Evaluation of human platelet lysate versus fetal bovine serum for culture of mesenchymal stromal cells

Cytotherapy

Volumn 16, Issue 2, 2014, Pages 170-180

  Hemeda, Hatim ^a   Giebel, Bernd ^b   Wagner, Wolfgang ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Fetal bovine serum; Fetal calf serum; Mesenchymal stromal cells; Platelet lysate; Platelet lysate gel; Serum

Indexed keywords

GROWTH FACTOR; HEPARIN;

BIOSAFETY; CELL ACTIVITY; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL EXPANSION; CELL LYSATE; CELL PROLIFERATION; CELL VIABILITY; CHEMICAL COMPOSITION; CULTURE MEDIUM; EXOSOME; FETAL BOVINE SERUM; GELATINIZATION; GOLD STANDARD; HUMAN; HUMAN PLATELET LYSATE; MESENCHYMAL STROMA CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SERUM; THROMBOCYTE MEMBRANE;

FETAL BOVINE SERUM; FETAL CALF SERUM; MESENCHYMAL STROMAL CELLS; PLATELET LYSATE; PLATELET LYSATE GEL; SERUM;

ANIMALS; BLOOD PLATELETS; CATTLE; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL EXTRACTS; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; HUMANS; INFANT, NEWBORN; MESENCHYMAL STROMAL CELLS; SERUM;

EID: 84892462714     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2013.11.004     Document Type: Review

References (98)

