The contributions of lung macrophage and monocyte heterogeneity to influenza pathogenesis

Immunology and Cell Biology

Volumn 95, Issue 3, 2017, Pages 225-235

  Duan, Mubing ^a   Hibbs, Margaret L ^b   Chen, Weisan ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PNEUMONIA; CELL HETEROGENEITY; GENE TARGETING; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; INFLUENZA; INFLUENZA A VIRUS; LUNG ALVEOLUS MACROPHAGE; MONOCYTE; NONHUMAN; REVIEW; VIRAL CLEARANCE; VIRUS DETECTION; VIRUS PNEUMONIA; ANIMAL; LUNG; MACROPHAGE; MICROBIOLOGY; PATHOLOGY; PNEUMONIA; VIROLOGY;

ANIMALS; HUMANS; INFLUENZA, HUMAN; LUNG; MACROPHAGES; MONOCYTES; PNEUMONIA; TRANSCRIPTION, GENETIC;

EID: 84991737339     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.97     Document Type: Review

References (123)

1. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013; 38: 792-804.
2. Hoeffel G, Chen J, Lavin Y, Low D, Almeida FF, See P et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 2015; 42: 665-678.
3. Schulz C, Perdiguero EG, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012; 336: 86-90.
4. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013; 38: 79-91.
5. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I et al. Transcriptomebased network analysis reveals a spectrum model of human macrophage activation. Immunity 2014; 40: 274-288.
6. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 2012; 13: 1118-1128.
7. Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med 2013; 210: 1977-1992.
8. Schneider C, Nobs SP, Kurrer M, Rehrauer H, Thiele C, Kopf M. Induction of the nuclear receptor PPAR-gamma by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat Immunol 2014; 15: 1026-1037.
9. Epelman S, Lavine KJ, Beaudin AE, Sojka DK, Carrero JA, Calderon B et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014; 40: 91-104.
10. Sheng J, Ruedl C, Karjalainen K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 2015; 43: 382-393.
11. Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol 2014; 15: 929-937.
12. Hagemeyer N, Kierdorf K, Frenzel K, Xue J, Ringelhan M, Abdullah Z et al. Transcriptome-based profiling of yolk sac-derived macrophages reveals a role for Irf8 in macrophage maturation. EMBO J 2016; 35: 1730-1744.
13. Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 2015; 518: 547-551.
14. Ginhoux F, Guilliams M. Tissue-resident macrophage ontogeny and homeostasis. Immunity 2016; 44: 439-449.
15. Scott CL, Zheng F, De Baetselier P, Martens L, Saeys Y, De Prijck S et al. Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat Commun 2016; 7: 10321.
16. Gibbings SL, Goyal R, Desch AN, Leach SM, Prabagar M, Atif SM et al. Transcriptome analysis highlights the conserved difference between embryonic and postnatal-derived alveolar macrophages. Blood 2015; 126: 1357-1366.
17. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 2014; 159: 1312-1326.
18. van de Laar L, Saelens W, De Prijck S, Martens L, Scott CL, Van Isterdael G et al. Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 2016; 44: 755-768.
19. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F et al. Epigenetic programming of monocyte-To-macrophage differentiation and trained innate immunity. Science 2014; 345: 1251086.
20. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-To-macrophage differentiation and polarization: new molecules and patterns of gene expression. Journal of immunology 2006; 177: 7303-7311.
21. Desch AN, Gibbings SL, Goyal R, Kolde R, Bednarek J, Bruno T et al. Flow cytometric analysis of mononuclear phagocytes in nondiseased human lung and lung-draining lymph nodes. Am J Respir Crit Care Med 2016; 193: 614-626.
22. Maisonnasse P, Bouguyon E, Piton G, Ezquerra A, Urien C, Deloizy C et al. The respiratory DC/macrophage network at steady-state and upon influenza infection in the swine biomedical model. Mucosal Immunol 2015; 9: 835-849.
23. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 2013; 49: 503-510.
24. Lehnert BE, Valdez YE, Sebring RJ, Lehnert NM, Saunders GC, Steinkamp JA. Airway intra-luminal macrophages: evidence of origin and comparisons to alveolar macrophages. Am J Respir Cell Mol Biol 1990; 3: 377-391.
