Contained Mycobacterium tuberculosis infection induces concomitant and heterologous protection

English version

Autoři: Johannes Nemeth ^aff001; Gregory S. Olson ^aff001; Alissa C. Rothchild ^aff001; Ana N. Jahn ^aff001; Dat Mai ^aff001; Fergal J. Duffy ^aff001; Jared L. Delahaye ^aff001; Sanjay Srivatsan ^aff002; Courtney R. Plumlee ^aff001; Kevin B. Urdahl ^aff001; Elizabeth S. Gold ^aff001; Alan Aderem ^aff001; Alan H. Diercks ^aff001
Působiště autorů: Seattle Children’s Research Institute, Seattle, Washington, United States of America ^aff001; Medical Scientist Training Program, University of Washington School of Medicine, Seattle, Washington, United States of America ^aff002; Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America ^aff003
Vyšlo v časopise: Contained Mycobacterium tuberculosis infection induces concomitant and heterologous protection. PLoS Pathog 16(7): e1008655. doi:10.1371/journal.ppat.1008655
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008655

Souhrn

Progress in tuberculosis vaccine development is hampered by an incomplete understanding of the immune mechanisms that protect against infection with Mycobacterium tuberculosis (Mtb), the causative agent of tuberculosis. Although the M72/ASOE1 trial yielded encouraging results (54% efficacy in subjects with prior exposure to Mtb), a highly effective vaccine against adult tuberculosis remains elusive. We show that in a mouse model, establishment of a contained and persistent yet non-pathogenic infection with Mtb (“contained Mtb infection”, CMTB) rapidly and durably reduces tuberculosis disease burden after re-exposure through aerosol challenge. Protection is associated with elevated activation of alveolar macrophages, the first cells that respond to inhaled Mtb, and accelerated recruitment of Mtb-specific T cells to the lung parenchyma. Systems approaches, as well as ex vivo functional assays and in vivo infection experiments, demonstrate that CMTB reconfigures tissue resident alveolar macrophages via low grade interferon-γ exposure. These studies demonstrate that under certain circumstances, the continuous interaction of the immune system with Mtb is beneficial to the host by maintaining elevated innate immune responses.

Klíčová slova:

Aerosols – Alveolar macrophages – Immune response – Mouse models – Mycobacterium tuberculosis – Spleen – T cells – Tuberculosis

Zdroje

1. World Health Organization. GLOBAL TUBERCULOSIS REPORT. 2019;: 1–297.

2. Furin JF, Cox HC, Pai PMP. Tuberculosis. The Lancet. Elsevier Ltd; 2019;393: 1642–1656. doi: 10.1016/S0140-6736(19)30308-3

3. Wang CY. An Experimental Study of latent tuberculosis. Lancet. Elsevier; 1916;188: 417–419. doi: 10.1016/S0140-6736(00)58936-3

4. Lillebaek T, Dirksen A, Baess I, Strunge B, Thomsen VØ, Andersen AB. Molecular Evidence of Endogenous Reactivation of Mycobacterium tuberculosis after 33 Years of Latent Infection. J Infect Dis. Oxford University Press; 2002;185: 401–404. doi: 10.1086/338342 11807725

5. Neyrolles O, Hernandez-Pando R, Pietri-Rouxel F, Fornès P, Tailleux L, Payán JAB, et al. Is Adipose Tissue a Place for Mycobacterium tuberculosis Persistence? Sherman D, editor. PLoS ONE. Public Library of Science; 2006;1: e43. doi: 10.1371/journal.pone.0000043 17183672

6. Hernández-Pando R, Jeyanathan M, Mengistu G, Aguilar D, Orozco H, Harboe M, et al. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet. 2000;356: 2133–2138. doi: 10.1016/s0140-6736(00)03493-0 11191539

7. Behr MA, Waters WR. Is tuberculosis a lymphatic disease with a pulmonary portal? Lancet Infect Dis. 2014;14: 250–255. doi: 10.1016/S1473-3099(13)70253-6 24268591

8. Ganchua SKC, Cadena AM, Maiello P, Gideon HP, Myers AJ, Junecko BF, et al. Lymph nodes are sites of prolonged bacterial persistence during Mycobacterium tuberculosis infection in macaques. Behr MA, editor. PLoS Pathog. Public Library of Science; 2018;14: e1007337. doi: 10.1371/journal.ppat.1007337 30383808

9. Osler SW. The Principles and practice of medicine. 1903.

10. Houben RMGJ Dodd PJ. The Global Burden of Latent Tuberculosis Infection: A Re-estimation Using Mathematical Modelling. Metcalfe JZ, editor. PLoS Med. 2016;13: e1002152–13. doi: 10.1371/journal.pmed.1002152 27780211

