Reimagining the Transition of Mycobacterium Tuberculosis Research from Mammalian Models to Zebrafish
Keywords:
Mycobacterium tuberculosis, Animal models, Pathogenicity, Zebrafish, ImmunityAbstract
Tuberculosis is a highly contagious and infectious disease caused by the microorganism Mycobacterium tuberculosis (Mtb). Tuberculosis remains a significant global health concern, affecting millions of people worldwide. This article reviews the transition of Mtb research with several animal models, focusing on zebrafish as a unique approach. Traditionally, guinea pigs, rabbits, mice, and monkeys have been used, but zebrafish models offer a new perspective on Mtb research due to their similarity to human symptoms and mechanisms. Zebrafish models have been crucial in understanding immune responses, drug efficacy, and initial pathogenicity to bridge the gap between small and large mammalian models. The zebrafish model has shown promising approach in understanding Mtb's intracellular pathogenicity, impaired lysosome functioning and macrophage survival strategies. This model has the potential to overcome the limitations of other animal models, providing an essential resource for tuberculosis research.
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Alu, A., Han, X., Ma, X., Wu, M., Wei, Y., & Wei, X. (2020). The role of lysosome in regulated necrosis. Acta Pharmaceutica Sinica. B, 10(10), 1880–1903. https://doi.org/10.1016/j.apsb.2020.07.003
Berg, R. D., Levitte, S., O’Sullivan, M. P., O’Leary, S. M., Cambier, C. J., Cameron, J., Takaki, K. K., Moens, C. B., Tobin, D. M., Keane, J., & Ramakrishnan, L. (2016). Lysosomal Disorders Drive Susceptibility to Tuberculosis by Compromising Macrophage Migration. Cell, 165(1), 139–152. https://doi.org/10.1016/j.cell.2016.02.034
Cambier, C. J., O’Leary, S. M., O’Sullivan, M. P., Keane, J., & Ramakrishnan, L. (2017). Phenolic Glycolipid Facilitates Mycobacterial Escape from Microbicidal Tissue-Resident Macrophages. Immunity, 47(3), 552-565.e4. https://doi.org/10.1016/j.immuni.2017.08.003
Cooper, A. M. (2015). Mouse Model of Tuberculosis. Cold Spring Harbor Perspectives in Medicine, 5(2), a018556. https://doi.org/10.1101/cshperspect.a018556
Dannenberg, A. M. (2001). Pathogenesis of pulmonary Mycobacterium bovis infection: Basic principles established by the rabbit model. Tuberculosis, 81(1), 87–96. https://doi.org/10.1054/tube.2000.0260
Dannenberg, A. M. (2009). Liquefaction and cavity formation in pulmonary TB: A simple method in rabbit skin to test inhibitors. Tuberculosis, 89(4), 243–247. https://doi.org/10.1016/j.tube.2009.05.006
Dharmadhikari, A. S., & Nardell, E. A. (2008). What Animal Models Teach Humans about Tuberculosis. American Journal of Respiratory Cell and Molecular Biology, 39(5), 503–508. https://doi.org/10.1165/rcmb.2008-0154TR
Enriquez, J., Mims, B. M. D., Trasti, S., Furr, K. L., & Grisham, M. B. (2020). Genomic, microbial and environmental standardization in animal experimentation limiting immunological discovery. BMC Immunology, 21, 50. https://doi.org/10.1186/s12865-020-00380-x
Flynn, J. L., Capuano, S. V., Croix, D., Pawar, S., Myers, A., Zinovik, A., & Klein, E. (2003). Non-human primates: A model for tuberculosis research. Tuberculosis, 83(1), 116–118. https://doi.org/10.1016/S1472-9792(02)00059-8
Gong, W., Liang, Y., & Wu, X. (2020). Animal Models of Tuberculosis Vaccine Research: An Important Component in the Fight against Tuberculosis. BioMed Research International, 2020, e4263079. https://doi.org/10.1155/2020/4263079
Gouveia, A. C. C., Brugiolo, A. S. S., Alves, C. C. S., Silva, F. M. C., Mesquita, F. P., Gameiro, J., & Ferreira, A. P. (2013). Th2 Responses in OVA-Sensitized BALB/c Mice Are Down-Modulated by Mycobacterium bovis BCG Treatment. Journal of Clinical Immunology, 33(1), 235–245. https://doi.org/10.1007/s10875-012-9746-4
Gs, P., Ee, S., Ca, S., Dj, O., Im, O., & Rj, B. (2008). Disseminated disease severity as a measure of virulence of Mycobacterium tuberculosis in the guinea pig model. Tuberculosis (Edinburgh, Scotland), 88(4). https://doi.org/10.1016/j.tube.2007.12.003
Leung-Theung-Long, S., Gouanvic, M., Coupet, C.-A., Ray, A., Tupin, E., Silvestre, N., Marchand, J.-B., Schmitt, D., Hoffmann, C., Klein, M., Seegren, P., Huaman, M. C., Cristillo, A. D., & Inchauspé, G. (2015). A Novel MVA-Based Multiphasic Vaccine for Prevention or Treatment of Tuberculosis Induces Broad and Multifunctional Cell-Mediated Immunity in Mice and Primates. PLOS ONE, 10(11), e0143552. https://doi.org/10.1371/journal.pone.0143552
