2020, Number 2
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VacciMonitor 2020; 29 (2)
Mycobacterium tuberculosis genes and virulence determinants that contribute to the immune response evasion
Méndez-López MV
Language: Spanish
References: 56
Page: 83-92
PDF size: 558.63 Kb.
ABSTRACT
Pulmonary tuberculosis is a public health problem worldwide. The World Health Organization in 2018 reported about 10 million patients and 1.5 million deaths. Mycobacterium tuberculosis, an intracellular pathogen, is the causative agent of the disease. Experimental virulence studies have allowed to determine a set of virulence genes that confer the ability to resist the hostile environment in the macrophage, overcome the activity of the immune response and persist in the host. The objective of the publication is to present a review of the last 20 years investigations that have shown the genes or virulence factors of M. tuberculosis that contribute to the evasion of the immune response. According to the results of the investigations, there are multiple virulence factors and genes that participate in the evasion of the innate immune response such as ESAT-6, PknG, PhoP, ManLAM, SapM, katG, tpx, nuoG, sodA/secA2, pknE and Rv3654c/Rv3655c, while there are elements capable of modulating the adaptive immune response. The understanding of the interaction between the virulence genes and the activity of the immune system, are important to study new diagnostic methods, the design of new vaccines and therefore, to improve the control, prevention and treatment measures of tuberculosis.
REFERENCES
Organización Mundial de la Salud [Internet]. Ginebra: OMS; 2019. Centro de Prensa. Noticias descriptivas. Tuberculosis. Disponible en: https://www.who.int/es/news-room/fact-sheets/detail/tuberculosis (Actualizado: 17 de octubre de 2019; Consultado en línea: 18 de octubre de 2019).
Bańuls AL, Sanou A, Van-Ah N, Godreuil S. Mycobacterium tuberculosis: Ecology and evolution of a human bacterium. J of Med Microbiol. 2015;64:1261-9.
Knechel NA. Tuberculosis: Pathophysiology, clinical features, and diagnosis. Crit Care Nurse. 2009;29:34-43.
Van Cravel R, Ottenhoff THM, van der Meer JWM. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev. 2002;15:294-309.
Smith I. Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev. 2003;16:463-96.
Prozorov A, Fedorova I, Bekker B, Danilenko B. The virulence factors of Mycobacterium tuberculosis: Genetic control, new conceptions. Rus J Gen. 2014;50:775-97.
Voss G, Casimiro D, Neyrolles O, Williams A, Kaufmann S, McShane H, et al. Progress and challenges in TB vaccine development. F1000Res. 2018;7:199. doi:10.12688/ f1000research.13588.1 (Consultado en línea: 15 de Mayo del 2019).
Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998;393:537-44.
de Martino M, Lodi L, Galli L, Chiappini E. Immune Responses to Mycobacterium tuberculosis. A narrative Review. Front Pediatr. 2019;7:350-57. doi:10.3389/fped.2019.00350. (Consultado en línea: 15 de Enero del 2020).
Venketaraman V, Dayaram Y, Amin A, Ngo R, Green R, Talaue M, et al. Role of Glutathione in Macrophage Control of Mycobacteria. Infect Immun. 2003;71:1864-71.
Ciu-Huag L, Haiying L, Baoxue G. Innate immunity in tuberculosis: host defense vs pathogen evasion. Cell Mol Immunol. 2017;14:963-75.
Lerner TR, Borel S, Gutierrez MG. The innate immune response in human tuberculosis. Cell Microbiol. 2015;17:1277-85. doi: 10.1111/cmi.12480 (Consultado en línea: 28 de Julio del 2019).
Maertzdorf J, Tönnies M, Lozza L, Schommer-Leitner S, Mollenkopf H, Torsten T, et al. Mycobacterium tuberculosis invasion of the human lung: First contact. Front. Immunol. 2018;9:1346-57. doi: 10.3389/fimmu.2018.01346 (Consultado en línea: 28 de Julio del 2019).
