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Translational Research Paper

Deletion of autophagy inducer RB1CC1 results in degeneration of the retinal pigment epithelium

, , , , , , , , , & show all
Pages 939-953 | Received 22 Sep 2014, Accepted 10 Apr 2015, Published online: 15 Jun 2015

References

  • Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 2010; 22:124-31; PMID:20034776; http://dx.doi.org/10.1016/j.ceb.2009.11.014
  • Yoshimori, T. Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 2004; 313:453-8; PMID:14684184; http://dx.doi.org/10.1016/j.bbrc.2003.07.023
  • Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
  • Mizushima N. The pleiotropic role of autophagy: From protein metabolism to bactericide. Cell Death Differ 2005; 12:1535-41; PMID:16247501; http://dx.doi.org/10.1038/sj.cdd.4401728
  • Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6; PMID:15525940; http://dx.doi.org/10.1038/nature03029
  • Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/jcb.200412022
  • Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025-40; PMID:15657430; http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005
  • Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90:1383-435; PMID:20959619; http://dx.doi.org/10.1152/physrev.00030.2009
  • Linsenmeier RA, Padnick-Silver L. Metabolic dependence of photoreceptor on the choroid in the normal and detached retina. Invest Ophthalmol Vis Sci 2000; 41:3117-23; PMID:10967072
  • Wangsa-Wirawan ND, Linsenmeier RA. Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol 2003; 121:547-57; PMID:12695252; http://dx.doi.org/10.1001/archopht.121.4.547
  • Kevany BM, Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 2010; 25:8-15; PMID:20134024; http://dx.doi.org/10.1152/physiol.00038.2009
  • Strauss O. The retinal pigment epithelium in visual function. Physiol Rev 2005; 85:845-81; PMID:15987797; http://dx.doi.org/10.1152/physrev.00021.2004
  • Young RW. The renewal of photoreceptor cell outer segments. J Cell Biol 1967; 33:61-72; PMID:6033942; http://dx.doi.org/10.1083/jcb.33.1.61
  • Young RW, Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol 1969; 42:392-403; PMID:5792328; http://dx.doi.org/10.1083/jcb.42.2.392
  • LaVail MM. Legacy of the RCS rat: impact of a seminal study on retinal cell biology and retinal degenerative diseases. Prog Brain Res 2001; 131:617-27; PMID:11420975; http://dx.doi.org/10.1016/S0079-6123(01)31048-8
  • van Lookeren Campagne M, LeCouter J, Yaspan BL, Ye W. Mechanisms of age related macular degeneration and therapeutic opportunities. J Pathol 2014; 232:151-64; PMID:24105633; http://dx.doi.org/10.1002/path.4266
  • Reme CE, Autophagy in visual cells and pigment epithelium. Invest. Ophthalmol Vis Sci 1977; 16:807-14; PMID:302253
  • Wang AL, Lukas TJ, Yuan M, Du N, Tso MO, Neufeld AH. Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration. PLoS One 2009; 4:e4160; PMID:19129916; http://dx.doi.org/10.1371/journal.pone.0004160
  • Krohne TU, Stratmann NK, Kopitz J, Holz FG. Effects of lipid peroxidation products on lipofuscinogenesis and autophagy in human retinal pigment epithelial cells. Exp Eye Res 2010; 90:465-71; PMID:20059996; http://dx.doi.org/10.1016/j.exer.2009.12.011
  • Viiri J, Hyttinen JM, Ryhanen T, Rilla K, Paimela T, Kuusisto E, Siitonen A, Urtti A, Salminen A, Kaarniranta K. p62/sequestosome 1 as a regulator of proteasome inhibitor-induced autophagy in human retinal pigment epithelial cells. Mol Vis 2010; 16:1399-414; PMID:20680098
  • Mitter SK, Song C, Qi X, Mao H, Rao H, Akin DA, Lewin AS, Grant M, Dunn WA, Ding JD, et al. Dysregulated autophagy in the RPE is associated with increased susceptibility to oxidative stress and AMD. Autophagy 2014; 10(11):1989-2005; PMID:25484094.