Levitte, S., Adams, K. N., Berg, R. D., Cosma, C. L., Urdahl, K. B., & Ramakrishnan, L. (2016). Mycobacterial Acid Tolerance Enables Phagolysosomal Survival and Establishment of Tuberculous Infection In Vivo. Cell Host & Microbe, 20(2), 250–258. https://doi.org/10.1016/j.chom.2016.07.007
Li, H., & Li, H. (2023). Animal Models of Tuberculosis. In M. Christodoulides (Ed.), Vaccines for Neglected Pathogens: Strategies, Achievements and Challenges: Focus on Leprosy, Leishmaniasis, Melioidosis and Tuberculosis (pp. 139–170). Springer International Publishing. https://doi.org/10.1007/978-3-031-24355-4_7
Mantilla Galindo, A., Ocampo, M., & Patarroyo, M. A. (2019). Experimental models used in evaluating anti-tuberculosis vaccines: The latest advances in the field. Expert Review of Vaccines, 18(4), 365–377. https://doi.org/10.1080/14760584.2019.1583558
Martinot, A. J. (2018). Microbial Offense vs Host Defense: Who Controls the TB Granuloma? Veterinary Pathology, 55(1), 14–26. https://doi.org/10.1177/0300985817705177
Myllymäki, H., Niskanen, M., Oksanen, K. E., & Rämet, M. (2015). Animal models in tuberculosis research – where is the beef? Expert Opinion on Drug Discovery, 10(8), 871–883. https://doi.org/10.1517/17460441.2015.1049529
Myllymäki, H., Niskanen, M., Oksanen, K. E., Sherwood, E., Ahava, M., Parikka, M., & Rämet, M. (2017). Identification of novel antigen candidates for a tuberculosis vaccine in the adult zebrafish (Danio rerio). PLOS ONE, 12(7), e0181942. https://doi.org/10.1371/journal.pone.0181942
Namvarpour, M., Tebianian, M., Mansouri, R., Ebrahimi, S. M., & Kashkooli, S. (2019). Comparison of different immunization routes on the immune responses induced by Mycobacterium tuberculosis ESAT-6/CFP-10 recombinant protein. Biologicals, 59, 6–11. https://doi.org/10.1016/j.biologicals.2019.04.002
Oksanen, K. E., Halfpenny, N. J. A., Sherwood, E., Harjula, S.-K. E., Hammarén, M. M., Ahava, M. J., Pajula, E. T., Lahtinen, M. J., Parikka, M., & Rämet, M. (2013). An adult zebrafish model for preclinical tuberculosis vaccine development. Vaccine, 31(45), 5202–5209. https://doi.org/10.1016/j.vaccine.2013.08.093
Oksanen, K. E., Myllymäki, H., Ahava, M. J., Mäkinen, L., Parikka, M., & Rämet, M. (2016). DNA vaccination boosts Bacillus Calmette–Guérin protection against mycobacterial infection in zebrafish. Developmental & Comparative Immunology, 54(1), 89–96. https://doi.org/10.1016/j.dci.2015.09.001
Osman, M. M., Pagán, A. J., Shanahan, J. K., & Ramakrishnan, L. (2020). Mycobacterium marinum phthiocerol dimycocerosates enhance macrophage phagosomal permeabilization and membrane damage. PLOS ONE, 15(7), e0233252. https://doi.org/10.1371/journal.pone.0233252
Park, J.-H., Shim, D., Kim, K. E. S., Lee, W., & Shin, S. J. (2021). Understanding Metabolic Regulation Between Host and Pathogens: New Opportunities for the Development of Improved Therapeutic Strategies Against Mycobacterium Tuberculosis Infection. Frontiers in Cellular and Infection Microbiology, 11. https://www.frontiersin.org/-articles/10.3389/fcimb.2021.635335
Ramakrishnan, L. (2020). Mycobacterium tuberculosis pathogenicity viewed through the lens of molecular Koch’s postulates. Current Opinion in Microbiology, 54, 103–110. https://doi.org/10.1016/j.mib.2020.01.011
Roca, F. J., Whitworth, L. J., Redmond, S., Jones, A. A., & Ramakrishnan, L. (2019). TNF Induces Pathogenic Programmed Macrophage Necrosis in Tuberculosis through a Mitochondrial-Lysosomal-Endoplasmic Reticulum Circuit. Cell, 178(6), 1344-1361.e11. https://doi.org/10.1016/j.cell.2019.08.004
Seung, K. J., Keshavjee, S., & Rich, M. L. (2015). Multidrug-Resistant Tuberculosis and Extensively Drug-Resistant Tuberculosis. Cold Spring Harbor Perspectives in Medicine, 5(9), a017863. https://doi.org/10.1101/cshperspect.a017863
Singh, A. K., & Gupta, U. D. (2018). Animal models of tuberculosis: Lesson learnt. The Indian Journal of Medical Research, 147(5), 456–463. https://doi.org/10.4103/-ijmr.IJMR_554_18
Tran, V., Ahn, S. K., Ng, M., Li, M., & Liu, J. (2016). Loss of Lipid Virulence Factors Reduces the Efficacy of the BCG Vaccine. Scientific Reports, 6(1), Article 1. https://doi.org/10.1038/srep29076
Traver, D., Herbomel, P., Patton, E. E., Murphey, R. D., Yoder, J. A., Litman, G. W., Catic, A., Amemiya, C. T., Zon, L. I., & Trede, N. S. (2003). The zebrafish as a model organism to study development of the immune system. Advances in Immunology, 81, 253–330.
Yang, J., Zhang, L., Qiao, W., & Luo, Y. (2023). Mycobacterium tuberculosis: Pathogenesis and therapeutic targets. MedComm, 4(5), e353. https://doi.org/10.1002/mco2.353
Zhan, L., Tang, J., Sun, M., & Qin, C. (2017). Animal Models for Tuberculosis in Translational and Precision Medicine. Frontiers in Microbiology, 8, 717. https://doi.org/10.3389/fmicb.2017.00717