Ataxin-1 poly(Q)-induced proteotoxic stress and apoptosis are attenuated in neural cells by docosahexaenoic acid-derived neuroprotectin D1

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23726-23739

  Calandria, Jorgelina M ^a   Mukherjee, Pranab K ^a   De Rivero Vaccari, Juan Carlos ^a   Zhu, Min ^b   Petasis, Nicos A ^b   Bazan, Nicolas G ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURVIVAL; CELLULAR MODEL; DOCOSAHEXAENOIC ACID; NEURAL CELLS; POLYGLUTAMINE; PROTEIN EXPRESSIONS; PROTEIN MISFOLDING; PROTEOTOXIC STRESS; RETINAL PIGMENT EPITHELIAL; RPE CELL; SIGNALING PATHWAYS; UBIQUITIN;

BIOSYNTHESIS; GENE EXPRESSION; PHOSPHORYLATION; PROTEINS; STABILIZATION; UNSATURATED FATTY ACIDS;

CELL DEATH;

ARACHIDONATE 15 LIPOXYGENASE; ATAXIN 1; DOCOSAHEXAENOIC ACID; NEUROPROTECTIN D1; PIGMENT EPITHELIUM DERIVED FACTOR; POLYGLUTAMINE; PROTEIN BAX; PROTEIN KINASE B; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL DEATH; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INFLAMMATION; NERVE CELL; NEUROPROTECTION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACIDS; GREEN FLUORESCENT PROTEINS; HUMANS; LUCIFERASES; MICROSCOPY, FLUORESCENCE; MUTATION; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PEPTIDES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RETINAL PIGMENT EPITHELIUM; STRESS, PHYSIOLOGICAL; TRANSFECTION;

EID: 84863614157     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.287078     Document Type: Article

References (49)

