cis-2 and trans-2-eicosenoic Fatty Acids Inhibit Mycobacterium tuberculosis Virulence Factor Protein Tyrosine Phosphatase B

Yıl 2021, Cilt: 8 Sayı: 3, 873 - 882, 31.08.2021

Lalu Rudyat Telly Savalas Asih Lestari Munirah Munirah Suryawati Farida Dedy Suhendra Dina Asnawati Jannatin 'ardhuha Baiq Sarı Ningsih Jufrizal Syahri

https://doi.org/10.18596/jotcsa.896489

Öz

The present study aims to investigate the potential inhibitory effect of eicosenoic fatty acids on protein tyrosine phosphatase B of Mycobacterium tuberculosis (PtpB). PtpB is recognized to play a vital role in Mycobacterium tuberculosis (Mtb) successful latent infection. It prevents the fusion even between phagocytosed mycobacteria with lysosomes so that the bacteria escape from degradation. We have over-expressed recombinant Mtb PtpB within Escherichia coli BL21(DE3), and further, we have used the protein for inhibition assay with cis-2 and trans-eicosenoic fatty acids. It is revealed that at a concentration of 16 µM, cis-2- and trans-2-eicosenoic fatty acids can inhibit PtpB by 63.72% and 74.67%, respectively. Docking analysis has confirmed strong interactions of PtpB with cis-2 and trans-2-eicosenoic fatty acids, with the binding energy of -60.40 and -61.60 kcal/mol, respectively. These findings underline both fatty acids’ high potential to be further investigated to discover drugs against latent tuberculosis infection.

Anahtar Kelimeler

eicosenoic fatty acid, Latent tuberculosis infection, Protein tyrosine phosphatase B, molecular docking

