Cited by 610Mesenchymal stem cell researchPeriodontal Regeneration and TreatmentsHematopoietic Stem Cell Transplantation

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Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146(+) perivascular cells and fibroblasts

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Covas, Dimas T., Panepucci, Rodrigo A., Fontes, Aparecida M., Silva, Wilson A., Orellana, Maristela D., Freitas, Marcela C.C., Neder, Luciano, Santos, Anemari R.D., Peres, Luiz C., Jamur, Maria C., Zago, Marco A.·2008·Experimental Hematology

DOI 10.1016/j.exphem.2007.12.015

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Abstract

Objective The relationship of multipotent mesenchymal stromal cells (MSC) with pericytes and fibroblasts has not been established thus far, although they share many markers of primitive marrow stromal cells and the osteogenic, adipogenic, and chondrogenic differentiation potentials.Materials and methods We compared MSCs from adult or fetal tissues, MSC differentiated in vitro, fibroblasts and cultures of retinal pericytes obtained either by separation with anti-CD146 or adhesion. The characterizations included morphological, immunophenotypic, gene-expression profile, and differentiation potential.Results Osteogenic, adipocytic, and chondrocytic differentiation was demonstrated for MSC, retinal perivascular cells, and fibroblasts. Cell morphology and the phenotypes defined by 22 markers were very similar. Analysis of the global gene expression obtained by serial analysis of gene expression for 17 libraries and by reverse transcription polymerase chain reaction of 39 selected genes from 31 different cell cultures, revealed similarities among MSC, retinal perivascular cells, and hepatic stellate cells. Despite this overall similarity, there was a heterogeneous expression of genes related to angiogenesis, in MSC derived from veins, artery, perivascular cells, and fibroblasts. Evaluation of typical pericyte and MSC transcripts, such as NG2, CD146, CD271, and CD140B on CD146 selected perivascular cells and MSC by real-time polymerase chain reaction confirm the relationship between these two cell types. Furthermore, the inverse correlation between fibroblast-specific protein-1 and CD146 transcripts observed on pericytes, MSC, and fibroblasts highlight their potential use as markers of this differentiation pathway.Conclusion Our results indicate that human MSC and pericytes are similar cells located in the wall of the vasculature, where they function as cell sources for repair and tissue maintenance, whereas fibroblasts are more differentiated cells with more restricted differentiation potential.

