Activation of A1-adenosine receptors promotes leukocyte recruitment to the lung and attenuates acute lung injury in mice infected with influenza A/WSN/33 (H1N1) virus

Journal of Virology

Volumn 88, Issue 17, 2014, Pages 10214-10227

  Aeffner, Famke ^a,b   Woods, Parker S ^a   Davis, Ian C ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Flagship Biosciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A1 RECEPTOR;

ACUTE LUNG INJURY; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL MOTION; DEFICIENCY; DISEASE MODEL; IMMUNOLOGY; INFLUENZA VIRUS A H1N1; KNOCKOUT MOUSE; LEUKOCYTE; LUNG; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY;

ACUTE LUNG INJURY; ADOPTIVE TRANSFER; ANIMALS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; INFLUENZA A VIRUS, H1N1 SUBTYPE; LEUKOCYTES; LUNG; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTOR, ADENOSINE A1;

EID: 84906067110     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01068-14     Document Type: Article

References (85)

1. Clark N, Lynch J. 2011. Influenza: epidemiology, clinical features, therapy, and prevention. Semin. Respir. Crit. Care Med. 32:373-392. http://dx.doi.org/10.1055/s-0031-1283278.
2. Taubenberger JK, Morens DM. 2006. 1918 influenza: the mother of all pandemics. Emerg. Infect. Dis. 12:15-22. http://dx.doi.org/10.3201/eid1209.050979, http://dx.doi.org/10.3201/eid1201.050979.
3. Girard MP, Tam JS, Assossou OM, Kieny MP. 2010. The 2009 A (H1N1) influenza virus pandemic: a review. Vaccine 28:4895-4902. http://dx.doi.org/10.1016/j.vaccine.2010.05.031.
4. Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM, Kroneman M, Van Kerkhove MD, Mounts AW, Paget WJ, the GLa Collaborating Team MOR. 2013. Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study. PLoS Med. 10:e1001558. http://dx.doi.org/10.1371/journal.pmed.1001558.
5. Burnstock G, Brouns I, Adriaensen D, Timmermans JP. 2012. Purinergic signaling in the airways. Pharmacol. Rev. 64:834-868. http://dx.doi.org/10.1124/pr.111.005389.
6. Wolk KE, Lazarowski ER, Traylor ZP, Yu EN, Jewell NA, Durbin RK, Durbin JE, Davis IC. 2008. Influenza A virus inhibits alveolar fluid clearance in BALB/c mice. Am. J. Respir. Crit. Care Med. 178:969-976. http://dx.doi.org/10.1164/rccm.200803-455OC.
7. Aeffner F, Bratasz A, Flaño E, Powell KA, Davis IC. 2012. Post-infection A77-1726 treatment improves cardiopulmonary function in H1N1 influenza-infected mice. Am. J. Respir. Cell Mol. Biol. 47:543-551. http://dx.doi.org/10.1165/rcmb.2012-0112OC.
8. Kreindler JL, Shapiro SD. 2007. Lung turns to AA (adenosine analogues) to dry out. Nat. Med. 13:406-408. http://dx.doi.org/10.1038/nm0407-406.
9. Hasko G, Cronstein BN. 2004. Adenosine: an endogenous regulator of innate immunity. Trends Immunol. 25:33-39. http://dx.doi.org/10.1016/j.it.2003.11.003.
10. Yegutkin GG. 2008. Nucleotide-and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783:673-694. http://dx.doi.org/10.1016/j.bbamcr.2008.01.024.
11. Thompson LF, Eltzschig HK, Ibla JC, Van De Wiele CJ, Resta R, Morote-Garcia JC, Colgan SP. 2004. Crucial role for ecto-5=-nucleotidase (CD73) in vascular leakage during hypoxia. J. Exp. Med. 200:1395-1405. http://dx.doi.org/10.1084/jem.20040915.
12. Schepp C, Reutershan J. 2008. Bench-to-bedside review: Adenosine receptors-promising targets in acute lung injury? Crit. Care 12:226. http://dx.doi.org/10.1186/cc6990.
