The rational design of nitric oxide selectivity in single-walled carbon nanotube near-infrared fluorescence sensors for biological detection

Abstract

A major challenge in the synthesis of nanotube or nanowire sensors is to impart selective analyte binding through means other than covalent linkages, which compromise electronic and optical properties. We synthesized a 3,4-diaminophenyl-functionalized dextran (DAP-dex) wrapping for single-walled carbon nanotubes (SWNTs) that imparts rapid and selective fluorescence detection of nitric oxide (NO), a messenger for biological signalling. The near-infrared (nIR) fluorescence of SWNTDAP-dex is immediately and directly bleached by NO, but not by other reactive nitrogen and oxygen species. This bleaching is reversible and shown to be caused by electron transfer from the top of the valence band of the SWNT to the lowest unoccupied molecular orbital of NO. The resulting optical sensor is capable of real-time and spatially resolved detection of NO produced by stimulating NO synthase in macrophage cells. We also demonstrate the potential of the optical sensor for in vivo detection of NO in a mouse model.

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Figure 1: Schematic illustration for NO detection using SWNT–polymer hybrid.
Figure 2: nIR fluorescence response of SWNTDAP-dex hybrid (6) to NO.
Figure 3: Selectivity, sensitivity and bleaching rate of SWNTDAP-dex hybrid (6) for NO.
Figure 4: Spectroscopic analysis for the fluorescence bleaching mechanism of the SWNTDAP-dex hybrid by NO.
Figure 5: Biological NO detection using SWNTDAP-dex hybrid.

References

  1. 1

    Moncada, S., Palmer, R. M. J. & Higgs, E. A. Nitric-oxide – physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109–142 (1991).

  2. 2

    Bredt, D. S. & Snyder, S. H. Nitric oxide – a physiological messenger molecule. Ann. Rev. Biochem. 63, 175–195 (1994).

  3. 3

    Murad, F. Discovery of some of the biological effects of nitric oxide and its role in cell signaling (Nobel lecture). Angew. Chem. Int. Ed. 38, 1857–1868 (1999).

  4. 4

    Furchgott, R. F. Endothelium-derived relaxing factor: discovery, early studies, and identification as nitric oxide (Nobel lecture). Angew. Chem. Int. Ed. 38, 1870–1880 (1999).

  5. 5

    Ignarro, L. J. Nitric oxide: a unique endogenous signaling molecule in vascular biology (Nobel lecture). Angew. Chem. Int. Ed. 38, 1882–1892 (1999).

  6. 6

    Nagano, T. & Yoshimura, T. Bioimaging of nitric oxide. Chem. Rev. 102, 1235–1269 (2002).

  7. 7

    Kojima, H. et al. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal. Chem. 70, 2446–2453 (1998).

  8. 8

    Sasaki, E. et al. Highly sensitive near-infrared fluorescent probes for nitric oxide and their application to isolated organs. J. Am. Chem. Soc. 127, 3684–3685 (2005).

  9. 9

    Lim, M. H., Xu, D. & Lippard, S. J. Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nature Chem. Biol. 2, 375–380 (2006).

  10. 10

    Lim, M. H. & Lippard, S. J. Metal-based turn-on fluorescent probes for sensing nitric oxide. Acc. Chem. Res. 40, 41–51 (2007).

  11. 11

    Robinson, J. K., Bollinger, M. J. & Birks, J. W. Luminol/H2O2 chemiluminescence detector for the analysis of nitric oxide in exhaled breath. Anal. Chem. 71, 5131–5136 (1999).

  12. 12

    Dubey, M., Bernasek, S. L. & Schwartz, J. Highly sensitive nitric oxide detection using X-ray photoelectron spectroscopy. J. Am. Chem. Soc. 129, 6980–6981 (2007).

  13. 13

    Barone, P. W., Baik, S., Heller, D. A. & Strano, M. S. Near-infrared optical sensors based on single-walled carbon nanotubes. Nature Mater. 4, 86–92 (2005).

  14. 14

    Barone, P. W., Parker, R. S. & Strano, M. S. In vivo fluorescence detection of glucose using a single-walled carbon nanotube optical sensor: design, fluorophore properties, advantages, and disadvantages. Anal. Chem. 77, 7556–7562 (2005).