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Background
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Background
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Background
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Background
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“[8,9] The high expression of CD146 on the surface of hPCy-MSCs is also linked to the multipotency of these cells [10].”
Background
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Background
The Involvement of CD146 and Its Novel Ligand Galectin-1 in Apoptotic Regulation of Endothelial Cells
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Result
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Background
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Background
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Background
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“It has been shown that the high expression of CD146 on the surface of MSCs is linked with multipotency of these cells [29].”
Background
CD146 positive human dental pulp stem cells promote regeneration of dentin/pulp-like structures
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Background
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Cipriani, P., Carubbi, F., Liakouli, V., Marrelli, A., Perricone, C., Perricone, R., Alesse, E., & Giacomelli, R. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.10.004 · Cited by 64
Perivascular-Derived Mesenchymal Stem Cells
Yianni, V., & Sharpe, P. T. (2019) · Journal of Dental Research · doi:10.1177/0022034519862258 · Cited by 66
“This has resulted in more similarities being identified between MSCs and pericytes (reviewed extensively in : Caplan et al. 2008, and Feng et al. 2010 ) leading many researchers to an acceptance that in most tissues, pericytes are precursors of MSCs (Covas et al. 2008; Schwab and Gargett 2007).”
BackgroundInfluential
The role of mechanobiology in progression of rotator cuff muscle atrophy and degeneration
Gibbons, M. C., Singh, A., Engler, A. J., & Ward, S. R. (2017) · Journal of Orthopaedic Research® · doi:10.1002/jor.23662 · Cited by 63
Cardiac Nestin+ Mesenchymal Stromal Cells Enhance Healing of Ischemic Heart through Periostin-Mediated M2 Macrophage Polarization
Liao, Y., Li, G., Zhang, X., Huang, W., Xie, D., Dai, G., Zhu, S., Lu, D., Zhang, Z., Lin, J., et al. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.01.011 · Cited by 60
The biology of vascular calcification
Quaglino, D., Boraldi, F., & Lofaro, F. D. (2020) · International review of cytology · doi:10.1016/bs.ircmb.2020.02.007 · Cited by 64
Persistent Angiogenesis in the Autism Brain: An Immunocytochemical Study of Postmortem Cortex, Brainstem and Cerebellum
Azmitia, E. C., Saccomano, Z. T., Alzoobaee, M. F., Boldrini, M., & Whitaker‐Azmitia, P. M. (2015) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-015-2672-6 · Cited by 68
Discovering cardiac pericyte biology: From physiopathological mechanisms to potential therapeutic applications in ischemic heart disease
Avolio, E., & Madeddu, P. R. (2016) · Vascular Pharmacology · doi:10.1016/j.vph.2016.05.009 · Cited by 59
Adenosine production: a common path for mesenchymal stem-cell and regulatory T-cell-mediated immunosuppression
Bravo, M. D. O., Carvalho, J. L., & Saldanha‐Araújo, F. (2016) · Purinergic Signalling · doi:10.1007/s11302-016-9529-0 · Cited by 64
The Stem Cell Niche Should be a Key Issue for Cell Therapy in Regenerative Medicine
Becerra, J., Santos‐Ruiz, L., Andrades, J. A., & Marí‐Beffa, M. (2010) · Stem Cell Reviews and Reports · doi:10.1007/s12015-010-9195-5 · Cited by 64
“The recent demonstration of pericyte as a MSC supports the ubiquitous existence of MSCs at ubiquitous vascular SC niche [51, 60, 66 , 67] ruling out the necessity of a circulating stem cell.”
Background
In search of mechanisms associated with mesenchymal stem cell-based therapies for acute kidney injury.
de Almeida, D. C., Donizetti-Oliveira, C., Costa, P. B., Origassa, C. S. T., & Câmara, N. O. S. (2013) · Europe PMC (PubMed Central) · Cited by 61
Immunomodulatory Nature and Site Specific Affinity of Mesenchymal Stem Cells: a Hope in Cell Therapy
Lotfinejad, P., Shamsasenjan, K., Movassaghpour, A. A., Majidi, J., & Baradaran, B. (2013) · Europe PMC (PubMed Central) · doi:10.5681/apb.2014.002 · Cited by 63
Transcriptional Networks in Single Perivascular Cells Sorted from Human Adipose Tissue Reveal a Hierarchy of Mesenchymal Stem Cells
Hardy, W. R., Moldovan, N. I., Moldovan, L., Livak, K. J., Datta, K., Goswami, C. P., Corselli, M., Traktuev, D. O., Murray, I. R., Péault, B., et al. (2017) · Stem Cells · doi:10.1002/stem.2599 · Cited by 61
Mesenchymal Stem and Progenitor Cells in Normal and Dysplastic Hematopoiesis—Masters of Survival and Clonality?
Pleyer, L., Valent, P., & Greil, R. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071009 · Cited by 63
“Further refinements were introduced by the identification of SMA+CD146bright pericytes in humans [40,144,146,155], an observation that was further developed and gave rise to the model of the “perivascular arteriolar niche” or “pericytic arteriolar niche” (Figure 2C).”
Background
Pericytes, integral components of adult hematopoietic stem cell niches
da Bandeira, D. S., Casamitjana, J., & Crisan, M. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.11.006 · Cited by 62
