Inhibition of phosphodiesterase-4 during pneumococcal pneumonia reduces inflammation and lung injury in mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 55, Issue 1, 2016, Pages 24-34

  Tavares, Luciana P ^a   Garcia, Cristiana C ^b   Vago, Juliana P ^a   Queiroz Junior, Celso M ^a   Galvão, Izabela ^a   David, Bruna A ^a   Rachid, Milene A ^a   Silva, Patrícia M R ^b   Russo, Remo C ^a   Teixeira, Mauro M ^a   Sousa, Lirlândia P ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Annexin A1; Immunomodulation; Inflammation; Phosphodiesterase 4; Streptococcus pneumoniae

Indexed keywords

CEFTRIAXONE; LIPOCORTIN 1; PHOSPHODIESTERASE IV; ROLIPRAM; ANTIINFECTIVE AGENT; PHOSPHODIESTERASE IV INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL COUNT; BACTERIAL LOAD; CONTROLLED STUDY; ENZYME INHIBITION; EX VIVO STUDY; IMMUNOMODULATION; LUNG INJURY; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PROPHYLAXIS; PROTEIN EXPRESSION; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; ANIMAL; BAGG ALBINO MOUSE; COMPLICATION; DRUG EFFECTS; ENZYMOLOGY; LUNG; LUNG FUNCTION TEST; MACROPHAGE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PNEUMONIA; PNEUMONIA, PNEUMOCOCCAL;

ANIMALS; ANNEXIN A1; ANTI-BACTERIAL AGENTS; CEFTRIAXONE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; LUNG; LUNG INJURY; MACROPHAGES; MALE; MICE, INBRED BALB C; PHAGOCYTOSIS; PHOSPHODIESTERASE 4 INHIBITORS; PNEUMONIA; PNEUMONIA, PNEUMOCOCCAL; RESPIRATORY FUNCTION TESTS; ROLIPRAM; STREPTOCOCCUS PNEUMONIAE;

EID: 84988985119     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0083OC     Document Type: Article

References (50)

