Mechanisms of Development · doi:10.1016/j.mod.2009.06.1080 · Cited by 110
“Establishment of transgenic lines for zebrafish MCs should also be a useful tool to study the perivascular origin of mesenchymal stem cells and their potency in myogenesis, adipogenesis, chondrogenesis and tissue regeneration (Cossu and Bianco, 2003; Crisan et al., 2008).”
Farré-Guasch, E., Martí, C. D., Hernández-Alfaro, F. J., Klein‐Nulend, J., & Casals, N. (2010) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2009.0487 · Cited by 111
“Adipogenic differentiation of ASCs from BFP. ( A ) Oil Red stain to detect lipid vacuoles.”
InfluentialImpaired Therapeutic Capacity of Autologous Stem Cells in a Model of Type 2 Diabetes
Shin, L., & Peterson, D. A. (2012) · Stem Cells Translational Medicine · doi:10.5966/sctm.2011-0031 · Cited by 110
Structure and Functions of Blood Vessels and Vascular Niches in Bone
Ramasamy, S. K. (2017) · Stem Cells International · doi:10.1155/2017/5046953 · Cited by 125
“Blood vessels in bone are reported to provide nurturing microenvironments to haematopoietic stem cells (HSCs) [21, 22] and mesenchymal stem cells (MSCs) [23, 24].”
BackgroundOxidative Stress in Mesenchymal Stem Cell Senescence: Regulation by Coding and Noncoding RNAs
Vono, R., Jover, E., Spinetti, G., & Madeddu, P. R. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7294 · Cited by 112
“In vitro, pericytes show typical mesenchymal properties with the capacity to attach to tissue culture plastic, expand for multiple passages, and differentiate into osteogenic, chondrogenic, or adipogenic lineages (23).”
Endometrial Stem Cell Markers: Current Concepts and Unresolved Questions
Tempest, N., Maclean, A., & Hapangama, D. K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103240 · Cited by 108
“However, it is thought that the CD146+PDGF-Rβ+ subpopulation are similar to bone marrow and adipose tissue MSCs in their differentiation potential, and their perivascular location is also shared by MSCs in many other organs [43].”
BackgroundBone Metastasis: Find Your Niche and Fit in
Zhang, W., Bado, I., Wang, H., Lo, H.-C., & Zhang, X. H.-F. (2019) · Trends in cancer · doi:10.1016/j.trecan.2018.12.004 · Cited by 110
Sandiford, O. A., DONNELLY, R. J., El-Far, M. H., Burgmeyer, L. M., Sinha, G., Pamarthi, S. H., Sherman, L. S., Ferrer, A. I., DeVore, D. E., Patel, S. A., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2434 · Cited by 112
“We selected MSCs because they are among the first set of cells encountered by BCCs when they enter the perivascular niche of BM (26, 27).”
MethodKim, J. H., Jung, Y., Kim, B., & Kim, S. H. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.11.008 · Cited by 107
“It has been reported that substance P recruits not only MSCs, but also various angiogenic cells in vitro and in vivo, and these cells have been shown to participate in angiogenesis [5,35,36].”
Background
Metadata
- Authors
- Crisan, M., Yap, S., Casteilla, L., Chen, C.-W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., Norotte, C., Teng, P.-N., Traas, J., Schugar, R., Deasy, B. M., Badylak, S., Bűhring, H.-J., Giacobino, J.-P., Lazzari, L., Huard, J., & Péault, B.
- Affiliations
- University of Pittsburgh (US)
- Centre National de la Recherche Scientifique (FR)
- Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico (IT)
- McGowan Institute for Regenerative Medicine (US)
- Children's Hospital of Philadelphia (US)
- Corresponding author
- Péault, Bruno
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 3
- Issue
- 3
- Pages
- 301-313
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- OpenAlex
- W2076491580
- Cited by
- 3,991
- References
- 47
- Citations by year
- 2026: 77 · 2025: 92 · 2024: 130 · 2023: 175 · 2022: 173 · 2021: 247 · 2020: 240 · 2019: 247 · 2018: 271 · 2017: 259 · 2016: 291 · 2015: 296 · 2014: 281 · 2013: 305 · 2012: 301
- FWCI
- 91.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1816 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- D-Scholarship@Pitt (University of Pittsburgh) (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Medical Center, University of Pittsburgh
- National Heart, Lung, and Blood Institute (R21HL083057)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR049684, R01 AR49684-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- mesenchymal stem cells, perivascular cells, pericytes, stem cell origin, CD146, NG2, osteogenic differentiation, chondrogenic differentiation, adipogenesis, chemotaxis, skeletal muscle, pancreas, adipose tissue, placenta, adult stem cells, vascular wall
- MeSH terms
- Adolescent, Adult, Aged, Cell Movement, Fetus, Flow Cytometry, Humans, Middle Aged, Pericytes, Muscle Development, Fetal Stem Cells, Adult Stem Cells, Mesenchymal Stem Cells
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