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Carbon nanospikes have improved sensitivity and antifouling properties for adenosine, hydrogen peroxide, and histamine

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Abstract

Carbon nanospikes (CNSs) are a new nanomaterial that has enhanced surface roughness and surface oxide concentration, increasing the sensitivity for dopamine detection. However, CNS-modified electrodes (CNSMEs) have not been characterized for other neurochemicals, particularly those with higher oxidation potentials. The purpose of this study was to evaluate CNSMEs for the detection of adenosine, hydrogen peroxide (H2O2), and histamine. The sensitivity increased with CNSs, and signals at CNSMEs were about 3.3 times higher than CFMEs. Normalizing for surface area differences using background currents, CNSMEs show an increased signal of 4.8 times for adenosine, 1.5 times for H2O2, and 2 times for histamine. CNSMEs promoted the formation of secondary products for adenosine and histamine, which enables differentiation from other analytes with similar oxidation potentials. CNSs also selectively enhance the sensitivity for adenosine and histamine compared to H2O2. A scan rate test reveals that adenosine is more adsorption-controlled at CNS electrodes than CFMEs. CNSMEs are antifouling for histamine, with less fouling because the polymers formed after histamine electrooxidation do not adsorb due to an elevated number of edge planes. CNSMEs were useful for detecting each analyte applied in brain slices. Because of the hydrophilic surface compared to CFMEs, CNSMEs also have reduced biofouling when used in tissue. Therefore, CNSMEs are useful for tissue measurements of adenosine, hydrogen peroxide, and histamine with high selectivity and low fouling.

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References

  1. Huffman ML, Venton BJ. Electrochemical properties of different carbon-fiber microelectrodes using fast-scan cyclic voltammetry. Electroanalysis. 2008;20(22):2422–8. https://doi.org/10.1002/elan.200804343.

    Article  CAS  Google Scholar 

  2. Ganesana M, Lee ST, Wang Y, Venton BJ. Analytical techniques in neuroscience: recent advances in imaging, separation, and electrochemical methods. Anal. Chem. 2017;89(1):314–41. https://doi.org/10.1021/acs.analchem.6b04278.

    Article  CAS  PubMed  Google Scholar 

  3. Huffman ML, Venton BJ. Carbon-fiber microelectrodes for in vivo applications. The Analyst. 2009;134(1):18–24. https://doi.org/10.1039/B807563H.

    Article  CAS  PubMed  Google Scholar 

  4. Venton BJ, Cao Q. Fundamentals of fast-scan cyclic voltammetry for dopamine detection. Analyst. 2020;145:1158–68. https://doi.org/10.1039/C9AN01586H.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yang C, Denno ME, Pyakurel P, Venton BJ. Recent trends in carbon nanomaterial-based electrochemical sensors for biomolecules: a review. Anal Chim Acta. 2015;887:17–37. https://doi.org/10.1016/j.aca.2015.05.049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cao Q, Puthongkham P, Venton BJ. Review: new insights into optimizing chemical and 3D surface structures of carbon electrodes for neurotransmitter detection. Anal Meth. 2019;11(3):247–61. https://doi.org/10.1039/c8ay02472c.

    Article  CAS  Google Scholar 

  7. Yang C, Wang Y, Jacobs CB, Ivanov IN, Venton BJ. O2 plasma etching and antistatic gun surface modifications for CNT yarn microelectrode improve sensitivity and antifouling properties. Anal Chem. 2017;89(10):5605–11. https://doi.org/10.1021/acs.analchem.7b00785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Jacobs CB, Ivanov IN, Nguyen MD, Zestos AG, Venton BJ. High temporal resolution measurements of dopamine with carbon nanotube yarn microelectrodes. Anal Chem. 2014;86(12):5721–7. https://doi.org/10.1021/ac404050t.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schmidt AC, Wang X, Zhu Y, Sombers LA. Carbon nanotube yarn electrodes for enhanced detection of neurotransmitter dynamics in live brain tissue. ACS Nano. 2013;7(9):7864–73. https://doi.org/10.1021/nn402857u.

    Article  CAS  PubMed  Google Scholar 

  10. Wang J. Carbon-nanotube based electrochemical biosensors: a review. Electroanalysis. 2005;17(1):7–14. https://doi.org/10.1002/elan.200403113.

    Article  CAS  Google Scholar 

  11. Wang J, Deo RP, Poulin P, Mangey M. Carbon nanotube fiber microelectrodes. J Am Chem Soc. 2003;125(48):14706–7. https://doi.org/10.1021/ja037737j.

    Article  CAS  PubMed  Google Scholar 

  12. Zhang X, Li Q, Tu Y, Li Y, Coulter JY, Zheng L, Zhao Y, Jia Q, Peterson DE, Zhu Y. Strong carbon-nanotube fibers spun from long carbon-nanotube arrays. Small. 2007;3(2):244–8. https://doi.org/10.1002/smll.200600368.

