EGF stimulates lipoxin A4 synthesis and modulates repair in corneal epithelial cells through ERK and p38 activation

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 5, 2011, Pages 2240-2249

  Kenchegowda, Sachidananda ^a   Bazan, Nicolas G ^a   Bazan, Haydee E P ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; EPIDERMAL GROWTH FACTOR; LIPOXIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA CELL; CORNEA EPITHELIUM; ENZYME ACTIVATION; ENZYME INHIBITION; FATTY ACID SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RABBIT; SIGNAL TRANSDUCTION; WOUND CLOSURE; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; CAFFEIC ACIDS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; EPITHELIUM, CORNEAL; LIPOXINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; ORGAN CULTURE TECHNIQUES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RABBITS; TANDEM MASS SPECTROMETRY; WOUND HEALING;

EID: 79956027719     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6199     Document Type: Article

References (55)

1. Streilein JW. Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat Rev Immunol. 2003;3:879-889.
2. Bazan HEP, Ottino P. The role of platelet-activating factor in the corneal response to injury. Prog Retin Eye Res. 2002;21:449-464.
3. Bazan HEP. Cellular and molecular events in corneal wound healing: significance of lipid signaling. Exp Eye Res. 2005;80:453-463.
4. Kenchegowda S, Bazan HEP. Significance of lipid mediators in corneal injury and repair. J Lipid Res. 2010;51:879-891.
5. Bazan HEP, Birkle D, Beuerman RW, Bazan NG. Inflammationinduced stimulation of the synthesis of prostaglandins and lipoxygenase-reaction products in rabbit cornea. Curr Eye Res. 1985;4: 175-179.
6. Bazan HEP, Birkle DL, Beuerman RW, Bazan NG. Cryogenic lesion alters the metabolism of arachidonic acid in rabbit cornea layers. Invest Ophthalmol Vis Sci. 1985;26:474-480.
7. Bazan HEP. Corneal injury alters eicosanoid formation in the rabbit anterior segment in vivo. Invest Ophthalmol Vis Sci. 1987;28:314-319.
8. Brash AR. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem. 1999;274:23679-23682.
9. Bryant RW, Schewe T, Rapoport M, Bailey JM. Leukotriene formation by a purified reticulocyte lipoxygenase enzyme. Conversion of arachidonic acid and 15-hydroperoxy-eicosatetraenoic acid to 14,15-leukotriene A4. J Biol Chem. 1985;260:3548-3555.
10. Papayianni A, Serhan CN, Phillips ML, Rennke HG, Brady HR. Transcellular biosynthesis of lipoxin A4 during adhesion of platelets and neutrophils in experimental immune complex glomerulonephritis. Kidney Int. 1995;47:1295-12302.
11. Nigam S, Patabhiraman S, Ciccoli R, et al. The rat leukocyte-type 12-lipoxygenase exhibits an intrinsic hepoxilin A3 synthase activity. J Biol Chem. 2004;279:29023-29030.
12. Hurst JS, Balazy M, Bazan HEP, Bazan NG. The epithelium, endothelium, and stroma of the rabbit cornea generate (12S)-hydroxyl eicosatetraenoic acid as the main lipoxygenase metabolite in response to injury. J Biol Chem. 1991;266:6726-6730.
13. Liminga M, Fagrholm P, Oliw EH. Lipoxygenases in corneal epithelia of man and cynomolgus monkey. Exp Eye Res. 1994;59:313-321.
14. Gronert K, Maheshwari N, Khan N, Hassan IR, 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. 2005;280:15267-15278.
15. Guptha AG, Hirakata A, Proia AD. Effect of inhibitors of arachidonic acid metabolism on corneal reepithelialization in the rat. Exp Eye Res. 1993;56:701-708.
16. 1 activation. Biochem Pharmacol. 2008;76:654-661.
