5-Lipoxygenase, a key enzyme for leukotriene biosynthesis in health and disease

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 4, 2015, Pages 331-339

  Rådmark, Olof ^a   Werz, Oliver ^b   Steinhilber, Dieter ^c   Samuelsson, Bengt ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Arachidonic acid; Eicosanoid; Inflammation; Oxylipin

Indexed keywords

5,8,11 ICOSATRIENOIC ACID; 5,8,11,14,17 ICOSAPENTAENOIC ACID; ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONATE 5 LIPOXYGENASE ACTIVATING PROTEIN; CALCIUM ION; COACTOSIN LIKE PROTEIN; DIACYLGLYCEROL; DICER; GLUTATHIONE PEROXIDASE; LEUKOTRIENE; LEUKOTRIENE A4; LEUKOTRIENE B4; LEUKOTRIENE D4; LEUKOTRIENE E4; PROTEIN; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

BIOSYNTHESIS; CATALYSIS; CELL MEMBRANE; CELLULAR DISTRIBUTION; DISEASES; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FATTY ACID METABOLISM; HUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SEX DIFFERENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; HOMEOSTASIS; INFLAMMATION; METABOLISM; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; CATALYSIS; FATTY ACIDS, UNSATURATED; HOMEOSTASIS; HUMANS; INFLAMMATION; LEUKOTRIENES; MODELS, MOLECULAR; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84922553449     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.08.012     Document Type: Review

References (112)

1. B. Samuelsson Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation Science 220 4597 1983 568 575
2. A. Munoz-Garcia The importance of the lipoxygenase-hepoxilin pathway in the mammalian epidermal barrier Biochim. Biophys. Acta 1841 3 2014 401 408
3. O. Radmark Arachidonate 5-lipoxygenase Prostaglandins Other Lipid Mediat. 68-69 2002 211 234
4. M. Abramovitz 5-Lipoxygenase-activating protein stimulates the utilization of arachidonic acid by 5-lipoxygenase Eur. J. Biochem. 215 1 1993 105 111
5. M. Rakonjac Coactosin-like protein supports 5-lipoxygenase enzyme activity and up-regulates leukotriene A4 production Proc. Natl. Acad. Sci. U. S. A. 103 35 2006 13150 13155
6. D.K. MacMillan Eosinophil 15-lipoxygenase is a leukotriene A4 synthase J. Biol. Chem. 269 43 1994 26663 26668
7. W.S. Powell, and J. Rokach Biochemistry, biology and chemistry of the 5-lipoxygenase product 5-oxo-ETE Prog. Lipid Res. 44 2-3 2005 154 183
8. C.N. Serhan Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways Annu. Rev. Immunol. 25 2007 101 137
9. B.D. Levy Resolution of inflammation in asthma Clin. Chest Med. 33 3 2012 559 570
10. S.A. Gillmor The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity [published erratum appears in Nat Struct Biol 1998 Mar;5(3):242] Nat. Struct. Biol. 4 12 1997 1003 1009
11. N.C. Gilbert The structure of human 5-lipoxygenase Science 331 6014 2011 217 219
12. P. Eek Structure of a calcium-dependent 11R-lipoxygenase suggests a mechanism for Ca2 +-regulation J. Biol. Chem. 287 26 2012 22377 22386
13. A.K. Hafner Dimerization of human 5-lipoxygenase Biol. Chem. 392 12 2011 1097 1111
14. S. Kulkarni Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase J. Biol. Chem. 277 15 2002 13167 13174
15. J.B. Allard, and T.G. Brock Structural organization of the regulatory domain of human 5-lipoxygenase Curr. Protein Pept. Sci. 6 2 2005 125 131
16. Y.Y. Zhang Iron content of human 5-lipoxygenase, effects of mutations regarding conserved histidine residues J. Biol. Chem. 268 4 1993 2535 2541
