Human Platelet Lysate Can Replace Fetal Calf Serum as a Protein Source to Promote Expansion and Osteogenic Differentiation of Human Bone-Marrow-Derived Mesenchymal Stromal Cells
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Population Doublings
3.2. Alkaline Phosphatase Activity
3.3. Alizarin Red Staining
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Mendicino, M.; Bailey, A.M.; Wonnacott, K.; Puri, R.K.; Bauer, S.R. MSC-based product characterization for clinical trials: An FDA perspective. Cell Stem Cell 2014, 14, 141–145. [Google Scholar] [CrossRef] [Green Version]
- Price, P.J.; Gregory, E.A. Relationship between in vitro growth promotion and biophysical and biochemical properties of the serum supplement. In Vitro 1982, 18, 576–584. [Google Scholar] [CrossRef]
- Boone, C.W.; Mantel, N.; Caruso, T.D., Jr.; Kazam, E.; Stevenson, R.E. Quality control studies on fetal bovine serum used in tissue culture. In Vitro 1971, 7, 174–189. [Google Scholar] [CrossRef]
- Zheng, X.; Baker, H.; Hancock, W.S.; Fawaz, F.; McCaman, M.; Pungor, E., Jr. Proteomic analysis for the assessment of different lots of fetal bovine serum as a raw material for cell culture. Part IV. Application of proteomics to the manufacture of biological drugs. Biotechnol. Prog. 2006, 22, 1294–1300. [Google Scholar] [CrossRef]
- Sundin, M.; Ringden, O.; Sundberg, B.; Nava, S.; Gotherstrom, C.; Le Blanc, 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. [Google Scholar] [CrossRef]
- Knepper, P.A.; Mayanil, C.S.; Goossens, W.; McLone, D.C.; Hayes, E. The presence of transcription factors in fetal bovine sera. In Vitro Cell. Dev. Biol. Anim. 1998, 34, 170–173. [Google Scholar] [CrossRef]
- Gstraunthaler, G. Alternatives to the use of fetal bovine serum: Serum-free cell culture. Altex 2003, 20, 275–281. [Google Scholar]
- Baker, H.; DeAngelis, B.; Frank, O. Vitamins and other metabolites in various sera commonly used for cell culturing. Experientia 1988, 44, 1007–1010. [Google Scholar] [CrossRef]
- Psychogios, N.; Hau, D.D.; Peng, J.; Guo, A.C.; Mandal, R.; Bouatra, S.; Sinelnikov, I.; Krishnamurthy, R.; Eisner, R.; Gautam, B.; et al. The human serum metabolome. PLoS ONE 2011, 6, e16957. [Google Scholar] [CrossRef] [Green Version]
- Anderson, N.L.; Anderson, N.G. The human plasma proteome: History, character, and diagnostic prospects. Mol. Cell. Proteom. MCP 2002, 1, 845–867. [Google Scholar] [CrossRef] [Green Version]
- Shanskii, Y.D.; Sergeeva, N.S.; Sviridova, I.K.; Kirakozov, M.S.; Kirsanova, V.A.; Akhmedova, S.A.; Antokhin, A.I.; Chissov, V.I. Human platelet lysate as a promising growth-stimulating additive for culturing of stem cells and other cell types. Bull. Exp. Biol. Med. 2013, 156, 146–151. [Google Scholar] [CrossRef]
- 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. ATLA 2002, 30, 219–227. [Google Scholar] [CrossRef]
- Schallmoser, K.; Henschler, R.; Gabriel, C.; Koh, M.B.C.; Burnouf, T. Production and Quality Requirements of Human Platelet Lysate: A Position Statement from the Working Party on Cellular Therapies of the International Society of Blood Transfusion. Trends Biotechnol. 2020, 38, 13–23. [Google Scholar] [CrossRef]
- Rendu, F.; Brohard-Bohn, B. The platelet release reaction: Granules’ constituents, secretion and functions. Platelets 2001, 12, 261–273. [Google Scholar] [CrossRef]
- Nurden, A.T.; Nurden, P.; Sanchez, M.; Andia, I.; Anitua, E. Platelets and wound healing. Front. Biosci. J. Virtual Libr. 2008, 13, 3532–3548. [Google Scholar] [CrossRef]
- Schallmoser, K.; Bartmann, C.; Rohde, E.; Reinisch, A.; Kashofer, K.; Stadelmeyer, E.; Drexler, C.; Lanzer, G.; Linkesch, W.; Strunk, D. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 2007, 47, 1436–1446. [Google Scholar] [CrossRef]
