Autophagy protects the retina from light-induced degeneration

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7506-7518

  Chen, Yu ^a,b   Sawada, Osamu ^a   Kohno, Hideo ^a   Le, Yun Zheng ^c   Subauste, Carlos ^a   Maeda, Tadao ^a   Maeda, Akiko ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; ENDOPLASMIC RETICULUM; INTRACELLULAR DEGRADATION; LIGHT ILLUMINATION; PHOTO-ACTIVATED; PHOTORECEPTOR CELL; RETINAL DEGENERATIONS; ROD PHOTORECEPTORS;

CELL DEATH; CELL MEMBRANES; CHEMICAL ACTIVATION; CHROMOPHORES; GENES; MAMMALS; MITOCHONDRIA; OPHTHALMOLOGY; TRANSCRIPTION FACTORS; VISION;

ALDEHYDES;

ACTIVATING TRANSCRIPTION FACTOR 4; BECLIN 1; CELL PROTEIN; LC3B II PROTEIN; PROTEIN PARK2; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; AUTOPHAGY RELATED GENE 7; BECLIN 1 GENE; CELL SURVIVAL; CELL ULTRASTRUCTURE; CHROMATOPHORE; CONTROLLED STUDY; GENE; HUMAN; HUMAN CELL; LIGHT EXPOSURE; MITOPHAGY; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; ORGANELLE SHAPE; OXIDATIVE STRESS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RETINA CELL; RETINA DEGENERATION;

ALCOHOL DEHYDROGENASE; ALCOHOL OXIDOREDUCTASES; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; AUTOPHAGY; CELL DEATH; CELL LINE; HUMANS; LIGHT; LYSOSOMES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; PHOTIC STIMULATION; RETINA; RETINAL DEGENERATION; RHODOPSIN; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; VITAMIN A;

EID: 84875124248     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.439935     Document Type: Article

References (41)

