Retinal pigment epithelium, age-related macular degeneration and neurotrophic keratouveitis

International Journal of Molecular Medicine

Volumn 31, Issue 1, 2013, Pages 232-242

  Bianchi, Enrica ^a   Scarinci, Fabio ^b   Ripandelli, Guido ^b   Feher, Janos ^a   Pacella, Elena ^a   Magliulo, Giuseppe ^a   Gabrieli, Corrado Balacco ^a   Plateroti, Rocco ^a   Plateroti, Pasquale ^a   Mignini, Fiorenzo ^c   Artico, Marco ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE BIETTI   (Italy)

^c UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Age related macular degeneration; Electron microscopy; Light microscopy; Lipofuscin; Mitochondria; Morphometry; Peroxisomes; Pigment epithelium derived factor; Retinal pigment epithelium

Indexed keywords

CAPSAICIN; PIGMENT EPITHELIUM DERIVED FACTOR;

ADOLESCENT; ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL VACUOLE; CHILD; CLINICAL FEATURE; CONTROLLED STUDY; CONVALESCENCE; CORNEA OPACITY; CORNEA ULCER; ELECTRON MICROSCOPY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LACRIMATION; LEUKOCYTE; MALE; MICROSCOPY; MITOCHONDRION; MORPHOMETRICS; NEUROTROPHIC KERATOUVEITIS; NONHUMAN; PEROXISOME; PIGMENT EPITHELIUM; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RETINA MACULA AGE RELATED DEGENERATION; SCAR FORMATION; SCHOOL CHILD; UVEITIS; VITREORETINOPATHY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; CAPSAICIN; CHILD; CHILD, PRESCHOOL; EYE PROTEINS; FEMALE; HUMANS; MACULAR DEGENERATION; MALE; MICROSCOPY, ELECTRON; MIDDLE AGED; MITOCHONDRIA; NERVE GROWTH FACTORS; PIGMENT EPITHELIUM OF EYE; RATS; RATS, SPRAGUE-DAWLEY; RETINAL PIGMENT EPITHELIUM; SERPINS; TEARS; UVEITIS; YOUNG ADULT;

EID: 84873130704     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2012.1164     Document Type: Article

References (103)

