Lack of Niemann-Pick type C1 induces age-related degeneration in the mouse retina
Abstract
Niemann-Pick type C (NPC) disease is an inherited lysosomal storage disease and caused by mutations in Npc1 or Npc2, which mediate cooperatively the egress of cholesterol from lysosomes. The disease entails progressive neurodegeneration, whose cause is poorly understood. Here, we report that Npc1 is distributed in distinct layers of the mouse retina and that its deficiency causes striking retinal degeneration in 2-month-old mice with signs of age-related maculopathies. This includes impaired visual function, accumulation of lipofuscin in the retinal pigment epithelium layer, degeneration of photoreceptor outer segments, disruption of synaptic layers and an increase in autophagy markers in the ganglion cell layer. Moreover, the lack of Npc1 results in the upregulation of proteins that mediate cellular cholesterol release in the retina. Our findings suggest that Npc1 is required for normal retinal function and that its absence may serve as model to study age-related degeneration of the retina.
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Rodent and fruit fly models of NPC disease have extensive cholesterol accumulation in the RPE and retinal neurons, increased lipofuscin, and progressive photoreceptor degeneration.
“Rodent and fruit fly models of NPC disease have extensive cholesterol accumulation in the RPE and retinal neurons, increased lipofuscin, and progressive photoreceptor degeneration (Phillips et al., 2008; Claudepierre et al., 2010).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Claudepierre et al., 2010
Diseases that affect lysosomes often negatively impact the RPE, including Danon disease and lysosomal storage disorders such as Niemann Pick Type C.
“Unsurprisingly, diseases that affect lysosomes often negatively impact the RPE. These include Danon disease, caused by mutations in LAMP2, and lysosomal storage disorders such as Niemann Pick Type C, caused by mutations in the cholesterol transporters Niemann Pick C1 or C2 (NPC1 or NPC2) (Phillips et al., 2008; Claudepierre et al., 2010; Thompson et al., 2016).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Claudepierre et al., 2010
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Autophagy in the Pathogenesis of Disease
Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069 · see citing works
Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes
Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A., et al. (2008) · Autophagy · doi:10.4161/auto.5338 · Cited by 2,230 · see citing works
CNS synaptogenesis promoted by glia-derived cholesterol
Mauch, D. H., Nägler, K., Schumacher, S., Göritz, C., Müller, E.-C., Otto, A., & Pfrieger, F. W. (2001) · Science · doi:10.1126/science.294.5545.1354 · Cited by 1,711 · see citing works
Self-citationNiemann-Pick C1 Disease Gene: Homology to Mediators of Cholesterol Homeostasis
Carstea, E. D., Morris, J. A., Coleman, K. G., Loftus, S. K., Zhang, D., Cummings, C., Gu, J. Z., Rosenfeld, M. A., Pavan, W. J., Krizman, D. B., et al. (1997) · Science · doi:10.1126/science.277.5323.228 · Cited by 1,461 · see citing works
The cell biology of lysosomal storage disorders
Futerman, A., & van Meer, G. (2004) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1423 · Cited by 836 · see citing works
Lloyd‐Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., Churchill, G. C., Schuchman, E. H., Galione, A., & Platt, F. M. (2008) · Nature Medicine · doi:10.1038/nm.1876 · Cited by 832 · see citing works
Identification of HE1 as the Second Gene of Niemann-Pick C Disease
Naureckiene, S., Sleat, D. E., Lackland, H., Fensom, A. H., Vanier, M. T., Wattiaux, R., Jadot, M., & Lobel, P. (2000) · Science · doi:10.1126/science.290.5500.2298 · Cited by 823 · see citing works
Murine Model of Niemann-Pick C Disease: Mutation in a Cholesterol Homeostasis Gene
Loftus, S. K., Morris, J. A., Carstea, E. D., Gu, J. Z., Cummings, C., Brown, A., Ellison, J., Ohno, K., Rosenfeld, M. A., Tagle, D. A., et al. (1997) · Science · doi:10.1126/science.277.5323.232 · Cited by 798 · see citing works
Kwon, H. J., Abi-Mosleh, L., Wang, M. L., Deisenhofer, J., Goldstein, J. L., Brown, M. S., & Infante, R. E. (2009) · Cell · doi:10.1016/j.cell.2009.03.049 · Cited by 656 · see citing works
Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study
Patterson, M. C., Vecchio, D., Prady, H., Abel, L. A., & Wraith, J. E. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70194-1 · Cited by 608 · see citing works
(1992) · PubMed · Cited by 604 · see citing works
Molecular pathology of age-related macular degeneration
Ding, X., Patel, M., & Chan, C.-C. (2009) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2008.10.001 · Cited by 582 · see citing works
Vanier, M., & Millat, G. (2003) · Clinical Genetics · doi:10.1034/j.1399-0004.2003.00147.x · Cited by 578 · see citing works
Age-related accumulation and spatial distribution of lipofuscin in RPE of normal subjects.
