Abstract
Menstrual blood has been recognized as an easily accessible and inexpensive source of stem cells, in recent years. To establish a safe and efficient protocol for development of menstrual blood-derived stem cells (MenSCs) into osteoblasts, the effect of substitution of fetal bovine serum (FBS) with human platelet derivatives (HPDs) was evaluated during proliferation and osteogenic differentiation of MenSCs. To this aim, parallel experiments were carried out on cultured MenSCs in the presence of platelet-rich plasma, platelet-poor plasma, platelet gel supernatant, or human platelet releasate (HPR), and compared with cells cultured in conventional growth medium containing FBS. There was no significant difference between growth curves of cultured MenSCs in presence of different fortified media. However, the MenSCs demonstrated variant differentiation patterns in response to FBS replacement with HPDs. Mineralization, as judged by Alizarin red staining, was significantly higher in cells differentiated in the presence of HPR compared to cells that were fortified with other medium supplements. A greater osteocalcin production level, alkaline phosphatase activity, and mRNA expression of osteogenic-specific genes in differentiated MenSCs under HPR condition further confirmed our previous findings. Based on our data, FBS substitution by HPDs not only allows for successful MenSCs proliferation, but also promotes MenSCs development into osteoblasts. The effectiveness of HPR on osteogenic differentiation of MenSCs represents an important novel step toward safe and applied stem cell therapy of bone diseases.
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Arvidson, K., BasM, Abdallah, Applegate, L. A., Baldini, N., Cenni, E., Gomez-Barrena, E., et al. (2011). Bone regeneration and stem cells. Journal of Cellular and Molecular Medicine, 15, 718–746.
Henningson, C. T, Jr, Stanislaus, M. A., & Gewirtz, A. M. (2003). Embryonic and adult stem cell therapy. The Journal of Allergy and Clinical Immunology, 111, 745–753.
Edwards, R. G. (2004). Stem cells today: Bone marrow stem cells. Reproductive Biomedicine Online, 9, 541–583.
Czyz, J., Wiese, C., Rolletschek, A., Blyszczuk, P., Cross, M., & Wobus, A. M. (2003). Potential of embryonic and adult stem cells in vitro. Biological Chemistry, 384(10–11), 1391–1409.
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.
Gutierrez-Aranda, I., Ramos-Mejia, V., Bueno, C., Munoz-Lopez, M., Real, P. J., Mácia, A., et al. (2010). Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless of the site of injection. Stem Cells, 28, 1568–1570.
Meng, X., Ichim, T. E., Zhong, J., Rogers, A., Yin, Z., Jackson, J., et al. (2007). Endometrial regenerative cells: a novel stem cell population. Journal of Translational Medicine, 5, 57.
Patel, A. N., Park, E., Kuzman, M., Benetti, F., Silva, F. J., & Allickson, J. G. (2008). Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplantation, 17, 303–311.
Zhang, M. J., Liu, B., Xia, W., Sun, Z. Y., & Lu, K. H. (2009). Could cells from menstrual blood be a new source for cell-based therapies?. Medical Hypotheses, 72, 252–254.
Musina, R. A., Belyavski, A. V., Tarusova, O. V., Solovyova, E. V., & Sukhikh, G. T. (2008). Endometrial mesenchymal stem cells isolated from the menstrual blood. Bulletin of Experimental Biology and Medicine, 145, 539–543.
Masuda, H., Matsuzaki, Y., Hiratsu, E., Ono, M., Nagashima, T., Kajitani, T., et al. (2010). Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS One, 5(4), e10387.
Allickson, J. G., Sanchez, A., Yefimenko, N., Borlongan, C. V., & Sanberg, P. R. (2011). Recent studies assessing the proliferative capability of a novel adult stem cell identified in menstrual blood. The Open Stem Cell Journal, 3, 4–10.
Borlongan, C. V., Kaneko, Y., Maki, M., Yu, S. J., Ali, M., Allickson, J. G., et al. (2010). Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells and Development, 19(4), 439–452.
de Carvalho, Rodrigues D., Asensi, K. D., Vairo, L., Azevedo-Pereira, R. L., Silva, R., Rondinelli, E., et al. (2012). Human menstrual blood-derived mesenchymal cells as a cell source of rapid and efficient nuclear reprogramming. Cell Transplantation, 21, 2215–2224.