1. Shaw, C. A., and Höglinger, G. U. (2008) Neurodegenerative diseases. Neurotoxins as sufficient etiologic agents? Neuromolecular Med. 10, 1-9
2. Kalaria, R. N. (2010) Vascular basis for brain degeneration. Faltering controls and risk factors for dementia. Nutr. Rev. 68, S74-S87
3. Khusnutdinova, E., Gilyazova, I., Ruiz-Pesini, E., Derbeneva, O., Khusainova, R., Khidiyatova, I., Magzhanov, R., and Wallace, D. C. (2008) A mitochondrial etiology of neurodegenerative diseases. Evidence from Parkinson's disease. Ann. N.Y. Acad. Sci. 1147, 1-20
4. Cummings, C. J., Mancini, M. A., Antalffy, B., DeFranco, D. B., Orr, H. T., and Zoghbi, H. Y. (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19, 148-154 (Pubitemid 28248795)
5. Kaytor, M. D., and Warren, S. T. (1999) Aberrant protein deposition and neurological disease. J. Biol. Chem. 274, 37507-37510 (Pubitemid 30026802)
6. Dikshit, P., and Jana, N. R. (2008) Role of ubiquitin protein ligases in the pathogenesis of polyglutamine diseases. Neurochem. Res. 33, 945-951
7. de Chiara, C., Menon, R. P., Strom, M., Gibson, T. J., and Pastore, A. (2009) Phosphorylation of Ser-776 and 14-3-3 binding modulate ataxin-1 interaction with splicing factors. PLoS One. 4, e8372
8. Zoghbi, H. Y., and Orr, H. T. (2009) Pathogenic mechanisms of a polyglutamine-mediated neurodegenerative disease, spinocerebellar ataxia type 1. J. Biol. Chem. 284, 7425-7429
9. Abe, T., Abe, K., Aoki, M., Itoyama, Y., and Tamai, M. (1997) Ocular changes in patients with spinocerebellar degeneration and repeated trinucleotide expansion of spinocerebellar ataxia type 1 gene. Arch. Ophthalmol. 115, 231-236 (Pubitemid 27083796)
10. Isashiki, Y., Kii, Y., Ohba, N., and Nakagawa, M. (2001) Retinopathy associated with Machado-Joseph disease (spinocerebellar ataxia 3) with CAG trinucleotide repeat expansion. Am. J. Ophthalmol. 131, 808-810 (Pubitemid 32522660)
11. Saito, Y., Matsumura, K., Shimizu, S., Ichikawa, Y., Ochiai, K., Goto, J., Tsuji, S., and Shimizu, T. (2006) J. Neurol. Neurosurg. Psychiatry 77, 1293-1294
12. Liu, X., Garriga, P., and Khorana, H. G. (1996) Structure and function in rhodopsin. Correct folding and misfolding in two point mutants in the intradiscal domain of rhodopsin identified in retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 93, 4554-4559 (Pubitemid 26162800)
13. Saliba, R. S., Munro, P. M., Luthert, P. J., and Cheetham, M. E. (2002) The cellular fate of mutant rhodopsin. Quality control, degradation, and aggresome formation. J. Cell Sci. 115, 2907-2918
14. Mendes, H. F., van der Spuy, J., Chapple, J. P., and Cheetham, M. E. (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa. Implications for therapy. Trends Mol. Med. 11, 177-185
15. Tam, B. M., and Moritz, O. L. (2006) Characterization of rhodopsin P23Hinduced retinal degeneration in a Xenopus laevis model of retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 47, 3234-3241 (Pubitemid 351639681)
16. Balch, W. E., Morimoto, R. I., Dillin, A., and Kelly, J. W. (2008) Adapting proteostasis for disease intervention. Science 319, 916-919 (Pubitemid 351263754)
17. Morimoto, R. I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438
18. Thomas, M., Yu, Z., Dadgar, N., Varambally, S., Yu, J., Chinnaiyan, A. M., and Lieberman, A. P. (2005) The unfolded protein response modulates toxicity of the expanded glutamine androgen receptor. J. Biol. Chem. 280, 21264-21271 (Pubitemid 40805689)
19. Haynes, C. M., Titus, E. A., and Cooper, A. A. (2004) Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 15, 767-776 (Pubitemid 39194906)
20. Ron, D., and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529 (Pubitemid 46985379)
21. Hotamisligil, G. S. (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917
22. Gray, D. A., and Woulfe, J. (2005) Lipofuscin and aging: A matter of toxic waste. Sci. Aging Knowledge Environ. 2005, re1
23. Calandria, J. M., Marcheselli, V. L., Mukherjee, P. K., Uddin, J., Winkler, J. W., Petasis, N. A., and Bazan, N. G. (2009) Selective survival rescue in 15-lipoxygenase-1-deficient retinal pigment epithelial cells by the novel docosahexaenoic acid-derived mediator, neuroprotectin D1. J. Biol. Chem. 284, 17877-17882
24. Mukherjee, P. K., Marcheselli, V. L., Serhan, C. N., and Bazan, N. G. (2004) Neuroprotectin D1. A docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc.Natl. Acad. Sci. U.S.A. 101, 8491-8496 (Pubitemid 38736602)
25. Koshy, B., Matilla, T., Burright, E. N., Merry, D. E., Fischbeck, K. H., Orr, H. T., and Zoghbi, H. Y. (1996) Spinocerebellar ataxia type-1 and spinobulbar muscular atrophy gene products interact with glyceraldehyde-3- phosphate dehydrogenase. Hum. Mol. Genet. 5, 1311-1318 (Pubitemid 26335849)
26. Tsuda, H., Jafar-Nejad, H., Patel, A. J., Sun, Y., Chen, H. K., Rose, M. F., Venken, K. J., Botas, J., Orr, H. T., Bellen, H. J., and Zoghbi, H. Y. (2005) The AXH domain of ataxin-1 mediates neurodegeneration through its interaction with Gfi-1/Senseless proteins. Cell 122, 633-644 (Pubitemid 41191160)