11. Pai M, Behr MA, Dowdy D, Dheda K, Divangahi M, Boehme CC, et al. Tuberculosis. Nature Publishing Group; 2016;2: 16076–23. doi: 10.1038/nrdp.2016.76 27784885

12. Dutta NK, Karakousis PC. Latent tuberculosis infection: myths, models, and molecular mechanisms. Microbiol Mol Biol Rev. American Society for Microbiology; 2014;78: 343–371. doi: 10.1128/MMBR.00010-14 25184558

13. Andrews JR, Noubary F, Walensky RP, Cerda R, Losina E, Horsburgh CR. Risk of Progression to Active Tuberculosis Following Reinfection With Mycobacterium tuberculosis. Clinical Infectious Diseases. 2012;54: 784–791. doi: 10.1093/cid/cir951 22267721

14. Blaser N, Zahnd C, Hermans S, Salazar-Vizcaya L, Estill J, Morrow C, et al. Tuberculosis in Cape Town: An age-structured transmission model. Epidemics. Elsevier B.V; 2016;14: 54–61. doi: 10.1016/j.epidem.2015.10.001 26972514

15. Cadena AM, Hopkins FF, Maiello P, Carey AF, Wong EA, Martin CJ, et al. Concurrent infection with Mycobacterium tuberculosis confers robust protection against secondary infection in macaques. Salgame P, editor. PLoS Pathog. Public Library of Science; 2018;14: e1007305–17. doi: 10.1371/journal.ppat.1007305 30312351

16. Saljoughian N, Taheri T, Rafati S. Live Vaccination Tactics: Possible Approaches for Controlling Visceral Leishmaniasis. Frontiers in Immunology. Frontiers; 2014;5: 345–11. doi: 10.3389/fimmu.2014.00134 24744757

17. Doolan DL, Dobano C, Baird JK. Acquired Immunity to Malaria. Clin Microbiol Rev. 2009;22: 13–36. doi: 10.1128/CMR.00025-08 19136431

18. Brown SP, Grenfell BT. An unlikely partnership: parasites, concomitant immunity and host defence. Proceedings of the Royal Society of London Series B: Biological Sciences. 2001;268: 2543–2549. doi: 10.1098/rspb.2001.1821 11749708

19. Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonça LE, Pacis A, et al. BCG Educates Hematopoietic Stem Cells to Generate Protective Innate Immunity against Tuberculosis. Cell. Elsevier Inc; 2018;172: 176–182.e19. doi: 10.1016/j.cell.2017.12.031 29328912

20. Sathkumara HD, Pai S, Aceves-Sánchez M de J, Ketheesan N, Flores-Valdez MA, Kupz A. BCG Vaccination Prevents Reactivation of Latent Lymphatic Murine Tuberculosis Independently of CD4+ T Cells. Frontiers in Immunology. Frontiers; 2019;10: 475–11. doi: 10.3389/fimmu.2019.00475

21. Kupz A, Zedler U, Stäber M, Kaufmann SHE. A Mouse Model of Latent Tuberculosis Infection to Study Intervention Strategies to Prevent Reactivation. Neyrolles O, editor. PLoS ONE. Public Library of Science; 2016;11: e0158849. doi: 10.1371/journal.pone.0158849 27391012

22. Tornack J, Reece ST, Bauer WM, Vogelzang A, Bandermann S, Zedler U, et al. Human and Mouse Hematopoietic Stem Cells Are a Depot for Dormant Mycobacterium tuberculosis. Subbian S, editor. PLoS ONE. 2017;12: e0169119–18. doi: 10.1371/journal.pone.0169119 28046053

23. Marquis J-F, LaCourse R, Ryan L, North RJ, Gros P. Disseminated and rapidly fatal tuberculosis in mice bearing a defective allele at IFN regulatory factor 8. J Immunol. American Association of Immunologists; 2009;182: 3008–3015. doi: 10.4049/jimmunol.0800680 19234196

24. Cheng Y, Schorey JS. Mycobacterium tuberculosis-induced IFN-β production requires cytosolic DNA and RNA sensing pathways. J Exp Med. Rockefeller University Press; 2018;215: 2919–2935. doi: 10.1084/jem.20180508 30337468

25. Huaman MA, Deepe GS Jr, Fichtenbaum CJ. Elevated Circulating Concentrations of Interferon-Gamma in Latent Tuberculosis Infection. PAI. 2016;1: 291–13. doi: 10.20411/pai.v1i2.149 27853753

26. Vankayalapati R, Wizel B, Weis S, Klucar P, Shams H, Samten B, et al. Serum Cytokine Concentrations Do Not Parallel Mycobacterium tuberculosis–Induced Cytokine Production in Patients with Tuberculosis. Clinical Infectious Diseases. 2002;: 1–5.