- Bieback, K.; Hecker, A.; Kocaomer, A.; Lannert, H.; Schallmoser, K.; Strunk, D.; Kluter, H. Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 2009, 27, 2331–2341. [Google Scholar] [CrossRef]
- Viau, S.; Lagrange, A.; Chabrand, L.; Lorant, J.; Charrier, M.; Rouger, K.; Alvarez, I.; Eap, S.; Delorme, B. A highly standardized and characterized human platelet lysate for efficient and reproducible expansion of human bone marrow mesenchymal stromal cells. Cytotherapy 2019, 21, 738–754. [Google Scholar] [CrossRef]
- Kark, L.R.; Karp, J.M.; Davies, J.E. Platelet releasate increases the proliferation and migration of bone marrow-derived cells cultured under osteogenic conditions. Clin. Oral Implant. Res. 2006, 17, 321–327. [Google Scholar] [CrossRef]
- Hemeda, H.; Giebel, B.; Wagner, W. Evaluation of human platelet lysate versus fetal bovine serum for culture of mesenchymal stromal cells. Cytotherapy 2014, 16, 170–180. [Google Scholar] [CrossRef] [Green Version]
- Doucet, C.; Ernou, I.; Zhang, Y.; Llense, J.R.; Begot, L.; Holy, X.; Lataillade, J.J. Platelet lysates promote mesenchymal stem cell expansion: A safety substitute for animal serum in cell-based therapy applications. J. Cell. Physiol. 2005, 205, 228–236. [Google Scholar] [CrossRef] [PubMed]
- Barro, L.; Su, Y.T.; Nebie, O.; Wu, Y.W.; Huang, Y.H.; Koh, M.B.; Knutson, F.; Burnouf, T. A double-virally-inactivated (Intercept-solvent/detergent) human platelet lysate for in vitro expansion of human mesenchymal stromal cells. Transfusion 2019, 59, 2061–2073. [Google Scholar] [CrossRef] [PubMed]
- Xia, W.; Li, H.; Wang, Z.; Xu, R.; Fu, Y.; Zhang, X.; Ye, X.; Huang, Y.; Xiang, A.P.; Yu, W. Human platelet lysate supports ex vivo expansion and enhances osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. Cell Biol. Int. 2011, 35, 639–643. [Google Scholar] [CrossRef]
- Prins, H.J.; Rozemuller, H.; Vonk-Griffioen, S.; Verweij, V.G.; Dhert, W.J.; Slaper-Cortenbach, I.C.; Martens, A.C. Bone-forming capacity of mesenchymal stromal cells when cultured in the presence of human platelet lysate as substitute for fetal bovine serum. Tissue Eng. Part A 2009, 15, 3741–3751. [Google Scholar] [CrossRef]
- Lohmann, M.; Walenda, G.; Hemeda, H.; Joussen, S.; Drescher, W.; Jockenhoevel, S.; Hutschenreuter, G.; Zenke, M.; Wagner, W. Donor age of human platelet lysate affects proliferation and differentiation of mesenchymal stem cells. PLoS ONE 2012, 7, e37839. [Google Scholar] [CrossRef]
- Horn, P.; Bokermann, G.; Cholewa, D.; Bork, S.; Walenda, T.; Koch, C.; Drescher, W.; Hutschenreuther, G.; Zenke, M.; Ho, A.D.; et al. Impact of individual platelet lysates on isolation and growth of human mesenchymal stromal cells. Cytotherapy 2010, 12, 888–898. [Google Scholar] [CrossRef]
- Chevallier, N.; Anagnostou, F.; Zilber, S.; Bodivit, G.; Maurin, S.; Barrault, A.; Bierling, P.; Hernigou, P.; Layrolle, P.; Rouard, H. Osteoblastic differentiation of human mesenchymal stem cells with platelet lysate. Biomaterials 2010, 31, 270–278. [Google Scholar] [CrossRef]
- Capelli, C.; Domenghini, M.; Borleri, G.; Bellavita, P.; Poma, R.; Carobbio, A.; Mico, C.; Rambaldi, A.; Golay, J.; Introna, M. Human platelet lysate allows expansion and clinical grade production of mesenchymal stromal cells from small samples of bone marrow aspirates or marrow filter washouts. Bone Marrow Transplant. 2007, 40, 785–791. [Google Scholar] [CrossRef]
- Ben Azouna, N.; Jenhani, F.; Regaya, Z.; Berraeis, L.; Ben Othman, T.; Ducrocq, E.; Domenech, J. Phenotypical and functional characteristics of mesenchymal stem cells from bone marrow: Comparison of culture using different media supplemented with human platelet lysate or fetal bovine serum. Stem Cell Res. Ther. 2012, 3, 6. [Google Scholar] [CrossRef] [Green Version]