1. Eagle H. Nutrition needs of mammalian cells in tissue culture. Science 1955, 122:501-514.
2. 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, 8:315-317.
3. Horwitz E.M., Le B.K., Dominici M., Mueller I., Slaper-Cortenbach I., Marini F.C., et al. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy 2005, 7:393-395.
4. Lazarus H.M., Haynesworth S.E., Gerson S.L., Rosenthal N.S., Caplan A.I. 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, 16:557-564.
5. Barnes D., Sato G. Methods for growth of cultured cells in serum-free medium. Anal Biochem 1980, 102:255-270.
6. Bjare U. Serum-free cell culture. Pharmacol Ther 1992, 53:355-374.
7. Froud S.J. The development, benefits and disadvantages of serum-free media. Dev Biol Stand 1999, 99:157-166.
8. Gstraunthaler G. Alternatives to the use of fetal bovine serum: serum-free cell culture. ALTEX 2003, 20:275-281.
9. Jayme D.W., Epstein D.A., Conrad D.R. Fetal bovine serum alternatives. Nature 1988, 334:547-548.
10. Zimmerman A.M., Vierck J.L., O'Reilly B.A., Dodson M.V. Formulation of a defined medium to maintain cell health and viability in vitro. Methods Cell Sci 2000, 22:43-49.
11. Chase L.G., Yang S., Zachar V., Yang Z., Lakshmipathy U., Bradford J., et al. Development and characterization of a clinically compliant xeno-free culture medium in good manufacturing practice for human multipotent mesenchymal stem cells. Stem Cells Transl Med 2012, 1:750-758.
12. Patrikoski M., Juntunen M., Boucher S., Campbell A., Vemuri M.C., Mannerstrom B., et al. Development of fully defined xeno-free culture system for the preparation and propagation of cell therapy-compliant human adipose stem cells. Stem Cell Res Ther 2013, 4:27.
13. Chase L.G., Lakshmipathy U., Solchaga L.A., Rao M.S., Vemuri M.C. Anovel serum-free medium for the expansion of human mesenchymal stem cells. Stem Cell Res Ther 2010, 1:8.
14. Barnes D., Sato G. Serum-free cell culture: a unifying approach. Cell 1980, 22:649-655.
15. Hodgson J. To treat or not to treat: that is the question for serum. Biotechnology 1995, 13:333-338.
16. Jochems C.E., van der Valk J.B., Stafleu F.R., Baumans V. The use of fetal bovine serum: ethical or scientific problem?. Altern Lab Anim 2002, 30:219-227.
17. Tekkatte C., Gunasingh G.P., Cherian K.M., Sankaranarayanan K. "Humanized" stem cell culture techniques: the animal serum controversy. Stem Cells Int 2011, 2011:504723.
18. Sundin M., Ringden O., Sundberg B., Nava S., Gotherstrom C., Le B.K. No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients. Haematologica 2007, 92:1208-1215.
19. Horwitz E.M., Gordon P.L., Koo W.K., Marx J.C., Neel M.D., McNall R.Y., et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci U S A 2002, 99:8932-8937.
20. Gospodarowicz D., Ferrara N., Schweigerer L., Neufeld G. Structural characterization and biological functions of fibroblast growth factor. Endocr Rev 1987, 8:95-114.
21. Heldin C.H., Betsholtz C., Johnsson A., Nister M., Ek B., Ronnstrand L., et al. Platelet-derived growth factor: mechanism of action and relation to oncogenes. JCell Sci Suppl 1985, 3:65-76.
22. Carpenter G., Cohen S. Epidermal growth factor. Annu Rev Biochem 1979, 48:193-216.
23. Cohen S. Epidermal growth factor. In Vitro Cell Dev Biol 1987, 23:239-246.
24. van der Valk J., Mellor D., Brands R., Fischer R., Gruber F., Gstraunthaler G., et al. The humane collection of fetal bovine serum and possibilities for serum-free cell and tissue culture. Toxicol In Vitro 2004, 18:1-12.
25. Even M.S., Sandusky C.B., Barnard N.D. Serum-free hybridoma culture: ethical, scientific and safety considerations. Trends Biotechnol 2006, 24:105-108.
26. Spees J.L., Gregory C.A., Singh H., Tucker H.A., Peister A., Lynch P.J., et al. Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol Ther 2004, 9:747-756.
27. Selvaggi T.A., Walker R.E., Fleisher T.A. Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 1997, 89:776-779.
28. Mackensen A., Drager R., Schlesier M., Mertelsmann R., Lindemann A. Presence of IgE antibodies to bovine serum albumin in a patient developing anaphylaxis after vaccination with human peptide-pulsed dendritic cells. Cancer Immunol Immunother 2000, 49:152-156.
29. Tonti G.A., Mannello F. From bone marrow to therapeutic applications: different behaviour and genetic/epigenetic stability during mesenchymal stem cell expansion in autologous and foetal bovine sera?. Int J Dev Biol 2008, 52:1023-1032.
