Propofol inhibits superoxide production, elastase release, and chemotaxis in formyl peptide-activated human neutrophils by blocking formyl peptide receptor 1

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 6511-6519

  Yang, Shun Chin ^a,b   Chung, Pei Jen ^b   Ho, Chiu Ming ^a,c   Kuo, Chan Yen ^b   Hung, Min Fa ^b   Huang, Yin Ting ^b   Chang, Wen Yi ^b   Chang, Ya Wen ^b   Chan, Kwok Hon ^a,c   Hwang, Tsong Long ^b,d  

^a TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; ELASTASE; FORMYLPEPTIDE; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROPOFOL; PROTEIN KINASE B; SUPEROXIDE; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CALCIUM MOBILIZATION; CELL DIFFERENTIATION; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEGRANULATION; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; EMBRYO; ENZYME PHOSPHORYLATION; ENZYME RELEASE; HUMAN; HUMAN CELL; IC 50; LEUKOCYTE ACTIVATION; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

CHEMOTAXIS, LEUKOCYTE; HUMANS; HYPNOTICS AND SEDATIVES; IMMUNE SYSTEM DISEASES; IMMUNOBLOTTING; LEUKOCYTE DISORDERS; NEUTROPHIL ACTIVATION; NEUTROPHILS; PANCREATIC ELASTASE; PROPOFOL; RECEPTORS, FORMYL PEPTIDE; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84879121228     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202215     Document Type: Article

References (57)

1. Marik, P. E. 2005. Propofol: an immunomodulating agent. Pharmacotherapy 25: 28S-33S. (Pubitemid 40604876)
2. Taniguchi, T., K. Yamamoto, N. Ohmoto, K. Ohta, and T. Kobayashi. 2000. Effects of propofol on hemodynamic and inflammatory responses to endotoxemia in rats. Crit. Care Med. 28: 1101-1106. (Pubitemid 30262086)
3. Taniguchi, T., H. Kanakura, and K. Yamamoto. 2002. Effects of posttreatment with propofol on mortality and cytokine responses to endotoxin-induced shock in rats. Crit. Care Med. 30: 904-907. (Pubitemid 34297816)
4. Takao, Y., K. Mikawa, K. Nishina, and H. Obara. 2005. Attenuation of acute lung injury with propofol in endotoxemia. Anesth. Analg. 100: 810-816 (table of contents). (Pubitemid 40300081)
5. Chen, H. I., N. K. Hsieh, S. J. Kao, and C. F. Su. 2008. Protective effects of propofol on acute lung injury induced by oleic acid in conscious rats. Crit. Care Med. 36: 1214-1221. (Pubitemid 351482671)
6. Corcoran, T. B., A. Engel, H. Sakamoto, S. O'Callaghan-Enright, A. O'Donnell, J. A. Heffron, and G. Shorten. 2004. The effects of propofol on lipid peroxidation and inflammatory response in elective coronary artery bypass grafting. J. Cardiothorac. Vasc. Anesth. 18: 592-604. (Pubitemid 39369958)
7. An, K., H. Shu, W. Huang, X. Huang, M. Xu, L. Yang, K. Xu, and C. Wang. 2008. Effects of propofol on pulmonary inflammatory response and dysfunction induced by cardiopulmonary bypass. Anaesthesia 63: 1187-1192.
8. Shiratsuchi, H., Y. Kouatli, G. X. Yu, H. M. Marsh, and M. D. Basson. 2009. Propofol inhibits pressure-stimulated macrophage phagocytosis via the GABAA receptor and dysregulation of p130cas phosphorylation. Am. J. Physiol. Cell Physiol. 296: C1400-C1410.
9. Wheeler, D. W., A. J. Thompson, F. Corletto, J. Reckless, J. C. Loke, N. Lapaque, A. J. Grant, P. Mastroeni, D. J. Grainger, C. L. Padgett, et al. 2011. Anaesthetic impairment of immune function is mediated via GABA(A) receptors. PLoS One 6: e17152.
10. Chen, R. M., C. H. Wu, H. C. Chang, G. J. Wu, Y. L. Lin, J. R. Sheu, and T. L. Chen. 2003. Propofol suppresses macrophage functions and modulates mitochondrial membrane potential and cellular adenosine triphosphate synthesis. Anesthesiology 98: 1178-1185.
