RBM45 modulates the antioxidant response in amyotrophic lateral sclerosis through interactions with KEAP1

Molecular and Cellular Biology

Volumn 35, Issue 14, 2015, Pages 2385-2399

  Bakkar, Nadine ^a   Kousari, Arianna ^a   Kovalik, Tina ^a   Li, Yang ^a   Bowser, Robert ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; RBM45 PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; KEAP1 PROTEIN, HUMAN; NERVE PROTEIN; PROTEIN BINDING; RBM45 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE EXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; LUMBAR SPINAL CORD; MALE; MIDDLE AGED; MOTONEURON; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SPINAL CORD; ANIMAL; CELL CULTURE; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SPRAGUE DAWLEY RAT; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; GENE EXPRESSION; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; MALE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; NERVE TISSUE PROTEINS; PROTEIN BINDING; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA-BINDING PROTEINS; SPINAL CORD;

EID: 84932626537     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00087-15     Document Type: Article

References (63)

1. Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, Burrell JR, Zoing MC. 2011. Amyotrophic lateral sclerosis. Lancet 377: 942-955. http://dx.doi.org/10.1016/S0140-6736(10)61156-7.
2. Pratt AJ, Getzoff ED, Perry JJ. 2012. Amyotrophic lateral sclerosis: update and new developments. Degener Neurol Neuromuscul Dis 2012: 1-14. http://dx.doi.org/10.2147/DNND.S19803.
3. Byrne S, Walsh C, Lynch C, Bede P, Elamin M, Kenna K, McLaughlin R, Hardiman O. 2011. Rate of familial amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 82: 623-627. http://dx.doi.org/10.1136/jnnp.2010.224501.
4. Leigh PN, Whitwell H, Garofalo O, Buller J, Swash M, Martin JE, Gallo J-M, Weller RO, Anderton BH. 1991. Ubiquitin-immunoreactive intraneuronal inclusions in amyotrophic lateral sclerosis; morphology, distribution and specificity. Brain 114:775-788. http://dx.doi.org/10.1093/brain/114.2.775.
5. Turner MR, Bowser R, Bruijn L, Dupuis L, Ludolph A, McGrath M, Manfredi G, Maragakis N, Miller RG, Pullman SL, Rutkove SB, Shaw PJ, Shefner J, Fischbeck KH. 2013. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 14(Suppl 1):19-32. http://dx.doi.org/10.3109/21678421.2013.778554.
6. Lagier-Tourenne C, Polymenidou M, Cleveland DW. 2010. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 19:R46-R64. http://dx.doi.org/10.1093/hmg/ddq137.
7. Verma A, Tandan R. 2013. RNA quality control and protein aggregates in amyotrophic lateral sclerosis: a review. Muscle Nerve 47:330-338. http://dx.doi.org/10.1002/mus.23673.
8. Li YR, King OD, Shorter J, Gitler AD. 2013. Stress granules as crucibles of ALS pathogenesis. J Cell Biol 201:361-372. http://dx.doi.org/10.1083/jcb.201302044.
9. Collins M, Riascos D, Kovalik T, An J, Krupa K, Hood BL, Conrads TP, Renton AE, Traynor BJ, Bowser R. 2012. The RNA-binding motif 45 (RBM45) protein accumulates in inclusion bodies in amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration with TDP-43 inclusions (FTLD-TDP) patients. Acta Neuropathol 124:717-732. http://dx.doi.org/10.1007/s00401-012-1045-x.
10. Tamada H, Sakashita E, Shimazaki K, Ueno E, Hamamoto T, Kagawa Y, Endo H. 2002. cDNA cloning and characterization of Drb1, a new member of RRM-type neural RNA-binding protein. Biochem Biophys ResCommun 297:96-104. http://dx.doi.org/10.1016/S0006-291X(02)02132-0.
11. Hans F, Fiesel FC, Strong JC, Jackel S, Rasse TM, Geisler S, Springer W, Schulz JB, Voigt A, Kahle PJ. 2014. UBE2E ubiquitin-conjugating enzymes and ubiquitin isopeptidase Y regulate TDP-43 protein ubiquitination. J Biol Chem 289:19164-19179. http://dx.doi.org/10.1074/jbc.M114.561704.
12. Halliwell B. 2006. Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634-1658. http://dx.doi.org/10.1111/j.1471-4159.2006.03907.x.
13. Aguirre N, Beal MF, Matson WR, Bogdanov MB. 2005. Increased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis. Free Radic Res 39:383-388. http://dx.doi.org/10.1080/10715760400027979.
14. Andrus PK, Fleck TJ, Gurney ME, Hall ED. 1998. Protein oxidative damage in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 71:2041-2048.
