Abstract
Pertussis (or whooping cough) is a contagious disease mainly affecting infants and children and predominantly caused by Bordetella pertussis followed by Bordetella parapertussis. B. parapertussis causes a milder cough but usually symptomatically appears like B. pertussis infection. Thus the epidemiology of illness caused by B. parapertussis is not well understood. In this study, a sensitive and specific method for the rapid diagnosis of B. parapertussis is presented. The covalent immobilization of thiol-terminated DNA oligonucleotides (ss DNA SAM) on a silicon surface by disulfide bond formation is investigated with atomic force microscopy (AFM) and ellipsometry. The measurements indicated an average layer thickness of 5 ± 0.84 nm for 2 μg/μl concentration and 24 h incubation time. This thickness changed to 8.4 ± 0.92 nm for the same concentration (2 μg/μl) by altering the incubation time to 48 h. Ellipsometric data recorded before and after hybridization of B. parapertussis revealed an increase in mean grain area from 91 nm2 to 227 nm2 and a change in the refractive index from 1.489 to 1.648 for 2 μg/μl B. parapertussis, respectively. This change in the refractive index was used to evaluate the amount of adsorbed molecules and their density. The results showed that the density of adsorbed molecules increased from 0.2 to 0.97 g/cm3 after B. parapertussis attachment, respectively. To confirm the hybridization of B. parapertussis to ss DNA SAM, the ds DNA SAM was denatured and the ss DNA SAM surface was reproduced with an average height variation of 6.42 ± 0.75 nm. This showed the stability of the DNA film that can be tuned by varying the concentration and incubation time, thus providing a robust method for the label-free detection of B. parapertussis other than routinely used PCR detection.
Similar content being viewed by others
References
Templeton, K.E., Scheltinga, S.A., Van der Zee, A., Diederen, B.M.W., Kruijssen, A.M., Goossens, H., Kuijper, E., Claas, E.C.J.: Evaluation of real-time PCR for detection of and discrimination between Bordetella pertussis, Bordetella parapertussis, and Bordetella holmesii for clinical diagnosis. J. Clin. Microbiol. 41, 4121–4126 (2003)
Bottero, D., Gaillard, M.E., Errea, A., Moreno, G., Zurita, E., Pianciola, L., Rumbo, M., Hozbor, D.: Outer membrane vesicles derived from Bordetella parapertussis as anacellular vaccine against Bordetella parapertussis and Bordetella pertussis infection. Vaccine. 31, 5262–5268 (2013)
Bokhari, H., Said, F., Syed, M.A., Mughal, A., Kazi, Y.F., Heuvelman, K., Mooi, F.R.: Whooping cough in Pakistan: Bordetella pertussis vs Bordetella parapertussis in 2005-2009. Scand. J. Infect. Dis. 43, 818–820 (2011)
Elahi, S., Thompson, D.R., Strom, S., O'Connor, B., Babiuk, L.A., Gerdts, V.: Infection with Bordetella parapertussis but not Bordetella pertussis causes pertussis-like disease in older pigs. J. Infect. Dis. 198, 384–392 (2008)
Scanlon, K.M., Skerry, C., Carbonetti, N.H.: Novel therapies for the treatment of pertussis disease. Pathog. Dis. 73, 1–9 (2015)
