5-Lipoxygenase-activating protein rescues activity of 5-lipoxygenase mutations that delay nuclear membrane association and disrupt product formation

FASEB Journal

Volumn 30, Issue 5, 2016, Pages 1892-1900

  Gerstmeier, Jana ^a   Newcomer, Marcia E ^b   Dennhardt, Sophie ^a   Romp, Erik ^a   Fischer, Jana ^a   Werz, Oliver ^a   Garscha, Ulrike ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Arachidonic acid; HEK293; Inflammation; Leukotriene A4; Translocation

Indexed keywords

5 HYDROPEROXY 6,8,11,14 ICOSATETRAENOIC ACID; ALANINE; ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONATE 5 LIPOXYGENASE ACTIVATING PROTEIN; INDOLE DERIVATIVE; MK-886; PROTEIN BINDING;

ARTICLE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE MUTATION; HEK293 CELL LINE; HYDROLYSIS; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STABLE EXPRESSION; BINDING SITE; CELL MEMBRANE; CELL MOTION; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS;

5-LIPOXYGENASE-ACTIVATING PROTEINS; ARACHIDONATE 5-LIPOXYGENASE; BINDING SITES; CELL MEMBRANE; CELL MOVEMENT; CELL NUCLEUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; INDOLES; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84966415531     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201500210R     Document Type: Article

References (35)

