Neuroprotectin D1 restores corneal nerve integrity and function after damage from experimental surgery

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 6, 2013, Pages 4109-4116

  Cortina, Maria Soledad ^a   He, Jiucheng ^b   Russ, Tiffany ^b   Bazan, Nicolas G ^b   Bazan, Haydee E P ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

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

Author keywords

Corneal sensitivity; Dry eye; Neuroprotectin D1; Neuroregeneration; Pigment epithelial derived factor

Indexed keywords

15 HYDROXYICOSATETRAENOIC ACID; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; DOCOSAHEXAENOIC ACID; LIPOXIN A; NEUROPROTECTIN D1; OMEGA 3 FATTY ACID; PIGMENT EPITHELIUM DERIVED FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN CORNEAL SHIELD; CONTROLLED STUDY; CORNEA INJURY; CORNEA SENSIBILITY; FLUORESCENCE MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; KERATECTOMY; LACRIMATION; LIMIT OF QUANTITATION; MALE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RABBIT; SCHIRMER TEST;

CORNEAL SENSITIVITY; DRY EYE; NEUROPROTECTIN D1; NEUROREGENERATION; PIGMENT EPITHELIAL-DERIVED FACTOR;

ANIMALS; AXONS; CALCITONIN GENE-RELATED PEPTIDE; CELLS, CULTURED; CORNEA; DOCOSAHEXAENOIC ACIDS; DRUG COMBINATIONS; EYE PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; MICE; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURITES; OPHTHALMIC NERVE; RABBITS; RATS; SERPINS; TEARS; TRIGEMINAL GANGLION; TUBULIN;

EID: 84878972340     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12075     Document Type: Article

References (44)

