Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015 (2015), Article ID 101304, 11 pages
http://dx.doi.org/10.1155/2015/101304
Research Article

Nuclear Nox4 Role in Stemness Power of Human Amniotic Fluid Stem Cells

1Department of Surgical, Medical, Dental and Morphological Sciences with Interest in Transplant, Oncology and Regenerative Medicine, University of Modena and Reggio Emilia, Via Del Pozzo 71, 41100 Modena, Italy
2EURAC Research, Center for Biomedicine, Via Galvani 31, 39100 Bolzano, Italy
3Unit of Obstetrics & Gynecology, IRCCS-Arcispedale Santa Maria Nuova, Viale Umberto I 50, 42123 Reggio Emilia, Italy
4University of Modena e Reggio Emilia, Viale A. Allegri 9, 42121 Reggio Emilia, Italy

Received 10 September 2014; Revised 16 December 2014; Accepted 24 December 2014

Academic Editor: Jing Yi

Copyright © 2015 Tullia Maraldi 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. D. G. Phinney, “Functional heterogeneity of mesenchymal stem cells: implications for cell therapy,” Journal of Cellular Biochemistry, vol. 113, no. 9, pp. 2806–2812, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. P. De Coppi, G. Bartsch Jr., M. M. Siddiqui et al., “Isolation of amniotic stem cell lines with potential for therapy,” Nature Biotechnology, vol. 25, no. 1, pp. 100–106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Chaudhari, Z. Ye, and Y.-Y. Jang, “Roles of reactive oxygen species in the fate of stem cells,” Antioxidants and Redox Signaling, vol. 20, no. 12, pp. 1881–1890, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Ushio-Fukai and N. Urao, “Novel role of NADPH oxidase in angiogenesis and stem/progenitor cell function,” Antioxidants and Redox Signaling, vol. 11, no. 10, pp. 2517–2533, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Kietzmann, “Intracellular redox compartments: mechanisms and significances,” Antioxidants and Redox Signaling, vol. 13, no. 4, pp. 395–398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Ateghang, M. Wartenberg, M. Gassmann, and H. Sauer, “Regulation of cardiotrophin-1 expression in mouse embryonic stem cells by HIF-1α and intracellular reactive oxygen species,” Journal of Cell Science, vol. 119, no. 6, pp. 1043–1052, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Buggisch, B. Ateghang, C. Ruhe et al., “Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase,” Journal of Cell Science, vol. 120, no. 5, pp. 885–894, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Sauer, G. Rahimi, J. Hescheler, and M. Wartenberg, “Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells,” FEBS Letters, vol. 476, no. 3, pp. 218–223, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Schmelter, B. Ateghang, S. Helmig, M. Wartenberg, and H. Sauer, “Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation,” The FASEB Journal, vol. 20, no. 8, pp. 1182–1184, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Sharifpanah, M. Wartenberg, M. Hannig, H.-M. Piper, and H. Sauer, “Peroxisome proliferator-activated receptor α agonists enhance cardiomyogenesis of mouse ES cells by utilization of a reactive oxygen species-dependent mechanism,” Stem Cells, vol. 26, no. 1, pp. 64–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. Q. Xiao, Z. Luo, A. E. Pepe, A. Margariti, L. Zeng, and Q. Xu, “Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2,” The American Journal of Physiology: Cell Physiology, vol. 296, no. 4, pp. C711–C723, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Chen, M. T. Kirber, H. Xiao, Y. Yang, and J. F. Keaney Jr., “Regulation of ROS signal transduction by NADPH oxidase 4 localization,” Journal of Cell Biology, vol. 181, no. 7, pp. 1129–1139, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. R. K. Ambasta, P. Kumar, K. K. Griendling, H. H. H. W. Schmidt, R. Busse, and R. P. Brandes, “Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase,” Journal of Biological Chemistry, vol. 279, no. 44, pp. 45935–45941, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Block, Y. Gorin, and H. E. Abboud, “Subcellular localization of Nox4 and regulation in diabetes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 34, pp. 14385–14390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. L. L. Hilenski, R. E. Clempus, M. T. Quinn, J. D. Lambeth, and K. K. Griendling, “Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 4, pp. 677–683, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. Y.-M. Lee, B.-J. Kim, Y.-S. Chun et al., “NOX4 as an oxygen sensor to regulate TASK-1 activity,” Cellular Signalling, vol. 18, no. 4, pp. 499–507, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Kuroda, K. Nakagawa, T. Yamasaki et al., “The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells,” Genes to Cells, vol. 10, no. 12, pp. 1139–1151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Guida, T. Maraldi, E. Resca et al., “Inhibition of nuclear Nox4 activity by plumbagin: effect on proliferative capacity in human amniotic stem cells,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 680816, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Wang, T. Zhang, Q. Dong, E. C. Nice, C. Huang, and Y. Wei, “Redox homeostasis: the linchpin in stem cell self-renewal and differentiation,” Cell Death and Disease, vol. 4, article e537, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Zavatti, E. Resca, L. Bertoni et al., “Ferutinin promotes proliferation and osteoblastic differentiation in human amniotic fluid and dental pulp stem cells,” Life Sciences, vol. 92, no. 20-21, pp. 993–1003, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Guida, T. Maraldi, F. Beretti, M. Y. Follo, L. Manzoli, and A. de Pol, “Nuclear Nox4-derived reactive oxygen species in myelodysplastic syndromes,” BioMed Research International, vol. 2014, Article ID 456937, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Maraldi, L. Bertoni, M. Riccio