Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 13, pp 5259–5267 | Cite as

Ribokinase screened from T7 phage displayed Mycobacterium tuberculosis genomic DNA library had good potential for the serodiagnosis of tuberculosis

  • Dan Luo
  • Li Wang
  • Haican Liu
  • Lingling Li
  • Yating Liao
  • Xiaomei Yi
  • Xiaoliang Yan
  • Kanglin WanEmail author
  • Yanhua ZengEmail author
Biotechnologically relevant enzymes and proteins

Abstract

Tuberculosis caused by Mycobacterium tuberculosis (M. tuberculosis) is the leading cause of death among infectious diseases in the worldwide. Lack of more sensitive and effective diagnostic reagents has increased the awareness of rapid diagnosis for tuberculosis. In this study, T7 phage displayed genomic DNA library of M. tuberculosis was constructed to screen the antigens that specially bind with TB-positive serum from the whole genome of M. tuberculosis and to improve the sensitivity and specificity of tuberculosis serological diagnosis. After three rounds of biopanning, results of DNA sequencing and BLAST analysis showed that 19 positive phages displayed four different proteins and the occurrence frequency of the phage which displayed ribokinase was the highest. The results of indirect ELISA and dot immunoblotting indicated that representative phages could specifically bind to tuberculosis-positive serum. The prokaryotic expression vector containing the DNA sequence of ribokinase gene was then constructed and the recombinant protein was expressed and purified to evaluate the serodiagnosis value of ribokinase. The reactivity of the recombinant ribokinase with different clinical serum was detected and the sensitivities and specificities in tuberculosis serodiagnosis were 90% and 86%, respectively by screening serum from tuberculosis patients (n = 90) and uninfected individuals (n = 90) based on ELISA. Therefore, this study demonstrated that ribokinase had good potential for the serodiagnosis of tuberculosis.

Keywords

Ribokinase T7 phage displayed genomic DNA library Mycobacterium tuberculosis Serological diagnosis 

Notes

Funding information

This study was funded by “Prevention and Control of AIDS and Viral Hepatitis etc. Other Major Infectious Disease”—the Science and Technology Major Special Project of the 12th Five-Year Plan of China (grant number 10003006–002) and the National Natural Science Foundation of China (grant number 81871256).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

The study was approved by the ethics review board of University of South China.

