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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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Self-citationA molecular atlas of cell types and zonation in the brain vasculature
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ResultSpheroid Culture of Mesenchymal Stem Cells
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Self-citationPericytes of Multiple Organs Do Not Behave as Mesenchymal Stem Cells In Vivo
Guimarães‐Camboa, N., Cattaneo, P., Sun, Y., Moore‐Morris, T., Gu, Y., Dalton, N. D., Rockenstein, E. M., Masliah, E., Peterson, K. L., Stallcup, W. B., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.12.006 · Cited by 500
“As a substantial number of experiments indicating that pericytes are MSCs have been performed on pericytes from these organs (Chen et al., 2015; Crisan et al., 2008; Dellavalle et al., 2007, 2011; Paul et al., 2012; Tang et al., 2008), our results challenge the prevailing view of pericytes as…”
BackgroundResultInfluentialFibroblast heterogeneity: implications for human disease
Lynch, M. D., & Watt, F. M. (2018) · Journal of Clinical Investigation · doi:10.1172/jci93555 · Cited by 507
“This population of fibroblasts have the capacity to differentiate into multiple lineages (23) and have been termed mesenchymal stem or stromal cells (MSCs).”
ResultInfluentialReview of Signaling Pathways Governing MSC Osteogenic and Adipogenic Differentiation
James, A. W. (2013) · Scientifica · doi:10.1155/2013/684736 · Cited by 515
“Indeed, the perivascular origin of MSC has become an increasingly accepted theory [10–13].”
BackgroundSicari, B. M., Rubin, J. P., Dearth, C. L., Wolf, M. T., Ambrosio, F., Boninger, M. L., Turner, N. J., Weber, D. J., Simpson, T. W., Wyse, A. J., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008085 · Cited by 498
Self-citationTurinetto, V., Vitale, E., & Giachino, C. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071164 · Cited by 502
“These cells can be easily isolated and expanded from the stroma of virtually all organs, although the preferred sources are bone marrow and subcutaneous fat [1].”
BackgroundBringing new life to damaged bone: The importance of angiogenesis in bone repair and regeneration
Stegen, S., van Gastel, N., & Carmeliet, G. (2014) · Bone · doi:10.1016/j.bone.2014.09.017 · Cited by 495
“CD44 or CD146 [56,59]), Stro1 [60], platelet-derived growth factor receptor β [55], NG2 [61] and alpha smooth muscle actin (αSMA) [62].”
BackgroundIsolation and Culture of Epithelial Progenitors and Mesenchymal Stem Cells from Human Endometrium1
Gargett, C. E., Schwab, K. E., Zillwood, R. M., Nguyen, H. P. T., & Wu, D. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.075226 · Cited by 476
“Similarly, large endometrial stromal CFU demonstrate substantial proliferative capacity (30 PDs), greater than most human bone marrow, dental pulp, and adipose CFU-F (,20 PDs) [41, 46, 47], which have similar capacity to that of small endometrial stromal CFU (13 PDs), and less than that of human fetal muscle cells (40…”
BackgroundA stromal cell population that inhibits adipogenesis in mammalian fat depots
Schwalie, P. C., Dong, H., Zachara, M., Russeil, J., Alpern, D., Akchiche, N., Caprara, C., Sun, W., Schlaudraff, K.-U., Soldati, G., et al. (2018) · Nature · doi:10.1038/s41586-018-0226-8 · Cited by 463
Krampera, M., Galipeau, J., Shi, Y., Tarte, K., & Sensebé, L. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.02.010 · Cited by 465
“Despite a close relationship between these two cell types in terms of surface phenotype and qualitative in vitro assays (11,12), MSCs in general lack the contractility of pericytes and may show marked differences in gene expression (12), as well as by using more rigorous in vivo assays (13).”
Frenette, P. S., Pinho, S., Lucas, D., & Scheiermann, C. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095919 · Cited by 462
Zhao, H., Feng, J., Seidel, K., Shi, S., Klein, O. D., Sharpe, P. T., & Chai, Y. (2014) · Cell stem cell · doi:10.1016/j.stem.2013.12.013 · Cited by 464
“In addition, stem cells in other organs usually comprise a very small percentage of the entire population, but the MSC definition has included the majority of the cell population on the culture dish based on their high expression of classical MSC markers including CD73, CD105, Sca1 and others (Bianco et al., 2013; Cov…”
BackgroundTumour-associated mesenchymal stem/stromal cells: emerging therapeutic targets
Shi, Y., Du, L., Lin, L., & Wang, Y. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.193 · Cited by 463
Lin, H., Sohn, J., Shen, H., Langhans, M. T., & Tuan, R. S. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.06.026 · Cited by 455
“demonstrated the perivascular origin of MSCs [35].”
BackgroundChen, Q., Jin, M., Yang, F., Zhu, J., Xiao, Q., & Zhang, L. (2013) · Mediators of Inflammation · doi:10.1155/2013/928315 · Cited by 456
“Another source of stem/progenitor cells involved in vascular diseases is blood vessel wall harboring MSCs, EPCs, and other stem/progenitor cells [66, 67].”
BackgroundSelf-citationAdipose tissue stem cells meet preadipocyte commitment: going back to the future
Cawthorn, W. P., Scheller, E. L., & MacDougald, O. A. (2011) · Journal of Lipid Research · doi:10.1194/jlr.r021089 · Cited by 467
Nicotinamide mononucleotide increases muscle insulin sensitivity in prediabetic women
Yoshino, M., Yoshino, J., Kayser, B. D., Patti, G. J., Franczyk, M. P., Mills, K. F., Sindelar, M., Pietka, T., Patterson, B. W., Imai, S.-I., et al. (2021) · Science · doi:10.1126/science.abe9985 · Cited by 439
Bone Marrow Mesenchymal Stem Cells: Historical Overview and Concepts
Charbord, P. (2010) · Human Gene Therapy · doi:10.1089/hum.2010.115 · Cited by 459
“Pericytes from sites other than bone marrow may also give rise to MSC-like cells (Crisan et al. , 2008).”
