Transcellular biosynthesis of eicosanoid lipid mediators

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 4, 2015, Pages 377-382

  Capra, Valérie ^a   Rovati, G Enrico ^a   Mangano, Paolo ^b   Buccellati, Carola ^a   Murphy, Robert C ^c   Sala, Angelo ^a,d  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

^c UNIVERSITY OF COLORADO   (United States)

^d CNR Consiglio Nazionale delle Ricerche   (Italy)

Author keywords

Arachidonic acid; Cyclooxygenases; Eicosanoids; Lipoxygenases; Transcellular biosynthesis

Indexed keywords

ICOSANOID; LEUKOTRIENE A4; LIPOXIN; PROSTACYCLIN; THROMBOXANE A2; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID;

BIOSYNTHESIS; CELL COMMUNICATION; CELL METABOLISM; ENDOTHELIUM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; METABOLITE; NONHUMAN; PRIORITY JOURNAL; REVIEW; THROMBOCYTE; ANIMAL; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL COMMUNICATION; DOCOSAHEXAENOIC ACIDS; EICOSANOIDS; EICOSAPENTAENOIC ACID; EPOPROSTENOL; HUMANS; LEUKOTRIENE A4; LIPOXINS; SIGNAL TRANSDUCTION; THROMBOXANE A2;

EID: 84922496724     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.09.002     Document Type: Review

References (83)

