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Nano Research

, Volume 8, Issue 4, pp 1169–1179 | Cite as

Colourimetric redox-polyaniline nanoindicator for in situ vesicular trafficking of intracellular transport

  • Eun Bi Choi
  • Jihye Choi
  • Seo Ryung Bae
  • Hyun-Ouk Kim
  • Eunji Jang
  • Byunghoon Kang
  • Myeong-Hoon Kim
  • Byeongyoon Kim
  • Jin-Suck Suh
  • Kwangyeol Lee
  • Yong-Min Huh
  • Seungjoo Haam
Research Article

Abstract

Vesicular pH modulates the function of many organelles and plays a pivotal role in cell metabolism processes such as proliferation and apoptosis. Here, we introduce a simple colorimetric redox-polyaniline nanoindicator, which can detect and quantify a broader biogenic pH range with superior sensitivity compared to pre-established trafficking agents employing one-dimensional turn-on of the fluorescence resonance-energy-transfer (FRET) signal. We fabricated polyaniline-based nanoprobes, which exhibited convertible transition states according to the proton levels, as an in situ indicator of vesicular transport pH. Silica-coated Fe3O4-MnO heterometal nanoparticles were synthesised and utilised as a metal oxidant to polymerise the aniline monomer. Finally, silica-coated polyaniline nanoparticles with adsorbed cyanine dye fluorophores Cy3 and Cy7 (FPSNICy3 and FPSNICy7) were fabricated as proton-sensitive nanoindicators. Owing to the selective quenching induced by the local pH variations of vesicular transport, FPSNICy3 and FPSNICy7 demonstrated excellent intracellular trafficking and provided sensitive optical indication of minute proton levels.

Keywords

redox pH intracellular compartments organic quencher conducting polymer nanoindicator 

