Actin Cytoskeletal Disruption following Cryopreservation Alters the Biodistribution of Human Mesenchymal Stromal Cells In Vivo
Open accessAbstract
Mesenchymal stromal cells have shown clinical promise; however, variations in treatment responses are an ongoing concern. We previously demonstrated that MSCs are functionally stunned after thawing. Here, we investigated whether this cryopreservation/thawing defect also impacts the postinfusion biodistribution properties of MSCs. Under both static and physiologic flow, compared with live MSCs in active culture, MSCs thawed from cryopreservation bound poorly to fibronectin (40% reduction) and human endothelial cells (80% reduction), respectively. This reduction correlated with a reduced cytoskeletal F-actin content in post-thaw MSCs (60% reduction). In vivo, live human MSCs could be detected in murine lung tissues for up to 24 hr, whereas thawed MSCs were undetectable. Similarly, live MSCs whose actin cytoskeleton was chemically disrupted were undetectable at 24 hr postinfusion. Our data suggest that post-thaw cryopreserved MSCs are distinct from live MSCs. This distinction could significantly affect the utility of MSCs as a cellular therapeutic.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cryopreservation and subsequent thawing may stunt MSC potency, immunosuppressive properties, post-infusion biodistribution, engraftment, and clearance kinetics.
“The cryopreservation and subsequent thawing are other challenges in developing high-quality MSCs for clinical use, for they may stunt MSC potency, immunosuppressive properties, post-infusion biodistribution, engraftment, and clearance kinetics [336, 337].”
From Mechanisms, efficacy, and future perspectives of cellular-based therapies for liver fibrosis/cirrhosis: focusing on mesenchymal stromal cells (2025) · cites this paper as [336]
The Discussion reports reduced post-thaw immunosuppressive capacity, potential therapeutic potency, and binding and engraftment; the Results show reduced lung engraftment of thawed MSCs at 24 hours. The paper also examines post-infusion biodistribution, but it does not establish how cryopreservation changes clearance kinetics relative to live MSCs. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
Devine, S. M., Cobbs, C., Jennings, M., Bartholomew, A. M., & Hoffman, R. (2003) · Blood · doi:10.1182/blood-2002-06-1830 · Cited by 740 · see citing works
von Bahr, L., Batsis, I., Moll, G., Hägg, M., Szakos, A., Sundberg, B., Uzunel, M., Ringdén, O. T. H., & Blanc, K. L. (2012) · Stem Cells · doi:10.1002/stem.1118 · Cited by 578 · see citing works
Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells
Rüster, B., Göttig, S., Ludwig, R. J., Bistrian, R., Müller, S., Seifried, E., Gille, J., & Henschler, R. (2006) · Blood · doi:10.1182/blood-2006-05-025098 · Cited by 562 · see citing works
Eliopoulos, N., Stagg, J., Lejeune, L., Pommey, S., & Galipeau, J. (2005) · Blood · doi:10.1182/blood-2005-03-1004 · Cited by 560 · see citing works
Self-citationForces and Bond Dynamics in Cell Adhesion
Evans, E. A., & Calderwood, D. (2007) · Science · doi:10.1126/science.1137592 · Cited by 534 · see citing works
Gurtovenko, A. A., & Anwar, J. (2007) · The Journal of Physical Chemistry B · doi:10.1021/jp073113e · Cited by 491 · see citing works
Ugarte, D. A. D., Alfonso, Z., Zuk, P. A., Elbarbary, A. S., Zhu, M., Ashjian, P. H., Benhaim, P., Hedrick, M. H., & Fraser, J. K. (2003) · Immunology Letters · doi:10.1016/s0165-2478(03)00108-1 · Cited by 458 · see citing works
Galipeau, J. (2013) · Cytotherapy · doi:10.1016/j.jcyt.2012.10.002 · Cited by 448 · see citing works
Self-citationMolecular Basis for Dimethylsulfoxide (DMSO) Action on Lipid Membranes
Notman, R., Noro, M., O'Malley, B., & Anwar, J. (2006) · Journal of the American Chemical Society · doi:10.1021/ja063363t · Cited by 447 · see citing works
Beere, H. M. (2005) · Journal of Clinical Investigation · doi:10.1172/jci26471 · Cited by 415 · see citing works
François, M., Copland, I. B., Yuan, S., Romieu-Mourez, R., Waller, E. K., & Galipeau, J. (2012) · Cytotherapy · doi:10.3109/14653249.2011.623691 · Cited by 375 · see citing works
Self-citationGe, W., Jiang, J., Arp, J., Liu, W., Garcia, B. M., & Wang, H. (2010) · Transplantation · doi:10.1097/tp.0b013e3181fed001 · Cited by 350 · see citing works
Are Therapeutic Human Mesenchymal Stromal Cells Compatible with Human Blood?