Delori, F. C., Goger, D. G., & Dorey, C. K. (2001) · PubMed · Cited by 424 · see citing works
The adult form of Niemann-Pick disease type C
Sevin, M., Lesca, G., Baumann, N., Millat, G., Lyon‐Caen, O., Vanier, M. T., & Sedel, F. (2006) · Brain · doi:10.1093/brain/awl260 · Cited by 385 · see citing works
Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport
Sleat, D. E., Wiseman, J. A., El-Banna, M., Price, S. M., Vérot, L., Shen, M. M., Tint, G. S., Vanier, M. T., Walkley, S. U., & Lobel, P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308456101 · Cited by 365 · see citing works
Neurodegenerative lysosomal disorders: A continuum from development to late age
Nixon, R. A., Yang, D.-S., & Lee, J.-H. (2008) · Autophagy · doi:10.4161/auto.6259 · Cited by 362 · see citing works
Multiple mechanisms mediate cholesterol-induced synaptogenesis in a CNS neuron
Goritz, C., Mauch, D. H., & Pfrieger, F. W. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.02.006 · Cited by 330 · see citing works
Self-citationLiscum, L., & Faust, J. R. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)80136-3 · Cited by 321 · see citing works
Outsourcing in the brain: Do neurons depend on cholesterol delivery by astrocytes?
Pfrieger, F. W. (2003) · BioEssays · doi:10.1002/bies.10195 · Cited by 308 · see citing works
Self-citationMarked differences in cholesterol synthesis between neurons and glial cells from postnatal rats
Nieweg, K., Schaller, H., & Pfrieger, F. W. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.05917.x · Cited by 307 · see citing works
Self-citationLiscum, L., Ruggiero, R. M., & Faust, J. R. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.5.1625 · Cited by 307 · see citing works
Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration
Malek, G., Johnson, L. V., Mace, B. E., Saloupis, P., Schmechel, D. E., Rickman, D. W., Toth, C. A., Sullivan, P. M., & Rickman, C. B. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503015102 · Cited by 284 · see citing works
Consequences of NPC1 and NPC2 loss of function in mammalian neurons
Walkley, S. U., & Suzuki, K. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2004.08.011 · Cited by 274 · see citing works
PARTICIPATION OF THE RETINAL PIGMENT EPITHELIUM IN THE ROD OUTER SEGMENT RENEWAL PROCESS
Young, R. W., & Bok, D. (1969) · Journal of Cell Biology · doi:10.1083/jcb.42.2.392 · Cited by 271 · see citing works
Curcio, C. A., Presley, J. B., Malek, G., Medeiros, N. E., Avery, D. V., & Kruth, H. S. (2005) · Experimental Eye Research · doi:10.1016/j.exer.2005.04.012 · Cited by 254 · see citing works
Sokol, J., Blanchette‐Mackie, J., Kruth, H. S., Dwyer, N. K., Amende, L. M., Butler, J. D., Robinson, E., Patel, S., Brady, R. O., & Comly, M. E. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)69086-6 · Cited by 232 · see citing works
Macular degeneration: recent advances and therapeutic opportunities
Rattner, A., & Nathans, J. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn2007 · Cited by 230 · see citing works
Liao, G., Yao, Y., Liu, J., Yu, Z., Cheung, S., Xie, A., Liang, X., & Bi, X. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.070052 · Cited by 220 · see citing works
Pacheco, C. D., Kunkel, R., & Lieberman, A. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm100 · Cited by 219 · see citing works
The effect of age on human cone and rod ganzfeld electroretinograms.
