Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015 (2015), Article ID 486263, 11 pages
http://dx.doi.org/10.1155/2015/486263
Review Article

Reactive Oxygen Species in Mesenchymal Stem Cell Aging: Implication to Lung Diseases

1Department of Thoracic and Cardiovascular Surgery, School of Medicine, Kangwon National University, Chuncheon 200-701, Republic of Korea
2Institute of Medical Science, Kangwon National University, Chuncheon 200-701, Republic of Korea
3Adult Stem Cell Research Center, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Republic of Korea

Received 10 October 2014; Revised 15 April 2015; Accepted 1 May 2015

Academic Editor: Cristina Angeloni

Copyright © 2015 Se-Ran Yang 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. S.-W. Kim, H. Han, G.-T. Chae et al., “Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger's disease and ischemic limb disease animal model,” Stem Cells, vol. 24, no. 6, pp. 1620–1626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. H. S. Kim, J. W. Yun, T. H. Shin et al., “Human umbilical cord blood mesenchymal stem cell-derived PGE2 and TGF-β1 alleviate atopic dermatitis by reducing mast cell degranulation,” Stem Cells, vol. 33, no. 4, pp. 1254–1266, 2015. View at Publisher · View at Google Scholar
  3. J.-R. Park, J.-W. Jung, Y.-S. Lee, and K.-S. Kang, “The roles of Wnt antagonists Dkk1 and sFRP4 during adipogenesis of human adipose tissue-derived mesenchymal stem cells,” Cell Proliferation, vol. 41, no. 6, pp. 859–874, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. J. R. Park, E. Kim, J. Yang et al., “Isolation of human dermis derived mesenchymal stem cells using explants culture method: expansion and phenotypical characterization,” Cell and Tissue Banking, vol. 16, no. 2, pp. 209–218, 2015. View at Publisher · View at Google Scholar
  5. E. J. Eubanks, S. A. Tarle, and D. Kaigler, “Tooth storage, dental pulp stem cell isolation, and clinical scale expansion without animal serum,” Journal of Endodontics, vol. 40, no. 5, pp. 652–657, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. J. H. Oh, P. Mohebi, D. L. Farkas, and J. Tajbakhsh, “Towards expansion of human hair follicle stem cells in vitro,” Cell Proliferation, vol. 44, no. 3, pp. 244–253, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Hayflick, How and Why We Age, Ballantine Book, New York, NY, USA, 1st edition, 1994.
  8. W. A. Pryor, K. N. Houk, C. S. Foote et al., “Free radical biology and medicine: it's a gas, man!,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 291, no. 3, pp. R491–R511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. T. F. Slater, “Free-radical mechanisms in tissue injury,” Biochemical Journal, vol. 222, no. 1, pp. 1–15, 1984. View at Google Scholar · View at Scopus
  10. A. Cuadrado and A. R. Nebreda, “Mechanisms and functions of p38 MAPK signalling,” Biochemical Journal, vol. 429, pp. 403–417, 2010. View at Google Scholar
  11. A. M. Tormos, R. Taléns-Visconti, A. R. Nebreda, and J. Sastre, “P38 MAPK: a dual role in hepatocyte proliferation through reactive oxygen species,” Free Radical Research, vol. 47, no. 11, pp. 905–916, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Yu, J. Y. Lee, H. Kim et al., “A p38 MAPK-mediated alteration of COX-2/PGE2 regulates immunomodulatory properties in human mesenchymal stem cell aging,” PLoS ONE, vol. 9, no. 8, Article ID e102426, 2014. View at Publisher · View at Google Scholar
  13. H.-S. Kim, T.-H. Shin, B.-C. Lee et al., “Human umbilical cord blood mesenchymal stem cells reduce colitis in mice by activating NOD2 signaling to COX2,” Gastroenterology, vol. 145, no. 6, pp. 1392.e8–1403.e8, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. C. S. Velu, S. K. Niture, C. E. Doneanu, N. Pattabiraman, and K. S. Srivenugopal, “Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress,” Biochemistry, vol. 46, no. 26, pp. 7765–7780, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Borodkina, A. Shatrova, P. Abushik, N. Nikolsky, and E. Burova, “Interaction between ROS dependent DNA damage, mitochondria and p38 MAPK underlies senescence of human adult stem cells,” Aging, vol. 6, no. 6, pp. 481–495, 2014. View at Google Scholar