Borrero R, Álvarez N, Reyes F, Sarmiento ME, Acosta A. Mycobacterium tuberculosis: factores de virulencia. VacciMonitor. 2011;20(1):34-8. Disponible en: http://scielo.sld.cu/pdf/vac/v20n1/vac06111.pdf (Consultado en línea: 25 de Julio del 2019).
Armstrong JA, Hart PD. Response of cultured macrophages to Mycobacterium tuberculosis with observations on fusion of lysosomes with phagosomes. J Exp Med. 1971;134:713-40.
Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med. 2005;202:987-99.
Shukla S, Richardson ET, Athman JJ, Shi L, Wearsch PA, McDonald D, et al. Mycobacterium tuberculosis Lipoprotein LprG Binds Lipoarabinomannan and Determines Its Cell Envelope Localization to Control Phagolysosomal Fusion. PLoS Pathog. 2014;10(10):e1004471. doi:10.1371/journal.ppat.1004471 (Consultado en línea: 25 de Julio del 2019).
Walburger A, Koul A, Ferrari G, Nguyen L, Prescianotto-Baschong C, Huygen K, et al. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science. 2004;304:1800-04.
Sullivan J, Young E, McCann JR, Braunstein M. The Mycobacterium tuberculosis SecA2 System Subverts Phagosome Maturation to Promote Growth in Macrophages. Infect Immun. 2012;80:996-1006.
Zulauf E, Sullivan J, Braunstein M. The SecA2 pathway of Mycobacterium tuberculosis exports effectors that work in concert to arrest phagosome and autophagosome maturation. PLoS Pathog. 2018;14(4):e1007011. doi.org/10.1371/journal.ppat.1007011 (Consultado en línea: 15 de Enero del 2020).
Puri RV, Reddy PV, Tyagi AK. Secreted Acid Phosphatase (SapM) of Mycobacterium tuberculosis is Indispensable for Arresting Phagosomal Maturation and Growth of the Pathogen in Guinea Pig Tissues. PLoS ONE. 2013;8(7):e70514. doi:10.1371/journal.pone.0070514 (Consultado en línea: 15 de Enero del 2020).
Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 2012;8(2):e1002507. doi.org/10.1371/journal.ppat.1002507 (Consultado en línea: 10 de Mayo del 2019).
Augenstreich J, Arbues A, Simeone R, Haanappel E, Wegener A, Sayes F, et al. ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis. Cell Microbiol. 2017; 19(7):e12726. doi.org/10.1111/cmi.12726.
Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol. 1996;178:1274–82.
van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, et al. M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells. Cell. 2007;129:1287-98.
Pym A, Saint-Joanis B, Cole S. Effect of katG Mutations on the Virulence of Mycobacterium tuberculosis and the Implication for Transmission in Humans. Infect Immun. 2002;70:4955-60.
Weiss G, Schaible UE. Macrophage defense mechanisms against intracellular bacteria. Immunol Rev. 2015;264:182-203. doi:10.1111/imr.12266 (Consultado en línea: 10 de Diciembre del 2019).
Nieto LM, Mehaffy C, Creissen E, Troudt J, Troy A, Bielefeldt-Ohmann H, et al. Virulence of Mycobacterium tuberculosis after Acquisition of Isoniazid Resistance: Individual Nature of katG Mutants and the Possible Role of AhpC. PLoS ONE. 2016;11(11):e0166807. doi:10.1371/ journal.pone.0166807 (Consultado en línea: 10 de Febrero del 2020).
Hu Y, Coates AR. Acute and persistent Mycobacterium tuberculosis infections depend on the thiol peroxidase TpX. PLoS One. 2009;4(4):e5150. http://dx.doi.org/10.1371/journal.pone.0005150. (Consultado en línea: 2 de Mayo del 2019).