15. Ferrante RJ, Shinobu LA, Schulz JB, Matthews RT, Thomas CE, Kowall NW, Gurney ME, Beal MF. 1997. Increased 3-nitrotyrosine and oxidative damage in mice with a human copper/zinc superoxide dismutase mutation. Ann Neurol 42:326-334. http://dx.doi.org/10.1002/ana.410420309.
16. Miana-Mena FJ, Gonzalez-Mingot C, Larrode P, Munoz MJ, Olivan S, Fuentes-Broto L, Martinez-Ballarin E, Reiter RJ, Osta R, Garcia JJ. 2011. Monitoring systemic oxidative stress in an animal model of amyotrophic lateral sclerosis. J Neurol 258:762-769. http://dx.doi.org/10.1007/s00415-010-5825-8.
17. Nikolic-Kokic A, Stevic Z, Blagojevic D, Davidovic B, Jones DR, Spasic MB. 2006. Alterations in anti-oxidative defence enzymes in erythrocytes from sporadic amyotrophic lateral sclerosis (SALS) and familial ALS patients. Clin Chem Lab Med 44:589-593. http://dx.doi.org/10.1515/CCLM.2006.111.
18. Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH. 2004. Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden. Neurology 62:1758-1765. http://dx.doi.org/10.1212/WNL.62.10.1758.
19. Ferrante RJ, Browne SE, Shinobu LA, Bowling AC, Baik MJ, MacGarvey U, Kowall NW, Brown RH, Jr, Beal MF. 1997. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem 69:2064-2074.
20. D'Amico E, Factor-Litvak P, Santella RM, Mitsumoto H. 2013. Clinical perspective of oxidative stress in sporadic ALS. Free Radic Biol Med 65: 509-527. http://dx.doi.org/10.1016/j.freeradbiomed.2013.06.029.
21. Zhang DD. 2006. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38:769-789. http://dx.doi.org/10.1080/03602530600971974.
22. Taguchi K, Motohashi H, Yamamoto M. 2011. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16:123-140. http://dx.doi.org/10.1111/j.1365-2443.2010.01473.x.
23. Tong KI, Kobayashi A, Katsuoka F, Yamamoto M. 2006. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol Chem 387:1311-1320. http://dx.doi.org/10.1515/BC.2006.164.
24. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, Yamamoto M. 2010. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12:213-223. http://dx.doi.org/10.1038/ncb2021.
25. Chorley BN, Campbell MR, Wang X, Karaca M, Sambandan D, Bangura F, Xue P, Pi J, Kleeberger SR, Bell DA. 2012. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor alpha. Nucleic Acids Res 40:7416-7429. http://dx.doi.org/10.1093/nar/gks409.
26. Mimoto T, Miyazaki K, Morimoto N, Kurata T, Satoh K, Ikeda Y, Abe K. 2012. Impaired antioxydative Keap1/Nrf2 system and the downstream stress protein responses in the motor neuron of ALS model mice. Brain Res 1446:109-118. http://dx.doi.org/10.1016/j.brainres.2011.12.064.
27. Kraft AD, Resch JM, Johnson DA, Johnson JA. 2007. Activation of the Nrf2-ARE pathway in muscle and spinal cord during ALS-like pathology in mice expressing mutant SOD1. Exp Neurol 207:107-117. http://dx.doi.org/10.1016/j.expneurol.2007.05.026.
28. Guo Y, Zhang Y, Wen D, Duan W, An T, Shi P, Wang J, Li Z, Chen X, Li C. 2013. The modest impact of transcription factor Nrf2 on the course of disease in an ALS animal model. Lab Invest 93:825-833. http://dx.doi.org/10.1038/labinvest.2013.73.
29. Vargas MR, Burton NC, Kutzke J, Gan L, Johnson DA, Schafer M, Werner S, Johnson JA. 2013. Absence of Nrf2 or its selective overexpression in neurons and muscle does not affect survival in ALS-linked mutant hSOD1 mouse models. PLoS One 8:e56625. http://dx.doi.org/10.1371/journal.pone.0056625.
30. Vargas MR, Johnson DA, Sirkis DW, Messing A, Johnson JA. 2008. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J Neurosci 28:13574-13581. http://dx.doi.org/10.1523/JNEUROSCI.4099-08.2008.
31. Sarlette A, Krampfl K, Grothe C, Neuhoff N, Dengler R, Petri S. 2008. Nuclear erythroid 2-related factor 2-antioxidative response element signaling pathway in motor cortex and spinal cord in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 67:1055-1062. http://dx.doi.org/10.1097/NEN.0b013e31818b4906.
32. Tanji K, Maruyama A, Odagiri S, Mori F, Itoh K, Kakita A, Takahashi H, Wakabayashi K. 2013. Keap1 is localized in neuronal and glial cytoplasmic inclusions in various neurodegenerative diseases. J Neuropathol Exp Neurol 72:18-28. http://dx.doi.org/10.1097/NEN.0b013e31827b5713.