Weleber, R. G. (1981) · PubMed · Cited by 216 · see citing works
Cerebellar degeneration in the Niemann-Pick type C mouse
Higashi, Y., Murayama, S., Pentchev, P. G., & Suzuki, K. (1993) · Acta Neuropathologica · doi:10.1007/bf00227765 · Cited by 216 · see citing works
Cell-Autonomous Death of Cerebellar Purkinje Neurons with Autophagy in Niemann-Pick Type C Disease
Ko, D. C., Milenković, L., Beier, S., Manuel, H., Buchanan, J., & Scott, M. P. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010007 · Cited by 214 · see citing works
Niemann–Pick C2 (NPC2) and intracellular cholesterol trafficking
Storch, J., & Xu, Z. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2009.02.001 · Cited by 204 · see citing works
Cholesterol involvement in the pathogenesis of neurodegenerative diseases
Liu, J., Tang, Y., Zhou, S., Toh, B. H., McLean, C., & Li, H. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.07.013 · Cited by 204 · see citing works
Zacchigna, S., Oh, H., Wilsch‐Bräuninger, M., Missol‐Kolka, E., Jászai, J., Jansen, S., Tanimoto, N., Tonagel, F., Seeliger, M. W., Huttner, W. Β., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2034-08.2009 · Cited by 189 · see citing works
In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy
Seeliger, M. W., Beck, S. C., Pereyra-Muñoz, N., Dangel, S., Tsai, J.-Y., Luhmann, U. F. O., van de Pavert, S. A., Wijnholds, J., Samardzija, M., Wenzel, A., et al. (2005) · Vision Research · doi:10.1016/j.visres.2005.08.014 · Cited by 171 · see citing works
The lipofuscin fluorophore A2E perturbs cholesterol metabolism in retinal pigment epithelial cells
Lakkaraju, A., Finnemann, S. C., & Rodriguez-Boulan, E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702504104 · Cited by 162 · see citing works
The National Niemann–Pick C1 disease database: Report of clinical features and health problems
Garver, W. S., Francis, G. A., Jelínek, D., Shepherd, G. W., Flynn, J., Castro, G. R., Vockley, C. W., Coppock, D. L., Pettit, K. M., Heidenreich, R., et al. (2007) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.31735 · Cited by 162 · see citing works
Genetic variations and treatments that affect the lifespan of the NPC1 mouse
Liu, B., Li, H., Repa, J. J., Turley, S. D., & Dietschy, J. M. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m700525-jlr200 · Cited by 160 · see citing works
Cholesterol‐dependent balance between evoked and spontaneous synaptic vesicle recycling
Wasser, C. R., Ertunç, M., Liu, X., & Kavalali, E. T. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.123133 · Cited by 150 · see citing works
Huang, X., Suyama, K. L., Buchanan, J., Zhu, A. J., & Scott, M. P. (2005) · Development · doi:10.1242/dev.02079 · Cited by 149 · see citing works
Repa, J. J., Li, H., Frank-Cannon, T. C., Valasek, M. A., Turley, S. D., Tansey, M. G., & Dietschy, J. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4823-07.2007 · Cited by 148 · see citing works
Lysosome lipid storage disorder in NCTR-BALB/c mice. I. Description of the disease and genetics.
Morris, M. D., Bhuvaneswaran, C., Shio, H., & Fowler, S. (1982) · PubMed Central · Cited by 140 · see citing works
Choi, H. Y., Karten, B., Chan, T., Vance, J. E., Greer, W. L., Heidenreich, R. A., Garver, W. S., & Francis, G. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304553200 · Cited by 138 · see citing works
The natural history of Niemann–Pick disease type C in the UK
Imrie, J., Dasgupta, S., BESLEY, G. T. N., Harris, C. M., Heptinstall, L., Knight, S., Vanier, M. T., Fensom, A. H., Ward, C., Jacklin, E., et al. (2006) · Journal of Inherited Metabolic Disease · doi:10.1007/s10545-006-0384-7 · Cited by 133 · see citing works
Karten, B., Peake, K. B., & Vance, J. (2009) · Biochimica et Biophysica Acta · doi:10.1016/j.bbalip.2009.01.025 · Cited by 129 · see citing works
Electrophysiological analysis of visual function in mutant mice
Peachey, N. S., & Ball, S. L. (2003) · Documenta Ophthalmologica · doi:10.1023/a:1024448314608 · Cited by 114 · see citing works
Age-related changes in the retinal pigment epithelium of pigmented rats
Katz, M. L., & Robison, W. G. (1984) · Experimental Eye Research · doi:10.1016/0014-4835(84)90098-8 · Cited by 111 · see citing works
Cellular pathology of Niemann–Pick type C disease
Ikonen, E., & Hölttä‐Vuori, M. (2004) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2004.03.001 · Cited by 108 · see citing works
Mouse models of age-related macular degeneration
Elizabeth Rakoczy, P., Yu, M. J. T., Nusinowitz, S., Chang, B., & Heckenlively, J. R. (2006) · Experimental Eye Research · doi:10.1016/j.exer.2005.10.012 · Cited by 107 · see citing works
Alvarez, A. R., Klein, A. D., Castro, J., Cancino, G. I., Amigo, J. D., Mosqueira, M., Vargas, L. M., Yévenes, L. F., Bronfman, F. C., & Zanlungo, S. (2008) · The FASEB Journal · doi:10.1096/fj.07-102715 · Cited by 106 · see citing works
Clues to Neuro-Degeneration in Niemann-Pick Type C Disease from Global Gene Expression Profiling
Reddy, J. V., Ganley, I. G., & Pfeffer, S. R. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000019 · Cited by 104 · see citing works
Niemann–Pick C research from mouse to gene
Pentchev, P. G. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2004.08.005 · Cited by 99 · see citing works
Duncan, K. G., Hosseini, K., Bailey, K. R., Yang, H., Lowe, R., Matthes, M. T., Kane, J. P., LaVail, M. M., Schwartz, D. M., & Duncan, J. L. (2009) · British Journal of Ophthalmology · doi:10.1136/bjo.2008.144006 · Cited by 97 · see citing works
The clinical spectrum of fetal Niemann–Pick type C
Spiegel, R., Raas‐Rothschild, A., Reish, O., Regev, M., Meiner, V., Bargal, R., Sury, V., Meir, K. S., Nadjari, M., Hermann, G., et al. (2009) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.32642 · Cited by 96 · see citing works
Phillips, S. E., Woodruff, E. A., Liang, P., Patten, M., & Broadie, K. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5529-07.2008 · Cited by 93 · see citing works
High resolution fundus imaging by confocal scanning laser ophthalmoscopy in the mouse
Pâques, M., Simonutti, M., Roux, M. J., Picaud, S. A., Levavasseur, E., Bellman, C., & Sahel, J. (2005) · Vision Research · doi:10.1016/j.visres.2005.09.037 · Cited by 93 · see citing works
Self-citationEffects of cholesterol and apolipoprotein E on retinal abnormalities in ApoE-deficient mice.