- Brun, J.; Abruzzese, T.; Rolauffs, B.; Aicher, W.K.; Hart, M.L. Choice of xenogenic-free expansion media significantly influences the myogenic differentiation potential of human bone marrow-derived mesenchymal stromal cells. Cytotherapy 2016, 18, 344–359. [Google Scholar] [CrossRef]
- Boraldi, F.; Burns, J.S.; Bartolomeo, A.; Dominici, M.; Quaglino, D. Mineralization by mesenchymal stromal cells is variously modulated depending on commercial platelet lysate preparations. Cytotherapy 2018, 20, 335–342. [Google Scholar] [CrossRef] [Green Version]
- Riis, S.; Nielsen, F.M.; Pennisi, C.P.; Zachar, V.; Fink, T. Comparative Analysis of Media and Supplements on Initiation and Expansion of Adipose-Derived Stem Cells. Stem Cells Transl. Med. 2016, 5, 314–324. [Google Scholar] [CrossRef]
- Pachler, K.; Lener, T.; Streif, D.; Dunai, Z.A.; Desgeorges, A.; Feichtner, M.; Oller, M.; Schallmoser, K.; Rohde, E.; Gimona, M. A Good Manufacturing Practice-grade standard protocol for exclusively human mesenchymal stromal cell-derived extracellular vesicles. Cytotherapy 2017, 19, 458–472. [Google Scholar] [CrossRef] [Green Version]
- Mohammadi, S.; Nikbakht, M.; Malek Mohammadi, A.; Zahed Panah, M.; Ostadali, M.R.; Nasiri, H.; Ghavamzadeh, A. Human Platelet Lysate as a Xeno Free Alternative of Fetal Bovine Serum for the In Vitro Expansion of Human Mesenchymal Stromal Cells. Int. J. Hematol.-Oncol. Stem Cell Res. 2016, 10, 161–171. [Google Scholar]
- Schmitz, S.I.; Widholz, B.; Essers, C.; Becker, M.; Tulyaganov, D.U.; Moghaddam, A.; Gonzalo de Juan, I.; Westhauser, F. Superior biocompatibility and comparable osteoinductive properties: Sodium-reduced fluoride-containing bioactive glass belonging to the CaO-MgO-SiO2 system as a promising alternative to 45S5 bioactive glass. Bioact. Mater. 2020, 5, 55–65. [Google Scholar] [CrossRef]
- Widholz, B.; Tsitlakidis, S.; Reible, B.; Moghaddam, A.; Westhauser, F. Pooling of Patient-Derived Mesenchymal Stromal Cells Reduces Inter-Individual Confounder-Associated Variation without Negative Impact on Cell Viability, Proliferation and Osteogenic Differentiation. Cells 2019, 8, 633. [Google Scholar] [CrossRef] [Green Version]
- Reible, B.; Schmidmaier, G.; Moghaddam, A.; Westhauser, F. Insulin-Like Growth Factor-1 as a Possible Alternative to Bone Morphogenetic Protein-7 to Induce Osteogenic Differentiation of Human Mesenchymal Stem Cells in Vitro. Int. J. Mol. Sci. 2018, 19, 1674. [Google Scholar] [CrossRef] [Green Version]
- Reible, B.; Schmidmaier, G.; Prokscha, M.; Moghaddam, A.; Westhauser, F. Continuous stimulation with differentiation factors is necessary to enhance osteogenic differentiation of human mesenchymal stem cells in-vitro. Growth Factors 2017, 35, 179–188. [Google Scholar] [CrossRef]
- More, S.J.; Bicout, D.J.; Bøtner, A.; Butterworth, A.; Calistri, P.; Depner, K.R.; Edwards, S.A.; Garin-Bastuji, B.; Good, M.; Schmidt, C.G.; et al. Animal welfare aspects in respect of the slaughter or killing of pregnant livestock animals (cattle, pigs, sheep, goats, horses). EFSA J. 2017, 15, e04782. [Google Scholar]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Gstraunthaler, G.; Lindl, T.; van der Valk, J. A plea to reduce or replace fetal bovine serum in cell culture media. Cytotechnology 2013, 65, 791–793. [Google Scholar] [CrossRef] [Green Version]
- Strunk, D.; Lozano, M.; Marks, D.C.; Loh, Y.S.; Gstraunthaler, G.; Schennach, H.; Rohde, E.; Laner-Plamberger, S.; Oller, M.; Nystedt, J.; et al. International Forum on GMP-grade human platelet lysate for cell propagation: Summary. Vox Sang. 2018, 113, 80–87. [Google Scholar] [CrossRef]
- Pierce, J.; Benedetti, E.; Preslar, A.; Jacobson, P.; Jin, P.; Stroncek, D.F.; Reems, J.A. Comparative analyses of industrial-scale human platelet lysate preparations. Transfusion 2017, 57, 2858–2869. [Google Scholar] [CrossRef]
