Betulinic acid attenuates lung injury by modulation of inflammatory cytokine response in experimentally-induced polymicrobial sepsis in mice

Cytokine

Volumn 71, Issue 1, 2015, Pages 101-108

  Lingaraju, Madhu Cholenahalli ^a   Pathak, Nitya Nand ^a   Begum, Jubeda ^a   Balaganur, Venkanna ^a   Bhat, Rafia Ahmad ^a   Ramachandra, Harish Darasaguppe ^a   Ayanur, Anjaneya ^a   Ram, Mahendra ^a   Singh, Vishakha ^a   Kumar, Dhirendra ^a   Kumar, Dinesh ^a   Tandan, Surendra Kumar ^a  

^a INDIAN VETERINARY RESEARCH INSTITUTE   (India)

Author keywords

Cecal ligation and puncture; Cytokines; Inflammatory pulmonary insult; Matrix metalloproteinase (MMP) 9; Triterpenoid

Indexed keywords

BETULIC ACID; CYTOKINE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; NONSTEROID ANTIINFLAMMATORY AGENT; TRITERPENE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; IMMUNOMODULATION; LEUKOCYTE AGGREGATION; LUNG INJURY; LUNG PARENCHYMA; MALE; MIXED INFECTION; MORTALITY; MOUSE; MOUSE MODEL; NEUTROPHIL; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SEPSIS; SURVIVAL RATE; TISSUE LEVEL; WESTERN BLOTTING; ANIMAL; CECUM; COINFECTION; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; PATHOLOGY; ULTRASTRUCTURE;

ACUTE LUNG INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CECUM; COINFECTION; CYTOKINES; DISEASE MODELS, ANIMAL; INTERCELLULAR ADHESION MOLECULE-1; LUNG; MATRIX METALLOPROTEINASE 9; MICE; NF-KAPPA B; SEPSIS; TRITERPENES;

EID: 84910050504     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2014.09.004     Document Type: Article

References (44)

