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

Cell Reports

Volumn 18, Issue 8, 2017, Pages 1893-1905

  Saluzzo, Simona ^a,b,c   Gorki, Anna Dorothea ^a,b   Rana, Batika M J ^c   Martins, Rui ^a,b   Scanlon, Seth ^c   Starkl, Philipp ^a,b   Lakovits, Karin ^a,b   Hladik, Anastasiya ^a,b   Korosec, Ana ^a,b   Sharif, Omar ^a,b   Warszawska, Joanna M ^a,b   Jolin, Helen ^c   Mesteri, Ildiko ^d   McKenzie, Andrew N J ^c   Knapp, Sylvia ^a,b  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d University of Überlingen   (Germany)

Author keywords

alarmin; alveolar macrophage; first breath; immune homeostasis; lung; newborn; pneumoniae; S. pneumoniae

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 33;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNE RESPONSE; INNATE IMMUNITY; INTERFERON INDUCTION; LUNG; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS MACROPHAGE; LUNG INFLATION; LYMPHOID CELL; MOUSE; NEWBORN; NONHUMAN; PNEUMOCOCCAL INFECTION; UPREGULATION; ANIMAL; C57BL MOUSE; HOMEOSTASIS; IMMUNOLOGY; LYMPHOCYTE; MACROPHAGE; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANIMALS, NEWBORN; HOMEOSTASIS; IMMUNITY, INNATE; INTERLEUKIN-13; LUNG; LYMPHOCYTES; MACROPHAGES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; UP-REGULATION;

EID: 85013921443     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.071     Document Type: Article

References (69)

