Tissue source determines the differentiation potentials of mesenchymal stem cells: a comparative study of human mesenchymal stem cells from bone marrow and adipose tissue
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BACKGROUND: Mesenchymal stem cells (MSCs) possess intrinsic regeneration capacity as part of the repair process in response to injury, such as fracture or other tissue injury. Bone marrow and adipose tissue are the major sources of MSCs. However, which cell type is more effective and suitable for cell therapy remains to be answered. The intrinsic molecular mechanism supporting the assertion has also been lacking. METHODS: Human bone marrow-derived MSCs (BMSCs) and adipose tissue-derived MSCs (ATSCs) were isolated from bone marrow and adipose tissue obtained after total hip arthroplasty. ATSCs and BMSCs were incubated in standard growth medium. Trilineage differentiation including osteogenesis, adipogenesis, and chondrogenesis was performed by addition of relevant induction mediums. The expression levels of trilineage differentiation marker genes were evaluated by quantitative RT-PCR. The methylation status of CpG sites of Runx2, PPARγ, and Sox9 promoters were checked by bisulfite sequencing. In addition, ectopic bone formation and calvarial bone critical defect models were used to evaluate the bone regeneration ability of ATSCs and BMSCs in vivo. RESULTS: The results showed that BMSCs possessed stronger osteogenic and lower adipogenic differentiation potentials compared to ATSCs. There was no significant difference in the chondrogenic differentiation potential. The CpG sites of Runx2 promoter in BMSCs were hypomethylated, while in ATSCs they were hypermethylated. The CpG sites of PPARγ promoter in ATSCs were hypomethylated, while in BMSCs they were hypermethylated. The methylation status of Sox9 promoter in BMSCs was only slightly lower than that in ATSCs. CONCLUSIONS: The epigenetic memory obtained from either bone marrow or adipose tissue favored MSC differentiation along an osteoblastic or adipocytic lineage. The methylation status of the main transcription factors controlling MSC fate contributes to the differential differentiation capacities of different source-derived MSCs.
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Studies comparing the osteogenic potential of human BM-MSCs and ASCs have yielded mixed results.
“Regarding bone tissue engineering, studies comparing the osteogenic potential of human BM-MSCs and ASCs have yielded mixed results.”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [61]
The Background (page not provided) reports conflicting results from studies comparing ATSCs and BMSCs, but describes those results as concerning clinical application potential, not specifically osteogenic potential. In its own osteogenesis Results, the paper finds greater osteogenic differentiation in BMSCs than ATSCs. The claim therefore narrows the reported disagreement beyond what this source states. (LLM, conf=0.82)
Experimental — accuracy not yet measuredSome studies suggest that BM-MSCs exhibit greater osteogenic capacity than ASCs.
“Some suggest that BM-MSCs exhibit greater osteogenic capacity [58,59,60,61,62], while others propose that ASCs have equal or superior potential [58,63,64,65,66].”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [61]
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Cites
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
Stöckl, S., Göttl, C., Grifka, J. K., & Grässel, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350089 · Cited by 4,670 · see citing works
Liao, J., Wei, Q., Zou, Y., Fan, J., Song, D., Cui, J., Zhang, W., Zhu, Y., Ma, C., Hu, X. Y., et al. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000471945 · Cited by 2,742 · see citing works