27. Gern B, Plumlee C, Gerner M, Urdahl K. Investigating Immune Correlates of Protection to Tuberculosis Using an Ultra-Low Dose Infection in a Mouse Model. Open Forum Infectious Diseases. 2017;4: S47–S48. doi: 10.1093/ofid/ofx162.112

28. Rothchild AC, Olson GS, Nemeth J, Amon LM, Mai D, Gold ES, et al. Alveolar macrophages generate a noncanonical NRF2-driven transcriptional response to Mycobacterium tuberculosis in vivo. Sci Immunol. Science Immunology; 2019;4: eaaw6693. doi: 10.1126/sciimmunol.aaw6693 31350281

29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. PNAS. National Academy of Sciences; 2005;102: 15545–15550. doi: 10.1073/pnas.0506580102 16199517

30. Netea MG. Training innate immunity: the changing concept of immunological memory in innate host defence. Eur J Clin Invest. 2013;43: 881–884. doi: 10.1111/eci.12132 23869409

31. Harty JT, Bevan MJ. Specific Immunity to Listeria monocytogenes in the Absence if IFNy. Immunity. 1995;3: 106–117.

32. Sanlorenzo M, Vujic I, Carnevale-Schianca F, Pietro Quaglino, Gammaitoni L, Fierro MT, et al. Role of interferon in melanoma: old hopes and new perspectives. Expert Opinion on Biological Therapy. Taylor & Francis; 2017;17: 475–483. doi: 10.1080/14712598.2017.1289169 28274138

33. Aagaard C, Hoang T, Dietrich J, Cardona P-J, Izzo A, Dolganov G, et al. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nature Publishing Group; 2011;17: 189–194. doi: 10.1038/nm.2285 21258338

34. Orme IM. Characteristics and specificity of acquired immunologic memory to Mycobacterium tuberculosis infection. J Immunol. 1988 May 15;140(10):3589–93. 3129497

35. Flynn JL. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. Journal of Experimental Medicine. 1993;178: 2249–2254. doi: 10.1084/jem.178.6.2249 7504064

36. Cooper AM, Dalton D, Stewart T, Griffin J, Russell DG, Orme IM. Disseminated Tuberculosis in Interferon-g Gene-disrupted Mice. Journal of Experimental Medicine. 1993;178: 2243–2247. doi: 10.1084/jem.178.6.2243 8245795

37. Cooper AM, Magram J, Ferrante J, Orme IM. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with mycobacterium tuberculosis. Journal of Experimental Medicine. The Rockefeller University Press; 1997;186: 39–45. doi: 10.1084/jem.186.1.39 9206995

38. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, et al. Tumor necrosis factor-α is required in the protective immune response against mycobacterium tuberculosis in mice. Immunity. 1995;2: 561–572. doi: 10.1016/1074-7613(95)90001-2 7540941

39. Cohen SB, Gern BH, Delahaye JL, Adams KN, Plumlee CR, Winkler JK, et al. Alveolar Macrophages Provide an Early Mycobacterium tuberculosis Niche and Initiate Dissemination. Cell Host Microbe. Elsevier Inc; 2018;24: 439–446.e4. doi: 10.1016/j.chom.2018.08.001 30146391

40. Delahaye JL, Gern BH, Cohen SB, Plumlee CR, Shafiani S, Gerner MY, et al. Cutting Edge: Bacillus Calmette-Guérin-Induced T Cells Shape Mycobacterium tuberculosis Infection before Reducing the Bacterial Burden. J Immunol. American Association of Immunologists; 2019;203: 807–812. doi: 10.4049/jimmunol.1900108 31308091

41. Shafiani S, Tucker-Heard G, Kariyone A, Takatsu K, Urdahl KB. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. Journal of Experimental Medicine. 2010;207: 1409–1420. doi: 10.1084/jem.20091885 20547826

42. North RJ, Kirstein DP. T-cell-mediated concomitant immunity to syngeneic tumors. I. Activated macrophages as the expressors of nonspecific immunity to unrelated tumors and bacterial parasites. Journal of Experimental Medicine. 1977;145: 275–292. doi: 10.1084/jem.145.2.275 401860

43. Belkaid Y, Piccirillo C, Mendez S, Shevach E, Sacks D. CD4+CD25+regulatory T cells control Leishmania major persistence and immunity. Nature. 2002;420: 499–502. doi: 10.1038/nature01199

44. Brown SP, Grenfell BT. An unlikely partnership: parasites, concomitant immunity and host defence. Proceedings of the Royal Society of London Series B: Biological Sciences. 2001;268: 2543–2549. doi: 10.1098/rspb.2001.1821 11749708

45. Barry CE, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol. Nature Publishing Group; 2009;7: 845–855. doi: 10.1038/nrmicro2236 19855401

