260
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Attenuated Cytokine-Induced Memory-Like Natural Killer Cell Responses to Mycobacterium tuberculosis in Tuberculosis Patients

, ORCID Icon, , , , , ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 2349-2364 | Received 28 Feb 2023, Accepted 15 Apr 2023, Published online: 20 Apr 2023

References

  • World Health Organization. Global Tuberculosis Report 2022. Geneva: World Health Organization; 2022.
  • Shi YH, Zhu SW, Mao XZ, et al. Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell. 2006;18(3):651–664. doi:10.1105/tpc.105.040303
  • Harding E. WHO global progress report on tuberculosis elimination. Lancet Respir Med. 2020;8(1):19. doi:10.1016/S2213-2600(19)30418-7
  • Russell DG, VanderVen BC, Lee W, et al. Mycobacterium tuberculosis wears what it eats. Cell Host Microbe. 2010;8(1):68–76. doi:10.1016/j.chom.2010.06.002
  • Shah M, Dorman SE. Latent tuberculosis infection. N Engl J Med. 2021;385(24):2271–2280. doi:10.1056/NEJMcp2108501
  • Gengenbacher M, Kaufmann SH. Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev. 2012;36(3):514–532. doi:10.1111/j.1574-6976.2012.00331.x
  • Liu CH, Liu H, Ge B. Innate immunity in tuberculosis: host defense vs pathogen evasion. Cell Mol Immunol. 2017;14(12):963–975. doi:10.1038/cmi.2017.88
  • Maroof A, Beattie L, Zubairi S, Svensson M, Stager S, Kaye PM. Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity. 2008;29(2):295–305. doi:10.1016/j.immuni.2008.06.012
  • Bozzano F, Costa P, Passalacqua G, et al. Functionally relevant decreases in activatory receptor expression on NK cells are associated with pulmonary tuberculosis in vivo and persist after successful treatment. Int Immunol. 2009;21(7):779–791. doi:10.1093/intimm/dxp046
  • Ratcliffe LT, Lukey PT, MacKenzie CR, Ress SR. Reduced NK activity correlates with active disease in HIV- patients with multidrug-resistant pulmonary tuberculosis. Clin Exp Immunol. 1994;97(3):373–379. doi:10.1111/j.1365-2249.1994.tb06097.x
  • Esin S, Batoni G. Natural killer cells: a coherent model for their functional role in Mycobacterium tuberculosis infection. J Innate Immun. 2015;7(1):11–24. doi:10.1159/000363321
  • Lodoen MB, Lanier LL. Natural killer cells as an initial defense against pathogens. Curr Opin Immunol. 2006;18(4):391–398. doi:10.1016/j.coi.2006.05.002
  • Erkes DA, Selvan SR. Hapten-induced contact hypersensitivity, autoimmune reactions, and tumor regression: plausibility of mediating antitumor immunity. J Immunol Res. 2014;2014:175265. doi:10.1155/2014/175265
  • Terren I, Orrantia A, Astarloa-Pando G, Amarilla-Irusta A, Zenarruzabeitia O, Borrego F. Cytokine-induced memory-like NK cells: from the basics to clinical applications. Front Immunol. 2022;13:884648. doi:10.3389/fimmu.2022.884648
  • Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457(7229):557–561. doi:10.1038/nature07665
  • Abdul-Careem MF, Lee AJ, Pek EA, et al. Genital HSV-2 infection induces short-term NK cell memory. PLoS One. 2012;7(3):e32821. doi:10.1371/journal.pone.0032821
  • Paust S, Gill HS, Wang BZ, et al. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol. 2010;11(12):1127–1135. doi:10.1038/ni.1953
  • Reeves RK, Li H, Jost S, et al. Antigen-specific NK cell memory in rhesus macaques. Nat Immunol. 2015;16(9):927–932. doi:10.1038/ni.3227
  • Habib S, El Andaloussi A, Hisham A, Ismail N, Cell-Mediated NK. Regulation of protective memory responses against intracellular ehrlichial pathogens. PLoS One. 2016;11(4):e0153223. doi:10.1371/journal.pone.0153223
  • Choreno Parra JA, Martinez Zuniga N, Jimenez Zamudio LA, Jimenez Alvarez LA, Salinas Lara C, Zuniga J. Memory of natural killer cells: a new chance against mycobacterium tuberculosis? Front Immunol. 2017;8:967. doi:10.3389/fimmu.2017.00967
  • Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM. Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci U S A. 2009;106(6):1915–1919. doi:10.1073/pnas.0813192106
  • Gang M, Wong P, Berrien-Elliott MM, Fehniger TA. Memory-like natural killer cells for cancer immunotherapy. Semin Hematol. 2020;57(4):185–193. doi:10.1053/j.seminhematol.2020.11.003
  • Braverman J, Sogi KM, Benjamin D, Nomura DK, Stanley SA. HIF-1alpha is an essential mediator of IFN-gamma-dependent immunity to mycobacterium tuberculosis. J Immunol. 2016;197(4):1287–1297. doi:10.4049/jimmunol.1600266
  • Romee R, Rosario M, Berrien-Elliott MM, et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016;8(357):357ra123. doi:10.1126/scitranslmed.aaf2341
  • Roy Chowdhury R, Vallania F, Yang Q, et al. A multi-cohort study of the immune factors associated with M. tuberculosis infection outcomes. Nature. 2018;560(7720):644–648. doi:10.1038/s41586-018-0439-x
  • Abebe F. Immunological basis of early clearance of Mycobacterium tuberculosis infection: the role of natural killer cells. Clin Exp Immunol. 2021;204(1):32–40. doi:10.1111/cei.13565
  • Kolloli A, Subbian S. Host-directed therapeutic strategies for tuberculosis. Front Med. 2017;4:171. doi:10.3389/fmed.2017.00171
  • Wallis RS, O’Garra A, Sher A, Wack A. Host-directed immunotherapy of viral and bacterial infections: past, present and future. Nat Rev Immunol. 2023;23(2):121–133. doi:10.1038/s41577-022-00734-z
  • Grzywacz B, Kataria N, Verneris MR. CD56(dim)CD16(+) NK cells downregulate CD16 following target cell induced activation of matrix metalloproteinases. Leukemia. 2007;21(2):356–359. doi:10.1038/sj.leu.2404499
  • Romee R, Foley B, Lenvik T, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood. 2013;121(18):3599–3608. doi:10.1182/blood-2012-04-425397
  • Schierloh P, Yokobori N, Aleman M, et al. Increased susceptibility to apoptosis of CD56dimCD16+ NK cells induces the enrichment of IFN-gamma-producing CD56bright cells in tuberculous pleurisy. J Immunol. 2005;175(10):6852–6860. doi:10.4049/jimmunol.175.10.6852
  • Rao D, Venkataswamy MM, Vasanthapuram R, Satishchandra P, Desai A. Alterations in natural killer and dendritic cell subsets in individuals with HIV-associated neurotuberculosis. J Med Virol. 2018;90(5):899–906. doi:10.1002/jmv.25042
  • Esaulova E, Das S, Singh DK, et al. The immune landscape in tuberculosis reveals populations linked to disease and latency. Cell Host Microbe. 2021;29(2):165–178 e8. doi:10.1016/j.chom.2020.11.013
  • Sherwood ER, Burelbach KR, McBride MA, et al. Innate immune memory and the host response to infection. J Immunol. 2022;208(4):785–792. doi:10.4049/jimmunol.2101058
  • Terren I, Orrantia A, Mosteiro A, Vitalle J, Zenarruzabeitia O, Borrego F. Metabolic changes of Interleukin-12/15/18-stimulated human NK cells. Sci Rep. 2021;11(1):6472. doi:10.1038/s41598-021-85960-6
  • Tarannum M, Romee R. Cytokine-induced memory-like natural killer cells for cancer immunotherapy. Stem Cell Res Ther. 2021;12(1):592. doi:10.1186/s13287-021-02655-5
  • Lopez-Verges S, Milush JM, Pandey S, et al. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood. 2010;116(19):3865–3874. doi:10.1182/blood-2010-04-282301
  • Hazeldine J, Lord JM. The impact of ageing on natural killer cell function and potential consequences for health in older adults. Ageing Res Rev. 2013;12(4):1069–1078. doi:10.1016/j.arr.2013.04.003
  • Nielsen CM, White MJ, Goodier MR, Riley EM. Functional Significance of CD57 expression on human NK cells and relevance to disease. Front Immunol. 2013;4:422. doi:10.3389/fimmu.2013.00422
  • Garand M, Goodier M, Owolabi O, Donkor S, Kampmann B, Sutherland JS. Functional and phenotypic changes of natural killer cells in whole blood during mycobacterium tuberculosis infection and disease. Front Immunol. 2018;9:257. doi:10.3389/fimmu.2018.00257
  • Di Vito C, Mikulak J, Mavilio D. On the way to become a natural killer cell. Front Immunol. 2019;10:1812. doi:10.3389/fimmu.2019.01812
