Interleukin-6 displays lung anti-inflammatory properties and exerts protective hemodynamic effects in a double-hit murine acute lung injury

Respiratory Research

Volumn 18, Issue 1, 2017, Pages

  Voiriot, Guillaume ^a,b   Razazi, Keyvan ^a,b,c   Amsellem, Valérie ^a   Tran Van Nhieu, Jeanne ^b,c   Abid, Shariq ^a   Adnot, Serge ^a,b,c   Mekontso Dessap, Armand ^a,b,c   Maitre, Bernard ^a,b,c  

^a INSERM U955   (France)

^b FACULTÉ DE MÉDECINE   (France)

^c HENRI MONDOR HOSPITAL   (France)

Author keywords

Acute lung injury; Acute respiratory distress syndrome; Interleukin 6; Mechanical ventilation; Nitric oxide synthase; Pulmonary hypertension

Indexed keywords

INTERLEUKIN 6; N(G) NITROARGININE METHYL ESTER; RECOMBINANT INTERLEUKIN 6; ANTIINFLAMMATORY AGENT;

ACUTE LUNG INJURY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ARTIFICIAL VENTILATION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG MECHANISM; HEART OUTPUT; HISTOLOGY; KNOCKOUT MOUSE; LUNG EDEMA; LUNG HEMODYNAMICS; LUNG LAVAGE; LUNG RESISTANCE; LUNG VASOCONSTRICTION; MALE; MOUSE; NONHUMAN; PNEUMONIA; PULMONARY HYPERTENSION; SYSTOLIC BLOOD PRESSURE; TIDAL VOLUME; WILD TYPE; ANIMAL; BLOOD FLOW VELOCITY; C57BL MOUSE; IMMUNOLOGY; LUNG CIRCULATION; PATHOPHYSIOLOGY; PULMONARY ARTERY;

ACUTE LUNG INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD FLOW VELOCITY; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PULMONARY ARTERY; PULMONARY CIRCULATION;

EID: 85018488167     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/s12931-017-0553-6     Document Type: Article

References (60)

1. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med. 2005;353(16):1685-93.
2. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med. 2000;342(18):1334-49.
3. Gadient RA, Patterson PH. Leukemia inhibitory factor, Interleukin 6, and other cytokines using the GP130 transducing receptor: roles in inflammation and injury. Stem Cells. 1999;17(3):127-37.
4. Fattori E, Cappelletti M, Costa P, Sellitto C, Cantoni L, Carelli M, Faggioni R, Fantuzzi G, Ghezzi P, Poli V. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med. 1994;180(4):1243-50.
5. Tremblay L, Valenza F, Ribeiro SP, Li J, Slutsky AS. Injurious ventilatory strategies increase cytokines and c-fos m-RNA expression in an isolated rat lung model. J Clin Invest. 1997;99(5):944-52.
6. Veldhuizen RA, Slutsky AS, Joseph M, McCaig L. Effects of mechanical ventilation of isolated mouse lungs on surfactant and inflammatory cytokines. Eur Respir J. 2001;17(3):488-94.
7. Stüber F, Wrigge H, Schroeder S, Wetegrove S, Zinserling J, Hoeft A, Putensen C. Kinetic and reversibility of mechanical ventilation-associated pulmonary and systemic inflammatory response in patients with acute lung injury. Intensive Care Med. 2002;28(7):834-41.
8. Vaporidi K, Voloudakis G, Priniannakis G, Kondili E, Koutsopoulos A, Tsatsanis C, Georgopoulos D. Effects of respiratory rate on ventilator-induced lung injury at a constant PaCO2 in a mouse model of normal lung. Crit Care Med. 2008;36(4):1277-83.
9. Ranieri VM, Suter PM, Tortorella C, De Tullio R, Dayer JM, Brienza A, Bruno S, Slutsky AS. Effect of mechanical ventilation on inflammatory mediators in patients with acute respiratory distress syndrome: a randomized controlled trial. Jama J Am Med Assoc. 1999;282(1):54-61.
10. Parsons PE, Eisner MD, Thompson BT, Matthay MA, Ancukiewicz M, Bernard GR, Wheeler AP. Lower tidal volume ventilation and plasma cytokine markers of inflammation in patients with acute lung injury. Crit Care Med. 2005;33(1):1-6. discussion 230-232.
11. Frank JA, Parsons PE, Matthay MA. Pathogenetic significance of biological markers of ventilator-associated lung injury in experimental and clinical studies. Chest. 2006;130(6):1906-14.
12. Remick DG, Bolgos G, Copeland S, Siddiqui J. Role of interleukin-6 in mortality from and physiologic response to sepsis. Infect Immun. 2005;73(5):2751-7.
13. O'Malley K, Moldawer L. Interleukin-6: Still crazy after all these years. Crit Care Med. 2006;34(10):2690-1.
14. Ward NS, Waxman AB, Homer RJ, Mantell LL, Einarsson O, Du Y, Elias JA. Interleukin-6-induced protection in hyperoxic acute lung injury. Am J Respir Cell Mol Biol. 2000;22(5):535-42.
15. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, Lei XF, Achong MK. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 1998;101(2):311-20.
16. Jones MR, Quinton LJ, Simms BT, Lupa MM, Kogan MS, Mizgerd JP. Roles of interleukin-6 in activation of STAT proteins and recruitment of neutrophils during Escherichia coli pneumonia. J Infect Dis. 2006;193(3):360-9.
17. Bull TM, Clark B, McFann K, Moss M. National Institutes of Health/National Heart, Lung, and Blood Institute ARDS Network. Pulmonary vascular dysfunction is associated with poor outcomes in patients with acute lung injury. Am J Respir Crit Care Med. 2010;182(9):1123-8.
18. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Köhler G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 1994;368(6469):339-42.
19. Yardeni T, Eckhaus M, Morris HD, Huizing M, Hoogstraten-Miller S. Retro-orbital injections in mice. Lab Anim. 2011;40(5):155-60.
20. Arikan AA, Yu B, Mastrangelo MA, Tweardy DJ. Interleukin-6 treatment reverses apoptosis and blunts susceptibility to intraperitoneal bacterial challenge following hemorrhagic shock. Crit Care Med. 2006;34(3):771-7.
21. Matsushita K, Iwanaga S, Oda T, Kimura K, Shimada M, Sano M, Umezawa A, Hata J, Ogawa S. Interleukin-6/soluble interleukin-6 receptor complex reduces infarct size via inhibiting myocardial apoptosis. Lab Invest. 2005;85(10):1210-23.
22. Mekontso Dessap A, Voiriot G, Zhou T, Marcos E, Dudek SM, Jacobson JR, Machado R, Adnot S, Brochard L, Maitre B, Garcia JG. Conflicting physiological and genomic cardiopulmonary effects of recruitment maneuvers in murine acute lung injury. Am J Respir Cell Mol Biol. 2012;46(4):541-50.
