First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (2024)

First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (1) https://doi.org/10.1016/j.celrep.2017.01.071 · First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (2) Full text

Journal: Cell Reports, 2017, №8, p.1893-1905

Publisher: Elsevier BV

Authors:

  1. Simona Saluzzo
  2. Anna-Dorothea Gorki
  3. Batika M.J. Rana
  4. Rui Martins
  5. Seth Scanlon
  6. Philipp Starkl
  7. Karin Lakovits
  8. Anastasiya Hladik
  9. Ana Korosec
  10. Omar Sharif
  11. Joanna M. Warszawska
  12. Helen Jolin
  13. Ildiko Mesteri
  14. Andrew N.J. McKenzie
  15. Sylvia Knapp

Funders

  1. Wellcome Trust
  2. Medical Research Council
  3. Vienna Science and Technology Fund
  4. Austrian Science Fund
  5. Medizinische Universität Wien

List of references

  1. Barlow, Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity, J. Allergy Clin. Immunol., № 129, с. 191
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (3) https://doi.org/10.1016/j.jaci.2011.09.041
  2. Beers, The three R’s of lung health and disease: repair, remodeling, and regeneration, J. Clin. Invest., № 121, с. 2065
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (4) https://doi.org/10.1172/JCI45961
  3. Brestoff, Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity, Nature, № 519, с. 242
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (5) https://doi.org/10.1038/nature14115
  4. Chang, Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity, Nat. Immunol., № 12, с. 631
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (6) https://doi.org/10.1038/ni.2045
  5. Chen, Potential role for alternatively activated macrophages in the secondary bacterial infection during recovery from influenza, Immunol. Lett., № 141, с. 227
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (7) https://doi.org/10.1016/j.imlet.2011.10.009
  6. Chen, Myocardial pressure overload induces systemic inflammation through endothelial cell IL-33, Proc. Natl. Acad. Sci. USA, № 112, с. 7249
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (8) https://doi.org/10.1073/pnas.1424236112
  7. Chien, Bacterial pathogens and death during the 1918 influenza pandemic, N. Engl. J. Med., № 361, с. 2582
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (9) https://doi.org/10.1056/NEJMc0908216
  8. Chiu, Antiviral B cell and T cell immunity in the lungs, Nat. Immunol., № 16, с. 18
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (10) https://doi.org/10.1038/ni.3056
  9. De Filippo, Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation, Blood, № 121, с. 4930
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (11) https://doi.org/10.1182/blood-2013-02-486217
  10. de Kleer, Perinatal activation of the interleukin-33 pathway promotes type 2 immunity in the developing lung, Immunity, № 45, с. 1285
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (12) https://doi.org/10.1016/j.immuni.2016.10.031
  11. Gollwitzer, Lung microbiota promotes tolerance to allergens in neonates via PD-L1, Nat. Med., № 20, с. 642
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (13) https://doi.org/10.1038/nm.3568
  12. Gordon, Alternative activation of macrophages: mechanism and functions, Immunity, № 32, с. 593
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (14) https://doi.org/10.1016/j.immuni.2010.05.007
  13. Guery, Fine-tuning nucleophosmin in macrophage differentiation and activation, Blood, № 118, с. 4694
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (15) https://doi.org/10.1182/blood-2011-03-341255
  14. Guilliams, Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF, J. Exp. Med., № 210, с. 1977
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (16) https://doi.org/10.1084/jem.20131199
  15. Halim, Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation, Immunity, № 40, с. 425
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (17) https://doi.org/10.1016/j.immuni.2014.01.011
  16. Hardman, IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation, Eur. J. Immunol., № 43, с. 488
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (18) https://doi.org/10.1002/eji.201242863
  17. Hogan, Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function, Cell Stem Cell, № 15, с. 123
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (19) https://doi.org/10.1016/j.stem.2014.07.012
  18. Hussell, Alveolar macrophages: plasticity in a tissue-specific context, Nat. Rev. Immunol., № 14, с. 81
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (20) https://doi.org/10.1038/nri3600
  19. Kakkar, Interleukin 33 as a mechanically responsive cytokine secreted by living cells, J. Biol. Chem., № 287, с. 6941
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (21) https://doi.org/10.1074/jbc.M111.298703
  20. Kearley, Cigarette smoke silences innate lymphoid cell function and facilitates an exacerbated type I interleukin-33-dependent response to infection, Immunity, № 42, с. 566
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (22) https://doi.org/10.1016/j.immuni.2015.02.011
  21. Kim, Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease, Nat. Med., № 14, с. 633
