Cryopreservation of human bone marrow-derived mesenchymal stem cells with reduced dimethylsulfoxide and well-defined freezing solutions

Biotechnology Progress

Volumn 26, Issue 6, 2010, Pages 1635-1643

  Liu, Yang ^a,b   Xu, Xia ^b   Ma, Xuehu ^a   Martin Rendon, Enca ^c,d   Watt, Suzanne ^c,d   Cui, Zhanfeng ^b  

^a DALIAN UNIVERSITY OF TECHNOLOGY   (China)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cryopreservation; DMSO; Mesenchymal stem cells; Well defined freezing solutions

Indexed keywords

ADIPOGENIC; APOPTOTIC; BOVINE SERUM ALBUMINS; CELL MORPHOLOGY; CELL THERAPY; CELL VIABILITY; CHONDROGENIC DIFFERENTIATION; CRYO-PRESERVATION; DMSO; GROWTH DYNAMICS; HUMAN BONE MARROW; MESENCHYMAL STEM CELLS; METABOLIC ACTIVITY; OSTEOGENIC; POLYETHYLENE GLYCOLS (PEG); PROPANDIOL;

BIOLOGICAL MATERIALS PRESERVATION; BODY FLUIDS; BONE; CELL CULTURE; FREEZING; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; THAWING; TISSUE ENGINEERING;

STEM CELLS;

DIMETHYL SULFOXIDE; MACROGOL DERIVATIVE; TREHALOSE;

ARTICLE; CHEMISTRY; CRYOPRESERVATION; CYTOLOGY; FREEZING; HUMAN; MESENCHYMAL STEM CELL; SOLUTION AND SOLUBILITY;

CRYOPRESERVATION; DIMETHYL SULFOXIDE; FREEZING; HUMANS; MESENCHYMAL STEM CELLS; POLYETHYLENE GLYCOLS; SOLUTIONS; TREHALOSE;

BOVINAE;

EID: 78650200044     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.464     Document Type: Article

References (52)