Ong, J. M., Zorapapel, N. C., Rich, K. A., Wagstaff, R. E., Lambert, R. W., Rosenberg, S., Moghaddas, F., Pirouzmanesh, A., Aoki, A. M., & Kenney, M. C. (2001) · PubMed · Cited by 92 · see citing works
Bonnel, S., Mohand-Said, S., & Sahel, J.-A. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(03)00093-7 · Cited by 89 · cited 3× · see citing works
“The retinal pathology of Npc1-deficient mice mimics some of the symptoms of normal aging (Bonnel et al., 2003) and of age-related macular degeneration (ARMD) (Rattner and Nathans, 2006).”
BackgroundSelf-citationCholesterol Accumulation by Macrophages Impairs Phagosome Maturation
Huynh, K. K., Gershenzon, E., & Grinstein, S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806232200 · Cited by 89 · see citing works
Espinosa‐Heidmann, D. G., Sall, J. C., Hernandez, E. P., & Cousins, S. W. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.03-0910 · Cited by 82 · see citing works
The cherry‐red spot in Tay‐Sachs and other storage diseases
Kivlin, J. D., Sanborn, G. E., & Myers, G. G. (1985) · Annals of Neurology · doi:10.1002/ana.410170409 · Cited by 73 · see citing works
The APO(*)E3-Leiden mouse as an animal model for basal laminar deposit
Kliffen, M. (2000) · British Journal of Ophthalmology · doi:10.1136/bjo.84.12.1415 · Cited by 71 · see citing works
Retinal Degeneration in a Rodent Model of Smith-Lemli-Opitz Syndrome
Fliesler, S. J. (2004) · Archives of Ophthalmology · doi:10.1001/archopht.122.8.1190 · Cited by 64 · see citing works
Faubert, J., & Overbury, O. (2000) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2000.tb04693.x · Cited by 54 · see citing works
The Niemann-Pick C1 protein in recycling endosomes of presynaptic nerve terminals
Karten, B., Campenot, R. B., Vance, D. E., & Vance, J. E. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500482-jlr200 · Cited by 53 · see citing works
Chen, Y., Hu, Y., Moiseyev, G. P., Zhou, K., Chen, D., & Ma, J.-X. (2009) · Microvascular Research · doi:10.1016/j.mvr.2009.02.005 · Cited by 53 · see citing works
Brétillon, L., Acar, N., Seeliger, M. W., Santos, M., Maire, M. A., ́da, P. J., Martine, L., Gregoire, S., Joffre, C., Bron, A. M., et al. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-0808 · Cited by 53 · see citing works
Wang, M., Franklin, V., Sundaram, M., Kiss, R. S., Ho, K., Gallant, M., & Marcel, Y. L. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700326200 · Cited by 48 · see citing works
Boadu, E., Choi, H. Y., Lee, D. W. K., Waddington, E. I., Chan, T., Asztalos, B. F., Vance, J. E., Chan, A., Castro, G. R., & Francis, G. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606890200 · Cited by 40 · see citing works
Provost, A. C., Vede, L., Bigot, K., Keller, N., Tailleux, A., ̈s, J.-P. J., Savoldelli, M., Ameqrane, I., Lacassagne, E., Legeais, J., et al. (2009) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.08-2527 · Cited by 36 · see citing works
Melanization and phagocytosis: implications for age related macular degeneration.
