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Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Review

The impact of cryopreservation on bone marrow-derived mesenchymal stem cells: a systematic review

Authors: Soukaina Bahsoun, Karen Coopman, Elizabeth C. Akam

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Mesenchymal stem cells (MSCs) represent an invaluable asset for the field of cell therapy. Human Bone marrow-derived MSCs (hBM-MSCs) are one of the most commonly used cell types in clinical trials. They are currently being studied and tested for the treatment of a wide range of diseases and conditions. The future availability of MSCs therapies to the public will require a robust and reliable delivery process. Cryopreservation represents the gold standard in cell storage and transportation, but its effect on BM-MSCs is still not well established. A systematic review was conducted to evaluate the impact of cryopreservation on BM-MSCs and to attempt to uncover the reasons behind some of the controversial results reported in the literature. Forty-one in vitro studies were analysed, and their results organised according to the cell attributes they assess. It was concluded that cryopreservation does not affect BM-MSCs morphology, surface marker expression, differentiation or proliferation potential. However, mixed results exist regarding the effect on colony forming ability and the effects on viability, attachment and migration, genomic stability and paracrine function are undefined mainly due to the huge variabilities governing the cryopreservation process as a whole and to the lack of standardised assays.
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Literature
1.
go back to reference Friedenstein AJ, Chailakhjan RK, Lalykin KS. The development of fibroblast colonies in marrow and spleen cells. Cell Tissue Kinet. 1970;3:393–403.PubMed Friedenstein AJ, Chailakhjan RK, Lalykin KS. The development of fibroblast colonies in marrow and spleen cells. Cell Tissue Kinet. 1970;3:393–403.PubMed
2.
go back to reference Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976;4(5):267–74.PubMed Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976;4(5):267–74.PubMed
3.
go back to reference Prockop D. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–4.CrossRefPubMed Prockop D. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276(5309):71–4.CrossRefPubMed
4.
go back to reference Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25(11):2739–49.CrossRefPubMed Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25(11):2739–49.CrossRefPubMed
5.
go back to reference Afanasyev BV, Elstner EE, Zander ARAJ. friedenstein, founder of the mesenchymal stem cell concept. Cell Ther Transplant. 2009;1(3):35–8. Afanasyev BV, Elstner EE, Zander ARAJ. friedenstein, founder of the mesenchymal stem cell concept. Cell Ther Transplant. 2009;1(3):35–8.
6.
10.
go back to reference Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 1995;16(4):557–64.PubMed Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal NS, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 1995;16(4):557–64.PubMed
11.
go back to reference Lotfinejad P, Shamsasenjan K, Movassaghpour A, Majidi J, Baradaran B. Immunomodulatory nature and site specific mesenchymal stem cells: a hope in cell therapy. Adv Pharm Bull. 2014;4(1):5–13. Lotfinejad P, Shamsasenjan K, Movassaghpour A, Majidi J, Baradaran B. Immunomodulatory nature and site specific mesenchymal stem cells: a hope in cell therapy. Adv Pharm Bull. 2014;4(1):5–13.
12.
go back to reference Salem HK, Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010;28(3):585–96.PubMed Salem HK, Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010;28(3):585–96.PubMed
13.
go back to reference Abazari A, Hawkins BJ, Clarke DM, Mathew AJ. Biopreservation best practices: a cornerstone in the supply chain of cell-based therapies—MSC model case study. Cell Gene Ther Insights. 2017;3(10):853–71.CrossRef Abazari A, Hawkins BJ, Clarke DM, Mathew AJ. Biopreservation best practices: a cornerstone in the supply chain of cell-based therapies—MSC model case study. Cell Gene Ther Insights. 2017;3(10):853–71.CrossRef
14.
go back to reference Woods EJ, Thirumala S, Badhe-Buchanan SS, Clarke D, Mathew AJ. Off the shelf cellular therapeutics: factors to consider during cryopreservation and storage of human cells for clinical use. Cytotherapy. 2016;18(6):697–711.CrossRefPubMed Woods EJ, Thirumala S, Badhe-Buchanan SS, Clarke D, Mathew AJ. Off the shelf cellular therapeutics: factors to consider during cryopreservation and storage of human cells for clinical use. Cytotherapy. 2016;18(6):697–711.CrossRefPubMed
15.
go back to reference Mendicino M, Bailey AM, Wonnacott K, Puri RK, Bauer SR. MSC-based product characterization for clinical trials: an FDA perspective. Cell Stem Cell. 2014;14:141–5.PubMedCrossRef Mendicino M, Bailey AM, Wonnacott K, Puri RK, Bauer SR. MSC-based product characterization for clinical trials: an FDA perspective. Cell Stem Cell. 2014;14:141–5.PubMedCrossRef
16.
go back to reference Coopman K. Large-scale compatible methods for the preservation of human embryonic stem cells: current perspectives. Biotechnol Prog. 2011;27(6):1511–21.CrossRefPubMed Coopman K. Large-scale compatible methods for the preservation of human embryonic stem cells: current perspectives. Biotechnol Prog. 2011;27(6):1511–21.CrossRefPubMed
17.
go back to reference Marquez-Curtis LA, Janowska-Wieczorek A, McGann LE, Elliott JAW. Mesenchymal stromal cells derived from various tissues: biological, clinical and cryopreservation aspects. Cryobiology. 2015;71:181–97.CrossRefPubMed Marquez-Curtis LA, Janowska-Wieczorek A, McGann LE, Elliott JAW. Mesenchymal stromal cells derived from various tissues: biological, clinical and cryopreservation aspects. Cryobiology. 2015;71:181–97.CrossRefPubMed
18.