13. Factor P, Mutlu GM, Chen L, Mohameed J, Akhmedov AT, Meng FJ, Jilling T, Lewis ER, Johnson MD, Xu A, Kass D, Martino JM, Bellmeyer A, Albazi JS, Emala C, Lee HT, Dobbs LG, Matalon S. 2007. Adenosine regulation of alveolar fluid clearance. Proc. Natl. Acad. Sci. U. S. A. 104: 4083-4088. http://dx.doi.org/10.1073/pnas.0601117104.
14. Haskó G, Pacher P. 2012. Regulation of macrophage function by adenosine. Arterioscler. Thromb. Vasc. Biol. 32:865-869. http://dx.doi.org/10.1161/ATVBAHA.111.226852.
15. Barletta KE, Ley K, Mehrad B. 2012. Regulation of neutrophil function by adenosine. Arterioscler. Thromb. Vasc. Biol. 32:856-864. http://dx.doi.org/10.1161/ATVBAHA.111.226845.
16. Corriden R, Insel P. 2012. New insights regarding the regulation of chemotaxis by nucleotides, adenosine, and their receptors. Purinergic Signal. 8:587-598. http://dx.doi.org/10.1007/s11302-012-9311-x.
17. Neely CF, Jin J, Keith IM. 1997. A1-adenosine receptor antagonists block endotoxin-induced lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 272:L353-L361.
18. Abraham E. 2003. Neutrophils and acute lung injury. Crit. Care Med. 31:S195-S199. http://dx.doi.org/10.1097/01.CCM.0000057843.47705.E8.
19. Perrone LA, Plowden JK, García-Sastre A, Katz JM, Tumpey TM. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115. http://dx.doi.org/10.1371/journal.ppat.1000115.
20. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, García-Sastre A, Tolnay AE, Albrecht R, Pyles JA, Olson PH, Aicher LD, Rosenzweig ER, Murali-Krishna K, Clark EA, Kotur MS, Fornek JL, Proll S, Palermo RE, Sabourin CL, Katze MG. 2009. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. U. S. A. 106:3455-3460. http://dx.doi.org/10.1073/pnas.0813234106.
21. Sun D, Samuelson LC, Yang T, Huang Y, Paliege A, Saunders T, Briggs J, Schnermann J. 2001. Mediation of tubuloglomerular feedback by adenosine: evidence from mice lacking adenosine 1 receptors. Proc. Natl. Acad. Sci. U. S. A. 98:9983-9988. http://dx.doi.org/10.1073/pnas.171317998.
22. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
23. García-Sastre A, Durbin RK, Zheng H, Palese P, Gertner R, Levy DE, Durbin JE. 1998. The role of interferon in influenza virus tissue tropism. J. Virol. 72:8550-8558.
24. Aeffner F, Abdulrahman B, Hickman-Davis JM, Janssen PM, Amer A, Bedwell DM, Sorscher EJ, Davis IC. 2013. Heterozygosity for the F508del mutation in the cystic fibrosis transmembrane conductance regulator anion channel attenuates influenza severity. J. Infect. Dis. 208:780-789. http://dx.doi.org/10.1093/infdis/jit251.
25. Dada L, Gonzalez AR, Urich D, Soberanes S, Manghi TS, Chiarella SE, Chandel NS, Budinger GRS, Mutlu GM. 2012. Alcohol worsens acute lung injury by inhibiting alveolar sodium transport through the adenosine A1 receptor. PLoS One 7:e30448. http://dx.doi.org/10.1371/journal.pone.0030448.
26. Davis IC, Sullender WM, Hickman-Davis JM, Lindsey JR, Matalon S. 2004. Nucleotide-mediated inhibition of alveolar fluid clearance in BALB/c mice after respiratory syncytial virus infection. Am. J. Physiol. Lung Cell Mol. Physiol. 286:L112-L120. http://dx.doi.org/10.1152/ajplung.00218.2003.
27. Irvin CG, Bates JH. 2003. Measuring the lung function in the mouse: the challenge of size. Respir. Res. 4:4-13. http://dx.doi.org/10.1186/rr199.
