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

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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.

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References

  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.

    Article  Google Scholar 

  2. Han, J.; Burgess, K. Fluorescent indicators for intracellular pH. Chem. Rev. 2010, 110, 2709–2728.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  7. Busa, W. B.; Nuccitelli, R. Metabolic regulation via intracellular pH. Am. J. Physiol. 1984, 246, R409–438.

    Google Scholar 

  8. Casey, J. R.; Grinstein, S.; Orlowski, J. Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell. Biol. 2010, 11, 50–61.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  15. Loiselle, F. B.; Casey, J. R. Measurement of cell pH. Methods Mol. Biol. 2003, 227, 259–280.

    Google Scholar 

  16. Wray, S. Smooth muscle function and intracellular pH: Measurement, regulation and function. Am. J. Physiol. 1988, 254, C213–C225.

    Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  20. Uchiyama, S.; Makino, Y. Digital fluorescent pH sensors. Chem. Comm. 2009, 2646–2648.

    Google Scholar 

  21. Knoll, W.; Interfaces and thin films as seen by bound electromagnetic waves. Annu. Rev. Phys. Chem. 1998, 49, 569–638.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  25. Nakayama, M.; Tagashira, H.; Electrodeposition of layered manganese oxide nanocomposites intercalated with strong and weak polyelectrolytes. Langmuir 2006, 22, 3864–3869.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  33. Caruso, F.; Caruso, R. A.; Möhwald, H. Nanoengineering of inorganic and hybrid hollow spheres by colloidal templating. Science 1998, 282, 1111–1114.

    Article  Google Scholar 

  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. Maxfield, F. R.; Yamashiro, D. J. Endosome acidification and the pathways of receptor-mediated endocytosis. Adv. Exp. Med. Biol. 1987, 225, 189–198.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, College of Engineering, Yonsei University, Seoul, 120-749, Republic of Korea

    Eun Bi Choi, Jihye Choi, Seo Ryung Bae, Hyun-Ouk Kim, Eunji Jang, Byunghoon Kang, Myeong-Hoon Kim & Seungjoo Haam

  2. Department of Radiology, College of Medicine, Yonsei University, Seoul, 120-752, Republic of Korea

    Jin-Suck Suh & Yong-Min Huh

  3. Department of Chemistry, Korea University, Seoul, 136-701, Republic of Korea

    Byeongyoon Kim & Kwangyeol Lee

Authors
  1. Eun Bi Choi
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  2. Jihye Choi
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Correspondence to Yong-Min Huh or Seungjoo Haam.

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Choi, E.B., Choi, J., Bae, S.R. et al. Colourimetric redox-polyaniline nanoindicator for in situ vesicular trafficking of intracellular transport. Nano Res. 8, 1169–1179 (2015). https://doi.org/10.1007/s12274-014-0597-6

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  • DOI: https://doi.org/10.1007/s12274-014-0597-6

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