1. Barlow, J.L., Bellosi, A., Hardman, C.S., Drynan, L.F., Wong, S.H., Cruickshank, J.P., McKenzie, A.N.J., Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J. Allergy Clin. Immunol. 129 (2012), 191–198.e4.
2. Beers, M.F., Morrisey, E.E., The three R's of lung health and disease: repair, remodeling, and regeneration. J. Clin. Invest. 121 (2011), 2065–2073.
3. Brestoff, J.R., Kim, B.S., Saenz, S.A., Stine, R.R., Monticelli, L.A., Sonnenberg, G.F., Thome, J.J., Farber, D.L., Lutfy, K., Seale, P., Artis, D., Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 519 (2015), 242–246.
4. Chang, Y.-J., Kim, H.Y., Albacker, L.A., Baumgarth, N., McKenzie, A.N., Smith, D.E., Dekruyff, R.H., Umetsu, D.T., Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12 (2011), 631–638.
5. Chen, W.H., Toapanta, F.R., Shirey, K.A., Zhang, L., Giannelou, A., Page, C., Frieman, M.B., Vogel, S.N., Cross, A.S., Potential role for alternatively activated macrophages in the secondary bacterial infection during recovery from influenza. Immunol. Lett. 141 (2012), 227–234.
6. Chen, W.-Y., Hong, J., Gannon, J., Kakkar, R., Lee, R.T., Myocardial pressure overload induces systemic inflammation through endothelial cell IL-33. Proc. Natl. Acad. Sci. USA 112 (2015), 7249–7254.
7. Chien, Y.-W., Klugman, K.P., Morens, D.M., Bacterial pathogens and death during the 1918 influenza pandemic. N. Engl. J. Med. 361 (2009), 2582–2583.
8. Chiu, C., Openshaw, P.J., Antiviral B cell and T cell immunity in the lungs. Nat. Immunol. 16 (2015), 18–26.
9. De Filippo, K., Dudeck, A., Hasenberg, M., Nye, E., van Rooijen, N., Hartmann, K., Gunzer, M., Roers, A., Hogg, N., Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood 121 (2013), 4930–4937.
10. de Kleer, I.M., Kool, M., de Bruijn, M.J.W., Willart, M., van Moorleghem, J., Schuijs, M.J., Plantinga, M., Beyaert, R., Hams, E., Fallon, P.G., et al. Perinatal activation of the interleukin-33 pathway promotes type 2 immunity in the developing lung. Immunity 45 (2016), 1285–1298.
11. Gollwitzer, E.S., Saglani, S., Trompette, A., Yadava, K., Sherburn, R., McCoy, K.D., Nicod, L.P., Lloyd, C.M., Marsland, B.J., Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat. Med. 20 (2014), 642–647.
12. Gordon, S., Martinez, F.O., Alternative activation of macrophages: mechanism and functions. Immunity 32 (2010), 593–604.
13. Guery, L., Benikhlef, N., Gautier, T., Paul, C., Jego, G., Dufour, E., Jacquel, A., Cally, R., Manoury, B., Vanden Berghe, T., et al. Fine-tuning nucleophosmin in macrophage differentiation and activation. Blood 118 (2011), 4694–4704.
14. Guilliams, M., De Kleer, I., Henri, S., Post, S., Vanhoutte, L., De Prijck, S., Deswarte, K., Malissen, B., Hammad, H., Lambrecht, B.N., 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 (2013), 1977–1992.
15. Halim, T.Y.F., Steer, C.A., Mathä, L., Gold, M.J., Martinez-Gonzalez, I., McNagny, K.M., McKenzie, A.N.J., Takei, F., Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40 (2014), 425–435.
16. Hardman, C.S., Panova, V., McKenzie, A.N.J., IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation. Eur. J. Immunol. 43 (2013), 488–498.
17. Hogan, B.L.M., Barkauskas, C.E., Chapman, H.A., Epstein, J.A., Jain, R., Hsia, C.C.W., Niklason, L., Calle, E., Le, A., Randell, S.H., et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 15 (2014), 123–138.
18. Hussell, T., Bell, T.J., Alveolar macrophages: plasticity in a tissue-specific context. Nat. Rev. Immunol. 14 (2014), 81–93.
19. Kakkar, R., Hei, H., Dobner, S., Lee, R.T., Interleukin 33 as a mechanically responsive cytokine secreted by living cells. J. Biol. Chem. 287 (2012), 6941–6948.
20. Kearley, J., Silver, J.S., Sanden, C., Liu, Z., Berlin, A.A., White, N., Mori, M., Pham, T.-H., Ward, C.K., Criner, G.J., et al. Cigarette smoke silences innate lymphoid cell function and facilitates an exacerbated type I interleukin-33-dependent response to infection. Immunity 42 (2015), 566–579.
21. Kim, E.Y., Battaile, J.T., Patel, A.C., You, Y., Agapov, E., Grayson, M.H., Benoit, L.A., Byers, D.E., Alevy, Y., Tucker, J., et al. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14 (2008), 633–640.
