Actin cytoskeletal disruption following cryopreservation alters the biodistribution of human mesenchymal stromal cells in vivo

Stem Cell Reports

Volumn 3, Issue 1, 2014, Pages 60-72

  Chinnadurai, Raghavan ^a,b   Garcia, Marco A ^c   Sakurai, Yumiko ^a,e   Lam, Wilbur A ^a,e   Kirk, Allan D ^a,f   Galipeau, Jacques ^a,b,d   Copland, Ian B ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AFLAC   (United States)

^e Emory University   (United States)

^f EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; FIBRONECTIN; ACTIN; ALPHA INTEGRIN; ALPHA4 INTEGRIN; ALPHA5 INTEGRIN; BETA INTEGRIN; BETA3 INTEGRIN; CD51 ANTIGEN; CELL ADHESION MOLECULE; CYTOCHALASIN D; FLUORESCEIN ISOTHIOCYANATE; INTERCELLULAR ADHESION MOLECULE 1; L SELECTIN; PHALLOIDIN; STROMAL CELL DERIVED FACTOR 1; TETRASPANIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYOPRESERVATION; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; FREEZE THAWING; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG PARENCHYMA; MALE; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL CULTURE; ANIMAL; CELL CULTURE; CELL SURVIVAL; CYTOSKELETON; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; APOPTOSIS; BLOOD FLOW; CALCIUM TRANSPORT; CELL ADHESION; CELL COUNTING; CELL HOMING; CELL MIGRATION; CELL SURFACE; ENGRAFTMENT; EXTRACELLULAR CALCIUM; EXTRACELLULAR MATRIX; LIMIT OF DETECTION; LUNG; PROTEIN EXPRESSION; SRY GENE; THAWING; Y CHROMOSOME;

ACTINS; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CRYOPRESERVATION; CYTOSKELETON; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICE; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84904205093     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.05.003     Document Type: Article

References (49)

