Molecular regulators of resolution of inflammation: Potential therapeutic targets in the reproductive system

Reproduction

Volumn 142, Issue 1, 2011, Pages 15-28

  Hutchinson, James L ^a   Rajagopal, Shalini P ^a   Sales, Kurt J ^a   Jabbour, Henry N ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR5; COLLAGENASE 3; CYCLOOXYGENASE 2; FORMYLPEPTIDE RECEPTOR; G PROTEIN COUPLED RECEPTOR; GELATINASE A; GLUCOCORTICOID; HYDROXYICOSATETRAENOIC ACID; ICOSANOID; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; L SELECTIN; LEUKOTRIENE; LIPOCORTIN 1; LIPOXIN; LIPOXIN A; LIPOXIN B; LIPOXYGENASE; PLATELET DERIVED GROWTH FACTOR; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN ENDOPEROXIDE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN;

CELL POPULATION; DNA FLANKING REGION; FEMALE GENITAL SYSTEM FUNCTION; GENE OVEREXPRESSION; HUMAN; IMMUNOCOMPETENT CELL; LABOR; OVULATION; PHENOTYPE; PLEIOTROPY; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANNEXIN A1; ANTI-INFLAMMATORY AGENTS; EICOSANOIDS; FATTY ACIDS, OMEGA-3; FEMALE; GENITAL DISEASES, FEMALE; GENITALIA, FEMALE; GLUCOCORTICOIDS; HOMEOSTASIS; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, LIPOXIN; REPRODUCTION; SIGNAL TRANSDUCTION;

EID: 79960466395     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0069     Document Type: Review

References (135)

1. Andersen CY 2002 Possible new mechanism of cortisol action in female reproductive organs: physiological implications of the free hormone hypothesis. Journal of Endocrinology 173 211-217. (doi:10.1677/joe.0.1730211)
2. Ariel A & Serhan CN 2007 Resolvins and protectins in the termination program of acute inflammation. Trends in Immunology 28 176-183. (doi:10.1016/j.it.2007.02.007)
3. Ariel A, Fredman G, Sun YP, Kantarci A, Van Dyke TE, Luster AD & Serhan CN 2006 Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nature Immunology 7 1209-1216. (doi:10.1038/ni1392)
4. 4 receptor BLT1 and ChemR23 to regulate inflammation. Journal of Immunology 178 3912-3917.
5. 4 in rat glomerular mesangial cells: evidence for competition at a common receptor. PNAS 86 3438-3442. (doi:10.1073/pnas.86.9.3438)
6. 4: anti-inflammatory and anti-angiogenic impact on endothelial cells. Journal of Immunology 182 3819-3826. (doi:10.4049/jimmunol.0803175)
7. Bennett P, Slater D, Berger L & Moor G 1994 The expression of phospholipase A2 and lipocortins (annexins) I, II and V in human fetal membranes and placenta in association with labour. Prostaglandins 48 81-90. (doi:10.1016/0090-6980(94)90086-8)
8. 4 from alveolar macrophages in severe asthma. Respiratory Research 11 71-80. (doi:10.1186/1465-9921-11-71)
9. Brannstrom M, Pascoe V, Norman RJ & McClure N 1994 Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertility and Sterility 61 488-495. (Pubitemid 24083151)
10. Brezinski ME, Gimbrone MA Jr, Nicolaou KC & Serhan CN 1989 Lipoxins stimulate prostacyclin generation by human endothelial cells. FEBS Letters 245 167-172. (doi:10.1016/0014-5793(89)80214-5)
11. Brown NL, Slater DM, Alvi SA, Elder MG, Sullivan MHF & Bennett PR 1999 Expression of 5-lipoxygenase and 5-lipoxygenase-activating protein in human fetal membranes throughout pregnancy and at term. Molecular Human Repoduction 5 668-674. (doi:10.1093/molehr/5.7.668)
12. Burli RW, Xu H, Zou X, Muller K, Golden J, Frohn M, Adlam M, Plant MH, Wong M, McElvain M et al. 2006 Potent hFPRL1 (ALXR) agonists as potential anti-inflammatory agents. Bioorganic & Medicinal Chemistry Letters 16 3713-3718. (doi:10.1016/j.bmcl.2006.04.068)