23. Champion HC, Villnave DJ, Tower A, Kadowitz PJ, Hyman AL. A novel right-heart catheterization technique for in vivo measurement of vascular responses in lungs of intact mice. Am J Physiol Heart Circ Physiol. 2000;278(1):H8-H15.
24. Belperio JA, Keane MP, Burdick MD, Londhe V, Xue YY, Li K, Phillips RJ, Strieter RM. Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest. 2002;110(11):1703-16.
25. Nishina K, Mikawa K, Takao Y, Shiga M, Maekawa N, Obara H. Intravenous lidocaine attenuates acute lung injury induced by hydrochloric acid aspiration in rabbits. Anesthesiology. 1998;88(5):1300-9.
26. Kolliputi N, Waxman AB. IL-6 cytoprotection in hyperoxic acute lung injury occurs via suppressor of cytokine signaling-1-induced apoptosis signal-regulating kinase-1 degradation. Am J Respir Cell Mol Biol. 2009;40(3):314-24.
27. Leemans JC, Vervoordeldonk MJBM, Florquin S, van Kessel KP, van der Poll T. Differential role of interleukin-6 in lung inflammation induced by lipoteichoic acid and peptidoglycan from Staphylococcus aureus. Am J Respir Crit Care Med. 2002;165(10):1445-50.
28. Shanley TP, Foreback JL, Remick DG, Ulich TR, Kunkel SL, Ward PA. Regulatory effects of interleukin-6 in immunoglobulin G immune-complex-induced lung injury. Am J Pathol. 1997;151(1):193-203.
29. Imai Y, Kuba K, Neely GG, Yaghubian-Malhami R, Perkmann T, van Loo G, Ermolaeva M, Veldhuizen R, Leung YH, Wang H, Liu H, Sun Y, Pasparakis M, Kopf M, Mech C, Bavari S, Peiris JS, Slutsky AS, Akira S, Hultqvist M, Holmdahl R, Nicholls J, Jiang C, Binder CJ, Penninger JM. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell. 2008;133(2):235-49.
30. Gurkan OU, He C, Zielinski R, Rabb H, King LS, Dodd-o JM, D'Alessio FR, Aggarwal N, Pearse D, Becker PM. Interleukin-6 mediates pulmonary vascular permeability in a two-hit model of ventilator-associated lung injury. Exp Lung Res. 2011;37(10):575-84.
31. Goldman JL, Sammani S, Kempf C, Saadat L, Letsiou E, Wang T, Moreno-Vinasco L, Rizzo AN, Fortman JD, Garcia JG. Pleiotropic effects of interleukin-6 in a "two-hit" murine model of acute respiratory distress syndrome. Pulm Circ. 2014;4(2):280-8.
32. Wolters PJ, Wray C, Sutherland RE, Kim SS, Koff J, Mao Y, Frank JA. Neutrophil-derived IL-6 limits alveolar barrier disruption in experimental ventilator-induced lung injury. J Immunol. 2009;182(12):8056-62.
33. The Acute Respiratory Distress Syndrome Network. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med. 2000;342(18):1301-8.
34. Esteban A, Ferguson ND, Meade MO, Frutos-Vivar F, Apezteguia C, Brochard L, Raymondos K, Nin N, Hurtado J, Tomicic V, González M, Elizalde J, Nightingale P, Abroug F, Pelosi P, Arabi Y, Moreno R, Jibaja M, D'Empaire G, Sandi F, Matamis D, Montañez AM, Anzueto A. Evolution of mechanical ventilation in response to clinical research. Am J Respir Crit Care Med. 2008;177(2):170-7.
35. Halbertsma FJ, Vaneker M, Pickkers P, Snijdelaar DG, van Egmond J, Scheffer GJ, van der Hoeven HG. Hypercapnic acidosis attenuates the pulmonary innate immune response in ventilated healthy mice. Crit Care Med. 2008;36(8):2403-6.
36. Maniatis NA, Kardara M, Hecimovich D, Letsiou E, Castellon M, Roussos C, Shinin V, Votta-Vellis EG, Schwartz DE, Minshall RD. Role of caveolin-1expression in the pathogenesis of pulmonary edema in ventilator-induced lung injury. Pulm Circ. 2012;2(4):452-60.
37. Manitsopoulos N, Orfanos SE, Kotanidou A, Nikitopoulou I, Siempos I, Magkou C, Dimopoulou I, Zakynthinos SG, Armaganidis A, Maniatis NA. Inhibition of HMGCoA reductase by simvastatin protects mice from injurious mechanical ventilation. Respir Res. 2015;16:24.
38. Tasaka S, Inoue K-I, Miyamoto K, Nakano Y, Kamata H, Shinoda H, Hasegawa N, Miyasho T, Satoh M, Takano H, Ishizaka A. Role of interleukin-6 in elastase-induced lung inflammatory changes in mice. Exp Lung Res. 2010;36(6):362-72.
39. Allen GB, Suratt BT, Rinaldi L, Petty JM, Bates JHT. Choosing the frequency of deep inflation in mice: balancing recruitment against ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol. 2006;291(4):L710-717.
40. Dalrymple SA, Slattery R, Aud DM, Krishna M, Lucian LA, Murray R. Interleukin-6 is required for a protective immune response to systemic Escherichia coli infection. Infect Immun. 1996;64(8):3231-5.