    Article  CAS  PubMed  Google Scholar 

  13. Yang C, Jacobs CB, Nguyen MD, Ganesana M, Zestos AG, Ivanov IN, Puretzky AA, Rouleau CM, Geohegan DB, Venton BJ. Carbon nanotubes grown on metal microelectrodes for the detection of dopamine. Anal Chem. 2016;88(1):645–52. https://doi.org/10.1021/acs.analchem.5b01257.

    Article  CAS  PubMed  Google Scholar 

  14. G. Zestos, A.; Yang, C.; B. Jacobs, C.; Hensley, D.; Jill Venton, B. Carbon nanospikes grown on metal wires as microelectrode sensors for dopamine. Analyst 2015, 140 (21), 7283–7292. https://doi.org/10.1039/C5AN01467K.

  15. Sheridan LB, Hensley DK, Lavrik NV, Smith SC, Schwartz V, Liang C, Wu Z, Meyer HM, Rondinone AJ. Growth and electrochemical characterization of carbon nanospike thin film electrodes. J Electrochem Soc. 2014;161(9):H558. https://doi.org/10.1149/2.0891409jes.

    Article  CAS  Google Scholar 

  16. Song Y, Peng R, Hensley DK, Bonnesen PV, Liang L, Wu Z, Meyer HM III, Chi M, Ma C, Sumpter BG, Rondinone AJ. High-selectivity electrochemical conversion of CO2 to ethanol using a copper nanoparticle/N-doped graphene electrode. Chemistry Sel. 2016;1(19):6055–61. https://doi.org/10.1002/slct.201601169.

    Article  CAS  Google Scholar 

  17. Cao, Q.; Shao, Z.; Hensley, D.; Jill Venton, B. Carbon nanospike coated nanoelectrodes for measurements of neurotransmitters. Faraday Discuss. 2022, 233 (0), 303–314. https://doi.org/10.1039/D1FD00053E.

  18. Cao Q, Hensley DK, Lavrik NV, Venton BJ. Carbon nanospikes have better electrochemical properties than carbon nanotubes due to greater surface roughness and defect sites. Carbon. 2019;155:250–7. https://doi.org/10.1016/j.carbon.2019.08.064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jacobs CB, Vickrey TL, Venton BJ. Functional groups modulate the sensitivity and electron transfer kinetics of neurochemicals at carbon nanotube modified microelectrodes. Analyst. 2011;136(17):3557. https://doi.org/10.1039/c0an00854k.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Unwin PR, Güell AG, Zhang G. Nanoscale electrochemistry of Sp 2 carbon materials: from graphite and graphene to carbon nanotubes. Acc Chem Res. 2016;49(9):2041–8. https://doi.org/10.1021/acs.accounts.6b00301.

    Article  CAS  PubMed  Google Scholar 

  21. Puthongkham P, Yang C, Venton BJ. Carbon nanohorn-modified carbon fiber microelectrodes for dopamine detection. Electroanal. 2018;30(6):1073–81. https://doi.org/10.1002/elan.201700667.

    Article  CAS  Google Scholar 

  22. Puthongkham P, Venton BJ. Recent advances in fast-scan cyclic voltammetry. Analyst. 2020;145:1087–102. https://doi.org/10.1039/C9AN01925A.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Swamy BEK, Venton BJ. Subsecond detection of physiological adenosine concentrations using fast-scan cyclic voltammetry. Anal Chem. 2007;79(2):744–50. https://doi.org/10.1021/ac061820i.

    Article  CAS  PubMed  Google Scholar 

  24. Sanford AL, Morton SW, Whitehouse KL, Oara HM, Lugo-Morales LZ, Roberts JG, Sombers LA. Voltammetric detection of hydrogen peroxide at carbon fiber microelectrodes. Anal Chem. 2010;82(12):5205–10. https://doi.org/10.1021/ac100536s.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sarada BV, Rao TN, Tryk DA, Fujishima A. Electrochemical oxidation of histamine and serotonin at highly boron-doped diamond electrodes. Anal Chem. 2000;72(7):1632–8. https://doi.org/10.1021/ac9908748.

    Article  CAS  PubMed  Google Scholar 

  26. Puthongkham P, Lee ST, Venton BJ. Mechanism of histamine oxidation and electropolymerization at carbon electrodes. Anal Chem. 2019;91(13):8366–73. https://doi.org/10.1021/acs.analchem.9b01178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Manjunath S, Sakhare PM. Adenosine and adenosine receptors: newer therapeutic perspective. Ind J Pharmacol. 2009;41(3):97–105. https://doi.org/10.4103/0253-7613.55202.