25. Westphalen K, Gusarova GA, Islam MN, Subramanian M, Cohen TS, Prince AS et al. Sessile alveolar macrophages communicate with alveolar epithelium to modulate immunity. Nature 2014; 506: 503-506.
26. Duan M, Li WC, Vlahos R, Maxwell MJ, Anderson GP, Hibbs ML. Distinct macrophage subpopulations characterize acute infection and chronic inflammatory lung disease. J Immunol 2012; 189: 946-955.
27. Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW et al. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol 2006; 35: 227-235.
28. Dranoff G, Crawford AD, Sadelain M, Ream B, Rashid A, Bronson RT et al. Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 1994; 264: 713-716.
29. Stanley E, Lieschke GJ, Grail D, Metcalf D, Hodgson G, Gall JAM et al. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc Natl Acad Sci USA 1994; 91: 5592-5596.
30. Ikegami M, Hull WM, Yoshida M, Wert SE, Whitsett JA. SP-D and GM-CSF regulate surfactant homeostasis via distinct mechanisms. Am J Physiol Lung Cell Mol Physiol 2001; 281: L697-L703.
31. Gautier EL, Chow A, Spanbroek R, Marcelin G, Greter M, Jakubzick C et al. Systemic analysis of PPAR gamma in mouse macrophage populations reveals marked diversity in expression with critical roles in resolution of inflammation and airway immunity. J Immunol 2012; 189: 2614-2624.
32. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK. The peroxisome proliferator-Activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998; 391: 79-82.
33. Malur A, Mccoy AJ, Arce S, Barna BP, Kavuru MS, Malur AG et al. Deletion of PPAR gamma in alveolar macrophages is associated with a Th-1 pulmonary inflammatory response. J Immunol 2009; 182: 5816-5822.
34. Lu Q, Yokoyama CC, Williams JW, Baldridge MT, Jin X, DesRochers B et al. Homeostatic control of innate lung inflammation by Vici syndrome gene Epg5 and additional autophagy genes promotes influenza pathogenesis. Cell Host Microbe 2016; 19: 102-113.
35. Kanayama M, He YW, Shinohara ML. The lung is protected from spontaneous inflammation by autophagy in myeloid cells. J Immunol 2015; 194: 5465-5471.
36. Snelgrove RJ, Goulding J, Didierlaurent AM, Lyonga D, Vekaria S, Edwards L et al. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat Immunol 2008; 9: 1074-1083.
37. Meliopoulos VA, Van de Velde LA, Van de Velde NC, Karlsson EA, Neale G, Vogel P et al. An epithelial integrin regulates the amplitude of protective lung interferon responses against multiple respiratory pathogens. PLoS Pathog 2016; 12: e1005804.
38. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 2014; 14: 81-93.
39. Thepen T, Van Rooijen N, Kraal G. Alveolar macrophage elimination in vivo is associated with an increase in pulmonary immune response in mice. J Exp Med 1989; 170: 499-509.
40. Lauzon-Joset JF, Marsolais D, Langlois A, Bissonnette EY. Dysregulation of alveolar macrophages unleashes dendritic cell-mediated mechanisms of allergic airway inflammation. Mucosal Immunol 2014; 7: 155-164.
41. Sharma SK, Chintala NK, Vadrevu SK, Patel J, Karbowniczek M, Markiewski MM. Pulmonary alveolar macrophages contribute to the premetastatic niche by suppressing antitumor T cell responses in the lungs. J Immunol 2015; 194: 5529-5538.
42. Knapp S, Leemans JC, Florquin S, Branger J, Maris NA, Pater J et al. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am J Respir Crit Care Med 2003; 167: 171-179.
43. Schneider C, Nobs SP, Heer AK, Kurrer M, Klinke G, van Rooijen N et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog 2014; 10: e1004053.
44. Bang BR, Chun E, Shim EJ, Lee HS, Lee SY, Cho SH et al. Alveolar macrophages modulate allergic inflammation in a murine model of asthma. Exp Mol Med 2011; 43: 275-280.
