CD106 Identifies a Subpopulation of Mesenchymal Stem Cells with Unique Immunomodulatory Properties
Open accessAbstract
Mesenchymal stem cells (MSCs) reside in almost all of the body tissues, where they undergo self-renewal and multi-lineage differentiation. MSCs derived from different tissues share many similarities but also show some differences in term of biological properties. We aim to search for significant differences among various sources of MSCs and to explore their implications in physiopathology and clinical translation. We compared the phenotype and biological properties among different MSCs isolated from human term placental chorionic villi (CV), umbilical cord (UC), adult bone marrow (BM) and adipose (AD). We found that CD106 (VCAM-1) was expressed highest on the CV-MSCs, moderately on BM-MSCs, lightly on UC-MSCs and absent on AD-MSCs. CV-MSCs also showed unique immune-associated gene expression and immunomodulation. We thus separated CD106(+)cells and CD106(-)cells from CV-MSCs and compared their biological activities. Both two subpopulations were capable of osteogenic and adipogenic differentiation while CD106(+)CV-MSCs were more effective to modulate T helper subsets but possessed decreased colony formation capacity. In addition, CD106(+)CV-MSCs expressed more cytokines than CD106(-)CV-MSCs. These data demonstrate that CD106 identifies a subpopulation of CV-MSCs with unique immunoregulatory activity and reveal a previously unrecognized mechanism underlying immunomodulation of MSCs.
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CD106+ CV-MSCs can inhibit the Th1 polarization of CD4+ T cells and more effectively induce Tregs production compared to the CD106- subpopulation.
“Specifically, CD106+ CV-MSCs can inhibit the Th1 polarization of CD4+ T cells and more effectively induce Tregs production compared to the CD106- subpopulation [31].”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [31]
CD106+ CV-MSCs have higher expression levels of cytokines and a stronger effect on modulating T helper cells compared to the CD106- subpopulation.
“The CD106+ CV-MSCs had higher expression levels of cytokines and a stronger effect on modulating T helper cells compared to the CD106- subpopulation.”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [31]
CD106 is most highly expressed in human term placental chorionic villi MSCs compared with umbilical cord, adult bone marrow, and adipose tissue MSCs.
“The CD106 was most highly expressed in the CV-MSCs, whereas the CD106+ and CD106- subpopulations were evaluated for their biological properties.”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [31]
CD106+ was identified as a unique subpopulation of CV-MSCs with immunomodulatory properties.
“Overall, the CD106+ was identified as a unique subpopulation of CV-MSCs with immunomodulatory properties.”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [31]
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Cites
Multilineage potential of adult human mesenchymal stem cells
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999) · Science · doi:10.1126/science.284.5411.143 · Cited by 21,052 · see citing works
Multilineage Cells from Human Adipose Tissue: Implications for Cell-Based Therapies
Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P., & Hedrick, M. H. (2001) · Tissue Engineering · doi:10.1089/107632701300062859 · Cited by 7,956 · see citing works
Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S., & Gianni, A. M. (2002) · Blood · doi:10.1182/blood.v99.10.3838 · Cited by 3,226 · see citing works
Wegmann, T. G., Lin, H., Guilbert, L., & Mosmann, T. R. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90235-d · Cited by 2,852 · see citing works
Le Blanc, K., Rasmusson, I., Sundberg, B., Götherström, C., Hassan, M., Uzunel, M., & Ringdén, O. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16104-7 · Cited by 2,734 · see citing works
Ren, G., Zhang, L., Zhao, X., Xu, G., Zhang, Y., Roberts, A. I., Zhao, R. C., & Shi, Y. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2007.11.014 · Cited by 2,101 · see citing works
Immunomodulatory properties of mesenchymal stromal cells
Nauta, A. J., & Fibbe, W. E. (2007) · Blood · doi:10.1182/blood-2007-02-069716 · Cited by 1,787 · see citing works