go back to reference Gramlich OW, Burand AJ, Brown AJ, Deutsch RJ, Kuehn MH, Ankrum JA. Cryopreserved mesenchymal stromal cells maintain potency in a retinal ischemia/reperfusion injury model: toward an off-the-shelf therapy. Sci Rep. 2016;6:26463.PubMedPubMedCentralCrossRef Gramlich OW, Burand AJ, Brown AJ, Deutsch RJ, Kuehn MH, Ankrum JA. Cryopreserved mesenchymal stromal cells maintain potency in a retinal ischemia/reperfusion injury model: toward an off-the-shelf therapy. Sci Rep. 2016;6:26463.PubMedPubMedCentralCrossRef
19.
go back to reference Haack-Sorensen M, Bindslev L, Mortensen S, Friis T, Kastrup J. The influence of freezing and storage on the characteristics and functions of human mesenchymal stromal cells isolated for clinical use. Cytotherapy. 2007;9(4):328–37.CrossRefPubMed Haack-Sorensen M, Bindslev L, Mortensen S, Friis T, Kastrup J. The influence of freezing and storage on the characteristics and functions of human mesenchymal stromal cells isolated for clinical use. Cytotherapy. 2007;9(4):328–37.CrossRefPubMed
20.
go back to reference Chinnadurai R, Garcia MA, Sakurai Y, Lam WA, Kirk AD, Galipeau J, et al. Actin cytoskeletal disruption following cryopreservation alters the biodistribution of human mesenchymal stromal cells in vivo. Stem Cell Rep. 2014;3(1):60–72.CrossRef Chinnadurai R, Garcia MA, Sakurai Y, Lam WA, Kirk AD, Galipeau J, et al. Actin cytoskeletal disruption following cryopreservation alters the biodistribution of human mesenchymal stromal cells in vivo. Stem Cell Rep. 2014;3(1):60–72.CrossRef
21.
go back to reference Moll G, Geißler S, Catar R, Ignatowicz L, Hoogduijn MJ, Strunk D, et al. Cryopreserved or fresh mesenchymal stromal cells: only a matter of taste or key to unleash the full clinical potential of MSC therapy? Advances in experimental medicine and biology. Cham: Springer; 2016. p. 77–98. Moll G, Geißler S, Catar R, Ignatowicz L, Hoogduijn MJ, Strunk D, et al. Cryopreserved or fresh mesenchymal stromal cells: only a matter of taste or key to unleash the full clinical potential of MSC therapy? Advances in experimental medicine and biology. Cham: Springer; 2016. p. 77–98.
22.
go back to reference Galipeau J, Krampera M. The challenge of defining mesenchymal stromal cell potency assays and their potential use as release criteria. Cytotherapy. 2015;17(2):125–7.PubMedCrossRef Galipeau J, Krampera M. The challenge of defining mesenchymal stromal cell potency assays and their potential use as release criteria. Cytotherapy. 2015;17(2):125–7.PubMedCrossRef
23.
go back to reference Trento C, Bernardo ME, Nagler A, et al. Manufacturing mesenchymal stromal cells for the treatment of graft-versus-host disease: a survey among centers affiliated with the European Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2018;24(11):2365–70.PubMedPubMedCentralCrossRef Trento C, Bernardo ME, Nagler A, et al. Manufacturing mesenchymal stromal cells for the treatment of graft-versus-host disease: a survey among centers affiliated with the European Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2018;24(11):2365–70.PubMedPubMedCentralCrossRef
24.
go back to reference Bahsoun S, Coopman K, Forsyth NR, Akam EC. The role of dissolved oxygen levels on human mesenchymal stem cell culture success, regulatory compliance, and therapeutic potential. Stem Cells Dev. 2018;27(19):1303–21.PubMedCrossRef Bahsoun S, Coopman K, Forsyth NR, Akam EC. The role of dissolved oxygen levels on human mesenchymal stem cell culture success, regulatory compliance, and therapeutic potential. Stem Cells Dev. 2018;27(19):1303–21.PubMedCrossRef
25.
go back to reference Verdanova M, Pytlik R, Kalbacova MH. Evaluation of sericin as a fetal bovine serum-replacing cryoprotectant during freezing of human mesenchymal stromal cells and human osteoblast-like cells. Biopreserv Biobank. 2014;12(2):99–105.PubMedPubMedCentralCrossRef Verdanova M, Pytlik R, Kalbacova MH. Evaluation of sericin as a fetal bovine serum-replacing cryoprotectant during freezing of human mesenchymal stromal cells and human osteoblast-like cells. Biopreserv Biobank. 2014;12(2):99–105.PubMedPubMedCentralCrossRef
26.
go back to reference Matsumura K, Hayashi F, Nagashima T, Hyon SH. Long-term cryopreservation of human mesenchymal stem cells using carboxylated poly-l-lysine without the addition of proteins or dimethyl sulfoxide. J Biomater Sci Polym Ed. 2013;24(12):1484–97.PubMedCrossRef Matsumura K, Hayashi F, Nagashima T, Hyon SH. Long-term cryopreservation of human mesenchymal stem cells using carboxylated poly-l-lysine without the addition of proteins or dimethyl sulfoxide. J Biomater Sci Polym Ed. 2013;24(12):1484–97.PubMedCrossRef
27.
go back to reference Naaldijk Y, Staude M, Fedorova V, Stolzing A. Effect of different freezing rates during cryopreservation of rat mesenchymal stem cells using combinations of hydroxyethyl starch and dimethylsulfoxide. BMC Biotechnol. 2012;12(1):49.PubMedPubMedCentralCrossRef Naaldijk Y, Staude M, Fedorova V, Stolzing A. Effect of different freezing rates during cryopreservation of rat mesenchymal stem cells using combinations of hydroxyethyl starch and dimethylsulfoxide. BMC Biotechnol. 2012;12(1):49.PubMedPubMedCentralCrossRef
28.