45. Soroosh P, Doherty TA, Duan W, Mehta AK, Choi H, Adams YF et al. Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J Exp Med 2013; 210: 775-788.
46. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007; 8: 1086-1094.
47. Bedoret D, Wallemacq H, Marichal T, Desmet C, Quesada Calvo F, Henry E et al. Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J Clin Invest 2009; 119: 3723-3738.
48. Landsman L, Jung S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J Immunol 2007; 179: 3488-3494.
49. Cai Y, Sugimoto C, Arainga M, Alvarez X, Didier ES, Kuroda MJ. In vivo characterization of alveolar and interstitial lung macrophages in rhesus macaques: implications for understanding lung disease in humans. J Immunol 2014; 192: 2821-2829.
50. Srivastava M, Jung S, Wilhelm J, Fink L, Buhling F, Welte T et al. The inflammatory versus constitutive trafficking of mononuclear phagocytes into the alveolar space of mice is associated with drastic changes in their gene expression profiles. J Immunol 2005; 175: 1884-1893.
51. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19: 71-82.
52. Carlin LM, Stamatiades EG, Auffray C, Hanna RN, Glover L, Vizcay-Barrena G et al. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell 2013; 153: 362-375.
53. Landsman L, Varol C, Jung S. Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol 2007; 178: 2000-2007.
54. Winter C, Taut K, Srivastava M, Langer F, Mack M, Briles DE et al. Lung-specific overexpression of CC chemokine ligand (CCL) 2 enhances the host defense to Streptococcus pneumoniae infection in mice: role of the CCL2-CCR2 axis. J Immunol 2007; 178: 5828-5838.
55. Lin KL, Suzuki Y, Nakano H, Ramsburg E, Gunn MD. CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J Immunol 2008; 180: 2562-2572.
56. Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 2013; 38: 322-335.
57. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003; 19: 59-70.
58. Randolph GJ, Sanchez-Schmitz G, Liebman RM, Schakel K. The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J Exp Med 2002; 196: 517-527.
59. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. Avian flu: influenza virus receptors in the human airway. Nature 2006; 440: 435-436.
60. Thompson CI, Barclay WS, Zambon MC, Pickles RJ. Infection of human airway epithelium by human and avian strains of influenza a virus. J Virol 2006; 80: 8060-8068.
61. Yu WC, Chan RW, Wang J, Travanty EA, Nicholls JM, Peiris JS et al. Viral replication and innate host responses in primary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J Virol 2011; 85: 6844-6855.
62. Ng WC, Liong S, Tate MD, Irimura T, Denda-Nagai K, Brooks AG et al. The macrophage galactose-Type lectin can function as an attachment and entry receptor for influenza virus. J Virol 2014; 88: 1659-1672.
63. Shi Y, Wu Y, Zhang W, Qi J, Gao GF. Enabling the 'host jump': structural determinants of receptor-binding specificity in influenza A viruses. Nat Rev Microbiol 2014; 12: 822-831.
64. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, Chignard M et al. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 2007; 178: 3368-3372.
65. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA 2004; 101: 5598-5603.
66. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004; 303: 1529-1531.
67. Demaria O, Pagni PP, Traub S, de Gassart A, Branzk N, Murphy AJ et al. TLR8 deficiency leads to autoimmunity in mice. J Clin Invest 2010; 120: 3651-3662.
68. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006; 314: 997-1001.
69. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, Taxman DJ et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009; 30: 556-565.
70. Ichinohe T, Pang IK, Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 2010; 11: 404-410.
71. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003; 301: 640-643.
72. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003; 4: 161-167.
73. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005; 122: 669-682.
74. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H et al. IPS-1, an adaptor triggering RIG-I-And Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-988.
75. Wang L, Manji GA, Grenier JM, Al-Garawi A, Merriam S, Lora JM et al. PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing. J Biol Chem 2002; 277: 29874-29880.
76. Pothlichet J, Meunier I, Davis BK, Ting JP, Skamene E, von Messling V et al. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 2013; 9: e1003256.
77. Thomas PG, Dash P, Aldridge JR Jr, Ellebedy AH, Reynolds C, Funk AJ et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 2009; 30: 566-575.