17. T. Hammarberg Mutations at the C-terminal isoleucine and other potential iron ligands of 5-lipoxygenase Eur. J. Biochem. 230 2 1995 401 407
18. O. Radmark Arachidonate 5-lipoxygenase J Lipid Mediat. Cell Signal. 12 2-3 1995 171 184
19. M.D. Percival, and M. Ouellet The characterization of 5 histidine-serine mutants of human 5-lipoxygenase Biochem. Biophys. Res. Commun. 186 3 1992 1265 1270
20. D.R. Tomchick Structural and functional characterization of second-coordination sphere mutants of soybean lipoxygenase-1 Biochemistry 40 25 2001 7509 7517
21. H. Okamoto Mutation analysis of the human 5-lipoxygenase C-terminus: support for a stabilizing C-terminal loop Biochim. Biophys. Acta 1749 1 2005 123 131
22. M. Walther The N-terminal beta-barrel domain of mammalian lipoxygenases including mouse 5-lipoxygenase is not essential for catalytic activity and membrane binding but exhibits regulatory functions Arch. Biochem. Biophys. 516 1 2011 1 9
23. M. Rakonjac Ryge A mutation interfering with 5-lipoxygenase domain interaction leads to increased enzyme activity Arch. Biochem. Biophys. 545 2014 179 185
24. K. Hofheinz Conversion of pro-inflammatory murine Alox5 into an anti-inflammatory 15S-lipoxygenating enzyme by multiple mutations of sequence determinants Arch. Biochem. Biophys. 530 1 2013 40 47
25. K. Schwarz Alterations in leukotriene synthase activity of the human 5-lipoxygenase by site-directed mutagenesis affecting its positional specificity Biochemistry 39 47 2000 14515 14521
26. J.F. Evans What's all the FLAP about?: 5-lipoxygenase-activating protein inhibitors for inflammatory diseases Trends Pharmacol. Sci. 29 2 2008 72 78
27. P.J. Jakobsson Membrane-associated proteins in eicosanoid and glutathione metabolism (MAPEG). A widespread protein superfamily Am. J. Respir. Crit. Care Med. 161 2 Pt 2 2000 S20 S24
28. A.K. Mandal The membrane organization of leukotriene synthesis Proc. Natl. Acad. Sci. U. S. A. 10 17 2004 6587 6592 (Epub 2004 Apr 6514)
29. H. Plante 5-Lipoxygenase activating protein homodimer in human neutrophils. Evidence for a role in leukotriene synthesis Biochem. J. 393 2006 211 218
30. A.D. Ferguson Crystal structure of inhibitor-bound human 5-lipoxygenase-activating protein Science 317 5837 2007 510 512
31. A.K. Mandal The nuclear membrane organization of leukotriene synthesis Proc. Natl. Acad. Sci. U. S. A. 105 51 2008 20434 20439
32. T. Strid Distinct parts of leukotriene C(4) synthase interact with 5-lipoxygenase and 5-lipoxygenase activating protein Biochem. Biophys. Res. Commun. 381 4 2009 518 522
33. H.J. You Leukotriene synthesis in response to A23187 is inhibited by methyl- beta-cyclodextrin in RBL-2H3 cells Mol. Cells 23 1 2007 57 63
34. R.S. Boyd Protein profiling of plasma membranes defines aberrant signaling pathways in mantle cell lymphoma Mol. Cell. Proteomics 8 7 2009 1501 1515
35. D. Jethwaney Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils Proteome Sci. 5 2007 12
36. J. Esser Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration J. Allergy Clin. Immunol. 126 5 2010 1032 1040
37. X. Hou Coactosin accelerates cell dynamism by promoting actin polymerization Dev. Biol. 379 1 2013 53 63
38. P. Provost Interaction of 5-lipoxygenase with cellular proteins Proc. Natl. Acad. Sci. U. S. A. 96 5 1999 1881 1885
39. P. Provost 5-Lipoxygenase interacts with coactosin-like protein J. Biol. Chem. 276 19 2001 16520 16527
