The 5HT 1a receptor agonist 8-OH DPAT induces protection from lipofuscin accumulation and oxidative stress in the retinal pigment epithelium

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Thampi, Prajitha ^a   Rao, Haripriya Vittal ^a   Mitter, Sayak K ^a   Cai, Jun ^a   Mao, Haoyu ^a   Li, Hong ^a   Seo, Soojung ^a   Qi, Xiaoping ^a   Lewin, Alfred S ^a   Romano, Carl ^b   Boulton, Michael E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b ALCON RESEARCH LTD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 3 NITROTYROSINE; GLUTATHIONE; LIPOFUSCIN; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL ENZYME; SEROTONIN 1A AGONIST; SODIUM CHLORIDE; SUPEROXIDE; SUPEROXIDE DISMUTASE; ANTIOXIDANT; SEROTONIN 5 RECEPTOR; SEROTONIN AGONIST; SEROTONIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CELL LOSS; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; ELECTRORETINOGRAPHY; EYE PROTECTION; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; RETINA CELL; RETINA MACULA AGE RELATED DEGENERATION; TREATMENT RESPONSE; AGED; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; HUMAN; METABOLISM; MIDDLE AGED; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA MACULA DEGENERATION; VISION;

MUS;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; AGED; AGED, 80 AND OVER; ANIMALS; ANTIOXIDANTS; CELL LINE; CYTOPROTECTION; HUMANS; LIPOFUSCIN; MACULAR DEGENERATION; MICE; MIDDLE AGED; MITOCHONDRIA; OXIDATIVE STRESS; RECEPTORS, SEROTONIN; RETINAL PIGMENT EPITHELIUM; SEROTONIN RECEPTOR AGONISTS; SUPEROXIDES; VISION, OCULAR;

EID: 84859242539     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034468     Document Type: Article

References (56)

