Abstract
Neglected tropical diseases are those caused by infectious agents or parasites and are considered endemic in low-income populations. These diseases also have unacceptable indicators and low investment in research, drug production, and control. Tropical diseases such as leishmaniasis are some of the main causes of morbidity and mortality around the globe. Electrochemical immunosensors are promising tools for diagnostics against these diseases. One such benefit is the possibility of assisting diagnosis in isolated regions, where laboratory infrastructure is lacking. In this work, different peptides were investigated to detect antibodies against Leishmania in human and canine serum samples. The peptides evaluated (395-KKG and 395-G) have the same recognition site but differ on their solid-binding domains, which ensure affinity to spontaneously bind to either graphene oxide (GO) or graphene quantum dots (GQD). Cyclic voltammetry and differential pulse voltammetry were employed to investigate the electrochemical behavior of each assembly step and the role of each solid-binding domain coupled to its anchoring material. The graphene affinity peptide (395-G) showed better reproducibility and selectivity when coupled to GQD. Under the optimized set of experimental conditions, negative and positive human serum samples responses were distinguished based on a cut-off value of 82.5% at a 95% confidence level. The immunosensor showed selective behavior to antibodies against Mycobacterium leprae and Mycobacterium tuberculosis, which are similar antibodies and potentially sources of false positive tests. Therefore, the use of the graphene affinity peptide as a recognition site achieved outstanding performance for the detection of Leishmania antibodies.
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References
Cordeiro TAR, de Resende MAC, Moraes SC dos S, et al (2021) Electrochemical biosensors for neglected tropical diseases: a review. Talanta 234:. https://doi.org/10.1016/j.talanta.2021.122617
Kammona O, Tsanaktsidou E (2021) Nanotechnology-aided diagnosis, treatment and prevention of leishmaniasis. Int J Pharm 605:120761. https://doi.org/10.1016/j.ijpharm.2021.120761
Weng HB, Chen HX, Wang MW (2018) Innovation in neglected tropical disease drug discovery and development. Infect Dis Poverty 7:1–9. https://doi.org/10.1186/s40249-018-0444-1
World Healthy Organization (2023) Leishamaniasis. In: January 2023. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
Ahmad A, Ullah S, Syed F et al (2020) Biogenic metal nanoparticles as a potential class of antileishmanial agents: mechanisms and molecular targets. Nanomedicine 15:809–828. https://doi.org/10.2217/nnm-2019-0413
Oliveira SS, Ferreira CS, Branquinha MH et al (2021) Overcoming multi-resistant leishmania treatment by nanoencapsulation of potent antimicrobials. J Chem Technol Biotechnol 96:2123–2140. https://doi.org/10.1002/jctb.6633
Freire ML, Machado de Assis T, Oliveira E et al (2019) Performance of serological tests available in Brazil for the diagnosis of human visceral leishmaniasis. PLoS Negl Trop Dis 13:e0007484. https://doi.org/10.1371/journal.pntd.0007484
Farshchi F, Saadati A, Hasanzadeh M (2020) Optimized DNA-based biosensor for monitoring Leishmania infantum in human plasma samples using biomacromolecular interaction: a novel platform for infectious disease diagnosis. Anal Methods 12:4759–4768. https://doi.org/10.1039/D0AY01516D
Martins BR, Barbosa YO, Andrade CMR et al (2020) Development of an electrochemical immunosensor for specific detection of visceral leishmaniasis using gold-modified screen-printed carbon electrodes. Biosensors 10:1–15. https://doi.org/10.3390/BIOS10080081