Moll, G., Rasmusson‐Duprez, I., von Bahr, L., Connolly-Andersen, A.-M., Elgue, G., Funke, L., Hamad, O., Lönnies, H., Magnusson, P., Sánchez, J., et al. (2012) · Stem Cells · doi:10.1002/stem.1111 · Cited by 338 · see citing works
Antiapoptotic and Anti-inflammatory Mechanisms of Heat-Shock Protein Protection
Yenari, M. A., Liu, J., Zheng, Z., Vexler, Z. S., Lee, J. E., & Giffard, R. G. (2005) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2005.tb00012.x · Cited by 299 · see citing works
Tsai, M., Kita, A., Leach, J., Rounsevell, R., Huang, J. N., Moake, J., Ware, R. E., Fletcher, D. A., & Lam, W. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58753 · Cited by 297 · see citing works
Self-citationvan den Eijnde, S. M., van den Hoff, M. J. B., Reutelingsperger, C. P. M., van Heerde, W. L., Henfling, M. E. R., Vermeij‐Keers, C., Schütte, B., Borgers, M. J., & Ramaekers, F. C. S. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.20.3631 · Cited by 289 · see citing works
Huang, J., Zhang, Z., Guo, J., Ni, A., Deb, A., Zhang, L., Mirotsou, M., Pratt, R. E., & Dzau, V. J. (2010) · Circulation Research · doi:10.1161/circresaha.109.196030 · Cited by 240 · see citing works
Poncelet, A. J., Vercruysse, J., Saliez, A., & Gianello, P. (2007) · Transplantation · doi:10.1097/01.tp.0000258649.23081.a3 · Cited by 239 · see citing works
Cytoskeletal Changes of Mesenchymal Stem Cells During Differentiation
Yourek, G., Hussain, M. A., & Mao, J. J. (2007) · ASAIO Journal · doi:10.1097/mat.0b013e31802deb2d · Cited by 231 · see citing works
Sarkar, D., Spencer, J. A., Phillips, J. A., Zhao, W., Schäfer, S., Spelke, D. P., Mortensen, L. J., Ruíz, J. P., Vemula, P. K., Sridharan, R., et al. (2011) · Blood · doi:10.1182/blood-2010-10-311464 · Cited by 227 · see citing works
Cuesta, R., Laroia, G., & Schneider, R. J. (2000) · Genes & Development · doi:10.1101/gad.14.12.1460 · Cited by 197 · see citing works
The lymphocyte homing receptors: gatekeepers of the multistep paradigm
Sackstein, R. (2005) · Current Opinion in Hematology · doi:10.1097/01.moh.0000177827.78280.79 · Cited by 150 · see citing works
Castelo-Branco, M. T. L., Soares, I. D. P., Lopes, D. V., Buongusto, F., Martinusso, C. A., do Rosário, A., de Souza, S. A. L., Gutfilen, B., da Fonseca, L. M. B., Elia, C. C. S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033360 · Cited by 136 · see citing works
Human Mesenchymal Stem Cells Are Susceptible to Lysis by CD8 + T Cells and NK Cells
Crop, M. J., Korevaar, S. S., de Kuiper, R., IJzermans, J. N. M., van Besouw, N. M., Baan, C. C., Weimar, W., & Hoogduijn, M. J. (2011) · Cell Transplantation · doi:10.3727/096368910x564076 · Cited by 110 · see citing works
Kenis, H., Zandbergen, H. R., Hofstra, L., Petrov, A. D., Dumont, E. A. W. J., Blankenberg, F. G., Haider, N., Bitsch, N. J. J. E., Gijbels, M. J., Verjans, J. W. H., et al. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.068429 · Cited by 90 · see citing works
The Instant Blood-Mediated Inflammatory Reaction Characterized in Hepatocyte Transplantation
Gustafson, E., Elgue, G., Hughes, R. D., Mitry, R., Sánchez, J., Haglund, U., Meurling, S., Dhawan, A., Korsgren, O., & Nilsson, B. (2011) · Transplantation · doi:10.1097/tp.0b013e31820ae459 · Cited by 88 · see citing works
The effect of platelet lysate fibrinogen on the functionality of MSCs in immunotherapy
Copland, I. B., Garcia, M. A., Waller, E. K., Roback, J. D., & Galipeau, J. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.06.050 · Cited by 84 · see citing works
Self-citationRieger, A. M., Hall, B. E., Luong, L., Schang, L. M., & Barreda, D. R. (2010) · Journal of Immunological Methods · doi:10.1016/j.jim.2010.03.019 · Cited by 81 · see citing works
Response of the cell membrane–cytoskeleton complex to osmotic and freeze/thaw stresses
Ragoonanan, V., Hubel, A., & Aksan, A. (2010) · Cryobiology · doi:10.1016/j.cryobiol.2010.10.160 · Cited by 79 · see citing works
Do ABO Blood Group Antigens Hamper the Therapeutic Efficacy of Mesenchymal Stromal Cells?