- Fernandez-Rebollo, E.; Mentrup, B.; Ebert, R.; Franzen, J.; Abagnale, G.; Sieben, T.; Ostrowska, A.; Hoffmann, P.; Roux, P.F.; Rath, B.; et al. Human Platelet Lysate versus Fetal Calf Serum: These Supplements Do Not Select for Different Mesenchymal Stromal Cells. Sci. Rep. 2017, 7, 5132. [Google Scholar] [CrossRef]
- Schallmoser, K.; Strunk, D. Preparation of pooled human platelet lysate (pHPL) as an efficient supplement for animal serum-free human stem cell cultures. J. Vis. Exp. JoVE 2009. [Google Scholar] [CrossRef] [Green Version]
- Dominici, M.; Le Blanc, K.; 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. [Google Scholar] [CrossRef]
- Reis, M.; McDonald, D.; Nicholson, L.; Godthardt, K.; Knobel, S.; Dickinson, A.M.; Filby, A.; Wang, X.N. Global phenotypic characterisation of human platelet lysate expanded MSCs by high-throughput flow cytometry. Sci. Rep. 2018, 8, 3907. [Google Scholar] [CrossRef]
- Birmingham, E.; Niebur, G.L.; McHugh, P.E.; Shaw, G.; Barry, F.P.; McNamara, L.M. Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur. Cells Mater. 2012, 23, 13–27. [Google Scholar] [CrossRef]
- Westhauser, F.; Widholz, B.; Nawaz, Q.; Tsitlakidis, S.; Hagmann, S.; Moghaddam, A.; Boccaccini, A.R. Favorable angiogenic properties of the borosilicate bioactive glass 0106-B1 result in enhanced in vivo osteoid formation compared to 45S5 Bioglass. Biomater. Sci. 2019, 7, 5161–5176. [Google Scholar] [CrossRef]
- Aubin, J.E. Regulation of osteoblast formation and function. Rev. Endocr. Metab. Disord. 2001, 2, 81–94. [Google Scholar] [CrossRef]
- Hoemann, C.D.; El-Gabalawy, H.; McKee, M.D. In vitro osteogenesis assays: Influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol. Biol. 2009, 57, 318–323. [Google Scholar] [CrossRef] [PubMed]
- Huang, Z.; Nelson, E.R.; Smith, R.L.; Goodman, S.B. The sequential expression profiles of growth factors from osteoprogenitors [correction of osteroprogenitors] to osteoblasts in vitro. Tissue Eng. 2007, 13, 2311–2320. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Pons, M.; Nagel, G.; Zeyn, Y.; Beyer, M.; Laguna, T.; Brachetti, T.; Sellmer, A.; Mahboobi, S.; Conradi, R.; Butter, F.; et al. Human platelet lysate as validated replacement for animal serum to assess chemosensitivity. Altex 2019, 36, 277–288. [Google Scholar] [CrossRef] [Green Version]
Group | Protein Source and Concentration in ESM | Protein Source and Concentration in ODM |
---|---|---|
F1 | FCS 10% | FCS 1% |
F10 | FCS 10% | FCS 10% |
H1 | hPL 10% | hPL 1% |
H10 | hPL 10% | hPL 10% |
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Karadjian, M.; Senger, A.-S.; Essers, C.; Wilkesmann, S.; Heller, R.; Fellenberg, J.; Simon, R.; Westhauser, F. Human Platelet Lysate Can Replace Fetal Calf Serum as a Protein Source to Promote Expansion and Osteogenic Differentiation of Human Bone-Marrow-Derived Mesenchymal Stromal Cells. Cells 2020, 9, 918. https://doi.org/10.3390/cells9040918
Karadjian M, Senger A-S, Essers C, Wilkesmann S, Heller R, Fellenberg J, Simon R, Westhauser F. Human Platelet Lysate Can Replace Fetal Calf Serum as a Protein Source to Promote Expansion and Osteogenic Differentiation of Human Bone-Marrow-Derived Mesenchymal Stromal Cells. Cells. 2020; 9(4):918. https://doi.org/10.3390/cells9040918
Chicago/Turabian StyleKaradjian, Maria, Anne-Sophie Senger, Christopher Essers, Sebastian Wilkesmann, Raban Heller, Joerg Fellenberg, Rolf Simon, and Fabian Westhauser. 2020. "Human Platelet Lysate Can Replace Fetal Calf Serum as a Protein Source to Promote Expansion and Osteogenic Differentiation of Human Bone-Marrow-Derived Mesenchymal Stromal Cells" Cells 9, no. 4: 918. https://doi.org/10.3390/cells9040918