Advertisement

Journal of Applied Electrochemistry

, Volume 49, Issue 2, pp 229–239 | Cite as

A nitric oxide sensor fabricated through e-jet printing towards use in bioelectronics interfaces

  • Ryan T. MyersEmail author
  • Joseph Ayers
Research Article
First Online:
  • 37 Downloads
Part of the following topical collections:
  1. Sensors

Abstract

We have developed a methodology for electrohydrodynamic printing of a nitric oxide (NO) sensor. The primary features of this amperometric methodology include the printing of carbon and metallic-based inks, the conversion of Ag to Ag:AgCl as a reference electrode, and the deposition of a nitric oxide selective layer on the working electrode, followed by an encapsulation to define the working area. The efficacy and enhancements of multiple printed layers has been examined. Multiple working electrode chemistries and combinations are presented, including the use of silver, graphene, NiTsPc, and gold in various combinations. Selectivity for NO was accomplished via a Nafion® layer on the working electrode, effectively blocking interference from NO2− and NO3− at relatively high concentrations. The resultant flexible, thin film nitric oxide sensor is sensitive enough to monitor macrophage depolarization events without the need for additional micropipette or FRET-based electrochemical sensors. We demonstrate a valuable research tool that will have a high impact on the emerging field of synthetic biology by providing the capability to interface-engineered cellular sensors to microelectronics.

Graphical abstract

Keywords

Nitric oxide Electrohydrodynamic jet e-jet 3D printing Electrochemistry Bioelectronics 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Supported by ONR MURI # N000141110725.

Compliance with ethical standards

Conflict of interest

The authors have no financial and/or personal relationships with other people or organizations that could inappropriately influence (bias) their work.