  16. D. J. Kurz, S. Decary, Y. Hong, E. Trivier, A. Akhmedov, and J. D. Erusalimsky, “Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells,” Journal of Cell Science, vol. 117, no. 11, pp. 2417–2426, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Anversa, J. Kajstura, A. Leri, and R. Bolli, “Life and death of cardiac stem cells: a paradigm shift in cardiac biology,” Circulation, vol. 113, no. 11, pp. 1451–1463, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Torella, M. Rota, D. Nurzynska et al., “Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression,” Circulation Research, vol. 94, no. 4, pp. 514–524, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. J.-W. Jung, S. Lee, M.-S. Seo et al., “Histone deacetylase controls adult stem cell aging by balancing the expression of polycomb genes and jumonji domain containing 3,” Cellular and Molecular Life Sciences, vol. 67, no. 7, pp. 1165–1176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Yahata, T. Takanashi, Y. Muguruma et al., “Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells,” Blood, vol. 118, no. 11, pp. 2941–2950, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Liu, L. Cao, J. Chen et al., “Bmi1 regulates mitochondrial function and the DNA damage response pathway,” Nature, vol. 459, no. 7245, pp. 387–392, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Nakamura, M. Oshima, J. Yuan et al., “Bmi1 confers resistance to oxidative stress on hematopoietic stem cells,” PLoS ONE, vol. 7, no. 5, Article ID e36209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. S.-I. Imai, C. M. Armstrong, M. Kaeberlein, and L. Guarente, “Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase,” Nature, vol. 403, no. 6771, pp. 795–800, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Sasaki, B. Maier, A. Bartke, and H. Scrable, “Progressive loss of SIRT1 with cell cycle withdrawal,” Aging Cell, vol. 5, no. 5, pp. 413–422, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. H.-F. Yuan, C. Zhai, X.-L. Yan et al., “SIRT1 is required for long-term growth of human mesenchymal stem cells,” Journal of Molecular Medicine, vol. 90, no. 4, pp. 389–400, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Harman, “Aging: a theory based on free radical and radiation chemistry,” Journal of Gerontology, vol. 11, no. 3, pp. 298–300, 1956. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Lagouge, C. Argmann, Z. Gerhart-Hines et al., “Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α,” Cell, vol. 127, no. 6, pp. 1109–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Grosschedl, K. Giese, and J. Pagel, “HMG domain proteins: architectural elements in the assembly of nucleoprotein structures,” Trends in Genetics, vol. 10, no. 3, pp. 94–100, 1994. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Fusco and M. Fedele, “Roles of HMGA proteins in cancer,” Nature Reviews Cancer, vol. 7, no. 12, pp. 899–910, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. X. Zhou, K. F. Benson, H. R. Ashar, and K. Chada, “Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C,” Nature, vol. 376, no. 6543, pp. 771–774, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Nishino, I. Kim, K. Chada, and S. J. Morrison, “Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression,” Cell, vol. 135, no. 2, pp. 227–239, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. K.-R. Yu, S.-B. Park, J.-W. Jung et al., “HMGA2 regulates the in vitro aging and proliferation of human umbilical cord blood-derived stromal cells through the mTOR/p70S6K signaling pathway,” Stem Cell Research, vol. 10, no. 2, pp. 156–165, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. F. Ishikawa, E. Kaneko, T. Sugimoto et al., “A mitochondrial thioredoxin-sensitive mechanism regulates TGF-beta-mediated gene expression associated with epithelial-mesenchymal transition,” Biochemical and Biophysical Research Communications, vol. 443, no. 3, pp. 821–827, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Beerman, C. Bock, B. S. Garrison et al., “Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging,” Cell Stem Cell, vol. 12, no. 4, pp. 413–425, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. A.-Y. So, J.-W. Jung, S. Lee, H.-S. Kim, and K.-S. Kang, “DNA methyltransferase controls stem cell aging by regulating BMI1 and EZH2 through microRNAs,” PLoS ONE, vol. 6, no. 5, Article ID e19503, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. H. M. O'Hagan, W. Wang, S. Sen et al., “Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG islands,” Cancer Cell, vol. 20, no. 5, pp. 606–619, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. C. E. Campos, F. Molognoni, F. H. M. Melo et al., “Oxidative stress modulates DNA methylation during melanocyte anchorage blockade associated with malignant transformation,” Neoplasia, vol. 9, no. 12, pp. 1111–1121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Bose, M. Moors, R. Tofighi, A. Cascante, O. Hermanson, and S. Ceccatelli, “Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations,” Cell Death & Disease, vol. 1, no. 11, article e92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. D. Brain, “The respiratory tract and the environment,” Environmental Health Perspectives, vol. 20, pp. 113–126, 1977. View at Publisher · View at Google Scholar · View at Scopus