1. Friedman DS, O'Colmain BJ, Munoz B, Tomany SC, McCarty C, de Jong PT, Nemesure B, Mitchell P and Kempen J: Eye Diseases Prevalence Research Group. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 122: 564-572, 2004.
2. Klaver CC, Wolfs RC, Vingerling JR, Ofman A and De Jong PT: Age specific prevalence and causes of blindness and visual impairment in an older population: the Rotterdam Study. Arch Ophthalmol 116: 653-658, 1998.
3. Fine SL, Berger JW, Maguire MG and Ho AC: Age-related macular degeneration. N Engl J Med 342: 483-492, 2000.
4. McConnell V and Silvestri G: Age-related macular degeneration. Ulster Med J 74: 82-92, 2005.
5. Nowak JZ: Role of lipofuscin in pathogenesis of age-related macular degeneration (AMD). Mag Okul 2: 103-114, 2005 (In Polish).
6. Nowak JZ: Drusen, basal deposits, inflammation and age-related macular degeneration (AMD). Mag Okul 2: 174-186, 2005 (In Polish).
7. Bird AC, Bressler NM, Bressler SB, Chisholm IH, Coscas G, Davis MD, de Jong PT, Klaver CC, Klein BE, Klein R, et al: An international classification and grading system for age-related maculopathy and age-related macular degeneration. The International ARM Epidemiological Study Group. Surv Ophthalmol 39: 367-374, 1995.
8. Anderson DH, Mullins RF, Hageman GS and Johnson LV: A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol 134: 411-431, 2002.
9. Campochiaro PA: Ocular neovascularization and excessive vascular permeability. Expert Opin Biol Ther 4: 1395-1402, 2004.
10. Kijlstra A, La Heij EC and Hendrikse F: Immunological factors in the pathogenesis and treatment of age-related macular degeneration. Ocular Immunol Inflam 13: 3-11, 2005.
11. Klein R, Peto T, Bird A and Vannewkirk MR: The epidemiology of age-related macular degeneration. Am J Ophthalmol 137: 486-495, 2004.
12. Sparrow JR and Boulton M: RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 80: 595-606, 2005.
13. Wiktorowska-Owczarek A and Nowak JZ: Oxidative damage in age-related macular degeneration (AMD) and antioxidant protection as a therapeutic strategy. Pol J Environ Stud 15: 69-72, 2006.
14. Beatty S, Koh H, Phil M, Henson D and Boulton M: The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45: 115-134, 2000.
15. Dunaief JL, Dentchev T, Ying GS and Milam AH: The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 120: 1435-1442, 2002.
16. Winkler BS, Boulton ME, Gottsch JD and Sternberg P: Oxidative damage and age-related macular degeneration. Mol Vis 5: 32, 1999.
17. Hollyfield JG, Salomon RG and Crabb JW: Proteomic approaches to understanding age-related macular degeneration. Adv Exp Med Biol 533: 83-89, 2003.
18. Jin GF, Hurst JS and Godley BF: Rod outer segments mediate mitochondrial DNA damage and apoptosis in human retinal pigment epithelium. Curr Eye Res 23: 11-19, 2001.
19. Wolf G: Lipofuscin and macular degeneration. Nutr Rev 61: 342-346, 2003.
20. Shamsi FA and Boulton M: Inhibition of the RPE lysosomal and antioxidant activity by the age pigment lipofuscin. Invest Ophthalmol Vis Sci 42: 3041-3046, 2001.
21. Sundelin S, Wihlmark U, Nilsson SE and Brunk UT: Lipofuscin accumulation in cultured retinal pigment epithelial cells reduces their phagocytic capacity. Curr Eye Res 17: 851-857, 1998.
22. Rakoczy PE, Zhang D, Robertson T, Barnett NL, Papadimitriou J, Constable IJ and Lai CM: Progressive age-related changes similar to age-related macular degeneration in a transgenic mouse model. Am J Pathol 161: 1515-1524, 2002.
23. Shaban H, Borras C, Vina J and Richter C: Phosphatidylglycerol potently protects human retinal pigment epithelial cells against apoptosis induced by A2E, a compound suspected to cause age-related macula degeneration. Exp Eye Res 75: 99-108, 2002.
24. Suter M, Remé C, Grimm C, Wenzel A, Jaattela M, Esser P, Kociok N, Leist M and Richter C: Age-related macular degeneration. The lipofusion component N-retinyl-N-retinylidene ethanolamine detaches proapoptotic proteins from mitochondria and induces apoptosis in mammalian retinal pigment epithelial cells. J Biol Chem 275: 39625-39630, 2000.
25. Kroemer G and Reed JC: Mitochondrial control of cell death. Nat Med 6: 513-519, 2000.
26. Schon EA and Manfredi G: Neuronal degeneration and mitochondrial dysfunction. J Clin Invest 111: 303-312, 2003.
27. James AM and Murphy MP: How mitochondrial damage affects cell function. J Biomed Sci 9: 475-487, 2002.