Regulatory T cells mediate maternal tolerance to the fetus
Aluvihare, V. R., Kallikourdis, M., & Betz, A. G. (2004) · Nature Immunology · doi:10.1038/ni1037 · Cited by 1,661 · see citing works
Meisel, R., Zibert, A., Laryea, M. D., Göbel, U., Däubener, W., & Dilloo, D. (2004) · Blood · doi:10.1182/blood-2003-11-3909 · Cited by 1,638 · see citing works
Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy
Zappia, E., Casazza, S., Pedemonte, E., Benvenuto, F., Bonanni, I., Gerdoni, E., Giunti, D., Ceravolo, A., Cazzanti, F., Frassoni, F., et al. (2005) · Blood · doi:10.1182/blood-2005-04-1496 · Cited by 1,431 · see citing works
Multiple Female Reproductive Failures in Cyclooxygenase 2–Deficient Mice
Lim, H. J., Paria, B. C., Das, S., Dinchuk, J. E., Langenbach, R. I., Trzăskos, J. M., & Dey, S. K. (1997) · Cell · doi:10.1016/s0092-8674(00)80402-x · Cited by 1,426 · see citing works
Isolation of multipotent mesenchymal stem cells from umbilical cord blood
Lee, O. K., Kuo, T. K., Chen, W.-M., Lee, K.-D., Hsieh, S.-L., & Chen, T.-H. (2004) · Blood · doi:10.1182/blood-2003-05-1670 · Cited by 1,360 · see citing works
Role for Interferon-γ in the Immunomodulatory Activity of Human Bone Marrow Mesenchymal Stem Cells
Krampera, M., Cosmi, L., Angeli, R., Pasini, A., Liotta, F., Andreini, A., Santarlasci, V., Mazzinghi, B., Pizzolo, G., Vinante, F., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0008 · Cited by 1,311 · see citing works
Kolf, C. M., Cho, E., & Tuan, R. S. (2007) · Arthritis Research & Therapy · doi:10.1186/ar2116 · Cited by 951 · see citing works
Lu, L., Liu, Y.-J., Yang, S.-G., Zhao, Q., Wang, X., Gong, W., Han, Z., Xu, Z., Lu, Y., Liu, D., et al. (2006) · PubMed · Cited by 753 · see citing works
Self-citationNauta, A. J., Kruisselbrink, A. B., Lurvink, E. G. A., Willemze, R., & Fibbe, W. E. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2080 · Cited by 741 · see citing works
Ren, G., Zhao, X., Zhang, L., Zhang, J., L'Huillier, A., Ling, W., Roberts, A. I., Le, A. D., Shi, S., Shao, C., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902023 · Cited by 655 · see citing works
Human Placenta‐Derived Cells Have Mesenchymal Stem/Progenitor Cell Potential
Fukuchi, Y., Nakajima, H., Sugiyama, D., Hirose, I., Kitamura, T., & Tsuji, K. (2004) · Stem Cells · doi:10.1634/stemcells.22-5-649 · Cited by 646 · see citing works
IFN‐γ activation of mesenchymal stem cells for treatment and prevention of graft versus host disease
Polchert, D., Sobinsky, J., Douglas, G., Kidd, M. E., Moadsiri, A., Reina, E., Genrich, K., Mehrotra, S., Setty, S., Smith, B., et al. (2008) · European Journal of Immunology · doi:10.1002/eji.200738129 · Cited by 580 · see citing works
Mother's little helpers: mechanisms of maternal-fetal tolerance
Trowsdale, J., & Betz, A. G. (2006) · Nature Immunology · doi:10.1038/ni1317 · Cited by 576 · see citing works
Kwee, L., Baldwin, H. S., Shen, H. M., Stewart, C. L., Buck, C. E., Buck, C. A., & Labow, M. (1995) · Development · doi:10.1242/dev.121.2.489 · Cited by 557 · see citing works
Prasanna, S. J., Gopalakrishnan, D., Shankar, S. R., & Vasandan, A. B. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009016 · Cited by 468 · see citing works
A critical role for the programmed death ligand 1 in fetomaternal tolerance
Guleria, I., Khosroshahi, A., Ansari, M. J., Habicht, A., Azuma, M., Yagita∥, H., Noelle, R. J., Coyle, A. J., Mellor, A. L., Khoury, S. J., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050019 · Cited by 439 · see citing works
Simmons, P., Masinovsky, B. P., Longenecker, B. M., Berenson, R. J., Torok-Storb, B., & Gallatin, W. M. (1992) · Blood · doi:10.1182/blood.v80.2.388.388 · Cited by 419 · see citing works
IFN-γ and TNF-α differentially regulate immunomodulation by murine mesenchymal stem cells
English, K., Barry, F., Field-Corbett, C., & Mahon, B. P. (2007) · Immunology Letters · doi:10.1016/j.imlet.2007.04.001 · Cited by 417 · see citing works
Németh, K., Keane‐Myers, A., Brown, J. M., Metcalfe, D. D., Gorham, J. D., Bundoc, V., Hodges, M. G., Jelinek, I., Madala, S. K., Kárpáti, S., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910720107 · Cited by 407 · see citing works
Gurtner, G. C., Davis, V., Li, H., McCoy, M. J., Sharpe, A. H., & Cybulsky, M. I. (1995) · Genes & Development · doi:10.1101/gad.9.1.1 · Cited by 396 · see citing works