28. Traylor ZP, Aeffner F, Davis IC. 2013. Influenza A H1N1 induces declines in alveolar gas exchange in mice consistent with rapid post-infection progression from acute lung injury to ARDS. Influenza Other Respir. Viruses 7:472-479. http://dx.doi.org/10.1111/j.1750-2659.2012.00414.x.
29. Davis IC, Xu A, Gao Z, Hickman-Davis JM, Factor P, Sullender WM, Matalon S. 2007. Respiratory syncytial virus induces insensitivity to β-adrenergic agonists in mouse lung epithelium in vivo. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L281-L289. http://dx.doi.org/10.1152/ajplung.00458.2006.
30. Grenz A, Zhang H, Weingart J, von Wietersheim S, Eckle T, Schnermann J, Kohle C, Kloor D, Gleiter CH, Vallon V, Eltzschig HK, Osswald H. 2007. Lack of effect of extracellular adenosine generation and signaling on renal erythropoietin secretion during hypoxia. Am. J. Physiol. Renal Physiol. 293:F1501-F1511. http://dx.doi.org/10.1152/ajprenal.00243.2007.
31. The ARDS Definition Task Force, Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, Camporota L, Slutsky AS. 2012. Acute respiratory distress syndrome: the Berlin Definition. JAMA 307:2526-2533. http://dx.doi.org/10.1001/jama.2012.5669.
32. Zhou Y, Schneider DJ, Blackburn MR. 2009. Adenosine signaling and the regulation of chronic lung disease. Pharmacol. Ther. 123:105-116. http://dx.doi.org/10.1016/j.pharmthera.2009.04.003.
33. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM, the Acute Lung Injury in Animals Study Group. 2011. An official American Thoracic Society Workshop Report: features and measurements of experimental acute lung injury in animals. Am. J. Respir. Cell Mol. Biol. 44:725-738. http://dx.doi.org/10.1165/rcmb.2009-0210ST.
34. Talukder MA, Morrison RR, Ledent C, Mustafa SJ. 2003. Endogenous adenosine increases coronary flow by activation of both A2A and A2B receptors in mice. J. Cardiovasc. Pharmacol. 41:562-570. http://dx.doi.org/10.1097/00005344-200304000-00008.
35. Haynes J, Obiako B, Babal P, Stevens T. 1999. 5-(N-ethylcarboxamido)adenosine desensitizes the A2b-adenosine receptor in lung circulation. Am. J. Physiol. Heart Circ. Physiol. 276:H1877-H1883.
36. Teng B, Fil D, Tilley SL, Ledent C, Krahn T, Mustafa SJ. 2013. Functional and RNA expression profile of adenosine receptor subtypes in mouse mesenteric arteries. J. Cardiovasc. Pharmacol. 61:70-76. http://dx.doi.org/10.1097/FJC.0b013e318278575e.
37. Tawfik HE, Teng B, Morrison RR, Schnermann J, Mustafa SJ. 2006. Role of A1 adenosine receptor in the regulation of coronary flow. Am. J. Physiol. Heart Circ. Physiol. 291:H467-H472. http://dx.doi.org/10.1152/ajpheart.01319.2005.
38. McIntyre RC, Banerjee A, Bensard DD, Brew EC, Hahn AR, Fullerton DA. 1994. Adenosine A1-receptor mechanisms antagonize betaadrenergic pulmonary vasodilation in hypoxia. Am. J. Physiol. Heart Circ. Physiol. 267:H2179-H2185.
39. Wareing MD, Shea AL, Inglis CA, Dias PB, Sarawar SR. 2007. CXCR2 is required for neutrophil recruitment to the lung during influenza virus infection, but is not essential for viral clearance. Viral Immunol. 20:369-378. http://dx.doi.org/10.1089/vim.2006.0101.
40. Hemmers S, Teijaro JR, Arandjelovic S, Mowen KA. 2011. PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS One 6:e22043. http://dx.doi.org/10.1371/journal.pone.0022043.