  • Albayrak N, Dirix V, Aerts L, et al. Differential expression of maturation and activation markers on NK cells in patients with active and latent tuberculosis. J Leukoc Biol. 2022;111(5):1031–1042. doi:10.1002/JLB.4A1020-641RR
  • Zhuang L, Fulton RJ, Rettman P, et al. Activity of IL-12/15/18 primed natural killer cells against hepatocellular carcinoma. Hepatol Int. 2019;13(1):75–83. doi:10.1007/s12072-018-9909-3
  • Condos R, Rom WN, Schluger NW. Treatment of multidrug-resistant pulmonary tuberculosis with interferon-gamma via aerosol. Lancet. 1997;349(9064):1513–1515. doi:10.1016/S0140-6736(96)12273-X
  • Raju B, Hoshino Y, Kuwabara K, et al. Aerosolized gamma interferon (IFN-gamma) induces expression of the genes encoding the IFN-gamma-inducible 10-kilodalton protein but not inducible nitric oxide synthase in the lung during tuberculosis. Infect Immun. 2004;72(3):1275–1283. doi:10.1128/IAI.72.3.1275-1283.2004
  • Ulrichs T, Kaufmann SH. New insights into the function of granulomas in human tuberculosis. J Pathol. 2006;208(2):261–269. doi:10.1002/path.1906
  • Schneider BE, Korbel D, Hagens K, et al. A role for IL-18 in protective immunity against Mycobacterium tuberculosis. Eur J Immunol. 2010;40(2):396–405. doi:10.1002/eji.200939583
  • Harris LD, Khayumbi J, Ongalo J, et al. Distinct human NK cell phenotypes and functional responses to mycobacterium tuberculosis in adults from TB endemic and non-endemic regions. Front Cell Infect Microbiol. 2020;10:120. doi:10.3389/fcimb.2020.00120
  • Vankayalapati R, Barnes PF. Innate and adaptive immune responses to human Mycobacterium tuberculosis infection. Tuberculosis. 2009;89(Suppl 1):S77–80. doi:10.1016/S1472-9792(09)70018-6
  • Howard NC, Khader SA. Immunometabolism during Mycobacterium tuberculosis Infection. Trends Microbiol. 2020;28(10):832–850. doi:10.1016/j.tim.2020.04.010
  • Rao Y, Gai X, Le Y, et al. Enhanced Proinflammatory Cytokine Production and Immunometabolic Impairment of NK Cells Exposed to Mycobacterium tuberculosis and Cigarette Smoke. Front Cell Infect Microbiol. 2021;11:799276. doi:10.3389/fcimb.2021.799276
  • Kust SA, Streltsova MA, Panteleev AV, et al. HLA-DR-Positive NK cells expand in response to mycobacterium tuberculosis antigens and mediate mycobacteria-induced T cell activation. Front Immunol. 2021;12:662128. doi:10.3389/fimmu.2021.662128
  • Jayaraman P, Jacques MK, Zhu C, et al. TIM3 mediates T cell exhaustion during mycobacterium tuberculosis infection. PLoS Pathog. 2016;12(3):e1005490. doi:10.1371/journal.ppat.1005490
  • Khan N, Vidyarthi A, Amir M, Mushtaq K, Agrewala JN. T-cell exhaustion in tuberculosis: pitfalls and prospects. Crit Rev Microbiol. 2017;43(2):133–141. doi:10.1080/1040841X.2016.1185603
  • Wondmagegn T, Damtie D, Genetu M, Biadgo B, Lemma M, Negash M. T lymphocyte subpopulations and intestinal helminthes profile among tuberculosis patients co-infected with HIV before and after anti tubercular treatment at university of Gondar hospital, Northwest Ethiopia. BMC Infect Dis. 2020;20(1):109. doi:10.1186/s12879-020-4845-y
  • Schafer JL, Muller-Trutwin MC, Reeves RK. NK cell exhaustion: bad news for chronic disease? Oncotarget. 2015;6(26):21797–21798. doi:10.18632/oncotarget.5490
  • Netea MG, Quintin J, van der Meer JW. Trained immunity: a memory for innate host defense. Cell Host Microbe. 2011;9(5):355–361. doi:10.1016/j.chom.2011.04.006
  • Khader SA, Divangahi M, Hanekom W, et al. Targeting innate immunity for tuberculosis vaccination. J Clin Invest. 2019;129(9):3482–3491. doi:10.1172/JCI128877
  • Uppendahl LD, Felices M, Bendzick L, et al. Cytokine-induced memory-like natural killer cells have enhanced function, proliferation, and in vivo expansion against ovarian cancer cells. Gynecol Oncol. 2019;153(1):149–157. doi:10.1016/j.ygyno.2019.01.006