Moll, G., Hult, A. K., von Bahr, L., Alm, J. J., Heldring, N., Hamad, O. A., Funke, L., Larsson, S., Teramura, Y., Roelofs, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085040 · Cited by 77 · see citing works
Ion transport through dimethyl sulfoxide (DMSO) induced transient water pores in cell membranes
He, F., Liu, W., Zheng, S.-C., Zhou, L., Ye, B., & Qi, Z. (2012) · Molecular Membrane Biology · doi:10.3109/09687688.2012.687460 · Cited by 72 · see citing works
Cryopreservation of alginate encapsulated mesenchymal stromal cells
Pravdyuk, A. I., Petrenko, Y. A., Fuller, B. J., & Petrenko, Y. (2013) · Cryobiology · doi:10.1016/j.cryobiol.2013.02.002 · Cited by 69 · see citing works
Magnetic Cryopreservation for Dental Pulp Stem Cells
Lee, S., Huang, G., Shiung, J.-N., Huang, Y., Jeng, J., Kuo, T., Yang, J., & Yang, W. V. (2012) · Cells Tissues Organs · doi:10.1159/000331247 · Cited by 66 · see citing works
Liu, K., Yang, Y., & Mansbridge, J. N. (2000) · Tissue Engineering · doi:10.1089/107632700750022189 · Cited by 61 · see citing works
Pre-conditioned mesenchymal stem cells: a better way for cell-based therapy
Li, Q., Wang, Y., & Deng, Z. (2013) · Stem Cell Research & Therapy · doi:10.1186/scrt213 · Cited by 56 · see citing works
Effects of osmotic and cold shock on adherent human mesenchymal stem cells during cryopreservation
Xu, X., Liu, Y., Cui, Z., Wei, Y., & Zhang, L. (2012) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2012.09.004 · Cited by 53 · see citing works
Death and inflammation following somatic cell transplantation
Copland, I. B., & Galipeau, J. (2011) · Seminars in Immunopathology · doi:10.1007/s00281-011-0274-8 · Cited by 48 · see citing works
Self-citationde Boer, F., Dräger, A. M., van der Wall, E., Pinedo, H. M., & Schuurhuis, G. J. (1998) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1701495 · Cited by 44 · see citing works
Cryopreservation and Revival of Human Mesenchymal Stromal Cells
Haack‐Sørensen, M., Ekblond, A., & Kastrup, J. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3584-0_21 · Cited by 39 · see citing works
Actin polymerization stabilizes α4β1 integrin anchors that mediate monocyte adhesion
Rullo, J., Becker, H., Hyduk, S. J., Wong, J. C., Digby, G. C., Arora, P. D., Cano, A. P., Hartwig, J. H., McCulloch, C. A., & Cybulsky, M. I. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201107140 · Cited by 39 · see citing works
Hattori, Y., Kato, H., Nitta, M., & Takamoto, S. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(00)00615-9 · Cited by 36 · see citing works
Koenigsmann, M., Koenigsmann, M., Notter, M., Neuloh, M., Mücke, C., Thiel, E., & Berdel, W. (1998) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1701484 · Cited by 34 · see citing works
Richardson, J. D., Nelson, A. J., Zannettino, A. C. W., Gronthos, S., Worthley, S. G., & Psaltis, P. J. (2012) · Stem Cell Reviews and Reports · doi:10.1007/s12015-012-9366-7 · Cited by 34 · see citing works
Cryopreservation and Revival of Mesenchymal Stromal Cells
Haack‐Sørensen, M., & Kastrup, J. (2011) · Methods in molecular biology · doi:10.1007/978-1-60761-999-4_13 · Cited by 33 · see citing works
Tsai, H., Liu, G., Kung, M., Liu, L., Wu, J., Tang, C.-H., Huang, C., Chen, S., Lam, H., Wu, C., et al. (2013) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-12-0832 · Cited by 28 · see citing works
Himi, N., Hamaguchi, A., Hashimoto, K., Koga, T., Narita, K., & Miyamoto, O. (2012) · Advances in Medical Sciences · doi:10.2478/v10039-012-0044-4 · Cited by 23 · see citing works
Effects of cryostorage on human sperm chromatin integrity
Fortunato, A., Leo, R., & Liguori, F. (2012) · Zygote · doi:10.1017/s0967199412000032 · Cited by 23 · see citing works
Doerwald, L., Onnekink, C., van Genesen, S. T., JONG, W. W. D., & Lubsen, N. H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302914200 · Cited by 21 · see citing works
Durkut, S., Elçin, A. E., & Elçin, Y. M. (2013) · Artificial Cells Nanomedicine and Biotechnology · doi:10.3109/21691401.2013.837476 · Cited by 19 · see citing works
Flagged first, then by citations
1 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Shattering barriers toward clinically meaningful MSC therapies
Levy, O., Kuai, R., Siren, E. M. J., Bhere, D., Milton, Y., Nissar, N., De Biasio, M., Heinelt, M., Reeve, B., Abdi, R., et al. (2020) · Science Advances · doi:10.1126/sciadv.aba6884 · Cited by 694 · see citing works
Marquez-Curtis, L. A., Janowska-Wieczorek, A., McGann, L. E., & Elliott, J. A. W. (2015) · Cryobiology · doi:10.1016/j.cryobiol.2015.07.003 · Cited by 346 · see citing works
Reciprocal regulation of mesenchymal stem cells and immune responses
Wang, Y., Fang, J., Liu, B., Shao, C., & Shi, Y. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.10.001 · Cited by 330 · see citing works
The roles of reactive oxygen species and antioxidants in cryopreservation
Len, J. S., Koh, W. S. D., & Tan, S. (2019) · Bioscience Reports · doi:10.1042/bsr20191601 · Cited by 241 · see citing works
Moll, G., Geißler, S., Catar, R. A., Ignatowicz, L., Hoogduijn, M. J., Strunk, D., Bieback, K., & Ringdén, O. T. H. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-45457-3_7 · Cited by 175 · see citing works
Cell-based therapeutic strategies for multiple sclerosis