  40. D. J. Weiss, I. Bertoncello, Z. Borok et al., “Stem cells and cell therapies in lung biology and lung diseases,” Proceedings of the American Thoracic Society, vol. 8, no. 3, pp. 223–272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Yin, D. Zheng, G. V. Limmon et al., “Aging exacerbates damage and delays repair of alveolar epithelia following influenza viral pneumonia,” Respiratory Research, vol. 15, no. 1, article 116, 2014. View at Publisher · View at Google Scholar
  42. M. K. Paul, B. Bisht, D. O. Darmawan et al., “Dynamic changes in intracellular ROS levels regulate airway basal stem cell homeostasis through Nrf2-dependent Notch signaling,” Cell Stem Cell, vol. 15, no. 2, pp. 199–214, 2014. View at Publisher · View at Google Scholar
  43. G. Karoubi, L. Cortes-Dericks, I. Breyer, R. A. Schmid, and A. E. Dutly, “Identification of mesenchymal stromal cells in human lung parenchyma capable of differentiating into aquaporin 5-expressing cells,” Laboratory Investigation, vol. 89, no. 10, pp. 1100–1114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. V. N. Lama, L. Smith, L. Badri et al., “Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts,” The Journal of Clinical Investigation, vol. 117, no. 4, pp. 989–996, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. C. J. L. Murray and A. D. Lopez, “Alternative projections of mortality and disability by cause 1990–2020: Global Burden of Disease Study,” The Lancet, vol. 349, no. 9064, pp. 1498–1504, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Ito and P. J. Barnes, “COPD as a disease of accelerated lung aging,” Chest, vol. 135, no. 1, pp. 173–180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Hara, J. Araya, S. Ito et al., “Mitochondrial fragmentation in cigarette smoke-induced bronchial epithelial cell senescence,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 305, no. 10, pp. L737–L746, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Yao, S. Chung, J.-W. Hwang et al., “SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice,” Journal of Clinical Investigation, vol. 122, no. 6, pp. 2032–2045, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Rajendrasozhan, S.-R. Yang, V. L. Kinnula, and I. Rahman, “SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 177, no. 8, pp. 861–870, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. L. B. Ware and M. A. Matthay, “The acute respiratory distress syndrome,” The New England Journal of Medicine, vol. 342, no. 18, pp. 1334–1349, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. G. J. Quinlan, T. W. Evans, and J. M. C. Gutteridge, “4-hydroxy-2-nonenal levels increase in the plasma of patients with adult respiratory distress syndrome as linoleic acid appears to fall,” Free Radical Research, vol. 21, no. 2, pp. 95–106, 1994. View at Publisher · View at Google Scholar · View at Scopus
  52. S. J. Klebanoff, “Myeloperoxidase: friend and foe,” Journal of Leukocyte Biology, vol. 77, no. 5, pp. 598–625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. M. H. Gee, J. E. Gottlieb, K. H. Albertine, J. M. Kubis, S. P. Peters, and J. E. Fish, “Physiology of aging related to outcome in the adult respiratory distress syndrome,” Journal of Applied Physiology, vol. 69, no. 3, pp. 822–829, 1990. View at Google Scholar · View at Scopus
  54. L. S. Smith, S. A. Gharib, C. W. Frevert, and T. R. Martin, “Effects of age on the synergistic interactions between lipopolysaccharide and mechanical ventilation in mice,” The American Journal of Respiratory Cell and Molecular Biology, vol. 43, no. 4, pp. 475–486, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Liu, S. Chen, S. Cai et al., “Wnt5a through noncanonical Wnt/JNK or Wnt/PKC signaling contributes to the differentiation of mesenchymal stem cells into type II alveolar epithelial cells in vitro,” PLoS ONE, vol. 9, no. 3, Article ID e90229, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. M. A. Matthay, L. Robriquet, and X. Fang, “Alveolar epithelium: role in lung fluid balance and acute lung injury,” Proceedings of the American Thoracic Society, vol. 2, no. 3, pp. 206–213, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. K. le Blanc and M. F. Pittenger, “Mesenchymal stem cells: progress toward promise,” Cytotherapy, vol. 7, no. 1, pp. 36–45, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. N. Gupta, X. Su, B. Popov, J. W. Lee, V. Serikov, and M. A. Matthay, “Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice,” The Journal of Immunology, vol. 179, no. 3, pp. 1855–1863, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Li, D. Li, X. Liu, S. Tang, and F. Wei, “Human umbilical cord mesenchymal stem cells reduce systemic inflammation and attenuate LPS-induced acute lung injury in rats,” Journal of Inflammation, vol. 9, article 33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. E. S. Kim, Y. S. Chang, S. J. Choi et al., “Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells attenuates Escherichia coli-induced acute lung injury in mice,” Respiratory Research, vol. 12, article 108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. Z.