Cherry, J.D., Seaton, B.L.: Patterns of Bordetella parapertussis respiratory illnesses: 2008–2010. Clin. Inf. Dis. 54, 534–537 (2012)
Mastrantonio, P., Stefanelli, P., Giuliano, M., Rojas, Y.H., Ciofi degli Atti, M., Anemona, A., Tozzi, A.E.: Bordetella parapertussis infection in children: epidemiology, clinical symptoms, and molecular characteristics of isolates. J. Clin. Microbiol. 36, 999–1002 (1998)
Castillo, M.E., Bada, C., Aguila, D.O., Petrozzi-Helasvuo, V., Casabona-Ore, V., Reyes, I., Del Valle-Mendoza, J.: Detection of Bordetella pertussis using a PCR test in infants younger than one year old hospitalized with whooping cough in five Peruvian hospitals. Int. J. Inf. Dis. 41, 36–41 (2015)
Nikbin, V.S., Shahcheraghi, F., Lotfi, M.N., Zahraei, S.M., Parzadeh, M.: Comparison of culture and real-time PCR for detection of Bordetella pertussis isolated from patients in Iran. Iran. J. Microbiol. 5, 209–214 (2013)
Lind-Brandberg, L., Welinder-Olsson, C., Lagergård, T., Taranger, J,. Trollfors. B., Zackrisson, G.: Evaluation of PCR for diagnosis of Bordetella pertussis and Bordetella parapertussis infections. J. Clin. Microbiol. 36, 679–683 (1998)
Kurbakov, K.A., Konorov, E.A., Minaev, M.Y., Kuznetsova, O.A. Multiplex real-time PCR assay for detection and differentiation of Bordetella pertussis and Bordetella parapertussis. Iran. J. Microbiol. 6, 140–148 (2014)
Xu, Y., Xu, Y., Hou, Q., Yang, R., Zhang, S.: Triplex real-time PCR assay for detection and differentiation of Bordetella pertussis and Bordetella parapertussis. Acta Pathaologica Microbiologica et Immunologica Scandinavica. 118, 685–691 (2010)
Md Eshrat, E.A., Subhas, C.M.: Detection methodologies for pathogen and toxins. Sensors 17, 1885–1905 (2017)
Khalid, M.A., Mohammed, M.Z., Fouzi, M., Salman, A.A., Manal, A.A., Anees, A.A.: DNA-based nanobiosensors as an emerging platform for detection of disease. Sensors 15, 14539–14568 (2015)
Razin, S.: DNA probes and PCR in diagnosis of mycoplasma infections. Mol. Cell. Probes 8, 497–511 (1994)
Touahir, L., Allongue, P., Aureau, D., Boukherroub, R., Chazalviel, J.N., Galopin, E., Gouget-Laemmel, A.C., de Villeneuve, C.H., Moraillon, A., Niedziółka-Jönsson, J., Ozanam, F., Andresa, J.S., Sam, S., Solomon, I., Szunerits, S.: Molecular monolayers on silicon as substrates for biosensors. Bioelectrochem. 80, 17–25 (2010)
Georgiadis, R., Peterlinz, K.P., Peterson, A.W.: Quantitative measurements and modeling of kinetics in nucleic acid monolayer films using SPR spectroscopy. J. Am. Chem. Soc. 122, 3166–3173 (2000)
Kewu, L., Shuang, W., Liming, W., Hui, Y., Ning, J., Rui, X., Zhibin, W.: Fast and sensitive ellipsometry-based biosensing. Sensors 18, 1–13 (2018)
Javed, S., Said, F., Bokhari, H.: Bordetella parapertussis outbreak in Bisham, Pakistan in 2009-2010: fallout of the 9/11 syndrome. Epidemiol. Infect. 143, 2619–2623 (2015)
Xing, W., Cheng, J.: Electronic biosensor based on DNA self-assembled monolayer on gold electrode, Frontiers in Biochip Technology, Springer (2005).
