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Effects of SOD/catalase mimetic platinum nanoparticles on radiation-induced apoptosis in human lymphoma U937 cells

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Abstract

Since polyacrylic acid capped platinum nano-particles (nano-Pts) are known to have a unique ability to quench superoxide (O2 −) and hydrogen peroxide (H2O2), the anti-oxidant activity of nano-Pts against apoptosis induced by x-irradiation in human lymphoma U937 cells was investigated. DNA fragmentation assay, Annexin V-FITC/PI by flow cytometry and Giemsa staining revealed a significant decrease in apoptosis induced by 10 Gy, when cells were pre-treated with nano-Pts in a dose-dependent manner. Pre-treatment with nano-Pts significantly decreased radiation-induced reactive oxygen species (ROS) production, Fas expression and loss of mitochondrial membrane potential as determined by flow-cytometry. Furthermore, western blot analysis also showed that the expression of cleaved caspase-3, Bid and cytosolic cytochrome-c were significantly reduced in nano-Pts pretreated cells. Due to the catalase mimetic activity of nano-Pts, these results indicate that pre-treatment of U937 cells with nano-Pts significantly protect radiation-induced apoptosis by inhibiting intracellular ROS (mainly H2O2), which plays a key role in the induction of apoptosis, because of no practical observation of intracellular O2 − formation.

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Abbreviations

Nano-Pts:

Platinum nano particles

ROS:

Reactive oxygen species

H2O2 :

Hydrogen peroxide

O −2 :

Superoxide

OH:

Hydroxyl radical

OCl− :

Hypochlorite

NO:

Nitric oxide

ONOO:

Peroxynitrite

SOD:

Superoxide dismutase

References

  1. Borek C (2004) Antioxidants and Radiation Therapy. J Nutr 134:3207–3209

    Google Scholar 

  2. Riley PA (1994) Free radical in biology: oxidative stress and the effects of ionization radiation. Int J Radiat Biol 65:27–33

    Article  PubMed  CAS  Google Scholar 

  3. Miyata H, Doki Y, Yamamoto H et al (2001) Overexpression of CDC25B overrides radiation-induced G2-M arrest and results in increased apoptosis in esophageal cancer cells. Cancer Res 61:3188–3193

    PubMed  CAS  Google Scholar 

  4. Corbiere C, Liagre B, Terro F, Beneytout JL (2004) Induction of antiproliferative effect by diosgenin through activation of p53, release of apoptosis-inducing factor (AIF) and modulation of caspase-3 activity in different human cancer cells. Cell Res 14:188–196

    Article  PubMed  CAS  Google Scholar 

  5. Sasano N, Enomoto A, Hosoi Y et al (2007) Free radical scavenger edaravone suppresses X-ray induced apoptosis through p53 inhibition in MOLT-4 cells. J Radiat Res 48:495–503

    Article  PubMed  CAS  Google Scholar 

  6. Tominaga H, Kodama S, Matsuda N, Suzuki K, Watanabe M (2004) Involvement of reactive oxygen species (ROS) in the induction of genetic instability by radiation. J Radiat Res 45:181–188

    Article  PubMed  CAS  Google Scholar 

  7. Zhang B, Su Y, Ai G, Wang Y, Wang T, Wang F (2005) Involvement of Peroxiredoxin I in protecting cells from radiation-induced death. J Radiat Res 46:305–312

    Article  PubMed  CAS  Google Scholar 

  8. Bhattacharya R, Mukherjee P (2008) Biological properties of ‘‘naked’’ metal nanoparticles. Adv Drug Deliv Rev 60:1289–1306

    Article  PubMed  CAS  Google Scholar 

  9. Kajita M, Hikosaka K, Iitsuka M, Kanayama A, Toshima N, Miyamoto Y (2007) Platinum nanoparticle is a useful scavenger of superoxide anion and hydrogen peroxide. Free Radic Res 41:615–626

    Article  PubMed  CAS  Google Scholar 

  10. Yoshihisa Y, Zhao QL, Hassan MA et al (2010) SOD/catalase mimetic platinum nanoparticles inhibit heat-induced apoptosis in human lymphoma U937 and HH cells. Free Radic Res 45:326–335