A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation
Braun, D., Longman, R., & Albert, M. L. (2005) · Blood · doi:10.1182/blood-2005-03-0979 · Cited by 390 · see citing works
Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells
Gieseke, F., Böhringer, J., Bussolari, R., Dominici, M., Handgretinger, R., & Müller, I. (2010) · Blood · doi:10.1182/blood-2010-02-270777 · Cited by 269 · see citing works
Robin, C., Bollérot, K., Mendes, S., Haak, E., Crisan, M., Cerisoli, F., Lauw, I., Kaimakis, P., Jorna, R., Vermeulen, M. M., et al. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.08.020 · Cited by 234 · see citing works
Chen, K., Wang, D., Du, W. T., Han, Z., Ren, H., Chi, Y., Yang, S. G., Zhu, D., Bayard, F., & Han, Z. (2010) · Clinical Immunology · doi:10.1016/j.clim.2010.01.015 · Cited by 201 · see citing works
Self-citationKokovay, E., Wang, Y., Kusek, G., Wurster, R., Lederman, P. L., Lowry, N. A., Shen, Q., & Temple, S. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.06.016 · Cited by 199 · see citing works
Self-citationHsieh, J.-Y., Fu, Y.-S., Chang, S.-J., Tsuang, Y., & Wang, H. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0485 · Cited by 189 · see citing works
The Link between the PDL1 Costimulatory Pathway and Th17 in Fetomaternal Tolerance
D’Addio, F., Riella, L. V., Mfarrej, B. G., Chabtini, L., Adams, L. T., Yeung, M. Y., Yagita∥, H., Azuma, M., Sayegh, M. H., & Guleria, I. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002031 · Cited by 172 · see citing works
HLA-G is a Crucial Immunosuppressive Molecule Secreted by Adult Human Mesenchymal Stem Cells
Selmani, Z., Naji, A., Gaiffe, É., Obert, L., Tiberghien, P., Rouas‐Freiss, N., Carosella, E. D., & Deschaseaux, F. (2009) · Transplantation · doi:10.1097/tp.0b013e3181a2a4b3 · Cited by 150 · see citing works
Bieback, K., Kern, S., Kocaömer, A., Ferlik, K., & Bugert, P. (2008) · PubMed · Cited by 140 · see citing works
Jansen, B. J. H., Gilissen, C., Roelofs, H., Schaap-Oziemlak, A., Veltman, J. A., Raymakers, R. A. P., Jansen, J. H., Kögler, G., Figdor, C. G., Torensma, R., et al. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0288 · Cited by 139 · see citing works
Hwang, J. H., Shim, S. S., Seok, O. S., Lee, H. Y., Woo, S. K., Kim, B. H., Song, H. R., Lee, J. K., & Park, Y. K. (2009) · Journal of Korean Medical Science · doi:10.3346/jkms.2009.24.4.547 · Cited by 133 · see citing works
Simón, C., Valbuena, D., Krüssel, J.-S., Bernal, A., Murphy, C. R., Shaw, T., Pellicer, A., & Polan, M. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00275-1 · Cited by 130 · see citing works
Bernardo, M. E., Emons, J. A. M., Karperien, M., Nauta, A. J., Willemze, R., Roelofs, H., Romeo, S. O., Marchini, A., Rappold, G., Vukičević, S., et al. (2007) · Connective Tissue Research · doi:10.1080/03008200701228464 · Cited by 122 · see citing works
Terness, P., Kallikourdis, M., Betz, A. G., Rabinovich, G. A., Saito, S., & Clark, D. A. (2007) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2007.00510.x · Cited by 114 · see citing works
Guo, L., Zhang, X., Wang, H., Wang, X., Meng, C., Chan, C., Yew, D. T. W., Tsang, K. S., Li, K., Tsai, S., et al. (2008) · PROTEOMICS · doi:10.1002/pmic.200701195 · Cited by 113 · see citing works
Self-citationTumor Necrosis Factor- in the Female Reproductive Tract
Terranova, P. F., Hunter, V., Roby, K. F., & Hunt, J. S. (1995) · Experimental Biology and Medicine · doi:10.3181/00379727-209-43905b · Cited by 113 · see citing works
Cesario, A., Rocca, B., & Rutella, S. (2011) · Current Medicinal Chemistry · doi:10.2174/092986711795656063 · Cited by 77 · see citing works
CD14+ monocytes promote the immunosuppressive effect of human umbilical cord matrix stem cells
Wang, D., Chen, K., Du, W. T., Han, Z., Ren, H., Chi, Y., Yang, S. G., Bayard, F., Zhu, D., & Han, Z. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.04.018 · Cited by 51 · see citing works
Self-citationVacchio, M. S., & Hodes, R. J. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.8.4657 · Cited by 48 · see citing works
Mattsson, R., Holmdahl, R., Scheynius, A., Bernadotte, F., Mattsson, A., & van der Meide, P. H. (1991) · Journal of Reproductive Immunology · doi:10.1016/0165-0378(91)90012-f · Cited by 42 · see citing works
