Lipoxin A 4 activates ALX/FPR2 receptor to regulate conjunctival goblet cell secretion

Mucosal Immunology

Volumn 10, Issue 1, 2017, Pages 46-57

  Hodges, R R ^a   Li, D ^a   Shatos, M A ^a   Bair, J A ^a   Lippestad, M ^a   Serhan, C N ^b   Dartt, D A ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; FORMYLPEPTIDE RECEPTOR; LIPOCORTIN 1; LIPOXIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUCIN; PHOSPHOLIPASE A2; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PROTEIN FPR2; PROTEIN KINASE C; UNCLASSIFIED DRUG; LIPOXIN; LIPOXIN A(4) RECEPTOR, RAT; LIPOXIN RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; CELLULAR SECRETION; CONJUNCTIVA; CONTROLLED STUDY; ENZYME ACTIVATION; GOBLET CELL; MALE; NONHUMAN; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ALLERGIC CONJUNCTIVITIS; ANIMAL; BODILY SECRETIONS; CALCIUM SIGNALING; CELL CULTURE; DRY EYE; HUMAN; IMMUNOLOGY; INFLAMMATION; LACRIMAL FLUID; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BODILY SECRETIONS; CALCIUM SIGNALING; CELLS, CULTURED; CONJUNCTIVA; CONJUNCTIVITIS, ALLERGIC; DRY EYE SYNDROMES; GOBLET CELLS; HUMANS; INFLAMMATION; LIPOXINS; MALE; MUCINS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, LIPOXIN; TEARS;

EID: 85011016201     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.33     Document Type: Article

References (44)