Herne, T.M., Tarlov, M.J.: Characterization of DNA probes immobilized on gold surfaces. J. Am. Chem. Soc. 119, 8916–8920 (1997)
Bokhari, H., Said, F., Syed, M.A., Hussain, A., Kazi, Y.F., Kallonen, T., He, Q., King, A.J., Heuvelman, K., Mooi, F.R.: Molecular typing of Bordetella parapertussis isolates circulating in Pakistan. FEMS Immunol. Med. Microbiol. 63, 373–380 (2011)
Kriechbaumer, V., Tsargorodskaya, A., Mustafa, M.K., Vinogradova, T., Lacey, J., Smith, D.P., Abell, B.M., Nabok, A.: Study of receptor-chaperone interactions using the optical technique of spectroscopic ellipsometry. Biophys. J. 101, 504–511 (2011)
Ieva, B., Zigmas, B., Asta, M., Almira, R., Arunas, R.: Study of antibody/antigen binding kinetics by total internal reflection ellipsometry. Biosens. Bioelectron. 39, 170–176 (2013)
Campos-Ferreira, D.S., Souza, E.V.M., Nascimento, G.A., Zanforlin, D.M.L., Arruda, M.S., Beltrao, M.F., Melo, S.A.L., Bruneska, D., Lima-Filho, J.L.: Electrochemical DNA biosensor for the detection of human papillomavirus E6 gene inserted in recombinant plasmid. Arab. J. Chem. 9, 443–450 (2016)
Miriam, C., Florent, P., Olivier, M., Judikael, L.R., Gerard, B., Rose-Marie, S., Jorg, A., Ludocic, E.: Spectroscopic ellipsometry study of silver nanospheres and nanocubes in thin film layers. Opt. Mater. Express 7, 4241–4249 (2017)
Nabok, A.V., Tsargorodskaya, A., Holloway, A., Starodub, N.F., Gojster, O.: Registration of T-2 mycotoxin with total internal reflection ellipsometry and QCM impedance methods. Biosens. Bioelectron. 22, 885–890 (2007)
Tikhonravov, A.V., Trubetskov, M.K., Masetti, E., Krasilnikova, A.V., Kochikov, I.V.: Sensitivity of the ellipsometric angles psi and delta to the surface inhomogeneity. Conf Adv Opt Interference Coatings 3738, 0277–786X (1999)
Nabok, A., Tsargorodskayaa, A., Mustafa, M.K., Szekacs, I., Starodub, N.F., Szekacs, A.: Detection of low molecular weight toxins using an optical phase method of ellipsometry. Sensors Actuators B Chem. 154, 232–237 (2011)
Legay, G., Markey, L., Meunier- Prest, R., Finot, E.: Measurements of thickness dispersion in biolayers by scanning force microscopy and comparison with spectroscopic ellipsometry analysis. Ultramicroscopy 107, 1111–1117 (2007)
Hwall, M., Eugene, F., Weiwei, Z., Chowdhury, A., David, A., Adri, C.T.D., Srinivas, T.: Modified random sequential adsorption model for understanding kinetics of proteins adsorption at a liquid–solid interface. Langmuir 33, 7215–7224 (2017)
Corsel, J.W., Williems, G.M., Kop, J.M., Cuypers, P.A., Hermensn, W.T.: The role of intrinsic binding rate and transport rate in the adsorption of prothrombin, albumin, and fibrinogen to phospholipid bilayers. J. Colloid Interface Sci. 111, 544–554 (1986)
Pearson, C.E., Wang, Y., Griffith, J.D., Sinden, R.R.: Structural analysis of slipped-strand DNA (S-DNA) formed in (CTG)n. (CAG)n repeats from the myotonic dystrophy locus. Nucleic Acids Res. 26, 816–882 (1998)
Sun, Y., Zhu, X.: An ellipsometry-based biosensor for label-free, real-time, and in-situ detection of DNA–DNA and DNA–protein interactions. Chinese J. Phy. 52, 1398–1406 (2014)
Demirel, G., Mustafa, O.C., Garipcan, B., Piskin, E.: A novel DNA biosensor based on ellipsometry. Surf. Sci. 602, 952–959 (2008)
Mustafa, O.Ç., Filiz, S., Gökhan, D., Bora, G., Burcu, O., Burcu, Ç., Erhan, P.: Stepwise formation approach to improve ellipsometric biosensor response. Nanomedicine 5, 152–161 (2009)
Acknowledgements
This work was supported by the Higher Education Commission, Pakistan (HEC) development grant for ‘Designing and Fabrication of Micro and Nano Devices’ and the department of physics, COMSATS institute of Information Technology, Islamabad, Pakistan.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rafique, S., Idrees, M., Bokhari, H. et al. Ellipsometric-based novel DNA biosensor for label-free, real-time detection of Bordetella parapertussis. J Biol Phys 45, 275–291 (2019). https://doi.org/10.1007/s10867-019-09528-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-019-09528-2