Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 698-705 , October 2010

Cerium oxide nanoparticles protect gastrointestinal epithelium from radiation-induced damage by reduction of reactive oxygen species and upregulation of superoxide dismutase 2

  • Jimmie Colon, MS

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Cancer Research Institute, Orlando, Florida, USA
  • ,
  • Nelson Hsieh

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Cancer Research Institute, Orlando, Florida, USA
  • ,
  • Amber Ferguson

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Cancer Research Institute, Orlando, Florida, USA
  • ,
  • Patrick Kupelian, MD

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Department of Radiation Oncology, Orlando, Florida, USA
  • ,
  • Sudipta Seal, PhD

      Affiliations

    • Department of Mechanical, Materials and Aerospace Engineering, Advanced Materials Processing and Analysis Center (AMPAC), University of Central Florida, Orlando, Florida, USA
    • Nanoscience and Technology Center, University of Central Florida, Orlando, Florida, USA
  • ,
  • D. Wayne Jenkins, MD

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Department of Radiation Oncology, Orlando, Florida, USA
  • ,
  • Cheryl H. Baker, PhD

      Affiliations

    • M.D. Anderson Cancer Center Orlando, Cancer Research Institute, Orlando, Florida, USA
    • Burnett School of Biomedical Sciences, University of Central Florida, Orlando, Florida, USA
    • Corresponding Author InformationCorresponding author: Cancer Research Institute at M.D. Anderson Cancer Center Orlando, Orlando, Florida 32827, USA.

Received 20 July 2009 ,Accepted 25 January 2010.