Mizoguchi, T., Pinho, S., Ahmed, J. U., Kunisaki, Y., Hanoun, M., Mendelson, A., Ono, N., Kronenberg, H. M., & Frenette, P. S. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.03.013 · Cited by 451
“(Figure 2K) (Crisan et al., 2008; Morikawa et al., 2009; Pinho et al., 2013).”
Moll, G., Ankrum, J. A., Kamhieh-Milz, J., Bieback, K., Ringdén, O., Volk, H.-D., Geissler, S., & Reinke, P. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.12.006 · Cited by 440
“Another crucial paradigm shift was the intriguing conception of MSC in vivo identity as peri-vascular pericytes [33,34].”
Stromal cell diversity associated with immune evasion in human triple‐negative breast cancer
Wu, S. Z., Roden, D. L., Wang, C., Holliday, H., Harvey, K., Cazet, A., Murphy, K. J., Pereira, B., Al‐Eryani, G., Bartoniček, N., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019104063 · Cited by 454
“To investigate this, we generated cell-derived matrices (CDMs) to compare the ability of each human stromal subset to lay down collagen, as previously described (Cukierman et al, 2001).”
MethodSacchetti, B., Funari, A., Remoli, C., Giannicola, G., Kogler, G., Liedtke, S., Cossu, G., Serafini, M., Sampaolesi, M., Tagliafico, E., et al. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.05.011 · Cited by 428
“The other view sees ‘‘MSCs’’ as progenitors of multiple tissues Stem This is an open access article under the C beyond the range of skeletal tissues, such as skeletal muscle (Caplan, 1991, 2008; Crisan et al., 2008).”
BackgroundInfluentialMesenchymal Stem Cells in Tissue Repair
DiMarino, A. M., Caplan, A. I., & Bonfield, T. L. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00201 · Cited by 455
“The functional interaction of pericytes with the endothelial cells is thought to be the source for differentiation and definition of MSC differentiation (19).”
BackgroundFunctional heterogeneity of mesenchymal stem cells: Implications for cell therapy
Phinney, D. G. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24166 · Cited by 437
MSCs: Delivery Routes and Engraftment, Cell-Targeting Strategies, and Immune Modulation
Kean, T. J., Lin, P. Y., Caplan, A. I., & Dennis, J. E. (2013) · Stem Cells International · doi:10.1155/2013/732742 · Cited by 442
“At sites of injury, it has been established that most, if not all, MSCs are derived from perivascular mesenchymal cells, pericytes, that are on the tissue side of blood vessels and sinusoids [55, 56].”
BackgroundMesenchymal stem cells in fibrotic disease
El Agha, E., Kramann, R., Schneider, R. K., Li, X., Seeger, W., Humphreys, B. D., & Bellusci, S. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.07.011 · Cited by 430
Use of Mesenchymal Stem Cells for Therapy of Cardiac Disease
Karantalis, V., & Hare, J. M. (2015) · Circulation Research · doi:10.1161/circresaha.116.303614 · Cited by 432
“Thus, blood vessel walls harbor a reserve of progenitor cells that may be integral to the origin of the MSCs and other related adult stem cells.(84) In vitro, MSCs express α-smooth muscle actin and β-actin filaments,(85) whereas in in vivo studies, it is shown that MSCs express an endothelial phenotype that enhanced m…”
BackgroundGupta, R. K., Mepani, R. J., Kleiner, S., Lo, J. C., Khandekar, M. J., Cohen, P., Frontini, A., Bhowmick, D. C., Ye, L., Cinti, S., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.010 · Cited by 426
“…(Tang et al., 2008); in addition, several recent studies have clearly demonstrated that perivascular cells isolated from adipose tissue have the ability to differentiate into adipocytes (Amos et al., 2008; Crisan et al., 2008; Traktuev et al., 2008; Zannettino et al., 2008; Zimmerlin et al., 2010).”
ResultMesenchymal stem cells in joint disease and repair
Barry, F., & Murphy, M. J. (2013) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2013.109 · Cited by 425
Mesenchymal Stem Cells Migration Homing and Tracking
Sohni, A., & Verfaillie, C. M. (2013) · Stem Cells International · doi:10.1155/2013/130763 · Cited by 424
“As alluded earlier, MSCs can and have been isolated from multiple different tissues [41] with differences in the phenotype of the cells isolated [42].”
BackgroundStromal cells and stem cells in clinical bone regeneration
Grayson, W. L., Bunnell, B. A., Martin, E. C., Frazier, T. P., Hung, B. P., & Gimble, J. M. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.234 · Cited by 429
Normal and Leukemic Stem Cell Niches: Insights and Therapeutic Opportunities
Schepers, K., Campbell, T., & Passegue, E. A. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.014 · Cited by 431
“Perivascular BM MSCs may, in fact, share functional properties and developmental origins with pericytes that are more broadly found around the smallest blood vessels throughout the body (Crisan et al., 2008; Armulik et al., 2011).”
Dulauroy, S., Di Carlo, S. E., Langa, F., Eberl, G., & Peduto, L. (2012) · Nature Medicine · doi:10.1038/nm.2848 · Cited by 418
Origin and function of cartilage stem/progenitor cells in osteoarthritis
Jiang, Y., & Tuan, R. S. (2014) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2014.200 · Cited by 413
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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