28. Toescu EC, Myronova N and Verkhratsky A: Age-related structural and functional changes of brain mitochondria. Cell Calcium 28: 329-338, 2000.
29. Paradies G, Ruggiero FM, Petrosillo G and Quagliariello E: Age-dependent decline in the cytochrome c oxidase activity in rat heart mitochondria: role of cardiolipin. FEBS Lett 406: 136-138, 1997.
30. Crompton M: Mitochondria and aging: a role for the permeability transition. Aging Cell 3: 3-6, 2004.
31. Gabbita SP, Subramaniam R, Allouch F, Carney JM and Butterfield DA: Effects of mitochondrial respiratory stimulation on membrane lipids and proteins: an electron paramagnetic resonance investigation. Biochim Biophys Acta 1372: 163-173, 1998.
32. Rottenberg H and Wu S: Mitochondrial dysfunction in lymphocytes from old mice: enhanced activation of the permeability transition. Biochem Biophys Res Commun 240: 68-74, 1997.
33. Sugrue MM and Tatton WG: Mitochondrial membrane potential in aging cells. Biol Signals Recept 10: 176-188, 2001.
34. Battelli D, Bellei M, Arrigoni-Martelli E, Muscatello U and Bobyleva V: Interaction of carnitine with mitochondrial cardiolipin. Biochim Biophys Acta 1117: 33-36, 1992.
35. Zammit VA, Corstorphine CG, Kolodziej MP and Fraser F: Lipid molecular order in liver mitochondrial outer membranes, and sensitivity of carnitine palmitoyltransferase I to malonyl-CoA. Lipids 33: 371-376, 1998.
36. Beaumont K, Skowronski R, Vaughn DA and Fanestil DD: Interactions of lipids with peripheral-type benzodiazepine receptors. Biochem Pharmacol 37: 1009-1014, 1988.
37. Campbell AM, Capuano A and Chan SH: A cholesterol-binding and transporting protein from rat liver mitochondria. Biochim Biophys Acta 1567: 123-132, 2002.
38. Hansson M, Ellis E, Hunt MC, Schmitz G and Babiker A: Marked induction of sterol 27-hydroxylase activity and mRNA levels during differentiation of human cultured monocytes into macrophages. Biochim Biophys Acta 1593: 283-289, 2003.
39. Papadopoulos V: Peripheral benzodiazepine receptor: structure and function in health and disease. Ann Pharm Fr 61: 30-50, 2003.
40. Denton RM, Randle PJ, Bridges BJ, Cooper RH, Kerbey AL, Pask HT, Severson DL, Stansbie D and Whitehouse S: Regulation of mammalian pyruvate dehydrogenase. Mol Cell Biochem 9: 27-53, 1975.
41. Robison WG Jr and Kuwabara T: Microperoxisomes in the retinal pigment epithelium. Invest Ophthalmol 14: 866-872, 1975.
42. Szabo II, Adams C and Gulbins E: Ion channels and membrane rafts in apoptosis. Pflugers Arch 448: 304-312, 2004.
43. Beuerman RW and Stern ME: Neurogenic inflammation: a first line of defense for the ocular surface. Ocul Surf 3 (Suppl 4): S203-S206, 2005.
44. Troger J, Kieselbach G, Teuchner B, Kralinger M, Nguyen QA, Haas G, Yayan J, Gottinger W and Schmid E: Peptidergic nerves in the eye, their source and potential pathophysiological relevance. Brain Res Rev 53: 39-62, 2007.
45. Stern ME, Gao J, Siemasko KF, Beuerman RW and Pflugfelder SC: The role of the lacrimal functional unit in the pathophysiology of dry eye. Exp Eye Res 78: 409-416, 2004.
46. Kovacs I, Ludany A, Koszegi T, Fehér J, Kovacs B, Szolcsanyi J and Pintér E: Substance P released from sensory nerve endings influences tear secretion and goblet cell function in the rat. Neuropeptides 39: 395-402, 2005.
47. Feher J: Contribution of neurogenic inflammation to irritable eye syndrome. Adv Exp Med Biol 506: 1047-1050, 2002.
48. Baudouin C: A new approach for better comprehension of diseases of the ocular surface. J Fr Ophtalmol 30: 239-246, 2007 (In French).
49. Brecha NC, Sternini C, Anderson K and Krause JE: Expression and cellular localization of substance P/neurokinin A and neurokinin B mRNAs in the rat retina. Vis Neurosci 3: 527-535, 1989.
50. Caruso DM, Owczarzak MT and Pourcho RG: Colocalization of substance P and GABA in retinal ganglion cells: a computer-assisted visualization. Vis Neurosci 5: 389-394, 1990.
51. Bagnoli P, Dal Monte M and Casini G: Expression of neuropeptides and their receptors in the developing retina of mammals. Histol Histopathol 18: 1219-1242, 2003.
52. May A, Shepheard SL, Knorr M, Effert R, Wessing A, Hargreaves RJ, Goadsby PJ and Diener HC: Retinal plasma extravasation in animals but not in humans: implications for the pathophysiology of migraine. Brain 121: 1231-1237, 1998.
53. Gaspar MN, Ribeiro CA, Cunha-Vaz JG and Macedo TR: Effects of neuropeptides on the sumatriptan-disturbed circulation in the optic nerve head of rabbits. Pharmacology 70: 152-159, 2004.