References 

  1. Meissner K. Late radiogenic small bowel damage: guidelines for the general surgeon. Dig Surg. 1999;16:169–174
  2. Altman KI, Gerber GB, Okada S. Radiation biochemistry. New York: Academic Press; 1970;p. 112-26
  3. Arena V. Ionizing radiation and life. St. Louis: C.V. Mosby; 1971;p. 311-6
  4. Oberley LW, Lindgren AL, Baker SA, Stevens RH. Superoxide ion as the cause of the oxygen effect. Radiat Res. 1976;68:320–328
  5. Biaglow JE, Mitchell JB, Held K. The importance of peroxide and superoxide in the X-ray response. Int J Radiat Oncol Biol Phys. 1992;22:665–669
  6. Hall EJ. Radiobiology for the radiologist. Philadelphia: Lippincott Williams and Wilkins; 2000;p. 16-28
  7. Spitz DR, Azzam EI, Li JJ, Gius D. Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metast Rev. 2004;23:311–322
  8. Fang Y, Yang S, Wu G. Free radicals, antioxidants, and nutrition. Nutrition. 2002;18:872–879
  9. Natarajan AT, Palitti F. DNA repair and chromosomal alterations. Mutat Res. 2008;657:3–7
  10. Dumont M, Eille E, Stack C, Calingasan NY, Beal MF, Lin MT. Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB J. 2009;23:2459–2466
  11. Keller JN, Kindy MS, Holtsberg FW, Clair St, DK YenH, Germeyer A, et al. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci. 1998;18:687–697
  12. Murley JS, Kataoka Y, Weydert CJ, Oberley LW, Grdina DJ. Delayed cytoprotection after enhancement of SOD2 (MnSOD) gene expression in SA-NH mouse sarcoma cells exposed to WR-1065, the active metabolite of amifostine. Radiat Res. 2002;158:101–109
  13. Murley JS, Kataoka Y, Cao D, Li JJ, Oberley LW, Grdina DJ. Delayed radioprotection by NFκB-mediated induction of SOD2(MnSOD) in SA-NH tumor cells after exposure to clinically used thiol-containing drugs. Radiat Res. 2004;162:536–546
  14. Deluga GA, Salge JR, Schmidt LD, Verykios XE. Renewable hydrogen from ethanol by autothermal reforming. Science. 2004;303:993–997
  15. Otsuka K, Ushiyama T, Yamanaka I. Partial oxidation of methane using the redox of cerium oxide. Chem Lett. 1993;9:1517–1520
  16. Trovarelli A. Catalysis by ceria and related materials. London: Imperial College Press; 2002;p. 6-10
  17. Park S, Vohs JM, Gorte RJ. Direct oxidation of hydrocarbons in a solid-oxide fuel cell. Nature. 2000;404:265–267
  18. Rzigalinksi BA, Meehan K, Davis RM, Xu Y, Miles WC, Cohen CA. Radical nanomedicine. Nanomedicine (Lond). 2006;1:399–412
  19. Tarnuzzer RW, Colon J, Patil S, Seal S. Vacancy engineered ceria nanostructures for protection from radiation-induced cellular damage. Nano Lett. 2005;5:2573–2577
  20. Jianli N, Azfer A, Rogers LM, Wang X, Kolattukudy PE. Cardioprotective effects of cerium oxide nanoparticles in a transgenic murine model of cardiomyopathy. Cardiovasc Res. 2007;73:549–559
  21. Korsvik C, Patil S, Seal S, Self WT. Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanoparticles. Chem Commun (Camb). 2007;14:1056–1058
  22. Heckert EG, Karakoti AS, Seal S, Self WT. The role of cerium redox state in the SOD mimetic activity of nanoceria. Biomaterials. 2008;18:2705–2709
  23. Vincent A, Babu S, Heckert E, Dowding J, Hirst S, Inerbaev TM, et al. Protonated nanoparticle surface governing ligand tethering and cellular targeting. ACS Nano. 2009;5:1203–1211
  24. Colon J, Herrera L, Smith J, Patil S, Komanski C, Kupelian P, et al. Protection from radiation-induced pneumonitis using cerium oxide nanoparticles. Nanomed Nanotechnol Biol Med. 2009;5:225–231
  25. Hirst S, Karakoti AS, Tyler RD, Sriranganathan N, Seal S, Reilly CM. Anti-inflammatory properties of cerium oxide nanoparticles. Small. 2009;24:2848–2856
  26. Johnke RA, Smith ES, Cariveau MJ, Evans MJ, Kilburn JM, Bakken NTG, et al. Radioprotection of murine gastrointestinal epithelium by interleukin-1a involves down-regulation of the apoptotic response. Anticancer Res. 2008;28:3601–3608
  27. Kim J, Seok YM, Jung KJ, Park KM. Reactive oxygen species/oxidative stress contributes to progression of kidney fibrosis following transient ischemic injury in mice. Am J Renal Physiol. 2009;297:461–470
  28. Zhao W, Diz DI, Robbins ME. Oxidative damage pathways in relation to normal tissue injury. Br J Radiol. 2007;80:S23–31
  29. Rodriguez JA, Ma S, Liu P, Hrbek J, Evans J, Perez M. Activity of CeOx and TiOx nanoparticles grown on Au(111) in the water-gas shift reaction. Science. 2007;318:1757–1760
  30. Marshman E, Ottewell PD, Potten CS, Watson AJM. Caspase activation during spontaneous and radiation-induced apoptosis in the murine intestine. J Pathol. 2001;195:285–292
  31. Sies H. Oxidative stress. Oxidants and antioxidants. Exp Physiol. 1997;82:291–295
  32. Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J. 1996;10:709–720
  33. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160:1–40
  34. Rahman I. Regulation of nuclear factor-κB, activator protein-1, and glutathione levels by tumor necrosis factor-α and dexamethasone in alveolar epithelial cells. Biochem Pharmacol. 2000;60:1041–1049
  35. Rahman I, Biswas SK, Jimenez LA, Torres M, Forman HJ. Glutathione, stress responses, and redox signaling in lung inflammation. Antioxid Redox Signal. 2005;7:442–459
  36. Rahman I, MacNee W. Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic Biol Med. 2000;28:1405–1420
  37. Wong GH. Protective roles of cytokines against radiation: induction of mitochondrial MnSOD. Biochim Biophys Acta. 1995;1271:205–209
  38. Hirose K, Longo DL, Oppenheim JJ, Matsushima K. Overexpression of mitochondrial manganese superoxide dismutase promotes the survival of tumor cells exposed to interlukin-1, tumor necrosis factor, selected anticancer drugs, and ionizing radiation. FASEB J. 1993;7:361–368
  39. Sun J, Chen Y, Li M, Ge Z. Role of antioxidant enzymes on ionizing radiation resistance. Free Radic Biol Med. 1998;24:586–593
  40. Lin W, Huang Y, Zhou X, Ma Y. Toxicity of cerium oxide nanoparticles in human lung cancer cells. Int J Toxicol. 2006;25:451–457
  41. Murley JS, Kataoka Y, Baker KL, Diamond AM, Morgan WF, Grdina DJ. Manganese superoxide dismutase (SOD2)-mediated delayed radioprotection induced by the free thiol form of amifostine and tumor necrosis factor α. Radiat Res. 2007;167:465–474
  42. Flohe L, Brigelius-Flohe R, Saliou C, Traber MG, Packer L. Redox regulation of NF-κB activation. Free Radic Biol Med. 1997;22:1115–1126
  43. Murley J, Constantinou A, Kamath NS, Grdina DJ. WR1065, an active metabolite of amifostine, affects phosphorylation of topo-isomerase Πα leading to changes in enzyme activity and cell cycle progression in CHO AA8 cells. Cell Prolif. 1997;30:283–294

 This collaboration was made possible through the support of the M. D. Anderson Cancer Center Orlando, University of Central Florida, and the National Science Foundation.

PII: S1549-9634(10)00017-1

doi: 10.1016/j.nano.2010.01.010

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 698-705 , October 2010