Alveolar Macrophages Are Essential for Protection from Respiratory Failure and Associated Morbidity following Influenza Virus Infection
Acute respiratory viral infections can cause severe morbidity and pneumonia in infected individuals. Alveolar macrophages and various subsets of dendritic cells have been implicated in innate immunity and induction of anti-viral T cell responses that contribute to host defense against influenza virus infection. However, their relative importance in protection from pathology and disease severity has never been compared side by side. In this report, we demonstrate that mice lacking alveolar macrophages succumb to infection with low dose influenza virus and vaccinia virus infection due to respiratory failure. In contrast, mice lacking lymphoid CD8α+ and lung CD103+ DCs survived and showed little if any differences in disease severity compared to infected wild-type mice. These results indicate that therapies supporting AM and lung function may be beneficial during severe respiratory viral infection.
Vyšlo v časopise:
Alveolar Macrophages Are Essential for Protection from Respiratory Failure and Associated Morbidity following Influenza Virus Infection. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004053
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004053
Souhrn
Acute respiratory viral infections can cause severe morbidity and pneumonia in infected individuals. Alveolar macrophages and various subsets of dendritic cells have been implicated in innate immunity and induction of anti-viral T cell responses that contribute to host defense against influenza virus infection. However, their relative importance in protection from pathology and disease severity has never been compared side by side. In this report, we demonstrate that mice lacking alveolar macrophages succumb to infection with low dose influenza virus and vaccinia virus infection due to respiratory failure. In contrast, mice lacking lymphoid CD8α+ and lung CD103+ DCs survived and showed little if any differences in disease severity compared to infected wild-type mice. These results indicate that therapies supporting AM and lung function may be beneficial during severe respiratory viral infection.
Zdroje
1. TrapnellBC, WhitsettJA (2002) Gm-CSF regulates pulmonary surfactant homeostasis and alveolar macrophage-mediated innate host defense. Annual review of physiology 64: 775–802.
2. TrapnellBC, WhitsettJA, NakataK (2003) Pulmonary alveolar proteinosis. The New England journal of medicine 349: 2527–2539.
3. SeymourJF, PresneillJJ (2002) Pulmonary alveolar proteinosis: progress in the first 44 years. American Journal of Respiratory and Critical Care Medicine 166: 215–235.
4. KitamuraT, TanakaN, WatanabeJ, Uchida, KanegasakiS, et al. (1999) Idiopathic pulmonary alveolar proteinosis as an autoimmune disease with neutralizing antibody against granulocyte/macrophage colony-stimulating factor. The Journal of experimental medicine 190: 875–880.
5. SuzukiT, SakagamiT, RubinBK, NogeeLM, WoodRE, et al. (2008) Familial pulmonary alveolar proteinosis caused by mutations in CSF2RA. The Journal of experimental medicine 205: 2703–2710.
6. DranoffG, CrawfordAD, SadelainM, ReamB, RashidA, et al. (1994) Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 264: 713–716.
7. StanleyE, LieschkeGJ, GrailD, MetcalfD, HodgsonG, et al. (1994) Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proceedings of the National Academy of Sciences of the United States of America 91: 5592–5596.
8. NishinakamuraR, NakayamaN, HirabayashiY, InoueT, AudD, et al. (1995) Mice deficient for the IL-3/GM-CSF/IL-5 beta c receptor exhibit lung pathology and impaired immune response, while beta IL3 receptor-deficient mice are normal. Immunity 2: 211–222.
9. RobbL, DrinkwaterCC, MetcalfD, LiR, KöntgenF, et al. (1995) Hematopoietic and lung abnormalities in mice with a null mutation of the common beta subunit of the receptors for granulocyte-macrophage colony-stimulating factor and interleukins 3 and 5. Proceedings of the National Academy of Sciences of the United States of America 92: 9565–9569.
10. BerclazP-Y, ZsengellérZ, ShibataY, OtakeK, StrasbaughS, et al. (2002) Endocytic internalization of adenovirus, nonspecific phagocytosis, and cytoskeletal organization are coordinately regulated in alveolar macrophages by GM-CSF and PU.1. Journal of immunology 169: 6332–6342.
11. LeVineAM, ReedJA, KurakKE, CiancioloE, WhitsettJA (1999) GM-CSF-deficient mice are susceptible to pulmonary group B streptococcal infection. The Journal of clinical investigation 103: 563–569.
12. Gonzalez-JuarreroM, HattleJM, IzzoA, Junqueira-KipnisAP, ShimTS, et al. (2005) Disruption of granulocyte macrophage-colony stimulating factor production in the lungs severely affects the ability of mice to control Mycobacterium tuberculosis infection. Journal of Leukocyte Biology 77: 914–922.