Self-citationChen, J., Sanberg, P. R., Li, Y., Wang, L., Lü, M., Willing, A. E., Sanchez‐Ramos, J., & Chopp, M. (2001) · Stroke · doi:10.1161/hs1101.098367 · Cited by 1,347 · 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
Puissant‐Lubrano, B., Barreau, C., Bourin, P., Clavel, C., Corre, J., Bousquet, C., Taureau, C., Cousin, B., Abbal, M., Laharrague, P. F., et al. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05409.x · Cited by 957 · see citing works
Lee, R. H., Kim, B., Choi, I., Kim, H., Choi, H. S., Suh, K. T., Bae, Y. C., & Jung, J. S. (2004) · Cellular Physiology and Biochemistry · doi:10.1159/000080341 · Cited by 933 · see citing works
Human marrow stromal cell therapy for stroke in rat
Li, Y., Chen, J., Chen, X. G., Wang, L., Gautam, S. C., Xu, Y. X., Katakowski, M., Zhang, L. J., Lü, M., Janakiraman, N., et al. (2002) · Neurology · doi:10.1212/wnl.59.4.514 · Cited by 867 · see citing works
Mesenchymal Stem Cells as Therapeutics
Parekkadan, B., & Milwid, J. M. (2010) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-070909-105309 · Cited by 758 · see citing works
Human body epigenome maps reveal noncanonical DNA methylation variation
Schultz, M. D., He, Y., Whitaker, J. W., Hariharan, M., Mukamel, E. A., Leung, D., Rajagopal, N., Nery, J. R., Urich, M. A., Chen, H., et al. (2015) · Nature · doi:10.1038/nature14465 · Cited by 690 · see citing works
Haynesworth, S. E., Barer, M., & Caplan, A. I. (1992) · Bone · doi:10.1016/8756-3282(92)90363-2 · Cited by 645 · see citing works
Wagner, J. R., Busche, S., Ge, B., Kwan, T., Pastinen, T., & Blanchette, M. (2014) · Genome biology · doi:10.1186/gb-2014-15-2-r37 · Cited by 446 · see citing works
Hsiao, S. T.-F., Asgari, A., Lokmic, Z., Sinclair, R., Dusting, G. J., Lim, S. Y., & Dilley, R. J. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0674 · Cited by 410 · cited 1× · see citing works
“In addition, significant differences in the cytokine secretome and chemokine receptor expression between ATSCs and BMSCs have also been reported [14, 15].”
Huang, J. I., Kazmi, N., Durbhakula, M. M., Hering, T. M., Yoo, J. U., & Johnstone, B. (2005) · Journal of Orthopaedic Research® · doi:10.1016/j.orthres.2005.03.008.1100230621 · Cited by 225 · see citing works
Mesenchymal stem cells homing to improve bone healing
Lin, W., Xu, L., Zwingenberger, S., Gibon, E., Goodman, S. B., & Li, G. (2017) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2017.03.002 · Cited by 220 · see citing works
Self-citationHicks, A. U., Lappalainen, R. S., Narkilahti, S., Suuronen, R., Corbett, D., Sivenius, J., Hovatta, O., & Jolkkonen, J. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06599.x · Cited by 218 · see citing works
Zinn, R. L., Pruitt, K., Eguchi, S., Baylin, S. B., & Herman, J. G. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3396 · Cited by 210 · see citing works
Stem cell transplantation in multiple sclerosis: current status and future prospects
the Stem Cells in Multiple Sclerosis (STEMS) Consensus Group, Martino, G., Franklin, R. J. M., Evercooren, A. B., & Kerr, D. A. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.35 · Cited by 181 · see citing works
Poloni, A., Maurizi, G., Leoni, P., Serrani, F., Mancini, S., Frontini, A., Zingaretti, M. C., Siquini, W., Sarzani, R., & Cinti, S. (2012) · Stem Cells · doi:10.1002/stem.1067 · Cited by 138 · see citing works
Stem cell therapy for cardiac repair: benefits and barriers
Joggerst, S. J., & Hatzopoulos, A. K. (2009) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399409001124 · Cited by 135 · see citing works
