Advertisement

Analytical and Bioanalytical Chemistry

, Volume 411, Issue 27, pp 7127–7136 | Cite as

Construction of a novel cell-trappable fluorescent probe for hydrogen sulfide (H2S) and its bio-imaging application

  • Xiangpeng Lin
  • Yunling Chen
  • Shoujuan Wang
  • Keyin LiuEmail author
  • Fangong KongEmail author
Research Paper

Abstract

Fluorescence detection of H2S in living organisms is greatly advantageous because it is nondestructive and can be used for in situ analysis. We have constructed a novel rhodamine analogue dye (Rho630) by extending the conjugated system of rhodamine to create a novel cell-trappable H2S fluorescent probe Rho630-AM-H2S with red light emission. Its application for H2S fluorescence detection in living HeLa cells and zebrafish was investigated. As expected, Rho630-AM-H2S showed a huge fluorescence turn-on response of about 20-fold at 630 nm and good selectivity toward H2S in solution. An MTT assay demonstrated that the probe showed negligible cytotoxicity in the concentrations typically used in fluorescence imaging experiments. Cell imaging experiments revealed that compared with compound 4 without cell-trappable unit modification, Rho630-AM-H2S exhibited remarkably enhanced cell penetration ability, as an enormous fluorescence signal increase was observed at the red channel within 5 min after Rho630-AM-H2S was incubated with HeLa cells. Finally, the probe Rho630-AM-H2S was used to detect H2S in living HeLa cells and zebrafish with great fluorescence enhancement in the red channel.

Graphical abstract

Keywords

Rhodamine analogue Cell-trappable probe H2S detection Bio-imaging 

Notes

Funding information

This work was financially supported by NSFC (61605060, 31600472, 31570566, and 31800499), the Natural Science Foundation of Shandong Province (ZR2017LEM009), the Foundation of Key Laboratory of Pulp and Paper Science and Technology of Ministry of Education/Shandong Province of China (Nos. ZR201707 and ZR201710), the Key Research and Development Program of Shandong Province (No. 2019GSF107052; 2017GSF17130), the Foundation of Guangxi Key Laboratory of Clean Pulp & Papermaking and Pollution Control of China (KF201717), and the Undergraduate Innovation and Entrepreneurship Program.

Compliance with ethical standards

All animal procedures for this study were approved by the Animal Ethical Experimentation Committee of Shandong University according to the requirements of the National Act on the use of experimental animals (China).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

216_2019_2090_MOESM1_ESM.pdf (1.1 mb)
ESM 1 (PDF 1164 kb)

