Fish Physiology and Biochemistry

, Volume 38, Issue 4, pp 963–975 | Cite as

Impact of silicon-based quantum dots on the antioxidative system in white muscle of Carassius auratus gibelio

  • Loredana Stanca
  • Sorina Nicoleta Petrache
  • Mihaela Radu
  • Andreea Iren Serban
  • Maria Cristina Munteanu
  • Daniela Teodorescu
  • Andreea Cristina Staicu
  • Cornelia Sima
  • Marieta Costache
  • Constantin Grigoriu
  • Otilia Zarnescu
  • Anca Dinischiotu
Article

Abstract

Silicon-based quantum dots were intraperitoneally injected in individuals of Carassius auratus gibelio. Their effects on white muscle were investigated by following their distribution and impact on the antioxidative system. The GSH level significantly increased after 1 and 3 days of exposure by, respectively, 85.3 and 25.4%. Seven days later, GSH levels were similar to control concentrations. MDA concentration rose after three days by 46.9% and remained at the same level after 7 days. Protein thiol levels significantly decreased by 6.7 and 8.1% after 3 and 7 days, whereas advanced oxidation protein products increased by 12.7, respectively, 28.1% in the same time intervals. The protein reactive carbonyl groups were raised only after the first day of exposure and returned to the control level later on. SOD specific activity increased up to 48% after 7 days, while CAT activity increased by 328, 176, and 26% after 1, 3, and 7 days of treatment. GST specific activity was up-regulated by 87, 18, and 9%, while GR activity increased by 68, 34, and 9%. G6PD activity was up-regulated by 12, 22, and 50%, whereas GPx activity raised by 75 and 109% compared to control after, respectively, 1, 3, and 7 days. Our results suggest that oxidative stress induced by silicon-based quantum dots was not strong enough to cause permanent damage in the white muscle of crucian carp.

Keywords

Fish white muscle Silicon-based quantum dots Malondialdehyde Reduced glutathione Antioxidative enzymes Protein oxidation 

Notes

Acknowledgments

This study was financially supported by the National Research Council of Higher Education, Romania, grant number 127TE/2010 and Grant POSDRU 88/1.5/S/61150/2010 co-financed from European Social Fund by the Sectorial Operational Program for Development of Human Resources 2007–2010. The authors are grateful to COST CM1001/2010 Action for the opportunity to change ideas with experts in post-translational modifications of proteins. We also thank Prof. Radu Burlacu for his advice concerning statistical analysis.