Elman, J. S., Li, M., Wang, F., Gimble, J. M., & Parekkadan, B. (2014) · Journal of Inflammation · doi:10.1186/1476-9255-11-1 · Cited by 126 · see citing works
Kia, N. A., Bahrami, A. R., Ebrahimi, M., Matin, M. M., Neshati, Z., Almohaddesin, M. R., Aghdami, N., & Bidkhori, H. R. (2010) · Journal of Molecular Neuroscience · doi:10.1007/s12031-010-9446-6 · Cited by 101 · see citing works
Rasmussen, J. G., Fröbert, O., Holst‐Hansen, C., Kastrup, J., Baandrup, U. T., Zachar, V., Fink, T., & Simonsen, U. (2013) · Cell Transplantation · doi:10.3727/096368912x659871 · Cited by 96 · see citing works
Epigenetic programming of mesenchymal stem cells from human adipose tissue
Boquest, A. C., Noer, A., & Collas, P. (2006) · Stem Cell Reviews and Reports · doi:10.1007/bf02698059 · Cited by 90 · see citing works
Huang, S., Xu, L., Zhang, Y., Sun, Y., & Li, G. (2015) · Cell Transplantation · doi:10.3727/096368915x687219 · Cited by 84 · see citing works
Self-citationAnalysis of Allogeneic and Syngeneic Bone Marrow Stromal Cell Graft Survival in the Spinal Cord
Swanger, S. A., Neuhuber, B., Himes, B. T., Bakshi, A., & Fischer, I. (2005) · Cell Transplantation · doi:10.3727/000000005783982594 · Cited by 71 · see citing works
Lineage-Specific Promoter DNA Methylation Patterns Segregate Adult Progenitor Cell Types
Sørensen, A. L., Barrand, S., West, F. D., Vekterud, K., Boquest, A. C., Ährlund‐Richter, L., Stice, S. L., & Collas, P. (2009) · Stem Cells and Development · doi:10.1089/scd.2009.0309 · Cited by 62 · see citing works
Cho, Y. D., Yoon, W. J., Kim, W. J., Woo, K. M., Baek, J. H., Lee, G., Ku, Y., van Wijnen, A. J., & Ryoo, H. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.558064 · Cited by 62 · see citing works
Rui, Y., Lui, P. P. Y., Lee, W., & Chan, K. M. (2011) · International Orthopaedics · doi:10.1007/s00264-011-1417-1 · Cited by 56 · see citing works
Chung, C., Fujita, N., Kawahara, N., Yui, S., Nam, E., & Nishimura, R. (2013) · Journal of Veterinary Medical Science · doi:10.1292/jvms.12-0470 · Cited by 56 · see citing works
Danišovič, Ľ., Varga, I., Polák, Š., Ulicna, M., Böhmer, D., & Vojtaššák, J. (2009) · General Physiology and Biophysics · doi:10.4149/gpb_2009_01_56 · Cited by 55 · see citing works
DNA methylation of the Trip10 promoter accelerates mesenchymal stem cell lineage determination
Hsiao, S., Lee, K., Hsu, C., Tseng, M.-J., Jin, V. X., Sun, W.-S., Hung, Y.-C., Yeh, K.-T., Yan, P. S., Lai, Y.-Y., et al. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.08.048 · Cited by 46 · see citing works
Rui, Y., Xu, L., Chen, R., Zhang, T., Lin, S., Hou, Y., Liu, Y., Meng, F., Liu, Z., Ni, M., et al. (2015) · Scientific Reports · doi:10.1038/srep11056 · Cited by 45 · see citing works
Self-citationHoogduijn, M. J., & Dor, F. J. M. F. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00144 · Cited by 25 · see citing works
Epigenetic Reprogramming of Mesenchymal Stem Cells
Leu, Y., Huang, T. H. ‐., & Hsiao, S. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-9967-2_10 · Cited by 21 · see citing works
Cooper, G. M., Durham, E. L., Cray, J., Bykowski, M. R., DeCesare, G. E., Smalley, M. A., Mooney, M. P., Campbell, P. G., & Losee, J. E. (2010) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0b013e3181fad311 · Cited by 13 · see citing works
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Stem cell-based therapy for human diseases
Hoang, D. M., Pham, P. T., Bach, T. Q., Ngo, A. T. L., Nguyen, Q. T., Phan, T. T. K., Nguyen, G. H., Le, P. T. T., Hoang, V. T., Forsyth, N. R., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01134-4 · Cited by 1,074 · see citing works
Adipose-derived and bone marrow mesenchymal stem cells: A donor-matched comparison