13. BallingerMN (2006) Role of Granulocyte Macrophage Colony-Stimulating Factor during Gram-Negative Lung Infection with Pseudomonas aeruginosa. American Journal of Respiratory Cell and Molecular Biology 34: 766–774.
14. PaineR, PrestonAM, WilcoxenS, JinH, SiuBB, et al. (2000) Granulocyte-macrophage colony-stimulating factor in the innate immune response to Pneumocystis carinii pneumonia in mice. Journal of immunology (Baltimore, Md : 1950) 164: 2602–2609.
15. HoltPG, OliverJ, BilykN, McMenaminC, McMenaminPG, et al. (1993) Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. The Journal of experimental medicine 177: 397–407.
16. MartinezJA, KingTE, BrownK, JenningsCA, BorishL, et al. (1997) Increased expression of the interleukin-10 gene by alveolar macrophages in interstitial lung disease. The American journal of physiology 273: L676–683.
17. MacLeanJA, XiaW, PintoCE, ZhaoL, LiuHW, et al. (1996) Sequestration of inhaled particulate antigens by lung phagocytes. A mechanism for the effective inhibition of pulmonary cell-mediated immunity. The American journal of pathology 148: 657–666.
18. KumagaiY, TakeuchiO, KatoH, KumarH, MatsuiK, et al. (2007) Alveolar Macrophages Are the Primary Interferon-α Producer in Pulmonary Infection with RNA Viruses. Immunity 27: 240–252.
19. HelftJ, ManicassamyB, GuermonprezP, HashimotoD, SilvinA, et al. (2012) Cross-presenting CD103+ dendritic cells are protected from influenza virus infection. The Journal of clinical investigation 122: 4037–4047.
20. TumpeyTM, García-SastreA, TaubenbergerJK, PaleseP, SwayneDE, et al. (2005) Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. Journal of virology 79: 14933–14944.
21. KimHM, LeeY-W, LeeK-J, KimHS, ChoSW, et al. (2008) Alveolar macrophages are indispensable for controlling influenza viruses in lungs of pigs. Journal of virology 82: 4265–4274.
22. TateMD, PickettDL, Van RooijenN, BrooksAG, ReadingPC (2010) Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. Journal of virology 84: 7569–7580.
23. HuangH, LiH, ZhouP, JuD (2010) Protective effects of recombinant human granulocyte macrophage colony stimulating factor on H1N1 influenza virus-induced pneumonia in mice. Cytokine 51: 151–157.
24. HuangF-F, BarnesPF, FengY, DonisR, ChroneosZC, et al. (2011) GM-CSF in the Lung Protects Against Lethal Influenza Infection. American Journal of Respiratory and Critical Care Medicine
25. GreterM, HelftJ, ChowA, HashimotoD, MorthaA, et al. (2012) GM-CSF Controls Nonlymphoid Tissue Dendritic Cell Homeostasis but Is Dispensable for the Differentiation of Inflammatory Dendritic Cells. Immunity 36: 1031–1046.
26. EdelsonBT, BradstreetTR, WumeshKC, HildnerK, HerzogJW, et al. (2011) Batf3-Dependent CD11blow/− Peripheral Dendritic Cells Are GM-CSF-Independent and Are Not Required for Th Cell Priming after Subcutaneous Immunization. PloS one 6: e25660.
27. UnkelB, HoegnerK, ClausenBE, Lewe-SchlosserP, BodnerJ, et al. (2012) Alveolar epithelial cells orchestrate DC function in murine viral pneumonia. The Journal of clinical investigation 122(10): 3652–64.
28. HashimotoD, ChowA, NoizatC, TeoP, BeasleyMB, et al. (2013) Tissue-Resident Macrophages Self-Maintain Locally throughout Adult Life with Minimal Contribution from Circulating Monocytes. Immunity 38: 792–804.
29. GassonJC (1991) Molecular physiology of granulocyte-macrophage colony-stimulating factor. Blood 77: 1131–1145.
30. GeurtsvanKesselCH, WillartMAM, van RijtLS, MuskensF, KoolM, et al. (2008) Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. The Journal of experimental medicine 205: 1621–1634.
31. YonaS, KimK-W, WolfY, MildnerA, VarolD, et al. (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79–91.
32. GuilliamsM, De KleerI, HenriS, PostS, VanhoutteL, et al. (2013) Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. The Journal of experimental medicine 210: 1977–1992.
33. SpriggsMK, KollerBH, SatoT, MorrisseyPJ, FanslowWC, et al. (1992) Beta 2-microglobulin-, CD8+ T-cell-deficient mice survive inoculation with high doses of vaccinia virus and exhibit altered IgG responses. Proceedings of the National Academy of Sciences of the United States of America 89: 6070–6074.
34. XuR, JohnsonAJ, LiggittD, BevanMJ (2004) Cellular and humoral immunity against vaccinia virus infection of mice. Journal of immunology 172: 6265–6271.