References

  1. 1.
    Perridon BW, Leuvenink HGD, Hillebrands J-L, van Goor H, Bos EM. The role of hydrogen sulfide in aging and age-related pathologies. Aging-Us. 2016;8(10):2264–89.Google Scholar
  2. 2.
    Fernandes VS, Hernandez M. The role of nitric oxide and hydrogen sulfide in urinary tract function. Basic Clin Pharmacol. 2016;119:34–41.Google Scholar
  3. 3.
    Cuevasanta E, Moller MN, Alvarez B. Biological chemistry of hydrogen sulfide and persulfides. Arch Biochem Biophys. 2017;617:9–25.PubMedGoogle Scholar
  4. 4.
    Rose P, Moore PK, Zhu YZ. H2S biosynthesis and catabolism: new insights from molecular studies. Cell Mol Life Sci. 2017;74(8):1391–412.PubMedGoogle Scholar
  5. 5.
    Hou L, Zhu D, Ma Q, Zhang D, Liu X. H2S synthetase AtD-CDes involves in ethylene and drought regulated stomatal movement. Sci Bull. 2017;61(15):1171–5.Google Scholar
  6. 6.
    Sen N. Functional and molecular insights of hydrogen sulfide signaling and protein sulfhydration. J Mol Biol. 2017;429(4):543–61.PubMedGoogle Scholar
  7. 7.
    Perry SF, Tzaneva V. The sensing of respiratory gases in fish: mechanisms and signalling pathways. Respir Physiol Neurobiol. 2016;224:71–9.PubMedGoogle Scholar
  8. 8.
    Vicente JB, Colaco HG, Malagrino F, Santo PE, Gutierres A, Bandeiras TM, et al. A clinically relevant variant of the human hydrogen sulfide-synthesizing enzyme cystathionine beta-synthase: increased CO reactivity as a novel molecular mechanism of pathogenicity? Oxidative Med Cell Longev. 2017;2017:8940321.Google Scholar
  9. 9.
    Tomasova L, Dobrowolski L, Jurkowska H, Wrobel M, Huc T, Ondrias K, et al. Intracolonic hydrogen sulfide lowers blood pressure in rats. Nitric Oxide Biol Chem. 2016;60:50–8.Google Scholar
  10. 10.
    Liu X, Fu Z, Wu Y, Hu X Jr, Zhu T Jr, Jin C Jr. Neuroprotective effect of hydrogen sulfide on acute cauda equina injury in rats. Spine J. 2016;16(3):402–7.PubMedGoogle Scholar
  11. 11.
    Donatti AF, Soriano RN, Andrade Leite-Panissi CR, Branco LGS, de Souza AS. Anxiolytic-like effect of hydrogen sulfide (H2S) in rats exposed and re-exposed to the elevated plus-maze and open field tests. Neurosci Lett. 2017;642:77–85.PubMedGoogle Scholar
  12. 12.
    Garnett JP, Leiter JC. Hydrogen sulfide as a regulator of respiratory epithelial sodium transport: the role of sodium-potassium ATPase. Focus on “hydrogen sulfide contributes to hypoxic inhibition of airway transepithelial sodium absorption”. Am J Physiol-Reg I. 2016;311(3):564–5.Google Scholar
  13. 13.
    Hackfort BT, Mishra PK. Emerging role of hydrogen sulfide-microRNA crosstalk in cardiovascular diseases. Am J Physiol-Heart C. 2016;310(7):802–12.Google Scholar
  14. 14.
    Feliers D, Lee HJ, Kasinath BS. Hydrogen sulfide in renal physiology and disease. Antioxid Redox Signal. 2016;25(13):720–31.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Shefa U, Yeo SG, Kim M-S, Song IO, Jung J, Jeong NY, et al. Role of gasotransmitters in oxidative stresses, neuroinflammation, and neuronal repair. Biomed Res Int. 2017;2017:1689341.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Weber GJ, Pushpakumar S, Tyagi SC, Sen U. Homocysteine and hydrogen sulfide in epigenetic, metabolic and microbiota related renovascular hypertension. Pharmacol Res. 2016;113:300–12.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Li D-W, Qu L-L, Hu K, Long Y-T, Tian H. Monitoring of endogenous hydrogen sulfide in living cells using surface-enhanced raman scattering. Angew Chem Int Ed. 2015;4(43):12758–61.Google Scholar
  18. 18.