  15. 15

    Barone, P. W. & Strano, M. S. Reversible control of carbon nanotube aggregation for a glucose affinity sensor. Angew. Chem. Int. Ed. 45, 8138–8141 (2006).

  16. 16

    Jeng, E. S., Moll, A. E., Roy, A. C., Gastala, J. B. & Strano, M. S. Detection of DNA hybridization using the near-infrared band-gap fluorescence of single-walled carbon nanotubes. Nano Lett. 6, 371–375 (2006).

  17. 17

    Heller, D. A. et al. Optical detection of DNA conformational polymorphism on single-walled carbon nanotubes. Science 311, 508–511 (2006).

  18. 18

    Jin, H. et al. Divalent ion and thermally induced DNA conformational polymorphism on single-walled carbon nanotubes. Macromolecules 40, 6731–6739 (2007).

  19. 19

    Bachilo, S. M. et al. Structure-assigned optical spectra of single-walled carbon nanotubes. Science 298, 2361–2366 (2002).

  20. 20

    O'Connell, M. J. et al. Band gap fluorescence from individual single-walled carbon nanotubes. Science 297, 593–596 (2002).

  21. 21

    Heller, D. A., Baik, S., Eurell, T. E. & Strano, M. S. Single-walled carbon nanotube spectroscopy in live cells: towards long-term labels and optical sensors. Adv. Mater. 17, 2793–2799 (2005).

  22. 22

    Jin, H., Heller, D. A. & Strano, M. S. Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett. 8, 1577–1585 (2008).

  23. 23

    Strano, M. S. & Jin, H. Where is it heading? Single-particle tracking of single-walled carbon nanotubes. ACS Nano 2, 1749–1752 (2008).

  24. 24

    Choi, J. H. et al. Multimodal biomedical imaging with asymmetric single-walled carbon nanotube/iron oxide nanoparticle complexes. Nano Lett. 7, 861–867 (2007).

  25. 25

    Satishkumar, B. C. et al. Reversible fluorescence quenching in carbon nanotubes for biomolecular sensing. Nature Nanotech. 2, 560–564 (2007).

  26. 26

    Cognet, L. et al. Stepwise quenching of exciton fluorescence in carbon nanotubes by single-molecule reactions. Science 316, 1465–1468 (2007).

  27. 27

    Cherukuri, P. et al. Mammalian pharmacokinetics of carbon nanotubes using intrinsic near-infrared fluorescence. Proc. Natl Acad. Sci. USA 103, 18882–18886 (2006).

  28. 28

    Cherukuri, P., Bachilo, S. M., Litovsky, S. H. & Weisman, R. B. Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells. J. Am. Chem. Soc. 126, 15638–15639 (2004).

  29. 29

    Welsher, K., Liu, Z., Daranciang, D. & Dai, H. Selective probing and imaging of cells with single walled carbon nanotubes as near-infrared fluorescent molecules. Nano Lett. 8, 586–590 (2008).

  30. 30

    O'Connell, M. J., Eibergen, E. E. & Doorn, S. K. Chiral selectivity in the charge-transfer bleaching of single-walled carbon-nanotube spectra. Nature Mater. 4, 412–418 (2005).

  31. 31

    Walsh, A. G. et al. Screening of excitons in single, suspended carbon nanotubes. Nano Lett. 7, 1485–1488 (2007).

  32. 32

    Choi, J. H. & Strano, M. S. Solvatochromism in single-walled carbon nanotubes. Appl. Phys. Lett. 90, 223114 (2007).

  33. 33

    Klinke, C., Chen, J., Afzali, A. & Avouris, P. Charge transfer induced polarity switching in carbon nanotube transistors. Nano Lett. 5, 555–558 (2005).

  34. 34

    Shim, M., Javey, A., Kam, N. W. S. & Dai, H. Polymer functionalization for air-stable n-type carbon nanotube field-effect transistors. J. Am. Chem. Soc. 123, 11512–11513 (2001).

  35. 35

    Usrey, M. L., Lippmann, E. S. & Strano, M. S. Evidence for a two-step mechanism in electronically selective single-walled carbon nanotube reactions. J. Am. Chem. Soc. 127, 16129–16135 (2005).