Braz BA, Hospinal-Santiani M, Martins G, et al (2022) Graphene-binding peptide in fusion with SARS-CoV-2 antigen for electrochemical immunosensor construction. Biosensors (Basel) 12:. https://doi.org/10.3390/bios12100885
Gogola JL, Martins G, Gevaerd A et al (2021) Label-free aptasensor for p24-HIV protein detection based on graphene quantum dots as an electrochemical signal amplifier. Anal Chim Acta 1166:1–7. https://doi.org/10.1016/j.aca.2021.338548
Valenga MGP, Martins G, Martins TAC et al (2023) Biochar: an environmentally friendly platform for construction of a SARS-CoV-2 electrochemical immunosensor. Sci Total Environ 858:159797. https://doi.org/10.1016/j.scitotenv.2022.159797
Gevaerd A, Banks CE, Bergamini MF, Marcolino-Junior LH (2019) Graphene quantum dots modified screen-printed electrodes as electroanalytical sensing platform for diethylstilbestrol. Electroanalysis 31:838–843. https://doi.org/10.1002/elan.201800838
Gevaerd A, Banks CE, Bergamini MF, Marcolino-Junior LH (2020) Nanomodified screen-printed electrode for direct determination of Aflatoxin B1 in malted barley samples. Sens Actuators B Chem 307:. https://doi.org/10.1016/j.snb.2019.127547
Mansuriya B, Altintas Z (2020) Applications of graphene quantum dots in biomedical sensors. Sensors 20:1072. https://doi.org/10.3390/s20041072
Liberato MS, Mancini RSN, Factori IM et al (2019) Peptide-based assemblies on electrospun polyamide-6/chitosan nanofibers for detecting visceral leishmaniasis antibodies. ACS Appl Electron Mater 1:2086–2095. https://doi.org/10.1021/acsaelm.9b00476
Brazaca LC, dos Santos PL, de Oliveira PR, et al (2021) Biosensing strategies for the electrochemical detection of viruses and viral diseases – a review. Anal Chim Acta 1159:. https://doi.org/10.1016/j.aca.2021.338384
Cretich M, Gori A, D’Annessa I et al (2019) Peptides for infectious diseases: from probe design to diagnostic microarrays. Antibodies 8:23. https://doi.org/10.3390/antib8010023
Pandey S, Malviya G, Chottova Dvorakova M (2021) Role of peptides in diagnostics. Int J Mol Sci 22:8828. https://doi.org/10.3390/ijms22168828
ThomazSoccol V, Pasquali AKS, Pozzolo EM et al (2017) More than the eyes can see: the worrying scenario of canine leishmaniasis in the Brazilian side of the triple border. PLoS One 12:e0189182. https://doi.org/10.1371/journal.pone.0189182
MINISTÉRIO DA SAÚDE (2006) Manual de vigilância e controle da leishmaniose visceral
Alban SM, de Moura JF, Minozzo JC et al (2013) Identification of mimotopes of Mycobacterium leprae as potential diagnostic reagents. BMC Infect Dis 13:42. https://doi.org/10.1186/1471-2334-13-42
Pereira JC, Dos Santos SP, De Souza LMB et al (2021) The efficacy of recombinant protein lbk39 for the diagnosis of leishmaniosis in dogs. Parasitology 148:302–310. https://doi.org/10.1017/S0031182020001997
Lamiable A, Thévenet P, Rey J et al (2016) PEP-FOLD3: faster de novo structure prediction for linear peptides in solution and in complex. Nucleic Acids Res 44:W449–W454. https://doi.org/10.1093/nar/gkw329
Merrifield RB (1969) Solid-phase peptide synthesis. Adv Enzymol Relat Areas Mol Biol 221–96
Ramos MK, Zarbin AJG (2020) Graphene/copper oxide nanoparticles thin films as precursor for graphene/copper hexacyanoferrate nanocomposites. Appl Surf Sci 515:146000. https://doi.org/10.1016/j.apsusc.2020.146000
Lacina K, Věžník J, Sopoušek J et al (2023) Concentration and diffusion of the redox probe as key parameters for label-free impedimetric immunosensing. Bioelectrochemistry 149:108308. https://doi.org/10.1016/j.bioelechem.2022.108308
