About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2014 (2014), Article ID 456937, 11 pages
http://dx.doi.org/10.1155/2014/456937
Research Article

Nuclear Nox4-Derived Reactive Oxygen Species in Myelodysplastic Syndromes

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, 41124 Modena, Italy
2Department of Human Anatomic Sciences, University of Bologna, Via Irnerio 48, 40100 Bologna, Italy

Received 15 November 2013; Accepted 21 January 2014; Published 26 February 2014

Academic Editor: Cristina Angeloni

Copyright © 2014 Marianna Guida 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. F. V. Rassool, T. J. Gaymes, N. Omidvar et al., “Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia?” Cancer Research, vol. 67, no. 18, pp. 8762–8771, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. W. Guo, Z. Keckesova, J. L. Donaher et al., “Slug and Sox9 cooperatively determine the mammary stem cell state,” Cell, vol. 148, no. 5, pp. 1015–1028, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Mijović and G. J. Mufti, “The myelodysplastic syndromes: towards a functional classification,” Blood Reviews, vol. 12, no. 2, pp. 73–83, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. A. S. Watson, M. Mortensen, and A. K. Simon, “Autophagy in the pathogenesis of myelodysplastic syndrome and acute myeloid leukemia,” Cell Cycle, vol. 10, no. 11, pp. 1719–1725, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. S. D. Nimer, “Myelodysplastic syndromes,” Blood, vol. 111, no. 10, pp. 4841–4851, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Greenberg, C. Cox, M. M. LeBeau et al., “International scoring system for evaluating prognosis in myelodysplastic syndromes,” Blood, vol. 89, no. 6, pp. 2079–2088, 1997. View at Scopus
  7. O. A. Sedelnikova, C. E. Redon, J. S. Dickey, A. J. Nakamura, A. G. Georgakilas, and W. M. Bonner, “Role of oxidatively induced DNA lesions in human pathogenesis,” Mutation Research, vol. 704, no. 1–3, pp. 152–159, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Slupphaug, B. Kavli, and H. E. Krokan, “The interacting pathways for prevention and repair of oxidative DNA damage,” Mutation Research, vol. 531, no. 1-2, pp. 231–251, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Steinboeck, M. Hubmann, A. Bogusch, P. Dorninger, T. Lengheimer, and E. Heidenreich, “The relevance of oxidative stress and cytotoxic DNA lesions for spontaneous mutagenesis in non-replicating yeast cells,” Mutation Research, vol. 688, no. 1-2, pp. 47–52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Themeli, L. Petrikkos, M. Waterhouse et al., “Alloreactive microenvironment after human hematopoietic cell transplantation induces genomic alterations in epithelium through an ROS-mediated mechanism: in vivo and in vitro study and implications to secondary neoplasia,” Leukemia, vol. 24, no. 3, pp. 536–543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Sallmyr, J. Fan, K. Datta et al., “Internal tandem duplication of FLT3 (FLT3/ITD) induces increased ROS production, DNA damage, and misrepair: implications for poor prognosis in AML,” Blood, vol. 111, no. 6, pp. 3173–3182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. M. J. Farquhar and D. T. Bowen, “Oxidative stress and the myelodysplastic syndromes,” International Journal of Hematology, vol. 77, no. 4, pp. 342–350, 2003. View at Scopus
  13. H. Ghoti, J. Amer, A. Winder, E. Rachmilewitz, and E. Fibach, “Oxidative stress in red blood cells, platelets and polymorphonuclear leukocytes from patients with myelodysplastic syndrome,” European Journal of Haematology, vol. 79, no. 6, pp. 463–467, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Novotna, Y. Bagryantseva, M. Siskova, and R. Neuwirtova, “Oxidative DNA damage in bone marrow cells of patients with low-risk myelodysplastic syndrome,” Leukemia Research, vol. 33, no. 2, pp. 340–343, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. C. M. Peddie, C. R. Wolf, L. I. Mclellan, A. R. Collins, and D. T. Bowen, “Oxidative DNA damage in CD34+ myelodysplastic cells is associated with intracellular redox changes and elevated plasma tumour necrosis factor-α concentration,” British Journal of Haematology, vol. 99, no. 3, pp. 625–631, 1997. View at Scopus
  16. A. Sallmyr, J. Fan, and F. V. Rassool, “Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair,” Cancer Letters, vol. 270, no. 1, pp. 1–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. Q. Xu, S.-E. Simpson, T. J. Scialla, A. Bagg, and M. Carroll, “Survival of acute myeloid leukemia cells requires PI3 kinase activation,” Blood, vol. 102, no. 3, pp. 972–980, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Prata, T. Maraldi, D. Fiorentini, L. Zambonin, G. Hakim, and L. Landi, “Nox-generated ROS modulate glucose uptake in a leukaemic cell line,” Free Radical Research, vol. 42, no. 5, pp. 405–414, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Maraldi, C. Prata, F. Vieceli Dalla Sega et al., “NAD(P)H oxidase isoform Nox2 plays a prosurvival role in human leukaemia cells,” Free Radical Research, vol. 43, no. 11, pp. 1111–1121, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Maraldi, C. Prata, C. Caliceti et al., “VEGF-induced ROS generation from NAD(P)H oxidases protects human leukemic cells from apoptosis,” International Journal of Oncology, vol. 36, no. 6, pp. 1581–1589, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Finkel, “Intracellular redox regulation by the family of small GTPases,” Antioxidants and Redox Signaling, vol. 8, no. 9-10, pp. 1857–1863, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Ushio-Fukai, “Compartmentalization of redox signaling through NaDPH oxidase-derived rOS,” Antioxidants and Redox Signaling, vol. 11, no. 6, pp. 1289–1299, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. 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