22. Kim, H.Y., Chang, Y.J., Subramanian, S., Lee, H.H., Albacker, L.A., Matangkasombut, P., Savage, P.B., McKenzie, A.N.J., Smith, D.E., Rottman, J.B., et al. Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity. J. Allergy Clin. Immunol. 129 (2012), 216–227.e6.
23. Kopf, M., Brombacher, F., Hodgkin, P.D., Ramsay, A.J., Milbourne, E.A., Dai, W.J., Ovington, K.S., Behm, C.A., Köhler, G., Young, I.G., Matthaei, K.I., 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 (1996), 15–24.
24. Kopf, M., Schneider, C., Nobs, S.P., The development and function of lung-resident macrophages and dendritic cells. Nat. Immunol. 16 (2015), 36–44.
25. Kouzaki, H., Iijima, K., Kobayashi, T., O'Grady, S.M., Kita, H., 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 (2011), 4375–4387.
26. Lambrecht, B.N., Hammad, H., The immunology of asthma. Nat. Immunol. 16 (2015), 45–56.
27. Lamkanfi, M., Dixit, V.M., IL-33 raises alarm. Immunity 31 (2009), 5–7.
28. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
29. Lee, M.W., Odegaard, J.I., Mukundan, L., Qiu, Y., Molofsky, A.B., Nussbaum, J.C., Yun, K., Locksley, R.M., Chawla, A., Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 160 (2015), 74–87.
30. Liew, F.Y., Pitman, N.I., McInnes, I.B., Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat. Rev. Immunol. 10 (2010), 103–110.
31. Lu, J., Kang, J., Zhang, C., Zhang, X., The role of IL-33/ST2L signals in the immune cells. Immunol. Lett. 164 (2015), 11–17.
32. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M., The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25 (2004), 677–686.
33. Martin, N.T., Martin, M.U., Interleukin 33 is a guardian of barriers and a local alarmin. Nat. Immunol. 17 (2016), 122–131.
34. McKenzie, G.J., Emson, C.L., Bell, S.E., Anderson, S., Fallon, P., Zurawski, G., Murray, R., Grencis, R., McKenzie, A.N.J., Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9 (1998), 423–432.
35. Molofsky, A.B., Nussbaum, J.C., Liang, H.-E., Van Dyken, S.J., Cheng, L.E., Mohapatra, A., Chawla, A., Locksley, R.M., Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210 (2013), 535–549.
36. Molofsky, A.B., Savage, A.K., Locksley, R.M., Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity 42 (2015), 1005–1019.
37. Monin, L., Griffiths, K.L., Lam, W.Y., Gopal, R., Kang, D.D., Ahmed, M., Rajamanickam, A., Cruz-Lagunas, A., Zúñiga, J., Babu, S., et al. Helminth-induced arginase-1 exacerbates lung inflammation and disease severity in tuberculosis. J. Clin. Invest. 125 (2015), 4699–4713.
38. Monticelli, L.A., Sonnenberg, G.F., Abt, M.C., Alenghat, T., Ziegler, C.G., Doering, T.A., Angelosanto, J.M., Laidlaw, B.J., Yang, C.Y., Sathaliyawala, T., et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12 (2011), 1045–1054.
39. Mund, S.I., Stampanoni, M., Schittny, J.C., Developmental alveolarization of the mouse lung. Dev. Dyn. 237 (2008), 2108–2116.
40. Murphy, J., Summer, R., Wilson, A.A., Kotton, D.N., Fine, A., The prolonged life-span of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 38 (2008), 380–385.
41. Neill, D.R., Wong, S.H., Bellosi, A., Flynn, R.J., Daly, M., Langford, T.K., Bucks, C., Kane, C.M., Fallon, P.G., Pannell, R., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464 (2010), 1367–1370.
42. Nussbaum, J.C., Van Dyken, S.J., von Moltke, J., Cheng, L.E., Mohapatra, A., Molofsky, A.B., Thornton, E.E., Krummel, M.F., Chawla, A., Liang, H.-E., Locksley, R.M., Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502 (2013), 245–248.
43. Odegaard, J.I., Lee, M.-W., Sogawa, Y., Bertholet, A.M., Locksley, R.M., Weinberg, D.E., Kirichok, Y., Deo, R.C., Chawla, A., Perinatal licensing of thermogenesis by IL-33 and ST2. Cell 166 (2016), 841–854.
44. Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
45. Oliphant, C.J., Hwang, Y.Y., Walker, J.A., Salimi, M., Wong, S.H., Brewer, J.M., Englezakis, A., Barlow, J.L., Hams, E., Scanlon, S.T., et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41 (2014), 283–295.
46. Orr, A.W., Helmke, B.P., Blackman, B.R., Schwartz, M.A., Mechanisms of mechanotransduction. Dev. Cell 10 (2006), 11–20.
47. Peng, T., Frank, D.B., Kadzik, R.S., Morley, M.P., Rathi, K.S., Wang, T., Zhou, S., Cheng, L., Lu, M.M., Morrisey, E.E., Hedgehog actively maintains adult lung quiescence and regulates repair and regeneration. Nature 526 (2015), 578–582.