References

  1. Abebe F, Holm-Hansen C, Wiker HG, Bjune G (2007) Progress in serodiagnosis of Mycobacterium tuberculosis infection. Scand J Immunol 66(2-3):176–191CrossRefGoogle Scholar
  2. Baumann R, Kaempfer S, Chegou NN, Oehlmann W, Loxton AG, Kaufmann SH, van Helden PD, Black GF, Singh M, Walzl G (2014) Serologic diagnosis of tuberculosis by combining classes against selected mycobacterial targets. J Inf Secur 69:581–589Google Scholar
  3. Beghetto E, De Paolis F, Montagnani F, Cellesi C, Gargano N (2009) Discovery of new Mycoplasma pneumoniae antigens by use of a whole–genome lambda display library. Microbes Infect 11(1):66–73CrossRefGoogle Scholar
  4. Chen Y, Cao S, Liu Y, Zhang X, Wang W, Li C (2018) Potential role for Rv2026c- and Rv2421c- specific antibody responses in diagnosing active tuberculosis. Clin Chim Acta 487:369–376CrossRefGoogle Scholar
  5. De Paolis F, Beghetto E, Spadoni A, Montagnani F, Felici F, Oggioni MR, Gargano N (2007) Identification of a human immunodominant B–cell epitope within the immunoglobulin A1 protease of Streptococcus pneumoniae. BMC Microbiol 7:113CrossRefGoogle Scholar
  6. Deng X, Wang L, You X, Dai P, Zeng Y (2018) Advances in the T7 phage display system (review). Mol Med Rep 17:714–720Google Scholar
  7. Di Cristina M, Del Porto P, Buffolano W, Beghetto E, Spadoni A, Guglietta S, Piccolella E, Felici F, Gargano N (2004) The Toxoplasma gondii bradyzoite antigens BAG1 and MAG1 induce early humoral and cell-mediated immune responses upon human infection. Microbes Infect 6:164–171CrossRefGoogle Scholar
  8. Domina M, Lanza Cariccio V, Benfatto S, Venza M, Venza I, Borgogni E, Castellino F, Midiri A, Galbo R, Romeo L, Biondo C, Masignani V, Teti G, Felici F, Beninati C (2016) Functional characterization of a monoclonal antibody epitope using a lambda phage displayed–deep sequencing platform. Sci Rep 6:31458CrossRefGoogle Scholar
  9. Ebrahimizadeh W, Rajabibazl M (2014) Bacteriophage vehicles for phage display: biology, mechanism, and application. Curr Microbiol 69:109–120CrossRefGoogle Scholar
  10. Kori LD, Hofmann A, Patel BK (2012) Expression, purification, crystallization and preliminary X–ray diffraction analysis of a ribokinase from the thermohalophile Halothermothrix orenii. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:240–243CrossRefGoogle Scholar
  11. Krishna P, Jain A, Bisen PS (2016) Microbiome diversity in the sputum of patients with pulmonary tuberculosis. Eur J Clin Microbiol Infect Dis 35:1205–1215CrossRefGoogle Scholar
  12. Luo L, Zhu L, Yue J, Liu J, Liu G, Zhang X, Wang H, Xu Y (2017) Antigens Rv0310c and Rv1255c are promising novel biomarkers for the diagnosis of Mycobacterium tuberculosis infection. Emerg Microbes Infect 6:e64CrossRefGoogle Scholar
  13. Machado D, Couto I, Viveiros M (2018) A rapid molecular assays for detection of tuberculosis. Pneumonia (Nathan) 10(1):4CrossRefGoogle Scholar
  14. Osei E, Der J, Owusu R, Kofie P, Axame WK (2017) The burden of HIV on Tuberculosis patients in the Volta region of Ghana from 2012 to 2015: implication for Tuberculosis control. BMC Infect Dis 17:504CrossRefGoogle Scholar
  15. Park J, Gupta RS (2008) Adenosine kinase and ribokinase– the RK family of proteins. Cell Mol Life Sci 65:2875–2896CrossRefGoogle Scholar
  16. Piggott AM, Karuso P (2016) Identifying the cellular targets of natural products using T7 phage display. Nat Prod Rep 33:626–636CrossRefGoogle Scholar
  17. Qiang X, Sun K, Xing L, Xu Y (2017) Discovery of a polystyrene binding peptide isolated from phage displayed library and its application in peptide immobilization. Sci Rep 7:2673CrossRefGoogle Scholar
  18. Roupie V, Alonso-Velasco E, Van Der Heyden S, Holbert S, Duytschaever L, Berthon P, Van Dosselaer I, Van Campe W, Mostin L, Biet F, Roels S, Huygen K, Fretin D (2018) Evaluation of mycobacteria-specific gamma interferon and antibody responses before and after a single intradermal skin test in cattle naturally exposed to M. avium subsp. paratuberculosis and experimentally infected with M. bovis. Vet Immunol Immunopathol 196:35–47CrossRefGoogle Scholar
  19. Sakamoto K, Kawata Y, Masuda Y, Umemoto T, Ito T, Asami T, Takekawa S, Ohtaki T, Inooka H (2016) Discovery of an artificial peptide agonist to the fibroblast growth factor receptor 1c/βklotho complex from random peptide T7 phage display. Biochem Biophys Res Commun 480:55–60CrossRefGoogle Scholar
