All-trans-retinal induces Bax activation via DNA damage to mediate retinal cell apoptosis

Experimental Eye Research

Volumn 123, Issue , 2014, Pages 27-36

  Sawada, Osamu ^a,b   Perusek, Lindsay ^a   Kohno, Hideo ^a,c   Howell, Scott J ^a   Maeda, Akiko ^a   Matsuyama, Shigemi ^a   Maeda, Tadao ^a  

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

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

All trans retinal; Apoptosis; Bcl 2 associated protein; DNA damage; Oxidative stress; P53; Retina; Visual cycle

Indexed keywords

LACTATE DEHYDROGENASE; PROTEIN BAX; PROTEIN P53; RETINAL;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; DNA DAMAGE; ENZYME ACTIVATION; IMMUNOCHEMISTRY; IN VITRO STUDY; LIGHT EXPOSURE; MOUSE; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RETINA CELL; RETINA DEGENERATION; RETINA NEUROEPITHELIAL LAYER;

ALL-TRANS-RETINAL; APOPTOSIS; BCL-2-ASSOCIATED × PROTEIN; DNA DAMAGE; OXIDATIVE STRESS; P53; RETINA; VISUAL CYCLE;

ALCOHOL OXIDOREDUCTASES; ANIMALS; APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; COLORIMETRY; DEOXYGUANOSINE; DISEASE MODELS, ANIMAL; DNA DAMAGE; GENE DELETION; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; L-LACTATE DEHYDROGENASE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; RETINA; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; RETINALDEHYDE; TOMOGRAPHY, OPTICAL COHERENCE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84899835220     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.04.003     Document Type: Article

References (47)