go back to reference Liu Y, Xu X, Ma X, Martin-Rendon E, Watt S, Cui Z. Cryopreservation of human bone marrow-derived mesenchymal stem cells with reduced dimethylsulfoxide and well-defined freezing solutions. Biotechnol Prog. 2010;26(6):1635–43.PubMedCrossRef Liu Y, Xu X, Ma X, Martin-Rendon E, Watt S, Cui Z. Cryopreservation of human bone marrow-derived mesenchymal stem cells with reduced dimethylsulfoxide and well-defined freezing solutions. Biotechnol Prog. 2010;26(6):1635–43.PubMedCrossRef
29.
go back to reference Liu Y, Xu X, Xuehu M, Liu J, Cui Z. Effect of various freezing solutions on cryopreservation of mesenchymal stem cells from different animal species. Cryo-Letters. 2011;32(5):425–35.PubMed Liu Y, Xu X, Xuehu M, Liu J, Cui Z. Effect of various freezing solutions on cryopreservation of mesenchymal stem cells from different animal species. Cryo-Letters. 2011;32(5):425–35.PubMed
30.
go back to reference Heng BC. Effect of Rho-associated kinase (ROCK) inhibitor Y-27632 on the post-thaw viability of cryopreserved human bone marrow-derived mesenchymal stem cells. Tissue Cell. 2009;41(5):376–80.CrossRefPubMed Heng BC. Effect of Rho-associated kinase (ROCK) inhibitor Y-27632 on the post-thaw viability of cryopreserved human bone marrow-derived mesenchymal stem cells. Tissue Cell. 2009;41(5):376–80.CrossRefPubMed
31.
go back to reference Renzi S, Lombardo T, Dotti S, Dessi SS, De Blasio P, Ferrari M. Mesenchymal stromal cell cryopreservation. Biopreserv Biobank. 2012;10(3):276–81.CrossRefPubMed Renzi S, Lombardo T, Dotti S, Dessi SS, De Blasio P, Ferrari M. Mesenchymal stromal cell cryopreservation. Biopreserv Biobank. 2012;10(3):276–81.CrossRefPubMed
32.
go back to reference Mitchell A, Rivas KA, Smith R, Watts AE. Cryopreservation of equine mesenchymal stem cells in 95% autologous serum and 5% DMSO does not alter post-thaw growth or morphology in vitro compared to fetal bovine serum or allogeneic serum at 20 or 95% and DMSO at 10 or 5%. Stem Cell Res Ther. 2015;6(1):231.PubMedPubMedCentralCrossRef Mitchell A, Rivas KA, Smith R, Watts AE. Cryopreservation of equine mesenchymal stem cells in 95% autologous serum and 5% DMSO does not alter post-thaw growth or morphology in vitro compared to fetal bovine serum or allogeneic serum at 20 or 95% and DMSO at 10 or 5%. Stem Cell Res Ther. 2015;6(1):231.PubMedPubMedCentralCrossRef
33.
go back to reference Mamidi MK, Nathan KG, Singh G, Thrichelvam ST, Mohd Yusof NAN, Fakharuzi NA, et al. Comparative cellular and molecular analyses of pooled bone marrow multipotent mesenchymal stromal cells during continuous passaging and after successive cryopreservation. J Cell Biochem. 2012;113(3):3153–64.CrossRefPubMed Mamidi MK, Nathan KG, Singh G, Thrichelvam ST, Mohd Yusof NAN, Fakharuzi NA, et al. Comparative cellular and molecular analyses of pooled bone marrow multipotent mesenchymal stromal cells during continuous passaging and after successive cryopreservation. J Cell Biochem. 2012;113(3):3153–64.CrossRefPubMed
34.
go back to reference Lechanteur C, Briquet A, Giet O, Delloye O, Baudoux E, Beguin Y. Clinical-scale expansion of mesenchymal stromal cells: a large banking experience. J Transl Med. 2016;14(1):145.PubMedPubMedCentralCrossRef Lechanteur C, Briquet A, Giet O, Delloye O, Baudoux E, Beguin Y. Clinical-scale expansion of mesenchymal stromal cells: a large banking experience. J Transl Med. 2016;14(1):145.PubMedPubMedCentralCrossRef
35.
go back to reference Kotobuki N, Hirose M, Takakura Y, Ohgushi H. Cultured autologous human cells for hard tissue regeneration: preparation and characterization of mesenchymal stem cells from bone marrow. Artif Organs. 2004;28(1):33–9.CrossRefPubMed Kotobuki N, Hirose M, Takakura Y, Ohgushi H. Cultured autologous human cells for hard tissue regeneration: preparation and characterization of mesenchymal stem cells from bone marrow. Artif Organs. 2004;28(1):33–9.CrossRefPubMed
36.
go back to reference Edamura K, Nakano R, Fujimoto K, Teshima K, Asano K, Tanaka S. Effects of cryopreservation on the cell viability, proliferative capacity and neuronal differentiation potential of canine bone marrow stromal cells. J Vet Med Sci. 2014;76(4):573–7.CrossRefPubMed Edamura K, Nakano R, Fujimoto K, Teshima K, Asano K, Tanaka S. Effects of cryopreservation on the cell viability, proliferative capacity and neuronal differentiation potential of canine bone marrow stromal cells. J Vet Med Sci. 2014;76(4):573–7.CrossRefPubMed
37.
go back to reference Kumazawa K, Sugimoto T, Yamazaki Y, Takeda A, Uchinuma E. Osteogenic potential, multipotency, and cytogenetic safety of human bone tissue-derived mesenchymal stromal cells (hBT-MSCs) after long-term cryopreservation. Kitasato Med J. 2014;44:95–103. Kumazawa K, Sugimoto T, Yamazaki Y, Takeda A, Uchinuma E. Osteogenic potential, multipotency, and cytogenetic safety of human bone tissue-derived mesenchymal stromal cells (hBT-MSCs) after long-term cryopreservation. Kitasato Med J. 2014;44:95–103.