1. Hudson L.D., Milberg J.A., Anardi D., Maunder R.J. Clinical risks for development of the acute respiratory distress syndrome. Am J Respir Crit Care Med 1995, 151:293-301.
2. Rubenfeld G.D., Caldwell E., Peabody E., Weaver J., Martin D.P., Neff M., et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005, 353:1685-1693.
3. Johnson E.R., Matthay M.A. Acute lung injury: epidemiology, pathogenesis, and treatment. J Aerosol Med Pulm Drug Deliv 2010, 23:243-252.
4. Carter A.B., Monick M.M., Hunninghake G.W. Lipopolysaccharide-induced NF-kappaB activation and cytokine release in human alveolar macrophages is PKC-independent and TK- and PC-PLC-dependent. Am J Respir Cell Mol Biol 1998, 18:384-391.
5. Gong Q., Yin H., Fang M., Xiang Y., Yuan C.L., Zheng G.Y., et al. Heme oxygenase-1 upregulation significantly inhibits TNF-α and Hmgb1 releasing and attenuates lipopolysaccharide-induced acute lung injury in mice. Int Immunopharmacol 2008, 8:792-798.
6. Erickson S.E., Martin G.S., Davis J.L., Matthay M.A., Eisner M.D. Recent trends in acute lung injury mortality: 1996-2005. Crit Care Med 2009, 37:1574-1579.
7. Hildebrand F., Pape H.C., Harwood P., Müller K., Hoevel P., Pütz C., et al. Role of adhesion molecule ICAM in the pathogenesis of polymicrobial sepsis. Exp Toxicol Pathol 2005, 56:281-290.
8. Zhao X., Dib M., Andersson E., Shi C., Widegren B., Wang X., et al. Alterations of adhesion molecule expression and inflammatory mediators in acute lung injury induced by septic and non-septic challenges. Lung 2005, 183:87-100.
9. Neviere R.R., Cepinskas G., Madorin W.S., Hoque N., Karmazyn M., Sibbald W.J., et al. LPS pretreatment ameliorates peritonitis-induced myocardial inflammation and dysfunction: role of myocytes. Am J Physiol 1999, 277:885-892.
10. Hoffmann U., Bertsch T., Dvortsak E., Liebetrau C., Lang S., Liebe V., et al. Matrix-metalloproteinases and their inhibitors are elevated in severe sepsis: prognostic value of TIMP-1 in severe sepsis. Scand J Infect Dis 2006, 38:867-872.
11. Cotroneo T.M., Hugunin K.M., Shuster K.A., Hwang H.J., Kakaraparthi B.N., Nemzek-Hamlin J.A. Effects of buprenorphine on a cecal ligation and puncture model in C57BL/6 mice. J Am Assoc Lab Anim Sci 2012, 51:357-365.
12. Dyson A., Singer M. Animal models of sepsis: why does preclinical efficacy fail to translate to the clinical setting?. Crit Care Med 2009, 37:30-37.
13. Rasaiah V.P., Malloy J.L., Lewis J.F., Veldhuizen R.A. Early surfactant administration protects against lung dysfunction in a mouse model of ARDS. Am J Physiol Lung Cell Mol Physiol 2003, 284:783-790.
14. Ekşioğlu-Demiralp E., Kardaş E.R., Ozgül S., Yağci T., Bilgin H., Sehirli O., et al. Betulinic acid protects against ischemia/reperfusion-induced renal damage and inhibits leukocyte apoptosis. Phytother Res 2010, 24:325-332.
15. Zhao H., Holmes S.S., Baker G.A., Challa S., Bose H.S., Song Z. Ionic derivatives of betulinic acid as novel HIV-1 protease inhibitors. J Enzyme Inhib Med Chem 2012, 27:715-721.
16. Takada Y., Aggarwal B.B. Betulinic acid suppresses carcinogen-induced NFkappa B activation through inhibition of I kappa B alpha kinase and p65 phosphorylation: abrogation of cyclooxygenase-2 and matrix metalloprotease-9. J Immunol 2003, 171:3278-3286.
17. Viji V., Helen A., Luxmi V.R. Betulinic acid inhibits endotoxin-stimulated phosphorylation cascade and pro-inflammatory prostaglandin E2 production in human peripheral blood mononuclear cells. Br J Pharmacol 2011, 162:1291-1303.
18. Nader M.A., Baraka H.N. Effect of betulinic acid on neutrophil recruitment and inflammatory mediator expression in lipopolysaccharide-induced lung inflammation in rats. Eur J Pharm Sci 2012, 46:106-113.
19. Zambon M., Vincent J.L. Mortality rates for patients with acute lung injury/ARDS have decreased over time. Chest 2008, 133:1120-1127.
20. Wichmann M.W., Haisken J.M., Ayala A., Chaudry I.H. Melatonin administration following hemorrhagic shock decreases mortality from subsequent septic challenge. J Surg Res 1996, 65:109-114.
21. van Zoelen M.A., Florquin S., Meijers J.C., de Beer R., de Vos A.F., de Boer O.J., et al. Platelet-activating factor receptor contributes to host defense against Pseudomonas aeruginosa pneumonia but is not essential for the accompanying inflammatory and procoagulant response. J Immunol 2008, 180:3357-3365.