Li, Y., Li, X., Zhao, H., Feng, R., Zhang, X., Tai, D., et al. (2013). Efficient induction of pluripotent stem cells from menstrual blood. Stem Cells and Development, 22(7), 1147–1158.
Sanberg, P. R., Borlongan, C. V., Saporta, S., & Cameron, D. F. (1996). Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain. Nature Biotechnology, 14, 1692–1695.
Sanberg, P. R., Borlongan, C. V., Othberg, A. I., Saporta, S., Freeman, T. B., & Cameron, D. F. (1997). Testis-derived Sertoli cells have a trophic effect on dopamine neurons and alleviate hemiparkinsonism in rats. Nature Medicine, 3, 1129–1132.
Zhong, Z., Patel, A. N., Ichim, T. E., Riordan, N. H., Wang, H., Min, W. P., et al. (2009). Feasibility investigation of allogeneic endometrial regenerative cells. Journal of Translational Medicine, 7, 15.
Darzi, S., Zarnani, A. H., Jeddi-Tehrani, M., Entezami, K., Mirzadegan, E., Akhondi, M. M., et al. (2012). Osteogenic differentiation of stem cells derived from menstrual blood- versus bone marrow in the presence of human platelet releasate. Tissue Engineering Part A, 18(15–16), 1720–1728.
Schallmoser, K., Bartmann, C., Rohde, E., Reinisch, A., Kashofer, K., Stadelmeyer, E., et al. (2007). Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion, 47, 1436–1446.
Capelli, C., Domenghini, M., Borleri, G., Bellavita, P., Poma, R., Carobbio, A., et al. (2007). 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 Transplantation, 40, 785–791.
Duan, J., Kuang, W., Tan, J., Li, H., Zhang, Y., Hirotaka, K., et al. (2011). Differential effects of platelet rich plasma and washed platelets on the proliferation of mouse MSC cells. Molecular Biology Reports, 38, 2485–2490.
Vater, C., Kasten, P., & Stiehler, M. (2011). Culture media for the differentiation of mesenchymal stromal cells. Acta Biomaterialia, 7, 463–477.
Chevallier, N., Anagnostou, F., Zilber, S., Bodivit, G., Maurin, S., Barrault, A., et al. (2010). Osteoblastic differentiation of human mesenchymal stem cells with platelet lysate. Biomaterials, 31, 270–278.
Carrancioa, S., Lo′pez-Holgadoa, N., Sánchez-Guijo, F. M., Villarón, E., Barbado, V., Tabera, S., et al. (2008). Optimization of mesenchymal stem cell expansion procedures by cell separation and culture conditions modification. Experimental Hematology, 36, 1014–1021.
Marx, R. E., Carlson, E. R., Eichstaedt, R. M., Schimmele, S. R., Strauss, J. E., & Georgeff, K. R. (1998). Platelet-rich plasma: Growth factor enhancement for bone grafts. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontics, 85, 638–646.
Weibrich, G., Hansen, T., Kleis, W., Buch, R., & Hitzler, W. E. (2004). Effect of platelet concentration in platelet-rich plasma on peri-implant bone regeneration. Bone, 34, 665–671.
Whitman, D. H., Berry, R. L., & Green, D. M. (1997). Platelet gel: an autologous alternative to fibrin glue with applications in oral and maxillofacial surgery. Journal of Oral and Maxillofacial Surgery, 55, 1294–1299.
Gruber, R., Karreth, F., Fischer, M. B., & Watzek, G. (2002). Platelet-released supernatants stimulate formation of osteoclast-like cells through a prostaglandin/RANKL-dependent mechanism. Bone, 30, 726–732.
Borzini, P., & Mazzucco, I. (2007). Platelet-rich plasma (PRP) and platelet derivatives for topical therapy. What is true from the biologic view point? ISBT Science Series, 2, 272–281.
Bieback, K., Hecker, A., Kocaömer, A., Lannert, H., Schallmoser, K., Strunk, D., et al. (2009). Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells, 27, 2331–2341.
Mannello, F., & Tonti, G. A. (2007). Concise review: No break- throughs for human mesenchymal and embryonic stem cell culture: Conditioned medium, feeder layer, or feeder- free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells, 25(7), 1603–1609.
