Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146(+) perivascular cells and fibroblasts
Open accessAbstract
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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Sorted by citations
Mesenchymal stem cell perspective: cell biology to clinical progress
Pittenger, M. F., Discher, D. E., Péault, B. M., Phinney, D. G., Hare, J. M., & Caplan, A. I. (2019) · npj Regenerative Medicine · doi:10.1038/s41536-019-0083-6 · Cited by 2,008 · see citing works
Cardiac Fibrosis: The Fibroblast Awakens
Travers, J. G., Kamal, F. A., Robbins, J., Yutzey, K. E., & Blaxall, B. C. (2016) · Circulation Research · doi:10.1161/circresaha.115.306565 · Cited by 1,596 · see citing works
Mechanisms involved in the therapeutic properties of mesenchymal stem cells
da Silva Meirelles, L., Fontes, A. M., Covas, D. T., & Caplan, A. I. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.10.002 · Cited by 1,436 · see citing works
“adipogenic, osteogenic and chondrogenic lineages ([25]; reviewed in [38]).”
BackgroundSelf-citationSu, S., Chen, J., Yao, H., Liu, J., Yu, S., Lao, L., Wang, M., Luo, M., Xing, Y., Chen, F., et al. (2018) · Cell · doi:10.1016/j.cell.2018.01.009 · Cited by 1,230 · see citing works
“We examined the expression of CD146, amarker for BMSCs but not expressed by fibroblasts (Covas et al., 2008).”
Concise Review: The Surface Markers and Identity of Human Mesenchymal Stem Cells
Lv, F., Tuan, R. S., Cheung, K., & Leung, V. (2014) · Stem Cells · doi:10.1002/stem.1681 · Cited by 986 · see citing works
Adipogenesis: From Stem Cell to Adipocyte
Tang, Q. Q., & Lane, M. D. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052110-115718 · Cited by 897 · see citing works
In Search of the In Vivo Identity of Mesenchymal Stem Cells
da Silva Meirelles, L., Caplan, A. I., & Nardi, N. B. (2008) · Stem Cells · doi:10.1634/stemcells.2007-1122 · Cited by 1,077 · see citing works
Viswanathan, S., Shi, Y., Galipeau, J., Krampera, M., Leblanc, K., Martin, I., Nolta, J., Phinney, D. G., & Sensebe, L. (2019) · Cytotherapy · doi:10.1016/j.jcyt.2019.08.002 · Cited by 839 · see citing works
Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease
Fan, D., Takawale, A., Lee, J., & Kassiri, Z. (2012) · Fibrogenesis & Tissue Repair · doi:10.1186/1755-1536-5-15 · Cited by 814 · see citing works
Mesenchymal stem cell–educated macrophages: A novel type of alternatively activated macrophages
Kim, J., & Hematti, P. (2009) · Experimental Hematology · doi:10.1016/j.exphem.2009.09.004 · Cited by 785 · see citing works
“Cells with similar characteristics to BM-MSCs have been found in most human tissues examined [4-6], as well as other animals [7-9].”
BackgroundZhang, Q., Shi, S., Liu, Y., Uyanne, J., Shi, Y., Shi, S., & Le, A. D. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902318 · Cited by 753 · see citing works
“As such, the so-called fibroblast population may represent a more differentiated subpopulation of MSCs (22, 76).”
BackgroundInfluentialHan, Y., Yang, J., Fang, J., Zhou, Y., Candi, E., Wang, J., Hua, D., Shao, C., & Shi, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00932-0 · Cited by 720 · see citing works
“Tissue specificity MSCs isolated from different sources can vary in their gene expression patterns and differentiation potentials.(14) There are several non-classical markers (such as CD36, CD163, CD271, CD200, CD273, CD274, CD146, CD248, and CD140b) that potentially distinguish MSCs of different sources.”
BackgroundConcise Review: Mesenchymal Stem Cells: From Roots to Boost
Andrzejewska, A., Łukomska, B., & Janowski, M. (2019) · Stem Cells · doi:10.1002/stem.3016 · Cited by 610 · see citing works
The origin of fibroblasts and mechanism of cardiac fibrosis
Krenning, G., Zeisberg, E. M., & Kalluri, R. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22322 · Cited by 601 · see citing works
“Furthermore, retinal pericytes were shown to display a phenotypical and functional overlap with fibroblast in vitro (Covas et al., 2008) and recent lineage tracing studies in the kidney revealed that CD73 þ pericytes were a source of fibroblast in the injured kidney (Humphreys et al., 2010).”