22. Asaduzzaman M., Zhang S., Lavasani S., Wang Y., Thorlacius H. LFA-1 and MAC-1 mediate pulmonary recruitment of neutrophils and tissue damage in abdominal sepsis. Shock 2008, 30:254-259.
23. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001, 29:1303-1310.
24. Remick D.G., Newcomb D.E., Bolgos G.L., Call D.R. Comparison of the mortality and inflammatory response of two models of sepsis: lipopolysaccharide versus cecal ligation and puncture. Shock 2000, 13:110-116.
25. Simons R.K., Junger W.G., Loomis W.H., Hoyt D.B. Acute lung injury in endotoxemic rats is associated with sustained circulating IL-6 levels and intrapulmonary CINC activity and neutrophil recruitment-role of circulating TNF-alpha and IL-beta?. Shock 1996, 6:39-45.
26. Rongione A.J., Kusske A.M., Kwan K., Ashley S.W., Reber H.A., McFadden D.W. Interleukin-10 protects against lethality of intra-abdominal infection and sepsis. J Gastrointest Surg 2000, 4:70-76.
27. Standiford T.J., Strieter R.M., Lukacs N.W., Kunkel S.L. Neutralization of IL-10 increases lethality in endotoxemia: cooperative effects of macrophage inflammatory protein-2 and tumor necrosis factor. J Immunol 1995, 155:2222-2229.
28. Walley K.R., Lukacs N.W., Standiford T.J., Strieter R.M., Kunkel S.L. Balance of inflammatory cytokines related to severity and mortality of murine sepsis. Infect Immun 1996, 64:4733-4738.
29. Hasan Z., Palani K., Rahman M., Thorlacius H. Targeting CD44 expressed on neutrophils inhibits lung damage in abdominal sepsis. Shock 2011, 35:567-572.
30. Steinberg K.P., Milberg J.A., Martin T.R., Maunder R.J., Cockrill B.A., Hudson L.D. Evolution of bronchoalveolar cell populations in the adult respiratory distress syndrome. Am J Respir Crit Care Med 1994, 150:113-122.
31. 1. Pharmacol Rev 2000, 52:349-374.
32. Parent C., Eichacker P.Q. Neutrophil and endothelial cell interactions in sepsis. The role of adhesion molecules. Infect Dis Clin North Am 1999, 13:427-447.
33. Puneet P., Hegde A., Ng S.W., Lau H.Y., Lu J., Moochhala S.M., et al. Preprotachykinin-A gene products are key mediators of lung injury in polymicrobial sepsis. J Immunol 2006, 176:3813-3820.
34. Wagner J.G., Birmingham N.P., Jackson-Humbles D., Jiang Q., Harkema J.R., Peden D.B. Supplementation with γ-tocopherol attenuates endotoxin-induced airway neutrophil and mucous cell responses in rats. Free Radical Biol Med 2013, 68:101-109.
35. Bossink A.W., Paemen L., Jansen P.M., Hack C.E., Thijs L.G., van Damme J. Plasma levels of the chemokines monocyte chemotactic proteins-1 and -2 are elevated in human sepsis. Blood 1995, 86:3841-3847.
36. Atkinson J.J., Senior R.M. Matrix metalloproteinase-9 in lung remodeling. Am J Respir Cell Mol Biol 2003, 8:12-24.
37. Ohbayashi H. Matrix metalloproteinases in lung diseases. Curr Protein Pept Sci 2002, 3:409-421.
38. Warner R.L., Beltran L., Younkin E.M., et al. Role of stromelysin 1 and gelatinase B in experimental acute lung injury. Am J Respir Cell Mol Biol 2001, 24:537-544.
39. Renckens R., Roelofs J.J., Florquin S., de Vos A.F., Lijnen H.R., van't Veer C., et al. Matrix metalloproteinase-9 deficiency impairs host defense against abdominal sepsis. J Immunol 2006, 176:3735-3741.
40. McQuibban G.A., Gong J.H., Wong J.P., Wallace J.L., Clark-Lewis I., Overall C.M. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 2002, 100:1160-1167.
41. Bureau F., Delhalle S., Bonizzi G., Fievez L., Dogne S., Kirschvink N., et al. Mechanisms of persistent NF-kappa B activity in the bronchi of an animal model of asthma. J Immunol 2000, 165:5822-5830.
42. Arnalich F., Garcia-Palomero E., López J., Jiménez M., Madero R., Renart J., et al. Predictive value of nuclear factor κB activity and plasma cytokine levels in patients with sepsis. Infect Immun 2000, 68:1942-1945.
43. Ichiki T., Jougasaki M., Setoguchi M., Imamura J., Nakashima H., Matsuoka T., et al. Cardiotrophin-1 stimulates intercellular adhesion molecule-1 and monocyte chemoattractant protein-1 in human aortic endothelial cells. Am J Physiol Heart Circ Physiol 2008, 294:750-763.
44. Collins T., Read M.A., Neish A.S., Whitley M.Z., Thanos D., Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers, FASEB J 1995, 9:899-909.