13. Chan J, Rabbitt EH, Innes BA, Bulmer JN, Stewart PM, Kilby MD & Hewison M 2007 Glucocorticoid-induced apoptosis in human decidua: a novel role for 11beta-hydroxysteroid dehydrogenase in late gestation. Journal of Endocrinology 195 7-15. (doi:10.1677/JOE-07-0289)
14. 4 on experimental endometriosis. European Journal of Obstetrics, Gynecology, and Reproductive Biology 145 200-204. (doi:10.1016/j.ejogrb.2009.05.015)
15. Chen K, Le Y, Liu Y, Gong W, Ying G, Huang J, Yoshimura T, Tessarollo L & Wang JM 2010a A critical role for the G protein-coupled receptor mFPR2 in airway inflammation and immune responses. Journal of Immunology 184 3331-3335. (doi:10.4049/jimmunol.0903022)
16. Chen QH, Zhou WD, Pu DM, Huang QS, Li T & Chen QX 2010b 15-Epi-lipoxinA(4) inhibits the progression of endometriosis in a murine model. Fertility and Sterility 93 1440-1447. (doi:10.1016/j.fertnstert.2009.01.107)
17. Claria J & Serhan CN 1995 Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. PNAS 92 9475-9479. (doi:10.1073/pnas.92.21.9475)
18. 4 modulates transmigration of human neutrophils across intestinal epithelial monolayers. Journal of Clinical Investigation 92 75-82. (doi:10.1172/JCI116601)
19. Conte FP, Menezes-de-Lima O Jr, Verri WA Jr, Cunha FQ, Penido C & Henriques MG 2010 Lipoxin A(4) attenuates zymosan-induced arthritis by modulating endothelin-1 and its effects. British Journal of Pharmacology 161 911-924. (doi:10.1111/j.1476-5381.2010.00950.x)
20. Corriveau S, Rousseau E, Berthiaume M & Pasquier JC 2010 Lipoxygenase and cyclooxygenase inhibitors reveal a complementary role of arachidonic acid derivatives in pregnant human myometrium. American Journal of Obstetrics and Gynaecology 203 266e261-266e267. (doi:10.1016/j.ajog.2010.06.009)
21. Curry TE Jr, Mann JS, Huang MH & Keeble SC 1992 Gelatinase and proteoglycanase activity during the periovulatory period in the rat. Biology of Reproduction 46 256-264. (doi:10.1095/biolreprod46.2.256)
22. De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ & Chertov O 2000 LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. Journal of Experimental Medicine 192 1069-1074. (doi:10.1084/jem.192.7.1069)
23. Duffy CD & Guiry PJ 2010 Recent advances in the chemistry and biology of stable synthetic lipoxin analogues. Medicinal Chemistry Communications 1 249-265. (doi:10.1039/c0md00136h)
24. Dufton N, Hannon R, Brancaleone V, Dalli J, Patel HB, Gray M, D'Acquisto F, Buckingham JC, Perretti M & Flower RJ 2010 Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. Journal of Immunology 184 2611-2619. (doi:10.4049/jimmunol.0903526)
25. El Kebir D, Jozsef L, Khreiss T, Pan W, Petasis NA, Serhan CN & Filep JG 2007 Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid A in human neutrophils: a novel mechanism for resolution of inflammation. Journal of Immunology 179 616-622. (Pubitemid 46986579)
26. Endo T & Kanayama K 1998 Phagocytotic activity of macrophages separated from corpus lutea of pseudopregnant rabbits. Journal of International Medical Research 26 248-251. (Pubitemid 29017173)
27. Ernst S, Lange C, Wilbers A, Goebeler V, Gerke V & Rescher U 2004 An annexin 1 N-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. Journal of Immunology 172 7669-7676. (Pubitemid 38747633)
28. Filep JG, Zouki C, Petasis NA, Hachicha M & Serhan CN 1999 Anti-inflammatory actions of lipoxin A(4) stable analogs are demonstrable in human whole blood: modulation of leukocyte adhesion molecules and inhibition of neutrophil-endothelial interactions. Blood 94 4132-4142.