Scolding, N. J., Pasquini, M. C., Reingold, S. C., Cohen, J. A., Sclerosis:, I. C. O. C.-B. T. F. M., Atkins, H. L., Banwell, B., Bar‐Or, A., Bebo, B. F., Bowen, J. D., et al. (2017) · Brain · doi:10.1093/brain/awx154 · Cited by 170 · see citing works
Self-citationChinnadurai, R., Copland, I. B., Garcia, M. A., Petersen, C. T., Lewis, C. N., Waller, E. K., Kirk, A. D., & Galipeau, J. (2016) · Stem Cells · doi:10.1002/stem.2415 · Cited by 169 · see citing works
Self-citationCottle, C., Porter, A. P., Lipat, A. J., Turner-Lyles, C., Nguyen, J., Moll, G., & Chinnadurai, R. (2022) · Current Stem Cell Reports · doi:10.1007/s40778-022-00212-1 · Cited by 153 · see citing works
Self-citationMoll, G., Ignatowicz, L., Catar, R. A., Luecht, C., Sadeghi, B., Hamad, O. A., Jungebluth, P., Dragun, D., Schmidtchen, A., & Ringdén, O. T. H. (2015) · Stem Cells and Development · doi:10.1089/scd.2015.0120 · Cited by 140 · see citing works
Mesenchymal Stromal Cells Anno 2019: Dawn of the Therapeutic Era? Concise Review
Hoogduijn, M. J., & Lombardo, E. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0073 · Cited by 138 · see citing works
Planat‐Benard, V., Varin, A., & Casteilla, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.626755 · Cited by 139 · see citing works
Cohen, J. A., Imrey, P. B., Planchon, S. M., Bermel, R. A., Fisher, E., Fox, R. J., Bar‐Or, A., Sharp, S. L., Skaramagas, T., Jagodnik, P., et al. (2017) · Multiple Sclerosis Journal · doi:10.1177/1352458517703802 · Cited by 123 · see citing works
Mesenchymal stromal cells in hepatic fibrosis/cirrhosis: from pathogenesis to treatment
Yang, X., Li, Q., Liu, W., Zong, C., Wei, L., Shi, Y., & Han, Z. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-00983-5 · Cited by 120 · see citing works
The impact of cryopreservation on bone marrow-derived mesenchymal stem cells: a systematic review
Bahsoun, S., Coopman, K., & Akam, E. C. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-02136-7 · Cited by 113 · see citing works
Pharmacokinetic characteristics of mesenchymal stem cells in translational challenges
Shan, Y., Zhang, M., Tao, E., Wang, J., Wei, N., Lü, Y., Liu, Q., Hao, K., Zhou, F., & Wang, G. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01936-8 · Cited by 123 · see citing works
Blanc, K. L., & Davies, L. C. (2018) · Cytotherapy · doi:10.1016/j.jcyt.2018.01.009 · Cited by 110 · see citing works
Dhere, T., Copland, I. B., Garcia, M. A., Chiang, K. Y., Chinnadurai, R., Prasad, M. A., Galipeau, J., & Kugathasan, S. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13717 · Cited by 109 · see citing works
Self-citationToward Development of iMesenchymal Stem Cells for Immunomodulatory Therapy
de Witte, S. F. H., Franquesa, M., Baan, C. C., & Hoogduijn, M. J. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00648 · Cited by 103 · see citing works
Braid, L. R., Wood, C. A., Wiese, D. M., & Ford, B. N. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.09.013 · Cited by 102 · see citing works
Giri, J., & Galipeau, J. (2020) · Blood Advances · doi:10.1182/bloodadvances.2020001711 · Cited by 97 · see citing works
Self-citationYong, K. W., Zaman, W. S. W. K., Xu, F., Abas, W. A. B. W., Choi, J. R., & Pingguan‐Murphy, B. (2015) · Biopreservation and Biobanking · doi:10.1089/bio.2014.0104 · Cited by 89 · see citing works
Cryopreserved mesenchymal stem cells regain functional potency following a 24-h acclimation period
Antebi, B., Asher, A. M., Rodriguez, L. A., Moore, R. K., Mohammadipoor, A., & Cancio, L. C. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-2038-5 · Cited by 83 · see citing works
Jayaraman, P., Lim, R., Ng, J., & Vemuri, M. C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.648472 · Cited by 72 · see citing works
Cell therapy for heart disease after 15 years: Unmet expectations
Nigro, P., Bassetti, B., Cavallotti, L., Catto, V., Carbucicchio, C., & Pompilio, G. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.02.015 · Cited by 69 · see citing works
Gramlich, O. W., Burand, A. J., Brown, A. J., Deutsch, R. J., Kuehn, M. H., & Ankrum, J. A. (2016) · Scientific Reports · doi:10.1038/srep26463 · Cited by 67 · see citing works
Chinnadurai, R., Copland, I. B., Ng, S., Garcia, M. A., Prasad, M., Arafat, D., Gibson, G. C., Kugathasan, S., & Galipeau, J. (2015) · Molecular Therapy · doi:10.1038/mt.2015.67 · Cited by 63 · see citing works
Self-citationPollock, K., Yu, G., Trane, R. M., Koran, M., Dosa, P. I., McKenna, D. H., & Hubel, A. (2016) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2016.0284 · Cited by 62 · see citing works
Chinnadurai, R., Rajan, D., Ng, S., McCullough, K., Arafat, D., Waller, E. K., Anderson, L. J., Gibson, G. C., & Galipeau, J. (2017) · Blood Advances · doi:10.1182/bloodadvances.2017006205 · Cited by 60 · see citing works
Self-citationPollock, K., Samsonraj, R. M., Dudakovic, A., Thaler, R., Stumbras, A. R., McKenna, D. H., Dosa, P. I., van Wijnen, A. J., & Hubel, A. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0347 · Cited by 56 · see citing works
Bahsoun, S., Coopman, K., & Akam, E. C. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-02054-2 · Cited by 55 · see citing works
“[41] referred MSC post-thaw low adherence capacity to disruption of F actin polymerisation rather than shedding of surface adhesion molecules.”
