Advances in the application of animal models and 3D cell models in tuberculosis research

doi:10.19982/j.issn.1000-6621.20240347

Abstract

Abstract:

Tuberculosis, caused by Mycobacterium tuberculosis (MTB), remains one of the world’s most significant infectious diseases, yet the mechanisms underlying MTB-host interactions are not fully understood. Animal models and 3D cell models offer a comprehensive and intricate experimental platform that facilitates the simulation of various aspects of tuberculosis pathophysiology. This review examines the application of these models in tuberculosis research, aiming to pave the way for advances in prevention, diagnosis, and treatment.

Key words: Tuberculosis, Disease models, animal, Review literature as topic

CLC Number:

R52
R378

Li Chaofan, Chen Zhi. Advances in the application of animal models and 3D cell models in tuberculosis research[J]. Chinese Journal of Antituberculosis, 2024, 46(12): 1527-1534. doi: 10.19982/j.issn.1000-6621.20240347

References 60

[1]	World Health Organization. Global tuberculosis report 2024. Geneva: World Health Organization, 2024.
[2]	Sankar P, Mishra BB. Early innate cell interactions with Mycobacterium tuberculosis in protection and pathology of tuberculosis. Front Immunol, 2023, 14: 1260859. doi:10.3389/fimmu.2023.1260859.
[3]	Chai Q, Lu Z, Liu CH. Host defense mechanisms against Mycobacterium tuberculosis. Cell Mol Life Sci, 2020, 77(10): 1859-1878. doi:10.1007/s00018-019-03353-5.
[4]	Fonseca KL, Rodrigues PNS, Olsson IAS, et al. Experimental study of tuberculosis: From animal models to complex cell systems and organoids. PLoS Pathog, 2017, 13(8): e1006421. doi:10.1371/journal.ppat.1006421.
[5]	Gong W, Liang Y, Wu X. Animal Models of Tuberculosis Vaccine Research: An Important Component in the Fight against Tuberculosis. Biomed Res Int, 2020, 2020: 4263079. doi:10.1155/2020/4263079.
[6]	Smith CM, Baker RE, Proulx MK, et al. Host-pathogen genetic interactions underlie tuberculosis susceptibility in genetically diverse mice. Elife, 2022, 11: e74419. doi:10.7554/eLife.74419.
[7]	Perlman RL. Mouse models of human disease: An evolutionary perspective. Evol Med Public Health, 2016, 2016(1): 170-176. doi:10.1093/emph/eow014.
[8]	朱婷婷, 王明哲, 刘万里. MTB感染小鼠动物模型的建立及研究现状. 疾病预防控制通报, 2024, 39(3):93-96. doi:10.13215/j.cnki.jbyfkztb.2401007.
[9]	Jia Q, Masleša-Galic'S, Nava S, et al. Listeria-vectored multi-antigenic tuberculosis vaccine protects C57BL/6 and BALB/c mice and guinea pigs against Mycobacterium tuberculosis challenge. Commun Biol, 2022, 5(1): 1388. doi:10.1038/s42003-022-04345-1.
[10]	Singh AK, Gupta UD. Animal models of tuberculosis: Lesson learnt. Indian J Med Res, 2018, 147(5): 456-463. doi:10.4103/ijmr.IJMR_554_18. pmid: 30082569
[11]	Plumlee CR, Duffy FJ, Gern BH, et al. Ultra-low Dose Aerosol Infection of Mice with Mycobacterium tuberculosis More Closely Models Human Tuberculosis. Cell Host Microbe, 2021, 29(1): 68-82. e5. doi:10.1016/j.chom.2020.10.003.
[12]	Plumlee CR, Barrett HW, Shao DE, et al. Assessing vaccine-mediated protection in an ultra-low dose Mycobacterium tuberculosis murine model. PLoS Pathog, 2023, 19(11): e1011825. doi:10.1371/journal.ppat.1011825.