ResultSpheroid Culture of Mesenchymal Stem Cells
Cesarz, Z., & Tamama, K. (2016) · Stem Cells International · doi:10.1155/2016/9176357 · Cited by 475 · see citing works
“[64] D.”
Stromal vascular progenitors in adult human adipose tissue
Zimmerlin, L., Donnenberg, V. S., Pfeifer, M. E., Meyer, E. M., Péault, B., Rubin, J. P., & Donnenberg, A. D. (2009) · Cytometry Part A · doi:10.1002/cyto.a.20813 · Cited by 497 · see citing works
“Vascular associated MSC, dubbed pericytes, were recently proposed to be a resident population in most of tissues of mesodermal origin (17,18), including fat.”
BackgroundKrampera, M., Galipeau, J., Shi, Y., Tarte, K., & Sensebé, L. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2013.02.010 · Cited by 465 · see citing works
“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).”
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 · see citing works
“cells have been characterized, suggesting that they may represent the same population, at least in some tissues (Covas et al., 2008; Schwab and Gargett, 2007).”
BackgroundInfluentialLin, H., Sohn, J., Shen, H., Langhans, M. T., & Tuan, R. S. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.06.026 · Cited by 448 · see citing works
“They concluded that the gene expression profiles and differentiation capacities were similar between MSCs and perivascular stromal cells [34].”
ResultStromal 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 436 · see citing works
“MEF2C is a well-defined regulator for establishing vSMCs during development, highlighting a likely vSMC origin of the described PVL cells (Creemers et al, 2006; Gordon et al, 2009).”
BackgroundRussell, K. C., Phinney, D. G., Lacey, M. R., Barrilleaux, B. L., Meyertholen, K., & O’Connor, K. C. (2010) · Stem Cells · doi:10.1002/stem.312 · Cited by 439 · see citing works
Functional 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 · see citing works
“However, while the surface phenotype and transcriptome of peri-vascular cells, pericytes and fibroblasts resemble that of marrow-derived MSCs [Covas et al., 2008, pp. 7–9], the latter generally lack the contractility of pericytes and all four lineages exhibit distinct differences in differentiation…”
BackgroundDual origin of mesenchymal stem cells contributing to organ growth and repair
Feng, J., Mantesso, A., Bari, C. D., Nishiyama, A., & Sharpe, P. T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015449108 · Cited by 412 · see citing works
The Tunica Adventitia of Human Arteries and Veins As a Source of Mesenchymal Stem Cells
Corselli, M., Chen, C.-W., Sun, B., Yap, S., Rubin, J. P., & Péault, B. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0200 · Cited by 393 · see citing works
“Only recently were similarities noticed to exist between MSC and perivascular cells [10–14].”
Trafficking and differentiation of mesenchymal stem cells
Liu, Z., Zhuge, Y., & Velazquez, O. C. (2009) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22091 · Cited by 370 · see citing works
“Recently, it has been reported that MSCs isolated from multiple adult and fetal organs as well as pericytes that reside in close proximity within the vascular wall are positive for the perivascular marker CD146 and display similar properties, such as the capacity for differentiation towards adipogenic, osteogenic, and…”
BackgroundArthur, A., Zannettino, A. C. W., & Gronthos, S. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21592 · Cited by 332 · see citing works
“More recently, Covas et al. (2008) demonstrated that MSC positive for the perivascular marker, CD146 isolated from multiple adult and fetal organs, and pericytes reside in close proximity within the vasculature wall and display similar properties, such as the capacity for differentiation towards…”
BackgroundMarkers Distinguishing Mesenchymal Stem Cells from Fibroblasts Are Downregulated with Passaging
Halfon, S., Abramov, N., Grinblat, B., & Ginis, I. (2010) · Stem Cells and Development · doi:10.1089/scd.2010.0040 · Cited by 327 · see citing works
Perivascular Ancestors of Adult Multipotent Stem Cells
Corselli, M., Chen, C.-W., Crisan, M., Lazzari, L., & Péault, B. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.191643 · Cited by 309 · see citing works
Coffelt, S. B., Marini, F. C., Watson, K., Zwezdaryk, K. J., Dembinski, J. L., LaMarca, H. L., Tomchuck, S. L., zu Bentrup, K. H., Danka, E. S., Henkle, S. L., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900244106 · Cited by 292 · see citing works
Campagnolo, P., Cesselli, D., Zen, A. A. H., Beltrami, A. P., Kränkel, N., Katare, R., Angelini, G. D., Emanueli, C., & Madeddu, P. R. (2010) · Circulation · doi:10.1161/circulationaha.109.899252 · Cited by 292 · see citing works
Natural history of mesenchymal stem cells, from vessel walls to culture vessels
Murray, I. R., West, C. C., Hardy, W. R., James, A. W., Park, T. S., Nguyen, A. T., Tawonsawatruk, T., Lazzari, L., Soo, C. B., & Péault, B. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1462-6 · Cited by 291 · see citing works
“Pericytes have been recognized as a distinct cellular entity that share a common immunophenotype and differentiation potential to mesenchymal stem/progenitor cells [26].”