41. Narasaraju T, Ng HH, Phoon MC, Chow VTK. 2010. MCP-1 antibody treatment enhances damage and impedes repair of the alveolar epithelium in influenza pneumonitis. Am. J. Respir. Cell Mol. Biol. 42:732-743. http://dx.doi.org/10.1165/rcmb.2008-0423OC.
42. Narasaraju T, Yang E, Samy RP, Ng HH, Poh WP, Liew AA, Phoon MC, Van Rooijen N, Chow VT. 2011. Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am. J. Pathol. 179:199-210. http://dx.doi.org/10.1016/j.ajpath.2011.03.013.
43. Tate MD, Pickett DL, Van Rooijen N, Brooks AG, Reading PC. 2010. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J. Virol. 84:7569-7580. http://dx.doi.org/10.1128/JVI.00291-10.
44. Schneider C, Nobs SP, Heer AK, Kurrer M, Klinke G, Van Rooijen N, Vogel J, Kopf M. 2014. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog. 10:e1004053. http://dx.doi.org/10.1371/journal.ppat.1004053.
45. Huang FF, Barnes PF, Feng Y, Donis R, Chroneos ZC, Idell S, Allen T, Perez DR, Whitsett JA, Dunussi-Joannopoulos K, Shams H. 2011. GM-CSF in the lung protects against lethal influenza infection. Am. J. Respir. Crit. Care Med. 184:259-268. http://dx.doi.org/10.1164/rccm.201012-2036OC.
46. Murphy EA, Davis JM, McClellan JL, Carmichael MD, Rooijen NV, Gangemi JD. 2011. Susceptibility to infection and inflammatory response following influenza virus (H1N1, A/PR/8/34) challenge: role of macrophages. J. Interferon Cytokine Res. 31:501-508. http://dx.doi.org/10.1089/jir.2010.0143.
47. Paul S, Elsinga PH, Ishiwata K, Dierckx RA, van Waarde A. 2011. Adenosine A(1) receptors in the central nervous system: their functions in health and disease, and possible elucidation by PET imaging. Curr. Med. Chem. 18:4820-4835. http://dx.doi.org/10.2174/092986711797535335.
48. Carman AJ, Mills JH, Krenz A, Kim DG, Bynoe MS. 2011. Adenosine receptor signaling modulates permeability of the blood-brain barrier. J. Neurosci. 31:13272-13280. http://dx.doi.org/10.1523/JNEUROSCI.3337-11.2011.
49. Moreno JL, Kurita M, Holloway T, López J, Cadagan R, Martínez-Sobrido L, García-Sastre A, González-Maeso J. 2011. Maternal influenza viral infection causes schizophrenia-like alterations of 5-HT2A and mGlu2 receptors in the adult offspring. J. Neurosci. 31:1863-1872. http://dx.doi.org/10.1523/JNEUROSCI.4230-10.2011.
50. Fatemi SH, Folsom TD, Rooney RJ, Mori S, Kornfield TE, Reutiman TJ, Kneeland RE, Liesch SB, Hua K, Hsu J, Patel DH. 2012. The viral theory of schizophrenia revisited: abnormal placental gene expression and structural changes with lack of evidence for H1N1 viral presence in placentae of infected mice or brains of exposed offspring. Neuropharmacology 62: 1290-1298. http://dx.doi.org/10.1016/j.neuropharm.2011.01.011.
51. Aronsson F, Lannebo C, Paucar M, Brask J, Kristensson K, Karlsson H. 2002. Persistence of viral RNA in the brain of offspring to mice infected with influenza A/WSN/33 virus during pregnancy. J. Neurovirol. 8:353-357. http://dx.doi.org/10.1080/13550280290100480.
52. Beraki S, Aronsson F, Karlsson H, Ogren SO, Kristensson K. 2005. Influenza A virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Mol. Psychiatry 10:299-308. http://dx.doi.org/10.1038/sj.mp.4001545.
53. Mori I, Kimura Y. 2001. Neuropathogenesis of influenza virus infection in mice. Microbes Infect. 3:475-479. http://dx.doi.org/10.1016/S1286-4579(01)01403-4.