40. J. Esser Coactosin-like protein functions as a stabilizing chaperone for 5-lipoxygenase: role of tryptophan 102 Biochem. J. 425 1 2009 265 274
41. C. Feisst Hyperforin is a novel type of 5-lipoxygenase inhibitor with high efficacy in vivo Cell. Mol. Life Sci. 66 16 2009 2759 2771
42. T.G. Brock Capturing proteins that bind polyunsaturated fatty acids: demonstration using arachidonic acid and eicosanoids Lipids 43 2008 161 169
43. P. Provost Coactosin-like protein, a human F-actin-binding protein: critical role lysine-75 Biochem. J. 359 Part 2 2001 255 263
44. E. Liepinsh NMR structure of human coactosin-like protein. J Biomol NMR 30 2004 353 356
45. M.P. Perron, and P. Provost Protein components of the microRNA pathway and human diseases Methods Mol. Biol. 487 2009 369 385
46. P. Provost Ribonuclease activity and RNA binding of recombinant human Dicer EMBO J. 21 21 2002 5864 5874
47. V. Dincbas-Renqvist Human Dicer C-terminus functions as a 5-lipoxygenase binding domain Biochim. Biophys. Acta 1789 2 2009 99 108
48. A. Sala Transcellular biosynthesis of eicosanoids Pharmacol. Rep. 62 3 2010 503 510
49. O. Werz, and D. Steinhilber Development of 5-lipoxygenase inhibitors - lessons from cellular enzyme regulation Biochem. Pharmacol. 70 3 2005 327 333
50. C.C. Leslie Regulation of the specific release of arachidonic acid by cytosolic phospholipase A2 Prostaglandins Leukot. Essent. Fatty Acids 70 4 2004 373 376
51. O. Werz 5-Lipoxygenase: cellular biology and molecular pharmacology Curr. Drug Targets Inflamm. Allergy 1 1 2002 23 44
52. O. Werz Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes Blood 99 2002 1044 1052
53. O. Rådmark 5-Lipoxygenase: regulation of expression and enzyme activity Trends Biochem. Sci. 32 7 2007 332 341
54. E. Krump Suppression of leukotriene B-4 biosynthesis by endogenous adenosine in ligand-activated human neutrophils J. Exp. Med. 186 8 1997 1401 1406
55. N. Flamand Cyclic AMP-mediated inhibition of 5-lipoxygenase translocation and leukotriene biosynthesis in human neutrophils Mol. Pharmacol. 62 2 2002 250 256
56. C. Pergola ERK-mediated regulation of leukotriene biosynthesis by androgens: a molecular basis for gender differences in inflammation and asthma Proc. Natl. Acad. Sci. U. S. A. 105 2008 19881 19886
57. C. Pergola Testosterone suppresses phospholipase D, causing sex differences in leukotriene biosynthesis in human monocytes FASEB J. 25 10 2011 3377 3387
58. T. Hammarberg The N-terminal domain of 5-lipoxygenase binds calcium and mediates calcium stimulation of enzyme activity J. Biol. Chem. 275 49 2000 38787 38793
59. T. Hammarberg, and O. Rådmark 5-Lipoxygenase binds calcium Biochemistry 38 14 1999 4441 4447
60. X.S. Chen Determinants of 5-lipoxygenase nuclear localization using green fluorescent protein 5-lipoxygenase fusion proteins J. Biol. Chem. 273 47 1998 31237 31244
61. K.V. Reddy Mg2 + activates 5-lipoxygenase in vitro: dependency on concentrations of phosphatidylcholine and arachidonic acid Biochemistry 39 2000 1840 1848
62. D. Aharony, and R.L. Stein Kinetic mechanism of guinea pig neutrophil 5-lipoxygenase J. Biol. Chem. 261 25 1986 11512 11519
63. E. Burkert The C2-like beta-barrel domain mediates the Ca2 +-dependent resistance of 5-lipoxygenase activity against inhibition by glutathione peroxidase-1 J. Biol. Chem. 278 44 2003 42846 42853
