Biochemical evaluation and molecular docking studies on encapsulated astaxanthin for the growth inhibition of Mycobacterium tuberculosis

Suganya Vasudevan; Anuradha Venkatraman; Syed Ali Mohammed Yahoob; Sasirekha; Malathi Jojula; Ravikumar Sundaram; P Boomi

doi:10.7324/JABB.2021.95.1s6

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Abstract

Astaxanthin, a tetraterpenoid compound was formulated as liposomes and screened for anti-tubercular activity against different strains of Mycobacterium tuberculosis: MTB, MDR-TB, and H37Rv isolated from the patient sputum samples. Minimum inhibitory concentration (MIC) was determined by proportion-based method. The molecular docking analysis of astaxanthin with various mycobacterial drug target proteins were performed using in silico tools. Encapsulated astaxanthin showed better inhibition of MTB with MIC value of 500 μg/ml against all the selected strains. The docking analysis provided the interacting amino acid residues of selected mycobacterial enzymes and mode of ligand–protein interaction. Based on the present study, it was concluded that encapsulated astaxanthin could be a better cost-effective natural compound for the treatment of tuberculosis among the patients which will combat side effects in comparison with the first line AntiTB drugs like rifampicin and isoniazid.

Keyword: Mycobacterium tuberculosis antitubercular activity molecular docking liposomal encapsulation astaxanthin

Citation:

Vasudevan S, Venkatraman A, Yahoob SAM, Sasirekha, Jojula M, Sundaram R, Boomi P. Biochemical evaluation and molecular docking studies on encapsulated astaxanthin for the growth inhibition of Mycobacterium tuberculosis. J Appl Biol Biotech, 2021;9(S1):31–39.

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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2. Centers for Disease Control and Prevention (CDC). Trends in tuberculosis-United States. MMWR Morb Mortal Wkly Rep 2005;18:245-9.
3. Cubillos-Ruiz A, Sandoval A, Ritacco V, López B, Robledo J, Correa N. Genomic signatures of the haarlem lineage of Mycobacterium tuberculosis: implications of strain genetic variation in drug and vaccine development. J Clin Microbiol 2010;48:3614-23. https://doi.org/10.1128/JCM.00157-10
4. Alix E, Godreuil S, Blanc-Potard AB. Identification of a Haarlem genotype-specific single nucleotide polymorphism in the mgt C virulence gene of Mycobacterium tuberculosis. J Clin Microbiol 2006;44:2093-8. https://doi.org/10.1128/JCM.00278-06
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6. Chidambaram S, Swaminathan R. In-vitro antimycobacterial activity of selected Indian medicinal plants to resistant strains of Mycobacterium tuberculosis. Int J Pharm Sci Res 2016;7:4130-3.
7. Beena D, Rawat S. Antituberculosis drug research: a critical overview. Med Res Rev 2013;33:693-764. https://doi.org/10.1002/med.21262
8. O'Niel MJ, Smith A, Heckelman PE. The Merck Index.13th edition, Merck & Co. Inc., New Jersey, p 1785, 2001.
9. Reddy VM, Reddy KR. Synthesis and antimicrobial activity of some novel 4-(1H-benzd]imidazol-2yl)-1,3-thiazol-2-amines. Chem Pharm Bull 2001;58:953-6.
10. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and application. Crit Rev Food Sci Nutr 2006;46:185-96. https://doi.org/10.1080/10408690590957188
11. Yuan JP, Chen F, Li X, Li Z. Carotenoid composition in the green microalga chlorococcum. Food Chem 2002;76:319-25. https://doi.org/10.1016/S0308-8146(01)00279-5
12. Dhankhar J, Kadian SS, Sharma A. Astaxanthin: A Potential Carotenoid. Int J Pharm Sci Res 2012;3:1246-359.
13. Suntress EZ. Liposomal antioxidants for protection against oxidantInduced damage. J Toxicol 2011;2011:1-6. https://doi.org/10.1155/2011/152474
14. Suganya V, Anuradha V, Syed Ali M, Sangeetha P, Bhuvana P. In vitro antioxidant activity of microencapsulated and non-encapsulated astaxanthin. Asian J Sci Technol 2017;8:6391-404.
15. Murahari D, Tanniru S, Poonem L, Paramesh A, Sudheer Kumar K, Jojula M, et al. Anti- mycobacterial screening methods for new compounds identification. Euro J Biomed Pharma Sci 2018;5:584-9.
16. Narender M, Jaswanth SB, Umasankar K, Malathi J, Reddy AR, Umadevi KR, et al. Synthesis, in vitro antimycobacterial evaluation and docking studies of some new 5,6,7,8-tetrahydropyrido [4',3':4,5] thieno [2,3-d] pyrimidin-4(3H)-one schiff bases. Bioorg Med Chem Lett 2016;26:836-40. https://doi.org/10.1016/j.bmcl.2015.12.083
17. Bikadi Z, Hazai E. Application of the PM6 semi-empirical method to modelling proteins enhances docking accuracy of Autodock. J Cheminform 2009;1:1-5. https://doi.org/10.1186/1758-2946-1-15
18. Morris GM, Goodsell DS. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 1998;19:1639-62. https://doi.org/10.1002/(SICI)1096-987X(19981115)19:14<1639::AID-JCC10>3.0.CO;2-B
19. Solis FJ, Wets RJB. Minimization by random search techniques. Math Operations Res 1981;6:19-30. https://doi.org/10.1287/moor.6.1.19
20. Vivek K, Fatima A, Faridi U, Arvind S, Shanker K, Kumar JK, et al. Antimicrobial potential of Glycyrrhizaglabraroots. J Ethanopharmacol 2008;116:377-80. https://doi.org/10.1016/j.jep.2007.11.037
21. Ganihiama DU, Sureram S, Sangher S, Honqmanee P, Aree T, Mahidol C, et al. Antimycobacterial activity of natural products and synthetic agents: pyrrolodiquinolines and vermelhotin as anti-tubercular leads against clinical multidrug resistant isolates of Mycobacterium tuberculosis. Eur J Med Chem 2015;89:1-2. https://doi.org/10.1016/j.ejmech.2014.10.026
22. Gemechu A, Giday M, Worku A, Ameni G. In vitro Anti-mycobacterial activity of selected medicinal plants against Mycobacterium tuberculosis and Mycobacterium bovis Strains. BMC Complement Altern Med 2013;13:1-6. https://doi.org/10.1186/1472-6882-13-291
23. Calvori C, Frontali L, Leoni L, Tecce G. Effect of rifampicin on protein synthesis. Nature 1965;207:417-8. https://doi.org/10.1038/207417a0
24. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 2001;104:901-12. https://doi.org/10.1016/S0092-8674(01)00286-0
25. Feklistov A, Mekler V, Jiang Q, Westblade LF, Irschik H, Jansen R, et al. Rifamycins do not function by allosteric modulation of binding of Mg2 + to the RNA. PNAS 2008;105:14820-5. https://doi.org/10.1073/pnas.0802822105
26. Zhenhua Z. Total variation based denoising model for bioinformatics images. Int J BioaAutomation 2016;20:457-70.
27. Timmins GS, Master S, Rusnak F, Deretic V. Nitric oxide generated from isoniazid activation by KatG: source of nitric oxide and activity against Mycobacterium tuberculosis. Antimicrob Agents Chem 2004;48:3006-9. https://doi.org/10.1128/AAC.48.8.3006-3009.2004
28. Ahmad Z, Klinkenberg LG, Pinn ML, Fraig MM, Peloquin CA, Bishai WR, et al. Biphasic Kill curve of isoniazid reveals the presence of drug-tolerant, not drug-resistant, Mycobacterium tuberculosis in the guinea pig. J Infect Dis 2009;200:1136-43. https://doi.org/10.1086/605605
29. Judd FK, Mijch AM, Cockram A, Norman TR. Isoniazid and antidepressants: is there cause for concern. Int Clin Psychopharmacol 1994;9:123-5. https://doi.org/10.1097/00004850-199400920-00009