Destekleyen Kurum

Ministry of Research, Technology, and Higher Education, Republic of Indonesia

Proje Numarası

INSINAS Project nr 827/UN18.L1/PP/2018

Teşekkür

Siti Rosidah, our technical assistant

Kaynakça

• 1. WHO. Global Tuberculosis Report [Internet]. World Health Organization; URL: https://www.who.int/teams/global-tuberculosis-programme/tb-reports.
• 2. Houben RMGJ, Dodd PJ. The Global Burden of Latent Tuberculosis Infection: A Re-estimation Using Mathematical Modelling. Metcalfe JZ, editor. PLoS Med. 2016 Oct 25;13(10):e1002152. DOI: https://doi.org/10.1371/journal.pmed.1002152. 3. Desjardins M, Huber L, Parton R, Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. Journal of Cell Biology. 1994 Mar 1;124(5):677–88. DOI: https://doi.org/10.1083/jcb.124.5.677.
• 4. Upadhyay S, Mittal E, Philips JA. Tuberculosis and the art of macrophage manipulation. Pathogens and Disease [Internet]. 2018 Jun 1 [cited 2021 Jul 28];76(4): fty037. URL: https://academic.oup.com/femspd/article/doi/10.1093/femspd/fty037/4970761.
• 5. Pahari S, Kaur G, Negi S, Aqdas M, Das DK, Bashir H, et al. Reinforcing the Functionality of Mononuclear Phagocyte System to Control Tuberculosis. Front Immunol. 2018 Feb 9;9:193. DOI: https://doi.org/10.3389/fimmu.2018.00193.
• 6. Kansutton C, Jagannath C, Hunterjr R. Trehalose 6,6′-dimycolate on the surface of Mycobacterium tuberculosis modulates surface marker expression for antigen presentation and costimulation in murine macrophages. Microbes and Infection. 2009 Jan;11(1):40–8. DOI: https://doi.org/10.1016/j.micinf.2008.10.006.
• 7. Queval CJ, Brosch R, Simeone R. The Macrophage: A Disputed Fortress in the Battle against Mycobacterium tuberculosis. Front Microbiol. 2017 Nov 23;8:2284. DOI: https://doi.org/10.3389/fmicb.2017.02284.
• 8. Rankine-Wilson LI, Shapira T, Sao Emani C, Av-Gay Y. From infection niche to therapeutic target: the intracellular lifestyle of Mycobacterium tuberculosis. Microbiology [Internet]. 2021 Apr 7 [cited 2021 Jul 28];167(4). URL: https://www.microbiologyresearch.org/content/journal/micro/10.1099/mic.0.001041.
• 9. Stutz MD, Clark MP, Doerflinger M, Pellegrini M. Mycobacterium tuberculosis : Rewiring host cell signaling to promote infection. J Leukoc Biol. 2018 Feb;103(2):259–68. DOI: https://doi.org/10.1002/JLB.4MR0717-277R.
• 10. Salina EG, Mollenkopf HJ, Kaufmann SHE, Kaprelyants AS. M. tuberculosis Gene Expression during Transition to the “Non-Culturable” State. Acta Naturae. 2009 Jul;1(2):73–7. URL: https://www.ncbi.nlm.nih.gov/pubmed/22649605.
• 11. Dutta NK, He R, Pinn ML, He Y, Burrows F, Zhang Z-Y, et al. Mycobacterial Protein Tyrosine Phosphatases A and B Inhibitors Augment the Bactericidal Activity of the Standard Anti-tuberculosis Regimen. ACS Infect Dis. 2016 Mar 11;2(3):231–9. DOI: https://doi.org/10.1021/acsinfecdis.5b00133.
• 12. Cowley SC, Babakaiff R, Av-Gay Y. Expression and localization of the Mycobacterium tuberculosis protein tyrosine phosphatase PtpA. Research in Microbiology. 2002 May;153(4):233–41. DOI: https://doi.org/10.1016/S0923-2508(02)01309-8.
• 13. Singh R, Rao V, Shakila H, Gupta R, Khera A, Dhar N, et al. Disruption of mptpB impairs the ability of Mycobacterium tuberculosis to survive in guinea pigs. Molecular Microbiology. 2003 Nov;50(3):751–62. DOI: https://doi.org/10.1046/j.1365-2958.2003.03712.x.
• 14. Wong D, Chao JD, Av-Gay Y. Mycobacterium tuberculosis-secreted phosphatases: from pathogenesis to targets for TB drug development. Trends in Microbiology. 2013 Feb;21(2):100–9. DOI: https://doi.org/10.1016/j.tim.2012.09.002.
• 15. Forrellad MA, Klepp LI, Gioffré A, Sabio y García J, Morbidoni HR, Santangelo M de la P, et al. Virulence factors of the Mycobacterium tuberculosis complex. Virulence. 2013 Jan;4(1):3–66. DOI: https://doi.org/10.4161/viru.22329.
• 16. Wong D, Bach H, Sun J, Hmama Z, Av-Gay Y. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proceedings of the National Academy of Sciences. 2011 Nov 29;108(48):19371–6. DOI: https://doi.org/10.1073/pnas.1109201108.