  36. 36

    Cui, Y., Wei, Q. Q., Park, H. K. & Lieber, C. M. Nanowire nanosensors for highly sensitive and selective detection of biological and chemical species. Science 293, 1289–1292 (2001).

  37. 37

    Eisenhut, M. et al. Melanoma uptake of Tc-99 m complexes containing the N--(2-diethylaminoethyl) benzamide structural element. J. Med. Chem. 45, 5802–5805 (2002).

  38. 38

    Mauzac, M. & Jozefonvicz, J. Anticoagulant activity of dextran derivatives. 1. Synthesis and characterization. Biomaterials 5, 301–304 (1984).

  39. 39

    Li, B. et al. Aqueous phosphoric acid as a mild reagent for deprotection of tert-butyl carbamates, esters, and ethers. J. Org. Chem. 71, 9045–9050 (2006).

  40. 40

    Kikuchi, K., Nagano, T. & Hirobe, M. Novel detection method of nitric oxide using horseradish peroxidase. Biol. Pharm. Bull. 19, 649–651 (1996).

  41. 41

    Zheng, M. & Diner, B. A. Solution redox chemistry of carbon nanotubes. J. Am. Chem. Soc. 126, 15490–15494 (2004).

  42. 42

    Jin, H., Heller, D. A., Kim, J. H. & Strano, M. S. Stochastic analysis of stepwise fluorescence quenching reactions on single-walled carbon nanotubes: single molecule sensors. Nano Lett. 8, 4299–4304 (2008).

  43. 43

    Kuimova, M. K., Yahioglu, G. & Ogilby, P. R. Singlet oxygen in a cell: spatially dependent lifetimes and quenching rate constants. J. Am. Chem. Soc. 131, 332–340 (2009).

  44. 44

    Ricciardolo, F. L. M., Sterk, P. J., Gaston, B. & Folkerts, G. Nitric oxide in health and disease of the respiratory system. Physiol. Rev. 84, 731–765 (2004).

  45. 45

    Zhuang, J. C. & Wogan, G. N. Growth and viability of macrophages continuously stimulated to produce nitric oxide. Proc. Natl Acad. Sci. USA 94, 11875–11880 (1997).

  46. 46

    Pike, C. J., Overman, M. J. & Cotman, C. W. Amino-terminal deletions enhance aggregation of beta-amyloid peptides in-vitro. J. Biol. Chem. 270, 23895–23898 (1995).

  47. 47

    Fenoglio, I. et al. Reactivity of carbon nanotubes: free radical generation or scavenging activity? Free Radic. Biol. Med. 40, 1227–1233 (2006).

  48. 48

    Galano, A. Carbon nanotubes as free-radical scavengers. J. Phys. Chem. C 112, 8922–8927 (2008).

  49. 49

    Bartberger, M. D. et al. The reduction potential of nitric oxide (NO) and its importance to NO biochemistry. Proc. Natl Acad. Sci. USA 99, 10958–10963 (2002).

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Acknowledgements

This work was supported by a Beckman Young Investigator Award to M.S.S., the National Science Foundation and a seed grant from the Center for Environmental Health and Science at the Massachusetts Institute of Technology (MIT). J.H. Kim is grateful for a postdoctoral fellowship from the Korea Research Foundation Grant funded by the Korean Government (KRF-2007-357-D00086). We also thank W.M. Deen in the Department of Chemical Engineering at MIT for discussions on NO diffusion.

Author information

J.H.K. and M.S.S. conceived and designed the experiments. J.H.K. performed the experiments and analysed the data. D.A.H., H.J., P.W.B., C.S. and J.Z. assisted in doing experiments. L.J.T., G.N.W. and S.R.T. discussed the results of biological NO detection and commented on them. J.H.K. and M.S.S. co-wrote the paper.

Correspondence to Michael S. Strano.

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Kim, J., Heller, D., Jin, H. et al. The rational design of nitric oxide selectivity in single-walled carbon nanotube near-infrared fluorescence sensors for biological detection. Nature Chem 1, 473–481 (2009). https://doi.org/10.1038/nchem.332

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