29. Filep JG, Khreiss T & Jozsef L 2005 Lipoxins and aspirin-triggered lipoxins in neutrophil adhesion and signal transduction. Prostaglandins, Leukotrienes, and Essential Fatty Acids 73 257-262. (doi:10.1016/j.plefa.2005. 05.014)
30. 4 receptors in HL-60 cells. Blood 81 3395-3403.
31. 4 receptor. Journal of Experimental Medicine 180 253-260. (doi:10.1084/jem.180.1.253)
32. Flower RJ 1988 Eleventh Gaddum memorial lecture. Lipocortin and the mechanism of action of the glucocorticoids. British Journal of Pharmacology 94 987-1015.
33. Forsman H & Dahlgren C 2010 The FPR2-induced rise in cytosolic calcium in human neutrophils relies on an emptying of intracellular calcium stores and is inhibited by a gelsolin-derived PIP2-binding peptide. BMC Cell Biology 11 52. (doi:10.1186/1471-2121-11-52)
34. Gastardelo TS, Damazo AS, Dalli J, Flower RJ, Perretti M & Oliani SM 2009 Functional and ultrastructural analysis of annexin A1 and its receptor in extravasating neutrophils during acute inflammation. American Journal of Pathology 174 177-183. (doi:10.2353/ajpath.2009.080342)
35. Gaytan M, Bellido C, Morales C, Sanchez-Criado JE & Gaytan F 2006 Effects of selective inhibition of cyclooxygenase and lipooxygenase pathways in follicle rupture and ovulation in the rat. Reproduction 132 571-577. (doi:10.1530/rep.1.01236)
36. 4 analogs attenuate induction of intestinal epithelial proinflammatory gene expression and reduce the severity of dextran sodium sulfate-induced colitis. Journal of Immunology 168 5260-5267.
37. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ & Willoughby DA 1999 Inducible cyclooxygenase may have antiinflammatory properties. Nature Medicine 5 698-701. (doi:10.1038/9550)
38. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N & Brady HR 2000 Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. Journal of Immunology 164 1663-1667. (Pubitemid 30108713)
39. 4 receptor that is regulated by interleukin (IL)-13 and interferon gamma and inhibits tumor necrosis factor alpha-induced IL-8 release. Journal of Experimental Medicine 187 1285-1294. (doi:10.1084/jem.187.8.1285)
40. Gronert K, Martinsson-Niskanen T, Ravasi S, Chiang N & Serhan CN 2001 Selectivity of recombinant human leukotriene D(4), leukotriene B(4), and lipoxin A(4) receptors with aspirin-triggered 15-epi-LXA(4) and regulation of vascular and inflammatory responses. American Journal of Pathology 158 3-9. (doi:10.1016/S0002-9440(10)63937-5)
41. Gurpide E, Markiewicz L, Schatz F & Hirata F 1986 Lipocortin output by human endometrium in vitro. Journal of Clinical Endocrinology and Metabolism 63 162-166. (doi:10.1210/jcem-63-1-162)
42. Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, Berg G, Sharma S, Buer J & Ernerudh J 2008 Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS ONE 3 e2078. (doi:10.1371/journal.pone.0002078)
43. Hannon R, Croxtall JD, Getting SJ, Roviezzo F, Yona S, Paul-Clark MJ, Gavins FN, Perretti M, Morris JF, Buckingham JC et al. 2003 Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB Journal 17 253-255.