Sarangarajan, R., & Apte, S. (2005) · PubMed · Cited by 35 · see citing works
Lee, S., Kim, J. H., Kim, J. H., Chung, M. J., Wen, Q., Chung, H., Kim, K. W., & Yu, Y. S. (2007) · PubMed · Cited by 33 · see citing works
Palmer, M. L. (1985) · Archives of Ophthalmology · doi:10.1001/archopht.1985.01050060077030 · Cited by 26 · see citing works
Fliesler, S. J., Richards, M. J., Miller, C. ‐., & Cenedella, R. J. (2000) · Lipids · doi:10.1007/s11745-000-0525-y · Cited by 22 · see citing works
Stage-Specific Association of Apolipoprotein A-I and E in Developing Mouse Retina
車田, 真., Onishi, A., Imai, H., Ishii, K., Kobayashi, T., & Sato, S. B. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0902 · Cited by 19 · see citing works
Effect of aging on multifocal oscillatory potentials
Kurtenbach, A., & Weiss, M. (2002) · Journal of the Optical Society of America A · doi:10.1364/josaa.19.000190 · Cited by 16 · see citing works
Ophthalmologic Aspects of Lipid Storage Diseases
Brady, R. O. (1978) · Ophthalmology · doi:10.1016/s0161-6420(78)35592-5 · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 80 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Cholesterol metabolism in neurons and astrocytes
Pfrieger, F. W., & Ungerer, N. (2011) · Progress in Lipid Research · doi:10.1016/j.plipres.2011.06.002 · Cited by 500 · see citing works
Self-citationThe cell biology of the retinal pigment epithelium
Lakkaraju, A., Umapathy, A., Tan, L. X., Daniele, L., Philp, N. J., Boesze-Battaglia, K., & Williams, D. S. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100846 · Cited by 422 · see citing works
Cholesterol in the retina: The best is yet to come
Pikuleva, I. A., & Curcio, C. A. (2014) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2014.03.002 · Cited by 282 · see citing works
Autophagy Impairment Induces Premature Senescence in Primary Human Fibroblasts
Kang, H. T., Lee, K. B., Kim, S. Y., Choi, H. R., & Park, S. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023367 · Cited by 254 · see citing works
Autophagy in the eye: Development, degeneration, and aging
Boya, P., Esteban‐Martínez, L., Serrano‐Puebla, A., Gómez‐Sintes, R., & Villarejo‐Zori, B. (2016) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2016.08.001 · Cited by 231 · see citing works
Niemann-Pick C disease and mobilization of lysosomal cholesterol by cyclodextrin
Vance, J. E., & Karten, B. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r047837 · Cited by 167 · see citing works
The ins and outs of cholesterol in the vertebrate retina
Fliesler, S. J., & Brétillon, L. (2010) · Journal of Lipid Research · doi:10.1194/jlr.r010538 · Cited by 153 · see citing works
Phagocytosis by the Retinal Pigment Epithelium: Recognition, Resolution, Recycling
Kwon, W., & Freeman, S. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604205 · Cited by 157 · see citing works
Spatial Distribution of the Pathways of Cholesterol Homeostasis in Human Retina
Zheng, W., Reem, R. E., Omarova, S., Huang, S., DiPatre, P. L., Charvet, C. D., Curcio, C. A., & Pikuleva, I. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037926 · Cited by 131 · see citing works
Chen, P. M., Gombart, Z. J., & Chen, J. W. (2011) · Cell & Bioscience · doi:10.1186/2045-3701-1-10 · Cited by 122 · see citing works
Cuenca, N., Ortuño‐Lizarán, I., & Pinilla, I. (2017) · Ophthalmology · doi:10.1016/j.ophtha.2017.09.016 · Cited by 129 · see citing works
Curcio, C. A. (2018) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-24883 · Cited by 127 · see citing works
Regulated efflux of photoreceptor outer segment-derived cholesterol by human RPE cells
Storti, F., Raphael, G., Griesser, V., Klee, K., Drawnel, F., Willburger, C., Scholz, R., Langmann, T., von Eckardstein, A., Fingerle, J., et al. (2017) · Experimental Eye Research · doi:10.1016/j.exer.2017.09.008 · Cited by 64 · see citing works
Shortened primary cilium length and dysregulated Sonic hedgehog signaling in Niemann-Pick C1 disease
Canterini, S., Dragotto, J., Dardis, A., Zampieri, S., Stefano, M. E. D., Mangia, F., Erickson, R. P., & Fiorenza, M. T. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx118 · Cited by 63 · see citing works
Autophagy in the retinal pigment epithelium: a new vision and future challenges
Intartaglia, D., Giamundo, G., & Conte, I. (2021) · FEBS Journal · doi:10.1111/febs.16018 · Cited by 62 · see citing works
