Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 476789, 11 pages
http://dx.doi.org/10.1155/2014/476789
Review Article

The Functional Role of MnSOD as a Biomarker of Human Diseases and Therapeutic Potential of a New Isoform of a Human Recombinant MnSOD

Molecular Biology and Viral Oncology Unit, Department of Experimental Oncology, Istituto Nazionale per lo Studio e la Cura dei Tumori “Fondazione G. Pascale”—IRCCS, Naples, Italy

Received 9 October 2013; Accepted 19 November 2013; Published 6 January 2014

Academic Editor: Maria Lina Tornesello

Copyright © 2014 Antonella Borrelli 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. A. S. Kathiria, L. D. Butcher, L. A. Feagins, R. F. Souza, C. R. Boland, and A. L. Theiss, “Prohibitin 1 modulates mitochondrial stress-related autophagy in human colonic epithelial cells,” PLoS One, vol. 7, no. 2, Article ID e31231, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. R. B. Hamanaka and N. S. Chandel, “Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes,” Trends in Biochemical Sciences, vol. 35, no. 9, pp. 505–513, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Matés, C. Pérez-Gómez, and I. Núñez de Castro, “Antioxidant enzymes and human diseases,” Clinical Biochemistry, vol. 32, no. 8, pp. 595–603, 1999. View at Publisher · View at Google Scholar
  4. J. M. Matés, J. A. Segura, F. J. Alonso, and J. Márquez, “Roles of dioxins and heavy metals in cancer and neurological diseases using ROS-mediated mechanisms,” Free Radical Biology and Medicine, vol. 49, no. 9, pp. 1328–1341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. J. M. Matés, J. A. Segura, F. J. Alonso, and J. Márquez, “Intracellular redox status and oxidative stress: implications for cell proliferation, apoptosis, and carcinogenesis,” Archives of Toxicology, vol. 82, no. 5, pp. 273–299, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Raj, T. Ide, A. U. Gurkar et al., “Selective killing of cancer cells by a small molecule targeting the stress response to ROS,” Nature, vol. 475, no. 7355, pp. 231–234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Sosa, T. Moliné, R. Somoza, R. Paciucci, H. Kondoh, and M. E. LLeonart, “Oxidative stress and cancer: an overview,” Ageing Research Reviews, vol. 12, no. 1, pp. 376–390, 2013. View at Publisher · View at Google Scholar
  8. S. Boillée, V. C. Velde, and D. W. Cleveland, “ALS: a disease of motor neurons and their nonneuronal neighbors,” Neuron, vol. 52, no. 1, pp. 39–59, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. W. Brazier, S. R. Doctrow, C. L. Masters, and S. J. Collins, “A manganese-superoxide dismutase/catalase mimetic extends survival in a mouse model of human prion disease,” Free Radical Biology and Medicine, vol. 45, no. 2, pp. 184–192, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Christen, “Oxidative stress and Alzheimer disease,” The American Journal of Clinical Nutrition, vol. 71, no. 2, pp. 621S–629S, 2000. View at Google Scholar
  11. H. Fukui and C. T. Moraes, “The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis?” Trends in Neurosciences, vol. 31, no. 5, pp. 251–256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. R. L. Miller, M. James-Kracke, G. Y. Sun, and A. Y. Sun, “Oxidative and inflammatory pathways in Parkinson's disease,” Neurochemical Research, vol. 34, no. 1, pp. 55–65, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J.-F. Wang, “Defects of mitochondrial electron transport chain in bipolar disorder: implications for mood-stabilizing treatment,” The Canadian Journal of Psychiatry, vol. 52, no. 12, pp. 753–762, 2007. View at Google Scholar · View at Scopus
  14. E. Crimi, L. J. Ignarro, and C. Napoli, “Microcirculation and oxidative stress,” Free Radical Research, vol. 41, no. 12, pp. 1364–1375, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Hoshino, M. Okamoto, S. Takei, Y. Sakazaki, T. Iwanaga, and H. Aizawa, “Redox-regulated mechanisms in asthma,” Antioxidants & Redox Signaling, vol. 10, no. 4, pp. 769–783, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Figueroa-Romero, M. Sadidi, and E. L. Feldman, “Mechanisms of disease: the oxidative stress theory of diabetic neuropathy,” Reviews in Endocrine and Metabolic Disorders, vol. 9, no. 4, pp. 301–314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Hoshino and M. Mishima, “Redox-based therapeutics for lung diseases,” Antioxidants & Redox Signaling, vol. 10, no. 4, pp. 701–704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Aslan, A. Cort, and I. Yucel, “Oxidative and nitrative stress markers in glaucoma,” Free Radical Biology and Medicine, vol. 45, no. 4, pp. 