[13]	Soldevilla P, Vilaplana C, Cardona PJ. Mouse Models for Mycobacterium tuberculosis Pathogenesis: Show and Do Not Tell. Pathogens, 2022, 12(1): 49. doi:10.3390/pathogens12010049.
[14]	Seto S, Nakamura H, Guo TC, et al. Spatial multiomic profiling reveals the novel polarization of foamy macrophages within necrotic granulomatous lesions developed in lungs of C3HeB/FeJ mice infected with Mycobacterium tuberculosis. Front Cell Infect Microbiol, 2022, 12: 968543. doi:10.3389/fcimb.2022.968543.
[15]	Ramey ME, Kaya F, Bauman AA, et al. Drug distribution and efficacy of the DprE 1 inhibitor BTZ-043 in the C3HeB/FeJ mouse tuberculosis model. Antimicrob Agents Chemother, 2023, 67(11):e0059723. doi:10.1128/aac.00597-23.
[16]	Nandi B, Behar SM. Regulation of neutrophils by interferon-γ limits lung inflammation during tuberculosis infection. J Exp Med, 2011, 208(11): 2251-2262. doi:10.1084/jem.20110919.
[17]	Allie N, Grivennikov SI, Keeton R, et al. Prominent role for T cell-derived tumour necrosis factor for sustained control of Mycobacterium tuberculosis infection. Sci Rep, 2013, 3: 1809. doi:10.1038/srep01809.
[18]	Corleis B, Bastian M, Hoffmann D, et al. Animal models for COVID-19 and tuberculosis. Front Immunol, 2023, 14: 1223260. doi:10.3389/fimmu.2023.1223260.
[19]	Brendel C, Rio P, Verhoeyen E. Humanized mice are precious tools for evaluation of hematopoietic gene therapies and preclinical modeling to move towards a clinical trial. Biochem Pharmacol, 2020, 174: 113711. doi:10.1016/j.bcp.2019.113711.
[20]	Lepard M, Yang JX, Afkhami S, et al. Comparing Current and Next-Generation Humanized Mouse Models for Advancing HIV and HIV/Mtb Co-Infection Studies. Viruses, 2022, 14(9): 1927. doi:10.3390/v14091927.
[21]	Bohórquez JA, Adduri S, Ansari D, et al. A novel humanized mouse model for HIV and tuberculosis co-infection studies. Front Immunol, 2024, 15: 1395018. doi:10.3389/fimmu.2024.1395018.
[22]	Yang F, Labani-Motlagh A, Bohorquez JA, et al. Bacteriophage therapy for the treatment of Mycobacterium tuberculosis infections in humanized mice. Commun Biol, 2024, 7(1): 294. doi:10.1038/s42003-024-06006-x.
[23]	Sergeeva M, Romanovskaya-Romanko E, Zabolotnyh N, et al. Mucosal Influenza Vector Vaccine Carrying TB10.4 and HspX Antigens Provides Protection against Mycobacterium tuberculosis in Mice and Guinea Pigs. Vaccines (Basel), 2021, 9(4): 394. doi:10.3390/vaccines9040394.
[24]	Yang HJ, Wang D, Wen X, et al. One Size Fits All? Not in In Vivo Modeling of Tuberculosis Chemotherapeutics. Front Cell Infect Microbiol, 2021, 11: 613149. doi:10.3389/fcimb.2021.613149.
[25]	Eckhardt E, Li Y, Mamerow S, et al. Pharmacokinetics and Efficacy of the Benzothiazinone BTZ-043 against Tuberculous Mycobacteria inside Granulomas in the Guinea Pig Model. Antimicrob Agents Chemother, 2023, 67(4): e0143822. doi:10.1128/aac.01438-22.
[26]	Creissen E, Izzo L, Dawson C, et al. Guinea Pig Model of Mycobacterium tuberculosis Infection. Curr Protoc, 2021, 1(12): e312. doi:10.1002/cpz1.312.
[27]	Luo G, Zeng D, Liu J, et al. Temporal and cellular analysis of granuloma development in mycobacterial infected adult zebrafish. J Leukoc Biol, 2024, 115(3): 525-535. doi:10.1093/jleuko/qiad145.