44. Harris JG, Flower RJ & Perretti M 1995 Alteration of neutrophil trafficking by a lipocortin 1 N-terminus peptide. European Journal of Pharmacology 279 149-157. (doi:10.1016/0014-2999(95)00145-B)
45. Hashii K, Fujiwara H, Yoshioka S, Kataoka N, Yamada S, Hirano T, Mori T, Fujii S & Maeda M 1998 Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Human Reproduction 13 2738-2744. (Pubitemid 28482718)
46. Hayhoe RP, Kamal AM, Solito E, Flower RJ, Cooper D & Perretti M 2006 Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement. Blood 107 2123-2130. (doi:10.1182/blood-2005-08-3099)
47. 4R. Blood 101 1572-1581. (doi:10.1182/blood-2002-05-1431)
48. Hofer G, Bieglmayer C, Kopp B & Janisch H 1993 Measurement of eicosanoids in menstrual fluid by the combined use of high pressure chromatography and radioimmunoassay. Prostaglandins 45 413-426. (doi:10.1016/0090-6980(93)90118-Q)
49. Jabbour HN, Sales KJ, Catalano RD & Norman JE 2009 Inflammatory pathways in female reproductive health and disease. Reproduction 138 903-919. (doi:10.1530/REP-09-0247)
50. Kaitu'u-Lino TJ, Morison NB & Salamonsen LA 2007 Neutrophil depletion retards endometrial repair in a mouse model. Cell Tissue Research 328 197-206. (doi:10.1007/s00441-006-0358-2)
51. Kalsotra A, Anakk S, Brommer CL, Kikuta Y, Morgan ET & Strobel HW 2007 Catalytic characterization and cytokine mediated regulation of cytochrome P450 4Fs in rat hepatocytes. Archives of Biochemistry and Biophysics 461 104-112. (doi:10.1016/j.abb.2007.02.027)
52. Kamal AM, Hayhoe RP, Paramasivam A, Cooper D, Flower RJ, Solito E & Perretti M 2006 Antiflammin-2 activates the human formyl-peptide receptor like 1. Scientific World Journal 6 1375-1384. (doi:10.1100/tsw.2006.247)
53. Kim JA, Gu J-L, Natarajan R, Berliner JA & Nadler JL 1995 A leukocyte type of 12-lipoxygenase Is expressed in human vascular and mononuclear cells: evidence for upregulation by angiotensin II. Arteriosclerosis, Thrombosis, and Vascular Biology 15 942-948.
54. 4 receptor BLT2 in VEGF-induced angiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology 29 915-920. (doi:10.1161/ATVBAHA.109.185793)
55. Koczulla R, von Degenfeld G, Kupatt C, Krotz F, Zahler S, Gloe T, Issbrucker K, Unterberger P, Zaiou M, Lebherz C et al. 2003 An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. Journal of Clinical Investigation 111 1665-1672. (doi:10.1172/JCI17545)
56. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee CH, Yang R, Petasis NA & Serhan CN 2010 Resolvin D1 binds human phagocytes with evidence for proresolving receptors. PNAS 107 1660-1665. (doi:10.1073/pnas.0907342107)
57. 2 production in gonadotropin-primed immature rats. Reproduction 137 59-66. (doi:10.1530/REP-08-0257)
58. Laresgoiti-Servitje E, Gomez-Lopez N & Olson DM 2010 An immunological insight into the origins of pre-eclampsia. Human Reproduction Update 16 510-524. (doi:10.1093/humupd/dmq007)
59. 4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clinical Science 77 195-203.
60. Lee HY, Kim SD, Shim JW, Kim HJ, Yun J, Baek SH, Kim K & Bae YS 2010 A pertussis toxin sensitive G-protein-independent pathway is involved in serum amyloid A-induced formyl peptide receptor 2-mediated CCL2 production. Experimental & Molecular Medicine 42 302-309. (doi:10.3858/emm.2010.42.4. 029)
61. Lei ZM & Rao CV 1992 The expression of 15-lipoxygenase gene and the presence of functional enzyme in cytoplasm and nuclei of pregnancy humanmyometria. Endocrinology 130 861-870. (doi:10.1210/en.130.2.861)
62. Levy BD, Clish CB, Schmidt B, Gronert K & Serhan CN 2001 Lipid mediator class switching during acute inflammation: signals in resolution. Nature Immunology 2 612-619. (doi:10.1038/89759)
63. Li Q, Cheon YP, Kannan A, Shanker S, Bagchi IC & Bagchi MK 2004 A novel pathway involving progesterone receptor, 12/15-lipoxygenase-derived eicosanoids, and peroxisome proliferator-activated receptor gamma regulates implantation in mice. Journal of Biological Chemistry 279 11570-11581. (doi:10.1074/jbc.M311773200)
64. Li CY, Lang JH, Liu HY & Zhou HM 2008 Expression of annexin-1 in patients with endometriosis. Chinese Medical Journal 121 927-931.
