Lipoxin and resolvin biosynthesis is dependent on 5-lipoxygenase activating protein

FASEB Journal

Volumn 29, Issue 12, 2015, Pages 5029-5043

  Lehmann, Christoph ^a   Homann, Julia ^a   Ball, Ann Katrin ^a   Blöcher, René ^a   Kleinschmidt, Thea K ^b   Basavarajappa, Devaraj ^b   Angioni, Carlo ^a   Ferreirós, Nerea ^a   Häfner, Ann Kathrin ^a   Rådmark, Olof ^b   Proschak, Ewgenij ^a   Haeggström, Jesper Z ^b   Geisslinger, Gerd ^a   Parnham, Michael J ^a   Steinhilber, Dieter ^a   Kahnt, Astrid Stefanie ^a  

^a GOETHE UNIVERSITY   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cytosolic phospholipase A2 ; LTA4 hydrolase; LTC4 synthase; Resolution of inflammation

Indexed keywords

3 [3 TERT BUTYLTHIO 1 (4 CHLOROBENZYL) 5 ISOPROPYL 2 INDOLYL] 2,2 DIMETHYLPROPIONIC ACID; ARACHIDONATE 5 LIPOXYGENASE ACTIVATING PROTEIN; LIPOXIN; LIPOXYGENASE; PHOSPHOLIPASE A2; RESOLVIN; UNCLASSIFIED DRUG; ARACHIDONATE 5 LIPOXYGENASE; DOCOSAHEXAENOIC ACID; INDOLE DERIVATIVE; LIPOXIN A; PHOSPHOLIPASE A2 GROUP IV; RECOMBINANT PROTEIN; RESOLVIN D1;

ARTICLE; BIOSYNTHESIS; BLOOD SAMPLING; CELL DIFFERENTIATION; CELL FREE SYSTEM; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKOCYTE COUNT; LIQUID CHROMATOGRAPHY; MACROPHAGE; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TANDEM MASS SPECTROMETRY; TRANSIENT TRANSFECTION; WESTERN BLOTTING; CYTOSOL; DRUG EFFECTS; ENZYMOLOGY; HEK293 CELL LINE; METABOLISM; TUMOR CELL LINE;

5-LIPOXYGENASE-ACTIVATING PROTEINS; ARACHIDONATE 5-LIPOXYGENASE; CELL LINE, TUMOR; CYTOSOL; DOCOSAHEXAENOIC ACIDS; GROUP IV PHOSPHOLIPASES A2; HEK293 CELLS; HUMANS; INDOLES; LIPOXINS; MACROPHAGES; NEUTROPHILS; RECOMBINANT PROTEINS;

EID: 84973432158     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-275487     Document Type: Article

References (45)

1. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'Neill, L. A., Perretti, M., Rossi, A. G., and Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332
2. Serhan, C. N., Chiang, N., and Van Dyke, T. E. (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361
3. Recchiuti, A. (2013) Resolvin D1 and its GPCRs in resolution circuits of inflammation. Prostaglandins Other Lipid Mediat. 107, 64-76
4. Edenius, C., Haeggström, J., and Lindgren, J. A. (1988) Transcellular conversion of endogenous arachidonic acid to lipoxins in mixed human platelet-granulocyte suspensions. Biochem. Biophys. Res. Commun. 157, 801-807
5. Serhan, C. N., and Sheppard, K. A. (1990) Lipoxin formation during human neutrophil-platelet interactions. Evidence for the transformation of leukotriene A4 by platelet 12-lipoxygenase in vitro. J. Clin. Invest. 85, 772-780
6. Romano, M., Chen, X. S., Takahashi, Y., Yamamoto, S., Funk, C. D., and Serhan, C. N. (1993) Lipoxin synthase activity of human platelet 12-lipoxygenase. Biochem. J. 296, 127-133
7. Levy, B. D., Romano, M., Chapman, H. A., Reilly, J. J., Drazen, J., and Serhan, C. N. (1993) Human alveolar macrophages have 15-lipoxygenase and generate 15(S)-hydroxy-5,8,11-cis-13-trans-eicosatetraenoic acid and lipoxins. J. Clin. Invest. 92, 1572-1579
8. Chavis, C., Vachier, I., Chanez, P., Bousquet, J., and Godard, P. (1996) 5(S),15(S)-dihydroxyeicosatetraenoic acid and lipoxin generation in human polymorphonuclear cells: dual specificity of 5-lipoxygenase towards endogenous and exogenous precursors. J. Exp. Med. 183, 1633-1643
9. Sun, Y.-P., Oh, S. F., Uddin, J., Yang, R., Gotlinger, K., Campbell, E., Colgan, S. P., Petasis, N. A., and Serhan, C. N. (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, antiinflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282, 9323-9334
10. Fiore, S., and Serhan, C. N. (1990) Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils. J. Exp. Med. 172, 1451-1457
11. Romano, M. (2010) Lipoxin and aspirin-triggered lipoxins. Scientific World Journal 10, 1048-1064
12. Levy, B. D. (2010) Resolvins and protectins: natural pharmacophores for resolution biology. Prostaglandins Leukot. Essent. Fatty Acids 82, 327-332
13. Basavarajappa, D., Wan, M., Lukic, A., Steinhilber, D., Samuelsson, B., and Rådmark, O. (2014) Roles of coactosin-like protein (CLP) and 5-lipoxygenase-activating protein (FLAP) in cellular leukotriene biosynthesis. Proc. Natl. Acad. Sci. USA 111, 11371-11376
14. Werz, O., Bürkert, E., Samuelsson, B., Rådmark, O., and Steinhilber, D. (2002) Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes. Blood 99, 1044-1052
15. Michel, A. A., Steinhilber, D., and Werz, O. (2008) Development of a method for expression and purification of the regulatory C2-like domain of human 5-lipoxygenase. Protein Expr. Purif. 59, 110-116
16. Brungs, M., Rådmark, O., Samuelsson, B., and Steinhilber, D. (1995) Sequential induction of 5-lipoxygenase gene expression and activity in Mono Mac 6 cells by transforming growth factor beta and 1,25-dihydroxyvitamin D3. Proc. Natl. Acad. Sci. USA 92, 107-111
17. Schröder, M., Häfner, A.-K., Hofmann, B., Rådmark, O., Tumulka, F., Abele, R., Dötsch, V., and Steinhilber, D. (2014) Stabilisation and characterisation of the isolated regulatory domain of human 5-lipoxygenase. Biochim. Biophys. Acta 1842, 1538-1547
18. Sisignano, M., Angioni, C., Ferreiros, N., Schuh, C.-D., Suo, J., Schreiber, Y., Dawes, J. M., Antunes-Martins, A., Bennett, D. L., McMahon, S. B., Geisslinger, G., and Scholich, K. (2013) Synthesis of lipid mediators during UVB-induced inflammatory hyperalgesia in rats and mice. PLoS One 8, e81228
19. Homann, J., Lehmann, C., Kahnt, A. S., Steinhilber, D., Parnham, M. J., Geisslinger, G., and Ferreirós, N. (2014) Chiral chromatography-tandem mass spectrometry applied to the determination of pro-resolving lipid mediators. J. Chromatogr. A 1360, 150-163
20. Werz, O., Brungs, M., and Steinhilber, D. (1996) Purification of transforming growth factor beta 1 from human platelets. Pharmazie 51, 893-896
21. Moser, D., Wittmann, S. K., Kramer, J., Blöcher, R., Achenbach, J., Pogoryelov, D., and Proschak, E. (2015) PENG: a neural gas-based approach for pharmacophore elucidation. method design, validation, and virtual screening for novel ligands of LTA4H. J. Chem. Inf. Model. 55, 284-293
22. Rådmark, O., and Samuelsson, B. (2010) Regulation of the activity of 5-lipoxygenase, a key enzyme in leukotriene biosynthesis. Biochem. Biophys. Res. Commun. 396, 105-110
23. Mancini, J. A., Waterman, H., and Riendeau, D. (1998) Cellular oxygenation of 12-hydroxyeicosatetraenoic acid and 15-hydroxyeicosatetraenoic acid by 5-lipoxygenase is stimulated by 5-lipoxygenase-activating protein. J. Biol. Chem. 273, 32842-32847
24. Mancini, J. A., Abramovitz, M., Cox, M. E., Wong, E., Charleson, S., Perrier, H., Wang, Z., Prasit, P., and Vickers, P. J. (1993) 5-Lipoxygenase-activating protein is an arachidonate binding protein. FEBS Lett. 318, 277-281
25. Abramovitz, M., Wong, E., Cox, M. E., Richardson, C. D., Li, C., and Vickers, P. J. (1993) 5-Lipoxygenase-activating protein stimulates the utilization of arachidonic acid by 5-lipoxygenase. Eur. J. Biochem. 215, 105-111