38.
go back to reference Moll G, Alm JJ, Davies LC, Von Bahr L, Heldring N, Stenbeck-Funke L, et al. Do cryopreserved mesenchymal stromal cells display impaired immunomodulatory and therapeutic properties? Stem Cells. 2014;32(9):2430–42.PubMedPubMedCentralCrossRef Moll G, Alm JJ, Davies LC, Von Bahr L, Heldring N, Stenbeck-Funke L, et al. Do cryopreserved mesenchymal stromal cells display impaired immunomodulatory and therapeutic properties? Stem Cells. 2014;32(9):2430–42.PubMedPubMedCentralCrossRef
39.
go back to reference Heino TJ, Alm JJ, Moritz N, Aro HT. Comparison of the osteogenic capacity of minipig and human bone marrow-derived mesenchymal stem cells. J Orthop Res. 2012;30(7):1019–25.CrossRefPubMed Heino TJ, Alm JJ, Moritz N, Aro HT. Comparison of the osteogenic capacity of minipig and human bone marrow-derived mesenchymal stem cells. J Orthop Res. 2012;30(7):1019–25.CrossRefPubMed
40.
go back to reference Luetzkendorf J, Nerger K, Hering J, Moegel A, Hoffmann K, Hoefers C, et al. Cryopreservation does not alter main characteristics of Good Manufacturing Process-grade human multipotent mesenchymal stromal cells including immunomodulating potential and lack of malignant transformation. Cytotherapy. 2015;17:186–98.CrossRefPubMed Luetzkendorf J, Nerger K, Hering J, Moegel A, Hoffmann K, Hoefers C, et al. Cryopreservation does not alter main characteristics of Good Manufacturing Process-grade human multipotent mesenchymal stromal cells including immunomodulating potential and lack of malignant transformation. Cytotherapy. 2015;17:186–98.CrossRefPubMed
41.
go back to reference Hirose M, Kotobuki N, Machida H, Kitamura S, Ohgushi H, Tateishi T. Osteogenic potential of cryopreserved human bone marrow-derived mesenchymal cells after thawing in culture. Mater Sci Eng C. 2004;24(3):355–9.CrossRef Hirose M, Kotobuki N, Machida H, Kitamura S, Ohgushi H, Tateishi T. Osteogenic potential of cryopreserved human bone marrow-derived mesenchymal cells after thawing in culture. Mater Sci Eng C. 2004;24(3):355–9.CrossRef
42.
go back to reference Davies OG, Smith AJ, Cooper PR, Shelton RM, Scheven BA. The effects of cryopreservation on cells isolated from adipose, bone marrow and dental pulp tissues. Cryobiology. 2014;69(2):342–7.CrossRefPubMed Davies OG, Smith AJ, Cooper PR, Shelton RM, Scheven BA. The effects of cryopreservation on cells isolated from adipose, bone marrow and dental pulp tissues. Cryobiology. 2014;69(2):342–7.CrossRefPubMed
43.
go back to reference Bissoyi A, Nayak B, Pramanik K, Sarangi SK. Targeting cryopreservation-induced cell death: a review. Biopreserv Biobank. 2014;12(1):23–34.CrossRefPubMed Bissoyi A, Nayak B, Pramanik K, Sarangi SK. Targeting cryopreservation-induced cell death: a review. Biopreserv Biobank. 2014;12(1):23–34.CrossRefPubMed
44.
go back to reference Carvalho KAT, Cury CC, Oliveira L, Cattaned RII, Malvezzi M, Francisco JC, et al. Evaluation of bone marrow mesenchymal stem cell standard cryopreservation procedure efficiency. Transplant Proc. 2008;40:839–41.CrossRefPubMed Carvalho KAT, Cury CC, Oliveira L, Cattaned RII, Malvezzi M, Francisco JC, et al. Evaluation of bone marrow mesenchymal stem cell standard cryopreservation procedure efficiency. Transplant Proc. 2008;40:839–41.CrossRefPubMed
45.
go back to reference François M, Copland IB, Yuan S, Romieu-Mourez R, Waller EK, Galipeau J. Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing. Cytotherapy. 2012;14(2):147–52.CrossRefPubMed François M, Copland IB, Yuan S, Romieu-Mourez R, Waller EK, Galipeau J. Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing. Cytotherapy. 2012;14(2):147–52.CrossRefPubMed
46.
go back to reference Zhu X, Yuan F, Li L, Zheng Y, Xiao Y, Yan F. Evaluation of canine bone marrow-derived mesenchymal stem cells after long-term cryopreservation. Zool Sci. 2013;30(12):1032–7.CrossRef Zhu X, Yuan F, Li L, Zheng Y, Xiao Y, Yan F. Evaluation of canine bone marrow-derived mesenchymal stem cells after long-term cryopreservation. Zool Sci. 2013;30(12):1032–7.CrossRef
47.
go back to reference Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.CrossRefPubMed Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.CrossRefPubMed
48.