30. Erickson G.A., Bolin S.R., Landgraf J.G. Viral contamination of fetal bovine serum used for tissue culture: risks and concerns. Dev Biol Stand 1991, 75:173-175.
31. Mellor D.J., Gregory N.G. Responsiveness, behavioural arousal and awareness in fetal and newborn lambs: experimental, practical and therapeutic implications. NZ Vet J 2003, 51:2-13.
32. Halme D.G., Kessler D.A. FDA regulation of stem-cell-based therapies. NEngl J Med 2006, 355:1730-1735.
33. Bieback K., Hecker A., Kocaomer A., Lannert H., Schallmoser K., Strunk D., et al. Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 2009, 27:2331-2341.
34. Kocaoemer A., Kern S., Kluter H., Bieback K. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 2007, 25:1270-1278.
35. Stute N., Holtz K., Bubenheim M., Lange C., Blake F., Zander A.R. Autologous serum for isolation and expansion of human mesenchymal stem cells for clinical use. Exp Hematol 2004, 32:1212-1225.
36. Koller M.R., Maher R.J., Manchel I., Oxender M., Smith A.K. Alternatives to animal sera for human bone marrow cell expansion: human serum and serum-free media. JHematother 1998, 7:413-423.
37. Yamaguchi M., Hirayama F., Wakamoto S., Fujihara M., Murahashi H., Sato N., et al. Bone marrow stromal cells prepared using AB serum and bFGF for hematopoietic stem cells expansion. Transfusion 2002, 42:921-927.
38. Vogel J.P., Szalay K., Geiger F., Kramer M., Richter W., Kasten P. Platelet-rich plasma improves expansion of human mesenchymal stem cells and retains differentiation capacity and in vivo bone formation in calcium phosphate ceramics. Platelets 2006, 17:462-469.
39. Nesselmann C., Ma N., Bieback K., Wagner W., Ho A., Konttinen Y.T., et al. Mesenchymal stem cells and cardiac repair. JCell Mol Med 2008, 12:1795-1810.
40. Marx R.E. Platelet-rich plasma: evidence to support its use. JOral Maxillofac Surg 2004, 62:489-496.
41. Müller I., Kordowich S., Holzwarth C., Spano C., Isensee G., Staiber A., et al. Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM. Cytotherapy 2006, 8:437-444.
42. Ng F., Boucher S., Koh S., Sastry K.S., Chase L., Lakshmipathy U., et al. PDGF, TGF-beta, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 2008, 112:295-307.
43. Senger D.R., Perruzzi C.A., Papadopoulos-Sergiou A., Van de W.L. Adhesive properties of osteopontin: regulation by a naturally occurring thrombin-cleavage in close proximity to the GRGDS cell-binding domain. Mol Biol Cell 1994, 5:565-574.
44. Doucet C., Ernou I., Zhang Y., Llense J.R., Begot L., Holy X., et al. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. JCell Physiol 2005, 205:228-236.
45. von Bonin M., Stolzel F., Goedecke A., Richter K., Wuschek N., Holig K., et al. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysate-containing medium. Bone Marrow Transplant 2009, 43:245-251.
46. Rauch C., Feifel E., Amann E.M., Spotl H.P., Schennach H., Pfaller W., et al. Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media. ALTEX 2011, 28:305-316.
47. Schallmoser K., Bartmann C., Rohde E., Reinisch A., Kashofer K., Stadelmeyer E., et al. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 2007, 47:1436-1446.
48. Horn P., Bokermann G., Cholewa D., Bork S., Walenda T., Koch C., et al. Impact of individual platelet lysates on isolation and growth of human mesenchymal stromal cells. Cytotherapy 2010, 12:888-898.
49. Schallmoser K., Strunk D. Preparation of pooled human platelet lysate (pHPL) as an efficient supplement for animal serum-free human stem cell cultures. JVis Exp 2009, 32:1523.
50. Schallmoser K., Strunk D. Generation of a pool of human platelet lysate and efficient use in cell culture. Methods Mol Biol 2013, 946:349-362.
51. Capelli C., Domenghini M., Borleri G., Bellavita P., Poma R., Carobbio A., et al. Human platelet lysate allows expansion and clinical grade production of mesenchymal stromal cellsfrom small samples of bone marrow aspirates or marrow filter washouts. Bone Marrow Transplant 2007, 40:785-791.
52. Holzwarth C., Vaegler M., Gieseke F., Pfister S.M., Handgretinger R., Kerst G., et al. Low physiologic oxygen tensions reduce proliferation and differentiation of human multipotent mesenchymal stromal cells. BMC Cell Biol 2010, 11:11.