[28]	Salina EG, Makarov V. Mycobacterium tuberculosis Dormancy: How to Fight a Hidden Danger. Microorganisms, 2022, 10(12): 2334. doi:10.3390/microorganisms10122334.
[29]	Cheng T, Kam JY, Johansen MD, et al. High content analysis of granuloma histology and neutrophilic inflammation in adult zebrafish infected with Mycobacterium marinum. Micron, 2020, 129: 102782. doi:10.1016/j.micron.2019.102782.
[30]	Gao Y, Li J, Guo X, et al. L-Tyrosine Limits Mycobacterial Survival in Tuberculous Granuloma. Pathogens, 2023, 12(5): 654. doi:10.3390/pathogens12050654.
[31]	Varela M, Meijer AH. A fresh look at mycobacterial pathogenicity with the zebrafish host model. Mol Microbiol, 2022, 117(3): 661-669. doi:10.1111/mmi.14838.
[32]	Muñoz-Sánchez S, Varela M, van der Vaart M, et al. Using Zebrafish to Dissect the Interaction of Mycobacteria with the Autophagic Machinery in Macrophages. Biology (Basel), 2023, 12(6): 817. doi:10.3390/biology12060817.
[33]	Basheer F, Sertori R, Liongue C, et al. Zebrafish: A Relevant Genetic Model for Human Primary Immunodeficiency (PID) Disorders?. Int J Mol Sci, 2023, 24(7): 6468. doi:10.3390/ijms24076468.
[34]	Saralahti AK, Uusi-Mäkelä MIE, Niskanen MT, et al. Integrating fish models in tuberculosis vaccine development. Dis Model Mech, 2020, 13(8): dmm045716. doi:10.1242/dmm.045716.
[35]	Bailone RL, Fukushima HCS, Ventura Fernandes BH, et al. Zebrafish as an alternative animal model in human and animal vaccination research. Lab Anim Res, 2020, 36: 13. doi:10.1186/s42826-020-00042-4. pmid: 32382525
[36]	Parikka M, Hammarén MM, Harjula SK, et al. Mycobacterium marinum causes a latent infection that can be reactivated by gamma irradiation in adult zebrafish. PLoS Pathog, 2012, 8(9): e1002944. doi:10.1371/journal.ppat.1002944.
[37]	Hunter L, Ruedas-Torres I, Agulló-Ros I, et al. Comparative pathology of experimental pulmonary tuberculosis in animal models. Front Vet Sci, 2023, 10: 1264833. doi:10.3389/fvets.2023.1264833.
[38]	涂振阳, 蓝常贡, 谢克恭, 等. 兔结核病模型的应用研究进展. 微生物学杂志, 2019, 39(6):102-108. doi:10.3969/j.issn.1005-7021.2019.06.014.
[39]	Hunter L, Hingley-Wilson S, Stewart GR, et al. Dynamics of Macrophage, T and B Cell Infiltration Within Pulmonary Granulomas Induced by Mycobacterium tuberculosis in Two Non-Human Primate Models of Aerosol Infection. Front Immunol, 2022, 12: 776913. doi:10.3389/fimmu.2021.776913.
[40]	Kauffman KD, Sakai S, Lora NE, et al. PD-1 blockade exacerbates Mycobacterium tuberculosis infection in rhesus macaques. Sci Immunol, 2021, 6(55): eabf3861. doi:10.1126/sciimmunol.abf3861.
[41]	Sibley L, Daykin-Pont O, Sarfas C, et al. Differences in host immune populations between rhesus macaques and cynomolgus macaque subspecies in relation to susceptibility to Mycobacterium tuberculosis infection. Sci Rep, 2021, 11(1): 8810. doi:10.1038/s41598-021-87872-x.
[42]	PLOS ONE Staff. Correction: reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load. PLoS One, 2015, 10(4): e0124221. doi:10.1371/journal.pone.0124221.