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (23) https://doi.org/10.1038/nm1770
  22. Kim, Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity, J. Allergy Clin. Immunol., № 129, с. 216
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (24) https://doi.org/10.1016/j.jaci.2011.10.036
  23. Kopf, IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses, Immunity, № 4, с. 15
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (25) https://doi.org/10.1016/S1074-7613(00)80294-0
  24. Kopf, The development and function of lung-resident macrophages and dendritic cells, Nat. Immunol., № 16, с. 36
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (26) https://doi.org/10.1038/ni.3052
  25. Kouzaki, The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses, J. Immunol., № 186, с. 4375
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (27) https://doi.org/10.4049/jimmunol.1003020
  26. Lambrecht, The immunology of asthma, Nat. Immunol., № 16, с. 45
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (28) https://doi.org/10.1038/ni.3049
  27. Lamkanfi, IL-33 raises alarm, Immunity, № 31, с. 5
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (29) https://doi.org/10.1016/j.immuni.2009.06.011
  28. Lavin, Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment, Cell, № 159, с. 1312
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (30) https://doi.org/10.1016/j.cell.2014.11.018
  29. Lee, Activated type 2 innate lymphoid cells regulate beige fat biogenesis, Cell, № 160, с. 74
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (31) https://doi.org/10.1016/j.cell.2014.12.011
  30. Liew, Disease-associated functions of IL-33: the new kid in the IL-1 family, Nat. Rev. Immunol., № 10, с. 103
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (32) https://doi.org/10.1038/nri2692
  31. Lu, The role of IL-33/ST2L signals in the immune cells, Immunol. Lett., № 164, с. 11
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (33) https://doi.org/10.1016/j.imlet.2015.01.008
  32. Mantovani, The chemokine system in diverse forms of macrophage activation and polarization, Trends Immunol., № 25, с. 677
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (34) https://doi.org/10.1016/j.it.2004.09.015
  33. Martin, Interleukin 33 is a guardian of barriers and a local alarmin, Nat. Immunol., № 17, с. 122
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (35) https://doi.org/10.1038/ni.3370
  34. McKenzie, Impaired development of Th2 cells in IL-13-deficient mice, Immunity, № 9, с. 423
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (36) https://doi.org/10.1016/S1074-7613(00)80625-1
  35. Molofsky, Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages, J. Exp. Med., № 210, с. 535
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (37) https://doi.org/10.1084/jem.20121964
  36. Molofsky, Interleukin-33 in tissue homeostasis, injury, and inflammation, Immunity, № 42, с. 1005
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (38) https://doi.org/10.1016/j.immuni.2015.06.006
  37. Monin, Helminth-induced arginase-1 exacerbates lung inflammation and disease severity in tuberculosis, J. Clin. Invest., № 125, с. 4699
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (39) https://doi.org/10.1172/JCI77378
  38. Monticelli, Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus, Nat. Immunol., № 12, с. 1045
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (40) https://doi.org/10.1038/ni.2131
  39. Mund, Developmental alveolarization of the mouse lung, Dev. Dyn., № 237, с. 2108
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (41) https://doi.org/10.1002/dvdy.21633
  40. Murphy, The prolonged life-span of alveolar macrophages, Am. J. Respir. Cell Mol. Biol., № 38, с. 380
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (42) https://doi.org/10.1165/rcmb.2007-0224RC
  41. Neill, Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity, Nature, № 464, с. 1367
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (43) https://doi.org/10.1038/nature08900
  42. Nussbaum, Type 2 innate lymphoid cells control eosinophil homeostasis, Nature, № 502, с. 245
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (44) https://doi.org/10.1038/nature12526
  43. Odegaard, Perinatal licensing of thermogenesis by IL-33 and ST2, Cell, № 166, с. 841
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (45) https://doi.org/10.1016/j.cell.2016.06.040
  44. Okabe, Tissue-specific signals control reversible program of localization and functional polarization of macrophages, Cell, № 157, с. 832
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (46) https://doi.org/10.1016/j.cell.2014.04.016
  45. Oliphant, MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion, Immunity, № 41, с. 283
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (47) https://doi.org/10.1016/j.immuni.2014.06.016
  46. Orr, Mechanisms of mechanotransduction, Dev. Cell, № 10, с. 11
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (48) https://doi.org/10.1016/j.devcel.2005.12.006