367–376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Nilsson, E. Bengtsson, G. N. Fredrikson, and H. Björkbacka, “Inflammation and immunity in diabetic vascular complications,” Current Opinion in Lipidology, vol. 19, no. 5, pp. 519–524, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Shoham, M. Hadziahmetovic, J. L. Dunaief, M. B. Mydlarski, and H. M. Schipper, “Oxidative stress in diseases of the human cornea,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1047–1055, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. Ungvari, C. Parrado-Fernandez, A. Csiszar, and R. de Cabo, “Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging,” Circulation Research, vol. 102, no. 5, pp. 519–529, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Boveris and A. Navarro, “Brain mitochondrial dysfunction in aging,” IUBMB Life, vol. 60, no. 5, pp. 308–314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. N. S. Brown and R. Bicknell, “Hypoxia and oxidative stress in breast cancer: oxidative stress—its effects on the growth, metastatic potential and response to therapy of breast cancer,” Breast Cancer Research, vol. 3, no. 5, pp. 323–327, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Csiszar, M. Wang, E. G. Lakatta, and Z. Ungvari, “Inflammation and endothelial dysfunction during aging: role of NF-κB,” Journal of Applied Physiology, vol. 105, no. 4, pp. 1333–1341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Toyokuni, “Molecular mechanisms of oxidative stress-induced carcinogenesis: from epidemiology to oxygenomics,” IUBMB Life, vol. 60, no. 7, pp. 441–447, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Mocellin, V. Bronte, and D. Nitti, “Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities,” Medicinal Research Reviews, vol. 27, no. 3, pp. 317–352, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Bartesaghi, G. Ferrer-Sueta, G. Peluffo et al., “Protein tyrosine nitration in hydrophilic and hydrophobic environments,” Amino Acids, vol. 32, no. 4, pp. 501–515, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Bonello, C. Zähringer, R. S. BelAiba et al., “Reactive oxygen species activate the HIF-1α promoter via a functional NFκB site,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 4, pp. 755–761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Du, Z. Adam, R. Rani, X. Zhang, and Q. Pang, “Oxidative stress in Fanconi anemia hematopoiesis and disease progression,” Antioxidants & Redox Signaling, vol. 10, no. 11, pp. 1909–1921, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Hidalgo and P. Donoso, “Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications,” Antioxidants & Redox Signaling, vol. 10, no. 7, pp. 1275–1312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Li, P. Sonveaux, Z. N. Rabbani et al., “Regulation of HIF-1α stability through S-nitrosylation,” Molecular Cell, vol. 26, no. 1, pp. 63–74, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Rubbo and R. Radi, “Protein and lipid nitration: role in redox signaling and injury,” Biochimica et Biophysica Acta, vol. 1780, no. 11, pp. 1318–1324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Salvemini, T. M. Doyle, and S. Cuzzocrea, “Superoxide, peroxynitrite and oxidative/nitrative stress in inflammation,” Biochemical Society Transactions, vol. 34, no. 5, pp. 965–970, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Souza, G. Peluffo, and R. Radi, “Protein tyrosine nitration—functional alteration or just a biomarker?” Free Radical Biology and Medicine, vol. 45, no. 4, pp. 357–366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. C. C. Winterbourn, “Reconciling the chemistry and biology of reactive oxygen species,” Nature Chemical Biology, vol. 4, no. 5, pp. 278–286, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. C. C. Winterbourn and M. B. Hampton, “Thiol chemistry and specificity in redox signaling,” Free Radical Biology and Medicine, vol. 45, no. 5, pp. 549–561, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. J. M. McCord and M. A. Edeas, “SOD, oxidative stress and human pathologies: a brief history and a future vision,” Biomedicine & Pharmacotherapy, vol. 59, no. 4, pp. 139–142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Pauling, “The discovery of the superoxide radical,” Trends in Biochemical Sciences, vol. 4, no. 11, pp. N270–N271, 1979. View at Google Scholar · View at Scopus
  39. T. Mann and D. Keilin, “Haemocuprein and hepatocuprein, copper protein compounds of blood and liver in mammals,” Proceedings of the Royal Society B, vol. 126, no. 844, pp. 303–315, 1938. View at Publisher · View at Google Scholar