  • Mitter SK, Rao HV, Qi X, Cai J, Sugrue A, Dunn WA Jr, Grant MB, Boulton ME. Autophagy in the retina: a potential role in age-related macular degeneration. Adv Exp Med Biol 2012; 723:83-90; PMID:22183319; http://dx.doi.org/10.1007/978-1-4614-0631-0_12
  • Valapala M, Wilson C, Hose S, Bhutto IA, Grebe R, Dong A, Greenbaum S, Gu L, Sengupta S, Can M, et al. Lysosomal-mediated waste clearance in retinal pigment epithelial cells is regulated by CRYBA1/bA3/A1-crystallin via V-ATPas-MTORC1 signaling. Autophagy 2014; 10:480-96; PMID:24468901; http://dx.doi.org/10.4161/auto.27292
  • Viiri J, Amadio M, Marchesi N, Hyttinen JM, Kivinen N, Sironen R, Rilla K, Akhtar S, Provenzani A, D'Agostino VG, et al. Autophagy activation clears ELAVL1/HuR-mediated accumulation of SQSTM1/p62 during proteasomal inhibition in human retinal pigment epithelial cells. PLoS One 2013; 8:e69563; PMID:23922739; http://dx.doi.org/10.1371/journal.pone.0069563
  • Rodríguez-Muela N, Koga H, García-Ledo L, de la Villa P, de la Rosa EJ, Cuervo AM, Boya P. Balance between autophagic pathways preserves retinal homeostasis. Aging Cell 2013; 12:478-88; http://dx.doi.org/10.1111/acel.12072
  • Ganley IG, Lam du H, Wang J, Ding X, Chen S, Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305.
  • Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DJ. ULK-Atg13–FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID:19225151; http://dx.doi.org/10.1091/mbc.E08-12-1249
  • Gammoh N, Florey O, Overholtzer M, Jiang X. Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and-independent autophagy. Nat Struct Mol Biol 2013; 20:144-9; PMID:23262492; http://dx.doi.org/10.1038/nsmb.2475
  • Nishimura T, Kaizuka T, Cadwell K, Sahani MH, Saitoh T, Akira S, Virgin HW, Mizushima N. FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep 2013; 14:284-91; PMID:23392225; http://dx.doi.org/10.1038/embor.2013.6
  • Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, Mizushima N. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 2008; 181:497-510; PMID:18443221; http://dx.doi.org/10.1083/jcb.200712064
  • Wang C, Liang CC, Bian ZC, Zhu Y, Guan JL. FIP200 is required for maintenance and differentiation of postnatal neural stem cells. Nat Neurosci 2013; 16:532-42; PMID:23542691; http://dx.doi.org/10.1038/nn.3365
  • Wei H, Wei S, Gan B, Peng X, Zou W, Guan JL. Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev 2011; 25:1510-27; PMID:21764854; http://dx.doi.org/10.1101/gad.2051011
  • Gan B, Peng X, Nagy T, Alcaraz A, Gu H, Guan J-L. Role of FIP200 in cardiac and liver development and its regulation of TNF and TSC-mTOR signaling pathways. J Cell Biol 2006; 175:121-33; PMID:17015619; http://dx.doi.org/10.1083/jcb.200604129
  • Iacovelli J, Zhao C, Wolkow N, Veldman P, Gollomp K, Ojha P, Lukinova N, King A, Feiner L, Esumi N, et al. Generation of Cre transgenic mice with postnatal RPE-specific ocular expression. Invest Ophthalmol Vis Sci 2011; 52:1378-83; PMID:21212186; http://dx.doi.org/10.1167/iovs.10-6347
  • Kim JY, Zhao H, Martinez J, Doggett TA, Kolesnikov AV, Tang PH, Ablonczy Z, Chan CC, Zhou Z, Green DR, et al. Noncanonical autophagy promotes the visual cycle. Cell 2013; 154:365-76; PMID:23870125; http://dx.doi.org/10.1016/j.cell.2013.06.012