65. Liu Y, Cousin JM, Hughes J, Van Damme J, Seckl JR, Haslett C, Dransfield I, Savill J & Rossi AG 1999 Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes. Journal of Immunology 162 3639-3646. (Pubitemid 29313619)
66. Liu Y, Tang X, Lu C, Han W, Guo S & Zhu D 2009 Expression of 15-lipoxygenase in pulmonary arteries after hypoxia. Pathology 41 476-483. (doi:10.1080/00313020903040970)
67. Lynch-Salamon DI, Everson WV & Myatt L 1992 Decrease in annexin I messenger ribonucleic acid expression in human amnion with labor. American Journal of Obstetrics and Gynaecology 167 1657-1663. (Pubitemid 23009306)
68. 4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. Journal of Experimental Medicine 183 137-146. (doi:10.1084/jem.183.1.137)
69. 4 receptor. Journal of Biological Chemistry 272 6972-6978. (doi:10.1074/jbc.272. 49.30993)
70. 4 analogs with increased biologic activity. FASEB Journal 12 487-494.
71. Maldonado-Pérez D, Golightly E, Denison F, Jabbour H & Norman J 2010 A role for lipoxins as anti-inflammatory and pro-resolutionmediators in human parturition. FASEB Journal 25 569-575. (doi:10.1096/fj.10-170340)
72. Mandal AK, Skoch J, Bacskai BJ, Hyman BT, Christmas P, Miller D, Yamin T-tD, Xu S, Wisniewski D & Evans JF 2004 The membrane organization of leukotriene synthesis. PNAS 101 6587-6592. (doi:10.1073/pnas.0308523101)
73. Maybin JA, Critchley HO & Jabbour HN 2010 Inflammatory pathways in endometrial disorders. Molecular Cell 335 42-51. (doi:10.1016/j.mce.2010.08.006)
74. McMahon B, Mitchell D, Shattock R, Martin F, Brady HR & Godson C 2002 Lipoxin, leukotriene, and PDGF receptors cross-talk to regulate mesangial cell proliferation. FASEB Journal 16 1817-1819.
75. Meola J, Rosa e Silva JC, Dentillo DB, da Silva WA Jr, Veiga-Castelli LC, Bernardes LA, Ferriani RA, de Paz CC, Giuliatti S & Martelli L 2010 Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertility and Sterility 93 1750-1773. (doi:10.1016/j.fertnstert. 2008.12.058)
76. Migeotte I, Communi D & Parmentier M 2006 Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine & Growth Factor Reviews 17 501-519. (doi:10.1016/j. cytogfr.2006.09.009)
77. 4 receptor in physiologically estrus cycle and pathologically endometriosis. Biomedicine & Pharmacotherapy 59 330-338. (doi:10.1016/j.biopha.2005.05.005)
78. van Mourik MS, Macklon NS & Heijnen CJ 2009 Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. Journal of Leukocyte Biology 85 4-19. (doi:10.1189/jlb.0708395)
79. Mulla A, Leroux C, Solito E & Buckingham JC 2005 Correlation between the antiinflammatory protein annexin 1 (lipocortin 1) and serum cortisol in subjects with normal and dysregulated adrenal function. Journal of Clinical Endocrinology and Metabolism 90 557-562. (doi:10.1210/jc.2004-1230)
80. Munck A, Guyre PM & Holbrook NJ 1984 Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews 5 25-44. (doi:10.1210/edrv-5-1-25)
81. Myatt L, Hirth J & Everson WV 1992 Changes in annexin (lipocortin) content in human amnion and chorion at parturition. Journal of Cellular Biochemistry 50 363-373. (doi:10.1002/jcb.240500405)
82. Nassar GM, Morrow JD, Roberts LJ II, Lakkis FG & Badr KF 1994 Induction of 15-lipoxygenase by interleukin-13 in human blood monocytes. Journal of Biological Chemistry 269 27631-27634.
83. Norling LV & Serhan CN 2010 Profiling in resolving inflammatory exudates identifies novel anti-inflammatory and pro-resolving mediators and signals for termination. Journal of Internal Medicine 268 15-24. (doi:10.1111/j.1365-2796.2010.02235.x)
84. 4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. Journal of Immunology 156 2264-2272.
