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Magnetic Fe3O4 nanoparticle catalyzed chemiluminescence for detection of nitric oxide in living cells

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Abstract

Direct and real-time measurement of nitric oxide (NO) in biological media is very difficult due to its transient nature. Fe3O4 nanoparticles (nanoFe3O4) because of their unique catalytic activities have attracted much attention as catalysts in a variety of organic and inorganic reactions. In this work, we have developed a magnetic Fe3O4 nanoparticle-based rapid-capture system for real-time detection of cellular NO. The basic principle is that the nanoFe3O4 can catalyze the decomposition of H2O2 in the system to generate superoxide anion (O2 ·−) and the O2 ·− can serve as an effective NO· trapping agent yielding peroxynitrite oxide anion, ONOO−. Then the concentration of NO in cells can be facilely determined via peroxynitrite-induced luminol chemiluminescence. The linear range of the method is from 10−4 to 10−8 mol/L, and the detection of limit (3σ, n = 11) is as low as 3.16 × 10−9 mol/L. By using this method, the NO concentration in 0.1 and 0.5 mg/L LPS-stimulated BV2 cells was measured as 4.9 and 11.3 μM, respectively. Surface measurements by synchrotron X-ray photoelectron spectroscopy (SRXPS) and scanning transmission X-ray microscopy (STXM) demonstrate the catalytic mechanism of the nanoFe3O4-based system is that the significantly excess Fe(II) exists on the surface of nanoFe3O4 and mediates the rapid heterogeneous electron transfer, thus presenting a new Fe2O3 phase on the surface.

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References

  1. Zhao YX, Fan L, Zhang Y, Zhao H, Li X, Li YP, et al. Hyper-branched Cu@Cu2O coaxial nanowires mesh electrode for ultra-sensitive glucose detection. ACS Appl Mater Interfaces. 2015;7:16802–12.

    Article  CAS  Google Scholar 

  2. Li JL, Xie JL, Gao LX, Li CM. Au nanoparticles–3D graphene hydrogel nanocomposite to boost synergistically in situ detection sensitivity toward cell-released nitric oxide. ACS Appl Mater Interfaces. 2015;7:2726–34.

    Article  CAS  Google Scholar 

  3. Lu C, Liu XJ, Li YF, Yu F, Tang LH, Hu YJ, et al. Multifunctional janus hematite–silica nanoparticles: mimicking peroxidase-like activity and sensitive colorimetric detection of glucose. ACS Appl Mater Interfaces. 2015;7:15395–402.

    Article  CAS  Google Scholar 

  4. Shahbazi F, Amani K. Synthesis, characterization and heterogeneous catalytic activity of diamine-modified silica-coated magnetite-polyoxometalate nanoparticles as a novel magnetically-recoverable nanocatalyst. Catal Commun. 2014;55:57–64.

    Article  CAS  Google Scholar 

  5. Kim S, Lee J, Jang S, Lee H, Sung D, Chang JH. High efficient chromogenic catalysis of tetramethylbenzidine with horseradish peroxidase immobilized magnetic nanoparticles. Biochem Eng J. 2016;105:406–11.

    Article  CAS  Google Scholar 

  6. Nadejdea C, Neamtua M, Schneiderb RJ, Hodoroabab VD, Ababeic G, Panne U. Catalytical degradation of relevant pollutants from waters using magnetic nanocatalysts. Appl Surf Sci. 2015;352:42–8.

    Article  Google Scholar 

  7. Gawandea MB, Mongab Y, Zborila R, Sharma RK. Silica-decorated magnetic nanocomposites for catalytic applications. Coordin Chem Rev. 2015;288:118–43.

    Article  Google Scholar 

  8. Azgomi N, Mokhtary M. Nano-Fe3O4@SiO2 supported ionic liquid as an efficient catalyst for the synthesis of 1,3-thiazolidin-4-ones under solvent-free conditions. J Mol Catal A-Chem. 2015;398:58–64.

    Article  CAS  Google Scholar 

  9. Gawande MB, Zboril R, Malgras V, Yamauchi Y. Integrated nanocatalysts: a unique class of heterogeneous catalysts. J Mater Chem A. 2015;3:8241–5.

    Article  CAS  Google Scholar 

  10. Garry PS, Ezra M, Rowland MJ, Westbrook J, Pattinson KTS. The role of the nitric oxide pathway in brain injury and its treatment—from bench to bedside. Exp Neurol. 2015;263:235–43.