  40. W. Huber, T. L. Schulte, S. Carson, R. E. Goldhamer, and E. E. Vogin, “Some chemical and pharmacologic properties of a novel anti-inflammatory protein,” Toxicology and Applied Pharmacology, vol. 12, p. 308, 1968. View at Google Scholar
  41. P. F. Knowles, J. F. Gibson, F. M. Pick, and R. C. Bray, “Electron-spin-resonance evidence for enzymic reduction of oxygen to a free radical, the superoxide ion,” Biochemical Journal, vol. 111, no. 1, pp. 53–58, 1969. View at Google Scholar · View at Scopus
  42. J. M. McCord and I. Fridovich, “Superoxide dismutase. an enzymic function for erythrocuprein (hemocuprein),” The Journal of Biological Chemistry, vol. 244, no. 22, pp. 6049–6055, 1969. View at Google Scholar · View at Scopus
  43. J. M. McCord and I. Fridovich, “The reduction of cytochrome c by milk xanthine oxidase,” The Journal of Biological Chemistry, vol. 243, no. 21, pp. 5753–5760, 1968. View at Google Scholar · View at Scopus
  44. A. Pica, A. Di Santi, F. Basile et al., “Anti-Cancer, anti-Necrotic and Imaging Tumor Marker role of a novel form of Manganese Superoxide Dismutase and its leader peptide,” International Journal of Biology and Biomedical Engineering, vol. 4, no. 3, pp. 53–60, 2010. View at Google Scholar
  45. L. Banci, I. Bertini, F. Cramaro, R. Del Conte, and M. S. Viezzoli, “The solution structure of reduced dimeric copper zinc superoxide dismutase: the structural effects of dimerization,” European Journal of Biochemistry, vol. 269, no. 7, pp. 1905–1915, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. S. I. Liochev and I. Fridovich, “Mechanism of the peroxidase activity of Cu, Zn superoxide dismutase,” Free Radical Biology and Medicine, vol. 48, no. 12, pp. 1565–1569, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Cho, S. Kang, S. J. Seo, Y. Kim, and G. Jung, “The transcriptional repression of the human Cu/Zn superoxide dismutase(sod1) gene by the anticancer drug, mitomycin C(MMC),” Biochemistry and Molecular Biology International, vol. 42, no. 5, pp. 949–956, 1997. View at Google Scholar · View at Scopus
  48. T. Fukai and M. Ushio-Fukai, “Superoxide dismutases: role in redox signaling, vascular function, and diseases,” Antioxidants & Redox Signaling, vol. 15, no. 6, pp. 1583–1606, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. J. M. Matés and F. Sánchez-Jiménez, “Role of reactive oxygen species in apoptosis: implications for cancer therapy,” The International Journal of Biochemistry & Cell Biology, vol. 32, no. 2, pp. 157–170, 2000. View at Google Scholar
  50. M.-L. Sentman, T. Brännström, and S. L. Marklund, “EC-SOD and the response to inflammatory reactions and aging in mouse lung,” Free Radical Biology and Medicine, vol. 32, no. 10, pp. 975–981, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. R. P. Bowler, M. Nicks, D. A. Olsen et al., “Furin proteolytically processes the heparin-binding region of extracellular superoxide dismutase,” The Journal of Biological Chemistry, vol. 277, no. 19, pp. 16505–16511, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Buschfort-Papewalis, T. Moritz, B. Liedert, and J. Thomale, “Down-regulation of DNA repair in human CD34+ progenitor cells corresponds to increased drug sensitivity and apoptotic response,” Blood, vol. 100, no. 3, pp. 845–853, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Nozik-Grayck, H. B. Suliman, and C. A. Piantadosi, “Extracellular superoxide dismutase,” The International Journal of Biochemistry & Cell Biology, vol. 37, no. 12, pp. 2466–2471, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. E. D. Levin, N. C. Christopher, S. Lateef et al., “Extracellular superoxide dismutase overexpression protects against aging-induced cognitive impairment in mice,” Behavior Genetics, vol. 32, no. 2, pp. 119–125, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Carlioz and D. Touati, “Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life?” The EMBO Journal, vol. 5, no. 3, pp. 623–630, 1986. View at Google Scholar · View at Scopus
  56. S. B. Farr, R. D'Ari, and D. Touati, “Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 21, pp. 8268–8272, 1986. View at Google Scholar · View at Scopus
  57. T. Shimizu, H. Nojiri, S. Kawakami, S. Uchiyama, and T. Shirasawa, “Model mice for tissue-specific deletion of the manganese superoxide dismutase gene,” Geriatrics & Gerontology International, vol. 10, no. 1, pp. S70–S79, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. S. K. Dhar and D. K. St. Clair, “Manganese superoxide dismutase regulation and cancer,” Free Radical Biology and Medicine, vol. 52, no. 11-12, pp. 2209–2222, 2012. View at Publisher · View at Google Scholar
