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BioMed Research International
Volume 2016, Article ID 8196078, 13 pages
http://dx.doi.org/10.1155/2016/8196078
Research Article

Poly-L-lysine Prevents Senescence and Augments Growth in Culturing Mesenchymal Stem Cells Ex Vivo

1Cell Therapy Centre, Severance Hospital, Seoul 03722, Republic of Korea
2Department of Laboratory Medicine, Yonsei University College of Medicine, Seoul 03722, Republic of Korea
3Department of Plastic and Reconstructive Surgery, Yonsei University College of Medicine, Seoul 03722, Republic of Korea

Received 18 March 2016; Accepted 23 May 2016

Academic Editor: Giulio Mengozzi

Copyright © 2016 June Seok Heo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. S. A. Wexler, C. Donaldson, P. Denning-Kendall, C. Rice, B. Bradley, and J. M. Hows, “Adult bone marrow is a rich source of human mesenchymal ‘stem’ cells but umbilical cord and mobilized adult blood are not,” British Journal of Haematology, vol. 121, no. 2, pp. 368–374, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Kögler, S. Sensken, and P. Wernet, “Comparative generation and characterization of pluripotent unrestricted somatic stem cells with mesenchymal stem cells from human cord blood,” Experimental Hematology, vol. 34, no. 11, pp. 1589–1595, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Barlow, G. Brooke, K. Chatterjee et al., “Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells,” Stem Cells and Development, vol. 17, no. 6, pp. 1095–1107, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Busser, C. De Bruyn, F. Urbain et al., “fIsolation of adipose-derived stromal cells without enzymatic treatment: expansion, phenotypical, and functional characterization,” Stem Cells and Development, vol. 23, no. 19, pp. 2390–2400, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. P. H. Lee, J. E. Lee, H.-S. Kim et al., “A randomized trial of mesenchymal stem cells in multiple system atrophy,” Annals of Neurology, vol. 72, no. 1, pp. 32–40, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Mazzini, K. Mareschi, I. Ferrero et al., “Autologous mesenchymal stem cells: clinical applications in amyotrophic lateral sclerosis,” Neurological Research, vol. 28, no. 5, pp. 523–526, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Wagner, P. Horn, M. Castoldi et al., “Replicative senescence of mesenchymal stem cells: a continuous and organized process,” PLoS ONE, vol. 3, no. 5, Article ID e2213, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Hayflick, “The limited in vitro lifetime of human diploid cell strains,” Experimental Cell Research, vol. 37, no. 3, pp. 614–636, 1965. View at Publisher · View at Google Scholar · View at Scopus
  10. M. M. Bonab, K. Alimoghaddam, F. Talebian, S. H. Ghaffari, A. Ghavamzadeh, and B. Nikbin, “Aging of mesenchymal stem cell in vitro,” BMC Cell Biology, vol. 7, article 14, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Itahana, J. Campisi, and G. P. Dimri, “Mechanisms of cellular senescence in human and mouse cells,” Biogerontology, vol. 5, no. 1, pp. 1–10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Loft, P. H. Danielsen, L. Mikkelsen, L. Risom, L. Forchhammer, and P. Møller, “Biomarkers of oxidative damage to DNA and repair,” Biochemical Society Transactions, vol. 36, no. 5, pp. 1071–1076, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. W. L. Grayson, F. Zhao, B. Bunnell, and T. Ma, “Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells,” Biochemical and Biophysical Research Communications, vol. 358, no. 3, pp. 948–953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. W. L. Grayson, F. Zhao, R. Izadpanah, B. Bunnell, and T. Ma, “Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs,” Journal of Cellular Physiology, vol. 207, no. 2, pp. 331–339, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Ren, Y. Cao, Q. Zhao et al., “Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions,” Biochemical and Biophysical Research Communications, vol. 347, no. 1, pp. 12–21, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. K. R. Shibata, T. Aoyama, Y. Shima et al., “Expression of the p16INK4A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion,” STEM CELLS, vol. 25, no. 9, pp. 2371–2382, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Abedin and N. King, “Diverse evolutionary paths to cell adhesion,” Trends in Cell Biology, vol. 20, no. 12, pp. 734–742, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Michel, T. Tonon, D. Scornet, J. M. Cock, and B. Kloareg, “The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes,” New Phytologist, vol. 188, no. 1, pp. 82–97, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. B. de Kruijff and P. R. Cullis, “The influence of poly(L-lysine) on phospholipid polymorphism. Evidence that electrostatic polypeptide-phospholipid interactions can modulate bilayer/non-bilayer transitions,” Biochimica et Biophysica Acta, vol. 601, no. 1, pp. 235–240, 1980. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Pachmann and W. Leibold, “Insolubilization of protein antigens on polyacrylic plastic beads using poly-l-lysine,” Journal of Immunological Methods, vol. 12, no. 1-2, pp. 81–89, 1976. View at Publisher · View at Google Scholar · View at Scopus