1. McGilligan, V.E. et al. Staphylococcus aureus activates the NLRP3 inflammasome in human and rat conjunctival goblet cells. PLoS One 8, e74010 (2013).
2. Contreras-Ruiz, L., Ghosh-Mitra, A., Shatos, M.A., Dartt, D.A. &Masli, S. Modulation of conjunctival goblet cell function by inflammatory cytokines. Mediators Inflamm. 2013, 636812 (2013).
3. Dartt, D.A. &Masli, S. Conjunctival epithelial and goblet cell function in chronic inflammation and ocular allergic inflammation. Curr. Opin. Allergy Clin. Immunol. 14, 464-470 (2014).
4. Leonardi, A., Motterle, L. &Bortolotti, M. Allergy and the eye. Clin. Exp. Immunol. 153 ((Suppl 1)), 17-21 (2008).
5. Serhan, C.N. Pro-resolving lipid mediators are leads for resolution physiology. Nature 510, 92-101 (2014).
6. Chiang, N., Arita, M. &Serhan, C.N. Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot. Essent. Fatty Acids 73, 163-177 (2005).
7. Li, D. et al. Resolvin D1 and aspirin-triggered resolvin D1 regulate histamine-stimulated conjunctival goblet cell secretion. Mucosal Immunol. 6, 1119-1130 (2013).
8. Dartt, D.A., Hodges, R.R., Li, D., Shatos, M.A., Lashkari, K. &Serhan, C.N. Conjunctival goblet cell secretion stimulated by leukotrienes is reduced by resolvins D1 and E1 to promote resolution of inflammation. J. Immunol. 186, 4455-4466 (2011).
9. Chiang, N., Takano, T., Arita, M., Watanabe, S. &Serhan, C.N. A novel rat lipoxin A4 receptor that is conserved in structure and function. B.r J. Pharmacol. 139, 89-98 (2003).
10. Motohashi, E. et al. Regulatory expression of lipoxin A4 receptor in physiologically estrus cycle and pathologically endometriosis. Biomed. Pharmacother. 59, 330-338 (2005).
11. Gronert, K., Maheshwari, N., Khan, N., Hassan, I.R., Dunn, M. &Laniado Schwartzman, M. A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense. J. Biol. Chem. 280, 15267-15278 (2005).
12. Gronert, K. Lipoxins in the eye and their role in wound healing. Prostaglandins Leukot. Essent. Fatty Acids 73, 221-229 (2005).
13. Cooray, S.N. et al. Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses. Proc. Natl. Acad. Sci. USA 110, 18232-18237 (2013).
14. Li, D., Carozza, R.B., Shatos, M.A., Hodges, R.R. &Dartt, D.A. Effect of histamine on Ca(2+)-dependent signaling pathways in rat conjunctival goblet cells. Invest. Ophthalmol. Vis. Sci. 53, 6928-6938 (2012).
15. Hayashi, D., Li, D., Hayashi, C., Shatos, M., Hodges, R.R. &Dartt, D.A. Role of histamine and its receptor subtypes in stimulation of conjunctival goblet cell secretion. Invest. Ophthalmol. Vis. Sci. 53, 2993-3003 (2012).
16. Clish, C.B., O'Brien, J.A., Gronert, K., Stahl, G.L., Petasis, N.A. &Serhan, C.N. Local and systemic delivery of a stable aspirin-triggered lipoxin prevents neutrophil recruitment in vivo. Proc. Natl. Acad. Sci. USA 96, 8247-8252 (1999).
17. Takano, T., Fiore, S., Maddox, J.F., Brady, H.R., Petasis, N.A. &Serhan, C.N. Aspirin-triggered 15-epi-lipoxin A4 (LXA4) and LXA4 stable analogues are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J. Exp. Med. 185, 1693-1704 (1997).
18. Chiang, N. et al. The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol. Rev. 58, 463-487 (2006).
19. Rios, J.D., Shatos, M.A., Urashima, H. &Dartt, D.A. Effect of OPC-12759 on EGF receptor activation, p44/p42 MAPK activity, and secretion in conjunctival goblet cells. Exp. Eye Res. 86, 629-636 (2008).
20. Hodges, R.R., Bair, J.A., Carozza, R.B., Li, D., Shatos, M.A. &Dartt, D.A. Signaling pathways used by EGF to stimulate conjunctival goblet cell secretion. Exp. Eye Res. 103, 99-113 (2012).
21. Hodges, R.R., Guilbert, E., Shatos, M.A., Natarajan, V. &Dartt, D.A. Phospholipase D1, but not D2, regulates protein secretion via Rho/ROCK in a Ras/Raf-independent, MEK-dependent manner in rat lacrimal gland. Invest. Ophthalmol. Vis. Sci. 52, 2199-2210 (2011).
22. Zoukhri, D. &Dartt, D.A. Cholinergic activation of phospholipase D in lacrimal gland acini is independent of protein kinase C and calcium. Am. J. Physiol. 268 (3 Pt 1), C713-C720 (1995).
23. Huster, M., Frei, E., Hofmann, F. &Wegener, J.W. A complex of Ca(V)1.2/ PKC is involved in muscarinic signaling in smooth muscle. FASEB J. 24, 2651-2659 (2010).
