A novel role for iron in modulating the activity and membrane-binding ability of a trimmed soybean lipoxygenase-1

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 1725-1736

  Dainese, Enrico ^a   Angelucci, Clotilde B ^a   Sabatucci, Annalaura ^a   De Filippis, Vincenzo ^b   Mei, Giampiero ^c   Maccarrone, Mauro ^a,d  

^a UNIVERSITY OF TERAMO   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Enzyme activity; Enzyme structure; Limited proteolysis; Metal substitution; Pathogen infection

Indexed keywords

CALCIUM ION; GLYCEROL; IRON; LIPOXYGENASE; LIPOXYGENASE I; METAL ION; UNCLASSIFIED DRUG; VISCOGEN;

ARTICLE; BINDING AFFINITY; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; ISOLATION PROCEDURE; MEMBRANE BINDING; PRIORITY JOURNAL; SOYBEAN; STEADY STATE; STRUCTURE ANALYSIS; SUBSTITUTION REACTION; ULTRAVIOLET RADIATION;

APOENZYMES; BINDING SITES; CIRCULAR DICHROISM; IRON; KINETICS; LIPOSOMES; LIPOXYGENASE; METALS; SOYBEANS; SPECTROPHOTOMETRY, ATOMIC; SUBSTRATE SPECIFICITY;

ANIMALIA; GLYCINE MAX;

EID: 77953526759     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-141390     Document Type: Article

References (68)