  59. B. Meyrick and M. A. Magnuson, “Identification and functional characterization of the bovine manganous superoxide dismutase promoter,” American Journal of Respiratory Cell and Molecular Biology, vol. 10, no. 1, pp. 113–121, 1994. View at Google Scholar · View at Scopus
  60. S. L. Church, J. W. Grant, E. U. Meese, and J. M. Trent, “Sublocalization of the gene encoding manganese superoxide dismutase (MnSOD/SOD2) to 6q25 by fluorescence in Situ hybridization and somatic cell hybrid mapping,” Genomics, vol. 14, no. 3, pp. 823–825, 1992. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Bravard, L. Sabatier, F. Hoffschir, M. Ricoul, C. Luccioni, and B. Dutrillaux, “SOD2: a new type of tumor-suppressor gene?” The International Journal of Cancer, vol. 51, no. 3, pp. 476–480, 1992. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Borrello, M. E. De Leo, and T. Galeotti, “Defective gene expression of MnSOD in cancer cells,” Molecular Aspects of Medicine, vol. 14, no. 3, pp. 253–258, 1993. View at Publisher · View at Google Scholar · View at Scopus
  63. D. K. St. Clair and J. C. Holland, “Complementary DNA encoding human colon cancer manganese superoxide dismutase and the expression of its gene in human cells,” Cancer Research, vol. 51, no. 3, pp. 939–943, 1991. View at Google Scholar · View at Scopus
  64. R. Izutani, S. Asano, M. Imano, D. Kuroda, M. Kato, and H. Ohyanagi, “Expression of manganese superoxide dismutase in esophageal and gastric cancers,” Journal of Gastroenterology, vol. 33, no. 6, pp. 816–822, 1998. View at Publisher · View at Google Scholar · View at Scopus
  65. J. C.-M. Ho, S. Zheng, S. A. A. Comhair, C. Farver, and S. C. Erzurum, “Differential expression of manganese superoxide dismutase and catalase in lung cancer,” Cancer Research, vol. 61, no. 23, pp. 8578–8585, 2001. View at Google Scholar · View at Scopus
  66. Y. Toh, S. Kuninaka, T. Oshiro et al., “Overexpression of manganese superoxide dismutase mRNA may correlate with aggressiveness in gastric and colorectal adenocarcinomas,” International Journal of Oncology, vol. 17, no. 1, pp. 107–112, 2000. View at Google Scholar · View at Scopus
  67. M. Malafa, J. Margenthaler, B. Webb, L. Neitzel, and M. Christophersen, “MnSOD expression is increased in metastatic gastric cancer,” Journal of Surgical Research, vol. 88, no. 2, pp. 130–134, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. A. M. L. Janssen, C. B. Bosman, W. van Duijn et al., “Superoxide dismutases in gastric and esophageal cancer and the prognostic impact in gastric cancer,” Clinical Cancer Research, vol. 6, no. 8, pp. 3183–3192, 2000. View at Google Scholar · View at Scopus
  69. C. Weydert, B. Roling, J. Liu et al., “Suppression of the malignant phenotype in human pancreatic cancer cells by the overexpression of manganese superoxide dismutase,” Molecular Cancer Therapeutics, vol. 2, no. 4, pp. 361–369, 2003. View at Google Scholar · View at Scopus
  70. L. W. Oberley and G. R. Buettner, “Role of superoxide dismutase in cancer: a review,” Cancer Research, vol. 39, no. 4, pp. 1141–1149, 1979. View at Google Scholar · View at Scopus
  71. Y. Soini, M. Vakkala, K. Kahlos, P. Pääkkö, and V. Kinnula, “MnSOD expression is less frequent in tumour cells of invasive breast carcinomas than in in situ carcinomas or non-neoplastic breast epithelial cells,” The Journal of Pathology, vol. 195, no. 2, pp. 156–162, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. T.-C. Chuang, J.-Y. Liu, C.-T. Lin et al., “Human manganese superoxide dismutase suppresses HER2/neu-mediated breast cancer malignancy,” FEBS Letters, vol. 581, no. 23, pp. 4443–4449, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. J. J. Cullen, C. Weydert, M. M. Hinkhouse et al., “The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma,” Cancer Research, vol. 63, no. 6, pp. 1297–1303, 2003. View at Google Scholar · View at Scopus
  74. Y. Hu, D. G. Rosen, Y. Zhou et al., “Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress,” The Journal of Biological Chemistry, vol. 280, no. 47, pp. 39485–39492, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Liu, T. D. Oberley, and L. W. Oberley, “Transfection and expression of MnSOD cDNA decreases tumor malignancy of human oral squamous carcinoma SCC-25 cells,” Human Gene Therapy, vol. 8, no. 5, pp. 585–595, 1997. View at Google Scholar · View at Scopus
  76. S. Venkataraman, X. Jiang, C. Weydert et al., “Manganese superoxide dismutase overexpression inhibits the growth of androgen-independent prostate cancer cells,” Oncogene, vol. 24, no. 1, pp. 77–89, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. J. J. Cullen, F. A. Mitros, and L. W. Oberley, “Expression of antioxidant enzymes in diseases of the human pancreas: another link between chronic pancreatitis and pancreatic cancer,” Pancreas, vol. 26, no. 1, pp. 23–27, 2003. View at Google Scholar