• 17. Zhou B, He Y, Zhang X, Xu J, Luo Y, Wang Y, et al. Targeting mycobacterium protein tyrosine phosphatase B for antituberculosis agents. Proceedings of the National Academy of Sciences. 2010 Mar 9;107(10):4573–8. DOI: https://doi.org/10.1073/pnas.0909133107.
• 18. Fan L, Wu X, Jin C, Li F, Xiong S, Dong Y. MptpB Promotes Mycobacteria Survival by Inhibiting the Expression of Inflammatory Mediators and Cell Apoptosis in Macrophages. Front Cell Infect Microbiol. 2018 May 25;8:171. DOI: https://doi.org/10.3389/fcimb.2018.00171.
• 19. Savalas LRT, Furqon BRN, Asnawati D, ’Ardhuha J, Sedijani P, Hadisaputra S, et al. Cis-2 and trans-2-eisocenoic fatty acids are novel inhibitors for Mycobacterium tuberculosis Protein tyrosine phosphatase A. Acta Biochim Pol [Internet]. 2020 Jun 18 [cited 2021 Jul 28]; DOI: https://doi.org/10.18388/abp.2020_5201.
• 20. Mascarello A, Mori M, Chiaradia-Delatorre LD, Menegatti ACO, Monache FD, Ferrari F, et al. Discovery of Mycobacterium tuberculosis Protein Tyrosine Phosphatase B (PtpB) Inhibitors from Natural Products. Maga G, editor. PLoS ONE. 2013 Oct 14;8(10):e77081. DOI: https://doi.org/10.1371/journal.pone.0077081. 21. Huyer G, Liu S, Kelly J, Moffat J, Payette P, Kennedy B, et al. Mechanism of Inhibition of Protein-tyrosine Phosphatases by Vanadate and Pervanadate. Journal of Biological Chemistry. 1997 Jan;272(2):843–51. DOI: https://doi.org/10.1074/jbc.272.2.843.
• 22. Dhanjal JK, Grover S, Sharma S, Singh A, Grover A. Structural insights into mode of actions of novel natural Mycobacterium protein tyrosine phosphatase B inhibitors. BMC Genomics. 2014;15(Suppl 1):S3. DOI: https://doi.org/10.1186/1471-2164-15-S1-S3.
• 23. Laemmli UK. Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature. 1970 Aug;227(5259):680–5. DOI: https://doi.org/10.1038/227680a0.
• 24. Savalas LRT, Sedijani P, Hadisaputra S, Ardhuha J, Lestari CA, Wahidah EN. Expression of Mycobacterium tuberculosis Protein Tyrosine Phosphatase B in Escherichia coli and Its Recovery from Inclusion Body. J Bio Bio Edu. 2017 Dec 31;9(3):530. DOI: https://doi.org/10.15294/biosaintifika.v9i3.12384.
• 25. Pace CN, Grimsley GR, Scholtz JM, Shaw KL. Protein Stability. In: John Wiley & Sons Ltd, editor. Protein Science Encyclopedia [Internet]. Chichester, UK: John Wiley & Sons, Ltd; 2014 [cited 2021 Jul 28]. p. a0003002.pub3. URL: https://onlinelibrary.wiley.com/doi/10.1002/9780470015902.a0003002.pub3.
• 26. Mascarello A, Chiaradia LD, Vernal J, Villarino A, Guido RVC, Perizzolo P, et al. Inhibition of Mycobacterium tuberculosis tyrosine phosphatase PtpA by synthetic chalcones: Kinetics, molecular modeling, toxicity and effect on growth. Bioorganic & Medicinal Chemistry. 2010 Jun 1;18(11):3783–9. DOI: https://doi.org/10.1016/j.bmc.2010.04.051.
• 27. Chiaradia LD, Martins PGA, Cordeiro MNS, Guido RVC, Ecco G, Andricopulo AD, et al. Synthesis, Biological Evaluation, And Molecular Modeling of Chalcone Derivatives As Potent Inhibitors of Mycobacterium tuberculosis Protein Tyrosine Phosphatases (PtpA and PtpB). J Med Chem. 2012 Jan 12;55(1):390–402. DOI: https://doi.org/10.1021/jm2012062.
• 28. Chai Q, Wang L, Liu CH, Ge B. New insights into the evasion of host innate immunity by Mycobacterium tuberculosis. Cell Mol Immunol. 2020 Sep;17(9):901–13. DOI: https://doi.org/10.1038/s41423-020-0502-z.
• 29. Mascarello A, Mori M, Chiaradia-Delatorre LD, Menegatti ACO, Monache FD, Ferrari F, et al. Discovery of Mycobacterium tuberculosis Protein Tyrosine Phosphatase B (PtpB) Inhibitors from Natural Products. Maga G, editor. PLoS ONE. 2013 Oct 14;8(10):e77081. DOI: https://doi.org/10.1371/journal.pone.0077081.
• 30. Liu Z, Wang Q, Li S, Cui H, Sun Z, Chen D, et al. Polypropionate Derivatives with Mycobacterium tuberculosis Protein Tyrosine Phosphatase B Inhibitory Activities from the Deep-Sea-Derived Fungus Aspergillus fischeri FS452. J Nat Prod. 2019 Dec 27;82(12):3440–9. DOI: https://doi.org/10.1021/acs.jnatprod.9b00834.
• 31. Vickers CF, Silva APG, Chakraborty A, Fernandez P, Kurepina N, Saville C, et al. Structure-Based Design of MptpB Inhibitors That Reduce Multidrug-Resistant Mycobacterium tuberculosis Survival and Infection Burden in Vivo. J Med Chem. 2018 Sep 27;61(18):8337–52. DOI: https://doi.org/10.1021/acs.jmedchem.8b00832.