Interleukin‐1 in reproductive strategies
Paulesu, L. R., Jantra, S., Ietta, F., Brizzi, R., & Bigliardi, E. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00292.x · Cited by 37 · see citing works
Liu, M., Yang, S. G., Shi, L., Du, W. T., Liu, P. X., Xu, J., Gu, D. S., Liang, L., Dong, C. L., & Han, Z. (2010) · Platelets · doi:10.3109/09537101003602483 · Cited by 16 · see citing works
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Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro
Yang, Y.-H. K., Ogando, C. R., See, C. W., Chang, T.-Y., & Barabino, G. A. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0876-3 · Cited by 637 · see citing works
Biological functions of mesenchymal stem cells and clinical implications
Naji, A., Eitoku, M., Favier, B., Deschaseaux, F., Rouas‐Freiss, N., & Suganuma, N. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03125-1 · Cited by 628 · see citing works
Madrigal, M., Rao, K. S. J., & Riordan, N. H. (2014) · Journal of Translational Medicine · doi:10.1186/s12967-014-0260-8 · Cited by 615 · see citing works
Mesenchymal stem cells: Immunomodulatory capability and clinical potential in immune diseases
Zhao, Q., Ren, H., & Han, Z. (2015) · Journal of Cellular Immunotherapy · doi:10.1016/j.jocit.2014.12.001 · Cited by 303 · see citing works
Self-citationMattar, P., & Bieback, K. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00560 · Cited by 301 · see citing works
A Brief Overview of Global Trends in MSC-Based Cell Therapy
Jovic, D., Yu, Y., Wang, D., Wang, K., Li, H., Xu, F., Liu, C., Liu, J., & Luo, Y. (2022) · Stem Cell Reviews and Reports · doi:10.1007/s12015-022-10369-1 · Cited by 295 · see citing works
Proangiogenic Features of Mesenchymal Stem Cells and Their Therapeutic Applications
Tao, H., Han, Z., Han, Z., & Li, Z. (2016) · Stem Cells International · doi:10.1155/2016/1314709 · Cited by 277 · see citing works
Self-citationWu, M., Zhang, R., Zou, Q., Chen, Y., Zhou, M., Li, X., Ran, R., & Chen, Q. (2018) · Scientific Reports · doi:10.1038/s41598-018-23396-1 · Cited by 206 · see citing works
Adipose-derived stem cells secretome and its potential application in “stem cell-free therapy”
Trzyna, A., & Banaś-Ząbczyk, A. (2021) · Biomolecules · doi:10.3390/biom11060878 · Cited by 201 · see citing works
Advances in regenerative therapy: A review of the literature and future directions
Ntege, E. H., Sunami, H., & Shimizu, Y. (2020) · Regenerative Therapy · doi:10.1016/j.reth.2020.01.004 · Cited by 197 · see citing works
Adipose-derived mesenchymal stromal/stem cells: An update on their phenotype in vivo and in vitro
Baer, P. C. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i3.256 · Cited by 189 · see citing works
Galland, S., & Stamenkovic, I. (2020) · The Journal of Pathology · doi:10.1002/path.5357 · Cited by 165 · see citing works
Mesenchymal stem cell subpopulations: phenotype, property and therapeutic potential
Mo, M., Wang, S., Zhou, B. Y., Li, H., & Wu, Y. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2229-7 · Cited by 142 · 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
Immunomodulatory properties of human placental mesenchymal stem/stromal cells
Abumaree, M., Abomaray, F., Alshabibi, M. A., Alaskar, A. S., & Kalionis, B. (2017) · Placenta · doi:10.1016/j.placenta.2017.04.003 · Cited by 141 · see citing works
Du, W., Li, X., Chi, Y., Ma, F., Li, Z., Yang, S., Song, B., Cui, J., Ma, T., Li, J., et al. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0297-0 · Cited by 114 · see citing works
Self-citationMardpour, S., Hassani, S., Mardpour, S., Sayahpour, F. A., Vosough, M., Ai, J., Aghdami, N., Hamidieh, A. A., & Baharvand, H. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26413 · Cited by 110 · see citing works
Sun, C., Wang, L., Wang, H., Huang, T., Yao, W., Li, J., & Zhang, X. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01660-4 · Cited by 108 · see citing works
Self-citationHe, N., Kong, Y., Lei, X., Liu, Y., Wang, J., Xu, C., Wang, Y., Du, L., Ji, K., wang, Q., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0949-3 · Cited by 100 · see citing works