  24. 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
  25. 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
  26. J. W. Vardiman, N. L. Harris, and R. D. Brunning, “The World Health Organization (WHO) classification of the myeloid neoplasms,” Blood, vol. 100, no. 7, pp. 2292–2302, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Matsuo, R. A. F. MacLeod, C. C. Uphoff et al., “Two acute monocytic leukemia (AML-M5a) cell lines (MOLM-13 and MOLM-14) with interclonal phenotypic heterogeneity showing MLL-AF9 fusion resulting from an occult chromosome insertion, ins(11;9)(q23;p22p23),” Leukemia, vol. 11, no. 9, pp. 1469–1477, 1997. View at Scopus
  28. C. Fabre, G. Carvalho, E. Tasdemir et al., “NF-κB inhibition sensitizes to starvation-induced cell death in high-risk myelodysplastic syndrome and acute myeloid leukemia,” Oncogene, vol. 26, no. 28, pp. 4071–4083, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. 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
  30. 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
  31. J. Bertacchini, F. Beretti, V. Cenni et al., “The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression,” The FASEB Journal, vol. 27, no. 6, pp. 2145–2155, 2013.
  32. 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
  33. 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.
  34. 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.
  35. 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 Scopus
  36. 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
  37. 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
  38. 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.
  39. 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
  40. J. L. Kissil, M. J. Walmsley, L. Hanlon et al., “Requirement for Rac1 in a K-ras-induced lung cancer in the mouse,” Cancer Research, vol. 67, no. 17, pp. 8089–8094, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Ranjan, V. Anathy, P. M. Burch, K. Weirather, J. D. Lambeth, and N. H. Heintz, “Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelial cells,” Antioxidants and Redox Signaling, vol. 8, no. 9-10, pp. 1447–1460, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. 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
  43. M. L. Heaney and D. W. Golde, “Myelodysplasia,” The New England Journal of Medicine, vol. 340, no. 21, pp. 1649–1660, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. S. J. Corey, M. D. Minden, D. L. Barber, H. Kantarjian, J. C. Y. Wang, and A. D. Schimmer, “Myelodysplastic syndromes: the complexity of stem-cell diseases,” Nature Reviews Cancer, vol. 7, no. 2, pp. 118–129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. M. J. Walter, D. Shen, L. Ding et al., “Clonal Architecture of Secondary Acute Myeloid Leukemia,” The New England Journal of Medicine, vol. 366, no. 12, pp. 1090–1098, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. D. G. Gilliland and M. S. Tallman, “Focus on acute leukemias,” Cancer Cell, vol. 1, no. 5, pp. 417–420, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Mori, R. Morosetti, E. Hoflehner, M. Lübbert, H. Mizoguchi, and H. P. Koeffler, “Allelic loss in the progression of myelodysplastic syndrome,” Cancer Research, vol. 60, no. 11, pp. 3039–3042, 2000. View at Scopus
  48. N. Mori, R. Morosetti, H. Mizoguchi, and H. P. Koeffler, “Progression of myelodysplastic syndrome: allelic loss on chromosomal arm 1p,” British Journal of Haematology, vol. 122, no. 2, pp. 226–230, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. R. A. Padua, B.-A. Guinn, A. I. Al-Sabah et al., “RAS, FMS and p53 mutations and poor clinical outcome in myelodysplasias: a 10-year follow-up,” Leukemia, vol. 12, no. 6, pp. 887–892, 1998. View at Scopus
  50. P. Fenaux, “Chromosome and molecular abnormalities in myelodysplastic syndromes,” International Journal of Hematology, vol. 73, no. 4, pp. 429–437, 2001. View at Scopus
  51. X. Deng, F. Gao, and W. S. May Jr., “Bcl2 retards G1/S cell cycle transition by regulating intracellular ROS,” Blood, vol. 102, no. 9, pp. 3179–3185, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. K. D. Mills, D. O. Ferguson, and F. W. Alt, “The role of DNA breaks in genomic instability and tumorigenesis,” Immunological Reviews, vol. 194, pp. 77–95, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Kochetkova, P. O. Iversen, A. F. Lopez, and M. F. Shannon, “Deoxyribonucleic acid triplex formation inhibits granulocyte macrophage colony-stimulating factor gene expression and suppresses growth in juvenile myelomonocytic leukemic cells,” Journal of Clinical Investigation, vol. 99, no. 12, pp. 3000–3008, 1997. View at Scopus
  54. R. Serù, P. Mondola, S. Damiano et al., “HaRas activates the NADPH oxidase complex in human neuroblastoma cells via extracellular signal-regulated kinase 1/2 pathway,” Journal of Neurochemistry, vol. 91, no. 3, pp. 613–622, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. A. M. Martelli, L. Cocco, S. Capitani, S. Miscia, S. Papa, and F. A. Manzoli, “Nuclear phosphatidylinositol 3,4,5-trisphosphate, phosphatidylinositol 3-kinase, Akt, and PTen: emerging key regulators of anti-apoptotic signaling and carcinogenesis,” European Journal of Histochemistry, vol. 51, pp. 125–131, 2007. View at Scopus
  56. M. J. Zeitz, K. S. Malyavantham, B. Seifert, and R. Berezney, “Matrin 3: chromosomal distribution and protein interactions,” Journal of Cellular Biochemistry, vol. 108, no. 1, pp. 125–133, 2009. View at Publisher · View at Google Scholar · View at Scopus