Mohamed-Ahmed, S., Fristad, I., Lie, S. A., Suliman, S., Mustafa, K., Vindenes, H., & Idris, S. B. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0914-1 · Cited by 515 · see citing works
Challenges in Clinical Development of Mesenchymal Stromal/Stem Cells: Concise Review
Mastrolia, I., Foppiani, E. M., Murgia, A., Candini, O., Samarelli, A. V., Grisendi, G., Veronesi, E., Horwitz, E. M., & Dominici, M. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0044 · Cited by 353 · see citing works
Lee, Y., Chan, Y.-H., Hsieh, S., Lew, W.-Z., & Feng, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205015 · Cited by 246 · see citing works
Allogeneic vs. autologous mesenchymal stem/stromal cells in their medication practice
Li, C., Zhao, H., Cheng, L., & Wang, B. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00698-y · Cited by 188 · see citing works
Self-citationLin, Y.-H., Chen, Y.-H., Chang, H.-Y., Au, H., Tzeng, C., & Huang, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082385 · Cited by 187 · see citing works
Wright, A., Arthaud-Day, M. L., & Weiss, M. L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.632717 · Cited by 150 · see citing works
Fernández‐Santos, M. E., García‐Arranz, M., Andreu, E. J., García-Hernández, A. M., López-Parra, M., Villarón, E. M., Sepúlveda, P., Fernández‐Avilés, F., García‐Olmo, D., Prósper, F., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.918565 · Cited by 144 · see citing works
Recent Development in Therapeutic Cardiac Patches
Mei, X., & Cheng, K. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.610364 · Cited by 125 · see citing works
Transplantation of human umbilical cord mesenchymal stem cells to treat premature ovarian failure
Shareghi-Oskoue, O., Maleki, L. A., & Yousefi, M. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02529-w · Cited by 124 · see citing works
Signaling network regulating osteogenesis in mesenchymal stem cells
Thomas, S., & Jaganathan, B. G. (2021) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-021-00635-1 · Cited by 127 · see citing works
Hussey, G. S., Molina, C. P., Cramer, M. C., Tyurina, Y. Y., Tyurin, V. A., Lee, Y. C., El-Mossier, S. O., Murdock, M. H., Timashev, P. S., Kagan, V. E., et al. (2020) · Science Advances · doi:10.1126/sciadv.aay4361 · Cited by 109 · see citing works
Advanced injectable hydrogels for cartilage tissue engineering
Zhu, S., Li, Y., He, Z., Ji, L., Zhang, W., Yu, T., Luo, J., Yu, D., Zhang, Q., & Bi, Q. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.954501 · Cited by 96 · see citing works
Cheng, S., Nethi, S. K., Rathi, S., Layek, B., & Prabha, S. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.259796 · Cited by 85 · see citing works
Li, R., Lin, S., Zhu, M., Deng, Y., Chen, X., Wei, K., Xu, J., Li, G., & Bian, L. (2019) · Science Advances · doi:10.1126/sciadv.aaw3896 · Cited by 82 · see citing works
Self-citationMollentze, J., Durandt, C., & Pepper, M. S. (2021) · Stem Cells International · doi:10.1155/2021/9919361 · Cited by 77 · see citing works
Mechanistic advances in osteoporosis and anti‐osteoporosis therapies
Wang, H., Luo, Y., Wang, H., Li, F., Yu, F., & Ye, L. (2023) · MedComm · doi:10.1002/mco2.244 · Cited by 76 · see citing works
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Halim, A., Ariyanti, A. D., Luo, Q., & Song, G. (2020) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-09979-4 · Cited by 70 · see citing works
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Gou, Y., Huang, Y., Luo, W., Li, Y., Zhao, P., Zhong, J., Dong, X., Guo, M., Li, A., Hao, A., et al. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.12.003 · Cited by 80 · see citing works
Mesenchymal Stem/Progenitor Cells: The Prospect of Human Clinical Translation