54. Aronsson F, Robertson B, Ljunggren HG, Kristensson K. 2003. Invasion and persistence of the neuroadapted influenza virus A/WSN/33 in the mouse olfactory system. Viral Immunol. 16:415-423. http://dx.doi.org/10.1089/088282403322396208.
55. Asp L, Holtze M, Powell SB, Karlsson H, Erhardt S. 2010. Neonatal infection with neurotropic influenza A virus induces the kynurenine pathway in early life and disrupts sensorimotor gating in adult Tap1-/-mice. Int. J. Neuropsychopharmacol. 13:475-485. http://dx.doi.org/10.1017/S1461145709990253.
56. Wang S, Le T, Kurihara N, Chida J, Cisse Y, Yano M, Kido H. 2010. Influenza virus-cytokine-protease cycle in the pathogenesis of vascular hyperpermeability in severe influenza. J. Infect. Dis. 202:991-1001. http://dx.doi.org/10.1086/656044.
57. Castrucci MR, Kawaoka Y. 1993. Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 67:759-764.
58. Yamada T, Yamanaka I, Takahashi M, Nakajima S. 1996. Invasion of brain by neurovirulent influenza A virus after intranasal inoculation. Parkinsonism Relat. Disord. 2:187-193. http://dx.doi.org/10.1016/S1353-8020(96)00024-7.
59. Tumpey TM, García-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, van Rooijen N, Katz JM, Basler CF. 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. J. Virol. 79:14933-14944. http://dx.doi.org/10.1128/JVI.79.23.14933-14944.2005.
60. Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y. 2004. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703-707. http://dx.doi.org/10.1038/nature02951.
61. Hillaire MLB, Rimmelzwaan GF, Kreijtz JHCM. 2013. Clearance of influenza virus infections by T cells: risk of collateral damage? Curr. Opin. Virol. 3:430-437. http://dx.doi.org/10.1016/j.coviro.2013.05.002.
62. Thammavongsa V, Kern JW, Missiakas DM, Schneewind O. 2009. Staphylococcus aureus synthesizes adenosine to escape host immune responses. J. Exp. Med. 206:2417-2427. http://dx.doi.org/10.1084/jem.20090097.
63. Crane JK, Olson RA, Jones HM, Duffey ME. 2002. Release of ATP during host cell killing by enteropathogenic E. coli and its role as a secretory mediator. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G74-G86.
64. Tasca T, Bonan CD, Carli GA, Sarkis J. 2004. Trichomonas vaginalis: cytochemical localization of a NTPDase1 and an ecto-5=-nucleotidase and effects of adenine nucleotides on cellular viability. Parasitol. Res. 93:300-303. http://dx.doi.org/10.1007/s00436-004-1126-4.
65. Liu P, Pian Y, Li X, Liu R, Xie W, Zhang C, Zheng Y, Jiang Y, Yuan Y. 19 January 2014. Streptococcus suis adenosine synthase functions as an effector in evasion of PMN-mediated innate immunity. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jiu050.
66. Haskó G, Linden J, Cronstein B, Pacher P. 2008. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat. Rev. Drug Discov. 7:759-770. http://dx.doi.org/10.1038/nrd2638.
67. Marchese A. 2014. Endocytic trafficking of chemokine receptors. Curr. Opin. Cell Biol. 27:72-77. http://dx.doi.org/10.1016/j.ceb.2013.11.011.
68. Jacobson K, Balasubramanian R, Deflorian F, Gao ZG. 2012. G proteincoupled adenosine (P1) and P2Y receptors: ligand design and receptor interactions. Purinergic Signal. 8:419-436. http://dx.doi.org/10.1007/s11302-012-9294-7.
69. Raman D, Sobolik-Delmaire T, Richmond A. 2011. Chemokines in health and disease. Exp. Cell Res. 317:575-589. http://dx.doi.org/10.1016/j.yexcr.2011.01.005.
70. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12:1203-1207. http://dx.doi.org/10.1038/nm1477.