BackgroundCD146, a multi-functional molecule beyond adhesion
Wang, Z., & Yan, X. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.11.049 · Cited by 281 · see citing works
“Thus CD146 has been seen as a marker for MSCs isolated from multiple adult and fetal organs [71,72,75], suggesting that CD146 is probably actively involved in differentiation and organogenesis during development.”
BackgroundResultPeriodontal Ligament Stem Cells: Current Status, Concerns, and Future Prospects
Zhu, W., & Liang, M. (2015) · Stem Cells International · doi:10.1155/2015/972313 · Cited by 281 · see citing works
“Recent studies show that MSCs obtained from various tissue types (brain, lung, liver, kidney, muscle, skin, and bone marrow) also exhibit pericyte characteristics [24, 25].”
BackgroundThe angiogenic properties of mesenchymal stem/stromal cells and their therapeutic potential
Watt, S. M., Gullo, F., van der Garde, M., Markeson, D., Camicia, R., Khoo, C. P., & Zwaginga, J. J. (2013) · British Medical Bulletin · doi:10.1093/bmb/ldt031 · Cited by 273 · see citing works
Neurovascular Unit: a Focus on Pericytes
Sá-Pereira, I., Brites, D. M. T. O., & Brito, M. A. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8244-2 · Cited by 267 · see citing works
“[100] also showed a sharing of diverse markers between mesenchymal cells and retinal”
BackgroundDefining adipose tissue-derived stem cells in tissue and in culture.
Lin, C., Xin, Z., Deng, C., Ning, H., Lin, G., & Lue, T. F. (2010) · PubMed · doi:10.14670/hh-25.807 · Cited by 264 · see citing works
Zhang, X., Hirai, M., Cantero, S., Ciubotariu, R., Dobrila, L., Hirsh, A. G., Igura, K., Satoh, H., Yokomi, I., Nishimura, T., et al. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23042 · Cited by 248 · see citing works
“Recently, perivascular cells, including pericytes, have been proposed as the origin of MSC in various tissues [Covas et al., 2008; Corselli et al., 2010].”
BackgroundPericytes at the intersection between tissue regeneration and pathology: Figure 1
Birbrair, A., Zhang, T., Wang, Z., Messi, M. L., Mintz, A., & Delbono, O. (2014) · Clinical Science · doi:10.1042/cs20140278 · Cited by 243 · see citing works
Fibroblasts and Mesenchymal Stromal/Stem Cells Are Phenotypically Indistinguishable
Denu, R. A., Nemcek, S., Bloom, D. D., Goodrich, A. D., Kim, J., Mosher, D. F., & Hematti, P. (2016) · Acta Haematologica · doi:10.1159/000445096 · Cited by 245 · see citing works
“In addition, large-scale gene expression profiles demonstrate that fibroblasts and MSCs from a number of different sources show very similar patterns [19].”
BackgroundClinical utility of stem cells for periodontal regeneration
Hynes, K., Menicanin, D., Gronthos, S., & Bartold, P. M. (2012) · Periodontology 2000 · doi:10.1111/j.1600-0757.2012.00443.x · Cited by 239 · see citing works
“Of note, different markers (STRO-1, 3G5 and CD146) that identify perivascular elements in different tissues have been used to isolate partially purified multipotential mesenchymal stem cell-like populations (32, 60, 138, 143, 179).”