11. Hsing, C. H., M. C. Lin, P. C. Choi, W. C. Huang, J. I. Kai, C. C. Tsai, Y. L. Cheng, C. Y. Hsieh, C. Y. Wang, Y. P. Chang, et al. 2011. Anesthetic propofol reduces endotoxic inflammation by inhibiting reactive oxygen species-regulated Akt/IKKb/NF-kB signaling. PLoS One 6: e17598.
12. Jensen, A. G., C. Dahlgren, and C. Eintrei. 1993. Propofol decreases random and chemotactic stimulated locomotion of human neutrophils in vitro. Br. J. Anaesth. 70: 99-100. (Pubitemid 23019252)
13. Fröhlich, D., G. Rothe, B. Schwall, G. Schmitz, J. Hobbhahn, and K. Taeger. 1996. Thiopentone and propofol, but not methohexitone nor midazolam, inhibit neutrophil oxidative responses to the bacterial peptide FMLP. Eur. J. Anaesthesiol. 13: 582-588. (Pubitemid 26402385)
14. Davidson, J. A., S. J. Boom, F. J. Pearsall, P. Zhang, and G. Ramsay. 1995. Comparison of the effects of four i.v. anaesthetic agents on polymorphonuclear leucocyte function. Br. J. Anaesth. 74: 315-318.
15. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
16. Brown, K. A., S. D. Brain, J. D. Pearson, J. D. Edgeworth, S. M. Lewis, and D. F. Treacher. 2006. Neutrophils in development of multiple organ failure in sepsis. Lancet 368: 157-169.
17. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182. (Pubitemid 43290987)
18. Jordan, J. E., Z. Q. Zhao, and J. Vinten-Johansen. 1999. The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc. Res. 43: 860-878. (Pubitemid 29413185)
19. Abraham, E. 2003. Neutrophils and acute lung injury. Crit. Care Med. 31: S195-S199. (Pubitemid 36458167)
20. Looney, M. R., X. Su, J. A. Van Ziffle, C. A. Lowell, and M. A. Matthay. 2006. Neutrophils and their Fc gamma receptors are essential in a mouse model of transfusion-related acute lung injury. J. Clin. Invest. 116: 1615-1623.
21. Ye, R. D., F. Boulay, J. M. Wang, C. Dahlgren, C. Gerard, M. Parmentier, C. N. Serhan, and P. M. Murphy. 2009. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61: 119-161.
22. Ishibashi, K., S. Okazaki, and M. Hiramatsu. 2006. Simultaneous measurement of superoxide generation and intracellular Ca2+ concentration reveals the effect of extracellular Ca2+ on rapid and transient contents of superoxide generation in differentiated THP-1 cells. Biochem. Biophys. Res. Commun. 344: 571-580.
23. Hwang, T. L., H. W. Hung, S. H. Kao, C. M. Teng, C. C. Wu, and S. J. Cheng. 2003. Soluble guanylyl cyclase activator YC-1 inhibits human neutrophil functions through a cGMP-independent but cAMP-dependent pathway. Mol. Pharmacol. 64: 1419-1427.
24. Yu, H. P., P. W. Hsieh, Y. J. Chang, P. J. Chung, L. M. Kuo, and T. L. Hwang. 2011. 2-(2-Fluorobenzamido)benzoate ethyl ester (EFB-1) inhibits superoxide production by human neutrophils and attenuates hemorrhagic shock-induced organ dysfunction in rats. Free Radic. Biol. Med. 50: 1737-1748.
25. Ernst, S., C. Lange, A. Wilbers, V. Goebeler, V. Gerke, and U. Rescher. 2004. An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J. Immunol. 172: 7669-7676. (Pubitemid 38747633)
26. McHugh, D., C. Tanner, R. Mechoulam, R. G. Pertwee, and R. A. Ross. 2008. Inhibition of human neutrophil chemotaxis by endogenous cannabinoids and phytocannabinoids: evidence for a site distinct from CB1 and CB2. Mol. Pharmacol. 73: 441-450. (Pubitemid 351159214)
27. Stenfeldt, A. L., J. Karlsson, C. Wennerås, J. Bylund, H. Fu, and C. Dahlgren. 2007. The non-steroidal anti-inflammatory drug piroxicam blocks ligand binding to the formyl peptide receptor but not the formyl peptide receptor like 1. Biochem. Pharmacol. 74: 1050-1056. (Pubitemid 47284009)
28. Hwang, T. L., C. C. Wang, Y. H. Kuo, H. C. Huang, Y. C. Wu, L. M. Kuo, and Y. H. Wu. 2010. The hederagenin saponin SMG-1 is a natural FMLP receptor inhibitor that suppresses human neutrophil activation. Biochem. Pharmacol. 80: 1190-1200.