go back to reference Tokumoto S, Sotome S, Torigoe I, Omura K, Shinomiya K. Effects of cryopreservation on bone marrow derived mesenchymal cells of a nonhuman primate. J Med Dent Sci. 2008;55:137–43.PubMed Tokumoto S, Sotome S, Torigoe I, Omura K, Shinomiya K. Effects of cryopreservation on bone marrow derived mesenchymal cells of a nonhuman primate. J Med Dent Sci. 2008;55:137–43.PubMed
49.
go back to reference Lauterboeck L, Saha D, Chatterjee A, Hofmann N, Glasmacher B. Xeno-Free Cryopreservation of bone marrow-derived multipotent stromal cells from Callithrix jacchus. Biopreserv Biobank. 2016;14:530–8.CrossRefPubMed Lauterboeck L, Saha D, Chatterjee A, Hofmann N, Glasmacher B. Xeno-Free Cryopreservation of bone marrow-derived multipotent stromal cells from Callithrix jacchus. Biopreserv Biobank. 2016;14:530–8.CrossRefPubMed
50.
go back to reference Ginis I, Grinblat B, Shirvan MH. Evaluation of bone marrow-derived mesenchymal stem cells after cryopreservation and hypothermic storage in clinically safe medium. Tissue Eng Part C Methods. 2012;18(6):453–63.CrossRefPubMed Ginis I, Grinblat B, Shirvan MH. Evaluation of bone marrow-derived mesenchymal stem cells after cryopreservation and hypothermic storage in clinically safe medium. Tissue Eng Part C Methods. 2012;18(6):453–63.CrossRefPubMed
51.
go back to reference Ock SA, Rho GJ. Effect of dimethyl sulfoxide (DMSO) on cryopreservation of porcine mesenchymal stem cells (pMSCS). Cell Transplant. 2011;20(8):1231–9.CrossRefPubMed Ock SA, Rho GJ. Effect of dimethyl sulfoxide (DMSO) on cryopreservation of porcine mesenchymal stem cells (pMSCS). Cell Transplant. 2011;20(8):1231–9.CrossRefPubMed
52.
go back to reference Yuan Z, Lourenco SDS, Sage EK, Kolluri KK, Lowdell MW, Janes SM. Cryopreservation of human mesenchymal stromal cells expressing TRAIL for human anti-cancer therapy. Cytotherapy. 2016;18(7):860–9.PubMedPubMedCentralCrossRef Yuan Z, Lourenco SDS, Sage EK, Kolluri KK, Lowdell MW, Janes SM. Cryopreservation of human mesenchymal stromal cells expressing TRAIL for human anti-cancer therapy. Cytotherapy. 2016;18(7):860–9.PubMedPubMedCentralCrossRef
53.
go back to reference Squillaro T, Peluso G, Galderisi U. clinical trials with mesenchymal stem cells: an update. Cell Transplant. 2016;25(5):829–48.PubMedCrossRef Squillaro T, Peluso G, Galderisi U. clinical trials with mesenchymal stem cells: an update. Cell Transplant. 2016;25(5):829–48.PubMedCrossRef
54.
go back to reference Baust JM, Corwin W, Snyder KK, Van Buskirk R, Baust JG. Cryopreservation: evolution of molecular based strategies. Biobanking and cryopreservation of stem cells. Cham: Springer; 2016. p. 13–29.CrossRef Baust JM, Corwin W, Snyder KK, Van Buskirk R, Baust JG. Cryopreservation: evolution of molecular based strategies. Biobanking and cryopreservation of stem cells. Cham: Springer; 2016. p. 13–29.CrossRef
55.
go back to reference Chatterjee A, Saha D, Niemann H, Gryshkov O, Glasmacher B, Hofmann N. Effects of cryopreservation on the epigenetic profile of cells. Cryobiology. 2017;74:1–7.PubMedCrossRef Chatterjee A, Saha D, Niemann H, Gryshkov O, Glasmacher B, Hofmann N. Effects of cryopreservation on the epigenetic profile of cells. Cryobiology. 2017;74:1–7.PubMedCrossRef
56.
go back to reference De Wolf C, Van De Bovenkamp M, Hoefnagel M. Regulatory perspective on in vitro potency assays for human mesenchymal stromal cells used in immunotherapy. Cytotherapy. 2017;19:784–97.CrossRefPubMed De Wolf C, Van De Bovenkamp M, Hoefnagel M. Regulatory perspective on in vitro potency assays for human mesenchymal stromal cells used in immunotherapy. Cytotherapy. 2017;19:784–97.CrossRefPubMed
57.
go back to reference Robb KP, Fitzgerald JC, Barry F, Viswanathan S. Mesenchymal stromal cell therapy: progress in manufacturing and assessments of potency. Cytotherapy. 2019;21(3):289–306.CrossRefPubMed Robb KP, Fitzgerald JC, Barry F, Viswanathan S. Mesenchymal stromal cell therapy: progress in manufacturing and assessments of potency. Cytotherapy. 2019;21(3):289–306.CrossRefPubMed
58.
go back to reference Krampera M, Galipeau J, Shi Y, Tarte K, Sensebe L. Immunological characterization of multipotent mesenchymal stromal cells-The international society for cellular therapy (ISCT) working proposal. Cytotherapy. 2013;15(9):1054–61.CrossRefPubMed Krampera M, Galipeau J, Shi Y, Tarte K, Sensebe L. Immunological characterization of multipotent mesenchymal stromal cells-The international society for cellular therapy (ISCT) working proposal. Cytotherapy. 2013;15(9):1054–61.CrossRefPubMed
59.
go back to reference Galipeau J, Krampera M, Barrett J, Dazzi F, Deans RJ, DeBruijn J, et al. International Society for Cellular Therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy. 2016;18:151–9.CrossRefPubMed Galipeau J, Krampera M, Barrett J, Dazzi F, Deans RJ, DeBruijn J, et al. International Society for Cellular Therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy. 2016;18:151–9.CrossRefPubMed
60.