Efficacy of Periodontal Stem Cell Transplantation in the Treatment of Advanced Periodontitis
Park, J., Jeon, S. H., & Choung, P. (2010) · Cell Transplantation · doi:10.3727/096368910x519292 · Cited by 235 · see citing works
Wang, X., Sha, X.-J., Li, G., Yang, F.-S., Ji, K., Wen, L., Liu, S., Chen, L., Ding, Y., & Xuan, K. (2012) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2012.02.014 · Cited by 233 · see citing works
Chapter 4 Fibroblasts—A Diverse Population at the Center of It All
Sorrell, J. M., & Caplan, A. I. (2009) · International review of cytology · doi:10.1016/s1937-6448(09)76004-6 · Cited by 227 · see citing works
Mesenchymal markers on human adipose stem/progenitor cells
Zimmerlin, L., Donnenberg, V. S., Rubin, J. P., & Donnenberg, A. D. (2013) · Cytometry Part A · doi:10.1002/cyto.a.22227 · Cited by 225 · see citing works
Mesenchymal Stem Cells for Chronic Wound Healing: Current Status of Preclinical and Clinical Studies
Huang, Y., Gou, M., Da, L., Zhang, W., & Xie, H. (2020) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2019.0351 · Cited by 209 · see citing works
Perivascular Multipotent Progenitor Cells in Human Organs
Crisan, M., Chen, C., Corselli, M., Andriolo, G., Lazzari, L., & Péault, B. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04967.x · Cited by 204 · see citing works
The Adult Human Brain Harbors Multipotent Perivascular Mesenchymal Stem Cells
Paul, G., Özen, Í., Christophersen, N. S., Reinbothe, T. M., Bengzon, J., Visse, E., Jansson, K., Dannaeus, K., Henriques-Oliveira, C., Roybon, L., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035577 · Cited by 202 · see citing works
“Perivascular cells and MSC have previously been linked [8,13,29].”
BackgroundMesenchymal Stromal Cells and Tissue‐Specific Progenitor Cells: Their Role in Tissue Homeostasis
Klimczak, A., & Kozłowska, U. (2015) · Stem Cells International · doi:10.1155/2016/4285215 · Cited by 196 · see citing works
Vascular Wall Progenitor Cells in Health and Disease
Psaltis, P. J., & Simari, R. D. (2015) · Circulation Research · doi:10.1161/circresaha.116.305368 · Cited by 194 · see citing works
“come apparent that only a subset of pericytes express MSC markers and possess their multilineage plasticity.(65,93,99,100) As distinct from some earlier reports,(32,101) the prevailing view is that pericytes are classically CD34CD146CD31, whereas ADSCs are CD34CD146CD31, a phenotype also shared by MSCs from vascular a…”
BackgroundFunctional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo
Kurth, T. B., Dell’Accio, F., Crouch, V., Augello, A., Sharpe, P. T., & Bari, C. D. (2011) · Arthritis & Rheumatism · doi:10.1002/art.30234 · Cited by 194 · see citing works
Zha, K., Li, X., Yang, Z., Tian, G., Sun, Z., Sui, X., Dai, Y., Liu, S., & Guo, Q. (2021) · npj Regenerative Medicine · doi:10.1038/s41536-021-00122-6 · Cited by 195 · see citing works
Elahi, K. C., Klein, G., Avci‐Adali, M., Sievert, K. D., MacNeil, S., & Aicher, W. K. (2015) · Stem Cells International · doi:10.1155/2016/5646384 · Cited by 190 · see citing works
“Mesenchymal stromal cells have been described in and have been isolated from many different adult tissues, including bone marrow, adipose tissue, inner organs, and blood vessels and from rather “young sources” such as amniotic fluid, amniotic membrane, umbilical cord, or placenta [2, 14–22].”
Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle
Birbrair, A., Zhang, T., Wang, Z.-M., Messi, M. L., Mintz, A., & Delbono, O. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00171.2013 · Cited by 177 · see citing works
“Additionally, pericytes did not express the fibroblast markers FSP1(42) and Scleraxis (22, 55).”