1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284: 143-147.
2. 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: 355-359.
3. Kotobuki N, Hirose M, Machida H, Katou Y, Nuraki A, Takakura Y, Ohgushi H. Viability and osteogenic potential of cryopreserved human bone marrow-derived mesenchymal cells. Tissue Eng. 2005; 11: 663-673.
4. Kuleshova LL, Gouk SS, Hutmacher DW. Vitrification as a prospect for cryopreservation of tissue-engineered constructs. Biomaterials. 2007; 28: 1585-1596.
5. Luciano AM, Chigioni S, Lodde V, Franciosi F, Luvoni GC, Modina SC. Effect of different cryopreservation protocols on cytoskeleton and gap junction mediated communication integrity in feline germinal vesicle stage oocytes. Cryobiology. 2009; 59: 90-95.
6. Polge C, Smith AU, Parkes AS. Revival of spermatozoa after vitrification and dehydration at low temperature. Nature. 1949; 164: 666-666.
7. Nie Y, Bergendahl V, Hei DJ, Jones JM, Palecek SP. Scalable culture and cryopreservation of human embryonic stem cells on microcarriers. Biotechnol Prog. 2009; 25: 20-31.
8. Zhao J, Hao HN, Thomas RL, Lyman WD. An efficient method for the cryopreservation of fetal human liver hematopoietic progenitor cells. Stem Cells. 2001; 19: 212-218.
9. Yang H, Zhao H, Acker JP, Liu JZ, Akabuta J, McGann LE. Effect of dimethyl sulfoxide on post-thaw viability assessment of CD45+ and CD34+ cells of umbilical cord blood and mobilized peripheral blood. Cryobiology. 2005; 51: 165-175.
10. Milosevic J, Storch A, Schwarz J. Cryopreservation does not affect proliferation and multipotency of murine neural precursor cells. Stem Cells. 2005; 23: 681-688.
11. Liu GP, Zhou H, Li YL, Li G, Cui L, Liu W, Cao YL. Evaluation of the viability and osteogenic differentiation of cryopreserved human adipose-derived stem cells. Cryobiology. 2008; 57: 18-24.
12. Yeh HJ, Yao CL, Chen HI, Cheng HC, Hwang SM. Cryopreservation of human limbal stem cells ex vivo expanded on amniotic membrane. Cornea. 2008; 27: 327-333.
13. Liu GP, Shu CF, Cui L, Liu W, Cao YL. Tissue-engineered bone formation with cryopreserved human bone mesenchymal stem cells. Cryobiology. 2008; 56: 209-215.
14. Xiang Y, Zheng Q, Jia BB, Huang GP, Xie GG, Pan JJ, Wang JF. Ex vivo expansion, adipogenesis and neurogenesis of cryopreserved human bone marrow mesenchymal stem cells. Cell Bio Int. 2007; 31: 444-450.
15. Buchanan SS, Gross SA, Acker JP, Toner M, Carpenter JF, Pyatt DW. Cryopreservation of stem cells using trehalose: evaluation of the method using a human hematopoietic cell line. Stem Cells Dev. 2004; 13: 29-305.
16. Anchordoguy TJ, Cecchini CA, Crowe JH, Crowe LM. Insights into the cryoprotective mechanism of dimethyl sulfoxide for phospholipid bilayers. Cryobiology. 1991; 28: 467-473.
17. Junior AM, Arrais CA, Saboya R, Velasques RD, Junqueira PL, Dulley FL. Neurotoxicity associated with dimethylsulfoxide-preserved hematopoietic progenitor cell infusion. Bone Marrow Transpl. 2008; 41: 95-96.
18. Windrum P, Morris TCM. Severe neutotoxicity because of dimethyl sulphoxide following peripheral blood stem cell transplantation. Bone Marrow Transpl. 2003; 31: 315-315.
19. Arakawa T, Carpenter JF, Kita YA, Crowe JH. The basis for toxicity of certain cryoprotectants: a hypothesis. Cryobiology. 1990; 27: 401-415.
20. Rodrigues JP, Paraguassu-Braga FH, Carvalho L, Abdelhay E, Bouzas LF, Porto LC. Evaluation of trehalose and sucrose as cryoprotectants for hematopoietic stem cells of umbilical cord blood. Cryobiology. 2008; 56: 144-151.
21. Shahdadfar A, Frønsdal K, Haug T, Reinholt FP, Brinchmanna JE. In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells. 2005; 23: 1357-1366.
22. Lange C, Cakiroglu F, Spiess AN, Cappallo-Obermann H, Dierlamm J, Zander AR. Accelerated and safe expansion of human mesenchymal stromal cell in animal serum-free medium for transplantation and regenerative medicine. J Cell Physiol. 2007; 213: 18-26.
23. Hanslick JL, Lau K, Noguchi KK, Olney JW, Zorumski CF, Mennerick S, Farber NB. Dimethyl sulfoxide (DMSO) produces widespread apoptosis in the developing central nervous system. Neurobiol Dis. 2009; 34: 1-10.
24. Scheinkonig C, Kappicht S, Kolb HJ, Schleuning M. Adoption of long-term cultures to evaluate the cryoprotective potential of trehalose for freezing hematopoietic stem cells. Bone Marrow Transpl. 2004; 34: 531-536.
25. Ma W, O'Shaughnessy T, Chang E. Cryopreservation of adherent neuronal networks. Neurosci Lett. 2006; 403: 84-89.
26. Rosa AD, Francesco FD, Tirino GA, Ferraro GA, Desiderio V, Paino F, Pirozzi G, D'Andrea F, Papaccio G. A new method for cryopreserving adipose-derived stem cells: an attractive and suitable large-scale and long-term cell banking technology. Tissue Eng C. 2009; 15: 1-9.
27. Buchanan SS, Menze MA, Hand SC, Pyatt DW, Carpenter JF. Cryopreservation of human hematopoietic stem and progenitor cells loaded with trehalose: transient permeabilization via the adenosine triphosphate dependent P2Z receptor channel. Cell Preserv Technol. 2005; 3: 212-222.