go back to reference Samsonraj RM, Raghunath M, Nurcombe V, Hui JH, van Wijnen AJ, Cool SM. Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Transl Med. 2017;6(12):2173–85.PubMedPubMedCentralCrossRef Samsonraj RM, Raghunath M, Nurcombe V, Hui JH, van Wijnen AJ, Cool SM. Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Transl Med. 2017;6(12):2173–85.PubMedPubMedCentralCrossRef
61.
go back to reference Martino M, Morabito F, Messina G, Irrera G, Pucci G, Iacopino P. Fractionated infusions of cryopreserved stem cells may prevent DMSO- induced major cardiac complications in graft recipients. Haematologica. 1996;81(1):59–61.PubMed Martino M, Morabito F, Messina G, Irrera G, Pucci G, Iacopino P. Fractionated infusions of cryopreserved stem cells may prevent DMSO- induced major cardiac complications in graft recipients. Haematologica. 1996;81(1):59–61.PubMed
62.
go back to reference Zenhäusern R, Tobler A, Leoncini L, Hess OM, Ferrari P. Fatal cardiac arrhythmia after infusion of dimethyl sulfoxide-cryopreserved hematopoietic stem cells in a patient with severe primary cardiac amyloidosis and end-stage renal failure. Ann Hematol. 2000;79:523–6.CrossRefPubMed Zenhäusern R, Tobler A, Leoncini L, Hess OM, Ferrari P. Fatal cardiac arrhythmia after infusion of dimethyl sulfoxide-cryopreserved hematopoietic stem cells in a patient with severe primary cardiac amyloidosis and end-stage renal failure. Ann Hematol. 2000;79:523–6.CrossRefPubMed
63.
go back to reference Stamatovic D, Balint B, Tukic LJ, Elez M, Tarabar O, Ostojic G, et al. Severe neurotoxicity following peripheral blood stem cell transplantation. Bone Marrow Transplant. 2011;46:1110. Stamatovic D, Balint B, Tukic LJ, Elez M, Tarabar O, Ostojic G, et al. Severe neurotoxicity following peripheral blood stem cell transplantation. Bone Marrow Transplant. 2011;46:1110.
64.
go back to reference Windrum P, Morris TCM. Severe neurotoxicity because of dimethyl sulphoxide following peripheral blood stem cell transplantation. Bone Marrow Transplant. 2003;31:315.CrossRefPubMed Windrum P, Morris TCM. Severe neurotoxicity because of dimethyl sulphoxide following peripheral blood stem cell transplantation. Bone Marrow Transplant. 2003;31:315.CrossRefPubMed
65.
go back to reference Yong KW, Wan Safwani WKZ, Xu F, Wan Abas WAB, Choi JR, Pingguan-Murphy B. Cryopreservation of human mesenchymal stem cells for clinical applications: current methods and challenges. Biopreserv Biobank. 2015;13(4):231–9.CrossRefPubMed Yong KW, Wan Safwani WKZ, Xu F, Wan Abas WAB, Choi JR, Pingguan-Murphy B. Cryopreservation of human mesenchymal stem cells for clinical applications: current methods and challenges. Biopreserv Biobank. 2015;13(4):231–9.CrossRefPubMed
66.
go back to reference Al-Saqi SH, Saliem M, Quezada HC, Ekblad Å, Jonasson AF, Hovatta O, et al. Defined serum- and xeno-free cryopreservation of mesenchymal stem cells. Cell Tissue Bank. 2015;16(2):181–93.PubMedCrossRef Al-Saqi SH, Saliem M, Quezada HC, Ekblad Å, Jonasson AF, Hovatta O, et al. Defined serum- and xeno-free cryopreservation of mesenchymal stem cells. Cell Tissue Bank. 2015;16(2):181–93.PubMedCrossRef
67.
go back to reference Pollock K, Sumstad D, Kadidlo D, McKenna DH, Hubel A. Clinical mesenchymal stromal cell products undergo functional changes in response to freezing. Cytotherapy. 2015;17(1):38–45.PubMedCrossRef Pollock K, Sumstad D, Kadidlo D, McKenna DH, Hubel A. Clinical mesenchymal stromal cell products undergo functional changes in response to freezing. Cytotherapy. 2015;17(1):38–45.PubMedCrossRef
68.
go back to reference Chinnadurai R, Copland IB, Garcia MA, Petersen CT, Lewis CN, Waller EK, et al. Cryopreserved MSCs are susceptible to T-cell mediated apoptosis which is partly rescued by IFNγ licensing Raghavan. Stem Cells. 2016;34(9):2429–42.PubMedPubMedCentralCrossRef Chinnadurai R, Copland IB, Garcia MA, Petersen CT, Lewis CN, Waller EK, et al. Cryopreserved MSCs are susceptible to T-cell mediated apoptosis which is partly rescued by IFNγ licensing Raghavan. Stem Cells. 2016;34(9):2429–42.PubMedPubMedCentralCrossRef
69.
go back to reference Holubova M, Lysak D, Vlas T, Vannucci L, Jindra P. Expanded cryopreserved mesenchymal stromal cells as an optimal source for graft-versus-host disease treatment. Biologicals. 2014;42(3):139–44.PubMedCrossRef Holubova M, Lysak D, Vlas T, Vannucci L, Jindra P. Expanded cryopreserved mesenchymal stromal cells as an optimal source for graft-versus-host disease treatment. Biologicals. 2014;42(3):139–44.PubMedCrossRef
70.