Self-citationGosnell, M. E., Anwer, A. G., Mahbub, S. B., Perinchery, S. M., Inglis, D. W., Adhikary, P. P., Jazayeri, J. A., Cahill, M. A., Saad, S., Pollock, C. A., et al. (2016) · Scientific Reports · doi:10.1038/srep23453 · Cited by 93 · see citing works
Aging of mesenchymal stem cells: Implication in regenerative medicine
Yang, Y.-H. K. (2018) · Regenerative Therapy · doi:10.1016/j.reth.2018.09.002 · Cited by 93 · see citing works
Gao, Y., Chi, Y., Chen, Y., Wang, W., Li, H., Zheng, W., Zhu, P., An, J., Duan, Y., Sun, T., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39958-5 · Cited by 92 · see citing works
Self-citationLiang, L., Li, Z., Ma, T., Han, Z., Du, W., Geng, J., Jia, H., Zhao, M., Wang, J., Zhang, B., et al. (2016) · Cell Transplantation · doi:10.3727/096368916x692726 · Cited by 87 · see citing works
Self-citationTherapeutic Mesenchymal Stromal Cells for Immunotherapy and for Gene and Drug Delivery
Almeida-Porada, G. D., Atala, A., & Porada, C. D. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.01.005 · Cited by 88 · see citing works
Parolini, O., Souza‐Moreira, L., O’Valle, F., Magatti, M., Hernández‐Cortés, P., González‐Rey, E., & Delgado, M. (2013) · Arthritis & Rheumatology · doi:10.1002/art.38206 · Cited by 87 · see citing works
An update on stem cell therapy for Asherman syndrome
Benor, A. Z., Gay, S., & DeCherney, A. H. (2020) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-020-01801-x · Cited by 84 · see citing works
Single-Cell Transcriptomic Analysis Reveals the Cellular Heterogeneity of Mesenchymal Stem Cells
Zhang, C., Han, X., Liu, J., Chen, L., Lei, Y., Chen, K., Si, J., Wang, T.-Y., Zhou, H. F., Zhao, X., et al. (2022) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2022.01.005 · Cited by 87 · see citing works
Self-citationMolecular imaging for assessment of mesenchymal stem cells mediated breast cancer therapy
Leng, L., Wang, Y., He, N., Wang, D., Zhao, Q., Feng, G., Su, W., Xu, Y., Han, Z., Kong, D., et al. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.03.014 · Cited by 84 · see citing works
Self-citationMarklein, R. A., Klinker, M. W., Drake, K., Polikowsky, H. G., Lessey-Morillon, E. C., & Bauer, S. R. (2018) · Cytotherapy · doi:10.1016/j.jcyt.2018.10.008 · Cited by 82 · see citing works
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de Carvalho, A. É. S., Sousa, M. R. R., Alencar‐Silva, T., Carvalho, J. L., & Saldanha‐Araújo, F. (2019) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2019.05.006 · Cited by 79 · see citing works
Skeletal Stem Cells for Bone Development and Repair: Diversity Matters
Matsushita, Y., Ono, W., & Ono, N. (2020) · Current Osteoporosis Reports · doi:10.1007/s11914-020-00572-9 · Cited by 77 · see citing works
Wei, Y., Zhang, L., Chi, Y., Ren, X., Gao, Y., Song, B., Li, C., Han, Z., Zhang, L., & Han, Z. (2020) · Cell Proliferation · doi:10.1111/cpr.12862 · Cited by 76 · see citing works
Self-citationZhang, J., Chen, M., Liao, J., Chang, C., Liu, Y., Padhiar, A. A., Zhou, Y., & Zhou, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.716907 · Cited by 74 · see citing works
Growth plate skeletal stem cells and their transition from cartilage to bone
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Oh, S.-Y., Choi, Y. M., Kim, H. Y., Park, Y. S., Jung, S., Park, J., Woo, S., Ryu, K., Kim, H. S., & Jo, I. (2019) · Stem Cells · doi:10.1002/stem.3058 · Cited by 65 · see citing works
Zeng, X., Tang, Y., Hu, K., Wang, J., Liu, Y., Zhu, L., Liu, J., & Xu, J. (2017) · Medicine · doi:10.1097/md.0000000000009212 · Cited by 62 · see citing works
Origins of the breast milk‐derived cells; an endeavor to find the cell sources
Sani, M., Hosseini, S. M., Salmannejad, M., Aleahmad, F., Ebrahimi, S., Jahanshahi, S., & Talaei‐Khozani, T. (2015) · Cell Biology International · doi:10.1002/cbin.10432 · Cited by 60 · see citing works
Du, W., Reppel, L., Avercenc-Leger, L., Schenowitz, C., Huselstein, C., Bensoussan, D., Carosella, E. D., Han, Z., & Rouas‐Freiss, N. (2016) · Stem Cells and Development · doi:10.1089/scd.2016.0022 · Cited by 55 · see citing works
Self-citationImmune modulation via adipose derived Mesenchymal Stem cells is driven by donor sex in vitro
Mckinnirey, F., Herbert, B. R., Vesey, G., & McCracken, S. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-91870-4 · Cited by 54 · see citing works
Are mesenchymal stromal cells immune cells?
