Protective effects of luteolin against lipopolysaccharide-induced acute lung injury involves inhibition of MEK/ERK and PI3K/Akt pathways in neutrophils

Acta Pharmacologica Sinica

Volumn 31, Issue 7, 2010, Pages 831-838

  Lee, Jen Pei ^a   Li, Yi Ching ^b   Chen, Hung Yi ^c   Lin, Ruey Hseng ^c   Huang, Shiang Suo ^c   Chen, Hui Ling ^a   Kuan, Pai Chuan ^d   Liao, Mao Fang ^e   Chen, Chun Jung ^f   Kuan, Yu Hsiang ^b  

^a Da Chien General Hospital   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d Public Health Bureau Taoyuan County Government   (Taiwan)

^e FENG YUAN HOSPITAL   (Taiwan)

^f TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

acute lung injury; chemotaxis; luteolin; mitogen activated protein kinase; neutrophils; PI3K Akt; respiratory burst

Indexed keywords

FORMYLMETHIONYLLEUCYLPHENYLALANINE; LIPOPOLYSACCHARIDE; LUTEOLIN; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SUPEROXIDE; ANTIINFLAMMATORY AGENT; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL INFILTRATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; LEUKOCYTE; LEUKOCYTE ACTIVATION; LUNG; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN CONTENT; RESPIRATORY BURST; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; IC50; INFLAMMATION; INSTITUTE FOR CANCER RESEARCH MOUSE; LONICERA; METABOLISM; PATHOPHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; TOXICITY;

ACUTE LUNG INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INFLAMMATION; INHIBITORY CONCENTRATION 50; LIPOPOLYSACCHARIDES; LONICERA; LUTEOLIN; MALE; MICE; MICE, INBRED ICR; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEUTROPHILS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 77954532054     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2010.62     Document Type: Article

References (47)

1. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000; 342: 1334-1349
2. Brigham KL, Meyrick B. Endotoxin and lung injury. Am Rev Respir Dis 1986; 133: 913-927
3. Mei SHJ, McCarter SD, Deng Y, Parker CH, Liles CW, Stewart DJ. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLOS Med 2007; 4: 1525-1527
4. Moraes TJ, Zurawska JH, Downey GP. Neutrophil granule contents in the pathogenesis of lung injury. Curr Opin Hematol 2006; 13: 21-27
5. Guo RF, Ward PA. Role of oxidants in lung injury during sepsis. Antioxid Redox Sign 2007; 9: 1991-2002.
6. Faurschou M, Borregaard N. Neutrophil granules and secretary vesicles in infammation. Microbes Infect 2003; 5: 1317-1327
7. Klebano SJ. Myeloperoxidase: friend and foe. J Leukocyte Biol 2005; 77: 598-625.
8. Nauseef WM. How human neutrophils kill and degrade microbes: an integrated review. Immunol Rev 2007; 219: 88-102.
9. Abraham E. Neutrophils and acute lung injury. Crit Care Med 2003; 31: S195-9.
10. Lee JH, Ko WS, Kim YH, Kang HS, Kim HD, Choi BT. Antiinfammatory effect of the aqueous extract from Lonicera japonica fower is related to inhibition of NF-kappaB activation through reducing I-kappaBalpha degradation in rat liver. Int J Mol Med 2001; 7: 79-83.
11. López-Lázaro M. Distribution and biological activities of the favonoid luteolin. Mini Rev Med Chem 2009; 9: 31-59.
12. Yu SL, Zhang L, Sun L. Flos Lonicerae's research progress. Lishizhen Med Mater Med Res 2002; 13: 498-499 Chinese.
13. Liu X, Zhang M, He L, Li YP, Kang YK. Chinese herbs combined with Western medicine for severe acute respiratory syndrome (SARS). Cochrane Database Syst Rev 2006; CD004882.
14. Wu CY, Jan JT, Ma SH, Kuo CJ, Juan HF, Cheng YS, et al. Small molecules targeting severe acute respiratory syndrome human coronavirus. Proc Natl Acad Sci USA 2004; 101: 10012-10017
15. Ko HC, Wei BL, Chiou WF. The effect of medicinal plants used in Chinese folk medicine on RANTES secretion by virus-infected human epithelial cells. J Ethnopharmacol 2006; 107: 205-210
16. Kotanidou A, Xagorari A, Bagli E, Kitsanta P, Fotsis T, Papapetropoulos A, et al. Luteolin reduces lipopolysaccharide-induced lethal toxicity and expression of proinfammatory molecules in mice. Am J Respir Crit Care Med 2002; 165: 818-823
17. Das M, Ram A, Ghosh B. Luteolin alleviates bronchoconstriction and airway hyperreactivity in ovalbumin sensitized mice. Inflamm Res 2003; 52: 101-106
18. Tormakangas L, Vuorela P, Saario E, Leinonen M, Saikku P, Vuorela H. In vivo treatment of acute Chlamydia pneumoniae infection with the favonoids quercetin and luteolin and an alkyl gallate, octyl gallate, in a mouse model. Biochem Pharmacol 2005; 70: 1222-1230
19. Comalada M, Ballester I, Bailon E, Sierra S, Xaus J, Galvez J, et al. Inhibition of pro-inflammatory markers in primary bone marrow-derived mouse macrophages by naturally occurring flavonoids: analysis of the structure-activity relationship. Biochem Pharmacol 2006; 72: 1010-1021
20. Chen CY, Peng WH, Tsai KD, Hsu SL. Luteolin suppresses infamma-tion-associated gene expression by blocking NF-κB and AP-1 activation pathway in mouse alveolar macrophages. Life Sci 2007; 81: 1602-1614
21. Xagorari A, Papapetropoulos A, Mauromatis A, Economou M, Fotsis T, Roussos C. Luteolin inhibits an endotoxin-stimulated phosphorylation cascade and proinfammatory cytokine production in macrophages. J Pharmacol Exp Ther 2001; 296: 181-187
22. Harris GK, Qian Y, Leonard SS, Sbarra DC, Shi X. Luteolin and chrysin differentially inhibit cyclooxygenase-2 expression and scavenge reactive oxygen species but similarly inhibit prostaglandin-E2 formation in RAW 264.7 cells. J Nutr 2006; 136: 1517-1521
23. Lu HW, Sugahara K, Sagara Y, Masuoka N, Asaka Y, Manabe M, et al. Effect of three flavonoids, 5,7,3′,4′-tetrahydroxy-3-methoxy favone, luteolin, and quercetin, on the stimulus-induced superoxide generation and tyrosyl phosphorylation of proteins in human neutrophil. Arch Biochem Biophys 2001; 393: 73-77