Goyal R, Das AK, Singh R, Singh PK, Korpole S, Sarkar D. Phosphorylation of PhoP protein plays direct regulatory role in lipid biosynthesis of Mycobacterium tuberculosis. J Biol Chem. 2011;286:45197-208. doi:10.1074/jbc.M111.307447 (Consultado en línea: 15 de Julio del 2019).
Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, Smith I. The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol. 2006;60:312-30.
Gonzalo-Asensio J, Mostowy S, Harders-Westerveen J, Huygen K, Hernández-Pando R, Thole J, et al. PhoP: a missing piece in the intricate puzzle of Mycobacterium tuberculosis virulence. PLoS ONE. 2008;3(10):e3496. doi: 10.1371/journal.pone.0003496 (Consultado en línea: 4 de Julio del 2019).
Singh A, Crossman DK, Mai D, Guidry L, Voskuil MI, Renfrow MB, et al. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 2009;5(8):e1000545. doi: 10.1371/journal.ppat.1000545 (Consultado en línea: 30 de abril de 2019)
Sharp JD, Singh AK, Park ST, Lyubetskaya A, Peterson MW, Gomes AL, et al. Comprehensive Definition of the SigH Regulon of Mycobacterium tuberculosis Reveals Transcriptional Control of Diverse Stress Responses. PLoS ONE. 2016;11(3):e0152145. doi: 10.1371/journal.pone.0152145 (Consultado en línea: 10 de Diciembre del 2019).
Cowley S, Ko M, Pick N, Chow R, Downing KJ, Gordhan BG, et al. The Mycobacterium tuberculosis protein serine/threonine kinase PknG is linked to cellular glutamate/glutamine levels and is important for growth in vivo. Mol Microbiol. 2004;52:1691-702
Mehak K, Ashima B, Sandeep U, Pooja K, Raju R, Preeti J, et al. Protein kinase G confers survival advantage to Mycobacterium tuberculosis during latency-like conditions. J Biol Chem. 2017;292:16093-108.
Riendeau CJ, Kornfeld H. THP-1 cell apoptosis in response to Mycobacterial infection. Infect Immun. 2003;71:254-59.
Danelishvili L, Yamazaki Y, Selker J, Bermudez LE. Secreted Mycobacterium tuberculosis Rv3654c and Rv3655c proteins participate in the suppression of macrophage apoptosis. PLoS ONE. 2010;5(5):e10474. doi:10.1371/journal.pone.0010474 (Consultado en línea: 5 de Mayo del 2019).
Miller JL, Velmurugan K, Cowan MJ, Briken V. The type I NADH dehydrogenase of Mycobacterium tuberculosis counters phagosomal NOX2 activity to inhibit TNF-alpha-mediated host cell apoptosis. PLoS Pathog. 2010;6(4):e1000864. doi: 10.1371/journal.ppat.1000864 (Consultado en línea: 5 de Mayo del 2019).
Simone C. Signal-dependent control of autophagy and cell death in colorectal cancer cell: the role of the p38 pathway. Autophagy. 2007;3:468-71.
Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy. 2012;8:1357-70.
Chandra P, Ghanwat S, Matta SK, Swati S, Mansi M, Siddiqui Z, et al. Mycobacterium tuberculosis inhibits RAB7 recruitment to selectively modulate autophagy flux in macrophages. Sci Rep. 2015;5:16320. doi: 10.1038/srep16320 (Consultado en línea: 2 de Abril del 2019).
Shui W, Petzold CJ, Redding A, Liu J, Pitcher A, Sheu L, et al. Organelle membrane proteomics reveals differential influence of mycobacterial lipoglycans on macrophage phagosome maturation and autophagosome accumulation. J Proteome Res. 2011;10:339-48.
Saini NK, Baena A, Ng TW, Venkataswamy MM, Kennedy SC, Kunnath-Velayudhan S, et al. Suppression of autophagy and antigen presentation by Mycobacterium tuberculosis PE˙PGRS47. Nat Microbiol. 2016;1:16133. doi: 10.1038/nmicrobiol.2016.133 (Consultado en línea: 10 de Marzo del 2019).
