Abstract
A functional relationship between the growth and the progression of events associated with osteogenic differentiation of human amniotic mesenchymal stem cells (hAMSCs) has been a fundamental question, which remains unclear. This study is aimed at investigating the effects of low temperature and lactate individually, and in combination on the growth and osteogenic differentiation of hAMSCs. It was shown that the growth of hAMSCs in growth medium was inhibited by both low-cultivation temperature and lactate. By extending culture period at low temperature, cell growth declined gradually, while the ALP expression and calcium deposition increased progressively. However, the growth of hAMSCs induced in osteogenic medium at 37°C was markedly enhanced by additional lactate. The ALP expression and calcium deposition, on the contrary, were significantly depressed. Furthermore, the synergistic actions of long-term low temperature and lactate resulted in more intense inhibition on both cell growth and osteogenic differentiation. Therefore, these findings may imply the co-contribution of the culture environment on the selective manipulation on the growth capacity and osteogenic differentiation potential of hAMSCs.
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Kon, E., A. Muraglia, A. Corsi, P. Bianco, M. Marcacci, I. Martin, A. Boyde, I. Ruspantini, P. Chistolini, M. Rocca, R. Giardino, R. Cancedda, and R. Quarto (2000) Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J. Biomed. Mater. Res. 49: 328–337.
Petite, H., V. Viateau, W. Bensaid, A. Meunier, C. de Pollak, M. Bourguignon, K. Oudina, L. Sedel, and G. Guillemin (2000) Tissue-engineered bone regeneration. Nat. Biotechnol. 18: 959–963.
Barlow, S., G. Brooke, K. Chatterjee, G. Price, R. Pelekanos, T. Rossetti, M. Doody, D. Venter, S. Pain, K. Gilshenan, and K. Atkinson (2008) Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev. 17: 1095–1108.
Brooke, G., H. Tong, J. P. Levesque, and K. Atkinson (2008) Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev. 17: 929–940.
Bonab, M. M., K. Alimoghaddam, F. Talebian, S. H. Ghaffari, A. Ghavamzadeh, and B. Nikbin (2006) Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 7: 14.
Kretlow, J. D., Y. Q. Jin, W. Liu, W. J. Zhang, T. H. Hong, G. D. Zhou, L. S. Baggett, A. G. Mikos, and Y. L. Cao (2008) Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 9: 60.
Choi, K. M., Y. K. Seo, H. H. Yoon, K. Y. Song, S. Y. Kwon, H. S. Lee, and J. K. Park (2007) Effects of mechanical stimulation on the proliferation of bone marrow-derived human mesenchymal stem cells. Biotechnol. Bioprocess Eng. 12: 601–609.
Balint, E., P. Szabo, C. F. Marshall, and S. M. Sprague (2001) Glucose-induced inhibition of in vitro bone mineralization. Bone 28: 21–28.
Rodriguez, J. P., S. Rios, and M. Gonzalez (2002) Modulation of the proliferation and differentiation of human mesenchymal stem cells by copper. J. Cell Biochem. 85: 92–100.
Stein, G. S. and J. B. Lian (1993) Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr. Rev. 14: 424–442.
Kim, G. S., J. S. Hong, S. W. Kim, J. M. Koh, C. S. An, J. Y. Choi, and S. L. Cheng (2003) Leptin induces apoptosis via ERK/cPLA2/cytochrome c pathway in human bone marrow stromal cells. J. Biol. Chem. 278: 21920–21929.
Doucet, C., I. Ernou, Y. Zhang, J. R. Llense, L. Begot, X. Holy, and J. J. Lataillade (2005) Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J. Cell Physiol. 205: 228–236.
Qu, W. J., D. B. Zhong, P. F. Wu, J. F. Wang, and B. Han (2008) Sodium fluoride modulates caprine osteoblast proliferation and differentiation. J. Bone Miner. Metab. 26: 328–334.
Nagarathnamma, M. M. Rajan, and G. K. Sureshkumar (1997) Apoptosis extent increases in hybridoma cultures with temperature. Biotechnol. Lett. 19: 669–673.
Stolzing, A., S. Sethe, and A. M. Scutt (2006) Stressed stem cells: temperature response in aged mesenchymal stem cells. Stem Cells Dev. 15: 478–487.