1. Yang, Z., and Klionsky, D. J. (2010) Eaten alive. A history of macroautophagy. Nat. Cell Biol. 12, 814-822
2. Pickford, F., Masliah, E., Britschgi, M., Lucin, K., Narasimhan, R., Jaeger, P. A., Small, S., Spencer, B., Rockenstein, E., Levine, B., and Wyss-Coray, T. (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. J. Clin. Invest. 118, 2190-2199
3. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., and Mizushima, N. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889
4. Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N., Ohsumi, Y., Uchiyama, Y., Kominami, E., Tanaka, K., and Chiba, T. (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434
5. Mizushima, N., and Komatsu, M. (2011) Autophagy. Renovation of cells and tissues. Cell 147, 728-741
6. Remé, C. E., and Young, R. W. (1977) The effects of hibernation on cone visual cells in the ground squirrel. Invest. Ophthalmol. Vis. Sci. 16, 815-840
7. Remé, C. E., Wolfrum, U., Imsand, C., Hafezi, F., and Williams, T. P. (1999) Photoreceptor autophagy. Effects of light history on number and opsin content of degradative vacuoles. Invest. Ophthalmol. Vis. Sci. 40, 2398-2404
8. von Lintig, J., Kiser, P. D., Golczak, M., and Palczewski, K. (2010) The biochemical and structural basis for trans-to-cis isomerization of retinoids in the chemistry of vision. Trends Biochem. Sci. 35, 400-410
9. Maeda, A., Maeda, T., Golczak, M., and Palczewski, K. (2008) Retinopathy in mice induced by disrupted all-trans-retinal clearance. J. Biol. Chem. 283, 26684-26693
10. Portillo, J. A., Okenka, G., Reed, E., Subauste, A., Van Grol, J., Gentil, K., Komatsu, M., Tanaka, K., Landreth, G., Levine, B., and Subauste, C. S. (2010) The CD40-autophagy pathway is needed for host protection despite IFN-γ-dependent immunity and CD40 induces autophagy via control of P21 levels. PloS ONE 5, e14472
11. Le, Y. Z., Zheng, L., Zheng, W., Ash, J. D., Agbaga, M. P., Zhu, M., and Anderson, R. E. (2006) Mouse opsin promoter-directed Cre recombinase expression in transgenic mice. Mol. Vis. 12, 389-398
12. Wenzel, A., Reme, C. E., Williams, T. P., Hafezi, F., and Grimm, C. (2001) The Rpe65 L450M variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J. Neurosci. 21, 53-58
13. Mattapallil, M. J., Wawrousek, E. F., Chan, C. C., Zhao, H., Roychoudhury, J., Ferguson, T. A., and Caspi, R. R. (2012) 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. 53, 2921-2927
14. Chen, Y., Okano, K., Maeda, T., Chauhan, V., Golczak, M., Maeda, A., and Palczewski, K. (2012) Mechanism of all-trans-retinal toxicity with implications for stargardt disease and age-related macular degeneration. J. Biol. Chem. 287, 5059-5069
15. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J. D., Zhang, H., Zhu, L., Sun, W., Saperstein, D. A., Rieke, F., Baehr, W., and Palczewski, K. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem. 280, 18822-18832
16. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
17. Maeda, A., Maeda, T., Golczak, M., Chou, S., Desai, A., Hoppel, C. L., Matsuyama, S., and Palczewski, K. (2009) Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J. Biol. Chem. 284, 15173-15183
18. Lange, P. S., Chavez, J. C., Pinto, J. T., Coppola, G., Sun, C. W., Townes, T. M., Geschwind, D. H., and Ratan, R. R. (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J. Exp. Med. 205, 1227-1242
19. Maeda, A., Golczak, M., Maeda, T., and Palczewski, K. (2009) Limited roles of Rdh8, Rdh12, and Abca4 in all-trans-retinal clearance in mouse retina. Invest. Ophthalmol. Vis. Sci. 50, 5435-5443
20. Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E. L., Mizushima, N., Ohsumi, Y., Cattoretti, G., and Levine, B. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820
21. Yue, Z., Jin, S., Yang, C., Levine, A. J., and Heintz, N. (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 100, 15077-15082
22. Okano, K., Maeda, A., Chen, Y., Chauhan, V., Tang, J., Palczewska, G., Sakai, T., Tsuneoka, H., Palczewski, K., and Maeda, T. (2012) Retinal cone and rod photoreceptor cells exhibit differential susceptibility to light-induced damage. J. Neurochem. 121, 146-156
23. Holz, F. G., Gross-Jendroska, M., Eckstein, A., Hogg, C. R., Arden, G. B., and Bird, A. C. (1995) Colour contrast sensitivity in patients with agerelated Bruch's membrane changes. Ger. J. Ophthalmol. 4, 336-341
24. Shelley, E. J., Madigan, M. C., Natoli, R., Penfold, P. L., and Provis, J. M. (2009) Cone degeneration in aging and age-related macular degeneration. Arch. Ophthalmol. 127, 483-492
25. Jeon, C. J., Strettoi, E., and Masland, R. H. (1998) The major cell populations of the mouse retina. J. Neurosci. 18, 8936-8946
26. Youle, R. J., and Narendra, D. P. (2011) Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14
27. Dagda, R. K., Cherra, S. J., 3rd, Kulich, S. M., Tandon, A., Park, D., and Chu, C. T. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 284, 13843-13855
28. Esteve-Rudd, J., Campello, L., Herrero, M. T., Cuenca, N., and Martín-Nieto, J. (2010) Expression in the mammalian retina of parkin and UCHL1, two components of the ubiquitin-proteasome system. Brain Res. 1352, 70-82
29. Parish, C. A., Hashimoto, M., Nakanishi, K., Dillon, J., and Sparrow, J. (1998) Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc. Natl. Acad. Sci. U.S.A. 95, 14609-14613
30. Sparrow, J. R. (2010) Bisretinoids of RPE lipofuscin. Trigger for complement activation in age-related macular degeneration. Adv. Exp. Med. Biol. 703, 63-74
31. Maeda, A., Golczak, M., Chen, Y., Okano, K., Kohno, H., Shiose, S., Ishikawa, K., Harte, W., Palczewska, G., Maeda, T., and Palczewski, K. (2012) Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat. Chem. Biol. 8, 170-178
32. Aita, V. M., Liang, X. H., Murty, V. V., Pincus, D. L., Yu, W., Cayanis, E., Kalachikov, S., Gilliam, T. C., and Levine, B. (1999) Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59, 59-65
33. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676
34. Lee, I. H., Kawai, Y., Fergusson, M. M., Rovira, I. I., Bishop, A. J., Motoyama, N., Cao, L., and Finkel, T. (2012) Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science 336, 225-228
35. Oren, M. (2003) Decision making by p53. Life, death, and cancer. Cell Death Differ. 10, 431-442
36. Chipuk, J. E., Kuwana, T., Bouchier-Hayes, L., Droin, N. M., Newmeyer, D. D., Schuler, M., and Green, D. R. (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303, 1010-1014
37. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., Shen, J., Cookson, M. R., and Youle, R. J. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298
38. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803
39. Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y. L., Selkoe, D., Rice, S., Steen, J., LaVoie, M. J., and Schwarz, T. L. (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147, 893-906
40. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608
41. Palacino, J. J., Sagi, D., Goldberg, M. S., Krauss, S., Motz, C., Wacker, M., Klose, J., and Shen, J. (2004) Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J. Biol. Chem. 279, 18614-18622