53. Lange C., Cakiroglu F., Spiess A.N., Cappallo-Obermann H., Dierlamm J., Zander A.R. Accelerated and safe expansion of human mesenchymal stromal cells in animal serum-free medium for transplantation and regenerative medicine. JCell Physiol 2007, 213:18-26.
54. Denecke B., Horsch L.D., Radtke S., Fischer J.C., Horn P.A., Giebel B. Human endothelial colony-forming cells expanded with an improved protocol are a useful endothelial cell source for scaffold-based tissue engineering. JTissue Eng Regen Med 2013, [Epub ahead of print].
55. Kilian O., Flesch I., Wenisch S., Taborski B., Jork A., Schnettler R., et al. Effects of platelet growth factors on human mesenchymal stem cells and human endothelial cells in vitro. Eur J Med Res 2004, 9:337-344.
56. Mirabet V., Solves P., Minana M.D., Encabo A., Carbonell-Uberos F., Blanquer A., et al. Human platelet lysate enhances the proliferative activity of cultured human fibroblast-like cells from different tissues. Cell Tissue Bank 2008, 9:1-10.
57. Bernardo M.E., Avanzini M.A., Perotti C., Cometa A.M., Moretta A., Lenta E., et al. Optimization of in vitro expansion of human multipotent mesenchymal stromal cells for cell-therapy approaches: further insights in the search for a fetal calf serum substitute. JCell Physiol 2007, 211:121-130.
58. Lohmann M., Walenda G., Hemeda H., Joussen S., Drescher W., Jockenhoevel S., et al. Donor age of human platelet lysate affects proliferation and differentiation of mesenchymal stem cells. PLoS One 2012, 7:e37839.
59. Cholewa D., Stiehl T., Schellenberg A., Bokermann G., Joussen S., Koch C., et al. Expansion of adipose mesenchymal stromal cells is affected by human platelet lysate and plating density. Cell Transplant 2011, 20:1409-1422.
60. Walenda G., Hemeda H., Schneider R.K., Merkel R., Hoffmann B., Wagner W. Human platelet lysate gel provides a novel 3D-matrix for enhanced culture expansion of mesenchymal stromal cells. Tissue Eng Part C Methods 2012, 18:924-934.
61. Chan R.K., Liu P., Lew D.H., Ibrahim S.I., Srey R., Valeri C.R., et al. Expired liquid preserved platelet releasates retain proliferative activity. JSurg Res 2005, 126:55-58.
62. Sanchez A.R., Sheridan P.J., Kupp L.I. Is platelet-rich plasma the perfect enhancement factor? A current review. Int J Oral Maxillofac Implants 2003, 18:93-103.
63. Dugrillon A., Eichler H., Kern S., Kluter H. Autologous concentrated platelet-rich plasma (cPRP) for local application in bone regeneration. Int J Oral Maxillofac Surg 2002, 31:615-619.
64. Johansson L., Klinth J., Holmqvist O., Ohlson S. Platelet lysate: a replacement for fetal bovine serum in animal cell culture?. Cytotechnology 2003, 42:67-74.
65. Fekete N., Gadelorge M., Furst D., Maurer C., Dausend J., Fleury-Cappellesso S., et al. Platelet lysate from whole blood-derived pooled platelet concentrates and apheresis-derived platelet concentrates for the isolation and expansion of human bone marrow mesenchymal stromal cells: production process, content and identification of active components. Cytotherapy 2012, 14:540-554.
66. Kaplan D.R., Chao F.C., Stiles C.D., Antoniades H.N., Scher C.D. Plateletalpha granules contain a growth factor for fibroblasts. Blood 1979, 53:1043-1052.
67. Ledent E., Wasteson A., Berlin G. Growth factor release during preparation and storage of platelet concentrates. Vox Sang 1995, 68:205-209.
68. King S.M., Reed G.L. Development of platelet secretory granules. Semin Cell Dev Biol 2002, 13:293-302.
69. Reed G.L., Fitzgerald M.L., Polgar J. Molecular mechanisms of platelet exocytosis: insights into the "secrete" life of thrombocytes. Blood 2000, 96:3334-3342.
70. Marx R.E., Carlson E.R., Eichstaedt R.M., Schimmele S.R., Strauss J.E., Georgeff K.R. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998, 85:638-646.
71. Anitua E., Andia I., Ardanza B., Nurden P., Nurden A.T. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost 2004, 91:4-15.
72. Coppinger J.A., Cagney G., Toomey S., Kislinger T., Belton O., McRedmond J.P., et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood 2004, 103:2096-2104.
73. Walenda G., Abnaof K., Joussen S., Meurer S., Smeets H., Rath B., et al. TGF-beta1 does not induce senescence of multipotent mesenchymal stromal cells and has similar effects in early and late passages. PLoS One 2013, 8:e77656.
74. Sipe J.B., Zhang J., Waits C., Skikne B., Garimella R., Anderson H.C. Localization of bone morphogenetic proteins (BMPs)-2, -4, and -6 within megakaryocytes and platelets. Bone 2004, 35:1316-1322.