    Article  CAS  Google Scholar 

  28. Bjorness TE, Greene RW. Adenosine and sleep. Curr Neuropharmacol. 2009;7(3):238–45. https://doi.org/10.2174/157015909789152182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cunha RA. Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem Int. 2001;38(2):107–25. https://doi.org/10.1016/S0197-0186(00)00034-6.

    Article  CAS  PubMed  Google Scholar 

  30. Ross AE, Venton BJ. Nafion–CNT coated carbon-fiber microelectrodes for enhanced detection of adenosine. Analyst. 2012;137(13):3045. https://doi.org/10.1039/c2an35297d.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pajski ML, Venton BJ. Adenosine release evoked by short electrical stimulations in striatal brain slices is primarily activity dependent. ACS Chem Neurosci. 2010;1(12):775–87. https://doi.org/10.1021/cn100037d.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nguyen MD, Venton BJ. Fast-scan cyclic voltammetry for the characterization of rapid adenosine release. Comput Struct Biotechnol J. 2015;13:47–54. https://doi.org/10.1016/j.csbj.2014.12.006.

    Article  CAS  PubMed  Google Scholar 

  33. Pajski ML, Venton BJ. The mechanism of electrically stimulated adenosine release varies by brain region. Purinergic Signal. 2013;9(2):167–74. https://doi.org/10.1007/s11302-012-9343-2.

    Article  CAS  PubMed  Google Scholar 

  34. Roberts JG, Voinov MA, Schmidt AC, Smirnova TI, Sombers LA. The hydroxyl radical is a critical intermediate in the voltammetric detection of hydrogen peroxide. J Am Chem Soc. 2016;138(8):2516–9. https://doi.org/10.1021/jacs.5b13376.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Halliwell B. Oxidative stress and neurodegeneration: where are we now? J Neurochem. 2006;97(6):1634–58. https://doi.org/10.1111/j.1471-4159.2006.03907.x.

    Article  CAS  PubMed  Google Scholar 

  36. Avshalumov MV, Chen BT, Koós T, Tepper JM, Rice ME. Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive potassium channels. J Neurosci. 2005;25(17):4222–31. https://doi.org/10.1523/JNEUROSCI.4701-04.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hall SB, Khudaish EA, Hart AL. Electrochemical oxidation of hydrogen peroxide at platinum electrodes. Part 1. An adsorption-controlled mechanism. Electrochimica Acta. 1998;43(5):579–88. https://doi.org/10.1016/S0013-4686(97)00125-4.

    Article  CAS  Google Scholar 

  38. Han J-H, Boo H, Park S, Chung TD. Electrochemical oxidation of hydrogen peroxide at nanoporous platinum electrodes and the application to glutamate microsensor. Electrochimica Acta. 2006;52(4):1788–91. https://doi.org/10.1016/j.electacta.2005.12.060.

    Article  CAS  Google Scholar 

  39. Hashemi P, Dankoski EC, Wood KM, Ambrose RE, Wightman RM. In vivo electrochemical evidence for simultaneous 5-HT and histamine release in the rat substantia nigra pars reticulata following medial forebrain bundle stimulation. J Neurochem. 2011;118(5):749–59. https://doi.org/10.1111/j.1471-4159.2011.07352.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pihel K, Hsieh S, Jorgenson JW, Wightman RM. Quantal corelease of histamine and 5-hydroxytryptamine from mast cells and the effects of prior incubation. Biochem. 1998;37(4):1046–52. https://doi.org/10.1021/bi9714868.

    Article  CAS  Google Scholar 

  41. Liu J, Cao Y. An electrochemical sensor based on an anti-fouling membrane for the determination of histamine in fish samples. Anal Meth. 2021;13(5):685–94. https://doi.org/10.1039/D0AY01901A.

    Article  CAS  Google Scholar 

  42. Eivazzadeh-Keihan R, Bahojb Noruzi E, Chidar E, Jafari M, Davoodi F, Kashtiaray A, Ghafori Gorab M, Masoud Hashemi S, Javanshir S, Ahangari Cohan R, Maleki A, Mahdavi M. Applications of carbon-based conductive nanomaterials in biosensors. Chem Eng J. 2022;442:136183. https://doi.org/10.1016/j.cej.2022.136183.

    Article  CAS  Google Scholar 

  43. Weese ME, Krevh RA, Li Y, Alvarez NT, Ross AE. Defect sites modulate fouling resistance on carbon-nanotube fiber electrodes. ACS Sens. 2019;4(4):1001–7. https://doi.org/10.1021/acssensors.9b00161.