1. Spoorenberg SM, Bos WJ, Heijligenberg R, Voorn PG, Grutters JC, Rijkers GT, van de Garde EM. Microbial aetiology, outcomes, and costs of hospitalisation for community-acquired pneumonia: an observational analysis. BMC Infect Dis 2014;14:335.
2. Song JY, Eun BW, Nahm MH. Diagnosis of pneumococcal pneumonia: current pitfalls and the way forward. Infect Chemother 2013;45: 351-366.
3. Paterson GK, Orihuela CJ. Pneumococci: immunology of the innate host response. Respirology 2010;15: 1057-1063.
4. Steel HC, Cockeran R, Anderson R, Feldman C. Overview of communityacquired pneumonia and the role of inflammatory mechanisms in the immunopathogenesis of severe pneumococcal disease. Mediators Inflamm 2013;2013:490346.
5. Garcia CC, Russo RC, Guabiraba R, Fagundes CT, Polidoro RB, Tavares LP, Salgado AP, Cassali GD, Sousa LP, Machado AV, et al. Platelet-activating factor receptor plays a role in lung injury and death caused by Influenza A in mice. PLoS Pathog 2010;6: e1001171.
6. Ghoneim HE, McCullers JA. Adjunctive corticosteroid therapy improves lung immunopathology and survival during severe secondary pneumococcal pneumonia in mice. J Infect Dis 2014;209:1459-1468.
7. Tuomanen E, Rich R, Zak O. Induction of pulmonary inflammation by components of the pneumococcal cell surface. Am Rev Respir Dis 1987;135:869-874.
8. Majhi A, Kundu K, Adhikary R, Banerjee M, Mahanti S, Basu A, Bishayi B. Combination therapy with ampicillin and azithromycin in an experimental pneumococcal pneumonia is bactericidal and effective in down regulating inflammation in mice. J Inflamm (Lond) 2014;11:5.
9. Sousa LP, Lopes F, Silva DM, Tavares LP, Vieira AT, Rezende BM, Carmo AF, Russo RC, Garcia CC, Bonjardim CA, et al. PDE4 inhibition drives resolution of neutrophilic inflammation by inducing apoptosis in a PKA-PI3K/Akt-dependent and NF-kB-independent manner. J Leukoc Biol 2010;87:895-904.
10. Korhonen R, HömmöT, Keränen T, Laavola M, Hämäläinen M, Vuolteenaho K, Lehtimäki L, Kankaanranta H, Moilanen E. Attenuation of TNF production and experimentally induced inflammation by PDE4 inhibitor rolipram is mediated by MAPK phosphatase-1. Br J Pharmacol 2013;169:1525-1536.
11. Jin SL, Ding SL, Lin SC. Phosphodiesterase 4 and its inhibitors in inflammatory diseases. Chang Gung Med J 2012;35:197-210.
12. Page CP. Phosphodiesterase inhibitors for the treatment of asthma and chronic obstructive pulmonary disease. Int Arch Allergy Immunol 2014;165:152-164.
13. Koo MS, Manca C, Yang G, O?Brien P, Sung N, Tsenova L, Subbian S, Fallows D, Muller G, Ehrt S, et al. Phosphodiesterase 4 inhibition reduces innate immunity and improves isoniazid clearance of Mycobacterium tuberculosis in the lungs of infected mice. PLoS One 2011;6:e17091.
14. Soares AC, Souza DG, Pinho V, Vieira AT, Barsante MM, Nicoli JR, Teixeira M. Impaired host defense to Klebsiella pneumoniae infection in mice treated with the PDE4 inhibitor rolipram. Br J Pharmacol 2003;140:855-862.
15. Hannon R, Croxtall JD, Getting SJ, Roviezzo F, Yona S, Paul-Clark MJ, Gavins FN, Perretti M, Morris JF, Buckingham JC, Flower RJ. Aberrant inflammation and resistance to glucocorticoids in annexin 12/2 mouse. FASEB J 2003;17:253-255.
16. Garcia CC, Weston-Davies W, Russo RC, Tavares LP, Rachid MA, Alves-Filho JC, Machado AV, Ryffel B, Nunn MA, Teixeira MM. Complement C5 activation during influenza A infection in mice contributes to neutrophil recruitment and lung injury. PLoS One 2013;8:e64443.
17. Russo RC, Garcia CC, Barcelos LS, Rachid MA, Guabiraba R, Roffê E, Souza AL, Sousa LP, Mirolo M, Doni A, et al. Phosphoinositide 3-kinase g plays a critical role in bleomycin-induced pulmonary inflammation and fibrosis in mice. J Leukoc Biol 2011;89:269-282.
18. Solito E, McArthur S, Christian H, Gavins F, Buckingham JC, Gillies GE. Annexin A1 in the brain-undiscovered roles? Trends Pharmacol Sci 2008;29:135-142.
19. D?Amico M, Di Filippo C, La M, Solito E, McLean PG, Flower RJ, Oliani SM, Perretti M. Lipocortin 1 reduces myocardial ischemiareperfusion injury by affecting local leukocyte recruitment. FASEB J 2000;14:1867-1869.
20. Vago JP, Nogueira CR, Tavares LP, Soriani FM, Lopes F, Russo RC, Pinho V, Teixeira MM, Sousa LP. Annexin A1 modulates natural and glucocorticoid-induced resolution of inflammation by enhancing neutrophil apoptosis. J Leukoc Biol 2012;92:249-258.
21. Oliani SM, Paul-Clark MJ, Christian HC, Flower RJ, Perretti M. Neutrophil interaction with inflamed postcapillary venule endothelium alters annexin 1 expression. Am J Pathol 2001;158:603-615.
22. Vong L, D?Acquisto F, Pederzoli-Ribeil M, Lavagno L, Flower RJ, Witko-Sarsat V, Perretti M. Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3. J Biol Chem 2007;282: 29998-30004.
23. Dalli J, Consalvo AP, Ray V, Di Filippo C, D?Amico M, Mehta N, Perretti M. Proresolving and tissue-protective actions of annexin A1-based cleavage-resistant peptides are mediated by formyl peptide receptor 2/lipoxin A4 receptor. J Immunol 2013;190:6478-6487.