Mechanism of Inflammation in Age-Related Macular Degeneration: An Up-to-Date on Genetic Landmarks
Parmeggiani, F., Sorrentino, F. S., Romano, M. R., Costagliola, C., Semeraro, F., Incorvaia, C., D’Angelo, S., Perri, P., Nadai, K. D., Roversi, E. B., et al. (2013) · Mediators of Inflammation · doi:10.1155/2013/435607 · Cited by 61 · see citing works
Cholesterol homeostasis in the vertebrate retina: biology and pathobiology
Rao, S. R., & Fliesler, S. J. (2020) · Journal of Lipid Research · doi:10.1194/jlr.tr120000979 · Cited by 61 · see citing works
Pfrieger, F. W. (2023) · Progress in Lipid Research · doi:10.1016/j.plipres.2023.101225 · Cited by 51 · see citing works
Self-citationPerusek, L., Sahu, B., Parmar, T., Maeno, H., Arai, E., Le, Y.-Z., Subauste, C. S., Chen, Y., Palczewski, K., & Maeda, A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.682310 · Cited by 41 · see citing works
Masek, M., Etard, C., Hofmann, C., Hülsmeier, A. J., Zang, J., Takamiya, M., Gesemann, M., Neuhauss, S. C. F., Hornemann, T., Strähle, U., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28982-6 · Cited by 40 · see citing works
Olfactory Deficits in Niemann-Pick Type C1 (NPC1) Disease
Hovakimyan, M., Meyer, A., Lukáš, J., Luo, J., Gudziol, V., Hummel, T. R., Rolfs, A., Wree, A., & Witt, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082216 · Cited by 39 · see citing works
Cholesterol homeostasis regulated by ABCA1 is critical for retinal ganglion cell survival
Yang, J., Chen, Y., Zou, T., Bai, X., Yang, F., Wang, X., Huo, Y., Yan, B., Xu, Y., He, S., et al. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2126-2 · Cited by 38 · see citing works
Lacritin and other autophagy associated proteins in ocular surface health
Karnati, R., Talla, V., Peterson, K. M., & Laurie, G. W. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.08.015 · Cited by 37 · see citing works
Bräuer, A. U., Kuhla, A., Holzmann, C., Wree, A., & Witt, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184392 · Cited by 36 · see citing works
Membrane trafficking in the retinal pigment epithelium at a glance
Storm, T., Burgoyne, T., & Futter, C. E. (2020) · Journal of Cell Science · doi:10.1242/jcs.238279 · Cited by 34 · see citing works
Understanding and Treating Niemann–Pick Type C Disease: Models Matter
Pallottini, V., & Pfrieger, F. W. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21238979 · Cited by 34 · see citing works
Self-citationRole of retinal pigment epithelium in age-related macular disease: a systematic review
Bird, A. C. (2020) · British Journal of Ophthalmology · doi:10.1136/bjophthalmol-2020-317447 · Cited by 33 · see citing works
Mercer, A. J., Szalewski, R. J., Jackman, S. L., Hook, M. J. V., & Thoreson, W. B. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00779.2011 · Cited by 33 · see citing works
Retinal thinning in Gaucher disease patients and carriers: Results of a pilot study
McNeill, A., Roberti, G., Lascaratos, G., Hughes, D. A., Mehta, A. B., Garway‐Heath, D. F., & Schapira, A. H. V. (2013) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2013.04.001 · Cited by 32 · see citing works
Ramachandra Rao, S., Pfeffer, B. A., Más Gómez, N., Skelton, L. A., Keiko, U., Sparrow, J. R., Rowsam, A. M., Mitchell, C. H., & Fliesler, S. J. (2018) · Autophagy · doi:10.1080/15548627.2018.1490851 · Cited by 28 · see citing works
Fourgeux, C., Martine, L., Acar, N., Bron, A. M., Creuzot-Garcher, C. P., & Brétillon, L. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.01.118 · Cited by 28 · see citing works
Demais, V., Barthelemy, A., Perraut, M., Ungerer, N., Keime, C., Reibel, S., & Pfrieger, F. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0900-16.2016 · Cited by 28 · see citing works
Self-citationOrigin of Retinal Oscillatory Potentials in the Mouse, a Tool to Specifically Locate Retinal Damage
Liao, F., Liu, H., Navarro, S. M., de la Villa, P., & Germaín, F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043126 · Cited by 24 · see citing works
Retinal axonal degeneration in Niemann–Pick type C disease
Havla, J. B., Moser, M., Sztatecsny, C., Lotz-Havla, A. S., Maier, E. M., Hizli, B., Schinner, R., Kümpfel, T., Strupp, M. L., Brémovà-Ertl, T., et al. (2020) · Journal of Neurology · doi:10.1007/s00415-020-09796-2 · Cited by 23 · see citing works
Dinkel, L., Hummel, S., Zenatti, V., Malara, M., Tillmann, Y., Colombo, A., Monasor, L. S., Suh, J. H., Logan, T., Roth, S., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adl4616 · Cited by 22 · see citing works