Rady, D., Abbass, M. M. S., El‐Rashidy, A. A., Moshy, S. E., Radwan, I. A., Dörfer, C. E., & El‐Sayed, K. M. F. (2020) · Stem Cells International · doi:10.1155/2020/8837654 · Cited by 68 · see citing works
Mohamed‐Ahmed, S., Yassin, M. A., Rashad, A., Espedal, H., Idris, S. B., Finne‐Wistrand, A., Mustafa, K. B. E., Vindenes, H. A., & Fristad, I. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03315-5 · Cited by 66 · see citing works
Bouland, C., Philippart, P., Dequanter, D., Corrillon, F., Loeb, I., Bron, D., Lagneaux, L., & Meuleman, N. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.674084 · Cited by 65 · see citing works
Wruck, W., Graffmann, N., Spitzhorn, L., & Adjaye, J. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.717772 · Cited by 62 · see citing works
Liu, Y., Kuang, B., Rothrauff, B. B., Tuan, R. S., & Lin, H. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119336 · Cited by 62 · see citing works
Self-citationFabre, H., Ducret, M., Degoul, O., Rodríguez, J., Perrier‐Groult, E., Aubert‐Foucher, E., Pasdeloup, M., Auxenfans, C., McGUCKIN, C. P., Forraz, N., et al. (2019) · Stem Cells International · doi:10.1155/2019/2186728 · Cited by 60 · see citing works
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Wang, P., Cao, Y., Zhan, D., Wang, D., Wang, B., Liu, Y., Li, G., He, W., Wang, H., & Xu, L. (2018) · International Journal of Medical Sciences · doi:10.7150/ijms.27333 · Cited by 55 · see citing works
Self-citationDupuis, V., & Oltra, E. (2021) · World Journal of Stem Cells · doi:10.4252/wjsc.v13.i8.1094 · Cited by 54 · see citing works
Olmedo-Moreno, L., Aguilera, Y., Baliña-Sánchez, C., Martín‐Montalvo, A., & Capilla‐González, V. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14051112 · Cited by 54 · see citing works
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Santos, A. D., Balayan, A., Funderburgh, M. L., Ngo, J., Funderburgh, J. L., & Deng, S. X. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.19-27008 · Cited by 52 · see citing works
Mikłosz, A., Nikitiuk, B. E., & Chabowski, A. (2022) · Obesity Reviews · doi:10.1111/obr.13413 · Cited by 48 · see citing works
Pill, K., Melke, J., Mühleder, S., Pultar, M., Rohringer, S., Priglinger, E., Redl, H. R., Hofmann, S., & Holnthoner, W. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00156 · Cited by 50 · see citing works
Ra, K., Park, S. C., & Lee, B. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24055053 · Cited by 49 · see citing works
Li, N., Wang, J., Feng, G., Liu, Y., Shi, Y., Wang, Y., & Chen, L. (2024) · Regenerative Biomaterials · doi:10.1093/rb/rbae078 · Cited by 48 · see citing works
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Engineered Magnetic Nanocomposites to Modulate Cellular Function
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Hwang, J. W., Lee, N. K., Yang, J. H., Son, H. J., Bang, S. I., Chang, J. W., & Na, D. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093052 · Cited by 43 · see citing works
Calcat-i-Cervera, S., Sanz‐Nogués, C., & O’Brien, T. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.728496 · Cited by 42 · see citing works
Liu, S., Fang, X., Wen, X., Liu, J.-S., Alip, M., Sun, T., Wang, Y. Y., & Chen, H. (2024) · World Journal of Stem Cells · doi:10.4252/wjsc.v16.i3.245 · Cited by 41 · see citing works
Zhu, Y. M., Wei, S., Yan, K., Gu, Y., Lai, H., & Qiao, S. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.646690 · Cited by 40 · see citing works
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Gao, X., Ruzbarsky, J. J., Layne, J. E., Xiao, X. S., & Huard, J. (2024) · Life · doi:10.3390/life14030287 · Cited by 35 · see citing works
Mesenchymal Stromal Cells as Potential Antimicrobial for Veterinary Use—A Comprehensive Review