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References

  1. [1]
    Chiu, Y.-L.; Chen, S.-A.; Chen, J.-H.; Chen, K.-J.; Chen, H.-L.; Sung, H.-W. A dual-emission Förster resonance energy transfer nanoprobe for sensing/imaging pH changes in the biological environment. ACS Nano 2010, 4, 7467–7474.CrossRefGoogle Scholar
  2. [2]
    Han, J.; Burgess, K. Fluorescent indicators for intracellular pH. Chem. Rev. 2010, 110, 2709–2728.CrossRefGoogle Scholar
  3. [3]
    Andreev, O. A.; Dupuy, A. D.; Segala, M.; Sandugu, S.; Serra, D. A.; Chichester, C. O.; Engelman, D. M.; Reshetnyak, Y. K. Mechanism and uses of a membrane peptide that targets tumors and other acidic tissues in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 7893–7898.CrossRefGoogle Scholar
  4. [4]
    Schafer, F. Q.; Buettner, G. R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2011, 30, 1191–1212.CrossRefGoogle Scholar
  5. [5]
    Lewis, J. G.; Lin, K.Y.; Kothavale, A.; Flanagan, W. M.; Matteucci, M. D.; Deprince, R. B.; Mook, R. A.; Hendren, R. A.; Wagner, R. W. A serum-resistant cytofectin for cellular delivery of antisense oligodeoxynucleotides and plasmid DNA. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 3176–3181.CrossRefGoogle Scholar
  6. [6]
    Liu, Y.; Reineke, T. M. Poly(glycoamidoamine)s for gene delivery. Structural effects on cellular internalization, buffering capacity, and gene expression. Bioconjugate Chem. 2007, 18, 19–30.CrossRefGoogle Scholar
  7. [7]
    Busa, W. B.; Nuccitelli, R. Metabolic regulation via intracellular pH. Am. J. Physiol. 1984, 246, R409–438.Google Scholar
  8. [8]
    Casey, J. R.; Grinstein, S.; Orlowski, J. Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell. Biol. 2010, 11, 50–61.CrossRefGoogle Scholar
  9. [9]
    Reineke, T. M.; Davis, M. E. Structural effects of carbohydrate-containing polycations on gene delivery. 2. Charge center type. Bioconjugate Chem. 2003, 14, 255–261.CrossRefGoogle Scholar
  10. [10]
    Perez-Sala, D.; Collado-Escobar, D.; Mollinedo, F. Intracellular alkalinization suppresses lovastatin-induced apoptosis in HL-60 cells through the inactivation of a pH-dependent endonuclease. J. Biol. Chem. 1995, 270, 6235–6242.CrossRefGoogle Scholar
  11. [11]
    Shi, W.; Li, X.; Ma, H. A tunable ratiometric pH sensor based on carbon nanodots for the quantitative measurement of the intracellular pH of whole cells. Angew. Chem. Int. Edit. 2012, 51, 6432–6435.CrossRefGoogle Scholar
  12. [12]
    Peng, H. S.; Stolwijk, J. A.; Sun, L. N.; Wegener, J.; Wolfbeis, O. S. A nanogel for ratiometric fluorescent sensing of intracellular pH values. Angew. Chem. Int. Edit. 2010, 49, 4246–4249.CrossRefGoogle Scholar
  13. [13]
    Davies, T. A.; Fine, R. E.; Johnson, R. J.; Levesque, C. A.; Rathbun, W. H.; Seetoo, K. F.; Smith, S. J.; Strohmeier, G.; Volicer, L.; Delva, L.; Simons, E.R. Non-age related differences in thrombin responses by platelets from male patients with advanced Alzheimer’s disease. Biochem. Biophy. Res. Commun. 1993, 194, 537–543.CrossRefGoogle Scholar
  14. [14]
    Izumi, H.; Torigoe, T.; Ishiguchi, H.; Uramoto, H.; Yoshida, Y.; Tanabe, M.; Ise, T.; Murakami, T.; Yoshida, T.; Nomoto, M.; Kohno, K. Cellular pH regulators: Potentially promising molecular targets for cancer chemotherapy. Cancer. Treat. Rev. 2003, 29, 541–549.CrossRefGoogle Scholar
  15. [15]
    Loiselle, F. B.; Casey, J. R. Measurement of cell pH. Methods Mol. Biol. 2003, 227, 259–280.Google Scholar
  16. [16]
    Wray, S. Smooth muscle function and intracellular pH: Measurement, regulation and function. Am. J. Physiol. 1988, 254, C213–C225.Google Scholar
  17. [17]
    Mátyus, L.; Szöllosi, J.; Jenei, A. Steady-state fluorescence quenching applications for studying protein structure and dynamics. J. Photochem. Photobiol. B: Biol. 2006, 83, 223–236.CrossRefGoogle Scholar
  18. [18]
    Zhuang, X.; Ha, T.; Kim, H. D.; Centner, T.; Labeit, S.; Chu, S. Fluorescence quenching: A tool for single-molecule protein-folding study. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 14241–14244.CrossRefGoogle Scholar
  19. [19]