“, 2011) and few T and B lymphocytes (Covas et al., 2008).”
Background
Exploring the mesenchymal stem cell niche using high throughput screening
Ghaemi, S. R., Harding, F. J., Delalat, B., Gronthos, S., & Voelcker, N. H. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.06.022 · Cited by 62
Combination stem cell therapy for the treatment of medically refractory coronary ischemia: a Phase I study
Lasala, G. P., Silva, J. A., Kusnick, B. A., & Minguell, J. J. (2010) · Cardiovascular revascularization medicine · doi:10.1016/j.carrev.2010.01.001 · Cited by 59
“Bone marrow-derived mesenchymal stem cells (MSC) represent a source of pericyte progenitors [19] and also of angiogenic growth factors and extracellular matrix components [20,21].”
Background
Mesenchymal Stem Cells for Cartilage Regeneration of TMJ Osteoarthritis
Cui, D., Li, H., Xu, X., Ye, L., Zhou, X., Zheng, L., & Zhou, Y. (2017) · Stem Cells International · doi:10.1155/2017/5979741 · Cited by 61
“MSCs have been identified from various tissues, such as skeletal muscle [60], adipose tissue [61], the placenta [62], the bone [63], the deciduous teeth [64], and the synovium [65].”
Background
The Nell-1 Growth Factor Stimulates Bone Formation by Purified Human Perivascular Cells
Zhang, X., Péault, B., Chen, W., Li, W., Corselli, M., James, A. W., Lee, M., Siu, R. K., Pang, S., Zheng, Z. S., et al. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0705 · Cited by 58
Comparison between fibroblasts and mesenchymal stem cells derived from dermal and adipose tissue
Brohem, C. A., de Carvalho, C. M., Radoski, C. L., Santi, F. C., Baptista, M. C., Swinka, B. B., Urban, C. D. A., de Araujo, L. R. R., GRAF, R. M., Feferman, I. H. S., et al. (2013) · International Journal of Cosmetic Science · doi:10.1111/ics.12064 · Cited by 58
“It has recently been proposed that fibroblasts, myofibroblasts and smooth muscle vascular cells derive from a common stem cell and that MSC, fibroblasts and pericytes would be related cells that are present in the vascular wall and constitute an MSC compartment that extends throughout the entire organism [12].”
Background
Lung pericyte-like cells are functional interstitial immune sentinel cells
Hung, C. F., Mittelsteadt, K. L., Brauer, R., McKinney, B. L., Hallstrand, T. S., Parks, W. C., Chen, P., Schnapp, L. M., Liles, W. C., Duffield, J. S., et al. (2017) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00349.2016 · Cited by 58
Cell-Surface Expression of Neuron-Glial Antigen 2 (NG2) and Melanoma Cell Adhesion Molecule (CD146) in Heterogeneous Cultures of Marrow-Derived Mesenchymal Stem Cells
Russell, K. C., Tucker, H. A., Bunnell, B. A., Andreeff, M., Schober, W., Gaynor, A. S., Strickler, K. L., Lin, S., Lacey, M. R., & O'Connor, K. C. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0649 · Cited by 56
The Space of Disse: The Liver Hub in Health and Disease
Sanz-García, C., Fernández-Iglesias, A., Gracia-Sancho, J., Arráez-Aybar, L. A., Nevzorova, Y. A., & Cubero, F. J. (2021) · Livers · doi:10.3390/livers1010002 · Cited by 57
“Lately, several studies showed that activated HSCs (aHSCs) have a mesenchymal stem cell (MSC)-like phenotype, a heterogeneous group of multipotent stem cells that exemplifies an important element of the hematopoietic stem cell niche [6,7].”
Background
Platelet-derived growth factor receptors regulate mesenchymal stem cell fate: implications for neovascularization
Ball, S. G., Shuttleworth, C. A., & Kielty, C. M. (2009) · Expert Opinion on Biological Therapy · doi:10.1517/14712590903379510 · Cited by 57
“It is now generally accepted that blood vessel walls in the adult act as both a recipient and source of MSCs [10,11], fromwhere they may readily access the circulation and contribute to systemic tissue repair andcell replacement.”
Background
Human Fetal and Adult Bone Marrow-Derived Mesenchymal Stem Cells Use Different Signaling Pathways for the Initiation of Chondrogenesis
Brady, K., Dickinson, S. C., Guillot, P. V., Polak, J. M., Blom, A. W., Kafienah, W., & Hollander, A. P. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0301 · Cited by 56
“Pericytes have similar expression profiles and functional characteristics to MSCs and are thought to be the ancestral precursor of MSCs [43,44].”
Background
Bone marrow-derived mesenchymal stem cells enhance angiogenesis via their α6β1 integrin receptor
Carrion, B., Kong, Y. P., Kaigler, D., & Putnam, A. J. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.09.007 · Cited by 56
Osteoprotegerin, Pericytes and Bone-Like Vascular Calcification Are Associated with Carotid Plaque Stability
Davaine, J., Quillard, T., Brion, R., Lapérine, O., Guyomarch, B., Merlini, T., Chatelais, M., Guilbaud, F., Brennan, M. Á., Charrier, C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107642 · Cited by 56
“However, other cells including pericytes have also been previously shown to be involved in the vascular calcification process [8,9] and their potential as mesenchymal precursors has recently been highlighted [39].”
Background
Human Placenta-Derived CD146-Positive Mesenchymal Stromal Cells Display a Distinct Osteogenic Differentiation Potential
Ulrich, C., Abruzzese, T., Maerz, J. K., Ruh, M., Amend, B., Benz, K., Rolauffs, B., Abele, H., Hart, M. L., & Aicher, W. K. (2015) · Stem Cells and Development · doi:10.1089/scd.2014.0465 · Cited by 56