BackgroundCryopreservation of NK and T Cells Without DMSO for Adoptive Cell-Based Immunotherapy
Yao, X., & Matosevic, S. (2021) · BioDrugs · doi:10.1007/s40259-021-00494-7 · Cited by 54 · see citing works
Yao, X., Jovevski, J. J., Todd, M. F., Xu, R. F., Li, Y., Wang, J., & Matosevic, S. (2020) · Advanced Science · doi:10.1002/advs.201902938 · Cited by 54 · see citing works
Lohmann, S., Pool, M. B. F., Rozenberg, K. M., Keller, A. K., Moers, C., Møldrup, U., Møller, B. K., Lignell, S. J. M., Krag, S. R. P., Sierra-Párraga, J. M., et al. (2020) · American Journal of Transplantation · doi:10.1111/ajt.16473 · Cited by 53 · see citing works
Večerić‐Haler, Ž., Cerar, A., & Perše, M. (2017) · Stem Cells International · doi:10.1155/2017/7304643 · Cited by 51 · see citing works
Masterson, C. H., Curley, G. F., & Laffey, J. G. (2019) · Intensive Care Medicine Experimental · doi:10.1186/s40635-019-0235-4 · Cited by 51 · see citing works
Challenges in animal modelling of mesenchymal stromal cell therapy for inflammatory bowel disease
Chinnadurai, R. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i16.4779 · Cited by 50 · see citing works
Self-citationImproving mesenchymal stem/stromal cell potency and survival
Nolta, J. A., Galipeau, J., & Phinney, D. G. (2020) · Cytotherapy · doi:10.1016/j.jcyt.2020.01.004 · Cited by 47 · see citing works
Self-citationPollock, K., Budenske, J. W., McKenna, D. H., Dosa, P. I., & Hubel, A. (2016) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2175 · Cited by 42 · see citing works
Cellular Therapies for Treatment of Radiation Injury: Report from a NIH/NIAID and IRSN Workshop
DiCarlo, A. L., Tamarat, R., Rios, C. I., Benderitter, M., Czarniecki, C. W., Allio, T., Macchiarini, F., Maidment, B. W., & Jourdain, J.-R. (2017) · Radiation Research · doi:10.1667/rr14810.1 · Cited by 41 · see citing works
Effects, methods and limits of the cryopreservation on mesenchymal stem cells
Wang, J., & Li, R. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03954-3 · Cited by 40 · see citing works
Bárcia, R. N., Santos, J. M., Teixeira, M., Filipe, M., Pereira, A. R. S., Ministro, A., Água-Doce, A., Carvalheiro, M., Gaspar, M. M., Miranda, J. P., et al. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2016.11.008 · Cited by 40 · see citing works
Fu, X., Xu, B., Jiang, J., Du, X., Yu, X., Yan, Y., Li, S., Inglis, B. M., Ma, H., Wang, H., et al. (2020) · Clinical Proteomics · doi:10.1186/s12014-020-09279-6 · Cited by 40 · see citing works
Biosafety and Bioefficacy Assessment of Human Mesenchymal Stem Cells: What do we Know so Far?