[43]	Larson EC, Ellis-Connell A, Rodgers MA, et al. Pre-existing Simian Immunodeficiency Virus Infection Increases Expression of T Cell Markers Associated with Activation during Early Mycobacterium tuberculosis Coinfection and Impairs TNF Responses in Granulomas. J Immunol, 2021, 207(1): 175-188. doi:10.4049/jimmunol.2100073. pmid: 34145063
[44]	马嘉烨, 徐进川, 晏博, 等. 结核潜伏感染动物模型的研究进展. 微生物与感染, 2021, 16(5): 363-372. doi:10.3969/j.issn.1673-6184.2021.05.011.
[45]	郭佳俊, 邱燕, 胡璨, 等. 3D结核球模型的构建及特性验证:基于人髓系THP-1细胞与卡介苗. 南方医科大学学报, 2023, 43(12):2095-2102. doi:10.12122/j.issn.1673-4254.2023.12.14.
[46]	Mukundan S, Singh P, Shah A, et al. In Vitro Miniaturized Tuberculosis Spheroid Model. Biomedicines, 2021, 9(9): 1209. doi:10.3390/biomedicines9091209.
[47]	Bielecka MK, Tezera LB, Zmijan R, et al. A Bioengineered Three-Dimensional Cell Culture Platform Integrated with Microfluidics To Address Antimicrobial Resistance in Tuberculosis. mBio, 2017, 8(1): e02073-16. doi:10.1128/mBio.02073-16.
[48]	Demchenko A, Lavrov A, Smirnikhina S. Lung organoids: current strategies for generation and transplantation. Cell Tissue Res, 2022, 390(3): 317-333. doi:10.1007/s00441-022-03686-x. pmid: 36178558
[49]	Hughes T, Dijkstra KK, Rawlins EL, et al. Open questions in human lung organoid research. Front Pharmacol, 2023, 13: 1083017. doi:10.3389/fphar.2022.1083017.
[50]	Ettayebi K, Crawford SE, Murakami K, et al. Replication of human noroviruses in stem cell-derived human enteroids. Science, 2016, 353(6306): 1387-1393. doi:10.1126/science.aaf5211. pmid: 27562956
[51]	Estes MK, Ettayebi K, Tenge VR, et al. Human Norovirus Cultivation in Nontransformed Stem Cell-Derived Human Intestinal Enteroid Cultures: Success and Challenges. Viruses, 2019, 11(7): 638. doi:10.3390/v11070638.
[52]	Kühl L, Graichen P, von Daacke N, et al. Human Lung Organoids-A Novel Experimental and Precision Medicine Approach. Cells, 2023, 12(16): 2067. doi:10.3390/cells12162067.
[53]	Iakobachvili N, Leon-Icaza SA, Knoops K, et al. Mycobacteria-host interactions in human bronchiolar airway organoids. Mol Microbiol, 2022, 117(3): 682-692. doi:10.1111/mmi.14824.
[54]	Evans KV, Lee JH. Alveolar wars: The rise of in vitro models to understand human lung alveolar maintenance, regeneration, and disease. Stem Cells Transl Med, 2020, 9(8): 867-881. doi:10.1002/sctm.19-0433.
[55]	Corrò C, Novellasdemunt L, Li VSW. A brief history of organoids. Am J Physiol Cell Physiol, 2020, 319(1): C151-C165. doi:10.1152/ajpcell.00120.2020.
[56]	Lu T, Cao Y, Zhao P, et al. Organoid: a powerful tool to study lung regeneration and disease. Cell Regen, 2021, 10(1): 21. doi:10.1186/s13619-021-00082-8.
[57]	朱国峰, 刘晓清. 结核病比较免疫学时代的机遇和挑战. 结核与肺部疾病杂志, 2020, 1(4):195-212. doi:10.3969/j.issn.2096-8493.2020.03.002.
[58]	Basaraba RJ, Hunter RL. Pathology of Tuberculosis: How the Pathology of Human Tuberculosis Informs and Directs Animal Models. Microbiol Spectr, 2017, 5(3). doi:10.1128/microbiolspec.TBTB2-0029-2016.
[59]	钟鹏飞, 保鹏涛, 檀英霞. 人肺类器官用于肺结核病研究进展及前景. 中国药理学与毒理学杂志, 2022, 36(8):612-618. doi:10.3867/j.issn.1000-3002.2022.08.008.
[60]	Novelli G, Spitalieri P, Murdocca M, et al. Organoid factory: The recent role of the human induced pluripotent stem cells (hiPSCs) in precision medicine. Front Cell Dev Biol, 2023, 10: 1059579. doi:10.3389/fcell.2022.1059579.