24. Song JY, Nahm MH, Moseley MA. Clinical implications of pneumococcal serotypes: invasive disease potential, clinical presentations, and antibiotic resistance. J Korean Med Sci 2013;28:4-15.
25. Doerschuk CM, Markos J, Coxson HO, English D, Hogg JC. Quantitation of neutrophil migration in acute bacterial pneumonia in rabbits. J Appl Physiol (1985) 1994;77:2593-2599.
26. Bhowmick R, Tin Maung NH, Hurley BP, Ghanem EB, Gronert K, McCormick BA, Leong JM. Systemic disease during Streptococcus pneumoniae acute lung infection requires 12-lipoxygenase-dependent inflammation. J Immunol 2013;191:5115-5123.
27. Driver C. Pneumonia part 1: pathology, presentation and prevention. Br J Nurs 2012;21:103-106.
28. Chong J, Leung B, Poole P. Phosphodiesterase 4 inhibitors for chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2013;11:CD002309.
29. Toward TJ, Johnson FJ, Boult JE, Maillard JY. Airway function and reactivity, leukocyte influx and nitric oxide after inoculation with parainfluenza-3 virus: effects of dexamethasone or rolipram. Int Immunopharmacol 2005;5:771-782.
30. Page CP, Spina D. Phosphodiesterase inhibitors in the treatment of inflammatory diseases. Handb Exp Pharmacol 2011;204: 391-414.
31. Dowling RB, Johnson M, Cole PJ, Wilson R. The effect of rolipram, a type IV phosphodiesterase inhibitor, on Pseudomonas aeruginosa infection of respiratory mucosa. J Pharmacol Exp Ther 1997;282: 1565-1571.
32. Holthoff JH, Wang Z, Patil NK, Gokden N, Mayeux PR. Rolipram improves renal perfusion and function during sepsis in the mouse. J Pharmacol Exp Ther 2013;347:357-364.
33. Bao F, Fleming JC, Golshani R, Pearse DD, Kasabov L, Brown A, Weaver LC. A selective phosphodiesterase-4 inhibitor reduces leukocyte infiltration, oxidative processes, and tissue damage after spinal cord injury. J Neurotrauma 2011;28:1035-1049.
34. Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 2004;4:144-154.
35. Yende S, Tuomanen EI, Wunderink R, Kanaya A, Newman AB, Harris T, de Rekeneire N, Kritchevsky SB. Preinfection systemic inflammatory markers and risk of hospitalization due to pneumonia. Am J Respir Crit Care Med 2005;172:1440-1446.
36. Esposito S, Principi N. Pharmacotherapy for pneumococcal infections: an update. Expert Opin Pharmacother 2013;14:65-77.
37. Karlström A, Heston SM, Boyd KL, Tuomanen EI, McCullers JA. Tolllike receptor 2 mediates fatal immunopathology in mice during treatment of secondary pneumococcal pneumonia following influenza. J Infect Dis 2011;204:1358-1366.
38. Burgos J, Luján M, Larrosa MN, Fontanals D, Bermudo G, Planes AM, Puig M, Rello J, FalcóV, Pahissa A. Risk factors for respiratory failure in pneumococcal pneumonia: the importance of pneumococcal serotypes. Eur Respir J 2014;43:545-553.
39. Light RB. Pulmonary pathophysiology of pneumococcal pneumonia. Semin Respir Infect 1999;14:218-226.
40. Wright TW, Gigliotti F, Finkelstein JN, McBride JT, An CL, Harmsen AG. Immune-mediated inflammation directly impairs pulmonary function, contributing to the pathogenesis of Pneumocystis carinii pneumonia. J Clin Invest 1999;104:1307-1317.
41. Sousa LP, Alessandri AL, Pinho V, Teixeira MM. Pharmacological strategies to resolve acute inflammation. Curr Opin Pharmacol 2013;13:625-631.
42. Perretti M, D?Acquisto F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 2009;9:62-70.
43. Chiang N, Fredman G, Bäckhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 2012;484:524-528.
44. Gobbetti T, Coldewey SM, Chen J, McArthur S, le Faouder P, Cenac N, Flower RJ, Thiemermann C, Perretti M. Nonredundant protective properties of FPR2/ALX in polymicrobial murine sepsis. Proc Natl Acad Sci USA 2014;111:18685-18690.
45. Vanessa KH, Julia MG, Wenwei L, Michelle AL, Zarina ZR, Lina LH, Sylvie A. Absence of annexin A1 impairs host adaptive immunity against Mycobacterium tuberculosis in vivo. Immunobiology 2015;220:614-623.
46. Tsao FH, Meyer KC, Chen X, Rosenthal NS, Hu J. Degradation of annexin I in bronchoalveolar lavage fluid from patients with cystic fibrosis. Am J Respir Cell Mol Biol 1998;18:120-128.
47. Pederzoli-Ribeil M, Maione F, Cooper D, Al-Kashi A, Dalli J, Perretti M, D?Acquisto F. Design and characterization of a cleavage-resistant annexin A1 mutant to control inflammation in the microvasculature. Blood 2010;116:4288-4296.
48. Dalli J, Kraft BD, Colas RA, Shinohara M, Fredenburgh LE, Hess DR, Chiang N, Welty-Wolf K, Choi AM, Piantadosi CA, et al. The regulation of proresolving lipid mediator profiles in baboon pneumonia by inhaled carbon monoxide. Am J Respir Cell Mol Biol 2015;53:314-325.
49. Chiang N, Dalli J, Colas RA, Serhan CN. Identification of resolvin D2 receptor mediating resolution of infections and organ protection. J Exp Med 2015;212:1203-1217.
50. Lucas CD, Dorward DA, Tait MA, Fox S, Marwick JA, Allen KC, Robb CT, Hirani N, Haslett C, Duffin R, et al. Downregulation of Mcl-1 has anti-inflammatory pro-resolution effects and enhances bacterial clearance from the lung. Mucosal Immunol 2014;7: 857-868.