Braiek M, Rokbani K, Chrouda A et al (2012) An electrochemical immunosensor for detection of Staphylococcus aureus bacteria based on immobilization of antibodies on self-assembled monolayers-functionalized gold electrode. Biosensors 2:417–426. https://doi.org/10.3390/bios2040417
Eissa S, Zourob M (2021) Development of a low-cost cotton-tipped electrochemical immunosensor for the detection of SARS-CoV-2. Anal Chem 93:1826–1833. https://doi.org/10.1021/acs.analchem.0c04719
Shaikh MO, Srikanth B, Zhu P-Y, Chuang C-H (2019) Impedimetric immunosensor utilizing polyaniline/gold nanocomposite-modified screen-printed electrodes for early detection of chronic kidney disease. Sensors 19:3990. https://doi.org/10.3390/s19183990
Wang K, Lin X, Zhang M et al (2022) Review of electrochemical biosensors for food safety detection. Biosensors 12:959. https://doi.org/10.3390/bios12110959
Martins G, Gogola JL, Caetano FR et al (2019) Quick electrochemical immunoassay for hantavirus detection based on biochar platform. Talanta 204:163–171. https://doi.org/10.1016/j.talanta.2019.05.101
Biedulska M, Jakóbczyk P, Sosnowska M et al (2021) Cytocompatibility of stabilized black phosphorus nanosheets tailored by directly conjugated polymeric micelles for human breast cancer therapy. Sci Rep 11:9304. https://doi.org/10.1038/s41598-021-88791-7
Cui Y, Kim SN, Jones SE et al (2010) Chemical functionalization of graphene enabled by phage displayed peptides. Nano Lett 10:4559–4565. https://doi.org/10.1021/nl102564d
Hughes ZE, Walsh TR (2015) What makes a good graphene-binding peptide? Adsorption of amino acids and peptides at aqueous graphene interfaces. J Mater Chem B 3:3211–3221. https://doi.org/10.1039/C5TB00004A
Camden AN, Barr SA, Berry RJ (2013) Simulations of peptide-graphene interactions in explicit water. J Phys Chem B 117:10691–10697. https://doi.org/10.1021/jp403505y
Nazari-Vanani R, Sattarahmady N, Yadegari H et al (2018) Electrochemical quantitation of Leishmania infantum based on detection of its kDNA genome and transduction of non-spherical gold nanoparticles. Anal Chim Acta 1041:40–49. https://doi.org/10.1016/j.aca.2018.08.036
Cordeiro TAR, Martins HR, Franco DL et al (2020) Impedimetric immunosensor for rapid and simultaneous detection of chagas and visceral leishmaniasis for point of care diagnosis. Biosens Bioelectron 169:112573. https://doi.org/10.1016/j.bios.2020.112573
Ramos-Jesus J, Pontes-de-Carvalho LC, Melo SMB et al (2016) A gold nanoparticle piezoelectric immunosensor using a recombinant antigen for detecting Leishmania infantum antibodies in canine serum. Biochem Eng J 110:43–50. https://doi.org/10.1016/j.bej.2016.01.027
Acknowledgements
The authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (financial code 001 and CAPES 09/2020 Epidemias 88887.504861/2020-00 and 88881.505280/2020-01), Conselho Nacional de Pesquisa (CNPq) (grants 311290/2020-5 and 309803/2020-9), and Fundação Araucária (PBA2022011000056 and PDT2020221000003). The authors also acknowledge financial support from the Brazilian Institute of Science and Technology (INCT)—Nanomaterials for Life (Proc. Number 406079/2022-6).
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Braz, B.A., Hospinal-Santiani, M., Martins, G. et al. Disposable electrochemical platform based on solid-binding peptides and carbon nanomaterials: an alternative device for leishmaniasis detection. Microchim Acta 190, 321 (2023). https://doi.org/10.1007/s00604-023-05891-z
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DOI: https://doi.org/10.1007/s00604-023-05891-z