  78. L. Behrend, A. Mohr, T. Dick, and R. M. Zwacka, “Manganese superoxide dismutase induces p53-dependent senescence in colorectal cancer cells,” Molecular and Cellular Biology, vol. 25, no. 17, pp. 7758–7769, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. L. W. Oberley, “Mechanism of the tumor suppressive effect of MnSOD overexpression,” Biomedicine & Pharmacotherapy, vol. 59, no. 4, pp. 143–148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Zhao, Y. Xue, T. D. Oberley et al., “Overexpression of manganese superoxide dismutase suppresses tumor formation by modulation of activator protein-1 signaling in a multistage skin carcinogenesis model,” Cancer Research, vol. 61, no. 16, pp. 6082–6088, 2001. View at Google Scholar · View at Scopus
  81. Y. Zhao, T. D. Oberley, L. Chaiswing et al., “Manganese superoxide dismutase deficiency enhances cell turnover via tumor promoter-induced alterations in AP-1 and p53-mediated pathways in a skin cancer model,” Oncogene, vol. 21, no. 24, pp. 3836–3846, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. C. I. van de Wetering, M. C. Coleman, D. R. Spitz, B. J. Smith, and C. M. Knudson, “Manganese superoxide dismutase gene dosage affects chromosomal instability and tumor onset in a mouse model of T cell lymphoma,” Free Radical Biology and Medicine, vol. 44, no. 8, pp. 1677–1686, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. A. K. Holley, V. Bakthavatchalu, J. M. Velez-Roman, and D. K. St. Clair, “Manganese superoxide dismutase: guardian of the powerhouse,” International Journal of Molecular Sciences, vol. 12, no. 10, pp. 7114–7162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. A. K. Holley, S. K. Dhar, Y. Xu, and D. K. St Clair, “Manganese superoxide dismutase: beyond life and death,” Amino acids, vol. 42, no. 1, pp. 139–158, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. L. A. Ridnour, T. D. Oberley, and L. W. Oberley, “Tumor suppressive effects of MnSOD overexpression may involve imbalance in perokide generation versus peroxide removal,” Antioxidants & Redox Signaling, vol. 6, no. 3, pp. 501–512, 2004. View at Google Scholar · View at Scopus
  86. A. Kim, “Modulation of MnSOD in cancer: epidemiological and experimental evidence,” Toxicological Research, vol. 26, no. 2, pp. 83–93, 2010. View at Publisher · View at Google Scholar
  87. Y. Zhang, B. J. Smith, and L. W. Oberley, “Enzymatic activity is necessary for the tumor-suppressive effects of MnSOD,” Antioxidants & Redox Signaling, vol. 8, no. 7-8, pp. 1283–1293, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. N. Li, T. D. Oberley, L. W. Oberley, and W. Zhong, “Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has mutliple effects on cell phenotype,” Prostate, vol. 35, no. 3, pp. 221–233, 1998. View at Google Scholar
  89. C. A. Davis, A. S. Hearn, B. Fletcher et al., “Potent anti-tumor effects of an active site mutant of human manganese-superoxide dismutase: evolutionary conservation of product inhibition,” The Journal of Biological Chemistry, vol. 279, no. 13, pp. 12769–12776, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. C. Jang, V. I. Pérez, W. Song et al., “Overexpression of Mn superoxide dismutase does not increase life span in mice,” The Journals of Gerontology A, vol. 64, no. 11, pp. 1114–1125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. A. C. Maritim, R. A. Sanders, and J. B. Watkins III, “Diabetes, oxidative stress, and antioxidants: a review,” Journal of Biochemical and Molecular Toxicology, vol. 17, no. 1, pp. 24–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. B. Gao, S. C. Flores, J. A. Leff, S. K. Bose, and J. M. McCord, “Synthesis and anti-inflammatory activity of a chimeric recombinant superoxide dismutase: SOD2/3,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 284, no. 6, pp. L917–L925, 2003. View at Google Scholar · View at Scopus
  93. M. Inoue, I. Ebashi, N. Watanabe, and Y. Morino, “Synthesis of a superoxide dismutase derivative that circulates bound to albumin and accumulates in tissues whose pH is decreased,” Biochemistry, vol. 28, no. 16, pp. 6619–6624, 1989. View at Google Scholar · View at Scopus
  94. B. A. Freeman, S. L. Young, and J. D. Crapo, “Liposome-mediated augmentation of superoxide dismutase in endothelial cells prevents oxygen injury,” The Journal of Biological Chemistry, vol. 258, no. 20, pp. 12534–12542, 1983. View at Google Scholar · View at Scopus