References

  1. Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York and London, pp 673–677Google Scholar
  2. Aksenov MY, Aksenova MV, Butterfield DA, Geddes JW WRM (2001) Protein oxidation in the brain in Alzheimer’s disease. Neuroscience 103:373–383PubMedCrossRefGoogle Scholar
  3. Albertson RC, Cresko W, Detrich IHW, Postlethwait JH (2009) Evolutionary mutant models for human disease. Trends Genet 25:74–81PubMedCrossRefGoogle Scholar
  4. Alderman CJ, Shah S, Foreman JC, Cham BM, Katz DR (2002) The role of advanced oxidation protein products in regulation of dendritic cell function. Free Rad Biol Med 32:377–385PubMedCrossRefGoogle Scholar
  5. Anderson EJ, Neufer PD (2006) Type II skeletal myofibers possess unique properties. That potentiate mitochondrial H2O2 generation. Am J Physiol Cell Physiol 290:844–851CrossRefGoogle Scholar
  6. Bakalova R, Ohba H, Zhelev Z, Nagase T, Jose R, Ishikawa M, Baba Y (2004) Quantum dot anti-CD conjugate: are they potential photosensitizers or potentiators of classical photosensitizing agents in photodynamic therapy of cancer? Nano Lett 4:1567–1573CrossRefGoogle Scholar
  7. Bentolila LA, Ebenstein Y, Weiss S (2009) Quantum dots for in vivo small-animal imaging. J Nucl Med 50:493–496PubMedCrossRefGoogle Scholar
  8. Beutler E (1984) Red cell metabolism. In: Beutler E (ed) A manual of biochemical methods. Grune and Stratton, Orlando, pp 68–73Google Scholar
  9. Bruchez M, Moronne M, Gin P, Weiss S, Alivisatos AP (1998) Semiconductor nanocrystals as fluorescent biological labels. Science 281:2013−2016Google Scholar
  10. Catala A (2010) A synopsis of the process of lipid peroxidation since the discovery of the essential fatty acids. Biochem Biophys Res Commun 399:318–323PubMedCrossRefGoogle Scholar
  11. Chakraborty C, Hsu CS, Wen ZH, Lin CS, Agoramoorthy G (2009) Zebrafish: A complete animal model for in vivo drug discovery and development. Curr Drug Metab 10:116–124PubMedCrossRefGoogle Scholar
  12. Chan WCW, Nie S (1998) Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 281:2016–2018PubMedCrossRefGoogle Scholar
  13. Chan W-H, Shiao N-H (2008) Cytotoxic effect of CdSe quantum dots on mouse embryonic development. Acta Pharmacol Sin 28:259–266CrossRefGoogle Scholar
  14. Chang E, Thekkek N, Yu WW, Colvin VL, Drezek R (2006) Evaluation of quantum dot toxicity based on intracellular uptake. Small 2:1412–1417PubMedCrossRefGoogle Scholar
  15. Cho M, Cho WS, Choi M, Kim SJ, Han BS, Kim SH, Kim HO, Sheen YY, Jeong J (2009) The impact of size on tissue distribution and elimination by single intravenous injection of silica nanoparticles. Toxicol Lett 189:177–183PubMedCrossRefGoogle Scholar
  16. Colston JT, de la Rosa SD, Strader JR, Anderson MA, Freeman GL (2005) H2O2 activates Nox4 through PLA2-dependent arachidonic acid production in adult cardiac fibroblast. FEBS Lett 579:2533–2540PubMedCrossRefGoogle Scholar
  17. De Boeck G, Ngo TTH, Van Campenhout K, Blust R (2003) Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquat Toxicol 65:413–424PubMedCrossRefGoogle Scholar
  18. Debbage P, Jaschke W (2008) Molecular imaging with nanoparticles: giant roles for dwarf actors. Histochem Cell Biol 130:845–875PubMedCrossRefGoogle Scholar
  19. del Rio D, Pellegrini N, Colombi B, Bianchi M, Serafini M, Torta F, Tegoni SM, Musci M, Brighenti F (2003) Rapid fluorimetric method to detect total plasma malondialdehyde with mild derivatization conditions Clin Chem 49:690–692Google Scholar
  20. Dinu D, Marinescu D, Munteanu MC, Staicu AC, Costache M, Dinischiotu A (2010) Modulatory effects of deltamethrin on antioxidant defence mechanisms and lipid peroxidation in carassius auratus gibelio liver and intestine. Arch Env Contam Toxicol 58:757–764CrossRefGoogle Scholar
  21. Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress and other physiological effects. Aquatic Toxicol 84:415–430CrossRefGoogle Scholar
  22. Fields R, Dixon HBF (1971) Micro method for determination of reactive carbonyl groups in proteins and peptides, using 2, 4-dinitrophenylhydrazine. Biochem J 121:587–589PubMedGoogle Scholar
  23. Filipovska A, Murphy MP (2006) Overview of protein glutathionylation. Curr Protocols Toxicol 28:6.10.11–16.10.18Google Scholar