1. Friedman DS, O'Colmain BJ, Munoz B, Tomany SC, McCarty C, et al. (2004) Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 122: 564-572.
2. von Ruckmann A, Fitzke FW, Bird AC, (1999) Distribution of pigment epithelium autofluorescence in retinal disease state recorded in vivo and its change over time. Graefes Arch Clin Exp Ophthalmol 237: 1-9.
3. Lois N, Owens SL, Coco R, Hopkins J, Fitzke FW, et al. (2002) Fundus autofluorescence in patients with age-related macular degeneration and high risk of visual loss. Am J Ophthalmol 133: 341-349.
4. Holz FG, Bindewald-Wittich A, Fleckenstein M, Dreyhaupt J, Scholl HP, et al. (2007) Progression of geographic atrophy and impact of fundus autofluorescence patterns in age-related macular degeneration. Am J Ophthalmol 143: 463-472.
5. von Ruckmann A, Fitzke FW, Bird AC, (1997) In vivo fundus autofluorescence in macular dystrophies. Arch Ophthalmol 115: 609-615.
6. Boulton ME, (2009) Lipofuscin of the RPE. In: Lois N, Forrester JV, editors. Fundus Autofluorescence: Wolters Kluwer/Lippincott Williams and Wilkins pp. 14-26.
7. Curcio CA, Medeiros NE, Millican CL, (1996) Photoreceptor loss in age-related macular degeneration. Invest Ophthalmol Vis Sci 37: 1236-1249.
8. Boulton M, Rozanowska M, Rozanowski B, Wess T, (2004) The photoreactivity of ocular lipofuscin. Photochem Photobiol Sci 3: 759-764.
9. Sparrow JR, Boulton ME, (2005) RPE lipofuscin and its role in retinal pathology. Exp Eye Res 80: 595-606.
10. Holz FG, Bellman C, Staudt S, Schutt F, Volcker HE, (2001) Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration. Invest Ophthalmol Vis Sci 42: 1051-1056.
11. Solbach U, Keilhauer C, Knabben H, Wolf S, (1997) Imaging of retinal autofluorescence in patients with age-related macular degeneration. Retina 17: 385-389.
12. Schmitz-Valckenberg S, Bultmann S, Dreyhaupt J, Bindewald A, Holz FG, et al. (2004) Fundus autofluorescence and fundus perimetry in the junctional zone of geographic atrophy in patients with age-related macular degeneration. Invest Ophthalmol Vis Sci 45: 4470-4476.
13. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, et al. (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9: 1390-1397.
14. Malek G, Johnson LV, Mace BE, Saloupis P, Schmechel DE, et al. (2005) Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration. Proc Natl Acad Sci U S A 102: 11900-11905.
15. Justilien V, Pang JJ, Renganathan K, Zhan X, Crabb JW, et al. (2007) SOD2 knockdown mouse model of early AMD. Invest Ophthalmol Vis Sci 48: 4407-4420.
16. Hageman GS, Mullins RF, (1999) Molecular composition of drusen as related to substructural phenotype. Molecular Vision 5: 28.
17. Zhou J, Cai B, Jang YP, Pachydaki S, Schmidt AM, et al. (2005) Mechanisms for the induction of HNE- MDA- and AGE-adducts, RAGE and VEGF in retinal pigment epithelial cells. Exp Eye Res 80: 567-580.
18. Radu RA, Han Y, Bui TV, Nusinowitz S, Bok D, et al. (2005) Reductions in serum vitamin A arrest accumulation of toxic retinal fluorophores: a potential therapy for treatment of lipofuscin-based retinal diseases. Invest Ophthalmol Vis Sci 46: 4393-4401.
19. Travis GH, Golczak M, Moise AR, Palczewski K, (2007) Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu Rev Pharmacol Toxicol 47: 469-512.
20. Radu RA, Mata NL, Nusinowitz S, Liu X, Sieving PA, et al. (2003) Treatment with isotretinoin inhibits lipofuscin accumulation in a mouse model of recessive Stargardt's macular degeneration. Proc Natl Acad Sci U S A 100: 4742-4747.
21. Pucadyil TJ, Kalipatnapu S, Chattopadhyay A, (2005) The serotonin1A receptor: a representative member of the serotonin receptor family. Cell Mol Neurobiol 25: 553-580.
22. Collier RJ, Patel Y, Martin EA, Dembinska O, Hellberg M, et al. (2011) Agonists at the Serotonin Receptor (5-HT1A) Protect the Retina from Severe Photo-Oxidative Stress. Invest Ophthalmol Vis Sci 52: 2118-2126.
23. Collier RJ, Wang Y, Smith SS, Martin EA, Ornberg R, et al. (2011) Complement deposition and microglial activation in the outer retina in light-induced retinopathy: Inhibition by a 5-HT1A agonist. Invest Ophthalmol Vis Sci (in press).
24. Nash MS, Osborne NN, (1997) Pharmacologic evidence for 5-HT1A receptors associated with human retinal pigment epithelial cells in culture. Invest Ophthalmol Vis Sci 38: 510-519.
25. Ahlemeyer B, Krieglstein J, (1997) Stimulation of 5-HT1A receptor inhibits apoptosis induced by serum deprivation in cultured neurons from chick embryo. Brain Res 777: 179-186.
26. Suchanek B, Struppeck H, Fahrig T, (1998) The 5-HT1A receptor agonist BAY x 3702 prevents staurosporine-induced apoptosis. Eur J Pharmacol 355: 95-101.
27. Adayev T, El-Sherif Y, Barua M, Penington NJ, Banerjee P, (1999) Agonist stimulation of the serotonin1A receptor causes suppression of anoxia-induced apoptosis via mitogen-activated protein kinase in neuronal HN2-5 cells. J Neurochem 72: 1489-1496.
28. Semkova I, Wolz P, Krieglstein J, (1998) Neuroprotective effect of 5-HT1A receptor agonist, Bay X 3702, demonstrated in vitro and in vivo. Eur J Pharmacol 359: 251-260.
29. Peruche B, Backhauss C, Prehn JH, Krieglstein J, (1994) Protective effects of 5-HT1A receptor agonists against neuronal damage demonstrated in vivo and in vitro. J Neural Transm Park Dis Dement Sect 8: 73-83.
30. Kline AE, Yu J, Massucci JL, Zafonte RD, Dixon CE, (2002) Protective effects of the 5-HT1A receptor agonist 8-hydroxy-2-(di-n-propylamino)tetralin against traumatic brain injury-induced cognitive deficits and neuropathology in adult male rats. Neurosci Lett 333: 179-182.
