Posttranscriptional regulation of SOD1 gene expression under oxidative stress: Potential role of ELAV proteins in sporadic ALS

Neurobiology of Disease

Volumn 60, Issue , 2013, Pages 51-60

  Milani, Pamela ^a,b   Amadio, Marialaura ^b   Laforenza, Umberto ^b   Dell'Orco, Michela ^a,b   Diamanti, Luca ^a,b   Sardone, Valentina ^a,b   Gagliardi, Stella ^a   Govoni, Stefano ^b   Ceroni, Mauro ^a,b   Pascale, Alessia ^b   Cereda, Cristina ^a  

^a C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

ELAV proteins; Motor cortex; MRNA; Peripheral blood mononuclear cells; Posttranscriptional regulation; SOD1; Spinal cord; Sporadic amyotrophic lateral sclerosis

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; HU ANTIGEN; MESSENGER RNA; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ADULT; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ELAV GENE; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; MOLECULAR DOCKING; MOTOR CORTEX; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SOD1 GENE; SPINAL CORD; SPORADIC AMYOTROPHIC LATERAL SCLEROSIS; UPREGULATION;

ELAV PROTEINS; MOTOR CORTEX; MRNA; PERIPHERAL BLOOD MONONUCLEAR CELLS; POSTTRANSCRIPTIONAL REGULATION; SOD1; SPINAL CORD; SPORADIC AMYOTROPHIC LATERAL SCLEROSIS;

AMYOTROPHIC LATERAL SCLEROSIS; FEMALE; GENE EXPRESSION REGULATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MALE; MIDDLE AGED; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

EID: 84883648450     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.08.005     Document Type: Article

References (50)