1. B. Samuelsson Role of basic science in the development of new medicines: examples from the eicosanoid field J. Biol. Chem. 287 2012 10070 10080
2. J. Balsinde, M.V. Winstead, and E.A. Dennis Phospholipase A(2) regulation of arachidonic acid mobilization FEBS Lett. 531 2002 2 6
3. W.L. Smith, D.L. DeWitt, and R.M. Garavito Cyclooxygenases: structural, cellular, and molecular biology Annu. Rev. Biochem. 69 2000 145 182
4. D.F. Woodward, R.L. Jones, and S. Narumiya International Union of Basic and Clinical Pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress Pharmacol. Rev. 63 2011 471 538
5. J.B. Smith, and A.L. Willis Aspirin selectively inhibits prostaglandin production in human platelets Nat. New Biol. 231 1971 235 237
6. J.R. Vane Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs Nat. New Biol. 231 1971 232 235
7. T. Kobayashi, and S. Narumiya Function of prostanoid receptors: studies on knockout mice Prostaglandins Other Lipid Mediat. 68-69 2002 557 573
8. S. Narumiya, Y. Sugimoto, and F. Ushikubi Prostanoid receptors: structures, properties, and functions Physiol. Rev. 79 1999 1193 1226
9. B. Samuelsson Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation Science 220 1983 568 575
10. B. Samuelsson The discovery of the leukotrienes Am. J. Respir. Crit. Care Med. 161 2000 S2 S6
11. C.N. Serhan, M. Hamberg, and B. Samuelsson Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes Proc. Natl. Acad. Sci. U. S. A. 81 1984 5335 5339
12. C.A. Rouzer, and B. Samuelsson On the nature of the 5-lipoxygenase reaction in human leukocytes: enzyme purification and requirement for multiple stimulatory factors Proc. Natl. Acad. Sci. U. S. A. 82 1985 6040 6044
13. A.R. Brash, J.J. Murray, and J.A. Oates The 5-lipoxygenase and 15-lipoxygenase of neutrophils and eosinophils Prog. Clin. Biol. Res. 199 1985 143 152
14. T. Nabe, M. Miura, T. Kamiki, and S. Kohno Arachidonate 5-lipoxygenase and cyclooxygenase metabolites from guinea pig eosinophils and macrophages Jpn. J. Pharmacol. 83 2000 261 264
15. L. Macchia, M. Hamberg, M. Kumlin, J.H. Butterfield, and J.Z. Haeggstrom Arachidonic acid metabolism in the human mast cell line HMC-1: 5-lipoxygenase gene expression and biosynthesis of thromboxane Biochim. Biophys. Acta 1257 1995 58 74
16. P.J. Jakobsson, D. Steinhilber, B. Odlander, O. Radmark, H.E. Claesson, and B. Samuelsson On the expression and regulation of 5-lipoxygenase in human lymphocytes Proc. Natl. Acad. Sci. U. S. A. 89 1992 3521 3525
17. D.K. Miller, J.W. Gillard, P.J. Vickers, S. Sadowski, C. Leveille, J.A. Mancini, P. Charleson, R.A. Dixon, A.W. Ford-Hutchinson, and R. Fortin Identification and isolation of a membrane protein necessary for leukotriene production Nature 343 1990 278 281
18. G.K. Reid, S. Kargman, P.J. Vickers, J.A. Mancini, C. Leveille, D. Ethier, D.K. Miller, J.W. Gillard, R.A. Dixon, and J.F. Evans Correlation between expression of 5-lipoxygenase-activating protein, 5-lipoxygenase, and cellular leukotriene synthesis J. Biol. Chem. 265 1990 19818 19823
19. J.A. Mancini, M. Abramovitz, M.E. Cox, E. Wong, S. Charleson, H. Perrier, Z. Wang, P. Prasit, and P.J. Vickers 5-Lipoxygenase-activating protein is an arachidonate binding protein FEBS Lett. 318 1993 277 281
20. M. Back, W.S. Powell, S.E. Dahlen, J.M. Drazen, J.F. Evans, C.N. Serhan, T. Shimizu, T. Yokomizo, and G.E. Rovati Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR Review 7 Br. J. Pharmacol. 171 2014 3551 3574
21. T. Yokomizo Leukotriene B4 receptors: novel roles in immunological regulations Adv. Enzyme Regul. 51 2011 59 64
22. V. Capra, M. Back, S.S. Barbieri, M. Camera, E. Tremoli, and G.E. Rovati Eicosanoids and their drugs in cardiovascular diseases: focus on atherosclerosis and stroke Med. Res. Rev. 33 2013 364 438
23. A. Di Gennaro, and J.Z. Haeggstrom The leukotrienes: immune-modulating lipid mediators of disease Adv. Immunol. 116 2012 51 92
24. S. Bunting, R. Gryglewski, S. Moncada, and J.R. Vane Arterial walls generate from prostaglandin endoperoxides a substance (prostaglandin X) which relaxes strips of mesenteric and coeliac arteries and inhibits platelet aggregation Prostaglandins 12 1976 897 913