    Article  CAS  Google Scholar 

  11. Li HG, Horke S, Forstermann U. Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis. 2014;237:208–19.

    Article  CAS  Google Scholar 

  12. Weidinger A, Kozlov AV. Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomol. 2015;5:472–84.

    Article  CAS  Google Scholar 

  13. Bonavida B, Garban H. Nitric oxide-mediated sensitization of resistant tumor cells to apoptosis by chemo-immunotherapeutics. Redox Bio. 2015;6:486–94.

    Article  CAS  Google Scholar 

  14. Sander M, Slaga TJ, Harris CC. The 20th aspen cancer conference: mechanisms of toxicity, carcinogenesis, cancer prevention, and cancer therapy 2005. Mol Carcinog. 2010;49:410–28.

    CAS  Google Scholar 

  15. Navarro-Yepes J, Burns M, Anandhan A, Khalimonchuk O, Razo LM, Quintanilla-Vega B, et al. Oxidative stress, redox signaling, and autophagy: cell death versus survival. Antioxid Redox Sign. 2014;21:66–85.

    Article  CAS  Google Scholar 

  16. Wang B, Yin JJ, Zhou XY, Kurash I, Chai ZF, Zhao YL, et al. Physicochemical origin for free radical generation of iron oxide nanoparticles in biomicroenvironment: catalytic activities mediated by surface chemical states. J Phys Chem C. 2013;117:383–92.

    Article  CAS  Google Scholar 

  17. Wang B, Zhou XY, Wang DQ, Yin JJ, Chen HQ, Gao XF, et al. Structure and catalytic activities of ferrous centers confined on the interface between carbon nanotubes and humic acid. Nanoscale. 2015;7:2651–8.

    Article  CAS  Google Scholar 

  18. Miot J, Benzerara K, Morin G, Kappler A, Bernard S, Obst M, et al. Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim Cosmochim Acta. 2009;73:696–711.

    Article  CAS  Google Scholar 

  19. Hall CN, Garthwaite J. What is the real physiological NO concentration in vivo? Nitric Oxide. 2009;21:92–103.

    Article  CAS  Google Scholar 

  20. Huang KT, Huang Z, Kim-Shapiro DB. Nitric oxide red blood cell membrane permeability at high and low oxygen tension. Nitric Oxide. 2007;16:209–16.

    Article  CAS  Google Scholar 

  21. Lim MH, Xu D, Lippard SJ. Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nat Chem Biol. 2006;2:375–80.

    Article  CAS  Google Scholar 

  22. McQuade LE, Mab J, Lowe G, Ghatpande A, Gelperin A, Lippard SJ. Visualization of nitric oxide production in the mouse main olfactory bulb by a cell-trappable copper(II) fluorescent probe. Proc Nat Acad Sci USA. 2010;107:8525–30.

    Article  CAS  Google Scholar 

  23. Yang C, Cao YL, Tao Y, Zhao BL. The ESR method to determine nitric oxide in plants. Methods Enzymol. 2005;396:84–92.

    Article  Google Scholar 

  24. Samouilov A, Zweier JL. Analytical implications of iron dithiocarbamates for measurement of nitric oxide. Methods Enzymol. 2002;352:506–22.

    Article  CAS  Google Scholar 

  25. Kikuchi K, Nagano T, Beckman JS. In: Feelisch M, Stamler JS, editors. Methods in nitric oxide research. New York: John Wiley and Sons Ltd; 1996. p. 479–88.

    Google Scholar 

  26. Zeng TQ, Chen WW, Cirtiu CM, Moores A, Song GH, Li CJ. Fe3O4 nanoparticles: a robust and magnetically recoverable catalyst for three-component coupling of aldehyde, alkyne and amine. Green Chem. 2010;12:570–3.

    Article  CAS  Google Scholar 

  27. Shylesh S, Schünemann V, Thiel WR. Magnetically separable nanocatalysts: bridges between homogeneous and heterogeneous catalysis. Angew Chem Int Ed. 2010;49:3428–59.

    Article  CAS  Google Scholar 

  28. Gao LZ, Zhuang J, Nie L, Zhang JB, Zhang Y, Gu N, et al. Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nat Nanotechnol. 2007;2:577–83.

    Article  CAS  Google Scholar 

  29. Shi F, Tse MK, Poh MM, Brückner A, Zhang SM, Beller M. Tuning catalytic activity between homogeneous and heterogeneous catalysis: improved activity and selectivity of free nano-Fe2O3 in selective oxidations. Angew Chem Int Ed. 2007;46:8866–8.

    Article  CAS  Google Scholar 

  30. Zhang SX, Zhao XL, Niu HY, Shi YL, Cai YQ, Jiang GB. Superparamagnetic Fe3O4 nanoparticles as catalysts for the catalytic oxidation of phenolic and aniline compounds. J Hazar Mater. 2009;167:560–6.