26. Rouzer, C. A., Ford-Hutchinson, A. W., Morton, H. E., and Gillard, J. W. (1990) MK886, a potent and specific leukotriene biosynthesis inhibitor blocks and reverses the membrane association of 5-lipoxygenase in ionophore-challenged leukocytes. J. Biol. Chem. 265, 1436-1442
27. Kulkarni, S., Das, S., Funk, C. D., Murray, D., and Cho, W. (2002) Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J. Biol. Chem. 277, 13167-13174
28. Hörnig, C., Albert, D., Fischer, L., Hörnig, M., Rådmark, O., Steinhilber, D., and Werz, O. (2005) 1-Oleoyl-2-acetylglycerol stimulates 5-lipoxygenase activity via a putative (phospho)lipid binding site within the N-terminal C2-like domain. J. Biol. Chem. 280, 26913-26921
29. Charleson, S., Evans, J. F., Léger, S., Perrier, H., Prasit, P., Wang, Z., and Vickers, P. J. (1994) Structural requirements for the binding of fatty acids to 5-lipoxygenase-activating protein. Eur. J. Pharmacol. 267, 275-280
30. Norris, P. C., Gosselin, D., Reichart, D., Glass, C. K., and Dennis, E. A. (2014) Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc. Natl. Acad. Sci. USA 111, 12746-12751
31. Koeberle, A., Siemoneit, U., Northoff, H., Hofmann, B., Schneider, G., and Werz, O. (2009) MK-886, an inhibitor of the 5-lipoxygenase-activating protein, inhibits cyclooxygenase-1 activity and suppresses platelet aggregation. Eur. J. Pharmacol. 608, 84-90
32. Rao, N. L., Dunford, P. J., Xue, X., Jiang, X., Lundeen, K. A., Coles, F., Riley, J. P., Williams, K. N., Grice, C. A., Edwards, J. P., Karlsson, L., and Fourie, A. M. (2007) Anti-inflammatory activity of a potent, selective leukotriene A4 hydrolase inhibitor in comparison with the 5-lipoxygenase inhibitor zileuton. J. Pharmacol. Exp. Ther. 321, 1154-1160
33. Rao, N. L., Riley, J. P., Banie, H., Xue, X., Sun, B., Crawford, S., Lundeen, K. A., Yu, F., Karlsson, L., Fourie, A. M., and Dunford, P. J. (2010) Leukotriene A(4) hydrolase inhibition attenuates allergic airway inflammation and hyperresponsiveness. Am. J. Respir. Crit. Care Med. 181, 899-907
34. Petrich, K., Ludwig, P., Kühn, H., and Schewe, T. (1996) The suppression of 5-lipoxygenation of arachidonic acid in human polymorphonuclear leucocytes by the 15-lipoxygenase product (15S)-hydroxy-(5Z,8Z,11Z,13E)-eicosatetraenoic acid: structure-activity relationship and mechanism of action. Biochem. J. 314, 911-916
35. Fredman, G., Ozcan, L., Spolitu, S., Hellmann, J., Spite, M., Backs, J., and Tabas, I. (2014) Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-activated kinase pathway. Proc. Natl. Acad. Sci. USA 111, 14530-14535
36. Kaaman, M., Rydén, M., Axelsson, T., Nordström, E., Sicard, A., Bouloumié, A., Langin, D., Arner, P., and Dahlman, I. (2006) ALOX5AP expression, but not gene haplotypes, is associated with obesity and insulin resistance. Int. J. Obes. 30, 447-452
37. Horrillo, R., González-Périz, A., Martínez-Clemente, M., López-Parra, M., Ferré, N., Titos, E., Morán-Salvador, E., Deulofeu, R., Arroyo, V., and Clària, J. (2010) 5-Lipoxygenase activating protein signals adipose tissue inflammation and lipid dysfunction in experimental obesity. J. Immunol. 184, 3978-3987
38. Bäck, M., Sultan, A., Ovchinnikova, O., and Hansson, G. K. (2007) 5-Lipoxygenase-activating protein: a potential link between innate and adaptive immunity in atherosclerosis and adipose tissue inflammation. Circ. Res. 100, 946-949
39. Zhao, L., Moos, M. P. W., Gräbner, R., Pédrono, F., Fan, J., Kaiser, B., John, N., Schmidt, S., Spanbroek, R., Lötzer, K., Huang, L., Cui, J., Rader, D. J., Evans, J. F., Habenicht, A. J. R., and Funk, C. D. (2004) The 5-lipoxygenase pathway promotes pathogenesis of hyperlipidemia-dependent aortic aneurysm. Nat. Med. 10, 966-973
40. Kuhn, H., Banthiya, S., and van Leyen, K. (2015) Mammalian lipoxygenases and their biological relevance. Biochim. Biophys. Acta 1851, 308-330
41. Miki, Y., Yamamoto, K., Taketomi, Y., Sato, H., Shimo, K., Kobayashi, T., Ishikawa, Y., Ishii, T., Nakanishi, H., Ikeda, K., Taguchi, R., Kabashima, K., Arita, M., Arai, H., Lambeau, G., Bollinger, J. M., Hara, S., Gelb, M. H., and Murakami, M. (2013) Lymphoid tissue phospholipase A2 group IID resolves contact hypersensitivity by driving antiinflammatory lipid mediators. J. Exp. Med. 210, 1217-1234
42. Brezinski, M. E., and Serhan, C. N. (1990) Selective incorporation of (15S)-hydroxyeicosatetraenoic acid in phosphatidylinositol of human neutrophils: agonist-induced deacylation and transformation of stored hydroxyeicosanoids. Proc. Natl. Acad. Sci. USA 87, 6248-6252
43. Maclouf, J. A., and Murphy, R. C. (1988) Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets. A potential cellular source of leukotriene C4. J. Biol. Chem. 263, 174-181
44. Edenius, C., Heidvall, K., and Lindgren, J. A. (1988) Novel transcellular interaction: conversion of granulocyte-derived leukotriene A4 to cysteinyl-containing leukotrienes by human platelets. Eur. J. Biochem. 178, 81-86
45. Antoine, C., Murphy, R. C., Henson, P. M., and Maclouf, J. (1992) Time-dependent utilization of platelet arachidonic acid by the neutrophil in formation of 5-lipoxygenase products in platelet-neutrophil co-incubations. Biochim. Biophys. Acta 1128, 139-146