  21. K.-S. Park, J. Ahn, J. Y. Kim, H. Park, H. O. Kim, and S.-H. Lee, “Poly-L-lysine increases the ex vivo expansion and erythroid differentiation of human hematopoietic stem cells, as well as erythroid enucleation efficacy,” Tissue Engineering Part A, vol. 20, no. 5-6, pp. 1072–1080, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Cai, J. Lu, V. Sheen, and S. Wang, “Optimal poly(l-lysine) grafting density in hydrogels for promoting neural progenitor cell functions,” Biomacromolecules, vol. 13, no. 5, pp. 1663–1674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. A. I. Caplan and D. Correa, “The MSC: an injury drugstore,” Cell Stem Cell, vol. 9, no. 1, pp. 11–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Charbord, “Bone marrow mesenchymal stem cells: historical overview and concepts,” Human Gene Therapy, vol. 21, no. 9, pp. 1045–1056, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. H.-S. Kim, D.-Y. Choi, S. J. Yun et al., “Proteomic analysis of microvesicles derived from human mesenchymal stem cells,” Journal of Proteome Research, vol. 11, no. 2, pp. 839–849, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. M. S. Choudhery, M. Khan, R. Mahmood, A. Mehmood, S. N. Khan, and S. Riazuddin, “Bone marrow derived mesenchymal stem cells from aged mice have reduced wound healing, angiogenesis, proliferation and anti-apoptosis capabilities,” Cell Biology International, vol. 36, no. 8, pp. 747–753, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. H. Kim, D. S. Yoon, H. O. Kim, and J. W. Lee, “Characterization of different subpopulations from bone marrow-derived mesenchymal stromal cells by alkaline phosphatase expression,” Stem Cells and Development, vol. 21, no. 16, pp. 2958–2968, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. L.-X. Tay, C.-K. Lim, A. Mansor, and T. Kamarul, “Differential protein expression between chondrogenic differentiated MSCs, undifferentiated MSCs and adult chondroctyes derived from Oryctolagus cuniculus in vitro,” International Journal of Medical Sciences, vol. 11, no. 1, pp. 24–33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Pierantozzi, B. Gava, I. Manini et al., “Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2,” Stem Cells and Development, vol. 20, no. 5, pp. 915–923, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-C. Tsai, P.-F. Su, Y.-F. Huang, T.-L. Yew, and S.-C. Hung, “Oct4 and nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cells,” Molecular Cell, vol. 47, no. 2, pp. 169–182, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Ge, Y. Ju, Z. Xue et al., “Distal C terminus of CaV1.2 channels plays a crucial role in the neural differentiation of dental pulp stem cells,” PLoS ONE, vol. 8, no. 11, Article ID e81332, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. M.-L. Nueda, V. Baladrón, J.-J. García-Ramírez et al., “The novel gene EGFL9/Dlk2, highly homologous to Dlk1, functions as a modulator of adipogenesis,” Journal of Molecular Biology, vol. 367, no. 5, pp. 1270–1280, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Hoareau-Aveilla, M. Bonoli, M. Caizergues-Ferrer, and Y. Henry, “hNaf1 is required for accumulation of human box H/ACA snoRNPs, scaRNPs, and telomerase,” RNA, vol. 12, no. 5, pp. 832–840, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. S.-T. Liu, J. C. Hittle, S. A. Jablonski, M. S. Campbell, K. Yoda, and T. J. Yen, “Human CENP-I specifies localization of CENP-F, MAD1 and MAD2 to kinetochores and is essential for mitosis,” Nature Cell Biology, vol. 5, no. 4, pp. 341–345, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Than, X. Zhang, M. K.-S. Leow, C. L. Poh, S. K. Chong, and P. Chen, “Apelin attenuates oxidative stress in human adipocytes,” The Journal of Biological Chemistry, vol. 289, no. 6, pp. 3763–3774, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Shao, J. H. Wang, M. R. Pollak, and A. Wells, “α-actinin-4 is essential for maintaining the spreading, motility and contractility of fibroblasts,” PLoS ONE, vol. 5, no. 11, Article ID e13921, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. M.-Y. Lee, H.-D. Hofmann, and M. Kirsch, “Expression of ciliary neurotrophic factor receptor-α messenger RNA in neonatal and adult rat brain: an in situ hybridization study,” Neuroscience, vol. 77, no. 1, pp. 233–246, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Yasumi, T. Sakisaka, T. Hoshino et al., “Direct binding of Lgl2 to LGN during mitosis and its requirement for normal cell division,” Journal of Biological Chemistry, vol. 280, no. 8, pp. 6761–6765, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Christensen, P. Cloos, U. Toftegaard et al., “Characterization of E2F8, a novel E2F-like cell-cycle regulated repressor of E2F-activated transcription,” Nucleic Acids Research, vol. 33, no. 17, pp. 5458–5470, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Manser, T. Leung, H. Salihuddin, L. Tan, and L. Lim, “A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42,” Nature, vol. 363, no. 6427, pp. 364–367, 1993. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Diecke, A. Quiroga-Negreira, T. Redmer, and D. Besser, “FGF2 signaling in mouse embryonic fibroblasts is crucial for self-renewal of embryonic stem cells,” Cells Tissues Organs, vol. 188, no. 1-2, pp. 52–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Nakayama, Y. Miura, J. Ogino et al., “Detection of HEY1-NCOA2 fusion by fluorescence in-situ hybridization in formalin-fixed paraffin-embedded tissues as a possible diagnostic tool for mesenchymal chondrosarcoma,” Pathology International, vol. 62, no. 12, pp. 823–826, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Goicoechea, A. W. Orr, M. A. Pallero, P. Eggleton, and J. E. Murphy-Ullrich, “Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin,” The Journal of Biological Chemistry, vol. 275, no. 46, pp. 36358–36368, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Kim, K. Kim, S. H. Lee et al., “Identification of LRRc17 as a negative regulator of receptor activator of NF-κB ligand (RANKL)-induced osteoclast differentiation,” Journal of Biological Chemistry, vol. 284, no. 22, pp. 15308–15316, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Yoshioka and F. Ramirez, “Pro-alpha 1(XI) collagen. Structure of the amino-terminal propeptide and expression of the gene in tumor cell lines,” The Journal of Biological Chemistry, vol. 265, no. 11, pp. 6423–6426, 1990. View at Google Scholar · View at Scopus
  46. L. Zhang, M. Wang, X. Kang et al., “Oxidative stress and asthma: proteome analysis of chitinase-like proteins and FIZZ1 in lung tissue and bronchoalveolar lavage fluid,” Journal of Proteome Research, vol. 8, no. 4, pp. 1631–1638, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Khurana, H. McKean, H. Kim et al., “Silencing of HSulf-2 expression in MCF10DCIS.com cells attenuate ductal carcinoma in situ progression to invasive ductal carcinoma in vivo,” Breast Cancer Research, vol. 14, no. 2, article R43, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Morimoto-Tomita, K. Uchimura, A. Bistrup et al., “Sulf-2, a proangiogenic heparan sulfate endosulfatase, is upregulated in breast cancer,” Neoplasia, vol. 7, no. 11, pp. 1001–1010, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. A. W. Orr, M. A. Pallero, and J. E. Murphy-Ullrich, “Thrombospondin stimulates focal adhesion disassembly through Gi- and phosphoinositide 3-kinase-dependent ERK activation,” Journal of Biological Chemistry, vol. 277, no. 23, pp. 20453–20460, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Tanaka, Y. Okugawa, Y. Toiyama et al., “Brain-Derived Neurotrophic Factor (BDNF)-induced Tropomyosin-related kinase B (Trk B) signaling is a potential therapeutic target for peritoneal carcinomatosis arising from colorectal cancer,” PLoS ONE, vol. 9, no. 5, article e96410, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. J. You, D. S. Shin, D. Patel, Y. Gao, and A. Revzin, “Multilayered heparin hydrogel microwells for cultivation of primary hepatocytes,” Advanced Healthcare Materials, vol. 3, no. 1, pp. 126–132, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Xu, X. Zhu, H. S. Hahm et al., “Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 18, pp. 8129–8134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Z. Kuhn and R. S. Tuan, “Regulation of stemness and stem cell niche of mesenchymal stem cells: Implications in tumorigenesis and metastasis,” Journal of Cellular Physiology, vol. 222, no. 2, pp. 268–277, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. D. J. Rodda, J.-L. Chew, L.-H. Lim et al., “Transcriptional regulation of Nanog by OCT4 and SOX2,” Journal of Biological Chemistry, vol. 280, no. 26, pp. 24731–24737, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. D. S. Yoon, Y. H. Kim, H. S. Jung, S. Paik, and J. W. Lee, “Importance of Sox2 in maintenance of cell proliferation and multipotency of mesenchymal stem cells in low-density culture,” Cell Proliferation, vol. 44, no. 5, pp. 428–440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. T. M. Liu, Y. N. Wu, X. M. Guo, J. H. P. Hui, E. H. Lee, and B. Lim, “Effects of Ectopic Nanog and Oct4 overexpression on mesenchymal stem cells,” Stem Cells and Development, vol. 18, no. 7, pp. 1013–1022, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Ksiazek, “A comprehensive review on mesenchymal stem cell growth and senescence,” Rejuvenation Research, vol. 12, no. 2, pp. 105–116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. U. Herbig, W. A. Jobling, B. P. C. Chen, D. J. Chen, and J. M. Sedivy, “Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21CIP1, but not p16INK4a,” Molecular Cell, vol. 14, no. 4, pp. 501–513, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Tothova, R. Kollipara, B. J. Huntly et al., “FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress,” Cell, vol. 128, no. 2, pp. 325–339, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Ito, R. Sawada, Y. Fujiwara, Y. Seyama, and T. Tsuchiya, “FGF-2 suppresses cellular senescence of human mesenchymal stem cells by down-regulation of TGF-β2,” Biochemical and Biophysical Research Communications, vol. 359, no. 1, pp. 108–114, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. G. T. Yocum, L. B. Wilson, P. Ashari, E. K. Jordan, J. A. Frank, and A. S. Arbab, “Effect of human stem cells labeled with ferumoxides-poly-L-lysine on hematologic and biochemical measurements in rats,” Radiology, vol. 235, no. 2, pp. 547–552, 2005. View at Publisher · View at Google Scholar · View at Scopus