17. McMahon B, Mitchell S, Brady HR, Godson C. Lipoxins: revelations on resolution. Trends Pharmacol Sci. 2001;22:391-395.
18. Ariel A, Chiang N, Arita M, Petasis NA, Serhan CN. Aspirin-triggered lipoxin A4 and B4 analogs block extracellular signal-regulated kinase-dependent TNF-alpha secretion from human T cells. J Immunol. 2003;170:6266-6272.
19. Sheardown H, Cheng YL. Tear EGF concentration following corneal epithelial wound creation. J Ocul Pharmacol Ther. 1996;12: 239-243.
20. Wilson SE, Liang Q, Kim WJ. Lacrimal gland HGF, KGF, and EGF mRNA levels increase after corneal epithelial wounding. Invest Ophthalmol Vis Sci. 1999;40:2185-2190.
21. Wilson SE, Chen L, Mohan RR, Liang Q, Liu J. Expression of HGF, KGF, EGF and receptor messenger RNAs following corneal epithelial wounding. Exp Eye Res. 1999;68:377-397.
22. Kang SS, Li T, Xu D, Reinach PS, Lu L. Inhibitory effect of PGE2 on EGF-induced MAP kinase activity and rabbit corneal epithelial proliferation. Invest Ophthalmol Vis Sci. 2000;41:2164-2169.
23. Hill CS, Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell. 1995;80:199-211.
24. Sharma GD, He J, Bazan HE. p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades. J Biol Chem. 2003;278:21989-21997.
25. Wang Z, Yang H, Tachado SD, et al. Phosphatase-mediated crosstalk control of ERK and p38 MAPK signaling in corneal epithelial cells. Invest Ophthalmol Vis Sci. 2006;47:5267-5275.
26. Ottino P, Taheri F, Bazan HEP. Growth factor-induced proliferation in corneal epithelial cells is mediated by 12(S)-HETE. Exp Eye Res. 2003;76:613-622.
27. Sharma GD, Ottino P, Bazan HEP. Epidermal and hepatocyte growth factors, but not keratinocyte growth factor, modulate protein kinase C alpha translocation to the plasma membrane through 15(S)-hydroxyeicosatetraenoic acid synthesis. J Biol Chem. 2005;280:7917-7924.
28. Hurst J, Ma X, Bazan HEP. PAF binding to a single receptor in corneal epithelium plasma membrane. Invest Ophthalmol Vis Sci. 1999;40:790-795.
29. He J, Bazan HEP. Epidermal Growth Factor Synergism with TGF-1ß via PI-3 kinase activity in corneal keratocyte differentiation. Invest Ophthalmol Vis Sci. 2008;49:2936-2945.
30. Xu KP, Yu FS. Cross talk between c-Met and epidermal growth factor receptor during retinal pigment epithelial wound healing. Invest Ophthalmol Vis Sci. 2007;48:2242-2248.
31. Chandrasekher G, Kakazu AH, Bazan HE. HGF-and KGF-induced activation of PI-3K/p70 s6 kinase pathway in corneal epithelial cells: its relevance in wound healing. Exp Eye Res. 2001;73:191-202.
32. Winston BW, Chan ED, Johnson GL, Riches DW. Activation of p38mapk, MKK3, and MKK4 by TNF-alpha in mouse bone marrow-derived macrophages. J Immunol. 1997;159:4491-4497.
33. Fiore S, Serhan CN. Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factorprimed neutrophils. J Exp Med. 1990;172:1451-1457.
34. Devchand PR, Arita M, Hong S, et al. Human ALX receptor regulates neutrophil recruitment in transgenic mice: roles in inflammation and host defense. FASEB J. 2003;17:652-659.
35. Zieske JD, Takahashi H, Hutcheon AE. Dalbone AC. Activation of epidermal growth factor receptor during corneal epithelial migration. Invest Ophthalmol Vis Sci. 2000;41:1346-1355.
36. Schultz G, Khaw PT, Oxford K, MaCauley S, Van Setten G, Chegini N. Growth factors and ocular wound healing. Eye. 1994;8:184-187.
37. Wilson SE, He YG, Weng J, Zieske JD, Jester JV, Schultz GS. Effect of epidermal growth factor, hepatocyte growth factor, and keratinocyte growth factor, on proliferation, motility and differentiation of human corneal epithelial cells. Exp Eye Res. 1994;59:665-678.
