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Cytosolic phospholipase A2, lipoxygenase metabolites, and reactive oxygen species

  • Kim, Cheol-Min (School of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Joo-Young (School of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Jae-Hong (School of Life Sciences and Biotechnology, Korea University)
  • Published : 2008.08.31

Abstract

Reactive oxygen species (ROS) are generated in mammalian cells via both enzymatic and non-enzymatic mechanisms. Although certain ROS production pathways are required for the performance of specific physiological functions, excessive ROS generation is harmful, and has been implicated in the pathogenesis of a number of diseases. Among the ROS-producing enzymes, NADPH oxidase is widely distributed among mammalian cells, and is a crucial source of ROS for physiological and pathological processes. Reactive oxygen species are also generated by arachidonic acid (AA) metabolites, which are released from membrane phospholipids via the activity of cytosolic phospholipase $A_2$ ($cPLA_2$). In this study, we describe recent studies concerning the generation of ROS by AA metabolites. In particular, we have focused on the manner in which AA metabolism via lipoxygenase (LOX) and LOX metabolites contributes to ROS generation. By elucidating the signaling mechanisms that link LOX and LOX metabolites to ROS, we hope to shed light on the variety of physiological and pathological mechanisms associated with LOX metabolism.

Keywords

References

  1. Lambeth, J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189 . https://doi.org/10.1038/nri1312
  2. Edderkaoui, M., Hong, P., Vaquero, E. C., Lee, J. K., Fischer, L., Friess, H., Buchler, M. W., Lerch, M. M., Pandol, S. J. and Gukovskaya, A. S. (2005) Extracellular matrix stimulates reactive oxygen species production and increases pancreatic cancer cell survival through 5-lipoxygenase and NADPH oxidase. Am. J. Physiol. Gastrointest. Liver. Physiol. 289, G1137-47 . https://doi.org/10.1152/ajpgi.00197.2005
  3. Suh, Y. A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K. and Lambeth, J. D. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature. 401, 79-82 . https://doi.org/10.1038/43459
  4. Simon, H. U., Haj-Yehia, A. and Levi-Schaffer, F. (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 5, 415-418 . https://doi.org/10.1023/A:1009616228304
  5. Lee, S. R., Kwon, K. S., Kim, S. R. and Rhee, S. G. (1998) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273, 15366-15372 . https://doi.org/10.1074/jbc.273.25.15366
  6. Lee, S. R., Yang, K. S., Kwon, J., Lee, C., Jeong, W. and Rhee, S. G. (2002) Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 277, 20336-20342 . https://doi.org/10.1074/jbc.M111899200
  7. Torres, M. and Forman, H. J. (2003) Redox signaling and the MAP kinase pathways. Biofactors. 17, 287-296 . https://doi.org/10.1002/biof.5520170128
  8. Samuelsson, B., Dahlen, S. E., Lindgren, J. A., Rouzer, C. A. and Serhan, C. N. (1987) Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science. 237, 1171-1176 . https://doi.org/10.1126/science.2820055
  9. Funk, C. D. (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science. 294, 1871-1875 . https://doi.org/10.1126/science.294.5548.1871
  10. Kim, C. and Dinauer, M. C. (2006) Impaired NADPH oxidase activity in Rac2-deficient murine neutrophils does not result from defective translocation of p47phox and p67phox and can be rescued by exogenous arachidonic acid. J. Biol. Chem. 79, 223-234.
  11. Luchtefeld, M., Drexler, H. and Schieffer, B. (2003) 5- Lipoxygenase is involved in the angiotensin II-induced NAD (P)H-oxidase activation. Biochem. Biophys. Res. Commun. 308, 668-672 . https://doi.org/10.1016/S0006-291X(03)01456-6
  12. Shiose, A. and Sumimoto, H. (2000) Arachidonic acid and phosphorylation synergistically induce a conformational change of p47phox to activate the phagocyte NADPH oxidase. J. Biol. Chem. 275, 13793-13801 . https://doi.org/10.1074/jbc.275.18.13793