29. Yu, H. P. 2011. Role of anesthetic agents on cardiac and immune systems. Shock 36: 532-541.
30. Kokita, N., A. Hara, Y. Abiko, J. Arakawa, H. Hashizume, and A. Namiki. 1998. Propofol improves functional and metabolic recovery in ischemic reperfused isolated rat hearts. Anesth. Analg. 86: 252-258. (Pubitemid 28079471)
31. Yu, H. P., P. W. Lui, T. L. Hwang, C. H. Yen, and Y. T. Lau. 2006. Propofol improves endothelial dysfunction and attenuates vascular superoxide production in septic rats. Crit. Care Med. 34: 453-460.
32. Corcoran, T. B., A. Engel, H. Sakamoto, A. O'Shea, S. O'Callaghan-Enright, and G. D. Shorten. 2006. The effects of propofol on neutrophil function, lipid peroxidation and inflammatory response during elective coronary artery bypass grafting in patients with impaired ventricular function. Br. J. Anaesth. 97: 825-831. (Pubitemid 44823668)
33. Murphy, P. G., A. J. Ogilvy, and S. M. Whiteley. 1996. The effect of propofol on the neutrophil respiratory burst. Eur. J. Anaesthesiol. 13: 471-473. (Pubitemid 26326363)
34. Mikawa, K., H. Akamatsu, K. Nishina, M. Shiga, N. Maekawa, H. Obara, and Y. Niwa. 1998. Propofol inhibits human neutrophil functions. Anesth. Analg. 87: 695-700. (Pubitemid 28397501)
35. Gülçin, I., H. A. Alici, and M. Cesur. 2005. Determination of in vitro antioxidant and radical scavenging activities of propofol. Chem. Pharm. Bull. 53: 281-285. (Pubitemid 40879897)
36. Nadel, J. A. 2000. Role of neutrophil elastase in hypersecretion during COPD exacerbations, and proposed therapies. Chest 117: 386S-389S. (Pubitemid 30314472)
37. McDonald, B., K. Pittman, G. B. Menezes, S. A. Hirota, I. Slaba, C. C. Waterhouse, P. L. Beck, D. A. Muruve, and P. Kubes. 2010. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
38. Hofbauer, R., M. Frass, H. Salfinger, D. Moser, S. Hornykewycz, B. Gmeiner, and S. Kapiotis. 1999. Propofol reduces the migration of human leukocytes through endothelial cell monolayers. Crit. Care Med. 27: 1843-1847. (Pubitemid 29455114)
39. Nagata, T., M. Kansha, K. Irita, and S. Takahashi. 2001. Propofol inhibits FMLP-stimulated phosphorylation of p42 mitogen-activated protein kinase and chemotaxis in human neutrophils. Br. J. Anaesth. 86: 853-858. (Pubitemid 32514901)
40. Bhat, R., R. Axtell, A. Mitra, M. Miranda, C. Lock, R. W. Tsien, and L. Steinman. 2010. Inhibitory role for GABA in autoimmune inflammation. Proc. Natl. Acad. Sci. USA 107: 2580-2585.
41. Alam, S., D. L. Laughton, A. Walding, and A. J. Wolstenholme. 2006. Human peripheral blood mononuclear cells express GABAA receptor subunits. Mol. Immunol. 43: 1432-1442. (Pubitemid 43356383)
42. Forsman, H., E. Andréasson, J. Karlsson, F. Boulay, M. J. Rabiet, and C. Dahlgren. 2012. Structural characterization and inhibitory profile of formyl peptide receptor 2 selective peptides descending from a PIP2-binding domain of gelsolin. J. Immunol. 189: 629-637.