Yong, K. W., Choi, J. R., Dolbashid, A. S., & Zaman, W. S. W. K. (2018) · Regenerative Medicine · doi:10.2217/rme-2017-0078 · Cited by 38 · see citing works
Effects of Normothermic Machine Perfusion Conditions on Mesenchymal Stromal Cells
Sierra-Párraga, J. M., Rozenberg, K. M., Eijken, M., Leuvenink, H. G. D., Hunter, J. P., Merino, A. M., Moers, C., Møller, B. K., Ploeg, R. J., Baan, C. C., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00765 · Cited by 35 · see citing works
Mizuno, M., Matsuzaki, T., Ozeki, N., Katano, H., Koga, H., Takebe, T., Yoshikawa, H., & Sekiya, I. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02850-y · Cited by 33 · see citing works
Ding, Y., Liu, S., Liu, J., Jin, S., & Wang, J. (2024) · Cryobiology · doi:10.1016/j.cryobiol.2024.104847 · Cited by 33 · see citing works
Yea, J.-H., Kim, I., Sym, G., Park, J.-K., Lee, A.-Y., Cho, B. C., Bae, T. S., Kim, B. J., & Jo, C. H. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01906-1 · Cited by 33 · see citing works
Nguyen, D. C., Lewis, H. C., Joyner, C. J., Warren, V., Xiao, H., Kissick, H. T., Wu, R., Galipeau, J., & Lee, F. E.-H. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1463778 · Cited by 30 · see citing works
Self-citationMoeinabadi‐Bidgoli, K., Mazloomnejad, R., Maal, A. B., Aghdaei, H. A., Arki, M. K., Hossein‐Khannazer, N., & Vosough, M. (2023) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2023.2205017 · Cited by 32 · see citing works
Willer, H., Spohn, G., Morgenroth, K., Thielemann, C., Elvers-Hornung, S., Bugert, P., Delorme, B., Giesen, M., Schmitz‐Rixen, T., Seifried, E., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.976511 · Cited by 31 · see citing works
Chabot, D., Tremblay, T., Paré, I., Bazin, R., & Loubaki, L. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.04.005 · Cited by 28 · see citing works
Lim, J. Y., Park, S., Park, S. A., Jeon, J. H., Jung, H. Y., Yon, J.-M., Jeun, S., Lim, H. K., & Kim, S. W. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02489-1 · Cited by 26 · see citing works
Dave, C., Mei, S. H. J., McRae, A., Hum, C., Sullivan, K., Champagne, J., Ramsay, T., & McIntyre, L. (2022) · eLife · doi:10.7554/elife.75053 · Cited by 26 · see citing works
Burand, A. J., Gramlich, O. W., Brown, A. J., & Ankrum, J. A. (2016) · Stem Cells · doi:10.1002/stem.2528 · Cited by 25 · see citing works
Chen, S., Deng, X., Ma, K., Zhao, L., Huang, D., Li, Z., & Shao, Z. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/3459612 · Cited by 24 · see citing works
Mesenchymal stromal cells and chronic inflammatory bowel disease
Algeri, M., Conforti, A., Pitisci, A., Starc, N., Tomao, L., Bernardo, M. E., & Locatelli, F. (2015) · Immunology Letters · doi:10.1016/j.imlet.2015.06.018 · Cited by 24 · see citing works
Golan, M., Jelínková, Š., Kratochvílová, I., Skládal, P., Pešl, M., Rotrekl, V., & Přibyl, J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00804 · Cited by 24 · see citing works
Badner, A., Reinhardt, E. K., Nguyen, T. V., Midani, N., Marshall, A. T., Lepe, C. A., Echeverria-Rosario, K., Lepe, J. J., Torrecampo, V., Bertan, S. H., et al. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2021.0045 · Cited by 23 · see citing works
Hallmarks of MSCs: Key quality attributes for pharmacology and clinical use
Viswanathan, S., & Galipeau, J. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.05.008 · Cited by 25 · see citing works
Self-citationEe, M. T., & Thébaud, B. (2018) · Current Pediatric Reviews · doi:10.2174/1573396314666180911100503 · Cited by 22 · see citing works
Gao, L., Zhou, Q., Zhang, Y., Sun, S., Lv, L., Ma, P., Yang, J., Liu, M., Zhang, L., Wang, X., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147445 · Cited by 21 · see citing works
Fierro, F. A., Magner, N. L., Beegle, J. R., Dahlenburg, H., White, J. L., Zhou, P., Pepper, K. A., Fury, B., Coleal‐Bergum, D., Bauer, G., et al. (2018) · Transfusion · doi:10.1111/trf.14914 · Cited by 21 · see citing works
Khan, I. U., Yoon, Y., Choi, K. U., Jo, K. R., Kim, N., Lee, E., Kim, W. H., & Kweon, O. (2019) · Stem Cells International · doi:10.1155/2019/8537541 · Cited by 21 · see citing works
Ho, Y. K., Loke, K. M., Woo, J. Y., Lee, Y. L., & Too, H. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03198-z · Cited by 19 · see citing works
First Clinical Experiences Using Preconditioning Approaches to Improve MSC-Based Therapies