  • Yao J, Jia L, Shelby SJ, Ganios AM, Feathers K, Thompson DA, Zacks DN. Circadian and noncircadian modulation of autophagy in photoreceptors and retinal pigment epithelium. Invest Ophthalmol Vis Sci 2014; 55:3237-46; PMID:24781939; http://dx.doi.org/10.1167/iovs.13-13336
  • He L, Marioutina M, Dunaief JL, Marneros AG. Age- and gene-dosage-dependent cre-induced abnormalities in the retinal pigment epithelium. Am J Pathol 2014; 184:1660-7; PMID:24854863; http://dx.doi.org/10.1016/j.ajpath.2014.02.007
  • Gan B, Guan JL. FIP200, a key signaling node to coordinately regulate various cellular processes. Cell Signal 2008; 20:787-94; PMID:18036779; http://dx.doi.org/10.1016/j.cellsig.2007.10.021
  • Chen L, Yang P, Kijlstra A. Distribution, markers and functions of retinal microglia. Ocul Immunol Inflamm 2002; 10:27-39; PMID:12461701; http://dx.doi.org/10.1076/ocii.10.1.27.10328
  • Langmann T. Microglia activation in retinal degeneration. J Leukoc Biol 2007; 81:1345-51; PMID:17405851; http://dx.doi.org/10.1189/jlb.0207114
  • Cuenca N, Fernandez-Sanchez L, Campello L, Maneu V, De al Villa P, Lax P, Pinilla I. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases. Prog Retin Eye Res 2014; 43:17-75; PMID:25038518; http://dx.doi.org/10.1016/j.preteyeres.2014.07.001
  • Karlstetter M, Langmann T. Microglia in the aging retina. Adv Exp Med Biol 2014; 801:207-12; PMID:24664700; http://dx.doi.org/10.1007/978-1-4614-3209-8_27
  • Rizzolo LJ. Basement membrane stimulates the polarized distribution of integrins but not the Na,K-ATPase in the retinal pigment epithelium. Cell Regul 1991; 2:939-49.; PMID:1667092
  • Grossniklaus HE, Kang SJ, Berglin L. Animal models of choroidal and retinal neovascularization. Prog Retin Eye Res 2010; 29:500-19; PMID:20488255; http://dx.doi.org/10.1016/j.preteyeres.2010.05.003
  • Zacks DN, Ezra E, Terada Y, Michaud N, Connolly E, Gragoudas ES, Miller JW. Verteporfin photodynamic therapy in the rat model of choroidal neovascularization: angiographic and histologic characterization. Invest Ophthalmol Vis Sci 2002; 43:2384-91; PMID:12091441
  • Jiang A, Hu W, Meng H, Gao H, Qiao X. Loss of VLDL receptor activates retinal vascular endothelial cells and promotes angiogenesis. Invest Ophthalmol Vis Sci 2009; 50:844-50; PMID:18936153; http://dx.doi.org/10.1167/iovs.08-2447
  • Lippai M, Low P. The role of the selective adaptor p62 and ubiquitin-like proteins in autophagy. Biomed Res Int 2014; 2014:832704; PMID:25013806; http://dx.doi.org/10.1155/2014/832704
  • Ryhänen T, Hyttinen JM, Kopitz J, Rilla K, Kuusisto E, Mannermaa E, Viiri J, Holmberg CI, Immonen I, Meri S, et al. Crosstalk between Hsp70 molecular chaperone, lysosomes and proteasomes in autophagy-mediated proteolysis in human retinal pigment epithelial cells. J Cell Mol Med 2009; 13:3616-31; http://dx.doi.org/10.1111/j.1582-4934.2008.00577.x
  • Ohno-Matsui K. Parallel findings in age-related macular degeneration and Alzheimer disease. Prog Retin Eye Res 2011; 30:217-38; PMID:21440663; http://dx.doi.org/10.1016/j.preteyeres.2011.02.004
  • Zhao Y, Bhattacharjee S, Jones BM, Hill JM, Clement C, Sambamurti K, Dua P, Lukiw WJ. Beta-amyloid precursor protein (bAAP) processing in Alzheimer disease (AD) and age-related macular degeneration (AMD). Mol Neurobiol 2014; Epub ahead of print.