Everts, P. A., Brown Mahoney, C., Hoffmann, J. J., Schönberger, J. P., Box, H. A., van Zundert, A., et al. (2006). Platelet-rich plasma preparation using three devices: Implications for platelet activation and platelet growth factor release. Growth Factors, 24(3), 165–171.
Mazzocca, A. D., McCarthy, M. B., Chowaniec, D. M., Cote, M. P., Romeo, A. A., Bradley, J. P., et al. (2012). Platelet-rich plasma differs according to preparation method and human variability. Journal of Bone and Joint Surgery American Volume, 94, 308–316.
Rughetti, A., Giusti, I., D’Ascenzo, S., Leocata, P., Carta, G., Pavan, A., et al. (2008). Platelet gel-released supernatant modulates the angiogenic capability of human endothelial cells. Blood Transfusion, 6(1), 12–17.
Somers, P., Robyns, L., Nollet, E., De Somer, F., Cornelissen, M., Thierens, H., et al. (2012). Platelet gel supernatant as a potential tool to repopulate acellular heart valves. Cell Proliferation, 45(4), 378–385.
Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65, 55–63.
Jaiswal, N., Haynesworth, S. E., Caplan, A. I., & Bruder, S. P. (1997). Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. Journal of Cellular Biochemistry, 64, 295–312.
Carpenter, T. O., Moltz, K. C., Ellis, B., Andreoli, M., McCarthy, T. L., Centrella, M., et al. (1998). Osteocalcin production in primary osteoblast cultures derived from normal and Hyp mice. Endocrinology, 139(1), 35–43.
Kazemnejad, S., Allameh, A., Gharehbaghian, A., Soleimani, M., Amirizadeh, N., & Jazayeri, M. (2008). Efficient replacing of fetal bovine serum with human platelet releasate during propagation and differentiation of human bone-marrow-derived mesenchymal stem cells to functional hepatocyte like cells. Vox Sanguinis, 95, 149–158.
Bonewald, L. F., & Dallas, S. L. (1994). Role of active and latent transforming growth factor-b in bone formation. Journal of Cellular Biochemistry, 55, 350–357.
Centrella, M., Horowitz, M. C., Wozne, J. M., & McCarthy, T. L. (1994). Transforming growth factor-b gene family members and bone. Endocrine Reviews, 15, 27–39.
Maeda, S., Hayashi, M., Komiya, S., Imamura, T., & Miyazono, K. (2004). Endogenous TGF-beta signaling suppresses maturation of osteoblastic mesenchymal cells. The EMBO Journal, 23, 552–563.
Murphy, M. B., Blashki, D., Buchanan, R. M., Yazdi, I. K., Ferrari, M., Simmons, P. J., et al. (2012). Adult and umbilical cord blood-derived platelet-rich plasma for mesenchymal stem cell proliferation, chemotaxis, and cryo-preservation. Biomaterials, 33(21), 5308–5316.
Hamdan, A. A., Loty, S., Isaac, J., Bouchard, P., Berdal, A., & Sautier, J. M. (2009). Platelet-poor plasma stimulates the proliferation but inhibits the differentiation of rat osteoblastic cells in vitro. Clinical Oral Implants Research, 20(6), 616–623.
Rauch, Caroline, Feifel, Elisabeth, Amann, Eva-Maria, Spötl, Hans Peter, Schennach, Harald, Pfaller, Walter, et al. (2011). Alternatives to the use of fetal bovine serum: human platelet lysates as a serum substitute in cell culture media. ALTEX, 28(4/11), 305–316.
Kurita, M., Aiba-Kojima, E., Shigeura, T., Matsumoto, D., Suga, H., Inoue, K., et al. (2008). Differential effects of three preparations of human serum on expansion of various types of human cells. Plastic and Reconstructive Surgery, 122(2), 438–448.
Acknowledgments
This work was supported by a research grant from Research Vice-chancellor of Guilan University of Medical Science. We thank Mojtaba Hosseinpoor for technical assistance.
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Kazemnejad, S., Najafi, R., Zarnani, A.H. et al. Comparative Effect of Human Platelet Derivatives on Proliferation and Osteogenic Differentiation of Menstrual Blood-Derived Stem Cells. Mol Biotechnol 56, 223–231 (2014). https://doi.org/10.1007/s12033-013-9698-9
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DOI: https://doi.org/10.1007/s12033-013-9698-9