Hoogduijn, M. J. (2015) · Arthritis Research & Therapy · doi:10.1186/s13075-015-0596-3 · Cited by 54 · see citing works
Advantages and challenges of stem cell therapy for osteoarthritis (Review)
Loo, S., & Wong, N. K. (2021) · Biomedical Reports · doi:10.3892/br.2021.1443 · Cited by 53 · see citing works
New insights into the heterogeneity and functional diversity of human mesenchymal stem cells
Han, Z., Du, W. J., Han, Z., & Liang, L. (2017) · Bio-Medical Materials and Engineering · doi:10.3233/bme-171622 · Cited by 53 · see citing works
Self-citationImmune impairments in multiple myeloma bone marrow mesenchymal stromal cells
André, T., Najar, M., Stamatopoulos, B., Pieters, K., Pradier, O., Bron, D., Meuleman, N., & Lagneaux, L. (2014) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-014-1623-y · Cited by 51 · see citing works
Aghayan, H. R., Salimian, F., Abedini, A., Ghazi, S. F., Yunesian, M., Alavi-Moghadam, S., Makarem, J., Majidzadeh‐A, K., Hatamkhani, A., Moghri, M., et al. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02953-6 · Cited by 49 · see citing works
Unveiling heterogeneity in MSCs: exploring marker-based strategies for defining MSC subpopulations
Chen, S., Liang, B., & Xu, J. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05294-5 · Cited by 55 · see citing works
Sugiyama, Y., Sato, Y., Kitase, Y., Suzuki, T., Kondo, T., Mikrogeorgiou, A., Horinouchi, A., Maruyama, S., Shimoyama, Y., Tsuji, M., et al. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00757 · Cited by 48 · see citing works
Mesenchymal Stem Cell Transplantation for Ischemic Diseases: Mechanisms and Challenges
Nguyen, T.-T. V., Vu, N. B., & Pham, P. V. (2021) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-021-00334-3 · Cited by 46 · see citing works
Leukocytes Crossing the Endothelium: A Matter of Communication
Timmerman, I., Daniel, A. E., Kroon, J., & van Buul, J. D. (2016) · International review of cytology · doi:10.1016/bs.ircmb.2015.10.005 · Cited by 45 · see citing works
Huang, Q., Cheng, X., Luo, C., Yang, S., Li, S., Wang, B., Yuan, X., Yang, Y., Wen, Y., Liu, R., et al. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02411-9 · Cited by 44 · see citing works
Self-citationSrinivasan, A., Sathiyanathan, P., Yin, L., Liu, T. M., Lam, A., Ravikumar, M., Smith, R. A. A., Loh, H. P., Zhang, Y., Ling, L., et al. (2022) · Cytotherapy · doi:10.1016/j.jcyt.2021.11.009 · Cited by 44 · see citing works
Hao, D., He, C., Ma, B., Lankford, L., Reynaga, L., Farmer, D. L., Guo, F., & Wang, A. (2019) · Stem Cells International · doi:10.1155/2019/9695239 · Cited by 44 · see citing works
An Overview of Mesenchymal Stem Cell Heterogeneity and Concentration
Maličev, E., & Jazbec, K. (2024) · Pharmaceuticals · doi:10.3390/ph17030350 · Cited by 44 · see citing works
Zhang, J., Yuan, B., Zhang, H., & Li, H. (2019) · Oncology Letters · doi:10.3892/ol.2019.10221 · Cited by 41 · see citing works
Mennan, C., Garcia, J., McCarthy, H. S., Owen, S., Perry, J., Wright, K. T., Banerjee, R., Richardson, J. B., & Roberts, S. (2018) · Cartilage · doi:10.1177/1947603518769714 · Cited by 40 · see citing works
Bertheuil, N., Chaput, B., Menard, C., Varin, A., Laloze, J., Watier, É., & Tarte, K. (2018) · Annales de Chirurgie Plastique Esthétique · doi:10.1016/j.anplas.2018.07.005 · Cited by 40 · see citing works
Yang, Z., Dong, P., Fu, X., Li, Q., Ma, S., Wu, D., Kang, N., Liu, X., Li, Y., & Xiao, R. (2015) · Stem Cells · doi:10.1002/stem.2063 · Cited by 39 · see citing works
Self-citationZou, Y., Yang, X., Yuan, S., Zhang, P., Ye, Y.-L., & Li, Y. (2016) · Connective Tissue Research · doi:10.3109/03008207.2015.1127916 · Cited by 39 · see citing works
High throughput screening of mesenchymal stem cell lines using deep learning
Kim, G., Jeon, J. H., Park, K., Kim, S. W., Kim, D. H., & Lee, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-21653-y · Cited by 39 · see citing works
Human placental extract: a potential therapeutic in treating osteoarthritis
Gwam, C. U., Ohanele, C., Hamby, J., Chughtai, N., Mufti, Z., & Ma, X. (2021) · Annals of Translational Medicine · doi:10.21037/atm.2019.10.20 · Cited by 37 · see citing works
Hoffmann, A., Floerkemeier, T., Melzer, C., & Hass, R. (2016) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2153 · Cited by 39 · see citing works
Stem cells as a potential therapy for diabetes mellitus: a call-to-action in Latin America
Solís, M. A., Velásquez, I. M., Correa, R., & Huang, L. L. H. (2019) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-019-0415-0 · Cited by 38 · see citing works