go back to reference Bieback K, Kuçi S, Schäfer R. Production and quality testing of multipotent mesenchymal stromal cell therapeutics for clinical use. Transfusion. 2019;59:2164–73.CrossRefPubMed Bieback K, Kuçi S, Schäfer R. Production and quality testing of multipotent mesenchymal stromal cell therapeutics for clinical use. Transfusion. 2019;59:2164–73.CrossRefPubMed
71.
go back to reference Stacey GN, Connon CJ, Coopman K, Dickson AJ, Fuller B, Hunt CJ, et al. Preservation and stability of cell therapy products: recommendations from an expert workshop. Regen Med. 2017;12(5):553–64.CrossRefPubMed Stacey GN, Connon CJ, Coopman K, Dickson AJ, Fuller B, Hunt CJ, et al. Preservation and stability of cell therapy products: recommendations from an expert workshop. Regen Med. 2017;12(5):553–64.CrossRefPubMed
72.
go back to reference Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell. 2005;120(2):237–48.CrossRefPubMed Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell. 2005;120(2):237–48.CrossRefPubMed
73.
go back to reference Mason EF, Rathmell JC. Cell metabolism: An essential link between cell growth and apoptosis. Biochim et Biophys Acta Mol Cell Res. 2011;1813:645–54.CrossRef Mason EF, Rathmell JC. Cell metabolism: An essential link between cell growth and apoptosis. Biochim et Biophys Acta Mol Cell Res. 2011;1813:645–54.CrossRef
74.
go back to reference Baldari S, Di Rocco G, Piccoli M, Pozzobon M, Muraca M, Toietta G. Challenges and strategies for improving the regenerative effects of mesenchymal stromal cell-based therapies. Int J Mol Sci. 2017;18(10):2087.PubMedCentralCrossRef Baldari S, Di Rocco G, Piccoli M, Pozzobon M, Muraca M, Toietta G. Challenges and strategies for improving the regenerative effects of mesenchymal stromal cell-based therapies. Int J Mol Sci. 2017;18(10):2087.PubMedCentralCrossRef
75.
go back to reference Ward MR, Abadeh A, Connelly KA. Concise review: rational use of mesenchymal stem cells in the treatment of ischemic heart disease. Stem Cells Transl Med. 2018;7(7):543–50.PubMedPubMedCentralCrossRef Ward MR, Abadeh A, Connelly KA. Concise review: rational use of mesenchymal stem cells in the treatment of ischemic heart disease. Stem Cells Transl Med. 2018;7(7):543–50.PubMedPubMedCentralCrossRef
76.
go back to reference Baust JG, Snyder KK, Van Buskirk R, Baust JM. Integrating molecular control to improve cryopreservation outcome. Biopreserv Biobank. 2017;15(2):134–41.CrossRefPubMed Baust JG, Snyder KK, Van Buskirk R, Baust JM. Integrating molecular control to improve cryopreservation outcome. Biopreserv Biobank. 2017;15(2):134–41.CrossRefPubMed
78.
go back to reference González DA, Pando RH, Lim MÁG, Fraustro SA, Garcia AT. Therapeutic strategies of secretome of mesenchymal stem cell. Stromal cells-structure, function, and therapeutic implications. London: IntechOpen; 2018. González DA, Pando RH, Lim MÁG, Fraustro SA, Garcia AT. Therapeutic strategies of secretome of mesenchymal stem cell. Stromal cells-structure, function, and therapeutic implications. London: IntechOpen; 2018.
79.
go back to reference Merino-González C, Zuñiga FA, Escudero C, Ormazabal V, Reyes C, Nova-Lamperti E, et al. Mesenchymal stem cell-derived extracellular vesicles promote angiogenesis: potencial clinical application. Front Physiol. 2016;7:24.PubMedPubMedCentralCrossRef Merino-González C, Zuñiga FA, Escudero C, Ormazabal V, Reyes C, Nova-Lamperti E, et al. Mesenchymal stem cell-derived extracellular vesicles promote angiogenesis: potencial clinical application. Front Physiol. 2016;7:24.PubMedPubMedCentralCrossRef
81.
go back to reference Duscher D, Barrera J, Wong VW, Maan ZN, Whittam AJ, Januszyk M, et al. Stem cells in wound healing: the future of regenerative medicine? A mini-review. Gerontology. 2016;62:216–25.CrossRefPubMed Duscher D, Barrera J, Wong VW, Maan ZN, Whittam AJ, Januszyk M, et al. Stem cells in wound healing: the future of regenerative medicine? A mini-review. Gerontology. 2016;62:216–25.CrossRefPubMed
82.
go back to reference Vizoso FJ, Eiro N, Cid S, Schneider J, Perez-Fernandez R. Mesenchymal stem cell secretome: toward cell-free therapeutic strategies in regenerative medicine. Int J Mol Sci. 2017;18:1852.PubMedCentralCrossRef Vizoso FJ, Eiro N, Cid S, Schneider J, Perez-Fernandez R. Mesenchymal stem cell secretome: toward cell-free therapeutic strategies in regenerative medicine. Int J Mol Sci. 2017;18:1852.PubMedCentralCrossRef
83.
go back to reference Konala VBR, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R. The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy. 2016;18:13–24.CrossRefPubMed Konala VBR, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R. The current landscape of the mesenchymal stromal cell secretome: a new paradigm for cell-free regeneration. Cytotherapy. 2016;18:13–24.CrossRefPubMed
84.