Perivascular support of human hematopoietic stem/progenitor cells
Corselli, M., Chin, C. J., Parekh, C., Sahaghian, A., Wang, W., Ge, S., Evseenko, D., Wang, X., Montelatici, E., Lazzari, L., et al. (2013) · Blood · doi:10.1182/blood-2012-08-451864 · Cited by 189 · see citing works
Role of the endothelium in inflammatory bowel diseases
Cromer, W. E. (2011) · World Journal of Gastroenterology · doi:10.3748/wjg.v17.i5.578 · Cited by 171 · see citing works
Mesenchymal stem cell secretome and regenerative therapy after cancer
Zimmerlin, L., Park, T. S., Zambidis, E. T., Donnenberg, V. S., & Donnenberg, A. D. (2013) · Biochimie · doi:10.1016/j.biochi.2013.05.010 · Cited by 168 · see citing works
TGF-β/SMAD signaling regulation of mesenchymal stem cells in adipocyte commitment
Li, S., & Wu, J. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-1552-y · Cited by 167 · see citing works
Induced periosteum a complex cellular scaffold for the treatment of large bone defects
Cuthbert, R. J., Churchman, S. M., Tan, H. B., McGonagle, D., Jones, E., & Giannoudis, P. V. (2013) · Bone · doi:10.1016/j.bone.2013.08.009 · Cited by 159 · see citing works
Mesenchymal stromal cells and fibroblasts: a case of mistaken identity?
Hematti, P. (2012) · Cytotherapy · doi:10.3109/14653249.2012.677822 · Cited by 158 · see citing works
“(20) found signifi cant similarities between MSC and fi broblasts from different tissues but could not differentiate adipose tissue-derived MSC into osteoblasts.”
BackgroundChen, C.-W., Montelatici, E., Crisan, M., Corselli, M., Huard, J., Lazzari, L., & Péault, B. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.10.014 · Cited by 157 · see citing works
“At the same period, a functional and genetic comparison revealed striking similarities between mesenchymal stem cells classically established from various human tissues on the one hand, and CD146+ pericytes on the other hand [32].”
ResultHuman Myocardial Pericytes: Multipotent Mesodermal Precursors Exhibiting Cardiac Specificity
Chen, W. C. W., Baily, J. E., Corselli, M., Díaz, M. E., Sun, B., Xiang, G., Gray, G. A., Huard, J., & Péault, B. (2014) · Stem Cells · doi:10.1002/stem.1868 · Cited by 153 · see citing works
Multipotent stromal cells: One name, multiple identities
Soliman, H., Theret, M., Scott, W., Hill, L., Underhill, T. M., Hinz, B., & Rossi, F. M. V. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.09.001 · Cited by 147 · see citing works
Kordes, C., & Häussinger, D. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66027 · Cited by 148 · see citing works
“The expression of stem/progenitor cell–associated genes such as nestin in stellate cells of the liver and pancreas (86, 89, 92–94) and the potential of stellate cells to differentiate into hepatocyte-like cells in vitro (86, 92) indicate that stellate cells have stem cell characteristics.”
BackgroundImmune regulatory cell infusion for graft-versus-host disease prevention and therapy
Blazar, B. R., MacDonald, K. P. A., & Hill, G. R. (2018) · Blood · doi:10.1182/blood-2017-11-785865 · Cited by 146 · see citing works
Blasi, A., Martino, C., Balducci, L., Saldarelli, M., Soleti, A., Navone, S. E., Canzi, L., Cristini, S., Invernici, G., Parati, E. A., et al. (2011) · Vascular Cell · doi:10.1186/2045-824x-3-5 · Cited by 143 · see citing works
“This result expands on previous observations proposing that MSCs are different from fibroblasts and more similar to pericytes, [39] also because MSCs and pericytes are located in the wall of vasculature [6,40].”
Subramanian, A., Fong, C., Biswas, A., & Bongso, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127992 · Cited by 140 · see citing works
Mechanisms of T-Cell Immunosuppression by Mesenchymal Stromal Cells: What Do We Know So Far?
Haddad, R., & Saldanha-Araujo, F. (2014) · BioMed Research International · doi:10.1155/2014/216806 · Cited by 188 · see citing works
“001% of total mononuclear cells) [3, 6], it was demonstrated that MSCs can be obtained from virtually all adult and fetal human tissues [7].”