    Papapetropoulos A, Whiteman M, Cirino G. Pharmacological tools for hydrogen sulphide research: a brief, introductory guide for beginners. Br J Pharmacol. 2015;172(6):1633–7.PubMedGoogle Scholar
  19. 19.
    Li L, Zhang Y, Liu F, Su M, Liang L, Ge S, et al. Real-time visual determination of the flux of hydrogen sulphide using a hollow-channel paper electrode. Chem Commun. 2015;51(74):14030–3.Google Scholar
  20. 20.
    Xu T, Scafa N, Xu L-P, Zhou S, Al-Ghanem KA, Mahboob S, et al. Electrochemical hydrogen sulfide biosensors. Analyst. 2016;141(4):1185–95.PubMedGoogle Scholar
  21. 21.
    Li X, Gao X, Shi W, Ma H. Design strategies for water-soluble small molecular chromogenic and fluorogenic probes. Chem Rev. 2013;114(1):590–659.PubMedGoogle Scholar
  22. 22.
    Yang Y, Zhao Q, Feng W, Li F. Luminescent chemodosimeters for bioimaging. Chem Rev. 2012;113(1):192–270.PubMedGoogle Scholar
  23. 23.
    You L, Zha D, Anslyn EV. Recent advances in supramolecular analytical chemistry using optical sensing. Chem Rev. 2015;115(15):7840–92.PubMedGoogle Scholar
  24. 24.
    Zhou X, Lee S, Xu Z, Yoon J. Recent progress on the development of chemosensors for gases. Chem Rev. 2015;115(15):7944–8000.PubMedGoogle Scholar
  25. 25.
    Yu F, Han X, Chen L. Fluorescent probes for hydrogen sulfide detection and bioimaging. Chem Commun. 2014;50(82):12234–49.Google Scholar
  26. 26.
    Zhang D, Chen D, Kang J, Ye Y, Zhao Y, Xian M. Highly selective fluorescence off-on probes for biothiols and imaging in live cells. Org Biomol Chem. 2014;12(35):6837–41.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Duan Y-W, Yang X-F, Zhong Y, Guo Y, Li Z, Li H. A ratiometric fluorescent probe for gasotransmitter hydrogen sulfide based on a coumarin-benzopyrylium platform. Anal Chim Acta. 2015;859:59–65.PubMedGoogle Scholar
  28. 28.
    Qian Y, Lin J, Liu T, Zhu H. Living cells imaging for copper and hydrogen sulfide by a selective “on-off-on” fluorescent probe. Talanta. 2015;132:727–32.PubMedGoogle Scholar
  29. 29.
    Cui J, Zhang T, Sun Y-Q, Li D-P, Liu J-T, Zhao B-X. A highly sensitive and selective fluorescent probe for H2S detection with large fluorescence enhancement. Sensors Actuators B Chem. 2016;232:705–11.Google Scholar
  30. 30.
    Dai X, Zhang T, Liu Y-Z, Yan T, Li Y, Miao J-Y, et al. A ratiometric fluorescent probe for cysteine and its application in living cells. Sensors Actuators B Chem. 2015;207:872–7.Google Scholar
  31. 31.
    Peng B, Zhang C, Marutani E, Pacheco A, Chen W, Ichinose F, et al. Trapping hydrogen sulfide (H2S) with diselenides: the application in the design of fluorescent probes. Org Lett. 2015;17(6):1541–4.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Yuan L, Zuo Q-P. Reaction-based fluorescent probe for hydrogen sulfide with large signal-to-noise ratio in living cells and tissues. Sensors Actuators B Chem. 2014;196:151–5.Google Scholar
  33. 33.
    Hammers MD, Taormina MJ, Cerda MM, Montoya LA, Seidenkranz DT, Parthasarathy R, et al. A bright fluorescent probe for H2S enables analyte-responsive, 3D imaging in live zebrafish using light sheet fluorescence microscopy. J Am Chem Soc. 2015;137(32):10216–23.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Chen Y, Zhu C, Cen J, Bai Y, He W, Guo Z. Ratiometric detection of pH fluctuation in mitochondria with a new fluorescein/cyanine hybrid sensor. Chem Sci. 2015;6(5):3187–94.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Liu X-L, Du X-J, Dai C-G, Song Q-H. Ratiometric two-photon fluorescent probes for mitochondrial hydrogen sulfide in living cells. J Org Chem. 2014;79(20):9481–9.PubMedGoogle Scholar