48. Pichery, M., Mirey, E., Mercier, P., Lefrancais, E., Dujardin, A., Ortega, N., Girard, J.-P., 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 (2012), 3488–3495.
49. Price, A.E., Liang, H.-E., Sullivan, B.M., Reinhardt, R.L., Eisley, C.J., Erle, D.J., Locksley, R.M., Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA 107 (2010), 11489–11494.
50. Qiu, Y., Nguyen, K.D., Odegaard, J.I., Cui, X., Tian, X., Locksley, R.M., Palmiter, R.D., Chawla, A., Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157 (2014), 1292–1308.
51. Rijavec, M., Volarevic, S., Osolnik, K., Kosnik, M., Korosec, P., Natural killer T cells in pulmonary disorders. Respir. Med. 105:Suppl 1 (2011), S20–S25.
52. Roediger, B., Weninger, W., Group 2 innate lymphoid cells in the regulation of immune responses. Adv. Immunol. 125 (2015), 111–154.
53. Salgame, P., Yap, G.S., Gause, W.C., Effect of helminth-induced immunity on infections with microbial pathogens. Nat. Immunol. 14 (2013), 1118–1126.
54. Sanada, S., Hakuno, D., Higgins, L.J., Schreiter, E.R., McKenzie, A.N.J., Lee, R.T., IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J. Clin. Invest. 117 (2007), 1538–1549.
55. Saunders, S.P., Moran, T., Floudas, A., Wurlod, F., Kaszlikowska, A., Salimi, M., Quinn, E.M., Oliphant, C.J., Núñez, G., McManus, R., et al. 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 (2016), 482–491.
56. Schlenner, S.M., Madan, V., Busch, K., Tietz, A., Läufle, C., Costa, C., Blum, C., Fehling, H.J., Rodewald, H.R., Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 32 (2010), 426–436.
57. Schliehe, C., Flynn, E.K., Vilagos, B., Richson, U., Swaminathan, S., Bosnjak, B., Bauer, L., Kandasamy, R.K., Griesshammer, I.M., Kosack, L., et al. The methyltransferase Setdb2 mediates virus-induced susceptibility to bacterial superinfection. Nat. Immunol. 16 (2015), 67–74.
58. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T.K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., et al. 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 (2005), 479–490.
59. Sharif, O., Gawish, R., Warszawska, J.M., Martins, R., Lakovits, K., Hladik, A., Doninger, B., Brunner, J., Korosec, A., Schwarzenbacher, R.E., et al. The triggering receptor expressed on myeloid cells 2 inhibits complement component 1q effector mechanisms and exerts detrimental effects during pneumococcal pneumonia. PLoS Pathog., 10, 2014, e1004167.
60. Shinkai, Y., Rathbun, G., Lam, K.P., Oltz, E.M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A.M., et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68 (1992), 855–867.
61. Talbot, T.R., Hartert, T.V., Mitchel, E., Halasa, N.B., Arbogast, P.G., Poehling, K.A., Schaffner, W., Craig, A.S., Griffin, M.R., Asthma as a risk factor for invasive pneumococcal disease. N. Engl. J. Med. 352 (2005), 2082–2090.
62. Townsend, M.J., Fallon, P.G., Matthews, D.J., Jolin, H.E., McKenzie, A.N., T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 191 (2000), 1069–1076.
63. Treutlein, B., Brownfield, D.G., Wu, A.R., Neff, N.F., Mantalas, G.L., Espinoza, F.H., Desai, T.J., Krasnow, M.A., Quake, S.R., Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509 (2014), 371–375.
64. van der Poll, T., Opal, S.M., Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374 (2009), 1543–1556.
65. von Moltke, J., Locksley, R.M., I-L-C-2 it: type 2 immunity and group 2 innate lymphoid cells in homeostasis. Curr. Opin. Immunol. 31 (2014), 58–65.
66. Warszawska, J.M., Gawish, R., Sharif, O., Sigel, S., Doninger, B., Lakovits, K., Mesteri, I., Nairz, M., Boon, L., Spiel, A., et al. Lipocalin 2 deactivates macrophages and worsens pneumococcal pneumonia outcomes. J. Clin. Invest. 123 (2013), 3363–3372.
67. Wirtz, H.R., Dobbs, L.G., The effects of mechanical forces on lung functions. Respir. Physiol. 119 (2000), 1–17.
68. Woik, N., Kroll, J., Regulation of lung development and regeneration by the vascular system. Cell. Mol. Life Sci. 72 (2015), 2709–2718.
69. Wong, S.H., Walker, J.A., Jolin, H.E., Drynan, L.F., Hams, E., Camelo, A., Barlow, J.L., Neill, D.R., Panova, V., Koch, U., et al. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 13 (2012), 229–236.