    Article  PubMed  CAS  Google Scholar 

  11. Yoshihisa Y, Honda A, Zhao QL et al (2010) Protective effect of platinum nanoparticles against UV-light induced epidermal inflammation. Exp Dermatol 19:1000–1006

    Article  PubMed  CAS  Google Scholar 

  12. Roucoux A, Schulz J, Patin H (2002) Reduced transition metal colloids: a novel family of reusable catalyst? Chem Rev 102:3757–3778

    Article  PubMed  CAS  Google Scholar 

  13. Rehman MU, Yoshihisa Y, Miyamoto Y, Shimizu T (2012) The anti-inflammatory effect of platinum nanoparticles on the lipopolysaccharide induced inflammatory response in RAW 264.7 macrophages. Inflamm Res 61:1177–1185

    Article  PubMed  CAS  Google Scholar 

  14. Kim J, Takahashi M, Shimizu T et al (2008) Effects of potent antioxidant platinum nanoparticle, on life span of Caenorhabditis elegans. Mech Ageing Dev 129:322–331

    Article  PubMed  CAS  Google Scholar 

  15. Sellins KS, Cohen JJ (1987) Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J Immunol 139:3199–3206

    PubMed  CAS  Google Scholar 

  16. Royall JA, Ischiropoulos H (1993) Evaluation of 2′,7′-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 302:348–355

    Article  PubMed  CAS  Google Scholar 

  17. Setsukinai KI, Urano Y, Kakinumas K, Majima HJ, Nagano T (2003) Development of novel fluorescence probes that can reliably detect Reactive oxygen species and distinguish specific species. J Biol Chem 278:3170–3175

    Article  PubMed  Google Scholar 

  18. Toshima N, Yonezawa T (1998) Bimetallic nanoparticles novel materials for chemical and physical applications. New J Chem 22:1179–1201

    Article  CAS  Google Scholar 

  19. Mazza J, Rossi A, Weinberg JM (2010) Innovative uses of tumor necrosis factor alpha inhibitors. Dermatol Clin 28:559–575

    Article  PubMed  CAS  Google Scholar 

  20. Jamieson ER, Lippard SJ (1999) Structure, recognition, and processing of cisplatin–DNA adducts. Chem Rev 99:2467–2498

    Article  PubMed  CAS  Google Scholar 

  21. Asharani PV, Xinyi N, Hande MP, Valiyaveettil S (2010) DNA damage and p53-mediated growth arrest in human cells treated with platinum nanoparticles. Nanomedicine 5:51–64

    Article  PubMed  CAS  Google Scholar 

  22. Zhang X, Zhou X, Chen R, Zhang H (2012) Radiosensitization by inhibiting complex I activity in human hepatoma HepG2 cells to X-ray radiation. J Radiat Res 53:257–263

    Article  PubMed  Google Scholar 

  23. Hall EJ (2010) The physics and chemistry of radiation absorption. In: Hall EJ (ed) Radiobiology for the radiologist, 7th edn. Lippincott for Williams and Wilkins, New York, pp 1–16

    Google Scholar 

  24. Cui ZG, Kondo T, Feril JLB, Waki K, Inanami O, Kuwabara M (2004) Effects of antioxidants on x-ray or hyperthermia induced apoptosis in human lymphoma U937 cells. Apoptosis 9:757–763

    Article  PubMed  CAS  Google Scholar 

  25. Salganik RI (2001) The benefits and hazards of antioxidants: controlling apoptosis and other protective mechanism in cancer patients and the human population. J Am Coll Nutr 20:464S–475S

    Article  PubMed  CAS  Google Scholar 

  26. Bhuyan BK, Goppi VE (1989) Cell cycle specific inhibitors. Pharm Ther 42:307–348

    Article  CAS  Google Scholar 

  27. Yamada T, Ohyama H (1988) Radiation-induced interphase death of rat thymocytes in internally programmed (apoptosis). Int J Radiat Biol 53:65–75

    Article  CAS  Google Scholar 

  28. Cui ZG, Kondo T, Ogawa R et al (2004) Enhancement of radiation-induced apoptosis by 6-formylpterin. Free Radic Res 38:363–373