78. Iwasaki A, Pillai PS. Innate immunity to influenza virus infection. Nat Rev Immunol 2014; 14: 315-328.
79. Seo SU, Kwon HJ, Song JH, Byun YH, Seong BL, Kawai T et al. MyD88 signaling is indispensable for primary influenza A virus infection but dispensable for secondary infection. J Virol 2010; 84: 12713-12722.
80. Bradley LM, Douglass MF, Chatterjee D, Akira S, Baaten BJ. Matrix metalloprotease 9 mediates neutrophil migration into the airways in response to influenza virus-induced toll-like receptor signaling. PLoS Pathog 2012; 8: e1002641.
81. Teijaro JR, Walsh KB, Rice S, Rosen H, Oldstone MB. Mapping the innate signaling cascade essential for cytokine storm during influenza virus infection. Proc Natl Acad Sci USA 2014; 111: 3799-3804.
82. Koyama S, Ishii KJ, Kumar H, Tanimoto T, Coban C, Uematsu S et al. Differential role of TLR-And RLR-signaling in the immune responses to influenza A virus infection and vaccination. J Immunol 2007; 179: 4711-4720.
83. Pillai PS, Molony RD, Martinod K, Dong H, Pang IK, Tal MC et al. Mx1 reveals innate pathways to antiviral resistance and lethal influenza disease. Science 2016; 352: 463-466.
84. Kumagai Y, Takeuchi O, Kato H, Kumar H, Matsui K, Morii E et al. Alveolar macrophages are the primary interferon-Alpha producer in pulmonary infection with RNA viruses. Immunity 2007; 27: 240-252.
85. Goritzka M, Makris S, Kausar F, Durant LR, Pereira C, Kumagai Y et al. Alveolar macrophage-derived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J Exp Med 2015; 212: 699-714.
86. Tate MD, Ioannidis LJ, Croker B, Brown LE, Brooks AG, Reading PC. The role of neutrophils during mild and severe influenza virus infections of mice. PLoS ONE 2011; 6: e17618.
87. Seo SU, Kwon HJ, Ko HJ, Byun YH, Seong BL, Uematsu S et al. Type I interferon signaling regulates Ly6C(hi) monocytes and neutrophils during acute viral pneumonia in mice. PLoS Pathog 2011; 7: e1001304.
88. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. Plos Pathog 2008; 4: e1000115.
89. Brandes M, Klauschen F, Kuchen S, Germain RN. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 2013; 154: 197-212.
90. Eash KJ, Greenbaum AM, Gopalan PK, Link DC. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest 2010; 120: 2423-2431.
91. Wareing MD, Shea AL, Inglis CA, Dias PB, Sarawar SR. CXCR2 is required for neutrophil recruitment to the lung during influenza virus infection, but is not essential for viral clearance. Viral Immunol 2007; 20: 369-378.
92. Smith JA. Neutrophils, host-defense, and inflammation-A double-edged-sword. J Leukoc Biol 1994; 56: 672-686.
93. Lim K, Hyun YM, Lambert-Emo K, Capece T, Bae S, Miller R et al. Neutrophil trails guide influenza-specific CD8(+) T cells in the airways. Science 2015; 349: Aaa4352.
94. Aldridge Jr. J.R., Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, Franks J et al. TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci USA 2009; 106: 5306-5311.
95. Cao WP, Taylor AK, Biber RE, Davis WG, Kim JH, Reber AJ et al. Rapid differentiation of monocytes into type I IFN-producing myeloid dendritic cells as an antiviral strategy against influenza virus infection. J Immunol 2012; 189: 2257-2265.
96. Cline TD, Karlsson EA, Seufzer BJ, Schultz-Cherry S. The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J Virol 2013; 87: 1411-1419.
97. Londrigan SL, Short KR, Ma J, Gillespie L, Rockman SP, Brooks AG et al. Infection of mouse macrophages by seasonal influenza viruses can be restricted at the level of virus entry and at a late stage in the virus life cycle. J Virol 2015; 89: 12319-12329.