  95. J. F. Turrens, J. D. Crapo, and B. A. Freeman, “Protection against oxygen toxicity by intravenous injection of liposome-entrapped catalase and superoxide dismutase,” The Journal of Clinical Investigation, vol. 73, no. 1, pp. 87–95, 1984. View at Google Scholar · View at Scopus
  96. H. Marberger, W. Huber, and G. Bartsch, “Orgotein: a new antiinflammatory metalloprotein drug. evaluation of clinical efficacy and safety in inflammatory conditions of the urinary tract,” International Urology and Nephrology, vol. 6, no. 2, pp. 61–74, 1974. View at Google Scholar · View at Scopus
  97. S. Delanian, M. Martin, A. Bravard, C. Luccioni, and J.-L. Lefaix, “Cu/Zn superoxide dismutase modulates phenotypic changes in cultured fibroblasts from human skin with chronic radiotherapy damage,” Radiotherapy & Oncology, vol. 58, no. 3, pp. 325–331, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. J. Emerit, A. M. Michelson, H. G. Robert, G. Chomette, R. A. Guerin, and J. Blondon, “[Superoxide dismutase treatment of 2 cases of radiation-induced sclerosis],” La Semaine des Hôpitaux, vol. 59, no. 4, pp. 277–281, 1983. View at Google Scholar
  99. W. Land, H. Schneeberger, S. Schleibner et al., “The beneficial effect of human recombinant superoxide dismutase on acute and chronic rejection events in recipients of cadaveric renal transplants,” Transplantation, vol. 57, no. 2, pp. 211–217, 1994. View at Google Scholar · View at Scopus
  100. P. Matzinger, “The danger model: a renewed sense of self,” Science, vol. 296, no. 5566, pp. 301–305, 2002. View at Publisher · View at Google Scholar · View at Scopus
  101. T. M. Buetler, A. Krauskopf, and U. T. Ruegg, “Role of superoxide as a signaling molecule,” News in Physiological Sciences, vol. 19, no. 3, pp. 120–123, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. E. Werner, “GTPases and reactive oxygen species: switches for killing and signaling,” Journal of Cell Science, vol. 117, no. 2, pp. 143–153, 2004. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Ough, A. Lewis, Y. Zhang et al., “Inhibition of cell growth by overexpression of manganese superoxide dismutase (MnSOD) in human pancreatic carcinoma,” Free Radical Research, vol. 38, no. 11, pp. 1223–1233, 2004. View at Publisher · View at Google Scholar
  104. J. L. Arbiser, J. Petros, R. Klafter et al., “Reactive oxygen generated by Nox1 triggers the angiogenic switch,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 715–720, 2002. View at Publisher · View at Google Scholar · View at Scopus
  105. D. Sorescu, D. Weiss, B. Lassègue et al., “Superoxide production and expression of Nox family proteins in human atherosclerosis,” Circulation, vol. 105, no. 12, pp. 1429–1435, 2002. View at Publisher · View at Google Scholar · View at Scopus
  106. L. Chaiswing, W. Zhong, J. J. Cullen, L. W. Oberley, and T. D. Oberley, “Extracellular redox state regulates features associated with prostate cancer cell invasion,” Cancer Research, vol. 68, no. 14, pp. 5820–5826, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. A. M. Duffy, T. O'Brien, and J. M. McMahon, “Generation of antioxidant adenovirus gene transfer vectors encoding CuZnSOD, MnSOD, and catalase,” Methods in Molecular Biology, vol. 594, pp. 381–393, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. J.-Q. Yang, G. R. Buettner, F. E. Domann et al., “v-Ha-ras mitogenic signaling through superoxide and derived reactive oxygen species,” Molecular Carcinogenesis, vol. 33, no. 4, pp. 206–218, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Q. Yang, S. Li, F. E. Domann et al., “Superoxide generation in v-Ha-ras-transduced human keratinocyte HaCaT cells,” Molecular Carcinogenesis, vol. 26, no. 3, pp. 180–188, 1999. View at Google Scholar
  110. A. A. Tarhini, C. P. Belani, J. D. Luketich et al., “A phase I study of concurrent chemotherapy (paclitaxel and carboplatin) and thoracic radiotherapy with swallowed manganese superoxide dismutase plasmid liposome protection in patients with locally advanced stage III non-small-cell lung cancer,” Human Gene Therapy, vol. 22, no. 3, pp. 336–342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. M. W. Epperly, M. Carpenter, A. Agarwal, P. Mitra, S. Nie, and J. S. Greenberger, “Intraoral manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) radioprotective gene therapy decreases ionizing irradiation-induced murine mucosal cell cycling and apoptosis,” In Vivo, vol. 18, no. 4, pp. 401–410, 2004. View at Google Scholar · View at Scopus
  112. M. W. Epperly, C. J. Epstein, E. L. Travis, and J. S. Greenberger, “Decreased pulmonary radiation resistance of manganese superoxide dismutase (MnSOD)-deficient mice is corrected by human manganese superoxide dismutase-plasmid/liposome (SOD2-PL) intratracheal gene therapy,” Radiation Research, vol. 154, no. 4, pp. 365–374, 2000. View at Google Scholar · View at Scopus