1. al-Ubaidi M.R., Font R.L., Quiambao A.B., Keener M.J., Liou G.I., Overbeek P.A., Baehr W. Bilateral retinal and brain tumors in transgenic mice expressing simian virus 40 large T antigen under control of the human interphotoreceptor retinoid-binding protein promoter. J.Cell Biol. 1992, 119:1681-1687.
2. Allikmets R. Further evidence for an association of ABCR alleles with age-related macular degeneration. The International ABCR Screening Consortium. Am. J. Hum. Genet. 2000, 67:487-491.
3. Allikmets R., Shroyer N.F., Singh N., Seddon J.M., Lewis R.A., Bernstein P.S., Peiffer A., Zabriskie N.A., Li Y., Hutchinson A., Dean M., Lupski J.R., Leppert M. Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 1997, 277:1805-1807.
4. Benchimol S. p53-dependent pathways of apoptosis. Cell Death Differ. 2001, 8:1049-1051.
5. Bishayee K., Paul A., Ghosh S., Sikdar S., Mukherjee A., Biswas R., Boujedaini N., Khuda-Bukhsh A.R. Condurango-glycoside-A fraction of Gonolobus condurango induces DNA damage associated senescence and apoptosis via ROS-dependent p53 signalling pathway in HeLa cells. Mol. Cell. Biochem. 2013, 382:173-183.
6. Bordone M.P., Lanzani M.F., Lopez-Costa J.J., Chianelli M.S., Franco P., Saenz D.A., Rosenstein R.E. Bacterial lipopolysaccharide protects the retina from light-induced damage. J.Neurochem. 2012, 122:392-403.
7. Cabon L., Galan-Malo P., Bouharrour A., Delavallee L., Brunelle-Navas M.N., Lorenzo H.K., Gross A., Susin S.A. BID regulates AIF-mediated caspase-independent necroptosis by promoting BAX activation. Cell Death Differ. 2012, 19:245-256.
8. Chen Y., Okano K., Maeda T., Chauhan V., Golczak M., Maeda A., Palczewski K. Mechanism of all-trans-retinal toxicity with implications for stargardt disease and age-related macular degeneration. J.Biol. Chem. 2012, 287:5059-5069.
9. Chen Y., Palczewska G., Mustafi D., Golczak M., Dong Z., Sawada O., Maeda T., Maeda A., Palczewski K. Systems pharmacology identifies drug targets for Stargardt disease-associated retinal degeneration. J.Clin. Investig. 2013, 123:5119-5134.
10. Chen Y., Sawada O., Kohno H., Le Y.Z., Subauste C., Maeda T., Maeda A. Autophagy protects the retina from light-induced degeneration. J.Biol. Chem. 2013, 288:7506-7518.
11. -/- mouse model of Leber's congenital amaurosis. Apoptosis 2008, 13:329-342.
12. Cottet S., Schorderet D.F. Mechanisms of apoptosis in retinitis pigmentosa. Curr. Mol. Med. 2009, 9:375-383.
13. Cremers F.P., van de Pol D.J., van Driel M., den Hollander A.I., van Haren F.J., Knoers N.V., Tijmes N., Bergen A.A., Rohrschneider K., Blankenagel A., Pinckers A.J., Deutman A.F., Hoyng C.B. Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt's disease gene ABCR. Hum. Mol. Genet. 1998, 7:355-362.
14. Czabotar P.E., Colman P.M., Huang D.C. Bax activation by Bim?. Cell Death Differ. 2009, 16:1187-1191.
15. Dong K., Zhu H., Song Z., Gong Y., Wang F., Wang W., Zheng Z., Yu Z., Gu Q., Xu X., Sun X. Necrostatin-1 protects photoreceptors from cell death and improves functional outcome after experimental retinal detachment. Am. J. Pathol. 2012, 181:1634-1641.
16. Garaycoechea J.I., Crossan G.P., Langevin F., Daly M., Arends M.J., Patel K.J. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 2012, 489:571-575.
17. Gomez J.A., Gama V., Yoshida T., Sun W., Hayes P., Leskov K., Boothman D., Matsuyama S. Bax-inhibiting peptides derived from Ku70 and cell-penetrating pentapeptides. Biochem. Soc. Trans. 2007, 35:797-801.
18. Hahn P., Lindsten T., Lyubarsky A., Ying G.S., Pugh E.N., Thompson C.B., Dunaief J.L. Deficiency of Bax and Bak protects photoreceptors from light damage invivo. Cell Death Differ. 2004, 11:1192-1197.
19. Hahn P., Lindsten T., Ying G.S., Bennett J., Milam A.H., Thompson C.B., Dunaief J.L. Proapoptotic bcl-2 family members, Bax and Bak, are essential for developmental photoreceptor apoptosis. Investig. Ophthalmol. Vis. Sci. 2003, 44:3598-3605.
20. Hamann S., Schorderet D.F., Cottet S. Bax-induced apoptosis in Leber's congenital amaurosis: a dual role in rod and cone degeneration. PLoS One 2009, 4:e6616.
21. Jia L., Liu Z., Sun L., Miller S.S., Ames B.N., Cotman C.W., Liu J. Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: protection by (R)-alpha-lipoic acid. Investig. Ophthalmol. Vis. Sci. 2007, 48:339-348.