28. Pugh PA, Aankersmit AE, McGowan LT, Rervit HR. Cryopreservation of in vitro-produced bovine embryos: effects of protein type and concentration during freezing or of liposomes during culture on post-thaw survival. Theriogenology. 1998; 50: 495-506.
29. Leeuw FE, Leeuw AM, Daas JH, Colenbrander B, Verkleij AJ. Effects of various cryoprotective agents and membrane-stabilizing compound on bull sperm membrane integrity after cooling and freezing. Cryobiology. 1993; 30: 32-44.
30. Alvarez JG, Storey BT. Evidence that membrane stress contributes more than lipid peroxidation to sublethal cryodamage in cryopreserved human sperm: glycerol and other polyols as sole cryoprotectants. J Androl. 1993; 14: 199-209.
31. Cabrita E, Anel L, Herraez MP. Effect of external cryoprotectants as membrane stabilizers on cryopreserved rainbow trout sperm. Theriogenology. 2001; 56: 623-635.
32. Bricka M, Bessis M. Sur la conservation des érythrocytes par congélation à basse température en présence de polyvinyl-pyrrolidone et de dextran. C R Seances Soc Biol Fil. 1955; 149: 875-877.
33. Luo KH, Wu GQ, Wang QL, Sun Y, Liu HB. Effect of dimethylsulfoxide and hydroxyethyl starch in the preservation of fractionated human marrow cells. Cryobiology. 1994; 31: 349-354.
34. Clapisson G, Salinas C, Malacher P, Michallet M, Philip I, Philip T. Cryopreservation with hydroxyethylstarch (HES) + dimethylsulfoxide (DMSO) gives better results than DMSO alone. Electroc J Oncol. 1999; 1: 97-102.
35. Fuller BJ. Cryoprotectants: the essential antifreezes to protect life in the frozen state. CryoLetters. 2004; 25: 375-388.
36. Deible C, Petrosko P, Johnson P, Beckman E, Russel A and Wagner W. Molecular barriers to biomaterial thrombosis by modification of surface proteins with polyethylene glycol. Biomaterials. 1999; 20: 101-109.
37. Lu HX, Guo LK, Kawazoe N, Tateishi T, Chen GP. Effects of poly (L-lysine), poly (acrylic acid) and poly (ethylene glycol) on the adhesion, proliferation and chondrogenic differentiation of human mesenchymal stem cells. J Biomat Sci. 2009; 20: 577-589.
38. Fu J, Fiegel J, Krauland E, Hanes J. New polymeric carriers for controlled drug delivery following inhalation or injection. Biomaterials. 2002; 23: 4425-4433.
39. Monroy B, Honiger J, Darquy S, Reach G. Use of polyethyleneglycol for porcine islet cryopreservation. Cell Transplant. 1997; 6: 613-621.
40. Häggman HM, Ryynänen LA, Aronen TS and Krajnakova J. Cryopreservation of embryogenic cultures of Scots pine. Plant Cell Tissue Organ Cult. 1998; 54: 45-53.
41. Davies MG, Huynh TT, Fulton GJ, Svendsen E, Brockbank FG, Hagen PO. Controlling transplant vasculopathy in cryopreserved vein grafts with polyethylene glycol and glutathione during transport. Eur J Vas and Endovasc Surg. 1999; 17: 493-500.
42. Heng BC, Ye CP, Liu H, Toh WS, Rufaihah AJ, Yang Z, Bay BH, Ge Z, Ouyang HW, Lee EH, Cao T. Loss of viability during freeze-thaw of intact and adherent human embryonic stem cells with conventional slow-cooling protocols is predominantly due to apoptosis rather than cellular necrosis. J Biomed Sci. 2006; 13: 433-445.
43. Xu X, Cowley S, Flaim CJ, James W, Cui ZF. Enhancement of cell recovery rate of dissociated human embryonic stem cells after cryopreservation. Biotechnol Prog. 2010; 26: 781-788.
44. Xu X, Cowley S, Flaim CJ, James W, Seymour L, Cui ZF. The roles of apoptotic pathways in the low recovery rate after cryopreservation of dissociated human embryonic stem cells. Biotechnol Prog. 2010; 26: 827-837.
45. Yamato M, Okuhara M, Karikusa F, Kikuchi A, Sakurai Y, Okano T. Signal transduction and cytoskeletal reorganization are required for cell detachment from cell culture surfaces grafted with a temperature-responsive polymer. J Biomed Mater Res. 1999; 44: 44-52.
46. Xu X, Cui ZF, Wilkins RJ, Urban JP. Intracellular pH changes in isolated bovine articular chondrocytes during the loading and removal of cryoprotective agents. Cryobiology. 2003; 46: 161-173.
47. Hayashi T, Hayashi I, Shinohara T, Morishita Y, Nagamura H, Kusunoki Y, Kyoizumi S, Seyama T, Nakachi K. Radiation-induced apoptosis of stem/progenitor cells in human umbilical cord blood is associated with alterations in reactive oxygen and intracellular pH. Mutat Res. 2004; 556: 83-91.
48. Lonergan T, Bavister B, Brenner C. Mitochondria in stem cells. Mitochondrion. 2007; 7: 289-296.
49. Squirrell JM, Schramm RD, Paprocki AM, Wokosin DL, Bavister BD. Imaging mitochondrial organization in living primate oocytes and embryos using multiphoton microscopy. Microsc Microanal. 2003; 9: 190-201.
50. Lonergan T, Brenner C, Bavister B. Differentiation-related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol. 2006; 208: 149-153.
51. Dominici M, Blanc KL, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8: 315-317.
52. Sun XJ, Gan YK, Tang TT, Zhang XL, Dai KR. In vitro proliferation and differentiation of human mesenchymal stem cells cultured in autologous plasma derived from bone marrow. Tissue Eng A. 2008; 14: 391-400.