Russell, K. A., Garbin, L. C., Wong, J. M., & Koch, T. G. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.606404 · Cited by 36 · see citing works
Chatree, K., Sriboonaied, P., Phetkong, C., Wattananit, W., Chanchao, C., & Charoenpanich, A. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e15556 · Cited by 34 · see citing works
Ayaz‐Güner, Ş., Alessio, N., Acar, M. B., Aprile, D., Özcan, S., Bernardo, G. D., Peluso, G., & Galderisi, U. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00614-w · Cited by 33 · see citing works
Meng, H. Y. H., Lu, V., & Khan, W. S. (2021) · Pharmaceuticals · doi:10.3390/ph14121280 · Cited by 33 · see citing works
Blum, C., Schlegelmilch, K., Schilling, T., Shridhar, A., Rudert, M., Jakob, F. J., Dalton, P. D., Blunk, T., Flynn, L. E., & Gröll, J. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b00894 · Cited by 31 · see citing works
Winkel, A., Jaimes, Y., Melzer, C., Dillschneider, P., Hartwig, H., Stiesch, M., von der Ohe, J., Strauß, S., Vogt, P. M., Hamm, A., et al. (2020) · Cytotherapy · doi:10.1016/j.jcyt.2020.07.005 · Cited by 30 · see citing works
Choudhary, P., Gupta, A., & Singh, S. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01714-5 · Cited by 30 · see citing works
Wang, C.-Y., Hong, P., Wang, D., Cherng, J., Chang, S., Liu, C., Fang, T.-J., & Wang, Y.-W. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228632 · Cited by 29 · see citing works
Harnessing adipose stem cell diversity in regenerative medicine
Gui, C., Parson, J. C., & Meyer, G. (2021) · APL Bioengineering · doi:10.1063/5.0038101 · Cited by 23 · see citing works
Media matters: culture medium-dependent hypervariable phenotype of mesenchymal stromal cells
Fitzgerald, J. C., Shaw, G., Murphy, J. M., & Barry, F. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03589-w · Cited by 28 · see citing works
Gao, P., Kajiya, M., Motoike, S., Ikeya, M., & Yang, J. (2024) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2024.01.001 · Cited by 30 · see citing works
Harrell, C. R., Djonov, V., Volarevic, A., Arsenijević, A., & Volarević, V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084378 · Cited by 27 · see citing works
Ścieżyńska, A., Soszyńska, M., Szpak, P., Krześniak, N. E., Malejczyk, J., & Kalaszczyńska, I. (2021) · Cells · doi:10.3390/cells10051043 · Cited by 27 · see citing works
Muthu, S., Jeyaraman, M., Jain, R., Gulati, A., Jeyaraman, N., Prajwal, G. S., & Mishra, P. C. (2021) · Stem Cell Investigation · doi:10.21037/sci-2020-055 · Cited by 27 · see citing works
Rebelatto, C. L. K., Leite, L. M. B., Daga, D. R., Marsaro, D. B., Vaz, I. M., Jamur, V. R., de Aguiar, A. M., Vieira, T. B., Furman, B. P., Aguiar, C. O., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612955 · Cited by 28 · see citing works
Stachecka, J., Lemanska, W., Noak, M., & Szczerbal, I. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.11.175 · Cited by 26 · see citing works
Enhanced Proliferative and Osteogenic Potential of Periodontal Ligament Stromal Cells
Alves, L., Machado, V., Botelho, J., Mendes, J. J., Cabral, J. M. S., da Silva, C. L., & Carvalho, M. S. (2023) · Biomedicines · doi:10.3390/biomedicines11051352 · Cited by 26 · see citing works
Body fluid-derived stem cells — an untapped stem cell source in genitourinary regeneration
Huang, R., Li, Q., Ma, J., Atala, A., & Zhang, Y. (2023) · Nature Reviews Urology · doi:10.1038/s41585-023-00787-2 · Cited by 26 · see citing works
Yang, Y., Liu, S., He, C., Chen, Z., Lyu, T., Zeng, L., Wang, L., Zhang, F., Chen, H., & Zhao, R. C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.711005 · Cited by 25 · see citing works
Le, Q., Madhu, V., Hart, J., Farber, C. R., Zunder, E. R., Dighe, A. S., & Cui, Q. (2021) · World Journal of Stem Cells · doi:10.4252/wjsc.v13.i9.1248 · Cited by 25 · see citing works