Mouse mesenchymal stem cells inhibit high endothelial cell activation and lymphocyte homing to lymph nodes by releasing TIMP-1
Zanotti, L., Angioni, R., Calì, B., Soldani, C., Ploia, C., Moalli, F., Gargesha, M., D’Amico, G., Elliman, S. J., Tedeschi, G., et al. (2016) · Leukemia · doi:10.1038/leu.2016.33 · Cited by 57
Adipose-derived stromal cells for osteoarticular repair: trophic function versus stem cell activity
Ruetze, M., & Richter, W. (2014) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2014.9 · Cited by 55
Human hepatic stellate cell line (LX-2) exhibits characteristics of bone marrow-derived mesenchymal stem cells
Castilho–Fernandes, A., de Almeida, D. C., Fontes, A. M., Melo, F. U. F., Picanço‐Castro, V., de Freitas, M. C. C., Orellana, M. D., Palma, P. V. B., Hackett, P. B., Friedman, S. L., et al. (2011) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2011.09.002 · Cited by 56
Self-citation
Intrinsic Properties of Mesemchymal Stem Cells from Human Bone Marrow, Umbilical Cord and Umbilical Cord Blood Comparing the Different Sources of MSC
Lv, F., Lu, M., Cheung, K., Leung, V., & Zhou, G. (2012) · Current Stem Cell Research & Therapy · doi:10.2174/157488812804484611 · Cited by 55
“Although some researches implicated that AT-MSC lacked the ability to differentiate into osteoblasts [81], in a rat spine fusion model, both collagen sponge containing BM-MSC and AT-MSC transfected”
Characterization of human PDGFR-β-positive pericytes from IPF and non-IPF lungs
Wilson, C. L., Stephenson, S. E., Higuero, J. P., Feghali‐Bostwick, C. A., Hung, C. F., & Schnapp, L. M. (2018) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00289.2018 · Cited by 55
Isolation of Adipose-Derived Stromal Vascular Fraction Cells Using a Novel Point-of-Care Device: Cell Characterization and Review of the Literature
Brown, J. C., Shang, H., Li, Y., Yang, N., Patel, N., & Katz, A. J. (2017) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2016.0377 · Cited by 56
On the origin and development of glioblastoma: multifaceted role of perivascular mesenchymal stromal cells
Ah-Pine, F., Khettab, M., Bedoui, Y., Slama, Y., Daniel, M., Doray, B., & Gasque, P. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01605-x · Cited by 66
“In addition, it has been demonstrated that PC, originally defined by their vascular mural localization, have the same osteogenic, adipogenic, and myogenic potential as MSC and also express surface markers of MSC, such as CD44, CD73, CD90, and CD105 in vitro [80, 92].”
Background
Mesenchymal stem cells derived from Wharton's jelly: Comparative phenotype analysis between tissue and in vitro expansion
Margossian, T., Reppel, L., Makdissy, N., Stoltz, J., Bensoussan, D., & Huselstein, C. (2012) · Bio-Medical Materials and Engineering · doi:10.3233/bme-2012-0714 · Cited by 53
Perivascular-Like Cells Contribute to the Stability of the Vascular Network of Osteogenic Tissue Formed from Cell Sheet-Based Constructs
Mendes, L. F., Pirraco, R. P., Szymczyk, W., Frias, A. M., Santos, T. C., Reis, R. L., & Marques, A. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041051 · Cited by 53
“As previously described by others [28,38], we identified the presence of CD146 cells within the mononuclear fraction of human bone marrow aspirates.”
Bone Marrow Cells Immunomagnetically Selected For CD271+ Antigen Promote In Vitro the Repair of Articular Cartilage Defects
Hermida‐Gómez, T., Fuentes-Boquete, I. M., Gimeno, M. J., Muiños‐López, E., Díaz‐Prado, S., de Toro, F. J., & Blanco, F. J. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0346 · Cited by 53
“15 CD271 mRNA has been reported in BMMSCs. 21 Other research has shown that CD271 is a key marker of MSCs in BM and other tissues.”
Identical, similar or different? Learning about immunomodulatory function of mesenchymal stem cells isolated from various mouse tissues: bone marrow, spleen, thymus and aorta wall
Hegyi, B., Sági, B., Kovacs, J., Kiss, J., Urban, V. S., Meszaros, G., Monostori, É., & Uher, F. (2010) · International Immunology · doi:10.1093/intimm/dxq039 · Cited by 53
Modulation of Immunoregulatory Properties of Mesenchymal Stromal Cells by Toll‐Like Receptors: Potential Applications on GVHD
Sangiorgi, B., & Panepucci, R. A. (2016) · Stem Cells International · doi:10.1155/2016/9434250 · Cited by 53
“Although initially described in the bone marrow, these cells can be found virtually in all body tissues besides the perivascular niche, where they are believed to play diverse roles in tissue homeostasis [6].”
Self-citation
Diverse origins and activation of fibroblasts in cardiac fibrosis
Aujla, P. K., & Kassiri, Z. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109869 · Cited by 55
The effect of erythropoietin on autologous stem cell-mediated bone regeneration
Nair, A., Tsai, Y., Shah, K., Shen, J., Weng, H., Zhou, J., Sun, X., Saxena, R., Borrelli, J., & Tang, L. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.06.031 · Cited by 52
Mesenchymal stem cells promote the sustained expression of CD69 on activated T lymphocytes: roles of canonical and non‐canonical NF‐κB signalling
Saldanha‐Araújo, F., Haddad, R., Malmegrim, K. C. R., Souza, A. D. P. A., Palma, P. V. B., Araújo, A. G., Orellana, M. D., Voltarelli, J. C., Covas, D. T., Zago, M. A., et al. (2011) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2011.01391.x · Cited by 54
Self-citation