43. Simchowitz, L., L. C. Fischbein, I. Spilberg, and J. P. Atkinson. 1980. Induction of a transient elevation in intracellular levels of adenosine-3′,5′-cyclic monophosphate by chemotactic factors: an early event in human neutrophil activation. J. Immunol. 124: 1482-1491. (Pubitemid 10136005)
44. Smolen, J. E., H. M. Korchak, and G. Weissmann. 1980. Increased levels of cyclic adenosine-3′,5′-monophosphate in human polymorphonuclear leukocytes after surface stimulation. J. Clin. Invest. 65: 1077-1085. (Pubitemid 10043603)
45. Mahadeo, D. C., M. Janka-Junttila, R. L. Smoot, P. Roselova, and C. A. Parent. 2007. A chemoattractant-mediated Gi-coupled pathway activates adenylyl cyclase in human neutrophils. Mol. Biol. Cell 18: 512-522. (Pubitemid 46213220)
46. Serezani, C. H., M. N. Ballinger, D. M. Aronoff, and M. Peters-Golden. 2008. Cyclic AMP: master regulator of innate immune cell function. Am. J. Respir. Cell Mol. Biol. 39: 127-132.
47. Vlahos, C. J., W. F. Matter, R. F. Brown, A. E. Traynor-Kaplan, P. G. Heyworth, E. R. Prossnitz, R. D. Ye, P. Marder, J. A. Schelm, K. J. Rothfuss, et al. 1995. Investigation of neutrophil signal transduction using a specific inhibitor of phosphatidylinositol 3-kinase. J. Immunol. 154: 2413-2422.
48. Hwang, T. L., Y. C. Su, H. L. Chang, Y. L. Leu, P. J. Chung, L. M. Kuo, and Y. J. Chang. 2009. Suppression of superoxide anion and elastase release by C18 unsaturated fatty acids in human neutrophils. J. Lipid Res. 50: 1395-1408.
49. Rane, M. J., S. L. Carrithers, J. M. Arthur, J. B. Klein, and K. R. McLeish. 1997. Formyl peptide receptors are coupled to multiple mitogen-activated protein kinase cascades by distinct signal transduction pathways: role in activation of reduced nicotinamide adenine dinucleotide oxidase. J. Immunol. 159: 5070-5078. (Pubitemid 127471046)
50. Erol, A., R. Reisli, I. Reisli, R. Kara, and S. Otelcioglu. 2009. Effects of desflurane, sevoflurane and propofol on phagocytosis and respiratory burst activity of human polymorphonuclear leucocytes in bronchoalveolar lavage. Eur. J. Anaesthesiol. 26: 150-154.
51. Fröhlich, D., B. Trabold, G. Rothe, K. Hoerauf, and S. Wittmann. 2006. Inhibition of the neutrophil oxidative response by propofol: preserved in vivo function despite in vitro inhibition. Eur. J. Anaesthesiol. 23: 948-953. (Pubitemid 44622949)
52. Carp, H. 1982. Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. J. Exp. Med. 155: 264-275. (Pubitemid 12209828)
53. Marasco, W. A., S. H. Phan, H. Krutzsch, H. J. Showell, D. E. Feltner, R. Nairn, E. L. Becker, and P. A. Ward. 1984. Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J. Biol. Chem. 259: 5430-5439. (Pubitemid 14144994)
54. Hauser, C. J., T. Sursal, E. K. Rodriguez, P. T. Appleton, Q. Zhang, and K. Itagaki. 2010. Mitochondrial damage associated molecular patterns from femoral reamings activate neutrophils through formyl peptide receptors and P44/42 MAP kinase. J. Orthop. Trauma 24: 534-538.
55. Raoof, M., Q. Zhang, K. Itagaki, and C. J. Hauser. 2010. Mitochondrial peptides are potent immune activators that activate human neutrophils via FPR-1. J. Trauma 68: 1328-1332; discussion 1332-1324.
56. Zhang, Q., M. Raoof, Y. Chen, Y. Sumi, T. Sursal, W. Junger, K. Brohi, K. Itagaki, and C. J. Hauser. 2010. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107.
57. Cevik-Aras, H., C. Kalderén, A. Jenmalm Jensen, T. Oprea, C. Dahlgren, and H. Forsman. 2012. A non-peptide receptor inhibitor with selectivity for one of the neutrophil formyl peptide receptors, FPR 1. Biochem. Pharmacol. 83: 1655-1662.