38. Kitazawa T, Kinoshita S, Fujita K, et al. The mechanism of accelerated corneal epithelial healing by human epidermal growth factor. Invest Ophthalmol Vis Sci. 1990;31:1773-1778.
39. Islam M, Akhtar RA. Epidermal growth factor stimulates phospholipase cgamma1 in cultured rabbit corneal epithelial cells. Exp Eye Res. 2000;70:261-269.
40. Kang SS, Li T, Xu D, Reinach PS, Lu L. Inhibitory effect of PGE2 on EGF induced MAP kinase activity and rabbit corneal epithelial proliferation. Invest Ophthalmol Vis. Sci. 41:2164-2169, 2000.
41. Mazie AR, Spix JK, Block ER, Achebe HB, Klarlund JK. Epithelial cell motility is triggered by activation of the EGF receptor through phosphatidic acid signaling. J Cell Sci. 2006;119:1645-1654.
42. Wang Z, Yang H, Zhang F, Pan Z, Capo-Aponte J, Einach, PS. Dependence of EGF-induced increases in corneal epithelial proliferation and migration on GSK-3 inactivation. Invest Ophthalmol Vis Sci. 2009;50:4828-4835.
43. Yin J, Yu FS. ERK1/2 mediate wounding-and G-protein-coupled receptor ligands-induced EGFR activation via regulating ADAM17 and HB-EGF shedding. Invest Ophthalmol Vis Sci. 2009;50:132-139.
44. Block ER, Klarlund JK. Wounding sheets of epithelial cells activates the epidermal growth factor receptor through distinct shortand long-range mechanisms. Mol Biol Cell. 2008;19:4909-4917.
45. Lyu J, Lee KS, Joo CK. Transactivation of EGFR mediates insulinstimulated ERK1/2 activation and enhanced cell migration in human corneal epithelial cells. Mol Vis. 2006;12:1403-1410.
46. Xu KP, Yin J, Yu FS. Lysophosphatidic acid promoting corneal epithelial wound healing by transactivation of epidermal growth factor receptor. Invest Ophthalmol Vis Sci. 2007;48:636-643.
47. Yang H, Wang Z, Capó-Aponte JE, Zhang F, Pan Z, Reinach PS. Epidermal growth factor receptor transactivation by the cannabinoid receptor (CB1) and transient receptor potential vanilloid 1 (TRPV1) induces differential responses in corneal epithelial cells. Exp Eye Res. 2010;91:462-471.
48. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 1995;27:179-185.
49. Meloche S, Seuwen K, Pagès G, Pouysségur J. Biphasic and synergistic activation of p44mapk (ERK1) by growth factors: correlation between late phase activation and mitogenicity. Mol Endocrinol. 1992;6:845-854.
50. Leedom AJ, Sullivan AB, Dong B, Lau D, Gronert K. Endogenous LXA4 circuits are determinants of pathological angiogenesis in response to chronic injury. Am J Pathol. 2010;176:74-84.
51. Takahashi Y, Glasgow WC, Suzuki H, et al. Investigation of the oxygenation of phospholipids by the porcine leukocyte and human platelet arachidonate 12-lipoxygenases. Eur J Biochem. 1993; 218:165-171.
52. Li Z, Burns AR, Rumbaut RE, Smith CW. γδT cells are necessary for platelet and neutrophil accumulation in limbal vessels and efficient epithelial repair after corneal abrasion. Am J Pathol. 2007;171: 838-845.
53. Serhan CN. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol. 2007;25:101-137.
54. Bazan HE, Tao Y, DeCoster MA, Bazan NG. Platelet-activating factor induces cyclooxygenase-2 gene expression in corneal epithelium. Requirement of calcium in the signal transduction pathway. Invest Ophthalmol Vis Sci. 1997;38:2492-2501.
55. Chandrasekher G, Ma X, Lallier TE, Bazan HE. Delay of corneal epithelial wound healing and induction of keratocyte apoptosis by platelet-activating factor. Invest Ophthalmol Vis Sci. 2002;43: 1422-1428.