25. A. Sala, G. Rossoni, F. Berti, C. Buccellati, A. Bonazzi, J. Maclouf, and G. Folco Monoclonal anti-CD18 antibody prevents transcellular biosynthesis of cysteinyl leukotrienes in vitro and in vivo and protects against leukotriene-dependent increase in coronary vascular resistance and myocardial stiffness Circulation 101 2000 1436 1440
26. A. Sala, G. Rossoni, C. Buccellati, F. Berti, G. Folco, and J. Maclouf Formation of sulphidopeptide-leukotrienes by cell-cell interaction causes coronary vasoconstriction in isolated, cell-perfused heart of rabbit Br. J. Pharmacol. 110 1993 1206 1212
27. B.B. Weksler, A.J. Marcus, and E.A. Jaffe Synthesis of prostaglandin I2 (prostacyclin) by cultured human and bovine endothelial cells Proc. Natl. Acad. Sci. U. S. A. 74 1977 3922 3926
28. A.J. Marcus, B.B. Weksler, and E.A. Jaffe Enzymatic conversion of prostaglandin endoperoxide H2 and arachidonic acid to prostacyclin by cultured human endothelial cells J. Biol. Chem. 253 1978 7138 7141
29. A.J. Marcus, B.B. Weksler, E.A. Jaffe, and M.J. Broekman Synthesis of prostacyclin from platelet-derived endoperoxides by cultured human endothelial cells J. Clin. Invest. 66 1980 979 986
30. F. Merhi-Soussi, Z. Dominguez, O. Macovschi, M. Dubois, A. Savany, M. Lagarde, and A.F. Prigent Human lymphocytes stimulate prostacyclin synthesis in human umbilical vein endothelial cells. Involvement of endothelial cPLA2 J. Leukoc. Biol. 68 2000 881 889
31. S. Karim, A. Habib, S. Levy-Toledano, and J. Maclouf Cyclooxygenase-1 and -2 of endothelial cells utilize exogenous or endogenous arachidonic acid for transcellular production of thromboxane J. Biol. Chem. 271 1996 12042 12048
32. N. Maugeri, V. Evangelista, A. Celardo, G. Dell'Elba, N. Martelli, P. Piccardoni, G. de Gaetano, and C. Cerletti Polymorphonuclear leukocyte-platelet interaction: role of P-selectin in thromboxane B2 and leukotriene C4 cooperative synthesis Thromb. Haemost. 72 1994 450 456
33. N. Maugeri, V. Evangelista, P. Piccardoni, G. Dell'Elba, A. Celardo, G. de Gaetano, and C. Cerletti Transcellular metabolism of arachidonic acid: increased platelet thromboxane generation in the presence of activated polymorphonuclear leukocytes Blood 80 1992 447 451
34. A. Sala, T. Testa, and G. Folco Leukotriene A4, and not leukotriene B4, is the main 5-lipoxygenase metabolite released by bovine leukocytes FEBS Lett. 388 1996 94 98
35. A. Sala, M. Bolla, S. Zarini, R. Muller-Peddinghaus, and G. Folco Release of leukotriene A4 versus leukotriene B4 from human polymorphonuclear leukocytes J. Biol. Chem. 271 1996 17944 17948
36. F. Fitzpatrick, W. Liggett, J. McGee, S. Bunting, D. Morton, and B. Samuelsson Metabolism of leukotriene A4 by human erythrocytes. A novel cellular source of leukotriene B4 J. Biol. Chem. 259 1984 11403 11407
37. J.E. McGee, and F.A. Fitzpatrick Erythrocyte-neutrophil interactions: formation of leukotriene B4 by transcellular biosynthesis Proc. Natl. Acad. Sci. U. S. A. 83 1986 1349 1353
38. J.A. Mancini, R.J. Waugh, J.A. Thompson, J.F. Evans, M. Belley, R. Zamboni, and R.C. Murphy Structural characterization of the covalent attachment of leukotriene A3 to leukotriene A4 hydrolase Arch. Biochem. Biophys. 354 1998 117 124
39. S.J. Feinmark, and P.J. Cannon Endothelial cell leukotriene C4 synthesis results from intercellular transfer of leukotriene A4 synthesized by polymorphonuclear leukocytes J. Biol. Chem. 261 1986 16466 16472
40. H.E. Claesson, and J. Haeggstrom Human endothelial cells stimulate leukotriene synthesis and convert granulocyte released leukotriene A4 into leukotrienes B4, C4, D4 and E4 Eur. J. Biochem. 173 1988 93 100
41. J. Maclouf, R.C. Murphy, and P.M. Henson Transcellular sulfidopeptide leukotriene biosynthetic capacity of vascular cells Blood 74 1989 703 707
42. C. Edenius, K. Heidvall, and J.A. Lindgren Novel transcellular interaction: conversion of granulocyte-derived leukotriene A4 to cysteinyl-containing leukotrienes by human platelets Eur. J. Biochem. 178 1988 81 86