1. Brash, A. R. (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J. Biol. Chem. 274, 23679-23682
2. Kuhn, H., and Thiele, B. J. (1999) The diversity of the lipoxygenase family. Many sequence data but little information on biological significance. FEBS Lett. 449, 7-11
3. Kuhn, H., and Borngraber, S. (1999) Mammalian 15-lipoxygenases. Enzymatic properties and biological implications. Adv. Exp. Med. Biol. 447, 5-28
4. Funk, C. D. (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875
5. Walther, M., Wiesner, R., and Kuhn, H. (2004) Investigations into calcium-dependent membrane association of 15-lipoxygenase-1. Mechanistic roles of surface-exposed hydrophobic amino acids and calcium. J. Biol. Chem. 279, 3717-3725
6. Taccone-Gallucci, M., Manca-di-Villahermosa, S., and Maccarrone, M. (2008) Leukotrienes. N. Engl. J. Med. 358, 746
7. Kim, E. S., Choi, E., Kim, Y., Cho, K., Lee, A., Shim, J., Rakwal, R., Agrawal, G. K., and Han, O. (2003) Dual positional specificity and expression of non-traditional lipoxygenase induced by wounding and methyl jasmonate in maize seedlings. Plant Mol. Biol. 52, 1203-1213
8. Grechkin, A. (1998) Recent developments in biochemistry of the plant lipoxygenase pathway. Prog. Lipid Res. 37, 317-352
9. Radmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. (2007) 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32, 332-341
10. Kuhn, H., Saam, J., Eibach, S., Holzhutter, H. G., Ivanov, I., and Walther, M. (2005) Structural biology of mammalian lipoxygenases: enzymatic consequences of targeted alterations of the protein structure. Biochem. Biophys. Res. Commun. 338, 93-101
11. Boyington, J. C., Gaffney, B. J., and Amzel, L. M. (1993) The three-dimensional structure of an arachidonic acid 15-lipoxygenase. Science 260, 1482-1486 (Pubitemid 23273261)
12. Minor, W., Steczko, J., Stec, B., Otwinowski, Z., Bolin, J. T., Walter, R., and Axelrod, B. (1996) Crystal structure of soybean lipoxygenase L-1 at 1.4 A resolution. Biochemistry 35, 10687-10701
13. Dainese, E., Sabatucci, A., van Zadelhoff, G., Angelucci, C. B., Vachette, P., Veldink, G. A., Agro, A. F., and Maccarrone, M. (2005) Structural stability of soybean lipoxygenase-1 in solution as probed by small angle X-ray scattering. J. Mol. Biol. 349, 143-152
14. Hammel, M., Walther, M., Prassl, R., and Kuhn, H. (2004) Structural Flexibility of the N-terminal β-barrel domain of 15-lipoxygenase-1 probed by small angle X-ray scattering. functional consequences for activity regulation and membrane binding. J. Mol. Biol. 343, 917-929
15. Mei, G., Di Venere, A., Nicolai, E., Angelucci, C. B., Ivanov, I., Sabatucci, A., Dainese, E., Kuhn, H., and Maccarrone, M. (2008) Structural properties of plant and mammalian lipoxygenases. Temperature-dependent conformational alterations and membrane binding ability. Biochemistry 47, 9234-9242
16. van Leyen, K., Duvoisin, R. M., Engelhardt, H., and Wiedmann, M. (1998) A function for lipoxygenase in programmed organelle degradation. Nature 395, 392-395
17. Grullich, C., Duvoisin, R. M., Wiedmann, M., and van Leyen, K. (2001) Inhibition of 15-lipoxygenase leads to delayed organelle degradation in the reticulocyte. FEBS Lett. 489, 51-54
18. Maccarrone, M., Melino, G., and Finazzi-Agro, A. (2001) Lipoxygenases and their involvement in programmed cell death. Cell. Death Differ. 8, 776-784
19. Baba, A., Sakuma, S., Okamoto, H., Inoue, T., and Iwata, H. (1989) Calcium induces membrane translocation of 12-lipoxygenase in rat platelets. J. Biol. Chem. 264, 15790-15795
20. Watson, A., and Doherty, F. J. (1994) Calcium promotes membrane association of reticulocyte 15-lipoxygenase. Biochem. J. 298 (Pt. 2), 377-383 (Pubitemid 24072480)
21. Maccarrone, M., Salucci, M. L., van Zadelhoff, G., Malatesta, F., Veldink, G., Vliegenthart, J. F., and Finazzi-Agro, A. (2001) Tryptic digestion of soybean lipoxygenase-1 generates a 60 kDa fragment with improved activity and membrane binding ability. Biochemistry 40, 6819-6827
22. Forneris, F., and Mattevi, A. (2008) Enzymes without borders: mobilizing substrates, delivering products. Science 321, 213-216
23. Vachette, P., Dainese, E., Vasyliev, V. B., Di Muro, P., Beltramini, M., Svergun, D. I., DeFilippis, V., and Salvato, B. (2002) A key structural role for active site type 3 copper ions in human ceruloplasmin. J. Biol. Chem. 277, 40823-40831