Lopez‐Yus, M., García-Sobreviela, M. P., del Moral, R., & Arbonés-Mainar, J. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087468 · Cited by 25 · see citing works
Kanawa, M., Igarashi, A., Fujimoto, K., Higashi, Y., Kurihara, H., Sugiyama, M., Saskianti, T., Kato, Y., & Kawamoto, T. (2018) · Stem Cells International · doi:10.1155/2018/9530932 · Cited by 25 · see citing works
Sakai, Y., Fukunishi, S., Takamura, M., Kawaguchi, K., Inoue, O., Usui, S., Takashima, S., Seki, A., Asai, A., Tsuchimoto, Y., et al. (2021) · Regenerative Therapy · doi:10.1016/j.reth.2021.04.003 · Cited by 25 · see citing works
The Role and Involvement of Stem Cells in Periodontology
Goriuc, A., Foia, L. G., Cojocaru, K.-A., Diaconu-Popa, D. A., Sandu, D., & Luchian, I. A. (2023) · Biomedicines · doi:10.3390/biomedicines11020387 · Cited by 24 · see citing works
Henze, K., Herten, M., Haversath, M., Busch, A., Brandau, S., Hackel, A. M., Flohé, S. B., & Jäger, M. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1461-0 · Cited by 24 · see citing works
Lyu, J., Hashimoto, Y., Honda, Y., & Matsumoto, N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179478 · Cited by 23 · see citing works
Кукољ, Т., Lazarević, J. J., Borojević, A., Ralević, U., Vujić, D., Jauković, A., Lazarević, N., & Bugarski, D. S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094915 · Cited by 23 · see citing works
Arakawa, M., Sakamoto, Y., Miyagawa, Y., Nito, C., Takahashi, S., Nitahara‐Kasahara, Y., Suda, S., Yamazaki, Y., Sakai, M., Kimura, K., et al. (2023) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2023.07.005 · Cited by 25 · see citing works
Gao, M., Sun, L., Xu, K., Zhang, L., Zhang, Y. L., He, T., Sun, R., Huang, H., Zhu, J., Zhang, Y., et al. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.111031 · Cited by 23 · see citing works
Melatonin and the Programming of Stem Cells
Hardeland, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23041971 · Cited by 22 · see citing works
Impact of Environmental and Epigenetic Changes on Mesenchymal Stem Cells during Aging
Smith, N., Shirazi, S., Cakouros, D., & Gronthos, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076499 · Cited by 23 · see citing works
Dong, K., Zhou, W., & Liu, Z.-H. (2022) · Journal of Periodontal & Implant Science · doi:10.5051/jpis.2106240312 · Cited by 21 · see citing works
Predicting multipotency of human adult stem cells derived from various donors through deep learning
Kim, H., Park, K., Yon, J.-M., Kim, S. W., Lee, S. Y., Jeong, I., Jang, J., Lee, S., & Cho, D. (2022) · Scientific Reports · doi:10.1038/s41598-022-25423-8 · Cited by 21 · see citing works
Epigenetics: Novel crucial approach for osteogenesis of mesenchymal stem cells
Wang, Z., Si, W., Zhong, M., Yang, Z., Xiong, W., Zhang, K., Yang, S., Li, H., & Guo, S. (2023) · Journal of Tissue Engineering · doi:10.1177/20417314231175364 · Cited by 21 · see citing works
Cao, Y., Wang, B., Wang, D., Zhan, D., Mai, C., Wang, P., Wei, Q., Liu, Y., Wang, H., He, W., et al. (2019) · International Journal of Genomics · doi:10.1155/2019/7076513 · Cited by 21 · see citing works
Self-citationČamernik, K., Mihelič, A., Mihalič, R., Marolt, D., Janež, A., Trebše, R., Marc, J., & Zupan, J. (2020) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-09964-x · Cited by 21 · see citing works
Tomecka, E., Lech, W., Zychowicz, M., Sarnowska, A., Murzyn, M., Ołdak, T., Domańska‐Janik, K., Bużańska, L., & Rozwadowska, N. (2021) · Cells · doi:10.3390/cells10040717 · Cited by 21 · see citing works
Lin, W., Chen, S., Wang, Y., Wang, M., Lee, W., Jiang, X., & Li, G. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03912-4 · Cited by 22 · see citing works