64. Y.Y. Zhang Analysis of a nucleotide-binding site of 5-lipoxygenase by affinity labelling: binding characteristics and amino acid sequences Biochem. J. 351 Pt 3 2000 697 707
65. C. Pergola Indirubin Core Structure of Glycogen Synthase Kinase-3 Inhibitors as Novel Chemotype for Intervention with 5-Lipoxygenase 2014 J. Med Chem
66. T. Puustinen Regulation of the human leukocyte 5-lipoxygenase: stimulation by micromolar Ca2 + levels and phosphatidylcholine vesicles Biochim. Biophys. Acta 960 3 1988 261 267
67. M. Noguchi Human 5-lipoxygenase associates with phosphatidylcholine liposomes and modulates LTA(4) synthetase activity Biochim. Biophys. Acta, Lipids Lipid Metab. 1215 3 1994 300 306
68. A.H. Pande Membrane fluidity is a key modulator of membrane binding, insertion, and activity of 5-lipoxygenase Biophys. J. 88 2005 4084 4094
69. C. Hornig 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 2005 26913 26921
70. D. Albert Induction of 5-lipoxygenase activation in polymorphonuclear leukocytes by 1-oleoyl-2-acetylglycerol Biochim. Biophys. Acta 1631 1 2003 85 93
71. D. Albert The role of diacylglyceride generation by phospholipase D and phosphatidic acid phosphatase in the activation of 5-lipoxygenase in polymorphonuclear leukocytes J. Leukoc. Biol. 83 4 2008 1019 1027
72. N.C. Gilbert Conversion of human 5-lipoxygenase to a 15-lipoxygenase by a point mutation to mimic phosphorylation at Serine-663 FASEB J. 26 8 2012 3222 3229
73. M. Luo Protein kinase A inhibits leukotriene synthesis by phosphorylation of 5-lipoxygenase on serine 523 J. Biol. Chem. 40 2004 41512 41520 (Epub 42004 Jul 41526)
74. M. Luo Phosphorylation by protein kinase a inhibits nuclear import of 5-lipoxygenase J. Biol. Chem. 280 49 2005 40609 40616
75. N. Flamand Phosphorylation of serine 271 on 5-lipoxygenase and its role in nuclear export J. Biol. Chem. 284 1 2009 306 313
76. H. Hanaka Stress-induced nuclear export of 5-lipoxygenase Biochem. Biophys. Res. Commun. 338 1 2005 111 116
77. O. Werz Arachidonic acid promotes phosphorylation of 5-lipoxygenase at Ser-271 by MAPK-activated protein kinase 2 (MK2) J. Biol. Chem. 277 17 2002 14793 14800
78. O. Werz Phorbol ester up-regulates capacities for nuclear translocation and phosphorylation of 5-lipoxygenase in Mono Mac 6 cells and human polymorphonuclear leukocytes Blood 97 8 2001 2487 2495
79. O. Werz Extracellular signal-regulated kinases phosphorylate 5-lipoxygenase and stimulate 5-lipoxygenase product formation in leukocytes FASEB J. 16 11 2002 1441 1443
80. S. Markoutsa Analysis of 5-lipoxygenase phosphorylation on molecular level by MALDI-MS FEBS J. 281 8 2014 1931 1947
81. M.E. Newcomer, and N.C. Gilbert Location, location, location: compartmentalization of early events in leukotriene biosynthesis J. Biol. Chem. 285 33 2010 25109 25114
82. X.S. Chen Determinants of 5-lipoxygenase nuclear localization using green fluorescent protein 5-lipoxygenase fusion proteins J. Biol. Chem. 273 47 1998 31237 31244
83. M. Luo Multiple nuclear localization sequences allow modulation of 5-lipoxygenase nuclear import Traffic 5 11 2004 847 854
84. M. Luo Nuclear localization of 5-lipoxygenase as a determinant of leukotriene B4 synthetic capacity Proc. Natl. Acad. Sci. U. S. A. 6 2003 6
85. A.M. Bair The nuclear membrane leukotriene synthetic complex is a signal integrator and transducer Mol. Biol. Cell 23 22 2012 4456 4464