85. 2-mediated immunosuppression by first trimester human decidual cells blocks activation of maternal leukocytes in the decidua with potential anti-trophoblast activity. Cellular Immunology 120 61-74. (doi:10.1016/0008-8749(89)90174-3)
86. 4-mediated induction of nitric oxide explains how aspirin inhibits acute inflammation. Journal of Experimental Medicine 200 69-78. (doi:10.1084/jem.20040566)
87. Pederzoli-Ribeil M, Maione F, Cooper D, Al-Kashi A, Dalli J, Perretti M & D'Acquisto F 2010 Design and characterization of a cleavage-resistant annexin A1 mutant to control inflammation in the microvasculature. Blood 116 4288-4296. (doi:10.1182/blood-2010-02-270520)
88. Perretti M & D'Acquisto F 2009 Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nature Reviews. Immunology 9 62-70. (doi:10.1038/nri2470)
89. Perretti M & Dalli J 2009 Exploiting the annexin A1 pathway for the development of novel anti-inflammatory therapeutics. British Journal of Pharmacology 158 936-946. (doi:10.1111/j.1476-5381.2009.00483.x)
90. Perretti M, Ahluwalia A, Harris JG, Goulding NJ & Flower RJ 1993 Lipocortin-1 fragments inhibit neutrophil accumulation and neutrophil-dependent edema in the mouse. A qualitative comparison with an anti-CD11b monoclonal antibody. Journal of Immunology 151 4306-4314.
91. Perretti M, Croxtall JD, Wheller SK, Goulding NJ, Hannon R & Flower RJ 1996 Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nature Medicine 2 1259-1262. (doi:10.1038/nm1196-1259)
92. 4 receptor. Nature Medicine 8 1296-1302. (doi:10.1038/nm786)
93. Rae M, Mohamad A, Price D, Hadoke PW, Walker BR, Mason JI, Hillier SG & Critchley HO 2009 Cortisol inactivation by 11beta-hydroxysteroid dehydrogenase-2 may enhance endometrial angiogenesis via reduced thrombospondin-1 in heavymenstruation. Journal of Clinical Endocrinology and Metabolism 94 1443-1450. (doi:10.1210/jc.2008-1879)
94. Ramstedt U, Serhan CN, Nicolaou KC, Webber SE, Wigzell H & Samuelsson B 1987 Lipoxin A-induced inhibition of human natural killer cell cytotoxicity: studies on stereospecificity of inhibition and mode of action. Journal of Immunology 138 266-270. (Pubitemid 17218429)
95. Rees MC, DiMarzo V, Tippins JR, Morris HR & Turnbull AC 1987 Leukotriene release by endometrium and myometrium throughout the menstrual cycle in dysmenorrhoea and menorrhagia. Journal of Endocrinology 113 291-295. (doi:10.1677/joe.0.1130291)
96. Robb AO, Din JN, Mills NL, Smith IB, Blomberg A, Zikry MN, Raftis JB, Newby DE & Denison FC 2010 The influence of the menstrual cycle, normal pregnancy and pre-eclampsia on platelet activation. Thrombosis and Haemostasis 103 372-378. (doi:10.1160/TH08-12-0780)
97. 4 modifies platelet-derived growth factor-induced pro-fibrotic gene expression in human renal mesangial cells. American Journal of Pathology 167 683-694. (doi:10.1016/S0002-9440(10)62043-3)
98. Romano M, Chen X, Takahashi Y, Yamamoto S, Funk C & Serhan C 1993 Lipoxin synthase activity of human platelet 12-lipoxygenase. Journal of Biochemistry 296 127-133. (Pubitemid 23344739)
99. Romisch J, Schuler E, Bastian B, Burger T, Dunkel FG, Schwinn A, Hartmann AA & Paques EP 1992 Annexins I to VI: quantitative determination in different human cell types and in plasma after myocardial infarction. Blood Coagulation & Fibrinolysis 3 11-17. (doi:10.1097/00001721-199202000-00003)
100. Rosengarth A & Luecke H 2003 A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. Journal of Molecular Biology 326 1317-1325. (doi:10.1016/S0022-2836(03)00027-5)
101. Rydberg EK, Krettek A, Ullstrom C, Ekstrom K, Svensson PA, Carlsson LM, Jonsson-Rylander AC, Hansson GI, McPheat W, Wiklund O et al. 2004 Hypoxia increases LDL oxidation and expression of 15-lipoxygenase-2 in human macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology 24 2040-2045. (doi:10.1161/01.ATV.0000144951.08072.0b)
102. Salamonsen LA 2003 Tissue injury and repair in the female human reproductive tract. Reproduction 125 301-311. (doi:10.1530/rep.0.1250301)
103. Samuelsson B, Dahlen S, Lindgren J, Rouzer C & Serhan C 1987 Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 237 1171-1176. (doi:10.1126/science.2820055)
104. Scannell M, Flanagan MB, deStefani A, Wynne KJ, Cagney G, Godson C & Maderna P 2007 Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. Journal of Immunology 178 4595-4605.