BackgroundIdentification of perivascular mesenchymal stromal/stem cells by flow cytometry
Corselli, M., Crisan, M., Murray, I. R., West, C. C., Scholes, J., Codrea, F., Khan, N., & Péault, B. (2013) · Cytometry Part A · doi:10.1002/cyto.a.22313 · Cited by 135 · see citing works
Schugar, R. C., Chirieleison, S. M., Wescoe, K. E., Schmidt, B., Askew, Y. S., Nance, J. J., Evron, J. M., Péault, B., & Deasy, B. M. (2009) · BioMed Research International · doi:10.1155/2009/789526 · Cited by 135 · see citing works
“…Bruno Peault, and Bridget M. Deasy This open access publication is available at Digital Commons@Becker: https://digitalcommons.wustl.edu/ open_access_pubs/975 Hindawi Publishing Corporation Journal of Biomedicine and Biotechnology Volume 2009, Article ID 789526, 11 pages doi:10.1155/2009/789526”
BackgroundMethodInfluentialPeriosteum derived stem cells for regenerative medicine proposals: Boosting current knowledge
Ferretti, C. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i3.266 · Cited by 129 · see citing works
Stem cells in gastroenterology and hepatology
Quante, M., & Wang, T. C. (2009) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2009.195 · Cited by 130 · see citing works
Progenitor Cells Identified by PDGFR-Alpha Expression in the Developing and Diseased Human Heart
Chong, J. J. H., Reinecke, H., Iwata, M., Torok‐Storb, B., Stempien‐Otero, A., & Murry, C. E. (2013) · Stem Cells and Development · doi:10.1089/scd.2012.0542 · Cited by 128 · see citing works
“CD146 is a membrane glycoprotein expressed on endothelial cells and may mark mesenchymal stromal cells with increased pluripotency [27-28].”
BackgroundMesenchymal stromal cells: misconceptions and evolving concepts
Phinney, D. G., & Sensebé, L. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2012.11.005 · Cited by 125 · see citing works
“Nevertheless, closer scrutiny of these data reveal marked differences in expression levels of lineage-restricted messenger RNAs between pericytes and MSCs (10), and more rigorous in vivo assays demonstrate clear differences in function between cells from different tissues (11,12).”
BackgroundThe secretome of mesenchymal stem cells: Potential implications for neuroregeneration
Paul, G., & Anisimov, S. V. (2013) · Biochimie · doi:10.1016/j.biochi.2013.07.013 · Cited by 121 · see citing works
Pelekanos, R., Li, J., Gongora, M., Chandrakanthan, V., Scown, J., Suhaimi, N., Brooke, G. P., Christensen, M. E., Doan, T. B., Rice, A. M., et al. (2011) · Stem Cell Research · doi:10.1016/j.scr.2011.08.003 · Cited by 117 · see citing works
Mesenchymal Stem Cells and Pericytes: To What Extent Are They Related?
de Souza, L. E. B., Malta, T. M., Kashima, S. H., & Covas, D. T. (2016) · Stem Cells and Development · doi:10.1089/scd.2016.0109 · Cited by 117 · see citing works
Self-citationThe umbilical cord: a rich and ethical stem cell source to advance regenerative medicine
Forraz, N., & McGUCKIN, C. P. (2011) · Cell Proliferation · doi:10.1111/j.1365-2184.2010.00729.x · Cited by 115 · see citing works
Lindenmair, A., Hatlapatka, T., Kollwig, G., Hennerbichler, S., Gabriel, C., Wolbank, S., Redl, H. R., & Kasper, C. (2012) · Cells · doi:10.3390/cells1041061 · Cited by 115 · see citing works
Popov, C., Burggraf, M., Kreja, L., Ignatius, A. A., Schieker, M., & Docheva, D. (2015) · BMC Molecular Biology · doi:10.1186/s12867-015-0036-6 · Cited by 112 · see citing works
“For example, CD146 was shown as marker of stem cells localized in the vascular wall [16], Nestin was found predominantly in multipotent cells from the central nervous system [17] and STRO-1 was expressed on mesenchymal stem cells in bone marrow [18].”
BackgroundIsolation 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 · see citing works
Mesenchymal stem cell and regenerative medicine: regeneration versus immunomodulatory challenges.
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A novel and simple method for culturing pericytes from mouse brain
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“CD117 (c-kit), CD146 (the melanoma cell adhesion molecule described for pericytes, as well as for MSCs with colony-forming unit-fibroblast capacity) (17), and CD166 (ALCAM)] (20,45); ii) the epithelial marker CD326 (EpCAM); iii) the stage-specific embryonic antigen SSEA-4; iv) different types of integrins (CD49-a, CD4…”
BackgroundDPSCs from Inflamed Pulp Modulate Macrophage Function via the TNF-α/IDO Axis
Lee, S., Zhang, Q. Z., Karabucak, B., & Le, A. D. (2016) · Journal of Dental Research · doi:10.1177/0022034516657817 · Cited by 110 · see citing works
“The high proportion of CD146-positive cells may be correlated to increased blood vessel formation in inflamed pulp since CD146 is high in vascular endothelial cells, smooth muscle cells, and pericytes (Covas et al. 2008).”