54. Nucci C, Gasperi V, Tartaglione R, Cerulli A, Terrinoni A, Bari M, De Simone C, Agrò AF, Morrone LA, Corasaniti MT, Bagetta G and Maccarrone M: Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats. Invest Ophthalmol Vis Sci 48: 2997-3004, 2007.
55. Bronzetti E, Artico M, Kovacs I, Felici LM, Magliulo G, Vignone D, D'Ambrosio A, Forte F, Di Liddo R and Feher J: Expression of neurotransmitters and neurotrophins in neurogenic inflammation of the rat retina. Eur J Histochem 51: 251-260, 2007.
56. Szolcsanyi J: Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptide 38: 377-384, 2004.
57. Fujita S, Shimizu T, Izumi K, Fukuda T, Sameshima M and Ohba N: Capsaicin-induced neuroparalytic keratitis-like corneal changes in the mouse. Exp Eye Res 38: 165-175, 1984.
58. Ogilvy CS, Silverberg KR and Borges LF: Sprouting of corneal sensory fibers in rats treated at birth with capsaicin. Invest Ophthalmol Vis Sci 32: 112-121, 1991.
59. Gallar J, Pozo MA, Rebollo I and Belmonte C: Effects of capsaicin on corneal wound healing. Invest Ophthalmol Vis Sci 31: 1968-1974, 1990.
60. Waldrep JC and Crosson CE: Induction of keratouveitis by capsaicin. Curr Eye Res 7: 1173-1182, 1988.
61. Ritter S and Dinh TT: Capsaicin-induced neuronal degeneration in the brain and retina of preweanling rats. J Comp Neurol 296: 447-461, 1990.
62. Tombran-Tink J, Shivaram SM, Chader GJ, Johnson LV and Bok D: Expression, secretion, and age-related downregulation of pigment epithelium-derived factor, a serpin with neurotrophic activity. J Neurosci 15: 4992-5003, 1995.
63. Becerra SP, Palmer I, Kumar A, Steele F, Shiloach J, Notario V and Chader GJ: Overexpression of fetal human pigment epithelium-derived factor in Escherichia coli: a functionally active neurotrophic factor. J Biol Chem 268: 23148-23156, 1993.
64. Dawson DW, Volpert OV, Gillis P, Crawford SE, Xu H, Benedict W and Bouck NP: Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285: 245-258, 1999.
65. Chung C, Doll JA, Stellmach VM, Gonzales J, Surapureddi S, Cornwell M, Reddy JK and Crawford SE: Pigment epithelium-derived factor is an angiogenesis and lipid regulator that activates peroxisome proliferator-activated receptor alpha. Adv Exp Med Biol 617: 591-597, 2008.
66. Bouck N: PEDF: anti-angiogenic guardian of ocular function. Trends Mol Med 8: 330-334, 2002.
67. Spranger J, Osterhoff M, Reimann M, Mohlig M, Ristow M, Francis MK, Cristofalo V, Hammes HP, Shith G, Boulton M and Pfeiffer AF: Loss of the antiangiogenic pigment epithelium-derived factor in patients with angiogenic eye disease. Diabetes 50: 2641-2645, 2001.
68. Zingsheim HP and Plattner H: Electron microscopic methods in membrane biology. In: Methods in Membrane Biology. Korn ED (ed). Plenum Press, New York, NY, pp1-146, 1976.
69. Hirai K, Aliev G, Nunomura A, Fujioka H, Russell RL, Atwood CS, Johnson AB, Kress Y, Vinters HV, Tabaton M, Shimohama S, Cash AD, Siedlak SL, Harris PL, Jones PK, Petersen RB, Perry G and Smith MA: Mitochondrial abnormalities in Alzheimer's disease. J Neurosci 21: 3017-3023, 2001.
70. Kelley DE, He J, Menshikova EV and Ritov VB: Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
71. Gosker HR, Wouters EFM, van der Vusse GJ and Schols AMWJ: Skeletal muscle dysfunction in chronic obstructive pulmonary disease and chronic heart failure: underlying mechanisms and therapy perspectives. Am J Clin Nutr 71: 1033-1047, 2000.
72. Ben-Shachar D: Mitochondrial dysfunction in schizophrenia: a possible linkage to dopamine. J Neurochem 83: 1241-1251, 2002.
73. Fox DA, Poblenz AT, He L, Harris JB and Medrano CJ: Pharmacological strategies to block rod photoreceptor apoptosis caused by calcium overload: a mechanistic target-site approach to neuroprotection. Eur J Ophthalmol 13 (Suppl 3): S44-S56, 2003.
74. Tyni T, Johnson M, Eaton S, Pourfarzam M, Andrews R and Turnbull DM: Mitochondrial fatty acid beta-oxidation in the retinal pigment epithelium. Pediatr Res 52: 595-600, 2002.
75. Andrews RM, Griffiths PG, Johnson MA and Turnbull DM: Histochemical localisation of mitochondrial enzyme activity in human optic nerve and retina. Br J Ophthalmol 83: 231-235, 1999.
76. Hiltunen JK and Qin Y: Beta-oxidation-strategies for the metabolism of a wide variety of acyl-CoA esters. Biochem Biophys Acta 1484: 117-128, 2000.