Hindle, S. J., Hebbar, S., Schwudke, D., Elliott, C. J. H., & Sweeney, S. T. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.11.012 · Cited by 22 · see citing works
Palladino, G., Loizzo, S., Fortuna, A., Canterini, S., Palombi, F., Erickson, R. P., Mangia, F., & Fiorenza, M. T. (2015) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-015-0348-0 · Cited by 22 · see citing works
Defects in the retina of Niemann-pick type C 1 mutant mice
Yan, X., Ma, L. X., Hovakimyan, M., Lukáš, J., Wree, A., Frank, M., Guthoff, R. F., Rolfs, A., Witt, M., & Luo, J. (2014) · BMC Neuroscience · doi:10.1186/s12868-014-0126-2 · Cited by 19 · see citing works
Meyer, A., Gläser, A., Bräuer, A. U., Wree, A., Strotmann, J. M., Rolfs, A., & Witt, M. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00035 · Cited by 18 · see citing works
Marshall, C. A., Watkins‐Chow, D. E., Palladino, G., Deutsch, G. H., Chandran, K., Pavan, W. J., & Erickson, R. P. (2017) · Gene · doi:10.1016/j.gene.2017.12.006 · Cited by 18 · see citing works
Fourgeux, C., Bron, A. M., Acar, N., Creuzot-Garcher, C. P., & Brétillon, L. (2011) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2011.04.006 · Cited by 17 · see citing works
Neßlauer, A.-M., Gläser, A., Gräler, M. H., Engelmann, R., Müller‐Hilke, B., Frank, M., Burstein, C., Rolfs, A., Neidhardt, J., Wree, A., et al. (2019) · Lipids in Health and Disease · doi:10.1186/s12944-019-1088-2 · Cited by 17 · see citing works
Relevance of neuronal and glial NPC1 for synaptic input to cerebellar Purkinje cells
Buard, I., & Pfrieger, F. W. (2014) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2014.06.003 · Cited by 16 · see citing works
Self-citationGaspar, J., Mathieu, J., & Alvarez, P. J. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-02387-8 · Cited by 16 · see citing works
Contribution of Membrane Trafficking Perturbation to Retinal Toxicity
Khoh‐Reiter, S., Sokolowski, S. A., Jessen, B. A., Evans, M. G., Dalvie, D., & Lu, S. (2015) · Toxicological Sciences · doi:10.1093/toxsci/kfv059 · Cited by 15 · see citing works
Fernández-Navarro, J., Aldea, P., de Hoz, R., Salazar, J. J., Ramirez, A. I., Rojas, B., Gallego, B., Triviño, A., Tejerina, T., & Ramirez, J. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154800 · Cited by 15 · see citing works
Endoplasmic reticulum stress and the protein degradation system in ophthalmic diseases
Song, J., Wang, X.-G., Zhang, Z.-Y., Che, L., Fan, B., & Li, G. (2020) · PeerJ · doi:10.7717/peerj.8638 · Cited by 12 · see citing works
Cholesterol and oxysterols in retinal neuron-glia interactions: relevance for glaucoma
Masson, E., Serrano, J., Léger-Charnay, E., & Acar, N. (2024) · Frontiers in Ophthalmology · doi:10.3389/fopht.2023.1303649 · Cited by 11 · see citing works
Barthelemy, A., Demais, V., Stancu, I., Vasile, E., Houben, T., Reber, M., Pallottini, V., Perraut, M., Reibel, S., & Pfrieger, F. W. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105469 · Cited by 9 · see citing works
Self-citationEndo-Lysosome Function in the Retinal Pigment Epithelium in Health and Disease
Lakkaraju, A. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0631-0_92 · Cited by 9 · see citing works
Main Olfactory and Vomeronasal Epithelium Are Differently Affected in Niemann-Pick Disease Type C1
Witt, M., Thiemer, R., Meyer, A., Schmitt, O., & Wree, A. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113563 · Cited by 8 · see citing works
Li, J. K., Rao, Y. Q., Koh, S. K., Zhao, P., Zhou, L., & Li, J. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.965943 · Cited by 7 · see citing works
Hovakimyan, M., Petersen, J., Maass, F., Reichard, M., Witt, M., Lukáš, J., Stachs, O., Guthoff, R. F., Rolfs, A., & Wree, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028418 · Cited by 7 · see citing works
Landowski, M., Gogoi, P., Ikeda, S., & Ikeda, A. (2024) · Frontiers in Ophthalmology · doi:10.3389/fopht.2024.1355379 · Cited by 6 · see citing works
The Lysosome in Aging‐Related Neurodegenerative Diseases
Nixon, R. A. (2016) · Wiley eBooks · doi:10.1002/9781118978320.ch9 · Cited by 5 · see citing works
NPC1 plays a role in the trafficking of specific cargo to melanosomes
Rus, A. A., Militaru, I. V., Popa, I., Munteanu, C. V. A., Sima, L. E., Platt, N., Platt, F. M., & Petrescu, S. M. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105024 · Cited by 4 · see citing works