  20. Sakamoto K, Ishibashi Y, Adachi R, Matsumoto SI, Oki H, Kamada Y, Sogabe S, Zama Y, Sakamoto JI, Tani A (2017) Identification of cytidine–5–triphosphate synthase1–selective inhibitory peptide from random peptide library displayed on T7 phage. Peptides 94:56–63CrossRefGoogle Scholar
  21. San Segundo-Acosta P, Garranzo-Asensio M, Oeo-Santos C, Montero-Calle A, Quiralte J, Cuesta-Herranz J, Villalba M, Barderas R (2018) High–throughput screening of T7 phage display and protein microarrays as a methodological approach for the identification of IgE–reactive components. J Immunol Methods 456:44–53CrossRefGoogle Scholar
  22. Shi W, Zhao L, Li S, Xu G, Zeng Y (2018) Serological diagnosis of mycoplasma pneumoniae infection by using the mimic epitopes. World J Microbiol Biotechnol 34:82CrossRefGoogle Scholar
  23. Talwar H, Rosati R, Li J, Kissner D, Ghosh S, Madrid FF, Samavati L (2015) Development of a T7 phage display library to detect sarcoidosis and tuberculosis by a panel of novel antigens. Ebio medicine 2:341–350Google Scholar
  24. Talwar H, Talreja J, Samavati L (2016) T7 phage display library a promising strategy to detect tuberculosis specific biomarkers. Mycobact Dis 6:214CrossRefGoogle Scholar
  25. Talwar H, Hanoudi SN, Draghici S, Samavati L (2018) Novel T7 phage display library detects classifiers for active Mycobacterium tuberculosis infection. Viruses 10:375CrossRefGoogle Scholar
  26. Theron G, Peter J, van Zyl-Smit R, Mishra H, Streicher E, Murray S, Dawson R, Whitelaw A, Hoelscher M, Sharma S, Pai M, Warren R, Dheda K (2011) Evaluation of the Xpert MTB/RIF assay for the diagnosis of pulmonary tuberculosis in a high HIV prevalence setting. Am J Respir Crit Care Med 184:132–172CrossRefGoogle Scholar
  27. Wang Y, Wang L (2017) Vaccination with phage–displayed antigenic epitope. Methods Mol Biol 1625:225–235CrossRefGoogle Scholar
  28. Wang L, Deng X, Liu H, Zhao L, You X, Dai P, Wan K, Zeng Y (2016) The mimic epitopes of Mycobacterium tuberculosis screened by phage displayed peptide library have serodiagnostic potential for tuberculosis. Pathoge Dis 74.  https://doi.org/10.1093/femspd/ftw091
  29. Xu JN, Chen JP, Chen DL (2012) Serodiagnsis efficacy and immunogenicity of the fusion protein of Mycobacterium tuberculosis composed of the 10-kilodalton culture filtrate protein, ESAT-6, and the extracellular domain fragment of PPE68. Clin Vaccine Immunol 19(4):536–580CrossRefGoogle Scholar
  30. Yan ZH, Yi L, Wei PJ, Jia HY, Wang J, Wang XJ, Yang B, Gao X, Zhao YL, Zhang HT (2018) Evaluation of panels of Mycobacterium tuberculosis antigens for serodiagnosis of tuberculosis. Int J Tuberc Lung Dis 22(8):959–965CrossRefGoogle Scholar
  31. Yang Q, Liu Y, Huang F, He ZG (2011) Physical and functional interaction between D-ribokinase and topoisomerase I has opposite effects on their respective activity in Mycobacterium smegmatis and Mycobacterium tuberculosis. Arch Biochem Biophys 512(2):135–142CrossRefGoogle Scholar
  32. You X, Li R, Wan K, Liu L, Xie X, Zhao L, Wu N, Deng X, Wang L, Zeng Y (2017) Evaluation of Rv0220, Rv2958c, Rv2994 and Rv3347c of Mycobacterium tuberculosis for serodiagnosis of tuberculosis. Microb Biotechnol 10:604–611CrossRefGoogle Scholar
  33. Zhou F, Xu X, Wu S, Cui X, Fan L, Pan W (2015) Protein array identification of protein markers for serodiagnosis of Mycobacterium tuberculosis infection. Sci Rep 5:15349CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Dan Luo
    • 1
  • Li Wang
    • 1
  • Haican Liu
    • 2
  • Lingling Li
    • 1
  • Yating Liao
    • 1
  • Xiaomei Yi
    • 3
  • Xiaoliang Yan
    • 1
  • Kanglin Wan
    • 2
    Email author
  • Yanhua Zeng
    • 1
    Email author
  1. 1.Institute of Pathogenic Biology, Hengyang Medical College, Hunan Provincial Key Laboratory for Special Pathogens Prevention and Control, Hunan Province Cooperative Innovation Center for Molecular Target New Drug StudyUniversity of South ChinaHengyangPeople’s Republic of China
  2. 2.State Key Laboratory for Infectious Disease Prevention and Control/National Institute for communicable Disease Control and PreventionChinese Center for Disease Control and PreventionBeijingPeople’s Republic of China
  3. 3.Reproductive Medical CenterThe Affiliated First Hospital, University of South ChinaHengyangPeople’s Republic of China

Personalised recommendations