Testosterone suppresses phospholipase D, causing sex differences in leukotriene biosynthesis in human monocytes

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3377-3387

  Pergola, Carlo ^a   Rogge, Anja ^a   Dodt, Gabriele ^b   Northoff, Hinnak ^c   Weinigel, Christina ^d   Barz, Dagmar ^d   Rådmark, Olof ^e   Sautebin, Lidia ^f   Werz, Oliver ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d JENA UNIVERSITY HOSPITAL   (Germany)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

5 lipoxygenase; Extracellular signal regulated kinases; Inflammation; Sex hormones

Indexed keywords

5ALPHA ANDROSTAN 3 ONE; ARACHIDONATE 5 LIPOXYGENASE; ARACHIDONIC ACID; CHOLINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIACYLGLYCEROL; ESTRADIOL; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE D; PROGESTERONE;

ARTICLE; CELL SUSPENSION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; MONOCYTE; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROSTAGLANDIN SYNTHESIS; RADIOENZYMATIC ASSAY; SEX DIFFERENCE; WESTERN BLOTTING;

ADULT; ARACHIDONATE 5-LIPOXYGENASE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIHYDROTESTOSTERONE; DOWN-REGULATION; FEMALE; HUMANS; LEUKOTRIENES; MALE; MONOCYTES; PHOSPHOLIPASE D; PROTEIN TRANSPORT; SEX CHARACTERISTICS; TESTOSTERONE;

EID: 80053925891     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-182758     Document Type: Article

References (43)