  113. A. Mancini, A. Borrelli, A. Schiattarella et al., “Tumor suppressive activity of a variant isoform of manganese superoxide dismutase released by a human liposarcoma cell line,” The International Journal of Cancer, vol. 119, no. 4, pp. 932–943, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. A. Mancini, C. Garbi, F. D’Armiento, A. Borrelli, and F. S. Ambesi-Impiombato, “Culture and cloning of an adipocytes cell line from a human liposarcoma,” Bollettino dell'Istituto dei Tumori di Napoli, vol. 38, pp. 43–49, 1991. View at Google Scholar
  115. A. Mancini, A. Borrelli, S. Formisano et al., “Establishment and growth regulation of a novel ovarian cancer cell line from a poorly-differentiated adenocarcinoma: proposal for a new treatment,” European Journal of Gynaecological Oncology, vol. 20, no. 1, pp. 45–52, 1999. View at Google Scholar · View at Scopus
  116. A. Mancini, A. Borrelli, M. T. Masucci et al., “A conditioned medium from a human liposarcoma-derived cell line induces p53-dependent apoptosis in several tumor cell lines,” Oncology Reports, vol. 7, no. 3, pp. 629–637, 2000. View at Google Scholar · View at Scopus
  117. A. Mancini, A. Borrelli, A. Schiattarella et al., “Biophysical and biochemical characterization of a liposarcoma-derived recombinant MnSOD protein acting as an anticancer agent,” The International Journal of Cancer, vol. 123, no. 11, pp. 2684–2695, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Borrelli, A. Schiattarella, R. Mancini et al., “A recombinant MnSOD is radioprotective for normal cells and radiosensitizing for tumor cells,” Free Radical Biology and Medicine, vol. 46, no. 1, pp. 110–116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  119. A. Borrelli, A. Schiattarella, R. Mancini et al., “The leader peptide of a human rec. MnSOD as molecular carrier which delivers high amounts of cisplatin into tumor cells inducing a fast apoptosis in vitro,” International Journal of Cancer, vol. 128, no. 2, pp. 453–459, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. A. Borrelli, A. Schiattarella, A. Musella et al., “A molecular carrier to transport and deliver cisplatin into endometrial cancer cells,” Chemical Biology & Drug Design, vol. 80, no. 1, pp. 9–16, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. M. Guillaume, A. Rodriguez-Vilarrupla, J. Gracia-Sancho et al., “Recombinant human manganese superoxide dismutase reduces liver fibrosis and portal pressure in CCI4-cirrhotic rats,” Journal of Hepatology, vol. 58, no. 2, pp. 240–246, 2013. View at Publisher · View at Google Scholar
  122. S. Damiano, F. Trepiccione, R. Ciarcia et al., “A new recombinant MnSOD prevents the Cyclosporine A-induced renal impairment,” Nephrology Dialysis Transplantation, vol. 28, no. 8, pp. 2066–2072, 2013. View at Publisher · View at Google Scholar
  123. A. Pisani, M. Sabbatini, E. Riccio et al., “Effect of a recombinant manganese superoxide dismutase on prevention of contrast-induced acute kidney injury,” Clinical and Experimental Nephrology, 2013. View at Publisher · View at Google Scholar
  124. A. Garcia-Espana, S. Biria, M. Malumbres, B. Levin, D. Meruelo, and A. Pellicer, “Targeted gene transfer system using a streptavidin-transforming growth factor-α chimeric protein,” DNA and Cell Biology, vol. 18, no. 10, pp. 743–749, 1999. View at Publisher · View at Google Scholar · View at Scopus
  125. M. Johnson, “Chemotherapy treatment decision making by professionals and older patients with cancer: a narrative review of the literature,” European Journal of Cancer Care, vol. 21, no. 1, pp. 3–9, 2012. View at Publisher · View at Google Scholar · View at Scopus
  126. M. D. Garrett and I. Collins, “Anticancer therapy with checkpoint inhibitors: what, where and when?” Trends in Pharmacological Sciences, vol. 32, no. 5, pp. 308–316, 2011. View at Publisher · View at Google Scholar · View at Scopus
  127. C.-L. Yu and M.-H. Tsai, “Embryonic apoptosis-inducing proteins exhibited anticancer activity in vitro and in vivo,” Anticancer Research, vol. 21, no. 3B, pp. 1839–1856, 2001. View at Google Scholar · View at Scopus
  128. O. Firuzi, R. Miri, M. Tavakkoli, and L. Saso, “Antioxidant therapy: current status and future prospects,” Current Medicinal Chemistry, vol. 18, no. 25, pp. 3871–3888, 2011. View at Google Scholar · View at Scopus
  129. J. M. Matés, J. A. Segura, F. J. Alonso, and J. M. Márquez, “Natural antioxidants: therapeutic prospects for cancer and neurological diseases,” Mini-Reviews in Medicinal Chemistry, vol. 9, no. 10, pp. 1202–1214, 2009. View at Publisher · View at Google Scholar
