M1-like monocytes are a major immunological determinant of severity in previously healthy adults with life-threatening influenza

Journal of Clinical Investigation

Volumn 2, Issue 7, 2017, Pages

  Cole, Suzanne L ^a   Dunning, Jake ^b   Kok, Wai Ling ^a   Benam, Kambez Hajipouran ^a   Benlahrech, Adel ^a   Repapi, Emmanouela ^a   Martinez, Fernando O ^c   Drumright, Lydia ^b   Powell, Timothy J ^a   Bennett, Michael ^d   Elderfield, Ruth ^e   Thomas, Catherine ^f   Dong, Tao ^a   McCauley, John ^d   Liew, Foo Y ^g,h   Taylor, Stephen ^a   Zambon, Maria ^f   Barclay, Wendy ^e   Cerundolo, Vincenzo ^a   Openshaw, Peter J ^b   McMichael, Andrew J ^a   Ho, Ling Pei ^a   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f PUBLIC HEALTH ENGLAND   (United Kingdom)

^g UNIVERSITY OF GLASGOW   (United Kingdom)

^h SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85053080280     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/jci.insight.91868     Document Type: Article

References (56)

1. Influenza (Seasonal) Fact Sheet. World Health Organization. http://www.who.int/mediacentre/factsheets/fs211/en/. Updated November 2016. Accessed March 8, 2017.
2. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, et al. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med. 2009;360(25):2605-2615.
3. Gómez-Gómez A, et al. Severe pneumonia associated with pandemic (H1N1) 2009 outbreak, San Luis Potosí, Mexico. Emerging Infect Dis. 2010;16(1):27-34.
4. Louie JK, et al. Factors associated with death or hospitalization due to pandemic 2009 influenza A(H1N1) infection in California. JAMA. 2009;302(17):1896-1902.
5. La Gruta NL, Kedzierska K, Stambas J, Doherty PC. A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol. 2007;85(2):85-92.
6. Van Reeth K. Cytokines in the pathogenesis of influenza. Vet Microbiol. 2000;74(1-2):109-116.
7. Iwasaki A, Pillai PS. Innate immunity to influenza virus infection. Nat Rev Immunol. 2014;14(5):315-328.
8. Cole SL, Ho LP. Contribution of innate immune cells to pathogenesis of severe influenza virus infection. Clin Sci. 2017;131(4):269-283.
9. Abdul-Careem MF, et al. Critical role of natural killer cells in lung immunopathology during influenza infection in mice. J Infect Dis. 2012;206(2):167-177.
10. Duan S, Thomas PG. Balancing immune protection and immune pathology by CD8(+) T-cell responses to influenza infection. Front Immunol. 2016;7:25.
11. Almansa R, et al. Imbalanced pro- and anti-Th17 responses (IL-17/granulocyte colony-stimulating factor) predict fatal outcome in 2009 pandemic influenza. Crit Care. 2011;15(5):448.
12. de Jong MD, et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med. 2006;12(10):1203-1207.
13. Everitt AR, et al. IFITM3 restricts the morbidity and mortality associated with influenza. Nature. 2012;484(7395):519-523.
14. Elderfield RA, et al. Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza virus in humans in the United Kingdom. J Virol. 2014;88(22):13269-13283.
15. Brandau S, et al. Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J Leukoc Biol. 2011;89(2):311-317.
16. Bowers NL, Helton ES, Huijbregts RP, Goepfert PA, Heath SL, Hel Z. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog. 2014;10(3):e1003993.
17. Carmona-Rivera C, Kaplan MJ. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin Immunopathol. 2013;35(4):455-463.
18. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol. 2011;11(11):762-774.
19. 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. 2004;25(12):677-686.
20. Martinez FO, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood. 2013;121(9):e57-e69.
21. Murray PJ, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14-20.
22. Kok WL, et al. Pivotal Advance: Invariant NKT cells reduce accumulation of inflammatory monocytes in the lungs and decrease immune-pathology during severe influenza A virus infection. J Leukoc Biol. 2012;91(3):357-368.
23. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol. 2014;14(2):81-93.
24. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci. 2009;29(43):13435-13444.
25. Kadl A, et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res. 2010;107(6):737-746.
26. 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(4):503-510.