Self-citationGuo, X., Tang, Y., Zhang, P., Li, S., Chen, Y., Qian, B., Shen, H., & Zhao, N. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1263-4 · Cited by 20 · see citing works
Koaykul, C., Kim, M., Kawahara, Y., Yuge, L., & Kino‐oka, M. (2019) · Stem Cells and Development · doi:10.1089/scd.2019.0146 · Cited by 20 · see citing works
Gaus, S., Li, H., Li, S., Wang, Q., Kottek, T., Hahnel, S., Liu, X., Deng, Y., Ziebolz, D., Haak, R., et al. (2021) · BioMed Research International · doi:10.1155/2021/6697810 · Cited by 20 · see citing works
RetractedJauregui, C. E., Yoganarasimha, S., & Madurantakam, P. A. (2018) · Bioengineering · doi:10.3390/bioengineering5010008 · Cited by 20 · see citing works
Yang, Y., Yang, M., Shi, D., Chen, K., Zhao, J., He, S., Bai, Y., Shen, P., & Ni, H. (2021) · JOR Spine · doi:10.1002/jsp2.1184 · Cited by 19 · see citing works
Baron, 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
Palamà, M. E. F., Görgün, C., Rovere, M., Shaw, G., Reverberi, D., Formica, M., Quarto, E., Barry, F., Murphy, M. J., & Gentili, C. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1536843 · Cited by 18 · see citing works
Liu, T. M., Tew, W., Yang, Z., Lim, B., Hui, J. H. P., Lee, E. H., Loh, Y., & Cool, S. M. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-08094-x · Cited by 18 · see citing works
Monakova, A., Sagaradze, G. D., Basalova, N. A., Popov, V. S., Balabanyan, V. Y., & Efimenko, A. Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169414 · Cited by 18 · see citing works
Stem Cell-Based Therapy and Cell-Free Therapy as an Alternative Approach for Cardiac Regeneration
Deszcz, I. (2023) · Stem Cells International · doi:10.1155/2023/2729377 · Cited by 18 · see citing works
Kim, H. J., Kim, K., Kwon, Y.-R., Kim, B., & Kim, Y. (2018) · Biotechnology Letters · doi:10.1007/s10529-018-2561-0 · Cited by 18 · see citing works
- Authors
- Xu, L., Liu, Y., Sun, Y., Wang, B., Xiong, Y., Lin, W., Wei, Q., Wang, H., He, W., Wang, B., & Li, G.
- Affiliations
- Guangzhou University of Chinese Medicine (CN)
- Chinese University of Hong Kong (HK)
- Corresponding author
- He, Wei
- Li, Gang
- Venue
- Stem Cell Research & Therapy
- Published
- 2017-12
- Volume
- 8
- Issue
- 1
- Pages
- 275-275
- ISSN
- 1757-6512 (ISSN-L)
- PMC
- PMC5718061
- OpenAlex
- W2773440515
- Cited by
- 284
- References
- 36
- Citations by year
- 2026: 10 · 2025: 26 · 2024: 29 · 2023: 50 · 2022: 39 · 2021: 52 · 2020: 34 · 2019: 30 · 2018: 14
- FWCI
- 12.25
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Stem Cell Research & Therapy (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- City University of Hong Kong
- Lui Che Woo Institute of Innovative Medicine
- National Natural Science Foundation of China (14119115, 81772322, 81430049, 81371946)
- Chinese University of Hong Kong
- Hong Kong Government
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
- Keywords
- mesenchymal stem cells, bone marrow-derived stem cells, adipose-derived stem cells, trilineage differentiation, osteogenic differentiation, adipogenesis, chondrogenic differentiation, DNA methylation, Runx2, PPARγ, SOX9, epigenetic memory, bone regeneration, cell therapy
- MeSH terms
- Adipose Tissue, Bone Marrow Cells, Bone Regeneration, Cell Differentiation, Humans, Organ Specificity, Osteogenesis, Promoter Regions, Genetic, Skull, Biomarkers, Gene Expression, CpG Islands, DNA Methylation, Arthroplasty, Replacement, Hip, Chondrogenesis, Mesenchymal Stem Cell Transplantation, PPAR gamma, Adipogenesis, Core Binding Factor Alpha 1 Subunit, SOX9 Transcription Factor, Mesenchymal Stem Cells, Primary Cell Culture
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