24. Van der Donk, W. A., Tsai, A. L., and Kulmacz, R. J. (2002) The cyclooxygenase reaction mechanism. Biochemistry 41, 15451-15458
25. Matsuda, S., Suzuki, H., Yoshimoto, T., Yamamoto, S., and Miyatake, A. (1991) Analysis of non-heme iron in arachidonate 12-lipoxygenase of porcine leukocytes. Biochim. Biophys. Acta 1084, 202-204
26. Kariapper, M. S., Dunham, W. R., and Funk, M. O., Jr. (2001) Iron extraction from soybean lipoxygenase 3 and reconstitution of catalytic activity from the apoenzyme. Biochem. Biophys. Res. Commun. 284, 563-567
27. Di Venere, A., Salucci, M. L., van Zadelhoff, G., Veldink, G., Mei, G., Rosato, N., Finazzi-Agro, A., and Maccarrone, M. (2003) Structure-to-function relationship of mini-lipoxygenase, a 60-kDa fragment of soybean lipoxygenase-1 with lower stability but higher enzymatic activity. J. Biol. Chem. 278, 18281-18288
28. Finazzi-Agro, A., Avigliano, L., Veldink, G. A., Vliegenthart, J. F., and Boldingh, J. (1973) The influence of oxygen on the fluorescence of lipoxygenase. Biochim. Biophys. Acta 326, 462-470
29. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
30. Auld, D. S. (1988) Methods for metal substitution. Methods Enzymol. 158, 71-79
31. Welch, K. D., Davis, T. Z., and Aust, S. D. (2002) Iron autoxidation and free radical generation: effects of buffers, ligands, and chelators. Arch. Biochem. Biophys. 397, 360-369
32. Schilstra, M. J., Veldink, G. A., and Vliegenthart, J. F. (1994) The dioxygenation rate in lipoxygenase catalysis is determined by the amount of iron(III) lipoxygenase in solution. Biochemistry 33, 3974-3979
33. Maccarrone, M., Lorenzon, T., Guerrieri, P., and Agro, A. F. (1999) Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity. Eur. J. Biochem. 265, 27-34
34. Oldham, M. L., Brash, A. R., and Newcomer, M. E. (2005) Insights from the X-ray crystal structure of coral 8R-lipoxygenase: calcium activation via a C2-like domain and a structural basis of product chirality. J. Biol. Chem. 280, 39545-39552
35. Knapp, M. J., and Klinman, J. P. (2003) Kinetic studies of oxygen reactivity in soybean lipoxygenase-1. Biochemistry 42, 11466-11475
36. Yamanaka, K., Oikawa, H., Ogawa, H. O., Hosono, K., Shinmachi, F., Takano, H., Sakuda, S., Beppu, T., and Ueda, K. (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151, 2899-2905
37. Hornsten, L., Su, C., Osbourn, A. E., Hellman, U., and Oliw, E. H. (2002) Cloning of the manganese lipoxygenase gene reveals homology with the lipoxygenase gene family. Eur. J. Biochem. 269, 2690-2697
38. Haavik, J., Le Bourdelles, B., Martinez, A., Flatmark, T., and Mallet, J. (1991) Recombinant human tyrosine hydroxylase isozymes. Reconstitution with iron and inhibitory effect of other metal ions. Eur. J. Biochem. 199, 371-378
39. 1H-NMR spectroscopy. Eur. J. Biochem. 210, 23-31
40. Martinez, A., Abeygunawardana, C., Haavik, J., Flatmark, T., and Mildvan, A. S. (1993) Conformation and interaction of phenylalanine with the divalent cation at the active site of human recombinant tyrosine hydroxylase as determined by proton NMR. Biochemistry 32, 6381-6390 (Pubitemid 23208821)
41. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy. Kluwer Academic/Plenum, New York
42. Strickland, E. H. (1974) Aromatic contributions to circular dichroism spectra of proteins. CRC Crit. Rev. Biochem. 2, 113-175
43. Sreerama, N., Venyaminov, S. Y., and Woody, R. W. (2001) Analysis of protein circular dichroism spectra based on the tertiary structure classification. Anal. Biochem. 299, 271-274
44. Salvato, B., Beltramini, M., Ricchelli, F., and Tallandini, L. (1989) Cobalt substitution studies on bovine erythrocyte superoxide dismutase: evidence for a novel cobalt-superoxide dismutase derivative. Biochim. Biophys. Acta 998, 14-20
45. Bubacco, L., Magliozzo, R. S., Beltramini, M., Salvato, B., and Peisach, J. (1992) Preparation and spectroscopic characterization of a coupled binuclear center in cobalt(II)-substituted hemocyanin. Biochemistry 31, 9294-9303
46. 2 determines productive-mode orientation of the enzyme at the membrane surface. J. Mol. Biol. 344, 71-89
47. Pande, A. H., Qin, S., and Tatulian, S. A. (2005) Membrane fluidity is a key modulator of membrane binding, insertion, and activity of 5-lipoxygenase. Biophys. J. 88, 4084-4094