105. 4: a new class of ligand for the Ah receptor. Biochemistry 38 7594-7600. (doi:10.1021/bi982861e)
106. Serhan C 2005 Preface: special issue on lipoxins and aspirin-triggered lipoxins. Prostaglandins, Leukotrienes, and Essential Fatty Acids 73 139-321. (doi:10.1016/j.plefa.2005.07.001)
107. Serhan CN, Hamberg M & Samuelsson B 1984a Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. PNAS 81 5335-5339. (doi:10.1073/pnas.81.17.5335)
108. Serhan CN, Hamberg M & Samuelsson B 1984b Trihydroxytetraenes: a novel series of compounds formed from arachidonic acid in human leukocytes. Biochemistry and Biophysical Research Communications 118 943-949. (doi:10.1016/0006-291X(84)91486-4)
109. Serhan CN, Jain A, Marleau S, Clish C, Kantarci A, Behbehani B, Colgan SP, Stahl GL, Merched A, Petasis NA et al. 2003 Reduced inflammation and tissue damage in transgenic rabbits overexpressing 15-lipoxygenase and endogenous anti-inflammatory lipid mediators. Journal of Immunology 171 6856-6865. (Pubitemid 37532121)
110. Serhan CN, Chiang N & Van Dyke TE 2008 Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Reviews. Immunology 8 349-361. (doi:10.1038/nri2294)
111. 4 inhibits human monocyte apoptosis: involvement of ERK-2 and PI3-kinase. Prostaglandins & Other Lipid Mediators 91 10-17. (doi:10.1016/j.prostaglandins.2009.12.001)
112. 4 by 5-lipoxygenase mediates PPARgamma-dependent, neuroprotective effects of rosiglitazone in experimental stroke. Journal of Neuroscience 29 3875-3884. (doi:10.1523/JNEUROSCI.5529-08.2009)
113. 4 inhibits IL-1 beta-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. Journal of Immunology 164 2660-2666.
114. 4 and serum amyloid A via the common lipoxin A receptor. International Journal of Immunopathology and Pharmacology 17 145-156.
115. Solito E, Kamal A, Russo-Marie F, Buckingham JC, Marullo S & Perretti M 2003 A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB Journal 17 1544-1546.
116. Spanbroek R, Hildner M, Köhler A, Müller A, Zintl F, Kühn H, Rådmark O, Samuelsson B & Habenicht AJR 2001 IL-4 determines eicosanoid formation in dendritic cells by down-regulation of 5-lipoxygenase and up-regulation of 15-lipoxygenase 1 expression. PNAS 98 5152-5157. (doi:10.1073/pnas.091076998)
117. Spurr L, Nadkarni S, Pederzoli-Ribeil M, Goulding NJ, Perretti M & D'Acquisto F 2010 Comparative analysis of annexin A1-formyl peptide receptor 2/ALX expression in human leukocyte subsets. International Immunopharmacology 11 55-66. (doi:10.1016/j.intimp.2010.10.006)
118. Stenfeldt AL, Karlsson J, Wenneras C, Bylund J, Fu H & Dahlgren C 2007 Cyclosporin H, Boc-MLF and Boc-FLFLF are antagonists that preferentially inhibit activity triggered through the formyl peptide receptor. Inflammation 30 224-229. (doi:10.1007/s10753-007-9040-4)
119. Strausbaugh HJ & Rosen SD 2001 A potential role for annexin 1 as a physiologic mediator of glucocorticoid-induced L-selectin shedding from myeloid cells. Journal of Immunology 166 6294-6300. (Pubitemid 32440762)
120. Stygar D, Masironi B, Eriksson H & Sahlin L 2007 Studies on estrogen receptor (ER) {alpha} and {beta} responses on gene regulation in peripheral blood leukocytes in vivo using selective ER agonists. Journal of Endocrinology 194 101-119. (doi:10.1677/JOE-06-0060)
121. Sun M, Liu Y & Gibb W 1996 Distribution of annexin I and II in term human fetal membranes, decidua and placenta. Placenta 17 181-184. (doi:10.1016/S0143-4004(96)80012-9)
122. Tagoe CE, Marjanovic N, Park JY, Chan ES, Abeles AM, Attur M, Abramson SB & Pillinger MH 2008 Annexin-1 mediates TNF-alpha-stimulated matrix metalloproteinase secretion from rheumatoid arthritis synovial fibroblasts. Journal of Immunology 181 2813-2820.