1. Peters-Golden, M., and Henderson, W. R., Jr. (2007) Leukotrienes. N. Engl. J. Med. 357,1841-1854
2. Poeckel, D., and Funk, C. D. (2010) The 5-lipoxygenase/leukotriene pathway in preclinical models of cardiovascular disease. Cardiovasc. Res. 86,243-253
3. Wang, D., and Dubois, R. N. (2010) Eicosanoids and cancer. Nat. Rev. Cancer 10,181-193
4. Rådmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. (2015) 5-Lipoxygenase, a key enzyme for leukotriene biosynthesis in health and disease. Biochim. Biophys. Acta 1851, 331-339
5. Schneider, C., Pratt, D. A., Porter, N. A., and Brash, A. R. (2007) Control ofoxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14,473-488
6. Newcomer, M. E., andBrash, A. R. (2015)The structural basis for specificity in lipoxygenase catalysis. Protein Sci. 24, 298-309
7. Panossian, A., Hamberg, M., and Samuelsson, B. (1982) On the mechanism of biosynthesis of leukotrienes and related compounds. FEBS Lett. 150,511-513
8. Samuelsson, B. (1983) Leukotrienes: a new class of mediators of immediate hypersensitivity reactions and inflammation. Adv. Prostaglandin Thromboxane Leukot. Res. 11,1-13
9. Hill, E., Maclouf, J., Murphy, R. C., and Henson, P. M. (1992) Reversible membrane association of neutrophil 5-lipoxygenase is accompanied by retention of activity and a change in substrate specificity. J. Biol. Chem. 267, 22048-22053
10. 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
11. Rådmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. (2007) 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32,332-341
12. Wiseman, J. S., Skoog, M. T., Nichols, J. S., and Harrison, B. L. (1987) Kinetics of leukotriene A4 synthesis by 5-lipoxygenase from rat polymorphonuclear leukocytes. Biochemistry 26,5684-5689
13. Noguchi, M., Miyano, M., Matsumoto, T., and Noma, M. (1994) Human 5-lipoxygenase associates with phosphatidylcholine liposomes and modulates LTA4 synthetase activity. Biochim. Biophys. Acta 1215,300-306
14. Dixon, R. A., Diehl, R. E., Opas,E., Rands,E., Vickers,P. J., Evans,J.F., Gillard, J. W., and Miller, D. K. (1990) Requirement of a 5-lipoxygenase-activating protein for leukotriene synthesis. Nature 343, 282-284
15. Gerstmeier, J., Weinigel, C., Barz, D., Werz, O., and Garscha, U. (2014) An experimental cell-based model forstudyingthecell biology and molecular pharmacology of 5-lipoxygenase-activating protein in leukotriene biosynthesis. Biochim. Biophys. Acta 1840, 2961-2969
16. Evans, J. F., Ferguson, A. D., Mosley, R. T., and Hutchinson, J. H. (2008) What's all the FLAP about? 5-lipoxygenase-activating protein inhibitors for inflammatory diseases. Trends Pharmacol. Sci. 29,72-78
17. Gilbert, N. C., Bartlett, S. G., Waight, M. T., Neau, D. B., Boeglin, W. E., Brash, A. R., and Newcomer, M. E. (2011) The structure of human 5-lipoxygenase. Science 331, 217-219
18. Eek, P., Järving, R., Järving, I., Gilbert, N. C., Newcomer, M. E., and Samel, N. (2012) Structure of a calcium-dependent 11R-lipoxygenase suggests a mechanism for Ca2+ regulation. J. Biol. Chem. 287, 22377-22386
19. Järving, R., Lõokene, A., Kurg, R., Siimon, L., Järving, I., and Samel, N. (2012) Activation of 11R-lipoxygenase is fully Ca(2+)-dependent and controlled by the phospholipid composition of the target membrane. Biochemistry 51,3310-3320
20. Mitra, S., Bartlett, S. G., and Newcomer, M. E. (2015) Identification of the substrate access portal of 5-lipoxygenase. Biochemistry 54, 6333-6342
21. Pergola, C., Gerstmeier, J., Mönch, B., Çalişkan, B., Luderer, S., Weinigel, C., Barz, D., Maczewsky, J., Pace, S., Rossi, A., Sautebin, L., Banoglu, E., and Werz, O. (2014) The novel benzimidazole derivative BRP-7 inhibits leukotriene biosynthesis in vitro and in vivo by targeting 5-lipoxygenase-activating protein (FLAP). Br. J. Pharmacol. 171,3051-3064
22. Gerstmeier, J., Weinigel, C., Rummler, S., Radmark, O., Werz, O., and Garscha, U. (2016) Time-resolved in situ assembly of the leukotriene-synthetic 5-lipoxygenase/5-lipoxygenase-activating protein complex in blood leukocytes. FASEB J. 30, 276-285
23. Werz, O., and Steinhilber, D. (2005) Development of 5-lipoxygenase inhibitors-lessons from cellular enzyme regulation. Biochem. Pharmacol. 70,327-333
24. Chen, X. S., and Funk, C. D. (2001) The N-terminal "beta-barrel" domain of 5-lipoxygenase is essential for nuclear membrane translocation. J. Biol. Chem. 276, 811-818
25. 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
26. Kargman, S., Vickers, P. J., and Evans, J. F. (1992) A23187-induced translocation of 5-lipoxygenase in osteosarcoma cells. J. Cell Biol. 119, 1701-1709
27. Walther, M., Hofheinz, K., Vogel, R., Roffeis, J., and Kühn, H. (2011) The N-terminal b-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. 516,1-9
28. White, S. H., and Wimley, W. C. (1999) Membrane protein folding and stability: physical principles. Annu.Rev.Biophys.Biomol.Struct.28, 319-365
29. Coïc, Y. M., Vincent, M., Gallay, J., Baleux, F., Mousson, F., Beswick, V., Neumann, J. M., and de Foresta, B. (2005) Single-spanning membrane protein insertion in membrane mimetic systems: role and localization of aromatic residues. Eur. Biophys. J. 35, 27-39
30. MirAfzali, Z., Leipprandt, J. R., McCracken, J. L., and DeWitt, D. L. (2006) Topography ofthe prostaglandin endoperoxide H2 synthase-2 in membranes. J. Biol. Chem. 281, 28354-28364
31. Grauffel, C., Yang, B., He, T., Roberts, M. F., Gershenson, A., and Reuter, N. (2013) Cation-p interactions as lipid-specific anchors for phosphatidylinositol-specific phospholipase C. J. Am. Chem. Soc. 135, 5740-5750
32. Häfner, A. K., Cernescu, M., Hofmann, B., Ermisch, M., Hörnig, M., Metzner, J., Schneider, G., Brutschy, B., and Steinhilber, D. (2011) Dimerization of human 5-lipoxygenase. Biol. Chem. 392, 1097-1111
33. Bair, A. M., Turman, M. V., Vaine, C. A., Panettieri, R. A., Jr., and Soberman, R. J. (2012) The nuclear membrane leukotriene synthetic complex is a signal integrator and transducer. Mol. Biol. Cell 23,4456-4464
34. Mandal, A. K., Jones, P. B., Bair, A. M., Christmas, P., Miller, D., Yamin, T. T., Wisniewski, D., Menke, J., Evans, J. F., Hyman, B. T., Bacskai,B., Chen, M., Lee, D. M.,Nikolic, B., and Soberman, R. J. (2008) The nuclear membrane organization of leukotriene synthesis. Proc. Natl. Acad. Sci. USA 105, 20434-20439
35. Mandal, A. K., Skoch, J., Bacskai, B. J., Hyman, B. T., Christmas, P., Miller, D., Yamin, T. T., Xu, S., Wisniewski, D., Evans, J. F., and Soberman, R. J. (2004) The membrane organization of leukotriene synthesis. Proc. Natl. Acad. Sci. USA 101, 6587-6592