Le, B., Cressman, A., Morales, D. L. S., & Fierro, F. A. (2024) · Current Stem Cell Reports · doi:10.1007/s40778-023-00232-5 · Cited by 20 · see citing works
Castro, B., Martinez-Redondo, D., Gartzia, I., Alonso‐Varona, A., Garrido, P., & Palomares, T. (2019) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2797 · Cited by 19 · see citing works
Müllers, Y., Meiser, I., Stracke, F., Riemann, I., Lautenschläger, F., Neubauer, J. C., & Zimmermann, H. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211382 · Cited by 19 · see citing works
Guo, X., Li, S. N., Ji, Q., Lian, R., & Chen, J. (2015) · Human Cell · doi:10.1007/s13577-015-0116-4 · Cited by 19 · see citing works
Establishing a Quality Control System for Stem Cell-Based Medicinal Products in China
Yuan, B. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0498 · Cited by 18 · see citing works
Use of MSCs and MSC-Educated Macrophages to Mitigate Hematopoietic Acute Radiation Syndrome
Chinnadurai, R., Forsberg, M. H., Kink, J. A., Hematti, P., & Capitini, C. M. (2020) · Current Stem Cell Reports · doi:10.1007/s40778-020-00176-0 · Cited by 18 · see citing works
Self-citationZhang, M., Zhao, Y. T., Wang, L., Zheng, Y., Yu, H. M., Dong, X., He, W., Yin, Z., & Wang, Z. (2022) · Cell and Tissue Banking · doi:10.1007/s10561-021-09973-1 · Cited by 18 · see citing works
Chinnadurai, R., Bates, P. D., Kunugi, K. A., Nickel, K. P., DeWerd, L. A., Capitini, C. M., Galipeau, J., & Kimple, R. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.708950 · Cited by 17 · see citing works
Self-citationWang, Z., Hu, Y., Wang, X., Chen, Y., Wu, D., Ji, H., Yu, C., Fang, J., Pan, C., Wang, L., et al. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10556-8 · Cited by 16 · see citing works
Salmenkari, H., Laitinen, A., Forsgård, R. A., Holappa, M., Lindén, J., Pasanen, L., Korhonen, M. O., Korpela, R., & Nystedt, J. M. (2019) · Cytotherapy · doi:10.1016/j.jcyt.2018.11.011 · Cited by 16 · see citing works
Editorial: Next generation MSC therapy manufacturing, potency and mechanism of action analysis
Chinnadurai, R., Viswanathan, S., & Moll, G. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1192636 · Cited by 16 · see citing works
Self-citationSilva-Sousa, T., Usuda, J. N., Al-Arawe, N., Hinterseher, I., Catar, R. A., Luecht, C., Vallecillo-García, P., Riesner, K., Hackel, A. M., Schimke, L. F., et al. (2025) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szaf037 · Cited by 16 · see citing works
Chinnadurai, R., Sands, J. S., Rajan, D., Liu, X., Arafat, D., Das, R., Anania, F. A., Gibson, G. C., Kisseleva, T., & Galipeau, J. (2019) · Stem Cells · doi:10.1002/stem.3028 · Cited by 14 · see citing works
Self-citationNavakauskienė, R., Žukauskaitė, D., Borutinskaite, V. V., Bukreieva, T., Skliutė, G., Valatkaitė, E., Zentelytė, A., Piešinienė, L., & Shablii, V. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1140781 · Cited by 14 · see citing works
Li, C.-H., Zhao, J., Zhang, H., & Wang, B. (2023) · World Journal of Stem Cells · doi:10.4252/wjsc.v15.i4.105 · Cited by 14 · see citing works
Faircloth, T. U., Temple, S., Parr, R. N., Tucker, A. B., Rajan, D., Hematti, P., Kugathasan, S., & Chinnadurai, R. (2024) · Stem Cells · doi:10.1093/stmcls/sxae040 · Cited by 15 · see citing works
Self-citationCryopreservation of Immune Cells: Recent Progress and Challenges Ahead
Qi, K., Jia, D., Zhou, S., Zhang, K., Guan, F., Yao, M., & Sui, X. (2024) · Advanced Biology · doi:10.1002/adbi.202400201 · Cited by 15 · see citing works
Cellular Therapies for Treatment of Radiation Injury after a Mass Casualty Incident
Rios, C. I., Jourdain, J.-R., & DiCarlo, A. L. (2017) · Radiation Research · doi:10.1667/rr14835.1 · Cited by 14 · see citing works
Vawda, R., Badner, A., Hong, J., Mikhail, M., Dragas, R., Xhima, K., Jose, A., & Fehlings, M. G. (2020) · Stem Cells and Development · doi:10.1089/scd.2020.0079 · Cited by 14 · see citing works
Horiuchi, K., Ozeki, N., Endo, K., Mizuno, M., Katano, H., Akiyama, M., Tsuji, K., Koga, H., & Sekiya, I. (2021) · Scientific Reports · doi:10.1038/s41598-021-89239-8 · Cited by 13 · see citing works
Yoon, Y., Jung, T., Shahid, M. A., Khan, I. U., Kim, W. H., & Kweon, O. (2019) · Journal of Veterinary Science · doi:10.4142/jvs.2019.20.e63 · Cited by 13 · see citing works
Chinnadurai, R., Scandolara, R., Alese, O. B., Arafat, D., Ravindranathan, D., Farris, A. B., El‐Rayes, B. F., & Gibson, G. C. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.01632 · Cited by 11 · see citing works