22. Jurgensmeier J.M., Xie Z., Deveraux Q., Ellerby L., Bredesen D., Reed J.C. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4997-5002.
23. Kim R., Emi M., Tanabe K., Murakami S., Uchida Y., Arihiro K. Regulation and interplay of apoptotic and non-apoptotic cell death. J.Pathol. 2006, 208:319-326.
24. Kralova J., Dvorak M., Koc M., Kral V. p38 MAPK plays an essential role in apoptosis induced by photoactivation of a novel ethylene glycol porphyrin derivative. Oncogene 2008, 27:3010-3020.
25. Li Y., Yokota T., Gama V., Yoshida T., Gomez J.A., Ishikawa K., Sasaguri H., Cohen H.Y., Sinclair D.A., Mizusawa H., Matsuyama S. Bax-inhibiting peptide protects cells from polyglutamine toxicity caused by Ku70 acetylation. Cell Death Differ. 2007, 14:2058-2067.
26. Lu Z., Xu S. ERK1/2 MAP kinases in cell survival and apoptosis. IUBMB Life 2006, 58:621-631.
27. Maeda A., Golczak M., Chen Y., Okano K., Kohno H., Shiose S., Ishikawa K., Harte W., Palczewska G., Maeda T., Palczewski K. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat. Chem. Biol. 2012, 8:170-178.
28. Maeda A., Maeda T., Golczak M., Chou S., Desai A., Hoppel C.L., Matsuyama S., Palczewski K. Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J.Biol. Chem. 2009, 284:15173-15183.
29. Maeda A., Maeda T., Golczak M., Palczewski K. Retinopathy in mice induced by disrupted all-trans-retinal clearance. J.Biol. Chem. 2008, 283:26684-26693.
30. 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., Palczewski K. Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle invivo. J.Biol. Chem. 2005, 280:18822-18832.
31. Maeda A., Maeda T., Imanishi Y., Sun W., Jastrzebska B., Hatala D.A., Winkens H.J., Hofmann K.P., Janssen J.J., Baehr W., Driessen C.A., Palczewski K. Retinol dehydrogenase (RDH12) protects photoreceptors from light-induced degeneration in mice. J.Biol. Chem. 2006, 281:37697-37704.
32. Maeda A., Maeda T., Sun W., Zhang H., Baehr W., Palczewski K. Redundant and unique roles of retinol dehydrogenases in the mouse retina. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19565-19570.
33. Maeda T., Lem J., Palczewski K., Haeseleer F. Acritical role of CaBP4 in the cone synapse. Investig. Ophthalmol. Vis. Sci. 2005, 46:4320-4327.
34. Martinez-Mir A., Paloma E., Allikmets R., Ayuso C., del Rio T., Dean M., Vilageliu L., Gonzalez-Duarte R., Balcells S. Retinitis pigmentosa caused by a homozygous mutation in the Stargardt disease gene ABCR. Nat. Genet. 1998, 18:11-12.
35. Molday R.S. ATP-binding cassette transporter ABCA4: molecular properties and role in vision and macular degeneration. J.Bioenerg. Biomembr. 2007, 39:507-517.
36. Murakami Y., Miller J.W., Vavvas D.G. RIP kinase-mediated necrosis as an alternative mechanisms of photoreceptor death. Oncotarget 2011, 2:497-509.
37. Nickell S., Park P.S., Baumeister W., Palczewski K. Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J.Cell Biol. 2007, 177:917-925.
38. Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000, 102:849-862.
39. Palczewski K. Retinoids for treatment of retinal diseases. Trends Pharmacol. Sci. 2010, 31:284-295.
40. Smeenk L., van Heeringen S.J., Koeppel M., Gilbert B., Janssen-Megens E., Stunnenberg H.G., Lohrum M. Role of p53 serine 46 in p53 target gene regulation. PLoS One 2011, 6:e17574.
41. Travis G.H., Golczak M., Moise A.R., Palczewski K. Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu. Rev. Pharm. Toxicol. 2007, 47:469-512.
42. Trichonas G., Murakami Y., Thanos A., Morizane Y., Kayama M., Debouck C.M., Hisatomi T., Miller J.W., Vavvas D.G. Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21695-21700.
43. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J.Cell Biol. 1997, 139:1281-1292.
44. Wu B.X., Moiseyev G., Chen Y., Rohrer B., Crouch R.K., Ma J.X. Identification of RDH10, an all-trans retinol dehydrogenase, in retinal Muller cells. Investig. Ophthalmol. Vis. Sci. 2004, 45:3857-3862.
45. Xu Y. Regulation of p53 responses by post-translational modifications. Cell Death Differ. 2003, 10:400-403.
46. Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., Dong M.Q., Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325:332-336.
47. Zhang L., Salom D., He J., Okun A., Ballesteros J., Palczewski K., Li N. Expression of functional G protein-coupled receptors in photoreceptors of transgenic Xenopus laevis. Biochemistry 2005, 44:14509-14518.