  24. Ford T, Beitinger TL (2005) Temperature tolerance in the goldfish, Carassius auratus. J Therm Biol 30:147–152CrossRefGoogle Scholar
  25. Gao X, Cui J, Levenson RM, Chung LW, Nie S (2004) In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 22:969–976PubMedCrossRefGoogle Scholar
  26. Gatti AM, Kirkpatrick J, Gambarelli A, Capitani F, Hansen T, Eloy R, Clermont G (2008) ESEM evaluations of muscle/nanoparticles interface in a rat model. J Mater Sci Mater Med 19:1515–1522PubMedCrossRefGoogle Scholar
  27. Gerhard GS (2007) Small laboratory fish as models for aging research. Ageing Res Rev 6:64–72PubMedCrossRefGoogle Scholar
  28. Goldberg DM, Spooner RJ (1983) Glutathione reductase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 111. Verlag Chemie, Weinheim, pp 258–265Google Scholar
  29. Gomez-Cabrera MC, Borrás C, Pallardó FV, Sastre J, Ji LL, Vinã J (2005) Decreasing xanthine-oxidase -mediated oxidative stress prevents useful cellular adaptation to exercise in rats. JPhysiol 567:113–120CrossRefGoogle Scholar
  30. Green M, Howman E (2005) Semiconductor quantum dots and free radical induced DNA nicking. Chem Commun 1:121–123CrossRefGoogle Scholar
  31. Grigoriu C, Nicolae I, Ciupina V, Prodan G, Suematsu H, Yatsui K (2004) Influence of the experimental parameters on silicon nanoparticles produced by laser ablation. J Optoelectr Adv Mat 6:825–830Google Scholar
  32. Grigoriu C, Kuroki Y, Nicolae I, Zhu X, Hirai M, Suematsu H, Takata M, Yatsui K (2005) Photo and cathodoluminescence of Si/SiO2 nanoparticles produced by laser ablation. J Optoelectr Adv Mat 7:2979–2984Google Scholar
  33. Grosser T, Yusuff S, Cheskis E, Pack MA, FitzGerald GA (2002) Developmental expression of functional cyclooxigenases in zebrafish. Proc Natl Acad Sci 99:8418–8423PubMedCrossRefGoogle Scholar
  34. Haberland ME, Fong D, Cheng L (1988) Malondialdehyde-altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science 241:215–218PubMedCrossRefGoogle Scholar
  35. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  36. Hazen SL, Hsu FF, Gaut JP, Crowley JR, Heinecke JW (1999) Modification of proteins and lipids by myeloperoxidase. Methods Enzymol 300:88–105PubMedCrossRefGoogle Scholar
  37. Hegazi MM, Attia ZI, Ashour OA (2010) Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat Toxicol 15:118–125CrossRefGoogle Scholar
  38. Jamieson T, Bakhshi R, Petrova D, Pocock R, Imani M, Seifalian AM (2007) Biological applications of quantum dots. Biomaterials 28:4717–4732PubMedCrossRefGoogle Scholar
  39. Kaisto T, Rahkila P, Marjomäki V, Parton RG, Metsikkö K (1999) Endocytosis in skeletal muscle fibers. Exp Cell Res 253:551–560PubMedCrossRefGoogle Scholar
  40. Kim JS, Yoon TJ, Yu KN, Kim BG, Park SJ, Kim HW, Lee KH, Park SB, Lee JK, Cho MH (2006) Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol Sci 89:338–347PubMedCrossRefGoogle Scholar
  41. Kletzien RF, Harris PK, Foellmi LA (1994) Glucose-6-phosphate dehydrogenase: a “housekeeping” enzyme subject to tissue-specific regulation by hormones, nutrients and oxidant stress. FASEB J 8:174–181PubMedGoogle Scholar
  42. Lee K-H (2007) Quantum dots for molecular imaging. J Nucl Med 48:1408–1410PubMedCrossRefGoogle Scholar
  43. Li F, Zhang Z-P, Peng J, Ciu Z-Q, Pang D-W, Li K, Wei H-P, Zhou Y-F, Wen J-K, Zhang X-E (2009) Imaging viral behavior in mammalian cells with self- assembled capsid- quantum dot hybrid particles. Small 5:718–726PubMedCrossRefGoogle Scholar
  44. Li ZH, Zlabek V, Velisek J, Grabic R, Machova J, Randak T (2010) Physiological condition status and muscle-based biomarkers in rainbow trout (Oncorhynchus mykiss), after long-term exposure to carbamazepine. J Appl Toxicol 30:197–203PubMedGoogle Scholar
  45. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8:353–367PubMedCrossRefGoogle Scholar
  46. Liu T, Li L, Teng X, Huang X, Liu H, Chen D, Ren J, He J, Tang F (2011) Single and repeated dose toxicity of mesoporous hollow silica nanoparticles in intravenously exposed mice. Biomaterials 32:1657–1668PubMedCrossRefGoogle Scholar
  47. Lohr GW, Waller HD (1974) Glucose-6-phosphate dehydrogenase. In: Bergmeyer HV (ed) Methods of Enzymatic Analysis. Academic Press, New York and London, pp 744–751Google Scholar
  48. Lovric J, Bazzi HS, Cuie Y, Fortin GRA, Winnik FM, Maysinger D (2005) Differences in subcellular distribution and toxicity of green and red emitting CdTe quantum dots. J Mol Med 83:377–385PubMedCrossRefGoogle Scholar