et al., “Human amniotic fluid stem cells: neural differentiation in vitro and in vivo,” Cell and Tissue Research, vol. 357, no. 1, pp. 1–13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Maraldi, J. Bertacchini, M. Benincasa et al., “Reverse-phase protein microarrays (RPPA) as a diagnostic and therapeutic guide in multidrug resistant leukemia,” International Journal of Oncology, vol. 38, no. 2, pp. 427–435, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Cenni, J. Bertacchini, F. Beretti et al., “Lamin A Ser404 Is a nuclear target of akt phosphorylation in C2C12 cells,” Journal of Proteome Research, vol. 7, no. 11, pp. 4727–4735, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Cenni, A. Bavelloni, F. Beretti et al., “Ankrd2/ARPP is a novel Akt2 specific substrate and regulates myogenic differentiation upon cellular exposure to H2O2,” Molecular Biology of the Cell, vol. 22, no. 16, pp. 2946–2956, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. C. J. Hanson, M. D. Bootman, C. W. Distelhorst, T. Maraldi, and H. L. Roderick, “The cellular concentration of Bcl-2 determines its pro- or anti-apoptotic effect,” Cell Calcium, vol. 44, no. 3, pp. 243–258, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Resca, M. Zavatti, L. Bertoni et al., “Enrichment in c-Kit+ enhances mesodermal and neural differentiation of human chorionic placental cells,” Placenta, vol. 34, no. 7, pp. 526–535, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Pisciotta, M. Riccio, G. Carnevale et al., “Human serum promotes osteogenic differentiation of human dental pulp stem cells in vitro and in vivo,” PLoS ONE, vol. 7, no. 11, Article ID e50542, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Riccio, E. Resca, T. Maraldi et al., “Human dental pulp stem cells produce mineralized matrix in 2D and 3D cultures,” European Journal of Histochemistry, vol. 54, no. 4, article e46, 2010. View at Google Scholar · View at Scopus
  30. B. C. Dickinson, Y. Tang, Z. Chang, and C. J. Chang, “A nuclear-localized fluorescent hydrogen peroxide probe for monitoring sirtuin-mediated oxidative stress responses in vivo,” Chemistry and Biology, vol. 18, no. 8, pp. 943–948, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. A. R. Lippert, G. C. van de Bittner, and C. J. Chang, “Boronate oxidation as a bioorthogonal reaction approach for studying the chemistry of hydrogen peroxide in living systems,” Accounts of Chemical Research, vol. 44, no. 9, pp. 793–804, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. V. S. Lin, B. C. Dickinson, and C. J. Chang, “Boronate—based fluorescent probes: imaging hydrogen peroxide in living systems,” Methods in Enzymology, vol. 526, pp. 19–43, 2013, (Chapter 2 in Hydrogen Peroxide and Cell Signaling, Part A). View at Publisher · View at Google Scholar · View at Scopus
  33. B. C. Dickinson and C. J. Chang, “Chemistry and biology of reactive oxygen species in signaling or stress responses,” Nature Chemical Biology, vol. 7, no. 8, pp. 504–511, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. X. Zhang, S. Yalcin, D.-F. Lee et al., “FOXO1 is an essential regulator of pluripotency in human embryonic stem cells,” Nature Cell Biology, vol. 13, no. 9, pp. 1092–1101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. P. J. Cook, B. G. Ju, F. Telese, X. Wang, C. K. Glass, and M. G. Rosenfeld, “Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions,” Nature, vol. 458, no. 7238, pp. 591–596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. J. J. Tsai, J. A. Dudakov, K. Takahashi et al., “Nrf2 regulates haematopoietic stem cell function,” Nature Cell Biology, vol. 15, no. 3, pp. 309–316, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Lukosz, S. Jakob, N. Büchner, T.-C. Zschauer, J. Altschmied, and J. Haendeler, “Nuclear redox signaling,” Antioxidants and Redox Signaling, vol. 12, no. 6, pp. 713–742, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. A. I. Lamond and D. L. Spector, “Nuclear speckles: a model for nuclear organelles,” Nature Reviews Molecular Cell Biology, vol. 4, no. 8, pp. 605–612, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Brunet, L. B. Sweeney, J. F. Sturgill et al., “Stress-Dependent Regulation of FOXO Transcription Factors by the SIRT1 Deacetylase,” Science, vol. 303, no. 5666, pp. 2011–2015, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. A. G. Essers, S. Weijzen, A. M. M. de Vries-Smits et al., “FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK,” The EMBO Journal, vol. 23, no. 24, pp. 4802–4812, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Tolkunova, A. Malashicheva, V. N. Parfenov, C. Sustmann, R. Grosschedl, and A. Tomilin, “PIAS proteins as repressors of Oct4 function,” Journal of Molecular Biology, vol. 374, no. 5, pp. 1200–1212, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. V. N. Parfenov, G. N. Pochukalina, D. S. Davis, R. Reinbold, H. R. Schöler, and K. G. Murti, “Nuclear distribution of Oct-4 transcription factor in transcriptionally active and inactive mouse oocytes and its relation to RNA polymerase II and splicing factors,” Journal of Cellular Biochemistry, vol. 89, no. 4, pp. 720–732, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. 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
  44. C. Scheidereit, “IκB kinase complexes: gateways to NF-κB activation and transcription,” Oncogene, vol. 25, no. 51, pp. 6685–6705, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. M. McMahon, K. Itoh, M. Yamamoto et al., “The cap ‘n’ collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes,” Cancer Research, vol. 61, no. 8, pp. 3299–3307, 2001. View at Google Scholar · View at Scopus
  46. R. Liang and S. Ghaffari, “Stem cells, redox signaling, and stem cell aging,” Antioxidants and Redox Signaling, vol. 20, no. 12, pp. 1902–1916, 2014. View at Publisher · View at Google Scholar · View at Scopus