    Article  PubMed  CAS  Google Scholar 

  29. Nitobe J, Yamaguchi S, Okuyama M et al (2003) Reactive oxygen species regulate FLICE inhibitory protein (FLIP) and susceptibility to Fas-mediated apoptosis in cardiac myocytes. Cardiovasc Res 57:119–128

    Article  PubMed  CAS  Google Scholar 

  30. Embree-Ku M, Venturini D, Boekelheide K (2002) Fas is involved in the p53-dependent apoptotic response to ionizing radiation in mouse testis. Biol Reprod 66:1456–1461

    Article  PubMed  CAS  Google Scholar 

  31. Strasser A, Newton K (1999) FADD/MORT1, a signal transducer that can promote cell death or cell growth. Int J Biochem Cell Biol 31:533–537

    Article  PubMed  CAS  Google Scholar 

  32. Yin XM (2000) Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Res 10:161–167

    Article  PubMed  CAS  Google Scholar 

  33. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933

    PubMed  CAS  Google Scholar 

  34. Campion SN, Sandrof MA, Yamasaki H, Boekelheide K (2010) Suppression of radiation-induced testicular germ cell apoptosis by 2,5-hexanedione pretreatment. III. Candidate gene analysis identifies a role for Fas in the attenuation of X-ray–induced apoptosis. Toxicol Sci 117:466–474

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  35. Yu DY, Zhao QL, Wei ZL et al (2009) Enhancement of radiation induced apoptosis of human lymphoma U937 cells by sanazole. Apoptosis 14:655–664

    Article  PubMed  CAS  Google Scholar 

  36. Kolesnick R, Fuks Z (2003) Radiation and ceramide-induced apoptosis. Oncogene 22:5897–5906

    Article  PubMed  CAS  Google Scholar 

  37. Nomura M, Yoshimura Y, Kikuiri T et al (2011) Platinum nano particles suppress Osteoclastogenesis through scavenging of reactive oxygen species produced in RAW 264.7 cells. J Pharmacol Sci 117:243–252

    Article  PubMed  CAS  Google Scholar 

  38. Onizawa S, Aoshiba K, Kajita M, Miyamoto Y, Nagai A (2009) Platinum nanoparticle antioxidants inhibit pulmonary inflammation in mice exposed to cigarette smoke. Pulm Pharmacol Ther 22:340–349

    Article  PubMed  CAS  Google Scholar 

  39. Chen M, Wang J (2002) Initiator caspases in apoptosis signaling pathways. Apoptosis 7:313–319

    Article  PubMed  CAS  Google Scholar 

  40. Granville DJ, Gottlieb RA (2002) Mitochondria: regulators of cell death and survival. Sci World J 2:1569–1578

    Article  Google Scholar 

  41. Esposti MD (2002) The roles of Bid. Apoptosis 7:433–440

    Article  PubMed  CAS  Google Scholar 

  42. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Radiological Sciences, Graduate School of Medicine and Pharmaceutical Sciences University of Toyama, Toyama, Japan

    Paras Jawaid, Peng Li, Qing li Zhao, Mariame Ali Hassan & Takashi Kondo

  2. Department of Dermatology, Graduate School of Medicine and Pharmaceutical Sciences University of Toyama, Toyama, Japan

    Mati ur Rehman, Yoko Yoshihisa & Tadamichi Shimizu

  3. Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba, Japan

    Yusei Miyamoto

Authors
  1. Paras Jawaid
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  2. Mati ur Rehman
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  3. Yoko Yoshihisa
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  4. Peng Li
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  5. Qing li Zhao
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  6. Mariame Ali Hassan
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  7. Yusei Miyamoto
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  9. Takashi Kondo
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Correspondence to Takashi Kondo.

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Jawaid, P., Rehman, M.u., Yoshihisa, Y. et al. Effects of SOD/catalase mimetic platinum nanoparticles on radiation-induced apoptosis in human lymphoma U937 cells. Apoptosis 19, 1006–1016 (2014). https://doi.org/10.1007/s10495-014-0972-5

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