27. Ishida, M., Lui, G. M., Yamani, A., Sugino, I. K., and Zarbin, M. A. (1998) Culture of human retinal pigment epithelial cells from peripheral scleral flap biopsies. Curr. Eye Res. 17, 392-402 (Pubitemid 28176907)
28. Stark, D. T., and Bazan, N. G. (2011) Synaptic and extrasynaptic NMDA receptors differentially modulate neuronal cyclooxygenase-2 function, lipid peroxidation, and neuroprotection. J. Neurosci. 31, 13710-13721
29. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
30. Mukherjee, P. K., Marcheselli, V. L., Barreiro, S., Hu, J., Bok, D., and Bazan, N. G. (2007) Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling. Proc. Natl. Acad. Sci. U.S.A. 104, 13152-13157 (Pubitemid 351737608)
31. Mukherjee, P. K., Marcheselli, V. L., de Rivero Vaccari, J. C., Gordon, W. C., Jackson, F. E., and Bazan, N. G. (2007) Photoreceptor outer segment phagocytosis attenuates oxidative stress-induced apoptosis with concomitant neuroprotectin D1 synthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 13158-13163 (Pubitemid 351737609)
32. Chou, A. H., Yeh, T. H., Kuo, Y. L., Kao, Y. C., Jou, M. J., Hsu, C. Y., Tsai, S. R., Kakizuka, A., and Wang, H. L. (2006) Polyglutamine-expanded ataxin-3 activates mitochondrial apoptotic pathway by up-regulating Bax and down-regulating Bcl-xL. Neurobiol. Dis. 21, 333-345 (Pubitemid 43099857)
33. Wang, H. L., Yeh, T. H., Chou, A. H., Kuo, Y. L., Luo, L. J., He, C. Y., Huang, P. C., and Li, A. H. (2006) Polyglutamine-expanded ataxin-7 activates mitochondrial apoptotic pathway of cerebellar neurons by upregulating Bax and downregulating Bcl-xL. Cell. Signal. 18, 541-552
34. Lam, Y. C., Bowman, A. B., Jafar-Nejad, P., Lim, J., Richman, R., Fryer, J. D., Hyun, E.D., Duvick, L. A., Orr, H. T., Botas, J., and Zoghbi, H. Y. (2006) ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neuropathology. Cell 127, 1335-1347 (Pubitemid 44960413)
35. Marcheselli, V. L., Hong, S., Lukiw, W. J., Tian, X. H., Gronert, K., Musto, A., Hardy, M., Gimenez, J. M., Chiang, N., Serhan, C. N., and Bazan, N. G. (2003) Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J. Biol. Chem. 278, 43807-43817 (Pubitemid 37346009)
36. Chen, H. K., Fernandez-Funez, P., Acevedo, S. F., Lam, Y. C., Kaytor, M. D., Fernandez, M. H., Aitken, A., Skoulakis, E. M., Orr, H. T., Botas, J., and Zoghbi, H. Y. (2003) Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113, 457-468 (Pubitemid 36588749)
37. Azadi, S., Johnson, L. E., Paquet-Durand, F., Perez, M. T., Zhang, Y., Ekström, P. A., and van Veen, T. (2007) CNTF + BDNF treatment and neuroprotective pathways in the rd1 mouse retina. Brain Res. 1129, 116-129 (Pubitemid 46048765)
38. Wu, C. L., Hwang, C. S., Chen, S. D., Yin, J. H., and Yang, D. I. (2010) Neuroprotective mechanisms of brain-derived neurotrophic factor against 3-nitropropionic acid toxicity. Therapeutic implications for Huntington's disease. Ann. N.Y. Acad. Sci. 1201, 8-12
39. Zoghbi, H. Y., and Orr, H. T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-247 (Pubitemid 30350043)
40. Matilla-Duenas, A., Goold, R., and Giunti, P. (2008) Clinical, genetic, molecular, and pathophysiological insights into spinocerebellar ataxia type 1. Cerebellum 7, 106-114
41. Williams, A. J., and Paulson, H. L. (2008) Polyglutamine neurodegeneration. Protein misfolding revisited. Trends Neurosci. 31, 521-528
42. Bazan, N. G., Calandria, J. M., and Serhan, C. N. (2010) Rescue and repair during photoreceptor cell renewal mediated by docosahexaenoic acidderived neuroprotectin D1. J. Lipid Res. 51, 2018-2031
43. Cummings, C. J., Reinstein, E., Sun, Y., Antalffy, B., Jiang, Y., Ciechanover, A., Orr, H. T., Beaudet, A. L., and Zoghbi, H. Y. (1999) Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron 24, 879-892 (Pubitemid 30017667)
44. Cummings, C. J., Sun, Y., Opal, P., Antalffy, B., Mestril, R., Orr, H. T., Dillmann, W. H., and Zoghbi, H. Y. (2001) Overexpression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum. Mol. Genet. 10, 1511-1518 (Pubitemid 32684893)
45. Antony, R., Lukiw, W. J., and Bazan, N. G. (2010) Neuroprotectin D1 induces dephosphorylation of Bcl-xL in a PP2A-dependent manner during oxidative stress and promotes retinal pigment epithelial cell survival. J. Biol. Chem. 285, 18301-18308
46. de Chiara, C., Menon, R. P., and Pastore, A. (2008) Structural bases for recognition of Anp32/LANP proteins. FEBS J. 275, 2548-2560 (Pubitemid 351600094)
47. Kaytor, M. D., Byam, C. E., Tousey, S. K., Stevens, S. D., Zoghbi, H. Y., and Orr, H. T. (2005) A cell-based screen for modulators of ataxin-1 phosphorylation. Hum. Mol. Genet. 14, 1095-1105 (Pubitemid 40575885)
48. Crespo-Barreto, J., Fryer, J. D., Shaw, C. A., Orr, H. T., and Zoghbi, H. Y. (2010) Partial loss of ataxin-1 function contributes to transcriptional dysregulation in spinocerebellar ataxia type 1 pathogenesis. PLoS Genet. 6, e1001021
49. Mizutani, A., Wang, L., Rajan, H., Vig, P. J., Alaynick, W. A., Thaler, J. P., and Tsai, C. C. (2005) Boat, an AXH domain protein, suppresses the cytotoxicity of mutant ataxin-1. EMBO J. 24, 3339-3351 (Pubitemid 41348707)