1. H.M. Beere Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways J. Clin. Invest. 115 2005 2633 2639 (Pubitemid 41434386)
2. M.T. Castelo-Branco, I.D. Soares, D.V. Lopes, F. Buongusto, C.A. Martinusso, A. do Rosario Jr., S.A. Souza, B. Gutfilen, L.M. Fonseca, and C. Elia et al. Intraperitoneal but not intravenous cryopreserved mesenchymal stromal cells home to the inflamed colon and ameliorate experimental colitis PLoS ONE 7 2012 e33360
3. I.B. Copland, and J. Galipeau Death and inflammation following somatic cell transplantation Semin. Immunopathol. 33 2011 535 550
4. I.B. Copland, M.A. Garcia, E.K. Waller, J.D. Roback, and J. Galipeau The effect of platelet lysate fibrinogen on the functionality of MSCs in immunotherapy Biomaterials 34 2013 7840 7850
5. M.J. Crop, S.S. Korevaar, R. de Kuiper, J.N. IJzermans, N.M. van Besouw, C.C. Baan, W. Weimar, and M.J. Hoogduijn Human mesenchymal stem cells are susceptible to lysis by CD8(+) T cells and NK cells Cell Transplant. 20 2011 1547 1559
6. R. Cuesta, G. Laroia, and R.J. Schneider Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes Genes Dev. 14 2000 1460 1470 (Pubitemid 30421839)
7. F. De Boer, A.M. Dräger, E. Van der Wall, H.M. Pinedo, and G.J. Schuurhuis Changes in L-selectin expression on CD34-positive cells upon cryopreservation of peripheral blood stem cell transplants Bone Marrow Transplant. 22 1998 1103 1110 (Pubitemid 28554221)
8. D.A. De Ugarte, Z. Alfonso, P.A. Zuk, A. Elbarbary, M. Zhu, P. Ashjian, P. Benhaim, M.H. Hedrick, and J.K. Fraser Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow Immunol. Lett. 89 2003 267 270 (Pubitemid 37222456)
9. S.M. Devine, C. Cobbs, M. Jennings, A. Bartholomew, and R. Hoffman Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates Blood 101 2003 2999 3001 (Pubitemid 36857986)
10. L. Doerwald, C. Onnekink, S.T. van Genesen, W.W. de Jong, and N.H. Lubsen Translational thermotolerance provided by small heat shock proteins is limited to cap-dependent initiation and inhibited by 2-aminopurine J. Biol. Chem. 278 2003 49743 49750 (Pubitemid 37548807)
11. S. Durkut, A.E. Elçin, and Y.M. Elçin In vitro evaluation of encapsulated primary rat hepatocytes pre- and post-cryopreservation at -80°C and in liquid nitrogen Artif Cells Nanomed Biotechnol 2013 10.3109/21691401.2013.837476
12. N. Eliopoulos, J. Stagg, L. Lejeune, S. Pommey, and J. Galipeau Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice Blood 106 2005 4057 4065 (Pubitemid 41775910)
13. E.A. Evans, and D.A. Calderwood Forces and bond dynamics in cell adhesion Science 316 2007 1148 1153 (Pubitemid 46877469)
14. A. Fortunato, R. Leo, and F. Liguori Effects of cryostorage on human sperm chromatin integrity Zygote 21 2013 330 336
15. M. François, I.B. Copland, S. Yuan, R. Romieu-Mourez, E.K. Waller, and J. Galipeau Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing Cytotherapy 14 2012 147 152
16. J. Galipeau The mesenchymal stromal cells dilemma - does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 15 2013 2 8
17. W. Ge, J. Jiang, J. Arp, W. Liu, B. Garcia, and H. Wang Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression Transplantation 90 2010 1312 1320
18. A.A. Gurtovenko, and J. Anwar Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide J. Phys. Chem. B 111 2007 10453 10460 (Pubitemid 47441849)
19. E.K. Gustafson, G. Elgue, R.D. Hughes, R.R. Mitry, J. Sanchez, U. Haglund, S. Meurling, A. Dhawan, O. Korsgren, and B. Nilsson The instant blood-mediated inflammatory reaction characterized in hepatocyte transplantation Transplantation 91 2011 632 638
20. M. Haack-Sørensen, and J. Kastrup Cryopreservation and revival of mesenchymal stromal cells Methods Mol. Biol. 698 2011 161 174
21. Y. Hattori, H. Kato, M. Nitta, and S. Takamoto Decrease of L-selectin expression on human CD34+ cells on freeze-thawing and rapid recovery with short-term incubation Exp. Hematol. 29 2001 114 122 (Pubitemid 32054773)
22. F. He, W. Liu, S. Zheng, L. Zhou, B. Ye, and Z. Qi Ion transport through dimethyl sulfoxide (DMSO) induced transient water pores in cell membranes Mol. Membr. Biol. 29 2012 107 113
23. N. Himi, A. Hamaguchi, K. Hashimoto, T. Koga, K. Narita, and O. Miyamoto Calcium influx through the TRPV1 channel of endothelial cells (ECs) correlates with a stronger adhesion between monocytes and ECs Adv. Med. Sci. 57 2012 224 229
24. J. Huang, Z. Zhang, J. Guo, A. Ni, A. Deb, L. Zhang, M. Mirotsou, R.E. Pratt, and V.J. Dzau Genetic modification of mesenchymal stem cells overexpressing CCR1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium Circ. Res. 106 2010 1753 1762
25. H. Kenis, H.R. Zandbergen, L. Hofstra, A.D. Petrov, E.A. Dumont, F.D. Blankenberg, N. Haider, N. Bitsch, M. Gijbels, and J.W. Verjans et al. Annexin A5 uptake in ischemic myocardium: demonstration of reversible phosphatidylserine externalization and feasibility of radionuclide imaging J. Nucl. Med. 51 2010 259 267