46. Higgins JPT, Soares-Weiser K, López-López JA, Kakourou A, Chaplin K, Christensen H, et al. Association of BCG, DTP, and measles containing vaccines with childhood mortality: systematic review. BMJ. 2016;: i5170–13. doi: 10.1136/bmj.i5170 27737834

47. Usher NT, Chang S, Howard RS, Martinez A, Harrison LH, Santosham M, et al. Association of BCG Vaccination in Childhood With Subsequent Cancer Diagnoses: A 60-Year Follow-up of a Clinical Trial. JAMA Netw Open. 2019;2: e1912014. doi: 10.1001/jamanetworkopen.2019.12014 31553471

48. Jensen KJ, Larsen N, Biering-Sørensen S, Andersen A, Eriksen HB, Monteiro I, et al. Heterologous immunological effects of early BCG vaccination in low-birth-weight infants in Guinea-Bissau: a randomized-controlled trial. J Infect Dis. Oxford University Press; 2015;211: 956–967. doi: 10.1093/infdis/jiu508 25210141

49. Goodridge HS, Ahmed SS, Curtis N, Kollmann TR, Levy O, Netea MG, et al. Harnessing the beneficial heterologous effects of vaccination. Nat Rev Immunol. Nature Publishing Group; 2016. doi: 10.1038/nri.2016.43 27157064

50. Overwijk WW, Restifo NP. B16 as a Mouse Model for Human Melanoma. Hoboken, NJ, USA: John Wiley & Sons, Inc; 2001. pp. 453–33. doi: 10.1002/0471142735.im2001s39 18432774

51. Rothchild AC, Sissons JR, Shafiani S, Plaisier C, Min D, Mai D, et al. MiR-155–regulated molecular network orchestrates cell fate in the innate and adaptive immune response to Mycobacterium tuberculosis. PNAS. 2016;113: E6172–E6181. doi: 10.1073/pnas.1608255113 27681624

52. Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Wiley Subscription Services, Inc., A Wiley Company; 2011;81A: 343–350. doi: 10.1002/cyto.a.22012 22213571

53. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GRS, Perlman H. Flow Cytometric Analysis of Macrophages and Dendritic Cell Subsets in the Mouse Lung. American Journal of Respiratory Cell and Molecular Biology. American Thoracic Society; 2013;49: 503–510. doi: 10.1165/rcmb.2013-0086MA 23672262

54. Moguche AO, Shafiani S, Clemons C, Larson RP, Dinh C, Higdon LE, et al. ICOS and Bcl6-dependent pathways maintain a CD4 T cell population with memory-like properties during tuberculosis. J Exp Med. Rockefeller University Press; 2015;212: 715–728. doi: 10.1084/jem.20141518 25918344

55. Chen X, Shen Y, Draper W, Buenrostro JD, Litzenburger U, Cho SW, et al. ATAC-see reveals the accessible genome by transposase-mediated imaging and sequencing. Nat Methods. Nature Publishing Group; 2016;13: 1013–1020. doi: 10.1038/nmeth.4031 27749837

56. Wu TD, Watanabe CK. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005;21: 1859–1875. doi: 10.1093/bioinformatics/bti310 15728110

57. Wu TD, Nacu S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010;26: 873–881. doi: 10.1093/bioinformatics/btq057 20147302

58. Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. ATAC-seq: A Method for Assaying Chromatin Accessibility Genome-Wide. Hoboken, NJ, USA: John Wiley & Sons, Inc; 2001. pp. 21.29.1–21.29.9. doi: 10.1002/0471142727.mb2129s109 25559105

59. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based Analysis of ChIP-Seq (MACS). Genome Biology. 2015;: 1–9. doi: 10.1186/s13059-014-0572-2

60. Consortium TEP, Consortium TEP, data analysis coordination OC, data production DPL, data analysis LA, group W, et al. An integrated encyclopedia of DNA elements in the human genome. Nature. Nature Publishing Group; 2012;488: 57–74. doi: 10.1038/nature11361

61. Stark R, Brown G. DiffBind: Differential binding analysis of ChIP- Seq peak data. 2018;: 1–34.

62. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. Nature Publishing Group; 2012;481: 389–393. doi: 10.1038/nature10730 22217937

63. McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucl Acids Res. 2nd ed. 2012;40: 4288–4297. doi: 10.1093/nar/gks042 22287627

Článek Host prion protein expression levels impact prion tropism for the spleen

Článek Protein phosphatase 1 catalyzes HBV core protein dephosphorylation and is co-packaged with viral pregenomic RNA into nucleocapsids

Článek Updating the fungal infection-mammalian selection hypothesis at the end of the Cretaceous Period

Článek Timelines of infection and transmission dynamics of H1N1pdm09 in swine

Článek Mutant prion proteins increase calcium permeability of AMPA receptors, exacerbating excitotoxicity

Článek vyšel v časopise