References

  1. 1.
    Ayers J (2018) Biohybrid robots are synthetic biology systems. In: Prescott TJ, Verschure PMJ (eds) Living machines: a handbook of research in biomimetic and biohybrid systems. Oxford University Press, Oxford, pp 483–490Google Scholar
  2. 2.
    Prescott TJ, Verschure PMJ (2018) Living machines: a handbook of research in biomimetic and biohybrid systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  3. 3.
    Usoskin D, Furlan A, Islam S, Abdo H, Lönnerberg P, Lou D, Hjerling-Leffler J, Haeggström J, Kharchenko O, Kharchenko PV (2015) Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci 18(1):145–153CrossRefGoogle Scholar
  4. 4.
    Ferri G, Caselli E, Mattoli V, Mondini A, Mazzolai B, Dario P (2007) A biologically-inspired algorithm for gas/odor source localization in an indoor environment with no strong airflow: first experimental results. In: Proceedings of IEEE International Conference on Robotics and Automation, pp 566–571Google Scholar
  5. 5.
    Westphal A, Rulkov N, Ayers J, Brady D, Hunt M (2011) Controlling a lamprey-based robot with an electronic nervous system. Smart Struct Syst 8(1):37–54CrossRefGoogle Scholar
  6. 6.
    Ayers J, Witting J (2007) Biomimetic approaches to the control of underwater walking machines. Phil Trans R Soc Lond A 365:273–295CrossRefGoogle Scholar
  7. 7.
    Ayers J, Blustein D, Westphal A (2012) A conserved biomimetic control architecture for walking, swimming and flying robots. Biomim Biohybrid Syst 7375:1–12CrossRefGoogle Scholar
  8. 8.
    Bockaert J, Perroy J, Bécamel C, Marin P, Fagni L (2010) GPCR interacting proteins (GIPs) in the nervous system: roles in physiology and pathologies. Annu Rev Pharmacol Toxicol 50:89–109CrossRefGoogle Scholar
  9. 9.
    Wicher D (2010) Design principles of sensory receptors. Front Cell Neurosci 4:25Google Scholar
  10. 10.
    Hille B (1992) G protein-coupled mechanisms and nervous signaling. Neuron 9(2):187–195CrossRefGoogle Scholar
  11. 11.
    Hamm HE (1998) The many faces of G protein signaling. J Biol Chem 273(2):669–672CrossRefGoogle Scholar
  12. 12.
    Kaissling K-E (2017) Responses of insect olfactory neurons to single pheromone molecules. In: Olfactory concepts of insect control. Springer, BerlinGoogle Scholar
  13. 13.
    Radhika V, Proikas-Cezanne T, Jayaraman M, Onesime D, Ha JH, Dhanasekaran DN (2007) Chemical sensing of DNT by engineered olfactory yeast strain. Nat Chem Biol 3(6):325–330CrossRefGoogle Scholar
  14. 14.
    Imai R, Chang L, Ohta A, Bray EA, Takagi M (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170(2):243–248CrossRefGoogle Scholar
  15. 15.
    Adak S, Aulak KS, Stuehr DJ (2002) Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J Biol Chem 277(18):16167–16171CrossRefGoogle Scholar
  16. 16.
    Kanadia R, Kuo W, Mcnabb M, Botchway A (1998) Constitutive nitric oxide synthase in Saccharomyces cerevisiae. IUBMB Life 45(6):1081–1087CrossRefGoogle Scholar
  17. 17.
    Park J-U, Hardy M, Kang SJ, Barton K, Adair K, kishore Mukhopadhyay D, Lee CY, Strano MS, Alleyne AG, Georgiadis JG (2007) High-resolution electrohydrodynamic jet printing. Nat Mater 6(10):782–789CrossRefGoogle Scholar
  18. 18.
    Myers RT, Ayers J (2017) Two-stage silver sintering process improves sheet resistance, film uniformity, and layering properties via electrohydrodynamic jet printing. 3D Print Addit Manuf 4(3):165–171CrossRefGoogle Scholar
  19. 19.
    Sutano E, Shigeta K, Kim Y, Graf P, Hoeltzle D, Barton K, Alleyne A, Ferriera P, Rogers J (2011) A multi-material electrohydrodynamic jet (E-Jet) printing system. J Micromech Microeng 22(4):045008CrossRefGoogle Scholar
  20. 20.
    Mishra S, Barton KL, Alleyne AG, Ferreira PM, Rogers J (2010) High-speed and drop-on-demand printing with a pulsed electrohydrodynamic jet. J Micromech Microeng 20:1–8CrossRefGoogle Scholar
  21. 21.
    Barton K, Mishra S, Shorter K, Alleyne A, Ferreira P, Rogers J (2010) A desktop electrohydrodynamic jet printing system. Mecchatronics 20:611–616CrossRefGoogle Scholar
  22. 22.
    Mishra S, Barton K, Alleyne A, Ferreira P, Rogers J (2010) High-speed and drop-on-demand printing with a pulsed electrohydrodynamic jet. J Micromech Microeng 20(9):095026CrossRefGoogle Scholar
  23. 23.
    Pontie M, Lecture H, Bedioui F (1999) Improvement in the performance of a nickel complex-based electrochemical sensor for the detection of nitric oxide in solution. Sens Actuators B 56(1–2):1–5.  https://doi.org/10.1016/S0925-4005(99)00027-1 CrossRefGoogle Scholar
  24. 24.
    Pontié M, Gobin C, Pauporté T, Bedioui F, Devynck J (2000) Electrochemical nitric oxide microsensors: sensitivity and selectivity characterisation. Anal Chim Acta 411(1–2):175–185.  https://doi.org/10.1016/S0003-2670(00)00741-8 CrossRefGoogle Scholar
  25. 25.
    Lim FJ, Ananthanarayanan K, Luther J, Ho GW (2012) Influence of a novel fluorosurfactant modified PEDOT: PSS hole transport layer on the performance of inverted organic solar cells. J Mater Chem 22(48):25057–25064CrossRefGoogle Scholar
  26. 26.
    Miserere S, Ledru S, Ruillé N, Griveau S, Boujtita M, Bedioui F (2006) Biocompatible carbon-based screen-printed electrodes for the electrochemical detection of nitric oxide. Electrochem Commun 8(2):238–244CrossRefGoogle Scholar
  27. 27.
    Kannan P, John SA (2010) Highly sensitive electrochemical determination of nitric oxide using fused spherical gold nanoparticles modified ITO electrode. Electrochim Acta 55(10):3497–3503CrossRefGoogle Scholar
  28. 28.
    Thangavel S, Ramaraj R (2008) Polymer membrane stabilized gold nanostructures modified electrode and its application in nitric oxide detection. J Phys Chem C 112(50):19825–19830CrossRefGoogle Scholar
  29. 29.
    Ting SL, Guo CX, Leong KC, Kim D-H, Li CM, Chen P (2013) Gold nanoparticles decorated reduced graphene oxide for detecting the presence and cellular release of nitric oxide. Electrochim Acta 111:441–446CrossRefGoogle Scholar
  30. 30.
    Zhu M, Liu M, Shi G, Xu F, Ye X, Chen J, Jin L, Jin J (2002) Novel nitric oxide microsensor and its application to the study of smooth muscle cells. Anal Chim Acta 455(2):199–206CrossRefGoogle Scholar
  31. 31.
    Yu A, Liang Z, Cho J, Caruso F (2003) Nanostructured electrochemical sensor based on dense gold nanoparticle films. Nano Lett 3(9):1203–1207CrossRefGoogle Scholar
  32. 32.
    Yu A, Zhang X, Zhang H, Han D, Knight AR (2011) Preparation and electrochemical properties of gold nanoparticles containing carbon nanotubes-polyelectrolyte multilayer thin films. Electrochim Acta 56(25):9015–9019CrossRefGoogle Scholar
  33. 33.
    Brorson JR, Schumacker PT, Zhang H (1999) Nitric oxide acutely inhibits neuronal energy production. J Neurosci 19(1):147–158CrossRefGoogle Scholar
  34. 34.
    Instruments WP (2016) ISO-NOP Macrosensor for NO MeasurementGoogle Scholar
  35. 35.
    Bioscience N Cellometer Automatic Cell Counter. Internet. http://www.nexcelom.com/Literature/App%20Note%2006005%20Immunology.pdf
  36. 36.
    Hakim T, Sugimori K, Camporesi E, Anderson G (1996) Half-life of nitric oxide in aqueous solutions with and without haemoglobin. Physiol Meas 17(4):267CrossRefGoogle Scholar
  37. 37.
    Zacharia IG, Deen WM (2005) Diffusivity and solubility of nitric oxide in water and saline. Ann Biomed Eng 33(2):214–222CrossRefGoogle Scholar
  38. 38.
    Amatore C, Arbault S, Bouton C, Coffi K, Drapier JC, Ghandour H, Tong Y (2006) Monitoring in real time with a microelectrode the release of reactive oxygen and nitrogen species by a single macrophage stimulated by its membrane mechanical depolarization. ChemBioChem 7(4):653–661CrossRefGoogle Scholar
  39. 39.
    Patel BA, Galligan JJ, Swain GM, Bian X (2008) Electrochemical monitoring of nitric oxide released by myenteric neurons of the guinea pig ileum. Neurogastroenterol Motil 20(11):1243–1250CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of BioengineeringNortheastern UniversityNahantUSA
  2. 2.Department of Marine and Environmental SciencesNortheastern UniversityNahantUSA
  3. 3.Department of BiologyNortheastern UniversityNahantUSA
  4. 4.Marine Science CenterNortheastern UniversityNahantUSA

Personalised recommendations

Cite article

Buy options