Huang, Q., Yang, Y., Luo, C., Wen, Y., Liu, R., Li, S., Chen, T., Sun, H., & Tang, L. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1405-8 · Cited by 38 · see citing works
Yang, C., Wu, M., You, M., Chen, Y., Luo, M., & Chen, Q. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02158-3 · Cited by 38 · see citing works
Chia, W. K., Cheah, F., Aziz, N. H. A., Kampan, N. C., Shuib, S., Khong, T. Y., Tan, G. C., & Wong, Y. P. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2021.615508 · Cited by 38 · see citing works
Yang, C., Chen, Y., Li, F., You, M., Zhong, L., Li, W., Zhang, B., & Chen, Q. (2018) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-018-3284-1 · Cited by 36 · see citing works
Budgude, P., Kale, V. P., & Vaidya, A. (2020) · Cell Biology International · doi:10.1002/cbin.11313 · Cited by 36 · see citing works
Transplantation of dental tissue-derived mesenchymal stem cells ameliorates nephritis in lupus mice
Tang, X., Li, W., Wen, X., Zhang, Z., Chen, W., Yao, G., Chen, H., Wang, D., Shi, S., & Sun, L. (2019) · Annals of Translational Medicine · doi:10.21037/atm.2019.02.41 · Cited by 35 · see citing works
Investigating heterogeneities of live mesenchymal stromal cells using AI-based label-free imaging
Imboden, S., Liu, X., Lee, B. S., Payne, M. C., Hsieh, C., & Lin, N. Y. C. (2021) · Scientific Reports · doi:10.1038/s41598-021-85905-z · Cited by 35 · see citing works
Jung, S.-Y., Lee, S., Kim, H. J., Kim, S., Moon, J. H., Chung, H., Kang, S., & Park, C. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-00949-7 · Cited by 34 · see citing works
Kmiecik, G., Spoldi, V., Silini, A. R., & Parolini, O. (2014) · Stem Cell Reviews and Reports · doi:10.1007/s12015-014-9569-1 · Cited by 34 · see citing works
Perspective of placenta derived mesenchymal stem cells in acute liver failure
Saleh, M., Taher, M., Sohrabpour, A. A., Vaezi, A. A., Toosi, M. N., Kavianpour, M., Ghazvinian, Z., Abdolahi, S., & Verdi, J. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00433-z · Cited by 32 · see citing works
Application of Wharton jelly-derived mesenchymal stem cells in patients with pulmonary fibrosis
Saleh, M., Kiaei, S. Z. F., & Kavianpour, M. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02746-x · Cited by 36 · see citing works
Proteomic Profiling of Native Unpassaged and Culture‐Expanded Mesenchymal Stromal Cells (MSC)
Moravčíková, E., Meyer, E. M., Corselli, M., Donnenberg, V. S., & Donnenberg, A. D. (2018) · Cytometry Part A · doi:10.1002/cyto.a.23574 · Cited by 34 · see citing works
Lu, S., Ge, M., Zheng, Y., Li, J., Feng, X., Feng, S., Huang, J., Feng, Y., Yang, D., Shi, J., et al. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0620-4 · Cited by 33 · see citing works
Self-citationO’Connor, K. C. (2019) · Stem Cells International · doi:10.1155/2019/5924878 · Cited by 31 · see citing works
Dunn, C. M., Kameishi, S., Cho, Y.-K., Song, S. U., Grainger, D. W., & Okano, T. (2022) · Cells · doi:10.3390/cells11233738 · Cited by 30 · see citing works
Kwee, B. J., Lam, J., Akue, A. D., KuKuruga, M. A., Zhang, K., Gu, L., & Sung, K. E. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2105972118 · Cited by 30 · see citing works
Liu, J., Han, Z., Han, Z., & He, Z. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2953 · Cited by 30 · see citing works
Self-citationHarrington, J., Sloan, A. J., & Waddington, R. J. (2014) · Connective Tissue Research · doi:10.3109/03008207.2014.923859 · Cited by 29 · see citing works
Wang, X., Zhang, H., Nie, L., Xu, L., Chen, M., & Ding, Z. (2014) · Stem Cell Research & Therapy · doi:10.1186/scrt481 · Cited by 29 · see citing works
Immunoregulatory properties of mesenchymal stem cells: Micro-RNAs
Rostami, Z., Khorashadizadeh, M., & Naseri, M. (2020) · Immunology Letters · doi:10.1016/j.imlet.2019.12.011 · Cited by 28 · see citing works
Li, Y., Zou, Y., Yuan, S., Zhang, P., & Yang, X. (2016) · Drug Design Development and Therapy · doi:10.2147/dddt.s97463 · Cited by 28 · see citing works
Adult Stem Cell Functioning in the Tumor Micro-Environment
Jiang, Y., Wells, A. H., Sylakowski, K., Clark, A. M., & Ma, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102566 · Cited by 26 · see citing works
Fujita, R., Tamai, K., Aikawa, E., Nimura, K., Ishino, S., Kikuchi, Y., & Kaneda, Y. (2014) · Stem Cells · doi:10.1002/stem.1900 · Cited by 25 · see citing works
Stem cell‐like populations and immunoregulatory molecules in periodontal granulation tissue
Apatzidou, D. A., Nile, C. J., Bakopoulou, A., Konstantinidis, A. O., & Lappin, D. F. (2018) · Journal of Periodontal Research · doi:10.1111/jre.12551 · Cited by 28 · see citing works