-X. Liang, J.-P. Sun, P. Wang, Q. Tian, Z. Yang, and L.-A. Chen, “Bone marrow-derived mesenchymal stem cells protect rats from endotoxin-induced acute lung injury,” Chinese Medical Journal, vol. 124, no. 17, pp. 2715–2722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Yang, Y. Wen, J. Bin, Y. Hou-You, and W. Yu-Tong, “Protection of bone marrow mesenchymal stem cells from acute lung injury induced by paraquat poisoning,” Clinical Toxicology, vol. 49, no. 4, pp. 298–302, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. Z.-H. Qin, J.-F. Xu, J.-M. Qu et al., “Intrapleural delivery of MSCs attenuates acute lung injury by paracrine/endocrine mechanism,” Journal of Cellular and Molecular Medicine, vol. 16, no. 11, pp. 2745–2753, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. Y.-G. Zhu, X.-M. Feng, J. Abbott et al., “Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice,” Stem Cells, vol. 32, no. 1, pp. 116–125, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Maron-Gutierrez, J. D. Silva, F. F. Cruz et al., “Insult-dependent effect of bone marrow cell therapy on inflammatory response in a murine model of extrapulmonary acute respiratory distress syndrome,” Stem Cell Research and Therapy, vol. 4, no. 5, article 123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. C.-K. Sun, C.-H. Yen, Y.-C. Lin et al., “Autologous transplantation of adipose-derived mesenchymal stem cells markedly reduced acute ischemia-reperfusion lung injury in a rodent model,” Journal of Translational Medicine, vol. 9, article 118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Shin, Y. Kim, S. Jeong et al., “The therapeutic effect of human adult stem cells derived from adipose tissue in endotoxemic rat model,” International Journal of Medical Sciences, vol. 10, no. 1, pp. 8–18, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Zhang, S. D. Danchuk, K. M. Imhof et al., “Comparison of the therapeutic effects of human and mouse adipose-derived stem cells in a murine model of lipopolysaccharide-induced acute lung injury,” Stem Cell Research & Therapy, vol. 4, no. 1, article 13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. M.-H. Chien, M.-Y. Bien, C.-C. Ku et al., “Systemic human orbital fat-derived stem/stromal cell transplantation ameliorates acute inflammation in lipopolysaccharide-induced acute lung injury,” Critical Care Medicine, vol. 40, no. 4, pp. 1245–1253, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. G. Zhen, Z. Xue, J. Zhao et al., “Mesenchymal stem cell transplantation increases expression of vascular endothelial growth factor in papain-induced emphysematous lungs and inhibits apoptosis of lung cells,” Cytotherapy, vol. 12, no. 5, pp. 605–614, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. J. W. Huh, S.-Y. Kim, J. H. Lee et al., “Bone marrow cells repair cigarette smoke-induced emphysema in rats,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 301, no. 3, pp. L255–L266, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. S.-Y. Kim, J.-H. Lee, H. J. Kim et al., “Mesenchymal stem cell-conditioned media recovers lung fibroblasts from cigarette smoke-induced damage,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 302, no. 9, pp. L891–L908, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. X.-J. Guan, L. Song, F.-F. Han et al., “Mesenchymal stem cells protect cigarette smoke-damaged lung and pulmonary function partly via VEGF-VEGF receptors,” Journal of Cellular Biochemistry, vol. 114, no. 2, pp. 323–335, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. W. Gu, L. Song, X. M. Li, D. Wang, X. J. Guo, and W. G. Xu, “Mesenchymal stem cells alleviate airway inflammation and emphysema in COPD through down-regulation of cyclooxygenase-2 via p38 and ERK MAPK pathways,” Scientific Reports, vol. 5, article 8733, 2015. View at Publisher · View at Google Scholar
  75. A. M. Katsha, S. Ohkouchi, H. Xin et al., “Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model,” Molecular Therapy, vol. 19, no. 1, pp. 196–203, 2011. View at Publisher · View at Google Scholar · View at Scopus