24. Chae, Y.C. et al. Inhibition of muscarinic receptor-linked phospholipase D activationby associationwithtubulin. J. Biol.Chem. 280, 3723-3730 (2005).
25. Horikawa, Y. et al. Activation of mitogen-activated protein kinase by cholinergic agonists and EGF in human compared with rat cultured conjunctivalgoblet cells. Invest.Ophthalmol.Vis.Sci. 44, 2535-2544 (2003).
26. Kanno, H. et al. Cholinergic agonists transactivate EGFR and stimulate MAPK to induce goblet cell secretion. Am. J. Physiol. Cell Physiol. 284, C988-C998 (2003).
27. Hund, T.J. &Mohler, P.J. Role of CaMKII in cardiac arrhythmias. Trends Cardiovasc. Med. 25, 392-397 (2014).
28. Scannell, M. &Maderna, P. Lipoxins and annexin-1: resolution of inflammation and regulation of phagocytosis of apoptotic cells. TheScientificWorldJournal 6, 1555-1573 (2006).
29. Migeotte, I., Communi, D. &Parmentier, M. Formyl peptide receptors: a promiscuous subfamily ofGprotein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 17, 501-519 (2006).
30. Romano, M.,Maddox, J.F. &Serhan, C.N. Activation of human monocytes and the acute monocytic leukemia cell line (THP-1) by lipoxins involves unique signaling pathways for lipoxin A4 versus lipoxin B4: evidence for differential Ca2+ mobilization. J. Immunol. 157, 2149-2154 (1996).
31. Maddox, J.F., Hachicha, M., Takano, T., Petasis, N.A., Fokin, V.V. &Serhan, C.N. Lipoxin A4 stable analogs are potent mimetics that stimulate human monocytes and THP-1 cells via a G-protein-linked lipoxin A4 receptor. J. Biol. Chem. 272, 6972-6978 (1997).
32. Nigam, S., Fiore, S., Luscinskas, F.W.and Serhan, C.N. Lipoxin A4 and lipoxin B4 stimulate the release but not the oxygenation of arachidonic acid in human neutrophils: dissociation between lipid remodeling and adhesion. J. Cell. Physiol. 143, 512-523 (1990).
33. Fiore, S., Romano, M., Reardon, E.M. &Serhan, C.N. Induction of functional lipoxin A4 receptors in HL-60 cells. Blood 81, 3395-3403 (1993).
34. Martin-Liberal, J., Cameron, A.J., Claus, J., Judson, I.R., Parker, P.J. &Linch, M. Targeting protein kinase C in sarcoma. Biochim. Biophys. Acta 1846, 547-559 (2014).
35. Aziz, M.H. et al. Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene 29, 3100-3109 (2010).
36. Shah, B.H &Catt, K.J. Calcium-independent activation of extracellularly regulated kinases 1 and 2 by angiotensin II in hepatic C9 cells: roles of protein kinase Cdelta, Src/proline-rich tyrosine kinase 2, and epidermal growth receptor trans-activation. Mol. Pharmacol. 61, 343-351 (2002).
37. Arnette, D. et al. Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic beta cells. J. Biol. Chem. 278, 32517-32525 (2003).
38. Li, D., Jiao, J., Shatos, M.A., Hodges, R.R. &Dartt, D.A. Effect of VIP on intracellular [Ca2+], extracellular regulated kinase 1/2, and secretion in cultured rat conjunctival goblet cells. Invest. Ophthalmol. Vis. Sci. 54, 2872-2884 (2013).
39. Gao, Y., Kyungi, M., Zhang, Y., Su, J., Greenwood, M. &Gronert, K. Female-specific downregulation of tissue polymorphonuclear neutrophils drives impaired regulatory T cell and amplified effector T cell responses in autoimmune dry eye disease. J. Immunol. 195, 3086-3099 (2015).
40. Maderna, P. et al. FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J. 24, 4240-4249 (2010).
41. Chiang, N., Fierro, I.M., Gronert, K. &Serhan, C.N. Activation of lipoxin A(4) receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J. Exp. Med. 191, 1197-1208 (2000).
42. Shatos, M.A.,Rios, J.D., Tepavcevic, V.,Kano,H., Hodges, R. &Dartt,D.A. Isolation, characterization, and propagation of rat conjunctival goblet cells in vitro. Invest. Ophthalmol. Vis. Sci. 42, 1455-1464 (2001).
43. Shatos, M.A. et al. Isolation and characterization of cultured human conjunctival goblet cells. Invest. Ophthalmol. Vis. Sci. 44, 2477-2486 (2003).
44. Shatos, M.A.,Gu, J., Hodges,R.R., Lashkari, K. and Dartt, D.A. ERK/p44p42 mitogen-activated protein kinase mediates EGF-stimulated proliferation of conjunctival goblet cells in culture. Invest. Ophthalmol. Vis. Sci. 49, 3351-3359 (2008).