Fan, D., Zeng, M., Xia, Q., Wu, S., Ye, S., Rao, J., Lin, D., Zhang, H., Ma, H., Han, Z., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01695-7 · Cited by 24 · see citing works
Self-citationLow Molecular Weight Hyaluronic Acid Effect on Dental Pulp Stem Cells In Vitro
Schmidt, J., Pilbauerová, N., Soukup, T., Kleplová, T. S., & Suchánek, J. (2020) · Biomolecules · doi:10.3390/biom11010022 · Cited by 24 · see citing works
Isolation and characterization of multipotent mesenchymal stem cells in nasal polyps
Cho, J.-S., Park, J., Kang, J.-H., Kim, S. E., Park, I., & Lee, H.-M. (2014) · Experimental Biology and Medicine · doi:10.1177/1535370214553898 · Cited by 24 · see citing works
Paladino, F. V., Sardinha, L. R., Piccinato, C. A., & Goldberg, A. C. (2017) · Stem Cells International · doi:10.1155/2017/8492797 · Cited by 23 · see citing works
Yen, B. L., Liu, K., Sytwu, H., & Yen, M. (2022) · FEBS Journal · doi:10.1111/febs.16438 · Cited by 23 · see citing works
Schäck, L. M., Noack, S., Weist, R., Jagodzinski, M., Krettek, C., Büettner, M., & Hoffmann, A. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0290 · Cited by 23 · see citing works
Shan, Z., Hirai, Y., Nakayama, M., Hayashi, R., Yamasaki, T., Hasebe, R., Song, C., & Horiuchi, M. (2017) · Journal of General Virology · doi:10.1099/jgv.0.000907 · Cited by 22 · see citing works
Heterogeneity of Human Mesenchymal Stromal/Stem Cells
Wang, W., & Han, Z. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-11096-3_10 · Cited by 22 · see citing works
Self-citationCD317-Positive Immune Stromal Cells in Human “Mesenchymal Stem Cell” Populations
Kay, A. G., Fox, J. M., Hewitson, J. P., Stone, A. P., Robertson, S., James, S. R., Wang, X., Kapasa, E., Yang, X., & Genever, P. G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.903796 · Cited by 21 · see citing works
Tey, S.-R., Robertson, S., Lynch, E. M., & Suzuki, M. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00284 · Cited by 20 · see citing works
The Kidney Precision Medicine Project and Single-Cell Biology of the Injured Proximal Tubule
Janosevic, D., Luca, T. D., & Eadon, M. T. (2024) · American Journal Of Pathology · doi:10.1016/j.ajpath.2024.09.006 · Cited by 20 · see citing works
Sober, S. A., Darmani, H., Alhattab, D. M., & Awidi, A. (2021) · Archives of Medical Science · doi:10.5114/aoms/131088 · Cited by 20 · see citing works
Hyland, M., Mennan, C., Davies, R., Wilson, E., Tonge, D. P., Clayton, A., & Kehoe, O. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10586-2 · Cited by 20 · see citing works
Knockdown of IL-8 Provoked Premature Senescence of Placenta-Derived Mesenchymal Stem Cells
Li, J., Ma, F., Wang, Y., Chen, F., Lu, S., Chi, Y., Du, W., Song, B., Hu, L., Chen, H., et al. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0324 · Cited by 20 · see citing works
Self-citationBaron, M., Drohat, P., Crawford, B., Hornicek, F. J., Best, T. M., & Kouroupis, D. (2023) · Bioengineering · doi:10.3390/bioengineering10101187 · Cited by 19 · see citing works
- Authors
- Yang, Z. X., Han, Z.-B., Ji, Y. R., Wang, Y. W., Liang, L., Chi, Y., Yang, S. G., Li, L. N., Luo, W. F., Li, J. P., Chen, D. D., Du, W. J., Cao, X. C., Zhuo, G. S., Wang, T., & Han, Z. C.
- Affiliations
- Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
- Beijing Institute for Stem Cell and Regenerative Medicine (CN)
- Jinan University (CN)
- Tianjin Medical University General Hospital (CN)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-03-12
- Volume
- 8
- Issue
- 3
- Pages
- e59354
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3595282
- OpenAlex
- W2041436853
- Cited by
- 225
- References
- 49
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 18 · 2023: 14 · 2022: 28 · 2021: 22 · 2020: 22 · 2019: 25 · 2018: 20 · 2017: 16 · 2016: 13 · 2015: 10 · 2014: 15 · 2013: 3
- FWCI
- 6.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- School of Medicine, Indiana University
- National Key Research and Development Program of China (2011CB964802, 2011AA020118, 2011CB964800)
- Topics
- Health Sciences › Medicine › Genetics › 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, VCAM-1, umbilical cord, bone marrow, adipose tissue, immunomodulation, osteogenic differentiation, adipogenesis, cytokine expression, colony formation, cell subpopulations
- MeSH terms
- Adipose Tissue, Adult, Bone Marrow Cells, Cell Differentiation, Chorion, Female, T-Lymphocytes, Helper-Inducer, Humans, Osteocytes, Pregnancy, Umbilical Cord, Biomarkers, Gene Expression, Cytokines, Adipocytes, Vascular Cell Adhesion Molecule-1, Immunomodulation, Mesenchymal Stem Cells
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