  47. Peng, Hedgehog actively maintains adult lung quiescence and regulates repair and regeneration, Nature, № 526, с. 578
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (49) https://doi.org/10.1038/nature14984
  48. Pichery, Endogenous IL-33 is highly expressed in mouse epithelial barrier tissues, lymphoid organs, brain, embryos, and inflamed tissues: in situ analysis using a novel Il-33-LacZ gene trap reporter strain, J. Immunol., № 188, с. 3488
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (50) https://doi.org/10.4049/jimmunol.1101977
  49. Price, Systemically dispersed innate IL-13-expressing cells in type 2 immunity, Proc. Natl. Acad. Sci. USA, № 107, с. 11489
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (51) https://doi.org/10.1073/pnas.1003988107
  50. Qiu, Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat, Cell, № 157, с. 1292
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (52) https://doi.org/10.1016/j.cell.2014.03.066
  51. Rijavec, Natural killer T cells in pulmonary disorders, Respir. Med., № 105, с. S20
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (53) https://doi.org/10.1016/S0954-6111(11)70006-3
  52. Roediger, Group 2 innate lymphoid cells in the regulation of immune responses, Adv. Immunol., № 125, с. 111
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (54) https://doi.org/10.1016/bs.ai.2014.09.004
  53. Salgame, Effect of helminth-induced immunity on infections with microbial pathogens, Nat. Immunol., № 14, с. 1118
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (55) https://doi.org/10.1038/ni.2736
  54. Sanada, IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system, J. Clin. Invest., № 117, с. 1538
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (56) https://doi.org/10.1172/JCI30634
  55. Saunders, Spontaneous atopic dermatitis is mediated by innate immunity, with the secondary lung inflammation of the atopic march requiring adaptive immunity, J. Allergy Clin. Immunol., № 137, с. 482
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (57) https://doi.org/10.1016/j.jaci.2015.06.045
  56. Schlenner, Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus, Immunity, № 32, с. 426
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (58) https://doi.org/10.1016/j.immuni.2010.03.005
  57. Schliehe, The methyltransferase Setdb2 mediates virus-induced susceptibility to bacterial superinfection, Nat. Immunol., № 16, с. 67
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (59) https://doi.org/10.1038/ni.3046
  58. Schmitz, IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines, Immunity, № 23, с. 479
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (60) https://doi.org/10.1016/j.immuni.2005.09.015
  59. Sharif, The triggering receptor expressed on myeloid cells 2 inhibits complement component 1q effector mechanisms and exerts detrimental effects during pneumococcal pneumonia, PLoS Pathog., № 10, с. e1004167
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (61) https://doi.org/10.1371/journal.ppat.1004167
  60. Shinkai, RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement, Cell, № 68, с. 855
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (62) https://doi.org/10.1016/0092-8674(92)90029-C
  61. Talbot, Asthma as a risk factor for invasive pneumococcal disease, N. Engl. J. Med., № 352, с. 2082
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (63) https://doi.org/10.1056/NEJMoa044113
  62. Townsend, T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses, J. Exp. Med., № 191, с. 1069
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (64) https://doi.org/10.1084/jem.191.6.1069
  63. Treutlein, Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq, Nature, № 509, с. 371
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (65) https://doi.org/10.1038/nature13173
  64. van der Poll, Pathogenesis, treatment, and prevention of pneumococcal pneumonia, Lancet, № 374, с. 1543
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (66) https://doi.org/10.1016/S0140-6736(09)61114-4
  65. von Moltke, I-L-C-2 it: type 2 immunity and group 2 innate lymphoid cells in homeostasis, Curr. Opin. Immunol., № 31, с. 58
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (67) https://doi.org/10.1016/j.coi.2014.09.009
  66. Warszawska, Lipocalin 2 deactivates macrophages and worsens pneumococcal pneumonia outcomes, J. Clin. Invest., № 123, с. 3363
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (68) https://doi.org/10.1172/JCI67911
  67. Wirtz, The effects of mechanical forces on lung functions, Respir. Physiol., № 119, с. 1
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (69) https://doi.org/10.1016/S0034-5687(99)00092-4
  68. Woik, Regulation of lung development and regeneration by the vascular system, Cell. Mol. Life Sci., № 72, с. 2709
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (70) https://doi.org/10.1007/s00018-015-1907-1
  69. Wong, Transcription factor RORα is critical for nuocyte development, Nat. Immunol., № 13, с. 229
    First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment (71) https://doi.org/10.1038/ni.2208

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