  13. de Carvalho, D. D., Sadok, A., Bourgarel-Rey, V., Gattacceca, F., Penel, C., Lehmann, M. and Kovacic, H. (2008) Nox1 downstream of 12-lipoxygenase controls cell proliferation but not cell spreading of colon cancer cells. Int. J. Cancer. 122, 1757-1764 . https://doi.org/10.1002/ijc.23300
  14. Mahipal, S. V., Subhashini, J., Reddy, M. C., Reddy, M. M., Anilkumar, K., Roy, K. R., Reddy, G. V. and Reddanna, P. (2007) Effect of 15-lipoxygenase metabolites, 15-(S)-HPETE and 15-(S)-HETE on chronic myelogenous leukemia cell line K-562: reactive oxygen species (ROS) mediate caspase- dependent apoptosis. Biochem. Pharmacol. 74, 202- 214 . https://doi.org/10.1016/j.bcp.2007.04.005
  15. Schweiger, D., Furstenberger, G. and Krieg, P. (2007) Inducible expression of 15-lipoxygenase-2 and 8-lipoxygenase inhibits cell growth via common signaling pathways. J. Lipid Res. 48, 553-564 . https://doi.org/10.1194/jlr.M600311-JLR200
  16. Werz, O. and Steinhilber, D. (2006) Therapeutic options for 5-lipoxygenase inhibitors. Pharmacol. Ther. 112, 701-718 . https://doi.org/10.1016/j.pharmthera.2006.05.009
  17. Uchida, K. (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog. Lipid Res. 42, 318-343 . https://doi.org/10.1016/S0163-7827(03)00014-6
  18. Brash, A. R. (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J. Biol. Chem. 274, 23679-23682 . https://doi.org/10.1074/jbc.274.34.23679
  19. Choi, J. A., Kim, E. Y., Song, H., Kim, C. and Kim, J. H. (2008) Reactive oxygen species are generated through a BLT2-linked cascade in Ras-transformed cells. Free. Radic. Biol. Med. 44, 624-634 . https://doi.org/10.1016/j.freeradbiomed.2007.10.041
  20. Woo, C. H., Lee, Z. W., Kim, B. C., Ha, K. S. and Kim, J. H. (2000) Involvement of cytosolic phospholipase A2, and the subsequent release of arachidonic acid, in signalling by rac for the generation of intracellular reactive oxygen species in rat-2 fibroblasts. Biochem. J. 348 (Pt 3), 525-530 . https://doi.org/10.1042/0264-6021:3480525
  21. Lindsay, M. A., Perkins, R. S., Barnes, P. J. and Giembycz, M. A. (1998) Leukotriene B4 activates the NADPH oxidase in eosinophils by a pertussis toxin-sensitive mechanism that is largely independent of arachidonic acid mobilization. J. Immunol. 160, 4526-4534.
  22. Serezani, C. H., Aronoff, D. M., Jancar, S. and Peters-Golden, M. (2005) Leukotriene B4 mediates p47 phox phosphorylation and membrane translocation in polyunsaturated fatty acid-stimulated neutrophils. J. Biol. Chem. 78, 976-984.
  23. Nardi, M., Feinmark, S. J., Hu, L., Li, Z. and Karpatkin, S. (2004) Complement-independent Ab-induced peroxide lysis of platelets requires 12-lipoxygenase and a platelet NADPH oxidase pathway. J. Clin. Invest. 113, 973-980. https://doi.org/10.1172/JCI20726
  24. Woo, C. H., Eom, Y. W., Yoo, M. H., You, H. J., Han, H. J., Song, W. K., Yoo, Y. J., Chun, J. S. and Kim, J. H. (2000) Tumor necrosis factor-alpha generates reactive oxygen species via a cytosolic phospholipase A2-linked cascade. J. Biol. Chem. 275, 32357-32362 . https://doi.org/10.1074/jbc.M005638200
  25. Lo, Y. Y. and Cruz, T. F. (1995) Involvement of reactive oxygen species in cytokine and growth factor induction of c-fos expression in chondrocytes. J. Biol. Chem. 270, 11727-11730 . https://doi.org/10.1074/jbc.270.20.11727
  26. Bae, Y. S., Kang, S. W., Seo, M. S., Baines, I. C., Tekle, E., Chock, P. B. and Rhee, S. G. (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 217-221 . https://doi.org/10.1074/jbc.272.1.217
  27. Sundaresan, M., Yu, Z. X., Ferrans, V. J., Irani, K. and Finkel, T. (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 270, 296-299 . https://doi.org/10.1126/science.270.5234.296
  28. Colavitti, R., Pani, G., Bedogni, B., Anzevino, R., Borrello, S., Waltenberger, J. and Galeotti, T. (2002) Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor- 2/ KDR. J. Biol. Chem. 277, 3101-3108. https://doi.org/10.1074/jbc.M107711200