77. Kuksa V, Imanishi Y, Batten M, Palczewski K and Moise AR: Retinoid cycle in the vertebrate retina: experimental approaches and mechanisms of isomerization. Vision Res 43: 2959-2981, 2003.
78. Sparrow JR, Fishkin N, Zhou J, Cai B, Jang YP, Krane S, Itagaki Y and Nakanishi K: A2E, a byproduct of the visual cycle. Vision Res 43: 2983-2990, 2003.
79. Sprecher H: Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486: 219-231, 2000.
80. Hettema EH and Tabak HF: Transport of fatty acids and metabolites across the peroxisomal membrane. Biochim Biophys Acta 1486: 18-27, 2000.
81. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Wilson TM, Lenhard JM and Lehmann JM: Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc Natl Acad Sci USA 94: 4318-4323, 1997.
82. Kersten S, Desvergne B and Wahli W: Roles of PPARs in health and disease. Nature 405: 421-424, 2000.
83. Nagy L, Tontonoz P, Alvarez JGA, Chen H and Evans RM: Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 93: 229-240, 1998.
84. Murata T, He S, Hangai M, Ishibashi T, Xi XP, Kim S, Hsueh WA, Ryan SJ, Law RE and Hinton DR: Peroxisome proliferator-activated receptor-gamma ligands inhibit choroidal neovascularization. Invest Ophthalmol Vis Sci 41: 2309-2317, 2000.
85. Forman BM, Chen J and Evans RM: Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci USA 94: 4312-4317, 1997.
86. Keller H, Dreyer C, Medin J, Mahfoudi A, Ozato K and Wahli W: Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. Proc Natl Acad Sci USA 90: 2160-2164, 1993.
87. Brunk UT and Terman A: The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur J Biochem 269: 1996-2002, 2002.
88. Katz ML, Rice LM and Gao CL: Reversible accumulation of lipofuscin-like inclusions in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 40: 175-181, 1999.
89. Von Ruckmann A, Schmidt KG, Fitzke FW, Bird AC and Jacobi KW: Dynamics of accumulation and degradation of lipofuscin in retinal pigment epithelium in senile macular degeneration. Klin Monbl Augenheilkd 213: 32-37, 1998 (In German).
90. Kennedy CJ, Rakoczy PE and Constable IJ: Lipofuscin of the retinal pigment epithelium: a review. Eye (Lond) 9: 763-771, 1995.
91. Marmorstein AD, Marmorstein LY, Sakaguchi H and Hollyfield JG: Spectral profiling of autofluorescence associated with lipofuscin, Bruch's membrane, and sub-RPE deposits in normal and AMD eyes. Invest Ophthalmol Vis Sci 43: 2435-2441, 2002.
92. Feher J, Kovacs I, Artico M, Cavallotti C, Papale A and Balacco Gabrieli C: Mitochondrial aterations of retinal pigment epithelium in age-related macular degeneration. Neurobiol Aging 27: 983-993, 2006.
93. Furuno T, Kanno T, Arita K, Asami M, Utsumi T, Doi Y, Inoue M and Utsumi K: Roles of long chain fatty acids and carnitine in mitochondrial membrane permeability transition. Biochem Pharmacol 62: 1037-1046, 2001.
94. Pepe S: Mitochondrial function in ischaemia and reperfusion of the ageing heart. Clin Exp Pharmacol Physiol 27: 745-750, 2000.
95. Gunthorpe MJ and Szallasi A: Peripheral TRPV1 receptors as targets for drug development: new molecules and mechanisms. Curr Pharm Des 14: 32-41, 2008.
96. Lázár J, Szabó T, Marincsák R, Kovács L, Blumberg PM and Bíró T: Sensitization of recombinant vanilloid receptor-1 by various neurotrophic factors. Life Sci 75: 153-163, 2004.
97. Aloe L, Tirassa P and Lambiase A: The topical application of nerve growth factor as a pharmacological tool for human corneal and skin ulcers. Pharmacol Res 57: 253-258, 2008.
98. Feher J, Kovacs I, Pacella E, Keresz S, Spagnardi N and Balacco Gabrieli C: Pigment epithelium-derived factor (PEDF) attenuated capsaicin-induced neurotrophic keratouveitis. Invest Ophthalmol Vis Sci 50: 5173-5180, 2009.
99. Gao G, Li Y, Zhang D, Gee S, Crosson C and Ma J: Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett 489: 270-276, 2001.
100. Jin KL, Mao XO and Greenberg DA: Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97: 10242-10247, 2000.
101. Zachary I: Neuroprotective role of vascular endothelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14: 207-221, 2005.
102. Khaibullina AA, Rosenstein JM and Krum JM: Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures. Brain Res Dev Brain Res 148: 59-68, 2004.
103. Feher J, Papale A, Mannino G, Gualdi G and Balacco Gabrieli C: Mitotropic compounds for the treatment of age-related macular degeneration. The metabolic approach and a pilot study. Ophthalmologica 217: 351-357, 2003.