  36. 36.
    Xu SD, Fang CH, Tian GX, Chen Y, Dou YH, Kou JF, et al. Reduction of 4-azidonaphthalimide with different phosphine ligands and exploration of their spectroscopic properties. J Mol Struct. 2015;1102:197–202.Google Scholar
  37. 37.
    Zhang C, Zhang G, Feng L, Li J. A ratiometric fluorescent probe for sensitive and selective detection of hydrogen sulfide and its application for bioimaging. Sensors Actuators B Chem. 2015;216:412–7.Google Scholar
  38. 38.
    Gao M, Yu F, Chen H, Chen L. Near-infrared fluorescent probe for imaging mitochondrial hydrogen polysulfides in living cells and in vivo. Anal Chem. 2015;87(7):3631–8.PubMedGoogle Scholar
  39. 39.
    Li J, Yin C, Huo F. Chromogenic and fluorogenic chemosensors for hydrogen sulfide: review of detection mechanisms since the year 2009. RSC Adv. 2015;3:2191–206.Google Scholar
  40. 40.
    Xiang K, Liu Y, Li C, Tian B, Tong T, Zhang J. A colorimetric and ratiometric fluorescent probe with a large stokes shift for detection of hydrogen sulfide. Dyes Pigments. 2015;123:78–84.Google Scholar
  41. 41.
    Park CS, Ha TH, Choi S-A, Nguyen DN, Noh S, Kwon OS, et al. A near-infrared “turn-on” fluorescent probe with a self-immolative linker for the in vivo quantitative detection and imaging of hydrogen sulfide. Biosens Bioelectron. 2017;89:919–26.PubMedGoogle Scholar
  42. 42.
    Zhang K, Zhang J, Xi Z, Li L-Y, Gu X, Zhang Q-Z, et al. A new H2S-specific near-infrared fluorescence-enhanced probe that can visualize the H2S level in colorectal cancer cells in mice. Chem Sci. 2017;8(4):2776–81.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Wu Z, Liang D, Tang X. Visualizing hydrogen sulfide in mitochondria and lysosome of living cells and in tumors of living mice with positively charged fluorescent chemosensors. Anal Chem. 2016;88(18):9213–8.PubMedGoogle Scholar
  44. 44.
    Huang K, Liu M, Wang X, Cao D, Gao F, Zhou K, et al. Cascade reaction and FRET-based fluorescent probe for the colorimetric and ratiometric signaling of hydrogen sulfide. Tetrahedron Lett. 2015;56(24):3769–73.Google Scholar
  45. 45.
    Shimamoto K, Hanaoka K. Fluorescent probes for hydrogen sulfide (H2S) and sulfane sulfur and their applications to biological studies. Nitric Oxide Biol Chem. 2015;46:72–9.Google Scholar
  46. 46.
    Lakowicz JR. Principles of fluorescence spectroscopy. Boston: Springer US, Academic; 2006. p. 63–95.Google Scholar
  47. 47.
    Lakowicz JR. Principles of fluorescence spectroscopy. Boston: Springer US, Academic; 2006. p. 623–73.Google Scholar
  48. 48.
    Lin VS, Lippert AR, Chang CJ. Cell-trappable fluorescent probes for endogenous hydrogen sulfide signaling and imaging H2O2-dependent H2S production. Proc Natl Acad Sci U S A. 2013;110(18):7131–5.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Liu K, Shang H, Kong X, Ren M, Wang J-Y, Liu Y, et al. A novel near-infrared fluorescent probe for H2O2 in alkaline environment and the application for H2O2 imaging in vitro and in vivo. Biomaterials. 2016;100:162–71.PubMedGoogle Scholar
  50. 50.
    Zheng K, Lin W, Cheng D, Chen H, Liu Y, Liu K. A two-photon fluorescent turn-on probe for nitroxyl (HNO) and its bioimaging application in living tissues. Chem Commun. 2015;51(26):5754–7.Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Biobased Material and Green Papermaking, Key Laboratory of Pulp & Paper Science and Technology of Shandong Province/Ministry of Education, Qilu University of TechnologyShandong Academy of SciencesJinanChina

Personalised recommendations