    Coupland, P. G.; Briddon, S. J.; Aylott, J. W. Using fluorescent pH-sensitive nanosensors to report their intracellular location after Tat-mediated delivery. Integr. Biol. 2009, 1, 318–323.CrossRefGoogle Scholar
  20. [20]
    Uchiyama, S.; Makino, Y. Digital fluorescent pH sensors. Chem. Comm. 2009, 2646–2648.Google Scholar
  21. [21]
    Knoll, W.; Interfaces and thin films as seen by bound electromagnetic waves. Annu. Rev. Phys. Chem. 1998, 49, 569–638.CrossRefGoogle Scholar
  22. [22]
    Febvay, S.; Marini, D. M.; Belcher, A. M.; Clapham, D. E. Targeted cytosolic delivery of cell-impermeable compounds by nanoparticle-mediated, light-triggered endosome disruption. Nano. Lett. 2010, 10, 2211–2219.CrossRefGoogle Scholar
  23. [23]
    Li, N.; Chang, C.; Pan, W.; Tang, B. A multicolor nanoprobe for detection and imaging of tumor-related mrnas in living cells. Angew. Chem. Int. Edit. 2012, 51, 7426–7430.CrossRefGoogle Scholar
  24. [24]
    Gizdavic-Nikolaidis, M.; Travas-Sejdic, J.; Bowmaker, G. A.; Cooney, R. P.; Kilmartin, P. A. Conducting polymers as free radical scavengers. Synth. Metals 2004, 140, 225–232.CrossRefGoogle Scholar
  25. [25]
    Nakayama, M.; Tagashira, H.; Electrodeposition of layered manganese oxide nanocomposites intercalated with strong and weak polyelectrolytes. Langmuir 2006, 22, 3864–3869.CrossRefGoogle Scholar
  26. [26]
    Yang, J.; Choi, J.; Bang, D.; Kim E.; Lim, E.-K.; Park, H.; Suh J.-S.; Lee, K.; Yoo, K.-H.; Kim, E.-K.; et al. Convertible organic nanoparticles for near-infrared photothermal ablation of cancer cells. Angew. Chem. Int. Edit. 2011, 50, 441–444.CrossRefGoogle Scholar
  27. [27]
    Choi, J.; Hong, Y.; Lee, E.; Kim, M.-H.; Yoon, D. S.; Suh, J.; Huh, Y.; Haam, S.; Yang J. Redox-sensitive colorimetric polyaniline nanoprobes synthesized by a solvent-shift process. Nano. Res. 2013, 6, 356–364.CrossRefGoogle Scholar
  28. [28]
    Leff, D. V.; Ohara, P. C.; Heath, J. R.; Gelbart, W. M. Thermodynamic control of gold nanocrystal size: Experiment and theory. J. Phys. Chem. 1995, 99, 7036–7041.CrossRefGoogle Scholar
  29. [29]
    Talapin, D. V.; Rogach, A. L.; Haase, M.; Weller, H. Evolution of an ensemble of nanoparticles in a colloidal solution: Theoretical study. J. Phys. Chem. B 2001, 105, 12278–12285.CrossRefGoogle Scholar
  30. [30]
    Guo, S. R.; Gong, J.-Y.; Jiang, P.; Wu, M.; Lu, Y.; Yu, S. H. Biocompatible, luminescent silver@phenol formaldehyde resin core/shell nanospheres: Large-scale synthesis and application for in vivo bioimaging. Adv. Funct. Mater. 2008, 18, 872–879.CrossRefGoogle Scholar
  31. [31]
    Phan, V. N.; Lim, E.-K.; Kim, T.; Kim, M.; Choi, Y.; Kim, B.; Lee, M.; Oh, A.; Jin, J.; Chae, Y.; et al. A highly crystalline manganese-doped iron oxide nanocontainer with predesigned void volume and shape for theranostic applications. Adv. Mater. 2013, 25, 3202–3208.CrossRefGoogle Scholar
  32. [32]
    Kamata, K.; Lu, Y.; Xia, Y. Synthesis and characterization of monodispersed core-shell spherical colloids with movable cores. J. Am. Chem. Soc. 2003, 125, 2384–2385.CrossRefGoogle Scholar
  33. [33]
    Caruso, F.; Caruso, R. A.; Möhwald, H. Nanoengineering of inorganic and hybrid hollow spheres by colloidal templating. Science 1998, 282, 1111–1114.CrossRefGoogle Scholar
  34. [34]
    Jang, J.; Ha, J.; Lim, B. Synthesis and characterization of monodisperse silica-polyaniline core-shell nanoparticles. Chem. Comm. 2006, 1622–1624.Google Scholar
  35. [35]
    Maxfield, F. R.; Yamashiro, D. J. Endosome acidification and the pathways of receptor-mediated endocytosis. Adv. Exp. Med. Biol. 1987, 225, 189–198.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Eun Bi Choi
    • 1
  • Jihye Choi
    • 1
  • Seo Ryung Bae
    • 1
  • Hyun-Ouk Kim
    • 1
  • Eunji Jang
    • 1
  • Byunghoon Kang
    • 1
  • Myeong-Hoon Kim
    • 1
  • Byeongyoon Kim
    • 3
  • Jin-Suck Suh
    • 2
  • Kwangyeol Lee
    • 3
  • Yong-Min Huh
    • 2
  • Seungjoo Haam
    • 1
  1. 1.Department of Chemical and Biomolecular Engineering, College of EngineeringYonsei UniversitySeoulRepublic of Korea
  2. 2.Department of Radiology, College of MedicineYonsei UniversitySeoulRepublic of Korea
  3. 3.Department of ChemistryKorea UniversitySeoulRepublic of Korea

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