43. J.A. Maclouf, and R.C. Murphy Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets. A potential cellular source of leukotriene C4 J. Biol. Chem. 263 1988 174 181
44. J. Maclouf, R.C. Murphy, and P.M. Henson Transcellular biosynthesis of sulfidopeptide leukotrienes during receptor-mediated stimulation of human neutrophil/platelet mixtures Blood 76 1990 1838 1844
45. S.J. Feinmark, and P.J. Cannon Vascular smooth muscle cell leukotriene C4 synthesis: requirement for transcellular leukotriene A4 metabolism Biochim. Biophys. Acta 922 1987 125 135
46. A. Sala, S. Zarini, G. Folco, R.C. Murphy, and P.M. Henson Differential metabolism of exogenous and endogenous arachidonic acid in human neutrophils J. Biol. Chem. 274 1999 28264 28269
47. C.A. Dahinden, R.M. Clancy, M. Gross, J.M. Chiller, and T.E. Hugli Leukotriene C4 production by murine mast cells: evidence of a role for extracellular leukotriene A4 Proc. Natl. Acad. Sci. U. S. A. 82 1985 6632 6636
48. B. Odlander, P.J. Jakobsson, A. Rosen, and H.E. Claesson Human B and T lymphocytes convert leukotriene A4 into leukotriene B4 Biochem. Biophys. Res. Commun. 153 1988 203 208
49. T.D. Bigby, and N. Meslier Transcellular lipoxygenase metabolism between monocytes and platelets J. Immunol. 143 1989 1948 1954
50. J. Nowak, and G.A. FitzGerald Redirection of prostaglandin endoperoxide metabolism at the platelet-vascular interface in man J. Clin. Invest. 83 1989 380 385
51. F. Grimminger, G. Becker, and W. Seeger High yield enzymatic conversion of intravascular leukotriene A4 in blood-free perfused lungs J. Immunol. 141 1988 2431 2436
52. F. Grimminger, B. Kreusler, U. Schneider, E. von Witzleben, D. Walmrath, J. Neppert, and W. Seeger Human leukoagglutinating antibody evokes cooperative leukotriene synthesis in pulmonary microvasculature. Model of transfusion-related acute lung injury Circ. Res. 68 1991 503 512
53. G. Rossoni, A. Sala, F. Berti, T. Testa, C. Buccellati, C. Molta, R. Muller-Peddinghaus, J. Maclouf, and G.C. Folco Myocardial protection by the leukotriene synthesis inhibitor BAY X1005: importance of transcellular biosynthesis of cysteinyl-leukotrienes J. Pharmacol. Exp. Ther. 276 1996 335 341
54. A. Sala, G.M. Aliev, G. Rossoni, F. Berti, C. Buccellati, G. Burnstock, G. Folco, and J. Maclouf Morphological and functional changes of coronary vasculature caused by transcellular biosynthesis of sulfidopeptide leukotrienes in isolated heart of rabbit Blood 87 1996 1824 1832
55. A. Di Gennaro, C. Carnina, C. Buccellati, R. Ballerio, S. Zarini, F. Fumagalli, S. Viappiani, L. Librizzi, A. Hernandez, R.C. Murphy, G. Constantin, M. De Curtis, G. Folco, and A. Sala Cysteinyl-leukotriene receptor activation in brain inflammatory reactions and cerebral edema formation: a role for transcellular biosynthesis of cysteinyl leukotrienes FASEB J. 18 2004 839 841
56. J.E. Fabre, J.L. Goulet, E. Riche, M. Nguyen, K. Coggins, S. Offenbacher, and B.H. Koller Transcellular biosynthesis contributes to the production of leukotrienes during inflammatory responses in vivo J. Clin. Invest. 109 2002 1373 1380
57. S. Zarini, M.A. Gijon, A.E. Ransome, R.C. Murphy, and A. Sala Transcellular biosynthesis of cysteinyl leukotrienes in vivo during mouse peritoneal inflammation Proc. Natl. Acad. Sci. U. S. A. 106 2009 8296 8301
58. C.N. Serhan Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways Annu. Rev. Immunol. 25 2007 101 137
59. B. Samuelsson, S.E. Dahlen, J.A. Lindgren, C.A. Rouzer, and C.N. Serhan Leukotrienes and lipoxins: structures, biosynthesis, and biological effects Science 237 1987 1171 1176
60. K. Gronert, C.B. Clish, M. Romano, and C.N. Serhan Transcellular regulation of eicosanoid biosynthesis Methods Mol. Biol. 120 1999 119 144
61. M. Romano, X.S. Chen, Y. Takahashi, S. Yamamoto, C.D. Funk, and C.N. Serhan Lipoxin synthase activity of human platelet 12-lipoxygenase Biochem. J. 296 Pt 1 1993 127 133