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Vasudevan S [PubMed] [Google Scholar ]

Venkatraman A [PubMed] [Google Scholar ]

Yahoob S A M [PubMed] [Google Scholar ]

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Jojula M [PubMed] [Google Scholar ]

Sundaram R [PubMed] [Google Scholar ]

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By article title

1.Moravkova M, Slany M, Trcka I, Havelkova M, Svobodova J, Skoric M. Human-to-human and human-to-dog Mycobacterium tuberculosis transmission studied by IS6110 RFLP analysis: a case report. Vet Med 2011;56:314-7. https://doi.org/10.17221/1547-VETMED

2. Centers for Disease Control and Prevention (CDC). Trends in tuberculosis-United States. MMWR Morb Mortal Wkly Rep 2005;18:245-9.

3. Cubillos-Ruiz A, Sandoval A, Ritacco V, López B, Robledo J, Correa N. Genomic signatures of the haarlem lineage of Mycobacterium tuberculosis: implications of strain genetic variation in drug and vaccine development. J Clin Microbiol 2010;48:3614-23. https://doi.org/10.1128/JCM.00157-10

4. Alix E, Godreuil S, Blanc-Potard AB. Identification of a Haarlem genotype-specific single nucleotide polymorphism in the mgt C virulence gene of Mycobacterium tuberculosis. J Clin Microbiol 2006;44:2093-8. https://doi.org/10.1128/JCM.00278-06

5. WHO Global Tuberculosis Programme ., WHO, Geneva, Switzerland, 2010. Available via http://www.who.int/mediacentre/ factsheets/fs104/en/index.html.

6. Chidambaram S, Swaminathan R. In-vitro antimycobacterial activity of selected Indian medicinal plants to resistant strains of Mycobacterium tuberculosis. Int J Pharm Sci Res 2016;7:4130-3.

7. Beena D, Rawat S. Antituberculosis drug research: a critical overview. Med Res Rev 2013;33:693-764. https://doi.org/10.1002/med.21262

8. O'Niel MJ, Smith A, Heckelman PE. The Merck Index.13th edition, Merck & Co. Inc., New Jersey, p 1785, 2001.

9. Reddy VM, Reddy KR. Synthesis and antimicrobial activity of some novel 4-(1H-benzd]imidazol-2yl)-1,3-thiazol-2-amines. Chem Pharm Bull 2001;58:953-6.

10. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and application. Crit Rev Food Sci Nutr 2006;46:185-96. https://doi.org/10.1080/10408690590957188

11. Yuan JP, Chen F, Li X, Li Z. Carotenoid composition in the green microalga chlorococcum. Food Chem 2002;76:319-25. https://doi.org/10.1016/S0308-8146(01)00279-5

12. Dhankhar J, Kadian SS, Sharma A. Astaxanthin: A Potential Carotenoid. Int J Pharm Sci Res 2012;3:1246-359.

13. Suntress EZ. Liposomal antioxidants for protection against oxidantInduced damage. J Toxicol 2011;2011:1-6. https://doi.org/10.1155/2011/152474

14. Suganya V, Anuradha V, Syed Ali M, Sangeetha P, Bhuvana P. In vitro antioxidant activity of microencapsulated and non-encapsulated astaxanthin. Asian J Sci Technol 2017;8:6391-404.

15. Murahari D, Tanniru S, Poonem L, Paramesh A, Sudheer Kumar K, Jojula M, et al. Anti- mycobacterial screening methods for new compounds identification. Euro J Biomed Pharma Sci 2018;5:584-9.

16. Narender M, Jaswanth SB, Umasankar K, Malathi J, Reddy AR, Umadevi KR, et al. Synthesis, in vitro antimycobacterial evaluation and docking studies of some new 5,6,7,8-tetrahydropyrido [4',3':4,5] thieno [2,3-d] pyrimidin-4(3H)-one schiff bases. Bioorg Med Chem Lett 2016;26:836-40. https://doi.org/10.1016/j.bmcl.2015.12.083

17. Bikadi Z, Hazai E. Application of the PM6 semi-empirical method to modelling proteins enhances docking accuracy of Autodock. J Cheminform 2009;1:1-5. https://doi.org/10.1186/1758-2946-1-15

18. Morris GM, Goodsell DS. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 1998;19:1639-62. https://doi.org/10.1002/(SICI)1096-987X(19981115)19:14<1639::AID-JCC10>3.0.CO;2-B

19. Solis FJ, Wets RJB. Minimization by random search techniques. Math Operations Res 1981;6:19-30. https://doi.org/10.1287/moor.6.1.19

20. Vivek K, Fatima A, Faridi U, Arvind S, Shanker K, Kumar JK, et al. Antimicrobial potential of Glycyrrhizaglabraroots. J Ethanopharmacol 2008;116:377-80. https://doi.org/10.1016/j.jep.2007.11.037

21. Ganihiama DU, Sureram S, Sangher S, Honqmanee P, Aree T, Mahidol C, et al. Antimycobacterial activity of natural products and synthetic agents: pyrrolodiquinolines and vermelhotin as anti-tubercular leads against clinical multidrug resistant isolates of Mycobacterium tuberculosis. Eur J Med Chem 2015;89:1-2. https://doi.org/10.1016/j.ejmech.2014.10.026

22. Gemechu A, Giday M, Worku A, Ameni G. In vitro Anti-mycobacterial activity of selected medicinal plants against Mycobacterium tuberculosis and Mycobacterium bovis Strains. BMC Complement Altern Med 2013;13:1-6. https://doi.org/10.1186/1472-6882-13-291

23. Calvori C, Frontali L, Leoni L, Tecce G. Effect of rifampicin on protein synthesis. Nature 1965;207:417-8. https://doi.org/10.1038/207417a0

24. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 2001;104:901-12. https://doi.org/10.1016/S0092-8674(01)00286-0

25. Feklistov A, Mekler V, Jiang Q, Westblade LF, Irschik H, Jansen R, et al. Rifamycins do not function by allosteric modulation of binding of Mg2 + to the RNA. PNAS 2008;105:14820-5. https://doi.org/10.1073/pnas.0802822105

26. Zhenhua Z. Total variation based denoising model for bioinformatics images. Int J BioaAutomation 2016;20:457-70.

27. Timmins GS, Master S, Rusnak F, Deretic V. Nitric oxide generated from isoniazid activation by KatG: source of nitric oxide and activity against Mycobacterium tuberculosis. Antimicrob Agents Chem 2004;48:3006-9. https://doi.org/10.1128/AAC.48.8.3006-3009.2004

28. Ahmad Z, Klinkenberg LG, Pinn ML, Fraig MM, Peloquin CA, Bishai WR, et al. Biphasic Kill curve of isoniazid reveals the presence of drug-tolerant, not drug-resistant, Mycobacterium tuberculosis in the guinea pig. J Infect Dis 2009;200:1136-43. https://doi.org/10.1086/605605

29. Judd FK, Mijch AM, Cockram A, Norman TR. Isoniazid and antidepressants: is there cause for concern. Int Clin Psychopharmacol 1994;9:123-5. https://doi.org/10.1097/00004850-199400920-00009