31. Oosterink BJ, Harkany T, Luiten PG, (2003) Post-lesion administration of 5-HT1A receptor agonist 8-OH-DPAT protects cholinergic nucleus basalis neurons against NMDA excitotoxicity. Neuroreport 14: 57-60.
32. Piera MJ, Beaughard M, Michelin MT, Massingham R, (1995) Effects of the 5-hydroxytryptamine1A receptor agonists, 8-OH-DPAT, buspirone and flesinoxan, upon brain damage induced by transient global cerebral ischaemia in gerbils. Arch Int Pharmacodyn Ther 329: 347-359.
33. Ramos AJ, Rubio MD, Defagot C, Hischberg L, Villar MJ, et al. (2004) The 5HT1A receptor agonist, 8-OH-DPAT, protects neurons and reduces astroglial reaction after ischemic damage caused by cortical devascularization. Brain Res 1030: 201-220.
34. Torup L, Moller A, Sager TN, Diemer NH, (2000) Neuroprotective effect of 8-OH-DPAT in global cerebral ischemia assessed by stereological cell counting. Eur J Pharmacol 395: 137-141.
35. Burke JM, Skumatz CM, (1998) Autofluorescent inclusions in long-term postconfluent cultures of retinal pigment epithelium. Invest Ophthalmol Vis Sci 39: 1478-1486.
36. Wassell J, Ellis S, Burke J, Boulton M, (1998) Fluorescence properties of autofluorescent granules generated by cultured human RPE cells. Invest Ophthalmol Vis Sci 39: 1487-1492.
37. Wihlmark U, Wrigstad A, Roberg K, Brunk UT, Nilsson SE, (1996) Formation of lipofuscin in cultured retinal pigment epithelial cells exposed to pre-oxidized photoreceptor outer segments. Apmis 104: 272-279.
38. Brizee K, Ordy J, (1981) Age pigments, cell loss and functional implications in the brain. In: Sohal RS, editors. Age Pigments Elsevier/North Holland Biomedical Press pp. 317-334.
39. Brunk UT, Jones CB, Sohal RS, (1992) A novel hypothesis of lipofuscinogenesis and cellular aging based on interactions between oxidative stress and autophagocytosis. Mutat Res 275: 395-403.
40. Lin H, Xu H, Liang FQ, Liang H, Gupta P, et al. (2011) Mitochondrial DNA Damage and Repair in RPE Associated with Aging and Age-Related Macular Degeneration. Invest Ophthalmol Vis Sci 52: 3521-3529.
41. Liu Y, Fanburg BL, (2006) Serotonin-induced growth of pulmonary artery smooth muscle requires activation of phosphatidylinositol 3-kinase/serine-threonine protein kinase B/mammalian target of rapamycin/p70 ribosomal S6 kinase 1. Am J Respir Cell Mol Biol 34: 182-191.
42. Madhavan L, Freed WJ, Anantharam V, Kanthasamy AG, (2003) 5-hydroxytryptamine 1A receptor activation protects against N-methyl-D-aspartate-induced apoptotic cell death in striatal and mesencephalic cultures. J Pharmacol Exp Ther 304: 913-923.
43. Bezard E, Gerlach I, Moratalla R, Gross CE, Jork R, (2006) 5-HT1A receptor agonist-mediated protection from MPTP toxicity in mouse and macaque models of Parkinson's disease. Neurobiol Dis 23: 77-86.
44. de Freitas RL, Santos IM, de Souza GF, Tome Ada R, Saldanha GB, et al. (2010) Oxidative stress in rat hippocampus caused by pilocarpine-induced seizures is reversed by buspirone. Brain Res Bull 81: 505-509.
45. Rojo AI, Salinas M, Martin D, Perona R, Cuadrado A, (2004) Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J Neurosci 24: 7324-7334.
46. Sullivan NR, Crane JW, Damjanoska KJ, Carrasco GA, D'Souza DN, et al. (2005) Tandospirone activates neuroendocrine and ERK (MAP kinase) signaling pathways specifically through 5-HT1A receptor mechanisms in vivo. Naunyn Schmiedebergs Arch Pharmacol 371: 18-26.
47. Druse MJ, Tajuddin NF, Gillespie RA, Le P, (2006) The effects of ethanol and the serotonin(1A) agonist ipsapirone on the expression of the serotonin(1A) receptor and several antiapoptotic proteins in fetal rhombencephalic neurons. Brain Res 1092: 79-86.
48. Kukley M, Schaper C, Becker A, Rose K, Krieglstein J, (2001) Effect of 5-hydroxytryptamine 1A receptor agonist BAY X 3702 on BCL-2 and BAX proteins level in the ipsilateral cerebral cortex of rats after transient focal ischaemia. Neuroscience 107: 405-413.
49. Hsiung SC, Tamir H, Franke TF, Liu KP, (2005) Roles of extracellular signal-regulated kinase and Akt signaling in coordinating nuclear transcription factor-kappaB-dependent cell survival after serotonin 1A receptor activation. J Neurochem 95: 1653-1666.
50. Boulton ME, Marshall J, Mellerio J, (1983) Retinitis pigmentosa: a preliminary report on tissue culture studies of retinal pigment epithelial cells from eight affected human eyes. Exp Eye Res 37: 307-313.
51. Jarrett SG, Boulton ME, (2005) Antioxidant up-regulation and increased nuclear DNA protection play key roles in adaptation to oxidative stress in epithelial cells. Free Radic Biol Med 38: 1382-1391.
52. Boulton M, McKechnie NM, Breda J, Bayly M, Marshall J, (1989) The formation of autofluorescent granules in cultured human RPE. Invest Ophthalmol Vis Sci 30: 82-89.
53. Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, et al. (2005) Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem 280: 21061-21066.
54. Yakes FM, Van Houten B, (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 94: 514-519.
55. Timmers AM, Zhang H, Squitieri A, Gonzalez-Pola C, (2001) Subretinal injections in rodent eyes: effects on electrophysiology and histology of rat retina. Mol Vis 7: 131-137.
56. Cai J, Wu L, Qi X, Shaw L, Li Calzi S, et al. (2011) Placenta growth factor-1 exerts time-dependent stabilization of adherens junctions following VEGF-induced vascular permeability. PLoS One 6: e18076.