98. Levy O, Zarember KA, Roy RM, Cywes C, Godowski PJ, Wessels MR. Selective impairment of TLR-mediated innate immunity in human newborns: neonatal blood plasma reduces monocyte TNF-Alpha induction by bacterial lipopeptides, lipopolysaccharide, and imiquimod, but preserves the response to R-848. J Immunol 2004; 173: 4627-4634.
99. Marr N, Wang TI, Kam SH, Hu YS, Sharma AA, Lam A et al. Attenuation of respiratory syncytial virus-induced and RIG-I-dependent type I IFN responses in human neonates and very young children. J Immunol 2014; 192: 948-957.
100. Oshansky CM, Gartland AJ, Wong SS, Jeevan T, Wang D, Roddam PL et al. Mucosal immune responses predict clinical outcomes during influenza infection independently of age and viral load. Am J Respir Crit Care Med 2014; 189: 449-462.
101. Vlahos R, Bozinovski S. Role of alveolar macrophages in chronic obstructive pulmonary disease. Front Immunol 2014; 5: 435.
102. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006; 12: 1203-1207.
103. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF et al. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: A mechanism for the unusual severity of human disease? Lancet 2002; 360: 1831-1837.
104. Tate MD, Pickett DL, van Rooijen N, Brooks AG, Reading PC. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 2010; 84: 7569-7580.
105. Friesenhagen J, Boergeling Y, Hrincius E, Ludwig S, Roth J, Viemann D. Highly pathogenic avian influenza viruses inhibit effective immune responses of human blood-derived macrophages. J Leukocyte Biol 2012; 92: 11-20.
106. Tyner JW, Uchida O, Kajiwara N, Kim EY, Patel AC, O'Sullivan MP et al. CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection. Nat Med 2005; 11: 1180-1187.
107. Dawson TC, Beck MA, Kuziel WA, Henderson F, Maeda N. Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 2000; 156: 1951-1959.
108. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G et al. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 2008; 133: 235-249.
109. van Riel D, Leijten LM, van der Eerden M, Hoogsteden HC, Boven LA, Lambrecht BN et al. Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-Alpha induction. PLoS Pathog 2011; 7: e1002099.
110. Herold S, Steinmueller M, von Wulffen W, Cakarova L, Pinto R, Pleschka S et al. Lung epithelial apoptosis in influenza virus pneumonia: The role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 2008; 205: 3065-3077.
111. Sun J, Madan R, Karp CL, Braciale TJ. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med 2009; 15: 277-284.
112. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198: 962-970.
113. Jamieson AM, Pasman L, Yu S, Gamradt P, Homer RJ, Decker T et al. Role of tissue protection in lethal respiratory viral-bacterial coinfection. Science 2013; 340: 1230-1234.
114. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 2013; 191: 1250-1259.
115. Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A, Liu SY et al. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 2009; 119: 1910-1920.
116. Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferongamma during recovery from influenza infection. Nat Med 2008; 14: 558-564.
117. Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, Bebien M et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 2008; 205: 323-329.
118. Freire-de-Lima CG, Xiao YQ, Gardai SJ, Bratton DL, Schiemann WP, Henson PM. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem 2006; 281: 38376-38384.
119. Huynh ML, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 2002; 109: 41-50.
120. Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, Jakubzick C et al. Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 2011; 184: 547-560.
121. Goulding J, Godlee A, Vekaria S, Hilty M, Snelgrove R, Hussell T. Lowering the threshold of lung innate immune cell activation alters susceptibility to secondary bacterial superinfection. J Infect Dis 2011; 204: 1086-1094.
122. Kearns MT, Barthel L, Bednarek JM, Yunt ZX, Henson PM, Janssen WJ. Fas ligand-expressing lymphocytes enhance alveolar macrophage apoptosis in the resolution of acute pulmonary inflammation. Am J Physiol Lung Cell Mol Physiol 2014; 307: L62-L70.
123. Morris DG, Huang X, Kaminski N, Wang Y, Shapiro SD, Dolganov G et al. Loss of integrin alpha(v)beta6-mediated TGF-beta activation causes Mmp12-dependent emphysema. Nature 2003; 422: 169-173.