Self-citationChabot, D., Lewin, A., Loubaki, L., & Bazin, R. (2018) · Cytotherapy · doi:10.1016/j.jcyt.2018.05.010 · Cited by 11 · see citing works
Farag, A. A. G., Ngeun, S. K., Kaneda, M., Aboubakr, M., Elhaieg, A., Hendawy, H. A., & Tanaka, R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189908 · Cited by 10 · see citing works
Kim, M., Kim, Y., Lee, S., Kuk, M., Kim, A., Kim, W. H., & Kweon, O. (2015) · Journal of Veterinary Medical Science · doi:10.1292/jvms.15-0361 · Cited by 10 · see citing works
Galipeau, J. (2016) · Stem Cells · doi:10.1002/stem.2526 · Cited by 10 · see citing works
Self-citationAnbazhagan, M., Geem, D., Venkateswaran, S., Pelia, R. S., Kolachala, V. L., Dodd, A., Maddipatla, S. C., Cutler, D. J., Matthews, J. D., Chinnadurai, R., et al. (2023) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szad003 · Cited by 9 · see citing works
Self-citationOh, S.-J., Jo, C.-H., Kim, T.-S., Hong, C., Lee, S., Kang, Y., & Rho, G. (2023) · Life · doi:10.3390/life13061286 · Cited by 9 · see citing works
Allogeneic Versus Autologous Mesenchymal Stromal Cells and Donor-to-Donor Variability
Qayed, M. D., Copland, I. B., & Galipeau, J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802826-1.00004-0 · Cited by 9 · see citing works
Self-citationStorage and Delivery of Stem Cells for Cellular Therapies
Jesson, H., Robinson, N. J., Medcalf, N., & Coopman, K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-444-63265-4.00011-x · Cited by 9 · see citing works
Promoting Limb Salvage through Multi-Disciplinary Care of the Diabetic Patient
Salvo, N. L., Walsh, M. D., & Brewster, L. P. (2017) · Current Treatment Options in Cardiovascular Medicine · doi:10.1007/s11936-017-0547-1 · Cited by 9 · see citing works
Irdani, T., Mazzanti, B., Ballerini, L., Saccardi, R., & Torre, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0220055 · Cited by 9 · see citing works
Lederer, C. W., Koniali, L., Buerki‐Thurnherr, T., Papasavva, P. L., Grutta, S. L., Licari, A., Štaud, F., Bonifazi, D., & Kleanthous, M. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14040793 · Cited by 8 · see citing works
Alcayaga‐Miranda, F., Silva, J. D., Parada, N., da Silva, L. H. A., Cruz, F. F., Utreras‐Mendoza, Y., Hidalgo, Y., Cádiz, M. I., Tapia‐Limonchi, R., Espinoza, F., et al. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1031331 · Cited by 5 · see citing works
Bio-inspired Ice-controlling Materials for Cryopreservation of Cells and Tissues
Zheng, X., Liu, J., Liu, Z., & Wang, J. (2021) · 化学学报 · doi:10.6023/a21020043 · Cited by 5 · see citing works
Human Bone Marrow Mononuclear Cells Do Not Improve Limb Perfusion in the Hindlimb Ischemia Model
van Rhijn-Brouwer, F. C. C.-C., Gremmels, H., den Ouden, K., Teraa, M., Fledderus, J. O., & Verhaar, M. C. (2022) · Stem Cells and Development · doi:10.1089/scd.2021.0261 · Cited by 5 · see citing works
- Authors
- Chinnadurai, R., Garcia, M. A., Sakurai, Y., Lam, W. A., Kirk, A. D., Galipeau, J., & Copland, I. B.
- Affiliations
- Emory University (US)
- Emory Healthcare (US)
- Georgia Institute of Technology (US)
- Corresponding author
- Copland, Ian B.
- Venue
- Stem Cell Reports
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 3
- Issue
- 1
- Pages
- 60-72
- ISSN
- 2213-6711 (ISSN-L)
- PMC
- PMC4110775
- OpenAlex
- W2063790968
- Cited by
- 139
- References
- 51
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 13 · 2023: 12 · 2022: 12 · 2021: 10 · 2020: 13 · 2019: 13 · 2018: 9 · 2017: 14 · 2016: 15 · 2015: 8 · 2014: 2
- FWCI
- 6.52
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Stem Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Georgia Cancer Coalition
- Emory University (P30CA138292)
- Immune Tolerance Network (N01 AI15416)
- National Institutes of Health (n01ai15416-28-0-11, N01-AI-15416)
- Winship Cancer Institute (P30-CA138292)
- National Cancer Institute (P30CA138292)
- National Institute of Allergy and Infectious Diseases (N01 AI 15416, N01-AI-015416)
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
- Keywords
- mesenchymal stem cells, cryopreservation, actin cytoskeleton, F-actin, cell thawing, cell biodistribution, cell adhesion, fibronectin, endothelial cells, cell therapy
- MeSH terms
- Actins, Animals, Cell Survival, Cells, Cultured, Cytoskeleton, Female, Flow Cytometry, Humans, Male, Cryopreservation, Mice, Mesenchymal Stem Cells, Real-Time Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review