75. van den D.J., Mooren R., Vloon A.P., Stoelinga P.J., Jansen J.A. Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng 2006, 12:3067-3073.
76. Koch H., Jadlowiec J.A., Campbell P.G. Insulin-like growth factor-I induces early osteoblast gene expression in human mesenchymal stem cells. Stem Cells Dev 2005, 14:621-631.
77. Bissels U., Bosio A., Wagner W. MicroRNAs are shaping the hematopoietic landscape. Haematologica 2012, 97:160-167.
78. Bork S., Horn P., Castoldi M., Hellwig I., Ho A.D., Wagner W. Adipogenic differentiation of human mesenchymal stromal cells is down-regulated by microRNA-369-5p and up-regulated by microRNA-371. JCell Physiol 2011, 226:2226-2234.
79. Laine S.K., Hentunen T., Laitala-Leinonen T. Do microRNAs regulate bone marrow stem cell niche physiology?. Gene 2012, 497:1-9.
80. Heijnen H.F., Schiel A.E., Fijnheer R., Geuze H.J., Sixma J.J. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999, 94:3791-3799.
81. Johnstone R.M., Adam M., Hammond J.R., Orr L., Turbide C. Vesicle formation during reticulocyte maturation: association of plasma membrane activities with released vesicles (exosomes). JBiol Chem 1987, 262:9412-9420.
82. Ludwig A.K., Giebel B. Exosomes: small vesicles participating in intercellular communication. Int J Biochem Cell Biol 2012, 44:11-15.
83. Schorey J.S., Bhatnagar S. Exosome function: from tumor immunology to pathogen biology. Traffic 2008, 9:871-881.
84. Sinauridze E.I., Kireev D.A., Popenko N.Y., Pichugin A.V., Panteleev M.A., Krymskaya O.V., et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost 2007, 97:425-434.
85. Pienimaeki-Roemer A., Ruebsaamen K., Boettcher A., Orso E., Scherer M., Liebisch G., et al. Stored platelets alter glycerophospholipid and sphingolipid species, which are differentially transferred to newly released extracellular vesicles. Transfusion 2013, 53:612-626.
86. Wagner W., Bork S., Lepperdinger G., Joussen S., Ma N., Strunk D., et al. How to track cellular aging of mesenchymal stromal cells?. Aging 2010, 2:224-230.
87. Wagner W., Ho A.D., Zenke M. Different facets of aging in human mesenchymal stem cells. Tissue Eng Part B Rev 2010, 16:445-453.
88. Schellenberg A., Lin Q., Schuler H., Koch C.M., Joussen S., Denecke B., et al. Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging 2011, 3:873-888.
89. Schallmoser K., Bartmann C., Rohde E., Bork S., Guelly C., Obenauf A.C., et al. Replicative senescence-associated gene expression changes in mesenchymal stromal cells are similar under different culture conditions. Haematologica 2010, 95:867-874.
90. Koch C.M., Joussen S., Schellenberg A., Lin Q., Zenke M., Wagner W. Monitoring of cellular senescence by DNA-methylation at specific CpG sites. Aging Cell 2012, 11:366-369.
91. Kruman I.I., Miakisheva S.N., Gavriliuk B.K. Age-related changes in the growth-stimulating effect of serum on BHK-21 cells. Tsitologiia 1984, 26:1043-1047.
92. Andersen J.C. Advances in anticoagulation therapy: the role of selective inhibitors of factor Xa and thrombin in thromboprophylaxis after major orthopedic surgery. Semin Thromb Hemost 2004, 30:609-618.
93. Hemeda H., Kalz J., Walenda G., Lohmann M., Wagner W. Heparin concentration is critical for cell culture with human platelet lysate. Cytotherapy 2013, 15:1174-1181.
94. Toh W.S., Lim T.C., Kurisawa M., Spector M. Modulation of mesenchymal stem cell chondrogenesis in a tunable hyaluronic acid hydrogel microenvironment. Biomaterials 2012, 33:3835-3845.
95. Leisten I., Kramann R., Ventura Ferreira M.S., Bovi M., Neuss S., Ziegler P., et al. 3D co-culture of hematopoietic stem and progenitor cells and mesenchymal stem cells in collagen scaffolds as a model of the hematopoietic niche. Biomaterials 2012, 33:1736-1747.
96. Jockenhoevel S., Zund G., Hoerstrup S.P., Chalabi K., Sachweh J.S., Demircan L., et al. Fibrin gel: advantages of a new scaffold in cardiovascular tissue engineering. Eur J Cardiothorac Surg 2001, 19:424-430.
97. Bensaid W., Triffitt J.T., Blanchat C., Oudina K., Sedel L., Petite H. Abiodegradable fibrin scaffold for mesenchymal stem cell transplantation. Biomaterials 2003, 24:2497-2502.
98. Schallmoser K., Rohde E., Reinisch A., Bartmann C., Thaler D., Drexler C., et al. Rapid large-scale expansion of functional mesenchymal stem cells from unmanipulated bone marrow without animal serum. Tissue Eng Part C Methods 2008, 14:185-196.