62. S. Fiore, and C.N. Serhan Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils J. Exp. Med. 172 1990 1451 1457
63. C.N. Serhan, and K.A. Sheppard Lipoxin formation during human neutrophil-platelet interactions. Evidence for the transformation of leukotriene A4 by platelet 12-lipoxygenase in vitro J. Clin. Invest. 85 1990 772 780
64. J. Claria, and C.N. Serhan Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions Proc. Natl. Acad. Sci. U. S. A. 92 1995 9475 9479
65. J. Claria, M.H. Lee, and C.N. Serhan Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation Mol. Med. 2 1996 583 596
66. N. Chiang, E.A. Bermudez, P.M. Ridker, S. Hurwitz, and C.N. Serhan Aspirin triggers antiinflammatory 15-epi-lipoxin A4 and inhibits thromboxane in a randomized human trial Proc. Natl. Acad. Sci. U. S. A. 101 2004 15178 15183
67. N. Chiang, C.N. Serhan, S.E. Dahlen, J.M. Drazen, D.W. Hay, G.E. Rovati, T. Shimizu, T. Yokomizo, and C. Brink The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo Pharmacol. Rev. 58 2006 463 487
68. C. Godson, S. Mitchell, K. Harvey, N.A. Petasis, N. Hogg, and H.R. Brady Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages J. Immunol. 164 2000 1663 1667
69. C. Barnig, M. Cernadas, S. Dutile, X. Liu, M.A. Perrella, S. Kazani, M.E. Wechsler, E. Israel, and B.D. Levy Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma Sci. Transl. Med. 5 174 2013 10.1126/scitranslmed.3004812
70. S. Fiore, J.F. Maddox, H.D. Perez, and C.N. Serhan Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor J. Exp. Med. 180 1994 253 260
71. S. Fiore, S.W. Ryeom, P.F. Weller, and C.N. Serhan Lipoxin recognition sites. Specific binding of labeled lipoxin A4 with human neutrophils J. Biol. Chem. 267 1992 16168 16176
72. S. Krishnamoorthy, A. Recchiuti, N. Chiang, S. Yacoubian, C.H. Lee, R. Yang, N.A. Petasis, and C.N. Serhan Resolvin D1 binds human phagocytes with evidence for proresolving receptors Proc. Natl. Acad. Sci. U. S. A. 107 2010 1660 1665
73. J. Dalli, A.P. Consalvo, V. Ray, C. Di Filippo, M. D'Amico, N. Mehta, and M. Perretti Proresolving and tissue-protective actions of annexin A1-based cleavage-resistant peptides are mediated by formyl peptide receptor 2/lipoxin A4 receptor J. Immunol. 190 2013 6478 6487
74. H. Forsman, K. Onnheim, E. Andreasson, and C. Dahlgren What formyl peptide receptors, if any, are triggered by compound 43 and lipoxin A4? Scand. J. Immunol. 74 2011 227 234
75. J. Hanson, N. Ferreiros, B. Pirotte, G. Geisslinger, and S. Offermanns Heterologously expressed formyl peptide receptor 2 FPR2/ALX) does not respond to lipoxin A(4) Biochem. Pharmacol. 85 2013 1795 1802
76. C.N. Serhan, C.B. Clish, J. Brannon, S.P. Colgan, N. Chiang, and K. Gronert Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing J. Exp. Med. 192 2000 1197 1204
77. M. Arita, T. Ohira, Y.P. Sun, S. Elangovan, N. Chiang, and C.N. Serhan Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation J. Immunol. 178 2007 3912 3917
78. M. Arita, F. Bianchini, J. Aliberti, A. Sher, N. Chiang, S. Hong, R. Yang, N.A. Petasis, and C.N. Serhan Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1 J. Exp. Med. 201 2005 713 722
79. J.M. Schwab, N. Chiang, M. Arita, and C.N. Serhan Resolvin E1 and protectin D1 activate inflammation-resolution programmes Nature 447 2007 869 874
80. C.N. Serhan, S. Hong, K. Gronert, S.P. Colgan, P.R. Devchand, G. Mirick, and R.L. Moussignac Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals J. Exp. Med. 196 2002 1025 1037
81. S. Hong, K. Gronert, P.R. Devchand, R.L. Moussignac, and C.N. Serhan Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation J. Biol. Chem. 278 2003 14677 14687
82. G.M. Nassar, J.D. Morrow, L.J. Roberts II, F.G. Lakkis, and K.F. Badr Induction of 15-lipoxygenase by interleukin-13 in human blood monocytes J. Biol. Chem. 269 1994 27631 27634
83. B.D. Levy, M. Romano, H.A. Chapman, J.J. Reilly, J. Drazen, and C.N. Serhan Human alveolar macrophages have 15-lipoxygenase and generate 15(S)-hydroxy-5,8,11-cis-13-trans-eicosatetraenoic acid and lipoxins J. Clin. Invest. 92 1993 1572 1579