Yoon, S. K., J. Y. Song, and G. M. Lee (2003) Effect of low culture temperature on specific productivity, transcription level, and heterogeneity of erythropoietin in Chinese hamster ovary cells. Biotechnol. Bioeng. 82: 289–298.
Shui, C. and A. Scutt (2001) Mild heat shock induces proliferation, alkaline phosphatase activity, and mineralization in human bone marrow stromal cells and Mg-63 cells in vitro. J. Bone Miner. Res. 16: 731–741.
Stolzing, A. and A. Scutt (2006) Effect of reduced culture temperature on antioxidant defences of mesenchymal stem cells. Free Radic. Biol. Med. 41: 326–338.
Ozturk, S. S., M. R. Riley, and B. O. Palsson (1992) Effect of ammonia and lactate on hybridoma growth, metabolism, and antibody production. Biotechnol. Bioeng. 39: 418–431.
Follmar, K. E., F. C. Decroos, H. L. Prichard, H. T. Wang, D. Erdmann, and K. C. Olbrich (2006) Effect of glutamine, glucose, and oxygen concentration on the metabolism and proliferation of rabbit adipose-derived stem cells. Tissue Eng. 12: 3525–3533.
Grayson, W. L., F. Zhao, R. Izadpanah, B. Bunnell, and T. Ma (2006) Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J. Cell Physiol. 207: 331–339.
Wang, D. W., B. Fermor, J. M. Gimble, H. A. Awad, and F. Guilak (2005) Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J. Cell Physiol. 204: 184–191.
Nicoll S. B., A. Wedrychowska, N. R. Smith, and R. S. Bhatnagar (2001) Modulation of proteoglycan and collagen profiles in human dermal fibroblasts by high density micromass culture and treatment with lactic acid suggests change to a chondrogenic phenotype. Connect. Tissue Res. 42: 59–69.
Choi, Y. S., D. Y. Lee, I. Y. Kim, H. J. Kim, H. W. Park, T. B. Choe, and I. H. Kim (2007) Enhancement of erythropoietin production in recombinant Chinese hamster ovary cells by sodium lactate addition. Biotechnol. Bioprocess Eng. 12: 60–72.
Patel, S. D., E. T. Papoutsakis, J. N. Winter, and W. M. Miller (2000) The lactate issue revisited: novel feeding protocols to examine inhibition of cell proliferation and glucose metabolism in hematopoietic cell cultures. Biotechnol. Prog. 16: 885–892.
Chen, T., Y. Zhou, and W. S. Tan (2009) Influence of lactic acid on the proliferation, metabolism, and differentiation of rabbit mesenchymal stem cells. Cell Biol. Toxicol. 25: 573–586.
Fedde, K. N., L. Blair, J. Silverstein, S. P. Coburn, L. M. Ryan, R. S. Weinstein, K. Waymire, S. Narisawa, J. L. Millan, G. R. Macgregor, and M. P. Whyte (1999) Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J. Bone Miner. Res. 14: 2015–2026.
Ludwig, A., J. Tomeczkowski, and G. Kretzmer (1992) Influence of the temperature on the shear stress sensitivity of adherent BHK 21 cells. Appl. Microbiol. Biotechnol. 38: 323–327.
Ryoo, H. M., A. J. van Wijnen, J. L. Stein, J. B. Lian, and G. S. Stein (1997) Detection of a proliferation specific gene during development of the osteoblast phenol-type by mRNA differential display. J. Cell Biochem. 64: 106–116.
Siddhanti, S. R. and L. D. Quarles (1994) Molecular to pharmacologic control of osteoblast proliferation and differentiation. J. Cell Biochem. 55: 310–320.
Bellows, C. G., J. N. Heersche, and J. E. Aubin (1999) Aluminum accelerates osteoblastic differentiation but is cytotoxic in long-term rat calvaria cell cultures. Calcif. Tissue Int. 65: 59–65.
Cruz, H. J., C. M. Freitas, P. M. Alves, J. L. Moreira, and M. J. T. Carrondo (2000) Effects of ammonia and lactate on growth, metabolism, and productivity of BHK cells. Enzym. Microb. Technol. 27: 43–52.
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Chen, T., Zhou, Y. & Tan, WS. Effects of low temperature and lactate on osteogenic differentiation of human amniotic mesenchymal stem cells. Biotechnol Bioproc E 14, 708–715 (2009). https://doi.org/10.1007/s12257-009-0034-y
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DOI: https://doi.org/10.1007/s12257-009-0034-y