  49. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin-Phenol reagents. J Biol Chem 193:265–275PubMedGoogle Scholar
  50. Mahto SK, Yoon TH, Rhee SW (2010) Cytotoxic effects of surface-modified quantum dots on neuron-like PC12 cells cultured inside microfluidic devices. Biochip J 4:82–88CrossRefGoogle Scholar
  51. Malis CD, Bonventre JV (1986) Mechanism of calcium potentiation of oxygen free radical injury to renal mitochondria: A model for post-ischemic and toxic mitochondrial damage. J Biol Chem 261:14201–14208PubMedGoogle Scholar
  52. Månsson A, Sundberg M, Balaz M, Bunk R, Nicholls IA, Omling P, Tågerud S, Montelius L (2004) In vitro sliding of actin filaments labeled with single quantum dots. Biochem Biophys Res Commun 314:529–534PubMedCrossRefGoogle Scholar
  53. Micic OI, Sprague JR, Curtis CJ, Jones KM, Machol JL, Nozik AJ, Giessen H, Fluegel B, Mohs G, Peyghambarian N (1995) Synthesis and characterization of InP, GaP, and GaInP2 quantum dots. J Phys Chem 99:7754–7759CrossRefGoogle Scholar
  54. Mitchell DL, Fernandez AA, Nairn RS, Garcia R, Paniker L, Trono D, Thames HD, Gimenez-Conti I (2010) Ultraviolet A does not induce melanomas in a Xiphophorus hybrid fish model. Proc Natl Acad Sci 107:9329–9334PubMedCrossRefGoogle Scholar
  55. Moghimi SM, Hunter AC, Murray JC (2005) Nanomedicine: current status and future perspectives. FASEB J 19:311–330PubMedCrossRefGoogle Scholar
  56. Monteiro DA, De Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion) Comparative biochemistry and physiology. Toxicology pharmacology CBP 143:141–149Google Scholar
  57. Moyle PB, Cech JJJ (2004) Reproduction in fishes-an introduction in ichthyology. Prentice Hall Inc., NJGoogle Scholar
  58. Moylen JS, Reid MB (2007) Oxidative Stress chronic disease and muscle wasting. Muscle Nerve 35:411–429CrossRefGoogle Scholar
  59. Muller-Borer BJ, Collins MC, Gunst PR, Cascio WE, Kypson AP (2007) Quantum dot labeling of mesenchymal stem cells. J Nanobiotech 5:1–19CrossRefGoogle Scholar
  60. O’Farrell N, Houlton A, Horrocks BR (2006) Silicon nanoparticles: applications in cell biology and medicine. Int J Nanomed 1:451–472CrossRefGoogle Scholar
  61. Olaviyan CIO (1975) An introduction to West African ecology. Heinemann Educational Book Ltd, LondonGoogle Scholar
  62. Paoletti F, Mocali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NADP(H) oxidation. Methods Enzymol 186:209–221PubMedCrossRefGoogle Scholar
  63. Park JH, Gu L, von Maltzahn G, Ruoslahti E, Bhatia SN, Sailor MJ (2009) Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nat Mater 8:331–336PubMedCrossRefGoogle Scholar
  64. Pi QM, Zhang WJ, Zhou GD, Liu W, Cao Y (2010) Degradation or excretion of quantum dots in mouse embryonic stem cells. BMC Biotechnol 10:36–45PubMedCrossRefGoogle Scholar
  65. Powers SK, Jackson MJ (2008) Exercise -induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276PubMedCrossRefGoogle Scholar
  66. Powers SK, Duarte J, Kavazis AN, Talbert EE (2010) Reactive Oxygen species are signaling molecules for skeletal muscle adaptation. Exp Physiol 95:1–9PubMedCrossRefGoogle Scholar
  67. Raisuddin S, Lee J-S (2008) Fish models in impact assessment of carcinogenic potential of environmental chemical pollutants: An appraisal of hermaphroditic Mangrove Killifish Kryptolebias marmoratus. In: Murakami Y, Nakayama K, Kitamura S-I, Iwata H, Tanabe S (eds) Interdisciplinary studies on environmental chemistry-biological responses to chemical pollutants. Terrapub, Tokyo, pp 7–15Google Scholar
  68. Rajesh M, Sulochana KN, Coral K, Punitham R, Biswas J, Babu K, Ramakrishnan S (2004) Determination of carbonyl group content in plasma proteins as a useful marker to assess impairment in antioxidant defence in patients with Eales’ disease. Ind J Ophtal 52:139–144Google Scholar
  69. Rieger S, Kulkarmi RP, Darcy D, Fraser SE, Köster RW (2005) Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos. Dev Dyn 234:670–681PubMedCrossRefGoogle Scholar
  70. Riener C, Kada G, Gruber HJ (2002) Quick measurement of protein sulfhydryls with Ellman’s reagent and with 4, 4′-dithiodipyridine. Anal Bioanal Chem 373:266–276PubMedCrossRefGoogle Scholar