Authors: Covas, D. T., Panepucci, R. A., Fontes, A. M., Silva, W. A., Orellana, M. D., Freitas, M. C. C., Neder, L., Santos, A. R. D., Peres, L. C., Jamur, M. C., & Zago, M. A.
Affiliations: Universidade de São Paulo (BR)
Corresponding author: Covas, Dimas T.
ORCID: Covas, Dimas T.
Panepucci, Rodrigo A.
Fontes, Aparecida M.
Silva, Wilson A.
Orellana, Maristela D.
Freitas, Marcela C.C.
Neder, Luciano
Jamur, Maria C.
Zago, Marco A.
Venue: Experimental Hematology
Publisher: Elsevier BV
Published: 2008-05
Volume: 36
Issue: 5
Pages: 642-654
ISSN: 0301-472X (ISSN-L)
DOI: 10.1016/j.exphem.2007.12.015
OpenAlex: W1979782761
Cited by: 610
References: 93
Citations by year: 2026: 4 · 2025: 10 · 2024: 15 · 2023: 14 · 2022: 19 · 2021: 25 · 2020: 31 · 2019: 31 · 2018: 32 · 2017: 32 · 2016: 48 · 2015: 58 · 2014: 49 · 2013: 60 · 2012: 63
FWCI: 18.19
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, 5151 d)
Locations: Experimental Hematology (publishedVersion)
PubMed (publishedVersion)
Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
Funders: Scheme for Promotion of Academic and Research Collaboration
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Health Sciences › Dentistry › Periodontics › Periodontal Regeneration and Treatments
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Keywords: mesenchymal stem cells, pericytes, fibroblasts, CD146, hepatic stellate cells, gene expression profiling, osteogenic differentiation, adipogenesis, chondrogenic differentiation, angiogenesis, S100A4, NG2, p75 neurotrophin receptor, PDGFRβ, vascular wall cells, tissue repair
MeSH terms: Cell Differentiation, Cell Separation, Cells, Cultured, Fibroblasts, Flow Cytometry, Humans, Transcription, Genetic, Umbilical Cord, Cluster Analysis, Immunophenotyping, Reverse Transcriptase Polymerase Chain Reaction, Pericytes, Gene Expression Profiling, CD146 Antigen, Mesenchymal Stem Cells

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Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146(+) perivascular cells and fibroblasts

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