    Article  CAS  PubMed  Google Scholar 

  44. Ulyanov NB, James TL. RNA structural motifs that entail hydrogen bonds involving sugar–phosphate backbone atoms of RNA. New J Chem. 2010;34(5):910. https://doi.org/10.1039/b9nj00754g.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Li Y, Weese ME, Cryan MT, Ross AE. Amine-functionalized carbon-fiber microelectrodes for enhanced ATP detection with fast-scan cyclic voltammetry. Anal Meth. 2021;13(20):2320–30. https://doi.org/10.1039/D1AY00089F.

    Article  CAS  Google Scholar 

  46. Żeglin J, Piotrowski GP, Piękos R. A study of interaction between hydrogen peroxide and silica gel by FTIR spectroscopy and quantum chemistry. J Mol Struct. 2006;794(1–3):83–91. https://doi.org/10.1016/j.molstruc.2006.01.043.

    Article  CAS  Google Scholar 

  47. Engdahl A, Nelander B. The structure of the water–hydrogen peroxide complex. A matrix isolation study. Phys Chem Chem Phys. 2000;2(18):3967–70. https://doi.org/10.1039/B005861K.

    Article  CAS  Google Scholar 

  48. Lewandowski D, Bajerlein D, Schroeder G. Adsorption of hydrogen peroxide on functionalized mesoporous silica surfaces. Struct Chem. 2014;25(5):1505–12. https://doi.org/10.1007/s11224-014-0428-0.

    Article  CAS  Google Scholar 

  49. Luque GL, Rojas MI, Rivas GA, Leiva EPM. The origin of the catalysis of hydrogen peroxide reduction by functionalized graphene surfaces: a density functional theory study. Electrochimica Acta. 2010;56(1):523–30. https://doi.org/10.1016/j.electacta.2010.09.016.

    Article  CAS  Google Scholar 

  50. Majidi R, Karami AR. Detection of hydrogen peroxide with graphyne. Physica E-low-dimensional Syst Nanostruct. 2013;54:177–80. https://doi.org/10.1016/j.physe.2013.06.029.

    Article  CAS  Google Scholar 

  51. Omidi MH, Soleymanabadi H, Bagheri Z. Adsorption and dissociation of hydrogen peroxide on the defected carbon nanotubes. Struct Chem. 2015;26(2):485–90. https://doi.org/10.1007/s11224-014-0513-4.

    Article  CAS  Google Scholar 

  52. Nguyen MD, Lee ST, Ross AE, Ryals M, Choudhry VI, Venton BJ. Characterization of spontaneous, transient adenosine release in the caudate-putamen and prefrontal cortex. PLOS ONE. 2014;9(1):e87165. https://doi.org/10.1371/journal.pone.0087165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Graham MV, Cady NC. Nano and microscale topographies for the prevention of bacterial surface fouling. Coatings. 2014;4(1):37–59. https://doi.org/10.3390/coatings4010037.

    Article  CAS  Google Scholar 

  54. Khot G, Shirtcliffe N, Celikel T. Simultaneous detection of dopamine and serotonin with carbon-based electrodes; preprint. Biochem. 2021; https://doi.org/10.1101/2021.08.31.458352.

  55. Cao Q, Lucktong J, Shao Z, Chang Y-Y, Jill Venton B. Electrochemical treatment in KOH renews and activates carbon fiber microelectrode surfaces. Analy Bioanaly Chem. 2021;413(27):6737–46. https://doi.org/10.1007/s00216-021-03539-6.

    Article  CAS  Google Scholar 

  56. Takmakov P, Zachek MK, Keithley RB, Walsh PL, Donley C, McCarty GS, Wightman RM. Carbon microelectrodes with a renewable surface. Anal Chem. 2010;82(5):2020–8. https://doi.org/10.1021/ac902753x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was funded by NIH R01MH085159 and NIH R01NS125663. Carbon nanospike growth was conducted at the Center for Nanophase Materials Sciences, which is a DOE Office of Science User Facility under user agreement CNMS 2022-01117 and CNMS 2023-01815.

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Contributions

He Zhao: investigation; resources; and writing, original draft. Kailash Shrestha: brain slice puff-on testing. Dale K. Hensley: carbon nanospike growth. B. Jill Venton: project administration; visualization; and review, editing.

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Correspondence to B. Jill Venton.

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All animal experiments were approved by the University of Virginia Institutional Animal Care and Use Committee

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All animals were purchased from Charles River.

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Animals were used in accordance with the guidelines on animal welfare published by OLAW from NIH. Experiments were approved by the University of Virginia Institutional Animal Care and Use Committee.

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Zhao, H., Shrestha, K., Hensley, D.K. et al. Carbon nanospikes have improved sensitivity and antifouling properties for adenosine, hydrogen peroxide, and histamine. Anal Bioanal Chem 415, 6039–6050 (2023). https://doi.org/10.1007/s00216-023-04875-5

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