33. Guo Y, Wang Q, Zhang K, An T, Shi P, Li Z, Duan W, Li C. 2012. HO-1 induction in motor cortex and intestinal dysfunction inTDP-43A315Ttransgenic mice. Brain Res 1460:88-95. http://dx.doi.org/10.1016/j.brainres.2012.04.003.
34. Duan W, Li X, Shi J, Guo Y, Li Z, Li C. 2010. Mutant TAR DNA-binding protein-43 induces oxidative injury in motor neuron-like cell. Neuroscience 169:1621-1629. http://dx.doi.org/10.1016/j.neuroscience.2010.06.018.
35. Furukawa M, Xiong Y. 2005. BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol Cell Biol 25:162-171. http://dx.doi.org/10.1128/MCB.25.1.162-171.2005.
36. Kolarcik C, Bowser R. 2012. Retinoid signaling alterations in amyotrophic lateral sclerosis. Am J Neurodegener Dis 1:130-145.
37. Graber DJ, Harris BT. 2013. Purification and culture of spinal motor neurons from rat embryos. Cold Spring Harb Protoc 2013:319-326. http://dx.doi.org/10.1101/pdb.prot074161.
38. Ponti A, Schwarb P, Gulati A, Bäcker V. 2007. Huygens Remote Manager, a Web interface for high-volume batch deconvolution. Imaging Microsc 9:57-58. http://dx.doi.org/10.1002/imic.200790154.
39. Parker SJ, Meyerowitz J, James JL, Liddell JR, Crouch PJ, Kanninen KM, White AR. 2012. Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Neurochem Int 60:415-424. http://dx.doi.org/10.1016/j.neuint.2012.01.019.
40. Mazan-Mamczarz K, Lal A, Martindale JL, Kawai T, Gorospe M. 2006. Translational repression by RNA-binding protein TIAR. Mol Cell Biol 26:2716-2727. http://dx.doi.org/10.1128/MCB.26.7.2716-2727.2006.
41. Taupin JL, Tian Q, Kedersha N, Robertson M, Anderson P. 1995. The RNA-binding protein TIAR is translocated from the nucleus to the cytoplasm during Fas-mediated apoptotic cell death. Proc Natl Acad Sci U S A 92:1629-1633. http://dx.doi.org/10.1073/pnas.92.5.1629.
42. Seibenhener ML, Babu JR, Geetha T, Wong HC, Krishna NR, Wooten MW. 2004. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 24:8055-8068 http://dx.doi.org/10.1128/MCB.24.18.8055-8068.2004.
43. Fecto F, Yan J, Vemula SP, Liu E, Yang Y, Chen W, Zheng JG, Shi Y, Siddique N, Arrat H, Donkervoort S, Ajroud-Driss S, Sufit RL, Heller SL, Deng HX, Siddique T. 2011. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch Neurol 68:1440-1446. http://dx.doi.org/10.1001/archneurol.2011.250.
44. Teyssou E, Takeda T, Lebon V, Boillee S, Doukoure B, Bataillon G, Sazdovitch V, Cazeneuve C, Meininger V, LeGuern E, Salachas F, Seilhean D, Millecamps S. 2013. Mutations in SQSTM1 encoding p62 in amyotrophic lateral sclerosis: genetics and neuropathology. Acta Neuropathol 125:511-522. http://dx.doi.org/10.1007/s00401-013-1090-0.
45. Gal J, Strom AL, Kilty R, Zhang F, Zhu H. 2007. p62 accumulates and enhances aggregate formation in model systems of familial amyotrophic lateral sclerosis. J Biol Chem 282:11068-11077. http://dx.doi.org/10.1074/jbc.M608787200.
46. Mizuno Y, Amari M, Takatama M, Aizawa H, Mihara B, Okamoto K. 2006. Immunoreactivities of p62, an ubiquitin-binding protein, in the spinal anterior horn cells of patients with amyotrophic lateral sclerosis. J Neurol Sci 249:13-18. http://dx.doi.org/10.1016/j.jns.2006.05.060.
47. Sowa ME, Bennett EJ, Gygi SP, Harper JW. 2009. Defining the human deubiquitinating enzyme interaction landscape. Cell 138:389-403. http://dx.doi.org/10.1016/j.cell.2009.04.042.
48. Zhang DD, Lo SC, Sun Z, Habib GM, Lieberman MW, Hannink M. 2005. Ubiquitination of Keap1, a BTB-Kelch substrate adaptor protein for Cul3, targets Keap1 for degradation by a proteasome-independent pathway. J Biol Chem 280:30091-30099. http://dx.doi.org/10.1074/jbc.M501279200.
49. Barber SC, Shaw PJ. 2010. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic Biol Med 48:629-641. http://dx.doi.org/10.1016/j.freeradbiomed.2009.11.018.