    Article  CAS  Google Scholar 

  31. Guan GJ, Yang L, Mei QS, Zhang K, Zhang ZP, Han MY. Chemiluminescence switching on peroxidase-like Fe3O4 nanoparticles for selective detection and simultaneous determination of various pesticides. Anal Chem. 2012;84:9492–7.

    Article  CAS  Google Scholar 

  32. Radi R, Cosgrove TP, Beckman JS, Freeman BA. Biochem J Peroxynitrite-induced Luminol Chemiluminescence. 1993;290:51–7.

    CAS  Google Scholar 

  33. Huie RE, Padmaja S. The reaction of NO with superoxide. Free Radic Res Commun. 1993;18:195–8.

    Article  CAS  Google Scholar 

  34. Kagan VE, Kapralov AA, Croix CMT, Watkins SC, Kisin ER, Kotchey GP, et al. Lung macrophages “digest” carbon nanotubes using a superoxide/peroxynitrite oxidative pathway. ACS Nano. 2014;8:5610–21.

    Article  CAS  Google Scholar 

  35. Denicola A, Radi R. Peroxynitrite and drug-dependent toxicity. Toxicology. 2005;208:273–88.

    Article  CAS  Google Scholar 

  36. Chen SL, Jian L, Lang HQ. Optimization of peroxynitrite–luminol chemiluminescence system for detecting peroxynitrite in cell culture solution exposed to carbon disulphide. Luminescence. 2003;18:249–53.

    Article  Google Scholar 

  37. Lewis RS, Deen WM. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem Res Toxicol. 1994;7:568–74.

    Article  CAS  Google Scholar 

  38. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol. 1995;268:699–722.

    Google Scholar 

  39. Hetrick EM, Schoenfisch MH. Analytical chemistry of nitric oxide. Annu Rev Anal Chem. 2009;2:409–33.

    Article  CAS  Google Scholar 

  40. Nims RW, Cook JC, Krishna MC (1996) In: Packer L (ed) Methods in enzymology. Academic Press, pp 93–105

  41. Xue XF, Hanna K, Deng NS. Fenton-like oxidation of Rhodamine B in the presence of two types of iron (II, III) oxide. J Hazard Mater. 2009;166:407–14.

    Article  CAS  Google Scholar 

  42. Wang N, Zhu LH, Wang DL, Wang MQ, Lin ZF, Tang HQ. Sono-assisted preparation of highly-efficient peroxidase-like Fe3O4 magnetic nanoparticles for catalytic removal of organic pollutants with H2O2. Ultra Sonochem. 2010;17:526–33.

    Article  CAS  Google Scholar 

  43. Yan SM, Ge SH, Qiao W, Zuo YL. Synthesis of ferromagnetic semiconductor 0.67FeTiO3–0.33Fe2O3 powder by chemical co-precipitation. J Magn Magn Mater. 2010;322:824–6.

    Article  CAS  Google Scholar 

  44. Olasehinde EF, Takeda K, Sakugawa H. Photochemical production and consumption mechanisms of nitric oxide in seawater. Environ Sci Technol. 2010;44:8403–8.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to hte National Natural Science Foundation of China (11375211, 11475195, 11575209), first batch of Natural Science Foundation of Shandong Province (ZR2015BM001), and the Doctoral Startup Foundation of Qilu University of Technology (12042826).

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Authors and Affiliations

  1. School of Materials Science and Engineering, Qilu University of Technology, 3501 Daxue Rd., Jinan, Shandong, 250353, China

    Huiliang Wang & Mei Li

  2. Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics, Chinese Academy of Sciences, 19B Yu Quan Road, Shi JIng Shan District,, Beijing, 100049, China

    Huiliang Wang, Bing Wang, Meng Wang & Weiyue Feng

  3. Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China

    Ibrahim Kurash

  4. Shanghai Synchrotron Radiation Facility, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, 4288 Shuangzhu Hwy, Jiading,, Shanghai, 20180, China

    Xiangzhi Zhang

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  1. Huiliang Wang
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Correspondence to Mei Li or Bing Wang.

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Wang, H., Li, M., Wang, B. et al. Magnetic Fe3O4 nanoparticle catalyzed chemiluminescence for detection of nitric oxide in living cells. Anal Bioanal Chem 408, 5479–5488 (2016). https://doi.org/10.1007/s00216-016-9646-1

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  • DOI: https://doi.org/10.1007/s00216-016-9646-1

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