27. Cumulative number of confirmed human cases for avian influenza A (H5N1) reported to WHO. World Health Organization. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/. Accessed March 8, 2017.
28. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009;10:48.
29. Subramanian A, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-15550.
30. Beigel JH, et al. Avian influenza A (H5N1) infection in humans. N Engl J Med. 2005;353(13):1374-1385.
31. Klein SL, Pekosz A, Passaretti C, Anker M, Olukoya P. Sex, gender influenza in achieving gender equality health equity. Geneva, Switzerland; World Health Organization(42): 2010.
32. 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(4):2562-2572.
33. Perrone LA, Plowden JK, García-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(8):e1000115.
34. Josset L, et al. Implication of inflammatory macrophages, nuclear receptors, and interferon regulatory factors in increased virulence of pandemic 2009 H1N1 influenza A virus after host adaptation. J Virol. 2012;86(13):7192-7206.
35. 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(6):1951-1959.
36. Herold 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(13):3065-3077.
37. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol. 2013;191(3):1250-1259.
38. Wang J, et al. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat Commun. 2013;4:2106.
39. Inagaki Y, Yamagishi S, Amano S, Okamoto T, Koga K, Makita Z. Interferon-gamma-induced apoptosis and activation of THP-1 macrophages. Life Sci. 2002;71(21):2499-2508.
40. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13.
41. De Santo C, et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J Clin Invest. 2008;118(12):4036-4048.
42. Cloke T, Munder M, Taylor G, Müller I, Kropf P. Characterization of a novel population of low-density granulocytes associated with disease severity in HIV-1 infection. PLoS ONE. 2012;7(11):e48939.
43. Knight JS, Kaplan MJ. Lupus neutrophils: 'NET' gain in understanding lupus pathogenesis. Curr Opin Rheumatol. 2012;24(5):441-450.
44. Nyquist PA, Winkler CA, McKenzie LM, Yanek LR, Becker LC, Becker DM. Single nucleotide polymorphisms in monocyte chemoattractant protein-1 and its receptor act synergistically to increase the risk of carotid atherosclerosis. Cerebrovasc Dis. 2009;28(2):124-130.
45. Zhang YH, et al. Interferon-induced transmembrane protein-3 genetic variant rs12252-C is associated with severe influenza in Chinese individuals. Nat Commun. 2013;4:1418.
46. García-Ramírez RA, Ramírez-Venegas A, Quintana-Carrillo R, Camarena ÁE, Falfán-Valencia R, Mejía-Aranguré JM. TNF, IL6, and IL1B Polymorphisms Are Associated with Severe Influenza A (H1N1) Virus Infection in the Mexican Population. PLoS ONE. 2015;10(12):e0144832.
47. Aldridge JR, et al. TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci USA. 2009;106(13):5306-5311.
48. Oshansky CM, 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(4):449-462.
49. Hume DA, MacDonald KP. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood. 2012;119(8):1810-1820.
50. Börgeson E, et al. Lipoxin A4 attenuates obesity-induced adipose inflammation and associated liver and kidney disease. Cell Metab. 2015;22(1):125-137.
51. Shirey KA, et al. Role of the lipoxygenase pathway in RSV-induced alternatively activated macrophages leading to resolution of lung pathology. Mucosal Immunol. 2014;7(3):549-557.
52. Wolfs IM, et al. Reprogramming macrophages to an anti-inflammatory phenotype by helminth antigens reduces murine atherosclerosis. FASEB J. 2014;28(1):288-299.
53. Salomon R, Hoffmann E, Webster RG. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc Natl Acad Sci USA. 2007;104(30):12479-12481.
54. Denney L, et al. Reduction of natural killer but not effector CD8 T lymphocytes in three consecutive cases of severe/lethal H1N1/09 influenza A virus infection. PLoS ONE. 2010;5(5):e10675.
55. Powell TJ, et al. Examination of influenza specific T cell responses after influenza virus challenge in individuals vaccinated with MVA-NP+M1 vaccine. PLoS ONE. 2013;8(5):e62778.
56. Geiss GK, et al. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci USA. 2002;99(16):10736-10741.