50. Parakh S, Spencer DM, Halloran MA, Soo KY, Atkin JD. 2013. Redox regulation in amyotrophic lateral sclerosis. Oxid Med Cell Longev 2013: 408681. http://dx.doi.org/10.1155/2013/408681.
51. Cho HY. 2013. Genomic structure and variation of nuclear factor (erythroid-derived 2)-like 2. Oxid Med Cell Longev 2013:286524. http://dx.doi.org/10.1155/2013/286524.
52. LoGerfo A, Chico L, Borgia L, Petrozzi L, Rocchi A, D'Amelio A, Carlesi C, Caldarazzo Ienco E, Mancuso M, Siciliano G. 2014. Lack of association between nuclear factor erythroid-derived 2-like 2 promoter gene polymorphisms and oxidative stress biomarkers in amyotrophic lateral sclerosis patients. Oxid Med Cell Longev 2014:432626. http://dx.doi.org/10.1155/2014/432626.
53. von Otter M, Landgren S, Nilsson S, Celojevic D, Bergstrom P, Hakansson A, Nissbrandt H, Drozdzik M, Bialecka M, Kurzawski M, Blennow K, Nilsson M, Hammarsten O, Zetterberg H. 2010. Association of Nrf2-encoding NFE2L2 haplotypes with Parkinson's disease. BMC Med Genet 11:36. http://dx.doi.org/10.1186/1471-2350-11-36.
54. von Otter M, Landgren S, Nilsson S, Zetterberg M, Celojevic D, Bergstrom P, Minthon L, Bogdanovic N, Andreasen N, Gustafson DR, Skoog I, Wallin A, Tasa G, Blennow K, Nilsson M, Hammarsten O, Zetterberg H. 2010. Nrf2-encoding NFE2L2 haplotypes influence disease progression but not risk in Alzheimer's disease and age-related cataract. Mech Ageing Dev 131:105-110. http://dx.doi.org/10.1016/j.mad.2009.12.007.
55. Bergstrom P, von Otter M, Nilsson S, Nilsson AC, Nilsson M, Andersen PM, Hammarsten O, Zetterberg H. 2013. Association of NFE2L2 and KEAP1 haplotypes with amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 15:130-137. http://dx.doi.org/10.3109/21678421.2013.839708.
56. Barber SC, Mead RJ, Shaw PJ. 2006. Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochim Biophys Acta 1762:1051-1067. http://dx.doi.org/10.1016/j.bbadis.2006.03.008.
57. Orrell RW, Lane RJ, Ross M. 2007. Antioxidant treatment for amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst Rev 2007: CD002829. http://dx.doi.org/10.1002/14651858.CD002829.pub4.
58. Nanou A, Higginbottom A, Valori CF, Wyles M, Ning K, Shaw P, Azzouz M. 2013. Viral delivery of antioxidant genes as a therapeutic strategy in experimental models of amyotrophic lateral sclerosis. Mol Ther 21:1486-1496. http://dx.doi.org/10.1038/mt.2013.115.
59. Mead RJ, Higginbottom A, Allen SP, Kirby J, Bennett E, Barber SC, Heath PR, Coluccia A, Patel N, Gardner I, Brancale A, Grierson AJ, Shaw PJ. 2013. S[+] Apomorphine is a CNS penetrating activator of the Nrf2-ARE pathway with activity in mouse and patient fibroblast models of amyotrophic lateral sclerosis. Free Radic Biol Med 61:438-452. http://dx.doi.org/10.1016/j.freeradbiomed.2013.04.018.
60. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, Buratti E, Silani V, Ratti A. 2009. TDP-43 is recruited to stress granules in conditions of oxidative insult. J Neurochem 111:1051-1061. http://dx.doi.org/10.1111/j.1471-4159.2009.06383.x.
61. Meyerowitz J, Parker SJ, Vella LJ, Ng D, Price KA, Liddell JR, Caragounis A, Li QX, Masters CL, Nonaka T, Hasegawa M, Bogoyevitch MA, Kanninen KM, Crouch PJ, White AR. 2011. C-Jun N-terminal kinase controls TDP-43 accumulation in stress granules induced by oxidative stress. Mol Neurodegener 6:57. http://dx.doi.org/10.1186/1750-1326-6-57.
62. Yamaguchi A, Kitajo K. 2012. The effect of PRMT1-mediated arginine methylation on the subcellular localization, stress granules, and detergentinsoluble aggregates of FUS/TLS. PLoS One 7:e49267. http://dx.doi.org/10.1371/journal.pone.0049267.
63. Neumann M, Sampathu DM, Kwong LK, Truax AC, Miscenyi MC, Chou LT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130-133. http://dx.doi.org/10.1126/science.1134108.