85.
go back to reference Bruno S, Deregibus MC, Camussi G. The secretome of mesenchymal stromal cells: role of extracellular vesicles in immunomodulation. Immunol Lett. 2015;168:154–8.CrossRefPubMed Bruno S, Deregibus MC, Camussi G. The secretome of mesenchymal stromal cells: role of extracellular vesicles in immunomodulation. Immunol Lett. 2015;168:154–8.CrossRefPubMed
86.
go back to reference Chinnadurai R, Rajan D, Qayed M, Arafat D, Garcia M, Liu Y, et al. Potency analysis of mesenchymal stromal cells using a combinatorial assay matrix approach. Cell Rep. 2018;22(9):2504–17.PubMedPubMedCentralCrossRef Chinnadurai R, Rajan D, Qayed M, Arafat D, Garcia M, Liu Y, et al. Potency analysis of mesenchymal stromal cells using a combinatorial assay matrix approach. Cell Rep. 2018;22(9):2504–17.PubMedPubMedCentralCrossRef
87.
go back to reference Fung M, Yuan Y, Atkins H, Shi Q, Bubela T. Responsible translation of stem cell research: an assessment of clinical trial registration and publications. Stem Cell Rep. 2017;8:1190–201.CrossRef Fung M, Yuan Y, Atkins H, Shi Q, Bubela T. Responsible translation of stem cell research: an assessment of clinical trial registration and publications. Stem Cell Rep. 2017;8:1190–201.CrossRef
89.
go back to reference Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell. 2015;17(1):11–22.CrossRefPubMed Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell. 2015;17(1):11–22.CrossRefPubMed
90.
go back to reference Marks PW, Witten CM, Califf RM. Clarifying stem-cell therapy’s benefits and risks. N Engl J Med. 2017;376(11):1007–9.PubMedCrossRef Marks PW, Witten CM, Califf RM. Clarifying stem-cell therapy’s benefits and risks. N Engl J Med. 2017;376(11):1007–9.PubMedCrossRef
91.
go back to reference Bruder SP, Jaiswal N, Haynesworth SE. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem. 1997;64:278–94.PubMedCrossRef Bruder SP, Jaiswal N, Haynesworth SE. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem. 1997;64:278–94.PubMedCrossRef
92.
go back to reference Kotobuki N, Hirose M, Machida H, Katou Y, Muraki K, Takakura Y, et al. Viability and osteogenic potential of cryopreserved human bone marrow-derived mesenchymal cells. Tissue Eng. 2005;11:663–73.CrossRefPubMed Kotobuki N, Hirose M, Machida H, Katou Y, Muraki K, Takakura Y, et al. Viability and osteogenic potential of cryopreserved human bone marrow-derived mesenchymal cells. Tissue Eng. 2005;11:663–73.CrossRefPubMed
93.
go back to reference Xiang Y, Zheng Q, Jia B, Huang G, Xie C, Pan J, et al. Ex vivo expansion, adipogenesis and neurogenesis of cryopreserved human bone marrow mesenchymal stem cells. Cell Biol Int. 2007;31:444–50.CrossRefPubMed Xiang Y, Zheng Q, Jia B, Huang G, Xie C, Pan J, et al. Ex vivo expansion, adipogenesis and neurogenesis of cryopreserved human bone marrow mesenchymal stem cells. Cell Biol Int. 2007;31:444–50.CrossRefPubMed
94.
go back to reference Zhao ZG, Li WM, Chen ZC, You Y, Zou P. hematopoeisis capacity immunomodulatory effect andex vivo expasion poetntial of mesenhcymal stem cells are not impaired by cryopreservation. Cancer Invest. 2008;26(4):391–400.CrossRefPubMed Zhao ZG, Li WM, Chen ZC, You Y, Zou P. hematopoeisis capacity immunomodulatory effect andex vivo expasion poetntial of mesenhcymal stem cells are not impaired by cryopreservation. Cancer Invest. 2008;26(4):391–400.CrossRefPubMed
95.
go back to reference Doan CC, Truong NH, Vu NB, Nguyen TT, Nguyen HM, Nguyen KG, et al. Isolation, culture and cryopreservation of human bone marrow-derived mesenchymal stem cells. Int J Plant Anim Environ Sci. 2012;2(2):83–90. Doan CC, Truong NH, Vu NB, Nguyen TT, Nguyen HM, Nguyen KG, et al. Isolation, culture and cryopreservation of human bone marrow-derived mesenchymal stem cells. Int J Plant Anim Environ Sci. 2012;2(2):83–90.
96.
go back to reference Li H, Yan F, Lei L, Li Y, Xiao Y. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs. 2009;190(2):94–101.CrossRefPubMed Li H, Yan F, Lei L, Li Y, Xiao Y. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs. 2009;190(2):94–101.CrossRefPubMed
97.
go back to reference Nitsch S, Chatterjee A, Hofmann N, Glasmacher B. Impact of cryopreservation on histone modifications of mesenchymal stem cells. Biomedizinische Technik. 2014;59:S294–7. Nitsch S, Chatterjee A, Hofmann N, Glasmacher B. Impact of cryopreservation on histone modifications of mesenchymal stem cells. Biomedizinische Technik. 2014;59:S294–7.
98.
go back to reference Romanek J, Opiela J, Lipiński D, Smorąg Z. Effect of high hydrostatic pressure applied before cryopreservation on the survival rate and quality of porcine mesenchymal stem cells after thawing. Anim Biotechnol. 2018;29(4):283–92.CrossRefPubMed Romanek J, Opiela J, Lipiński D, Smorąg Z. Effect of high hydrostatic pressure applied before cryopreservation on the survival rate and quality of porcine mesenchymal stem cells after thawing. Anim Biotechnol. 2018;29(4):283–92.CrossRefPubMed
Metadata
Title
The impact of cryopreservation on bone marrow-derived mesenchymal stem cells: a systematic review
Authors
Soukaina Bahsoun
Karen Coopman
Elizabeth C. Akam
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-02136-7

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