26. M.P. Koenigsmann, M. Koenigsmann, M. Notter, M. Neuloh, C. Mücke, E. Thiel, and W.E. Berdel Adhesion molecules on peripheral blood-derived CD34+ cells: effects of cryopreservation and short-term ex vivo incubation with serum and cytokines Bone Marrow Transplant. 22 1998 1077 1085 (Pubitemid 28554217)
27. S.Y. Lee, G.W. Huang, J.N. Shiung, Y.H. Huang, J.H. Jeng, T.F. Kuo, J.C. Yang, and W.C. Yang Magnetic cryopreservation for dental pulp stem cells Cells Tissues Organs (Print) 196 2012 23 33
28. Y. Li, J. Chen, X.G. Chen, L. Wang, S.C. Gautam, Y.X. Xu, M. Katakowski, L.J. Zhang, M. Lu, N. Janakiraman, and M. Chopp Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery Neurology 59 2002 514 523 (Pubitemid 34919983)
29. Q. Li, Y. Wang, and Z. Deng Pre-conditioned mesenchymal stem cells: a better way for cell-based therapy Stem Cell Res Ther 4 2013 63
30. K. Liu, Y. Yang, and J. Mansbridge Comparison of the stress response to cryopreservation in monolayer and three-dimensional human fibroblast cultures: stress proteins, MAP kinases, and growth factor gene expression Tissue Eng. 6 2000 539 554
31. G. Moll, I. Rasmusson-Duprez, L. von Bahr, A.M. Connolly-Andersen, G. Elgue, L. Funke, O.A. Hamad, H. Lönnies, P.U. Magnusson, and J. Sanchez et al. Are therapeutic human mesenchymal stromal cells compatible with human blood? Stem Cells 30 2012 1565 1574
32. G. Moll, A. Hult, L. von Bahr, J.J. Alm, N. Heldring, O.A. Hamad, L. Stenbeck-Funke, S. Larsson, Y. Teramura, and H. Roelofs et al. Do ABO blood group antigens hamper the therapeutic efficacy of mesenchymal stromal cells? PLoS ONE 9 2014 e85040
33. R. Notman, M. Noro, B. O'Malley, and J. Anwar Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes J. Am. Chem. Soc. 128 2006 13982 13983 (Pubitemid 44657463)
34. A.J. Poncelet, J. Vercruysse, A. Saliez, and P. Gianello Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro, intracardiac injection elicits an immune response in vivo Transplantation 83 2007 783 790 (Pubitemid 46569198)
35. A.I. Pravdyuk, Y.A. Petrenko, B.J. Fuller, and A.Y. Petrenko Cryopreservation of alginate encapsulated mesenchymal stromal cells Cryobiology 66 2013 215 222
36. V. Ragoonanan, A. Hubel, and A. Aksan Response of the cell membrane-cytoskeleton complex to osmotic and freeze/thaw stresses Cryobiology 61 2010 335 344
37. J.D. Richardson, A.J. Nelson, A.C. Zannettino, S. Gronthos, S.G. Worthley, and P.J. Psaltis Optimization of the cardiovascular therapeutic properties of mesenchymal stromal/stem cells-taking the next step Stem Cell Rev. 9 2013 281 302
38. A.M. Rieger, B.E. Hall, T. Luong, L.M. Schang, and D.R. Barreda Conventional apoptosis assays using propidium iodide generate a significant number of false positives that prevent accurate assessment of cell death J. Immunol. Methods 358 2010 81 92
39. J. Rullo, H. Becker, S.J. Hyduk, J.C. Wong, G. Digby, P.D. Arora, A.P. Cano, J. Hartwig, C.A. McCulloch, and M.I. Cybulsky Actin polymerization stabilizes α4β1 integrin anchors that mediate monocyte adhesion J. Cell Biol. 197 2012 115 129
40. B. Rüster, S. Göttig, R.J. Ludwig, R. Bistrian, S. Müller, E. Seifried, J. Gille, and R. Henschler Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells Blood 108 2006 3938 3944 (Pubitemid 44864580)
41. R. Sackstein The lymphocyte homing receptors: gatekeepers of the multistep paradigm Curr. Opin. Hematol. 12 2005 444 450 (Pubitemid 41546474)
42. D. Sarkar, J.A. Spencer, J.A. Phillips, W. Zhao, S. Schafer, D.P. Spelke, L.J. Mortensen, J.P. Ruiz, P.K. Vemula, and R. Sridharan et al. Engineered cell homing Blood 118 2011 e184 e191
43. M. Tsai, A. Kita, J. Leach, R. Rounsevell, J.N. Huang, J. Moake, R.E. Ware, D.A. Fletcher, and W.A. Lam In vitro modeling of the microvascular occlusion and thrombosis that occur in hematologic diseases using microfluidic technology J. Clin. Invest. 122 2012 408 418
44. H.E. Tsai, G.S. Liu, M.L. Kung, L.F. Liu, J.C. Wu, C.H. Tang, C.H. Huang, S.C. Chen, H.C. Lam, C.S. Wu, and M.H. Tai Downregulation of hepatoma-derived growth factor contributes to retarded lung metastasis via inhibition of epithelial-mesenchymal transition by systemic POMC gene delivery in melanoma Mol. Cancer Ther. 12 2013 1016 1025
45. S.M. van den Eijnde, M.J. van den Hoff, C.P. Reutelingsperger, W.L. van Heerde, M.E. Henfling, C. Vermeij-Keers, B. Schutte, M. Borgers, and F.C. Ramaekers Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation J. Cell Sci. 114 2001 3631 3642 (Pubitemid 33041045)
46. L. von Bahr, I. Batsis, G. Moll, M. Hägg, A. Szakos, B. Sundberg, M. Uzunel, O. Ringden, and K. Le Blanc Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation Stem Cells 30 2012 1575 1578
47. X. Xu, Y. Liu, Z. Cui, Y. Wei, and L. Zhang Effects of osmotic and cold shock on adherent human mesenchymal stem cells during cryopreservation J. Biotechnol. 162 2012 224 231
48. M.A. Yenari, J. Liu, Z. Zheng, Z.S. Vexler, J.E. Lee, and R.G. Giffard Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection Ann. N Y Acad. Sci. 1053 2005 74 83 (Pubitemid 43031084)
49. G. Yourek, M.A. Hussain, and J.J. Mao Cytoskeletal changes of mesenchymal stem cells during differentiation ASAIO J. 53 2007 219 228 (Pubitemid 46597573)