1. Geissmann, F., Manz, M. G., Jung, S., Sieweke, M. H., Merad, M., and Ley, K. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327, 656-661
2. O'Connor, M. F., Motivala, S. J., Valladares, E. M., Olmstead, R., and Irwin, M. R. (2007) Sex differences in monocyte expression of IL-6: role of autonomic mechanisms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R145-R151 (Pubitemid 47096572)
3. Sondell, K., Athlin, L., Bjermer, L., Eriksson, S., and Norberg, B. (1990) The role of sex and age in yeast cell phagocytosis by monocytes from healthy blood donors. Mech. Ageing Dev. 51, 55-61 (Pubitemid 20013028)
4. Goetzl, E. J., Huang, M. C., Kon, J., Patel, K., Schwartz, J. B., Fast, K., Ferrucci, L., Madara, K., Taub, D. D., and Longo, D. L. (2010) Gender specificity of altered human immune cytokine profiles in aging. FASEB J. 24, 3580-3589
5. Kanda, N., Tsuchida, T., and Tamaki, K. (1997) Testosterone suppresses anti-DNA antibody production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum. 40, 1703-1711 (Pubitemid 27426165)
6. Miyagi, M., Morishita, M., and Iwamoto, Y. (1993) Effects of sex hormones on production of prostaglandin E2 by human peripheral monocytes. J. Periodontol. 64, 1075-1078 (Pubitemid 24019271)
7. Cutolo, M., Capellino, S., Montagna, P., Ghiorzo, P., Sulli, A., and Villaggio, B. (2005) Sex hormone modulation of cell growth and apoptosis of the human monocytic/macrophage cell line. Arthritis Res. Ther. 7, R1124-R1132
8. Morishita, M., Miyagi, M., and Iwamoto, Y. (1999) Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. J. Periodontology 70, 757-760 (Pubitemid 29340771)
9. Gosselin, J., and Borgeat, P. (1997) Epstein-Barr virus modulates 5-lipoxygenase product synthesis in human peripheral blood mononuclear cells. Blood 89, 2122-2130 (Pubitemid 27132129)
10. Surette, M. E., Nadeau, M., Borgeat, P., and Gosselin, J. (1996) Priming of human peripheral blood mononuclear cells with lipopolysaccharides for enhanced arachidonic acid release and leukotriene synthesis. J. Leukoc. Biol. 59, 709-715 (Pubitemid 26198082)
11. Peters-Golden, M., and Henderson, W. R., Jr. (2007) Leukotrienes. N. Engl. J. Med. 357, 1841-1854
12. Woods, J. W., Evans, J. F., Ethier, D., Scott, S., Vickers, P. J., Hearn, L., Heibein, J. A., Charleson, S., and Singer, I. I. (1993) 5-Lipoxygenase and 5-lipoxygenase-activating protein are localized in the nuclear envelope of activated human leukocytes. J. Exp. Med. 178, 1935-1946 (Pubitemid 23344852)
13. Esser, J., Rakonjac, M., Hofmann, B., Fischer, L., Provost, P., Schneider, G., Steinhilber, D., Samuelsson, B., and Radmark, O. (2009) Coactosin-like protein functions as a stabilizing chaperone for 5-lipoxygenase: role of tryptophan 102. Biochem. J. 425, 265-274
14. Hammarberg, T., Provost, P., Persson, B., and Radmark, O. (2000) The N-terminal domain of 5-lipoxygenase binds calcium and mediates calcium stimulation of enzyme activity. J. Biol. Chem. 275, 38787-38793 (Pubitemid 32009215)
15. Luo, M., Jones, S. M., Phare, S. M., Coffey, M. J., Peters-Golden, M., and Brock, T. G. (2004) Protein kinase A inhibits leukotriene synthesis by phosphorylation of 5-lipoxygenase on serine 523. J. Biol. Chem. 279, 41512-41520 (Pubitemid 39313592)
16. Werz, O., Klemm, J., Samuelsson, B., and Radmark, O. (2000) 5-lipoxygenase is phosphorylated by p38 kinase-dependent MAPKAP kinases. Proc. Natl. Acad. Sci. U. S. A. 97, 5261-5266 (Pubitemid 30313706)
17. Werz, O., Burkert, E., Fischer, L., Szellas, D., Dishart, D., Samuelsson, B., Radmark, O., and Steinhilber, D. (2002) Extracellular signal-regulated kinases phosphorylate 5-lipoxygenase and stimulate 5-lipoxygenase product formation in leukocytes. FASEB J. 16, 1441-1443
18. Hornig, C., Albert, D., Fischer, L., Hornig, M., Radmark, 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 (Pubitemid 41040726)
19. Albert, D., Pergola, C., Koeberle, A., Dodt, G., Steinhilber, D., and Werz, O. (2008) 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, 1019-1027 (Pubitemid 351959883)
20. Pergola, C., Dodt, G., Rossi, A., Neunhoeffer, E., Lawrenz, B., Northoff, H., Samuelsson, B., Radmark, O., Sautebin, L., and Werz, O. (2008) 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, 19881-19886
21. Chiang, N., Hurwitz, S., Ridker, P. M., and Serhan, C. N. (2006) Aspirin has a gender-dependent impact on antiinflammatory 15-epi-lipoxin A4 formation: a randomized human trial. Arterioscler. Thromb. Vasc. Biol. 26, e14-e17 (Pubitemid 43732186)