1. Muller LJ, Marfurt CF, Kruse F, Tervo TMT. Corneal nerves: structure, contents and function. Exp Eye Res. 2003;76:521-542.
2. He J, Bazan NG, Bazan HE. Mapping the entire human corneal nerve architecture. Exp Eye Res. 2010;91:513-523.
3. Patel DV, McGhee CN. Mapping of the normal human corneal sub-basal nerve plexus by in vivo laser scanning confocal microscopy. Invest Ophthalmol Vis Sci. 2005;46:4485-4488.
4. Rosenberg ME, Tervo TM, Immonen IJ, et al. Corneal structure and sensitivity in type 1 diabetes mellitus. Invest Ophthalmol Vis Sci. 2000;41:2915-2921.
5. Hovanesian JA, Shah SS, Maloney RK. Symptoms of dry eye and recurrent erosion syndrome after refractive surgery. J Cataract Refract Surg. 2001;27:577-584.
6. He J, Bazan HE. Mapping the nerve architecture of diabetic human corneas. Ophthalmology. 2012;119:956-964.
7. Lee BH, McLaren JW, Erie JC, et al. Reinnervation in the cornea after LASIK. Invest Ophthalmol Vis Sci. 2002;43:3660-3664.
8. Hamrah P, Cruzat A, Dastjerdi MH, et al. Corneal sensation and subbasal nerve alterations in patients with herpes simplex keratitis: an in vivo confocal microscopy study. Ophthalmology. 2010;117:1930-1936.
9. Rosenberg ME, Tervo TM, Müller LJ, Moilanen JA, Vesaluoma MH. In vivo confocal microscopy after herpes keratitis. Cornea. 2002;21:265-269.
10. Patel SV, Erie JC, McLaren JW, Bourne WM. Keratocyte density and recovery of subbasal nerves after penetrating keratoplasty and in late endothelial failure. Arch Ophthalmol. 2007;125: 1693-1698.
11. Chang-Ling T, Vannas A, Holden BA, O'Leary DJ. Incision depth affects the recovery of corneal sensitivity and neural regeneration in the cat. Invest Ophthalmol Vis Sci. 1990;31: 1533-1541.
12. Murphy CJ, Marfurt CF, McDermott A, et al. Spontaneous chronic corneal epithelial defects (SCCED) in dogs: clinical features, innervation, and effect of topical SP, with or without IGF-1. Invest Ophthalmol Vis Sci. 2001;42:2252-2261.
13. Bonfiglio V, Camillieri G, Avitabile T, et al. Effects of the COOHterminal tripeptide alpha-MSH(11-13) on corneal epithelial wound healing: role of nitric oxide. Exp Eye Res. 2006;83: 1366-1372.
14. Yamada N, Yanai R, Kawamoto K, et al. Promotion of corneal epithelial wound healing by a tetrapeptide (SSSR) derived from IGF-1. Invest Ophthalmol Vis Sci. 2006;47:3286-3292.
15. Chikamoto N, Chikama T, Yamada N, et al. Efficacy of substance P and insulin-like growth factor-1 peptides for preventing postsurgical superficial punctate keratopathy in diabetic patients. Jpn J Ophthalmol. 2009;53:464-469.
16. Bazan NG. Homeostatic regulation of photoreceptor cell integrity: significance of the potent mediator neuroprotectin D1 biosynthesized from docosahexaenoic acid: the Proctor lecture. Invest Ophthalmol Vis Sci. 2007;48:4866-4881.
17. Calandria JM, Marcheselli VL, Mukherjee PK, et al. Selective survival rescue in 15-lipoxygenase-1-deficient retinal pigment epithelial cells by the novel docosahexaenoic acid-derived mediator, neuroprotectin D1. J Biol Chem. 2009;284:17877-17882.
18. Bazan NG. Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci. 2006;29:263-271.
19. Tombran-Tink J, Barnstable CJ. PEDF: a multifaceted neurotrophic factor. Nat Rev Neurosci. 2003;4:628-636.
20. Mukherjee PK, Marcheselli VL, Barreiro S, et al. Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling. Proc Natl Acad Sci U S A. 2007;104:13152-13257.
21. Cortina MS, Bazan HE. Docosahexaenoic acid, protectins and dry eye. Curr Opin Clin Nutr Metab Care. 2011;14:132-137.
22. Cortina MS, He J, Li N, et al. Recovery of corneal sensitivity, calcitonin gene-related peptide-positive nerves, and increased wound healing induced by pigment epithelial-derived factor plus docosahexaenoic acid after experimental surgery. Arch Ophthalmol. 2012;130:76-83.
23. Esquenazi S, Bazan HE, Bui V, et al. Topical combination of NGF and DHA increases rabbit corneal nerve regeneration after photorefractive keratectomy. Invest Ophthalmol Vis Sci. 2005;46:3121-3127.
24. Linna TU, Vesaluoma MH, Pérez-Santonja JJ, et al. Effect of myopic LASIK on corneal sensitivity and morphology of subbasal nerves. Invest Ophthalmol Vis Sci. 2000;41:393-397.
25. Feiz V, Mannis MJ, Kandavel G, et al. Surface keratopathy after penetrating keratoplasty. Trans Am Ophthalmol Soc. 2001;99: 159-168.
26. Baker KS, Anderson SC, Romanowski EG, et al. Trigeminal ganglion neurons affect corneal epithelial phenotype. Influence on type VII collagen expression in vitro. Invest Ophthalmol Vis Sci. 1993;34:137-144.
27. Garcia-Hirschfeld J, Lopez-Briones LG, Belmonte C. Neurotrophic influences on corneal epithelial cells. Exp Eye Res. 1994;59:597-605.
28. Ueno H, Ferrari G, Hattori T, et al. Dependence of corneal stem/progenitor cells on ocular surface innervation. Invest Ophthalmol Vis Sci. 2012;53:867-872.
29. Yamada M, Ogata M, Kawai M, Mashima Y. Decreased substance P concentrations in tears from patients with corneal hypesthesia. Am J Ophthalmol. 2000;129:671-672.
30. Bazan NG, Molina MF, Gordon WC. Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annu Rev Nutr. 2011;31:321-351.
31. Belmonte C, Acosta CM, Gallar J. Neural basis of sensation in intact and injured corneas. Exp Eye Res. 2004;78:513-525.
32. Miljanović B, Trivedi KA, Dana MR, et al. Relation between dietary n-3 and n-6 fatty acids and clinically diagnosed dry eye syndrome in women. Am J Clin Nutr. 2005;82:887-893.
33. Brignole-Baudouin F, Baudouin C, Aragona P, et al. A multicentre, double-masked, randomized, controlled trial assessing the effect of oral supplementation of omega-3 and omega-6 fatty acids on a conjunctival inflammatory marker in dry eye patients. Acta Ophthalmol. 2011;89:e591-e597.
34. Erdinest N, Shmueli O, Grossman Y, et al. Anti-inflammatory effects of alpha linolenic acid on human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2012;53:4396-4406.
35. Kenchegowda S, He J, Bazan HE. Involvement of pigment epithelium-derived factor, docosahexaenoic acid and neuroprotectin D1 in corneal inflammation and nerve integrity after refractive surgery. Prostaglandins Leukot Essent Fatty Acids. 2013;88:27-31.
36. Cortina MS, He J, Li N, et al. Neuroprotectin D1 synthesis and corneal nerve regeneration after experimental surgery and treatment with PEDF plus DHA. Invest Ophthalmol Vis Sci. 2010;51:804-810.
37. Chan KY, Haschke RH. Isolation and culture of corneal cells and their interactions with dissociated trigeminal neurons. Exp Eye Res. 1982;35:137-156.
38. Emoto I, Beuerman RW. Stimulation of neurite growth by epithelial implants into corneal stroma. Neurosci Lett. 1987; 23:140-144.
39. Gronert K, Maheshwari N, Khan N, et al. A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense. J Biol Chem. 2005;280:15267-15278.
40. Calandria JM, Bazan NG. Neuroprotectin D1 modulates the induction of pro-inflammatory signaling and promotes retinal pigment epithelial cell survival during oxidative stress. Adv Exp Med Biol. 2010;664:663-670.
41. Bazan NG, Eady TN, Khoutorova L, et al. Novel aspirintriggered neuroprotectin D1 attenuates cerebral ischemic injury after experimental stroke. Exp Neurol. 2012;236:122-130.
42. Park CK, Lü N, Xu ZZ, et al. Resolving TRPV1- and TNF-amediated spinal cord synaptic plasticity and inflammatory pain with neuroprotectin D1. J Neurosci. 2011;31:15072-15085.
43. Li Z, Burns AR, Han L, et al. IL-17 and VEGF are necessary for efficient corneal nerve regeneration. Am J Pathol. 2011;178: 1106-1116.
44. Cruzat A, Witkin D, Baniasadi N, et al. Inflammation and the nervous system: the connection in the cornea in patients with infectious keratitis. Invest Ophthalmol Vis Sci. 2011;52:5136-5143.