48. Boyington, J. C., Gaffney, B. J., Amzel, L. M., Doctor, K. S., Mavrophilipos, D. V., Mavrophilipos, Z. V., Colom, A., and Yuan, S. M. (1994) The X-ray structure and biophysical studies of a 15-lipoxygenase. Ann. N. Y. Acad. Sci. 744, 310-313
49. Skrzypczak-Jankun, E. (1996) Flash-freezing causes a stress-induced modulation in a crystal structure of soybean lipoxygenase 13. Acta Crystallogr. D Biol. Crystallogr. 52, 959-965
50. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) Temperature- dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124, 3865-3874
51. Van der Heijdt, L. M., Schilstra, M. J., Feiters, M. C., Nolting, H. F., Hermes, C., Veldink, G. A., and Vliegenthart, J. F. (1995) Changes in the iron coordination sphere of Fe(II) lipoxygenase-1 from soybeans upon binding of linoleate or oleate. Eur. J. Biochem. 231, 186-191
52. Solomon, E. I., Zhou, J., Neese, F., and Pavel, E. G. (1997) New insights from spectroscopy into the structure/function relationships of lipoxygenases. Chem. Biol. 4, 795-808
53. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S. K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y. S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem. Rev. 100, 235-350
54. Myers, J. S., and Jakoby, W. B. (1975) Glycerol as an agent eliciting small conformational changes in alcohol dehydrogenase. J. Biol. Chem. 250, 3785-3789
55. Timasheff, S. N., and Arakawa, T. (1989) Stabilization of protein structure by solvents. In Protein Structure: A Practical Approach (Creighton, T. E., ed) pp. 331-345, IRL Press at Oxford University Press, New York
56. Messerschmidt, A., Ladenstein, R., Huber, R., Bolognesi, M., Avigliano, L., Petruzzelli, R., Rossi, A., and Finazzi-Agro, A. (1992) Refined crystal structure of ascorbate oxidase at 1.9 A resolution. J. Mol. Biol. 224, 179-205
57. Ducros, V., Brzozowski, A. M., Wilson, K. S., Brown, S. H., Ostergaard, P., Schneider, P., Yaver, D. S., Pedersen, A. H., and Davies, G. J. (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 A resolution. Nat. Struct. Biol. 5, 310-316
58. Titus, G. P., Mueller, H. A., Burgner, J., Rodriguez, D. C., Penalva, M. A., and Timm, D. E. (2000) Crystal structure of human homogentisate dioxygenase. Nat. Struct. Biol. 7, 542-546
59. Vassiliev, V. B., Kachurin, A. M., Beltramini, M., Rocco, G. P., Salvato, B., and Gaitskhoki, V. S. (1997) Copper depletion/repletion of human ceruloplasmin is followed by the changes in its spectral features and functional properties. J. Inorg. Biochem. 65, 167-174
60. Blechert, S., Brodschelm, W., Holder, S., Kammerer, L., Kutchan, T. M., Mueller, M. J., Xia, Z. Q., and Zenk, M. H. (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways. Proc. Natl. Acad. Sci. U. S. A. 92, 4099-4105
61. Tatulian, S. A., Steczko, J., and Minor, W. (1998) Uncovering a calcium-regulated membrane-binding mechanism for soybean lipoxygenase-1. Biochemistry. 37, 15481-15490
62. Carlile, A. J., Bindschedler, L. V., Bailey, A. M., Bowyer, P., Clarkson, J. M., and Cooper, R. M. (2000) Characterization of SNP1, a cell wall-degrading trypsin, produced during infection by Stagonospora nodorum. Mol. Plant Microbe Interact. 13, 538-550
63. Cristea, M., Engstrom, K., Su, C., Hornsten, L., and Oliw, E. H. (2005) Expression of manganese lipoxygenase in Pichia pastoris and site-directed mutagenesis of putative metal ligands. Arch. Biochem. Biophys. 434, 201-211
64. Challis, G. L., and Hopwood, D. A. (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc. Natl. Acad. Sci. U. S. A. 100 (Suppl. 2), 14555-14561
65. Xiao, K., Kinkel, L. L., and Samac, D. A. (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol. Control 23, 285-295
66. Komoda, T., Kishi, M., Abe, N., Sugiyama, Y., and Hirota, A. (2004) Novel lipoxygenase inhibitors, tetrapetalone B, C, and D from Streptomyces sp. Biosci. Biotechnol. Biochem. 68, 903-908
67. Decker, H., and Rimke, T. (1998) Tarantula hemocyanin shows phenoloxidase activity. J. Biol. Chem. 273, 25889-25892
68. Nillius, D., Jaenicke, E., and Decker, H. (2008) Switch between tyrosinase and catecholoxidase activity of scorpion hemocyanin by allosteric effectors. FEBS Lett. 582, 749-754