  71. Rowley AF (1996) The evolution of inflammatory mediators. Mediators Inflamm 5:3–13PubMedCrossRefGoogle Scholar
  72. Rutkowska M, Strzyewski K, Iskra M, Piorunka-Stolzmann M, Majewski W (2005) Increased protein carbonyl groups in the serum of men with chronic arterial occlusion and the effect of postoperative treatment. Med Sci Monit 11:79–83Google Scholar
  73. Sen CK, Packer L (1996) Antioxidant and redox regulation of gene transcription. FASEB J 10:709–720PubMedGoogle Scholar
  74. Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32:307–326PubMedCrossRefGoogle Scholar
  75. Shaw BJ, Handy RD (2011) Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environ Int 37:1083–1097PubMedCrossRefGoogle Scholar
  76. Son SW, Kim JH, Kim SH, Kim H, Chung AY, Choo JB, Oh CH, Park HC (2009) Intravital imaging in zebrafish using quantum dots. Skin Res Technol 15:157–160PubMedCrossRefGoogle Scholar
  77. Sun D, Yang K, Zheng G, Li Z, Cao Y (2010) Study on effect of peptide-conjugated near-infrared fluorescent quantum dots on the clone formation, proliferation, apoptosis and tumorigenicity ability of human buccal squamous cell carcinoma cell line BcaCD885. Int J Nanomed 5:401–405CrossRefGoogle Scholar
  78. Torres-Ramos YD, Garcia-Guillen ML, Olivares-Corichi IM, Hicks JJ (2009) Correlation of Plasma Protein Carbonyls and C-reactive Protein with GOLD Stage Progression in COPD Patients. Open Resp Med J 3:61–66CrossRefGoogle Scholar
  79. Walling MA, Novak JA, Shepard JRE (2009) Quantum dots for live cell and in vivo imaging. Int J Mol Sci 10:441–491PubMedCrossRefGoogle Scholar
  80. Winterbourn CC, Metodieva D (1994) The reactions superoxide with reduced glutathione. Arch Biochem Biophys 314:284–290PubMedCrossRefGoogle Scholar
  81. Witko-Sarsat V, Nguyen AT, Descamp S, Latsha B (1992) Microtitre plate assay for phagocyte derived taurine chloroaminea. J Clin Lab Annals 6:47–53CrossRefGoogle Scholar
  82. Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Ngnyen-Khoa T, Nguyen AT, Zingraff J, Yungers P, Deschamps-Latecha B (1996) Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49:1304–1313PubMedCrossRefGoogle Scholar
  83. Witko-Sarsat V, Friedlander M, Khoa TN, Capeillère-Blandin C, Nguyen AT, Cantelup S, Dayer J-M, Jungers P, Drüeke T, Descamps-Latscha B (1998) Advanced Oxidation Protein Products as Novel Mediators of Inflamation and Monocyte Activation in Chronic Renal Failure. J Immunol 161:2524–2532PubMedGoogle Scholar
  84. Wittbrodt J, Shima A, Schartl M (2002) Medaka- a model organism from the far East. Nature Rev Genet 3:53–64PubMedCrossRefGoogle Scholar
  85. Xie G, Sun J, Zhong G, Shi L, Zhang D (2010) Biodistribution and toxicity of intravenously administered silica nanoparticles in mice. Arch Toxicol 84:183–190PubMedCrossRefGoogle Scholar
  86. Yu WW, Peng X (2002) Formation of high-quality CdS and other II-VIs semiconductor nanocrystals in noncoordinating solvents: Tunable reactivity of monomers. Angew Chemie 41:2368–2371CrossRefGoogle Scholar
  87. Zhang H, Yee D, Wang C (2008) Quantum dots for cancer diagnosis and therapy: Biological and clinical perspectives. Nanomed 3:83–91CrossRefGoogle Scholar
  88. Zhang LW, Monteiro-Riviere NA (2009) Mechanisms of quantum dot nanoparticles cellular uptake. Toxicol Sci 110:138–155Google Scholar
  89. Zhu Z-J, Carboni R, Quercio JMJ, Yan B, Miranda OR, Anderton DL, Arcado KF, Rotello VM, Vachet RW (2010) Surface properties dictate uptake, distribution, excretion and toxicity of nanoparticles in fish. Small 6:2261–2265PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Loredana Stanca
    • 1
  • Sorina Nicoleta Petrache
    • 1
  • Mihaela Radu
    • 1
  • Andreea Iren Serban
    • 1
    • 2
  • Maria Cristina Munteanu
    • 1
  • Daniela Teodorescu
    • 1
  • Andreea Cristina Staicu
    • 1
  • Cornelia Sima
    • 3
  • Marieta Costache
    • 1
  • Constantin Grigoriu
    • 3
  • Otilia Zarnescu
    • 1
  • Anca Dinischiotu
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyFaculty of Biology, University of BucharestBucharestRomania
  2. 2.Department of Preclinical SciencesFaculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary MedicineBucharestRomania
  3. 3.Laser DepartmentNational Institute of Laser, Plasma and Radiation PhysicsBucharest-MagureleRomania

Personalised recommendations