1. Abdelmohsen K., Kuwano Y., Gorospe M. Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. BiolChem 2008, 389(3):243-255. (Mar).
2. Amadio M., Scapagnini G., Laforenza U., Intrieri M., Romeo L., Govoni S., et al. Post-transcriptional regulation of HSP70 expression following oxidative stress in SH-SY5Y cells: the potential involvement of the RNA-binding protein HuR. Curr. Pharm. Des. 2008, 14(26):2651-2658.
3. Amadio M., Pascale A., Wang J., Ho L., Quattrone A., Gandy S., et al. nELAV proteins alteration in Alzheimer's disease brain: a novel putative target for amyloid-beta reverberating on AbetaPP processing. J. Alzheimers Dis. 2009, 16(2):409-419.
4. Amadio M., Bucolo C., Leggio G.M., Drago F., Govoni S., et al. The PKCbeta/HuR/VEGF pathway in diabetic retinopathy. Biochem. Pharmacol. 2010, 80(8):1230-1237. (Oct. 15).
5. Antic D., Keene J.D. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am. J. Hum. Genet. 1997, 61(2):273-278. (Aug).
6. Babu G.N., Kumar A., Chandra R., Puri S.K., Singh R.L., Kalita J., et al. Oxidant-antioxidant imbalance in the erythrocytes of sporadic amyotrophic lateral sclerosis patients correlates with the progression of disease. Neurochem. Int. 2008, 52(6):1284-1289. (May).
7. Barber S.C., Shaw P.J. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 2010, 48(5):629-641. (Mar. 1).
8. Bogdanov M., Brown R.H., Matson W., Smart R., Hayden D., O'Donnell H., et al. Increased oxidative damage to DNA in ALS patients. Free Radic. Biol. Med. 2000, 29(7):652-658. (Oct. 1).
9. Bonnefont-Rousselot D., Lacomblez L., Jaudon M., Lepage S., Salachas F., Bensimon G., et al. Blood oxidative stress in amyotrophic lateral sclerosis. J. Neurol. Sci. 2000, 178(1):57-62. (Sep. 1).
10. Bosco D.A., Morfini G., Karabacak N.M., Song Y., Gros-Louis F., Pasinelli P., et al. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 2010, 13(11):1396-1403. (Nov).
11. Brooks B.R., Miller R.G., Swash M., Munsat T.L. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000, 1(5):293-299. (Dec).
12. Cereda C., Cova E., Di Poto C., Galli A., Mazzini G., Corato M., et al. Effect of nitric oxide on lymphocytes from sporadic amyotrophic lateral sclerosis patients: toxic or protective role?. Neurol. Sci. 2006, 27(5):312-316. (Nov).
13. Chang Y., Kong Q., Shan X., Tian G., Ilieva H., Cleveland D.W., et al. Messenger RNA oxidation occurs early in disease pathogenesis and promotes motor neuron degeneration in ALS. PLoS One 2008, 3(8):e2849. (Aug. 6).
14. Chen C.Y., Shyu A.B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 1995, 20(11):465-470. (Nov).
15. Colombrita C., Silani V., Ratti A. ELAV proteins along evolution: back to the nucleus. Mol. Cell. Neurosci. 2013, (Feb, pii: S1044-7431(13)00021-3). 10.1016/j.mcn.2013.02.003.
16. Cova E., Cereda C., Galli A., Curti D., Finotti C., Di Poto C., Corato M., et al. Modified expression of Bcl-2 and SOD1 proteins in lymphocytes from sporadic ALS patients. Neurosci. Lett. 2006, 399(3):186-190. (May. 22).
17. Cova E., Bongioanni P., Cereda C., Metelli M.R., Salvaneschi L., Bernuzzi S., et al. Time course of oxidant markers and antioxidant defenses in subgroups of amyotrophic lateral sclerosis patients. Neurochem. Int. 2010, 56(5):687-693. (Apr).
18. Cozzolino M., Pesaresi M.G., Gerbino V., Grosskreutz J., Carrì M.T. Amyotrophic lateral sclerosis: new insights into underlying molecular mechanisms and opportunities for therapeutic intervention. Antioxid. Redox Signal. 2012, 17(9):1277-1330. (Nov. 1).
19. Doller A., Pfeilschifter J., Eberhardt W. Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cell. Signal. 2008, 20(12):2165-2173. (Dec).
20. Doller A., Schlepckow K., Schwalbe H., Pfeilschifter J., Eberhardt W. Tandem phosphorylation of serines 221 and 318 by protein kinase Cdelta coordinates mRNA binding and nucleocytoplasmic shuttling of HuR. Mol. Cell Biol. 2010, 30(6):1397-1410. (Mar).
21. Ezzi S.A., Urushitani M., Julien J.P. Wild-type superoxide dismutase acquires binding and toxic properties of ALS-linked mutant forms through oxidation. J. Neurochem. 2007, 102(1):170-178. (Jul).
22. Gagliardi S., Cova E., Davin A., Guareschi S., Abel K., Alvisi E., et al. SOD1 mRNA expression in sporadic amyotrophic lateral sclerosis. Neurobiol. Dis. 2010, 39(2):198-203. (Aug).
23. Guareschi S., Cova E., Cereda C., Ceroni M., Donetti E., Bosco D.A., et al. An over-oxidized form of superoxide dismutase found in sporadic amyotrophic lateral sclerosis with bulbar onset shares a toxic mechanism with mutant SOD1. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(13):5074-5079. (Mar. 27).
24. Hofacker I.L. Vienna RNA, secondary structure server. Nucleic Acids Res. 2003, 31(13):3429-3431. (Jul. 1).
25. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8(7):533-543. (Jul).
26. Kilk A., Laan M., Torp A. Human CuZn superoxide dismutase enzymatic activity in cells is regulated by the length of the mRNA. FEBS Lett. 1995, 362(3):323-327. (Apr. 10).
27. Kuwano Y., Kim H.H., Abdelmohsen K., Pullmann R., Martindale J.L., Yang X., et al. MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell Biol. 2008, 28(14):4562-4575. (Jul).
28. Laforenza U., Gastaldi G., Polimeni M., Tritto S., Tosco M., Ventura U., Scaffino M.F., et al. Aquaporin-6 is expressed along the rat gastrointestinal tract and upregulated by feeding in the small intestine. BMC Physiol. 2009, 9:18. (Oct. 7).
29. Latorre E., Tebaldi T., Viero G., Spartà A.M., Quattrone A., Provenzani A. Downregulation of HuR as a new mechanism of doxorubicin resistance in breast cancer cells. Mol. Cancer 2012, 11:13. (Mar. 21).
30. López de Silanes I., Zhan M., Lal A., Yang X., Gorospe M. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(9):2987-2992. (Mar. 2).
31. Mata J., Marguerat S., Bähler J. Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem. Sci. 2005, 30(9):506-514. Sep.
32. Milani P., Gagliardi S., Cova E., Cereda C. SOD1 transcriptional and posttranscriptional regulation and its potential implications in ALS. Neurol. Res. Int. 2011, 2011:458427.
33. Milani P., Gagliardi S., Bongioanni P., Grieco G.S., Dezza M., Bianchi M., et al. Effect of the 50bp deletion polymorphism in the SOD1 promoter on SOD1 mRNA levels in Italian ALS patients. J. Neurol. Sci. 2012, 313(1-2):75-78. (Feb. 15).
34. Mougeot J.L.C., Li Z., Price A.E., Wright F.A., Brooks B.R. Microarray analysis of peripheral blood lymphocytes from ALS patients and the SAFE detection of the KEGG ALS pathway. BMC Med. Genomics 2011, 4:74. (Oct. 25).
35. Nagai K., Oubridge C., Ito N., Avis J., Evans P. The RNP domain: a sequence-specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem. Sci. 1995, 20(6):235-240. (Jun).
36. Oates N., Pamphlett R. An epigenetic analysis of SOD1 and VEGF in ALS. Amyotroph. Lateral Scler. 2007, 8(2):83-86. (Apr).
37. Park E.Y., Rho H.M. The transcriptional activation of the human copper/zinc superoxide dismutase gene by 2,3,7,8-tetrachlorodibenzo-p-dioxin through two different regulator sites, the antioxidant responsive element and xenobiotic responsive element. Mol. Cell. Biochem. 2002, 240(1-2):47-55. (Nov).
38. Pascale A., Govoni S. The complex world of post-transcriptional mechanisms: is their deregulation a common link for diseases? Focus on ELAV-like RNA-binding proteins. Cell. Mol. Life Sci. 2012, 69(4):501-517. (Feb).
39. Pascale A., Amadio M., Quattrone A. Defining a neuron: neuronal ELAV proteins. Cell. Mol. Life Sci. 2008, 65(1):128-140. (Jan).
40. Robberecht W. Oxidative stress in amyotrophic lateral sclerosis. J. Neurol. 2000, 247(Suppl. 1):I1-I6. (Mar).
41. Rojo A.I., Salinas M., Martín D., Perona R., Cuadrado A. Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J. Neurosci. 2004, 24(33):7324-7334. (Aug. 18).
42. Saunus J.M., French J.D., Edwards S.L., Beveridge D.J., Hatchell E.C., Wagner S.A., et al. Posttranscriptional regulation of the breast cancer susceptibility gene BRCA1 by the RNA binding protein HuR. Cancer Res. 2008, 68(22):9469-9478. (Nov. 15).
43. Schaljo B., Kratochvill F., Gratz N., Sadzak I., Sauer I., Hammer M., et al. Tristetraprolin is required for full anti-inflammatory response of murine macrophages to IL-10. J. Immunol. 2009, 183(2):1197-1206. (Jul. 15).
44. Schreiber E., Matthias P., Müller M.M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 1989, 17(15):6419. (Aug. 11).
45. Shaw P.J., Ince P.G., Falkous G., Mantle D. Oxidative damage to protein in sporadic motor neuron disease spinal cord. Ann. Neurol. 1995, 38(4):691-695. (Oct).
46. Simpson E.P., Yen A.A., Appel S.H. Oxidative stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Curr. Opin. Rheumatol. 2003, 15(6):730-736. (Nov).
47. Srikantan S., Gorospe M. HuR function in disease. Front. Biosci. 2012, 17:189-205. (Jan. 1).
48. Tenenbaum S.A., Lager P.J., Carson C.C., Keene J.D. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 2002, 26(2):191-198. (Feb).
49. Viiri J., Amadio M., Marchesi N., Hyttinen J.M.T., Kivinen N., Sironen R., Rilla K., Akhtar S., Provenzani A., D'Agostino V.G., Govoni S., Pascale A., Agostini H., Petrovski G., Salminen A., Kaarniranta K. Autophagy activation clears ELAVL1/HuR-mediated accumulation of SQSTM1/p62 during proteasomal inhibition in human retinal pigment epithelial cells. Plos One 2013, 8(7):e69563. (Jul 29). 10.1371/journal.pone.0069563.
50. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31(13):3406-3415. (Jul. 1).