  • Hyttinen JM, Amadio M, Viiri J, Pascale A, Salminen A, Kaarniranta K. Clearance of misfolded and aggregated proteins by aggrephagy and implications for aggregation diseases. Ageing Res Rev 2014:18C:16-28; http://dx.doi.org/10.1016/j.arr.2014.07.002
  • Mazzoni F, Safa H, Finnemann SC. Understanding photoreceptor outer segment phagocytosis: use and utility of RPE cells in culture. Exp Eye Res 2014; 126:51-60; PMID:24780752
  • Zheng W, Reem RE, Omarova S, Huang S, DiPatre PL, Charvet CD, Curcio CA, Pikuleva IA. Spatial distribution of the pathways of cholesterol homeostasis in human retina. PLoS One 2012; 7(5):e37926; PMID:22629470; http://dx.doi.org/10.1371/journal.pone.0037926
  • Tang PH, Kono M, Koutalos Y, Ablonczy Z, Crouch RK. New insights into retinoid metabolism and cycling within the retina. Prog Retin Eye Res 2013; 32:48-63; PMID:23063666; http://dx.doi.org/10.1016/j.preteyeres.2012.09.002
  • Ferris FL 3rd, Wilkinson CP, Bird A, Chakravarthy U, Chew E, Scaky K, Sadda SR, Beckman Initiative for Macular Research Classification Committee. Clinical classification of age-related macular degeneration. Ophthalmology 2013; 120:844-51; PMID:23332590; http://dx.doi.org/10.1016/j.ophtha.2012.10.036
  • Spaide RF, Curcio CA. Drusen characterization with multimodal imaging. Retina 2010; 30:1441-54; PMID:20924263; http://dx.doi.org/10.1097/IAE.0b013e3181ee5ce8
  • Kaarniranta K, Sinha D, Blasiak J, Kauppinen A, Vereb Z, Salminen A, Boulton ME, Petrovski G. Autophagy and heterophagy dysregulation leads to retinal pigment epithelium dysfunction and development of age-related macular degeneration. Autophagy 2013; 9:973-84; PMID:23590900; http://dx.doi.org/10.4161/auto.24546
  • Machalinska A, Lubinski W, Klos P, Kawa M, Baumer B, Penkala K, Grzegrzolka R, Karczewicz D, Wiszniewska B, Machalinski B. Sodium iodate selectively injures the posterior pole of the retina in a dose-dependent manner: morphological and electrophysiological study. Neurochem Res 2010; 35:1819-27; PMID:20725778; http://dx.doi.org/10.1007/s11064-010-0248-6
  • Ramkumar HL, Zhang J, Chan CC. Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD). Prog Retin Eye Res 2010; 29:169-90; PMID:20206286; http://dx.doi.org/10.1016/j.preteyeres.2010.02.002
  • Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, Cho WG, Kleinman ME, Ponicsan SL, Hauswirth WW, Chiodo VA, et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 2011; 471:325-30; PMID:21297615; http://dx.doi.org/10.1038/nature09830
  • Tarallo V, Hiran Y, Gelfand BD, Dridi S, Kerur N, Kim Y, Cho WG, Kaneko H, Fowler BJ, Bogdanovich S, et al. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 2012:149; 847-59; PMID:22541070; http://dx.doi.org/10.1016/j.cell.2012.03.036
  • Gibbings D, Mostowy S, Voinnet O. Autophagy selectively regulates miRNA homeostasis. Autophagy 2013; 14:1314-21.