Molecular Genetics and Metabolism
McNeill, A., Roberti, G., Lascaratos, G., Hughes, D. A., Mehta, A. B., Garway‐Heath, D. F., & Schapira, A. H. V. (2013) · Cited by 4 · see citing works
Vertical saccadic palsy and foveal retinal thinning in Niemann-Pick disease type C
Hopf, S., Hennermann, J. B., Schuster, A. K.-G., Pfeiffer, N., & Pitz, S. (2021) · PLoS ONE · doi:10.1371/journal.pone.0252825 · Cited by 4 · see citing works
Emri, E., Cappa, O., Kelly, C., Körtvely, E., SanGiovanni, J. P., McKay, B. S., Bergen, A. A. B., Simpson, D. A. C., & Lengyel, I. (2023) · Cells · doi:10.3390/cells12050773 · Cited by 3 · see citing works
Shahrivar, R. Y., Karami, F., & Karami, E. (2025) · PLoS ONE · doi:10.1371/journal.pone.0319401 · Cited by 3 · see citing works
Fourgeux, C., Martine, L., Gambert, S., Bron, A. M., Creuzot-Garcher, C. P., & Brétillon, L. (2015) · OCL · doi:10.1051/ocl/2014056 · Cited by 3 · see citing works
Onur, İ. U., Asula, M. F., Ekinci, C., & Mert, M. (2018) · International Ophthalmology · doi:10.1007/s10792-018-0939-6 · Cited by 3 · see citing works
Stathopoulos, A., Wang, J. J., Martin, S. F., & Zhang, S. X. (2025) · Biomolecules · doi:10.3390/biom15091228 · Cited by 2 · see citing works
AUTOPHAGY IN THE RETINA: DEVELOPMENT, PHYSIOLOGY AND PATHOLOGY
Boya, P. (2012) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814350457_0007 · Cited by 1 · see citing works
Autophagy in Ocular Pathophysiology
Mitter, S. K., & Boulton, M. E. (2016) · InTech eBooks · doi:10.5772/64667 · Cited by 1 · see citing works
Lysosome Dysfunction: An Emerging Mechanism of Xenobiotic‐Induced Toxicity
Lu, S., Jessen, B. A., Will, Y., & Stevens, G. (2016) · Wiley eBooks · doi:10.1002/9781118978320.ch19 · Cited by 1 · see citing works
Optimisation of protocols for detection of free cholesterol and Niemann-Pick type C 1 and 2 protein
Scott, L. (2010) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Fourgeux, C., Martine, L., Gambert, S., Bron, A. M., Creuzot-Garcher, C. P., & Brétillon, L. (2015) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2015.04.003
Movassagh, M. J., Mudvari, P., Kokkinaki, M., Edwards, N. J., Golestaneh, N., & Horvath, A. (2014) · Journal of Clinical Bioinformatics · doi:10.1186/2043-9113-4-14
Mercer, A. J. (2011) · DigitalCommons@UNMC
Cellular Organization of the Retinal Pigment Epithelium
Burgoyne, T., & Futter, C. E. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13820-1.00067-0
Léger-Charnay, E. (2019) · theses.fr (ABES) · doi:10.70675/72ca31b1zc2d8z41dbz9f66zcbe3f38a8b4a
The role of autophagy in ocular health: mechanisms, pathologies, and therapeutic strategies
Huang, M., Lin, Y., (25820), H. Z., Yuan, R., Zeng, L., Li, S., Yang, Q., Gong, M., Xiao, R., Jia, P., et al. (2026) · Biology Direct · doi:10.1186/s13062-026-00821-4
- Authors
- Claudepierre, T., Paques, M., Simonutti, M., Buard, I., Sahel, J., Maue, R. A., Picaud, S., & Pfrieger, F. W.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institut de la Vision (FR)
- Dartmouth College (US)
- Corresponding author
- Pfrieger, Frank W.
- Venue
- Molecular and Cellular Neuroscience
- Publisher
- Elsevier BV
- Published
- 2010-01
- Volume
- 43
- Issue
- 1
- Pages
- 164-176
- ISSN
- 1044-7431 (ISSN-L)
- OpenAlex
- W1998015808
- Cited by
- 77
- References
- 80
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 11 · 2019: 3 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 6 · 2014: 6 · 2013: 4 · 2012: 3
- FWCI
- 2.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular and Cellular Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Dartmouth College
- Topics
- Health Sciences › Medicine › Physiology › Lysosomal Storage Disorders Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- Niemann-Pick disease type C, NPC1, NPC2, retinal degeneration, age-related maculopathy, lipofuscin accumulation, retinal pigment epithelium, photoreceptor outer segments, retinal ganglion cells, autophagy, visual function, lysosomal storage disease, mouse model
- MeSH terms
- Niemann-Pick C1 Protein, Animals, Autophagy, Cholesterol, Electroretinography, Macular Degeneration, Mice, Inbred BALB C, Nerve Degeneration, Phagosomes, Proteins, Retina, Mice, Knockout, Intracellular Signaling Peptides and Proteins, Mice, Niemann-Pick Disease, Type C
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