71. Kash JC, Tumpey TM, Proll SC, Carter V, Perwitasari O, Thomas MJ, Basler CF, Palese P, Taubenberger JK, García-Sastre A, Swayne DE, Katze MG. 2006. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443:578-581. http://dx.doi.org/10.1038/nature05181.
72. García-Sastre A. 2011. Induction and evasion of type I interferon responses by influenza viruses. Virus Res. 162:12-18. http://dx.doi.org/10.1016/j.virusres.2011.10.017.
73. Zeng H, Goldsmith C, Thawatsupha P, Chittaganpitch M, Waicharoen S, Zaki S, Tumpey TM, Katz JM. 2007. Highly pathogenic avian influenza H5N1 viruses elicit an attenuated type I interferon response in polarized human bronchial epithelial cells. J. Virol. 81:12439-12449. http://dx.doi.org/10.1128/JVI.01134-07.
74. Chen Y, Yao Y, Sumi Y, Li A, To UK, Elkhal A, Inoue Y, Woehrle T, Zhang Q, Hauser C, Junger WG. 2010. Purinergic signaling: a fundamental mechanism in neutrophil activation. Sci. Signal. 3:ra45. http://dx.doi.org/10.1126/scisignal.2000549.
75. Neely CF, Keith IM. 1995. A1 adenosine receptor antagonists block ischemia-reperfusion injury of the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 268:L1036-L1046.
76. Ngamsri KC, Wagner R, Vollmer I, Stark S, Reutershan J. 2010. Adenosine receptor A1 regulates polymorphonuclear cell trafficking and microvascular permeability in lipopolysaccharide-induced lung injury. J. Immunol. 185:4374-4384. http://dx.doi.org/10.4049/jimmunol.1000433.
77. Fedson DS. 2005. Preparing for pandemic vaccination: an international policy agenda for vaccine development. J. Public Health Policy 26:4-29. http://dx.doi.org/10.1057/palgrave.jphp.3200008.
78. Poland GA. 2010. The 2009-2010 influenza pandemic: effects on pandemic and seasonal vaccine uptake and lessons learned for seasonal vaccination campaigns. Vaccine 28(Suppl 4):D3-D13. http://dx.doi.org/10.1016/j.vaccine.2010.08.024.
79. Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect. Dis. 12:36-44. http://dx.doi.org/10.1016/S1473-3099(11) 70295-X.
80. Newall AT, Wood JG, Oudin N, MacIntyre CR. 2010. Cost-effectiveness of pharmaceutical-based pandemic influenza mitigation strategies. Emerg. Infect. Dis. 16:224-230. http://dx.doi.org/10.3201/eid1602.090571.
81. Thorlund K, Awad T, Boivin G, Thabane L. 2011. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect. Dis. 11:134. http://dx.doi.org/10.1186/1471-2334-11-134.
82. Kumar A. 2011. Early versus late oseltamivir treatment in severely ill patients with 2009 pandemic influenza A (H1N1): speed is life. J. Antimicrob. Chemother. 66:959-963. http://dx.doi.org/10.1093/jac/dkr090.
83. Diaz E, Martin-Loeches I, Canadell L, Vidaur L, Suarez D, Socias L, Estella A, Gil RB, Guerrero JE, Valverdú-Vidal M, Vergara JC, López-Pueyo MJ, Magret M, Recio T, López D, Rello J, Rodriguez A, H1N1 SEMICYUC-CIBERES-REIPI Working Group (GETGAG). 2012. Corticosteroid therapy in patients with primary viral pneumonia due to pandemic (H1N1) 2009 influenza. J. Infect. 64:311-318. http://dx.doi.org/10.1016/j.jinf.2011.12.010.
84. Westall G, Paraskeva M. 2011. H1N1 influenza: critical care aspects. Semin. Respir. Crit. Care Med. 32:400-408. http://dx.doi.org/10.1055/s-0031-1283280.
85. Wilson CN. 2008. Adenosine receptors and asthma in humans. Br. J. Pharmacol. 155:475-486. http://dx.doi.org/10.1038/bjp.2008.361.