BackgroundIsolation of human mesenchymal stromal cells is more efficient by red blood cell lysis
Horn, P., Bork, S., Diehlmann, A., Walenda, T., Eckstein, V., Ho, A., & Wagner, W. (2008) · Cytotherapy · doi:10.1080/14653240802398845 · Cited by 107 · see citing works
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“35 More importantly, PDLSCs exhibited the abilities to form bone/cementum-like mineralized tissue and ligament structures similar to Sharpey’s fibers with an associated vasculature.”
BackgroundReconstruction of human elastic cartilage by a CD44 + CD90 + stem cell in the ear perichondrium
Kobayashi, S., Takebe, T., Inui, M., Iwai, S., Kan, H., Zheng, Y., Maegawa, J., & Taniguchi, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109767108 · Cited by 103 · see citing works
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“It has been widely accepted that Mcam as a marker for identifying MSCs isolated from bone marrow, and its higher expression on the cell surface may be linked to greater multipotency and differentiation potential [Covas et al., 2008; Russell et al., 2010].”
BackgroundAAOS Research Symposium Updates and Consensus: Biologic Treatment of Orthopaedic Injuries
LaPrade, R. F., Dragoo, J. L., Koh, J. L., Murray, I. R., Geeslin, A. G., & Chu, C. R. (2016) · Journal of the American Academy of Orthopaedic Surgeons · doi:10.5435/jaaos-d-16-00086 · Cited by 102 · see citing works
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“[4] Covas DT, Panepucci RA, Fontes AM, Silva WA Jr, Orellana MD, Freitas MC, et al.”
BackgroundPlacental Perivascular Cells for Human Muscle Regeneration
Park, T. S., Gavina, M., Chen, C.-W., Sun, B., Teng, P.-N., Huard, J., Deasy, B. M., Zimmerlin, L., & Péault, B. (2010) · Stem Cells and Development · doi:10.1089/scd.2010.0354 · Cited by 101 · see citing works
“Most cells expressing CD146 were also positive for PDGFR-b and NG2, further indicating their perivascular origin [23,26,27,32,33].”
Rossignoli, F., Caselli, A., Grisendi, G., Piccinno, M. S., Burns, J. S., Murgia, A., Veronesi, E., Loschi, P., Masini, C., Conte, P., et al. (2013) · BioMed Research International · doi:10.1155/2013/901821 · Cited by 97 · see citing works
Vascular Wall as a Reservoir for Different Types of Stem and Progenitor Cells
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“Although several studies have demonstrated similarities between peri-ECs of capillaries and MSCs (23, 88, 94, 96, 119), neither stringent cellular characterization, for example, in situ double immunostainings using different markers, nor exact cell-sorting analyses were performed yet to exactly…”
Cell Interaction with Nanopatterned Surface of Implants
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Isolation and Expansion of Mesenchymal Stem/Stromal Cells Derived from Human Placenta Tissue
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One-step derivation of cardiomyocytes and mesenchymal stem cells from human pluripotent stem cells.
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“There is strong evidence that bone marrow-derived mesenchymal stem cells (MSCs) have the potential to generate a vast array of growth factors, chemokines, and extracellular matrix molecules,(12-14) and closely share cellular and molecular properties with pericytes.(15,16) The purpose of the current clinical phase 1 in…”
BackgroundPerivascular cells as mesenchymal stem cells
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“2 Mesenchymal stem cells (MSCs) from other tissues Based on the typical mesenchymal stem cell properties of cells isolated from bone marrow such as colony-forming, self-renewal and mesenchymal lineage differentiation potentials, an increasing number of cell populations with MSClike characteristics have been reported f…”
BackgroundCharacterization of bone marrow derived mesenchymal stem cells in suspension
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“It is generally believed that BMMSCs are negative for hematopoietic cell markers such as CD14 and CD34 [5-13].”
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“demonstrated a similar gene expression profile of retinal PCs compared to MSCs from 12 different fetal and adult tissues [13], highlighting the close relationship of both cell populations.”
BackgroundResultInfluential
- 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
- Venue
- Experimental Hematology
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 36
- Issue
- 5
- Pages
- 642-654
- ISSN
- 0301-472X (ISSN-L)
- 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
- 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
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Urology › 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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