24. Loke WM, Proudfoot JM, Stewart S, McKinley AJ, Needs PW, Kroon PA, et al. Metabolic transformation has a profound effect on anti-inflammatory activity of flavonoids such as quercetin: lack of association between antioxidant and lipoxygenase inhibitory activity. Biochem Pharmacol 2008; 75: 1045-1053
25. Wagner JG, Harkema JR, Roth RA. Pulmonary leukostasis and the inhibition of airway neutrophil recruitment are early events in the endotoxemic rat. Shock 2002; 17: 151-158
26. Kuan YH, Lin RH, Chen YL, Tsao LT, Tzeng CC, Wang JP. Effective attenuation of acute lung injury in vivo and the formyl peptide-induced neutrophil activation in vitro by CYL-26z through the phosphoinositide 3-kinase gamma pathway. Biochem Pharmacol 2006; 72: 749-760
27. Strieter RM, Kunkel SL, Keane MP, Standiford TJ. Chemokines in lung injury: Thomas A. Neff Lecture. Chest 1999; 116: 103S-110S.
28. Corteling R, Wyss D, Trifilieff A. In vivo models of lung neutrophil activation. Comparison of mice and hamsters. BMC Pharmacol 2002; 2: 1-8.
29. Speyer CL, Rancilio NJ, McClintock SD, Crawford JD, Gao H, Sarma JV, et al. Regulatory effects of estrogen on acute lung infammation in mice. Am J Physiol Cell Physiol 2005; 288: C881-90.
30. Worthen GS, Nick JA. Leukocyte accumulation in the lung. In: Fishman AP, editor. vol.1. Pulmonary diseases disorders. New York: McGraw-Hill; 1998. p325-336.
31. Nick JA, Young SK, Brown KK, Avdi NJ, Arndt PG, Suratt BT, et al. Role of p38 mitogen-activated protein kinase in a murine model of pulmonary infammation. J Immunol 2000; 164: 2151-2159
32. Zu YL, Qi J, Gilchrist A, Fernandez GA, Vazquez-Abad D, Kreutzer DL, et al. p38 mitogen-activated protein kinase activation is required for human neutrophil function triggered by TNF-α or FMLP stimulation. J Immunol 1998; 160: 1982-1989
33. Kuroki M, O'Flaherty JT. Differential effects of a mitogen-activated protein kinase kinase inhibitor on human neutrophil responses to chemotactic factors. Biochem Biophys Res Commun 1997; 232: 474-477
34. Geest CR, Coffer PJ. MAPK signaling pathways in the regulation of hematopoiesis. J Leukoc Biol 2009; 86: 237-250
35. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, et al. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 2000; 287: 1040-1046
36. Yeh CC, Kao SJ, Lina CC. The immunomodulation of endotoxin-induced acute lung injury by hesperidin in vivo and in vitro. Life Sci 2007; 80: 1821-1831
37. Babior BM, Lambeth JD, Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys 2002; 397: 342-344
38. Selvatici R, Falzarano S, Mollica A, Spisani S. Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur J Pharmacol 2006; 534: 1-11
39. Majumdar S, Kane LH, Rossi MW, Volpp BD, Nauseef WM, Korchak HM. Protein kinase C isotypes and signal-transduction in human neutrophils: selective substrate specifcity of calcium-dependent beta-PKC and novel calcium-independent nPKC. Biochim Biophys Acta 1993; 1176: 276-286
40. El Benna J, Faust RP, Johnson JL, Babior BM. Phosphorylation of the respiratory burst oxidase subunit p47phox as determined by two-dimensional phosphopeptide mapping. Phosphorylation by protein kinase C, protein kinase A and a mitogen activated protein kinase. J Biol Chem 1996; 271: 6374-6378
41. Coxon PY, Rane MJ, Uriarte S, Powell DW, Singh S, Butt W, et al. MAPK-activated protein kinase-2 participates in p38 MAPK-dependent and ERK-dependent functions in human neutrophils. Cell Signal 2003; 15: 993-1001.
42. Heuertz RM, Tricomi SM, Ezekiel UR, Webster RO. C-reactive protein inhibits chemotactic peptide-induced p38 mitogen-activated protein kinase activity and human neutrophil movement. J Biol Chem 1999; 274: 17968-17974
43. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001; 70: 535-602.
44. Wymann MP, Zvelebil M, Laffargue M. Phosphoinositide 3-kinase signalling-which way to target? Trends Pharmacol Sci 2003; 24: 366-376
45. Sale EM, Sale GJ. Protein kinase B: signalling roles and therapeutic targeting. Cell Mol Life Sci 2008; 65: 113-127
46. Carroll EJ, Mueller R, Panico L. Chemotactic factors for bovine leukocytes. Am J Vet Res 1982; 43: 1661-1664
47. Schuh K, Pahl A. Inhibition of the MAP kinase ERK protects from lipopolysaccharide-induced lung injury. Biochem Pharmacol 2009; 77: 1827-1834