22. Haribabu, B., Verghese, M. W., Steeber, D. A., Sellars, D. D., Bock, C. B., and Snyderman, R. (2000) 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, 433-438 (Pubitemid 30629168)
23. Poeckel, D., Zemski Berry, K. A., Murphy, R. C., and Funk, C. D. (2009) 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, 21077-21089
24. Osman, M. (2003) Therapeutic implications of sex differences in asthma and atopy. Arch. Dis. Child. 88, 587-590
25. Werz, O., Burkert, E., Samuelsson, B., Radmark, O., and Steinhilber, D. (2002) Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes. Blood 99, 1044-1052 (Pubitemid 34527142)
26. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450
27. Preiss, J. E., Loomis, C. R., Bell, R. M., and Niedel, J. E. (1987) Quantitative measurement of sn-1,2-diacylglycerols. Methods Enzymol. 141, 294-300 (Pubitemid 17086016)
28. Paruch, S., El-Benna, J., Djerdjouri, B., Marullo, S., and Perianin, A. (2006) A role of p44/42 mitogen-activated protein kinases in formyl-peptide receptor-mediated phospholipase D activity and oxidant production. FASEB J. 20, 142-144 (Pubitemid 43100494)
29. Radmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. (2007) 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32, 332-341 (Pubitemid 47021417)
30. Murray, A. J. (2008) Pharmacological PKA inhibition: all may not be what it seems. Sci. Signal. 1, re4
31. Estrada, M., Espinosa, A., Muller, M., and Jaimovich, E. (2003) Testosterone stimulates intracellular calcium release and mitogen-activated protein kinases via a G protein-coupled receptor in skeletal muscle cells. Endocrinology 144, 3586-3597 (Pubitemid 36904438)
32. Benten, W. P., Lieberherr, M., Giese, G., Wrehlke, C., Stamm, O., Sekeris, C. E., Mossmann, H., and Wunderlich, F. (1999) Functional testosterone receptors in plasma membranes of T cells. FASEB J. 13, 123-133 (Pubitemid 29038282)
33. Albert, D., Buerkert, E., Steinhilber, D., and Werz, O. (2003) Induction of 5-lipoxygenase activation in polymorphonuclear leukocytes by 1-oleoyl-2-acetylglycerol. Biochim. Biophys. Acta 1631, 85-93 (Pubitemid 36165107)
34. Djerdjouri, B., Lenoir, M., Giroud, J. P., and Perianin, A. (1999) Contribution of mitogen-activated protein kinase to stimulation of phospholipase D by the chemotactic peptide fMet-Leu-Phe in human neutrophils. Biochem. Biophys. Res. Commun. 264, 371-375 (Pubitemid 29516094)
35. Bae, Y. S., Kim, Y., Kim, J. H., Lee, T. G., Suh, P. G., and Ryu, S. H. (2000) Independent functioning of cytosolic phospholipase A2 and phospholipase D1 in Trp-Lys-Tyr-Met-Val-D-Metinduced superoxide generation in human monocytes. J. Immunol. 164, 4089-4096 (Pubitemid 30215064)
36. Funk, C. D. (2005) Leukotriene modifiers as potential therapeutics for cardiovascular disease. Nat. Rev. Drug Discov. 4, 664-672
37. Choi, B. G., and McLaughlin, M. A. (2007) Why men's hearts break: cardiovascular effects of sex steroids. Endocrinol. Metab. Clin. North. Am. 36, 365-377 (Pubitemid 46817891)
38. Malkin, C. J., Pugh, P. J., Jones, R. D., Jones, T. H., and Channer, K. S. (2003) Testosterone as a protective factor against atherosclerosis- immunomodulation and influence upon plaque development and stability. J. Endocrinol. 178, 373-380 (Pubitemid 37220164)
39. English, K. M., Mandour, O., Steeds, R. P., Diver, M. J., Jones, T. H., and Channer, K. S. (2000) Men with coronary artery disease have lower levels of androgens than men with normal coronary angiograms. Eur. Heart J. 21, 890-894 (Pubitemid 30307417)
40. English, K. M., Steeds, R. P., Jones, T. H., Diver, M. J., and Channer, K. S. (2000) Low-dose transdermal testosterone therapy improves angina threshold in men with chronic stable angina: A randomized, double-blind, placebo-controlled study. Circulation 102, 1906-1911
41. Rosano, G. M., Leonardo, F., Pagnotta, P., Pelliccia, F., Panina, G., Cerquetani, E., della Monica, P. L., Bonfigli, B., Volpe, M., and Chierchia, S. L. (1999) Acute anti-ischemic effect of testosterone in men with coronary artery disease. Circulation 99, 1666-1670 (Pubitemid 29162477)
42. Arain, F. A., Kuniyoshi, F. H., Abdalrhim, A. D., and Miller, V. M. (2009) Sex/gender medicine. The biological basis for personalized care in cardiovascular medicine. Circ. J. 73, 1774-1782
43. Cutolo, M., Balleari, E., Giusti, M., Intra, E., and Accardo, S. (1991) Androgen replacement therapy in male patients with rheumatoid arthritis. Arthritis Rheum. 34, 1-5