123. Tanaka N, Espey L & Okamura H 1989 Increase in ovarian 15-hydroxyeicosatetraenoic acid during ovulation in the gonadotropin-primed immature rat. Endocrinology 125 1373-1377. (doi:10.1210/endo-125-3-1373)
124. Titos E, Clària J, Planagumà A, López-Parra M, González-Périz A, Gaya J, Miquel R, Arroyo V & Rodés J 2005 Inhibition of 5-lipoxygenase-activating protein abrogates experimental liver injury: role of Kupffer cells. Journal of Leukocyte Biology 78 871-878. (doi:10.1189/jlb.1204747)
125. Tsao FH, Chen X & Ts'ao CH 1995 Annexin I in female rabbit reproductive organs: varying levels in relation to maturity and pregnancy. Lipids 30 507-511. (doi:10.1007/BF02537024)
126. Vanderwall DK, Woods GL, Weber JA & Lichtenwalner AB 1994 Corpus luteal function in nonpregnant mares following intrauterine administration of prostaglandin E(2) or estradiol-17beta. Theriogenology 42 1069-1083. (doi:10.1016/0093-691X(94)90855-9)
127. Walther A, Riehemann K & Gerke V 2000 A novel ligand of the formyl peptide receptor: annexin I regulates neutrophil extravasation by interacting with the FPR. Molecular Cell 5 831-840. (doi:10.1016/S1097-2765(00)80323-8)
128. Wang F, Riley JC & Behrman HR 1993 Immunosuppressive levels of glucocorticoid block extrauterine luteolysins in the rat. Biology of Reproduction 49 66-73. (doi:10.1095/biolreprod49.1.66)
129. Wang J, Huang Y, Zhou J & Liu X 2010 Effect of lipoxin A(4) on IL-1beta production of monocytes and its possible mechanism in severe preeclampsia. Journal of Huazhong University of Science and Technology. Medical Sciences 30 767-770. (doi:10.1007/s11596-010-0655-6)
130. 4. Pediatric Research 64 393-398. (doi:10.1203/PDR. 0b013e318180e4af)
131. Weng X, Luecke H, Song IS, Kang DS, Kim SH & Huber R 1993 Crystal structure of human annexin I at 2.5 A resolution. Protein Science 2 448-458. (doi:10.1002/pro.5560020317)
132. Yang Y, Hutchinson P & Morand EF 1999 Inhibitory effect of annexin I on synovial inflammation in rat adjuvant arthritis. Arthritis and Rheumatism 42 1538-1544. (doi:10.1002/1529-0131(199907)42:7〈1538::AID-ANR29〉3.0. CO;2-3)
133. Yoshimoto T & Takahashi Y 2002 Arachidonate 12-lipoxygenases. Prostaglandins & Other Lipid Mediators 68-69 245-262. (doi:10.1016/S0090- 6980(02)00034-5)
134. Yuan M, Jordan F, McInnes IB, Harnett MM & Norman JE 2009 Leukocytes are primed in peripheral blood for activation during term and preterm labour. Molecular Human Reproduction 15 713-724. (doi:10.1093/molehr/gap054)
135. Zhang Z, Huang L, Zhao W & Rigas B 2010 Annexin 1 induced by anti-inflammatory drugs binds to NF-kappaB and inhibits its activation: anticancer effects in vitro and in vivo. Cancer Research 70 2379-2388. (doi:10.1158/0008-5472.CAN-09-4204)