41. Deutschman CS, Cereda M, Ochroch EA, Raj NR. Sepsis-induced cholestasis, steatosis, hepatocellular injury, and impaired hepatocellular regeneration are enhanced in interleukin-6 -/- mice. Crit Care Med. 2006;34(10):2613-20.
42. Bhargava R, Janssen W, Altmann C, Andrés-Hernando A, Okamura K, Vandivier RW, Ahuja N, Faubel S. Intratracheal IL-6 protects against lung inflammation in direct, but not indirect, causes of acute lung injury in mice. PLoS One. 2013;8(5):e61405.
43. Zapol WM, Snider MT. Pulmonary hypertension in severe acute respiratory failure. N Engl J Med. 1977;296(9):476-80.
44. Villar J, Blazquez MA, Lubillo S, Quintana J, Manzano JL. Pulmonary hypertension in acute respiratory failure. Crit Care Med. 1989;17(6):523-6.
45. Monchi M, Bellenfant F, Cariou A, Joly LM, Thebert D, Laurent I, Dhainaut JF, Brunet F. Early predictive factors of survival in the acute respiratory distress syndrome. A multivariate analysis. Am J Respir Crit Care Med. 1998;158(4):1076-81.
46. Boissier F, Katsahian S, Razazi K, Thille AW, Roche-Campo F, Leon R, Vivier E, Brochard L, Vieillard-Baron A, Brun-Buisson C, Mekontso DA. Prevalence and prognosis of cor pulmonale during protective ventilation for acute respiratory distress syndrome. Intensive Care Med. 2013;39(10):1725-33.
47. Vieillard-Baron A, Schmitt JM, Augarde R, Fellahi JL, Prin S, Page B, Beauchet A, Jardin F. Acute cor pulmonale in acute respiratory distress syndrome submitted to protective ventilation: incidence, clinical implications, and prognosis. Crit Care Med. 2001;29(8):1551-5.
48. Guervilly C, Forel JM, Hraiech S, Demory D, Allardet-Servent J, Adda M, Barreau-Baumstark K, Castanier M, Papazian L, Roch A. Right ventricular function during high-frequency oscillatory ventilation in adults with acute respiratory distress syndrome. Crit Care Med. 2012;40(5):1539-45.
49. Moloney ED, Evans TW. Pathophysiology and pharmacological treatment of pulmonary hypertension in acute respiratory distress syndrome. Eur Respir J. 2003;21(4):720-7.
50. Comini L, Pasini E, Bachetti T, Dreano M, Garotta G, Ferrari R. Acute haemodynamic effects of IL-6 treatment in vivo: involvement of vagus nerve in NO-mediated negative inotropism. Cytokine. 2005;30(5):236-42.
51. Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science. 1992;257(5068):387-9.
52. Kinugawa K, Takahashi T, Kohmoto O, Yao A, Aoyagi T, Momomura S, Hirata Y, Serizawa T. Nitric oxide-mediated effects of interleukin-6 on [Ca2+]i and cell contraction in cultured chick ventricular myocytes. Circ Res. 1994;75(2):285-95.
53. Yu X, Kennedy RH, Liu SJ. JAK2/STAT3, not ERK1/2, mediates interleukin-6-induced activation of inducible nitric-oxide synthase and decrease in contractility of adult ventricular myocytes. J Biol Chem. 2003;278(18):16304-9.
54. Yu X-W, Chen Q, Kennedy RH, Liu SJ. Inhibition of sarcoplasmic reticular function by chronic interleukin-6 exposure via iNOS in adult ventricular myocytes. J Physiol. 2005;566(Pt 2):327-40.
55. Bhagat K, Hingorani AD, Palacios M, Charles IG, Vallance P. Cytokine-induced venodilatation in humans in vivo: eNOS masquerading as iNOS. Cardiovasc Res. 1999;41(3):754-64.
56. Savale L, Tu L, Rideau D, Izziki M, Maitre B, Adnot S, Eddahibi S. Impact of interleukin-6 on hypoxia-induced pulmonary hypertension and lung inflammation in mice. Respir Res. 2009;10:6.
57. Fagan KA, Tyler RC, Sato K, Fouty BW, Morris Jr KG, Huang PL, McMurtry IF, Rodman DM. Relative contributions of endothelial, inducible, and neuronal NOS to tone in the murine pulmonary circulation. Am J Physiol. 1999;277(3 Pt 1):L472-478.
58. Vistnes M, Waehre A, Nygård S, Sjaastad I, Andersson KB, Husberg C, Christensen G. Circulating cytokine levels in mice with heart failure are etiology dependent. J Appl Physiol. 2010;108(5):1357-64.
59. Souza-Costa DC, Figueiredo-Lopes L, Alves-Filho JC, Semprini MC, Gerlach RF, Cunha FQ, Tanus-Santos JE. Protective effects of atorvastatin in rat models of acute pulmonary embolism: involvement of matrix metalloproteinase-9. Crit Care Med. 2007;35(1):239-45.
60. Schrader LI, Kinzenbaw DA, Johnson AW, Faraci FM, Didion SP. IL-6 deficiency protects against angiotensin II induced endothelial dysfunction and hypertrophy. Arterioscler Thromb Vasc Biol. 2007;27(12):2576-81.