86. B. Haribabu Targeted disruption of the leukotriene B-4 receptor in mice reveals its role in inflammation and platelet-activating factor-induced anaphylaxis J. Exp. Med. 192 3 2000 433 438
87. D. Poeckel Dual 12/15- and 5-lipoxygenase deficiency in macrophages alters arachidonic acid metabolism and attenuates peritonitis and atherosclerosis in ApoE knock-out mice J. Biol. Chem. 284 31 2009 21077 21089
88. J.L. Goulet Deficiency of 5-lipoxygenase abolishes sex-related survival differences in MRL-lpr/lpr mice J. Immunol. 163 1 1999 359 366
89. B. Samuelsson Leukotrienes and lipoxins: structures, biosynthesis, and biological effects Science 237 1987 1171 1176
90. R.A. Lewis Leukotrienes and other products of the 5-lipoxygenase pathway. Biochemistry and relation to pathobiology in human diseases N. Engl. J. Med. 323 10 1990 645 655
91. S.E. Dahlen Treatment of asthma with antileukotrienes: first line or last resort therapy? Eur. J. Pharmacol. 533 1-3 2006 40 56
92. M. Peters-Golden, and W.R. Henderson Jr. Leukotrienes N. Engl. J. Med. 357 18 2007 1841 1854
93. H. Harizi Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology Trends Mol. Med. 14 10 2008 461 469
94. T. Shimizu Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation Annu. Rev. Pharmacol. Toxicol. 49 2009 123 150
95. J.Z. Haeggstrom, and C.D. Funk Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease Chem. Rev. 111 10 2011 5866 5898
96. A. Di Gennaro, and J.Z. Haeggstrom Targeting leukotriene B4 in inflammation Expert Opin. Ther. Targets 18 1 2014 79 93
97. M. Kupczyk Which anti-inflammatory drug should we use in asthma? Pol. Arch. Med. Wewn. 121 12 2011 455 459
98. V. Capra Eicosanoids and their drugs in cardiovascular diseases: focus on atherosclerosis and stroke Med. Res. Rev. 33 2 2013 364 438
99. A. Di Gennaro, and J.Z. Haeggstrom The leukotrienes: immune-modulating lipid mediators of disease Adv. Immunol. 116 2012 51 92
100. W. Tian Leukotrienes in pulmonary arterial hypertension Immunol. Res. 58 2-3 2014 387 393
101. D. Wang, and R.N. Dubois Eicosanoids and cancer Nat. Rev. Cancer 10 3 2010 181 193
102. R. Massoumi, and A. Sjolander The role of leukotriene receptor signaling in inflammation and cancer Sci. World J. 7 2007 1413 1421
103. O. Radmark, and B. Samuelsson Microsomal prostaglandin E synthase-1 and 5-lipoxygenase: potential drug targets in cancer J. Intern. Med. 268 1 2010 5 14
104. M. Peters-Golden Leukotrienes: underappreciated mediators of innate immune responses J. Immunol. 174 2 2005 589 594
105. N. Flamand Leukotrienes: mediators that have been typecast as villains Cell. Mol. Life Sci. 64 19-20 2007 2657 2670
106. T. Yokomizo Leukotriene B4 receptors: novel roles in immunological regulations Adv. Enzym. Regul. 51 1 2011 59 64
107. N. Agarwal Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase Nature 460 7251 2009 98 102
108. D.M. Tobin, and L. Ramakrishnan TB: the Yin and Yang of lipid mediators Curr. Opin. Pharmacol. 13 4 2013 641 645
109. O. Soehnlein, and L. Lindbom Phagocyte partnership during the onset and resolution of inflammation Nat. Rev. Immunol. 10 6 2010 427 439
110. A. Ortega-Gomez Resolution of inflammation: an integrated view EMBO Mol. Med. 5 5 2013 661 674
111. Y. Chen Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia Nat. Genet. 41 7 2009 783 792
112. S. Adel Phosphorylation mimicking mutations of ALOX5 orthologs of different vertebrates do not alter reaction specificities of the enzymes Biochim Biophys Acta. 1841 10 2014 1460 1466