  130. J. M. Matés, J. A. Segura, F. J. Alonso, and J. Márquez, “Anticancer antioxidant regulatory functions of phytochemicals,” Current Medicinal Chemistry, vol. 18, no. 15, pp. 2315–2338, 2011. View at Google Scholar · View at Scopus
  131. D. Robbins and Y. Zhao, “The role of manganese superoxide dismutase in skin cancer,” Enzyme Research, Article ID 409295, 2011. View at Google Scholar
  132. A. de Souza Prestes, S. T. Stefanello, S. M. Salman et al., “Antioxidant activity of β-selenoamines and their capacity to mimic different enzymes,” Molecular and Cellular Biochemistry, vol. 365, no. 1-2, pp. 85–92, 2012. View at Publisher · View at Google Scholar · View at Scopus
  133. M. Safavi, A. Foroumadi, M. Nakhjiri et al., “Complexes of 2-hydroxyacetophenone semicarbazones: a novel series of superoxide dismutase mimetics,” Bioorganic & Medicinal Chemistry Letters, vol. 20, no. 10, pp. 3070–3073, 2010. View at Publisher · View at Google Scholar · View at Scopus
  134. R. Thomas and N. Sharifi, “SOD mimetics: a novel class of androgen receptor inhibitors that suppresses castration-resistant growth of prostate cancer,” Molecular Cancer Therapeutics, vol. 11, no. 1, pp. 87–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  135. B. S. Fleenor, D. R. Seals, M. L. Zigler, and A. L. Sindler, “Superoxide-lowering therapy with TEMPOL reverses arterial dysfunction with aging in mice,” Aging Cell, vol. 11, no. 2, pp. 269–276, 2012. View at Publisher · View at Google Scholar · View at Scopus
  136. H. Pan, J. N. Marsh, E. T. Christenson et al., “Postformulation peptide drug loading of nanostructures,” Methods in Enzymology, vol. 508, pp. 17–39, 2012. View at Publisher · View at Google Scholar · View at Scopus
  137. B. Baudin, “New aspects on angiotensin-converting enzyme: from gene to disease,” Clinical Chemistry and Laboratory Medicine, vol. 40, no. 3, pp. 256–265, 2002. View at Publisher · View at Google Scholar · View at Scopus
  138. S. P. Egusquiaguirre, M. Igartua, R. M. Hernández, and J. L. Pedraz, “Nanoparticle delivery systems for cancer therapy: advances in clinical and preclinical research,” Clinical and Translational Oncology, vol. 14, no. 2, pp. 83–93, 2012. View at Publisher · View at Google Scholar
  139. C. S. O. Paulo, R. Pires das Neves, and L. S. Ferreira, “Nanoparticles for intracellular-targeted drug delivery,” Nanotechnology, vol. 22, no. 49, Article ID 494002, 2011. View at Publisher · View at Google Scholar · View at Scopus
  140. R. T. Hogg, P. Thorpe, and R. D. Gerard, “Retargeting adenoviral vectors to improve gene transfer into tumors,” Cancer Gene Therapy, vol. 18, no. 4, pp. 275–287, 2011. View at Publisher · View at Google Scholar · View at Scopus
  141. Y. Kaneda, “Update on non-viral delivery methods for cancer therapy: possibilities of a drug delivery system with anticancer activities beyond delivery as a new therapeutic tool,” Expert Opinion on Drug Delivery, vol. 7, no. 9, pp. 1079–1093, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. Y. Namiki, T. Fuchigami, N. Tada et al., “Nanomedicine for cancer: lipid-based nanostructures for drug delivery and monitoring,” Accounts of Chemical Research, vol. 44, no. 10, pp. 1080–1093, 2011. View at Publisher · View at Google Scholar · View at Scopus
  143. X. Zhai, W. Huang, J. Liu et al., “Micelles from amphiphilic block copolyphosphates for drug delivery,” Macromolecular Bioscience, vol. 11, no. 11, pp. 1603–1610, 2011. View at Publisher · View at Google Scholar · View at Scopus
  144. M. V. Pasquetto, L. Vecchia, D. Covini, R. Digilio, and C. Scotti, “Targeted drug delivery using immunoconjugates: principles and applications,” Journal of Immunotherapy, vol. 34, no. 9, pp. 611–628, 2011. View at Publisher · View at Google Scholar · View at Scopus
  145. R. Dinarvand, N. Sepehri, S. Manoochehri, H. Rouhani, and F. Atyabi, “Polylactide-co-glycolide nanoparticles for controlled delivery of anticancer agents,” International Journal of Nanomedicine, vol. 6, pp. 877–895, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. K. Liu, X. Wang, W. Fan, Q. Zhu, J. Yang, J. Gao et al., “Degradable polyethylenimine derivate coupled to a bifunctional peptide R13 as a new gene-delivery vector,” International Journal of Nanomedicine, vol. 7, pp. 1149–1162, 2012. View at Google Scholar
  147. Y. Yang, Y.-M. Zhang, Y. Chen, D. Zhao, J.-T. Chen, and Y. Liu, “Construction of a graphene oxide based noncovalent multiple nanosupramolecular assembly as a scaffold for drug delivery,” Chemistry, vol. 18, no. 14, pp. 4208–4215, 2012. View at Publisher · View at Google Scholar · View at Scopus