  • Williams-Bey Y, Boularan C, Vural A, Huang NN, Hwang IY, Shan-Shi C, Kehri JH. Omega-3 free fatty acids suppress macrophage inflammasome activation by inhibiting NF-kB activation and enhancing autophagy. PLoS One 2014; 9(6):e97957; PMID:24911523; http://dx.doi.org/10.1371/journal.pone.0097957
  • Guo W, Sun Y, Liu W, Wu X, Guo L, Cai P, Wu X, Wu X, Shen Y, Shu Y, Gu Y, Xu Q. Small molecule-driven mitophagy-mediated NLRP3 inflammasome inhibition is responsible for the prevention of colitis-associated cancer. Autophagy 2014; 10:972-85; PMID:24879148; http://dx.doi.org/10.4161/auto.28374
  • Malek G, Johnson LV, Mace BE, Saloupis P, Schmechel DE, Rickman DW, Toth CA, Sullivan PM, Bowes Rickman C. Apolipoprotein E allele-dependent pathogenesis: a model for age-related macular degeneration. Proc Nat Acad Sci 2005; 102:11900-5; PMID:16079201; http://dx.doi.org/10.1073/pnas.0503015102
  • Curcio CA, Johnson M, Rudolf M, Huang JD. The oil spill in ageing Bruch membrane. Br J Ophthalmol 2011; 95:1638-45; PMID:21890786; http://dx.doi.org/10.1136/bjophthalmol-2011-300344
  • Pikuleva IA, Curcio CA. Cholesterol in the retina: the best is yet to come. Prog Retin Eye Res 2014; 41C:64-89; http://dx.doi.org/10.1016/j.preteyeres.2014.03.002
  • Liu K, Czaia MJ. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 2013; 20:3-11; PMID:22595754; http://dx.doi.org/10.1038/cdd.2012.63
  • Christian P, Sacco J, Adeli K. Autophagy: emerging roles in lipid homeostasis and metabolic control. Biochim Biophys Acta 2013; 1831:819-24; PMID:23274236; http://dx.doi.org/10.1016/j.bbalip.2012.12.009
  • Mattapallil MJ, Wawrousek EF, Chan CC, Zhao H, Roychoudhury J, Ferguson TA, Caspi RR. The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest Ophthalmol Vis Sci 2012; 53:2921-7; PMID:22447858; http://dx.doi.org/10.1167/iovs.12-9662
  • Papermaster, DS. Preparation of retinal rod outer segments. Methods Enzymol 1982; 81:48-52; PMID:6212746; http://dx.doi.org/10.1016/S0076-6879(82)81010-0
  • Shelby SJ, Colwill K, Dhe-Paganon S, Pawson T, Thompson DA. MERTK interactions with SH2-domain proteins in the retinal pigment epithelium. PLoS One 2013; 8(2):e53964; PMID:23390493; http://dx.doi.org/10.1371/journal.pone.0053964
  • Sparrow JR, Boulton M. RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 2005; 80:595-606; PMID:15862166; http://dx.doi.org/10.1016/j.exer.2005.01.007
  • Hadziahmetovic M1, Song Y, Ponnuru P, Iacovelli J, Hunter A, Haddad N, Beard J, Connor JR, Vaulont S, Dunaief JL. Age-dependent retinal iron accumulation and degeneration in hepcidin knockout mice. Invest Ophthalmol Vis Sci 2011; 52:109-18; PMID:20811044; http://dx.doi.org/10.1167/iovs.10-6113
  • Thompson DA, Khan NW, Othman MI, Chang B, Jia L, Grahek G, Wu Z, Hiriyanna S, Nellissery J, Li T, et al. Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15. PLoS ONE 2012; 7(5):e35865; PMID:22563472; http://dx.doi.org/10.1371/journal.pone.0035865
  • Hemati N, Feathers KL, Chrispell JD, Reed DM, Carlson TJ, Thompson DA. RPE65 surface epitopes, protein interactions, and expression in rod- and cone-dominant species. Mol Vis 2005; 11:1151-65; PMID:16379027

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