  29. Rubin, P. and Mollison, K. W. (2007) Pharmacotherapy of diseases mediated by 5-lipoxygenase pathway eicosanoids. Prostaglandins Other Lipid Mediat. 83, 188-197 . https://doi.org/10.1016/j.prostaglandins.2007.01.005
  30. Katsuyama, M., Fan, C. and Yabe-Nishimura, C. (2002) NADPH oxidase is involved in prostaglandin F2alpha-induced hypertrophy of vascular smooth muscle cells: induction of NOX1 by PGF2alpha. J. Biol. Chem. 277, 13438-13442 . https://doi.org/10.1074/jbc.M111634200
  31. Borgeat, P., Hamberg, M. and Samuelsson, B. (1976) Transformation of arachidonic acid and homo-gammalinolenic acid by rabbit polymorphonuclear leukocytes. Monohydroxy acids from novel lipoxygenases. J. Biol. Chem. 251, 7816-7820.
  32. Claria, J. and Arroyo, V. (2003) Prostaglandins and other cyclooxygenase-dependent arachidonic acid metabolites and the kidney in liver disease. Prostaglandins Other Lipid Mediat. 72, 19-33 . https://doi.org/10.1016/S1098-8823(03)00075-3
  33. Yokomizo, T., Izumi, T., Chang, K., Takuwa, Y. and Shimizu, T. (1997) A G-protein-coupled receptor for leukotriene B4 that mediates chemotaxis. Nature. 387, 620- 624.
  34. Woo, C. H., You, H. J., Cho, S. H., Eom, Y. W., Chun, J. S., Yoo, Y. J. and Kim, J. H. (2002) Leukotriene B(4) stimulates Rac-ERK cascade to generate reactive oxygen species that mediates chemotaxis. J. Biol. Chem. 277, 8572-8578. https://doi.org/10.1074/jbc.M104766200
  35. Woo, C. H., Yoo, M. H., You, H. J., Cho, S. H., Mun, Y. C., Seong, C. M. and Kim, J. H. (2003) Transepithelial migration of neutrophils in response to leukotriene B4 is mediated by a reactive oxygen species-extracellular signal- regulated kinase-linked cascade. J. Immunol. 170, 6273-6279. https://doi.org/10.4049/jimmunol.170.12.6273
  36. Perkins, R. S., Lindsay, M. A., Barnes, P. J. and Giembycz, M. A. (1995) Early signalling events implicated in leukotriene B4-induced activation of the NADPH oxidase in eosinophils: role of Ca2+, protein kinase C and phospholipases C and D. Biochem. J. 310 (Pt 3), 795-806. https://doi.org/10.1042/bj3100795
  37. Yokomizo, T., Kato, K., Terawaki, K., Izumi, T. and Shimizu, T. (2000) A second leukotriene B(4) receptor, BLT2. A new therapeutic target in inflammation and immunological disorders. J. Exp. Med. 192, 421-432 . https://doi.org/10.1084/jem.192.3.421
  38. Kamohara, M., Takasaki, J., Matsumoto, M., Saito, T., Ohishi, T., Ishii, H. and Furuichi, K. (2000) Molecular cloning and characterization of another leukotriene B4 receptor. J. Biol. Chem. 275, 27000-27004.
  39. Okuno, T., Iizuka, Y., Okazaki, H., Yokomizo, T., Taguchi, R. and Shimizu, T. (2008) 12(S)-Hydroxyheptadeca- 5Z, 8E, 10E-trienoic acid is a natural ligand for leukotriene B4 receptor 2. J. Exp. Med. 205, 759-766 . https://doi.org/10.1084/jem.20072329
  40. Sadok, A., Bourgarel-Rey, V., Gattacceca, F., Penel, C., Lehmann, M. and Kovacic, H. (2008) Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim. Biophys. Acta. 1783, 23-33 . https://doi.org/10.1016/j.bbamcr.2007.10.010
  41. Nie, D., Tang, K., Diglio, C. and Honn, K. V. (2000) Eicosanoid regulation of angiogenesis: role of endothelial arachidonate 12-lipoxygenase. Blood. 95, 2304-2311.
  42. Schewe, T., Halangk, W., Hiebsch, C. and Rapoport, S. M. (1975) A lipoxygenase in rabbit reticulocytes which attacks phospholipids and intact mitochondria. FEBS Lett. 60, 149-152 . https://doi.org/10.1016/0014-5793(75)80439-X
  43. Rapoport, S. M., Schewe, T., Wiesner, R., Halangk, W., Ludwig, P., Janicke-Hohne, M., Tannert, C., Hiebsch, C. and Klatt, D. (1979) The lipoxygenase of reticulocytes. Purification, characterization and biological dynamics of the lipoxygenase; its identity with the respiratory inhibitors of the reticulocyte. Eur. J. Biochem. 96, 545-561 . https://doi.org/10.1111/j.1432-1033.1979.tb13068.x
  44. Brash, A. R., Boeglin, W. E. and Chang, M. S. (1997) Discovery of a second 15S-lipoxygenase in humans. Proc. Natl. Acad. Sci. U.S.A. 94, 6148-6152. https://doi.org/10.1073/pnas.94.12.6148

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