35. BonfieldTL, ThomassenMJ, FarverCF, AbrahamS, KolozeMT, et al. (2008) Peroxisome proliferator-activated receptor-gamma regulates the expression of alveolar macrophage macrophage colony-stimulating factor. Journal of immunology 181: 235–242.
36. EverittAR, ClareS, PertelT, JohnSP, WashRS, et al. (2012) IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484: 519–523.
37. DonnellyLE, BarnesPJ (2012) Defective phagocytosis in airways disease. Chest 141: 1055–1062.
38. VremecD, LieschkeGJ, DunnAR, RobbL, MetcalfD, et al. (1997) The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. European journal of immunology 27: 40–44.
39. BogunovicM, GinhouxF, HelftJ, ShangL, HashimotoD, et al. (2009) Origin of the lamina propria dendritic cell network. Immunity 31: 513–525.
40. KingIL, KroenkeMA, SegalBM (2010) GM-CSF-dependent, CD103+ dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. The Journal of experimental medicine 207: 953–961.
41. DeschAN, RandolphGJ, MurphyK, GautierEL, KedlRM, et al. (2011) CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. The Journal of experimental medicine 208: 1789–1797.
42. KimTS, BracialeTJ (2009) Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PloS one 4: e4204.
43. McLellanAD, KappM, EggertA, LindenC, BommhardtU, et al. (2002) Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression. Blood 99: 2084–2093.
44. ValladeauJ, Clair-MoninotV, Dezutter-DambuyantC, PinJJ, KissenpfennigA, et al. (2002) Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. Journal of immunology 168: 782–792.
45. KissenpfennigA, HenriS, DuboisB, Laplace-BuilhéC, PerrinP, et al. (2005) Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22: 643–654.
46. BelzGT, SmithCM, KleinertL, ReadingP, BrooksA, et al. (2004) Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proceedings of the National Academy of Sciences of the United States of America 101: 8670–8675.
47. Ballesteros-TatoA, LeónB, LundFE, RandallTD (2010) Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8+ T cell responses to influenza. Nature Immunology 11: 216–224.
48. HuffmanJA, HullWM, DranoffG, MulliganRC, WhitsettJA (1996) Pulmonary epithelial cell expression of GM-CSF corrects the alveolar proteinosis in GM-CSF-deficient mice. The Journal of clinical investigation 97: 649–655.
49. PribulPK, HarkerJ, WangB, WangH, TregoningJS, et al. (2008) Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. Journal of virology 82: 4441–4448.
50. KashJC, TumpeyTM, ProllSC, CarterV, PerwitasariO, et al. (2006) Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443: 578–581.
51. ManicassamyB, ManicassamyS, Belicha-VillanuevaA, PisanelliG, PulendranB, et al. (2010) Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proceedings of the National Academy of Sciences of the United States of America 107: 11531–11536.
52. WakimLM, GuptaN, MinternJD, VilladangosJA (2013) Enhanced survival of lung tissue-resident memory CD8+ T cells during infection with influenza virus due to selective expression of IFITM3. Nature Immunology 14: 238–245.
53. SondereggerI, IezziG, MaierR, SchmitzN, KurrerM, et al. (2008) GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. The Journal of experimental medicine 205: 2281–2294.
54. HildnerK, EdelsonBT, PurthaWE, DiamondM, MatsushitaH, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science (New York, NY) 322: 1097–1100.
55. ImaiT, TakakuwaR, MarchandS, DentzE, BornertJ-M, et al. (2004) Peroxisome proliferator-activated receptor gamma is required in mature white and brown adipocytes for their survival in the mouse. Proceedings of the National Academy of Sciences of the United States of America 101: 4543–4547.
56. CatonML, Smith-RaskaMR, ReizisB (2007) Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. The Journal of experimental medicine 204: 1653–1664.
57. AltmanJD, MossPA, GoulderPJ, BarouchDH, McHeyzer-WilliamsMG, et al. (1996) Phenotypic analysis of antigen-specific T lymphocytes. Science (New York, NY) 274: 94–96.
58. MoserAB, JonesDS, RaymondGV, MoserHW (1999) Plasma and red blood cell fatty acids in peroxisomal disorders. Neurochemical research 24: 187–197.
59. BachmannMF, EcabertB, KopfM (1999) Influenza virus: a novel method to assess viral and neutralizing antibody titers in vitro. Journal of immunological methods 225: 105–111.
60. van RooijenN, SandersA (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. Journal of immunological methods 174: 83–93.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 4
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- The 2010 Cholera Outbreak in Haiti: How Science Solved a Controversy
- Coxsackievirus-Induced miR-21 Disrupts Cardiomyocyte Interactions via the Downregulation of Intercalated Disk Components
- An Overview of Respiratory Syncytial Virus
- , , , Genetic Variability: Cryptic Biological Species or Clonal Near-Clades?