Shin DM, Jeon BY, Lee HM, Jin HS, Yuk JM, Song CH, et al. Mycobacterium tuberculosis Eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog. 2010;6(12):e1001230. doi.org/10.1371/journal.ppat.1001230 (Consultado en línea: 3 de Abril del 2019).
Dao D, Kremer L, Rardel G, Molano A, Jacobs R, Porcelli SA, et al. Mycobacterium tuberculosis Lipomannan Induces Apoptosis and Interleukin-12 Production in Macrophages. Infect Immun. 2004;72:2067-74.
Pai R, Convery M, Hamilton TA, Boom WH, Harding CV. Inhibition of IFN-gamma induced class II transactivator expression by a 19 kDa lipoprotein from Mycobacterium tuberculosis: A potential mechanism for immune evasion. J Immunol. 2003;171:175-84.
Källenius G, Correia-Neves M, Buteme H, Hamasur B, Svenson SB. Lipoarabinomannan, and its related glycolipids, induce divergent and opposing immune responses to Mycobacterium tuberculosis depending on structural diversity and experimental variations. Tuberculosis. 2016;96:120-30.
Rojas M, García LF, Nigou J, Puzo G, Olivier M. Mannosylated lipoarabinomannan antagonize Mycobacterium tuberculosis-induced macrophage apoptosis by altering Ca+2-dependent cell signaling. J Infect Dis. 2000;182:240-51.
Herrera M, Torres M, Juarez E, Sada E. Mecanismos Moleculares de Respuesta inmune en la tuberculosis Pulmonar Humana. Rev Inst Nal Enf Resp Mex. 2005;18(4):327-36.
Portal-Celhay C, Tufariello JM, Srivastava S, Zhara A, Klevorn T, Grace PS, et al. Mycobacterium tuberculosis EsxH inhibits ESCRT-dependent CD4+ T-cell activation. Nat Microbiol. 2016;2:16232. doi: 10.1038/nmicrobiol.2016.232 (Consultado en línea: 10 de Enero del 2020).
Meng L, Tong J, Wang H, Tao Ch, Wang Q, Niu Ch, et al. PPE38 Protein of Mycobacterium tuberculosis Inhibits Macrophage MHC Class I Expression and Dampens CD8+ T Cell Responses. Front Cell Infect Microbiol. 2017;7:68. doi:10.3389/fcimb.2017.00068.14. (Consultado en línea: 10 de Enero del 2020).
Assis P, Espindola M, Paula-Silva F, Rios W, Pereira P, Leao S, et al. Mycobacterium tuberculosis expressing phospholipase C subverts PGE2 synthesis and induces necrosis in alveolar macrophages. BMC Microbiol. 2014;14:128. doi: 10.1186/1471-2180-14-128 (Consultado: 16 de Febrero del 2019).
Danelishvili L, Everman JL, Bermudez LE. Mycobacterium tuberculosis PPE68 and Rv2626c genes contribute to the host cell necrosis and bacterial escape from macrophages. Virulence. 2016; 7(1):23-32. doi: 10.1080/21505594.2015.1102832 (Consultado en línea: 3 de Marzo del 2019).
Houben D, Demangel C, van Ingen J, Perez J, Baldeon L, Abdallah AM, et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol. 2012;14(8):1287-98. doi:10.1111/j.1462-5822.2012.01799.x (Consultado en línea: 3 de Marzo del 2019).
Dallenga T, Repnik U, Corleis B, Eich J, Reimer R, Gareth W, et al. M. tuberculosis-Induced Necrosis of Infected Neutrophils Promotes Bacterial Growth Following Phagocytosis by Macrophages. Cell Host Microbe. 2017;22(4):519-30. doi: 10.1016/j.chom.2017.09.003 (Consultado en línea: 3 de Mayo del 2019).