The N-terminus of TDP-43 promotes its oligomerization and enhances DNA binding affinity

Biochemical and Biophysical Research Communications

Volumn 425, Issue 2, 2012, Pages 219-224

  Chang, Chung ke ^a   Wu, Tzong Huah ^b,c,d   Wu, Chu Ya ^b,e   Chiang, Ming hui ^a   Toh, Elsie Khai Woon ^a   Hsu, Yin Chih ^b   Lin, Ku Feng ^b   Liao, Yu heng ^a   Huang, Tai huang ^a,f   Huang, Joseph Jen Tse ^b  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b INSTITUTE OF CHEMISTRY   (Taiwan)

^c ACADEMIA SINICA   (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^f NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

Author keywords

DNA RNA binding; N terminus; Neurodegenerative disease; Oligomerization; TDP 43

Indexed keywords

DNA; TAR DNA BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; DNA BINDING; FRACTIONAL ANISOTROPY; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

CIRCULAR DICHROISM; DNA; DNA-BINDING PROTEINS; HUMANS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84865386915     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.07.071     Document Type: Article

References (33)

1. Buratti E., Baralle F.E. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front. Biosci. 2008, 13:867-878.
2. Kuo P.H., Doudeva L.G., Wang Y.T., Shen C.K., Yuan H.S. Structural insights into TDP-43 in nucleic-acid binding and domain interactions. Nucleic Acids Res. 2009, 37:1799-1808.
3. Buratti E., Brindisi A., Pagani F., Baralle F.E. Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipping of exon 9: a functional link with disease penetrance. Am. J. Hum. Genet. 2004, 74:1322-1325.
4. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
5. Ou S.H., Wu F., Harrich D., García-Martínez L.F., Gaynor R.B. Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol. 1995, 69:3584-3596.
6. Ayala Y.M., De Conti L., Avendano-Vazquez S.E., Dhir A., Romano M., D'Ambrogio A., Tollervey J., Ule J., Baralle M., Buratti E., Baralle F.E. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 2011, 30:277-288.
7. D'Ambrogio A., Buratti E., Stuani C., Guarnaccia C., Romano M., Ayala Y.M., Baralle F.E. Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. Nucleic Acids Res. 2009, 37:4116-4126.
8. Ling S.C., Albuquerque C.P., Han J.S., Lagier-Tourenne C., Tokunaga S., Zhou H., Cleveland D.W. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc. Natl. Acad. Sci. USA 2010, 107:13318-13323.
9. Johnson B.S., Snead D., Lee J.J., McCaffery J.M., Shorter J., Gitler A.D. TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. J. Biol. Chem. 2009, 284:20329-20339.
10. Gitcho M.A., Baloh R.H., Chakraverty S., Mayo K., Norton J.B., Levitch D., Hatanpaa K.J., White C.L., Bigio E.H., Caselli R., Baker M., Al-Lozi M.T., Morris J.C., Pestronk A., Rademakers R., Goate A.M., Cairns N.J. TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol. 2008, 63:535-538.
11. Kabashi E., Valdmanis P.N., Dion P., Spiegelman D., McConkey B.J., Vande Velde C., Bouchard J.-P., Lacomblez L., Pochigaeva K., Salachas F., Pradat P.-F., Camu W., Meininger V., Dupre N., Rouleau G.A. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:572-574.
12. Yokoseki A., Shiga A., Tan C.-F., Tagawa A., Kaneko H., Koyama A., Eguchi H., Tsujino A., Ikeuchi T., Kakita A., Okamoto K., Nishizawa M., Takahashi H., Onodera O. TDP-43 mutation in familial amyotrophic lateral sclerosis. Ann. Neurol. 2008, 63:538-542.
13. Chen A.K., Lin R.Y., Hsieh E.Z., Tu P.H., Chen R.P., Liao T.Y., Chen W., Wang C.H., Huang J.J. Induction of amyloid fibrils by the C-terminal fragments of TDP-43 in amyotrophic lateral sclerosis. J. Am. Chem. Soc. 2010, 132:1186-1187.
14. Tollervey J.R., Curk T., Rogelj B., Briese M., Cereda M., Kayikci M., Konig J., Hortobagyi T., Nishimura A.L., Zupunski V., Patani R., Chandran S., Rot G., Zupan B., Shaw C.E., Ule J. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 2011, 14:452-458.
15. Pesiridis G.S., Tripathy K., Tanik S., Trojanowski J.Q., Lee V.M. A "two-hit" hypothesis for inclusion formation by carboxyl-terminal fragments of TDP-43 protein linked to RNA depletion and impaired microtubule-dependent transport. J. Biol. Chem. 2011, 286:18845-18855.
16. Li H.Y., Yeh P.A., Chiu H.C., Tang C.Y., Tu B.P. Hyperphosphorylation as a defense mechanism to reduce TDP-43 aggregation. PLoS One 2011, 6:e23075.
17. Johnson B.S., McCaffery J.M., Lindquist S., Gitler A.D. A yeast TDP-43 proteinopathy model: exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc. Natl. Acad. Sci. USA 2008, 105:6439-6444.
18. Markley J.L., Bax A., Arata Y., Hilbers C.W., Kaptein R., Sykes B.D., Wright P.E., Wuthrich K. Recommendations for the presentation of NMR structures of proteins and nucleic acids. IUPAC-IUBMB-IUPAB inter-union task group on the standardization of data bases of protein and nucleic acid structures determined by NMR spectroscopy. J. Biomol. NMR 1998, 12:1-23.
19. Sreerama N., Woody R.W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 2000, 287:252-260.
20. Whitmore L., Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 2004, 32:W668-673.
21. Lakowicz J.R. Principles of Fluorescence Spectroscopy 1983, Plenum Press, New York.
22. Patel H.V., Vyas A.A., Vyas K.A., Liu Y.S., Chiang C.M., Chi L.M., Wu W. Heparin and heparan sulfate bind to snake cardiotoxin. Sulfated oligosaccharides as a potential target for cardiotoxin action. J. Biol. Chem. 1997, 272:1484-1492.
23. Yang Z.R., Thomson R., McNeil P., Esnouf R.M. RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 2005, 21:3369-3376.
24. Garcia P., Serrano L., Rico M., Bruix M. An NMR view of the folding process of a CheY mutant at the residue level. Structure 2002, 10:1173-1185.
25. Pervushin K., Riek R., Wider G., Wuthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 1997, 94:12366-12371.
26. S. Suzuki, Y. Muto, M. Inoue, T. Kigawa, T. Terada, M. Shirouzu, S. Yokoyama, Solution structure of the RNA binding domain of TAR DNA-binding protein-43. PDB ID: 2CQG.
27. F. He, Y. Muto, M. Inoue, T. Kigawa, M. Shirouzu, T. Terada, S. Yokoyama, Solution structure of RRM domain in TAR DNA-binding protein-43. PDB ID: 1WF0.
28. Price W.N., Chen Y., Handelman S.K., Neely H., Manor P., Karlin R., Nair R., Liu J., Baran M., Everett J., Tong S.N., Forouhar F., Swaminathan S.S., Acton T., Xiao R., Luft J.R., Lauricella A., DeTitta G.T., Rost B., Montelione G.T., Hunt J.F. Understanding the physical properties that control protein crystallization by analysis of large-scale experimental data. Nat. Biotechnol. 2009, 27:51-57.
29. Nonaka T., Kametani F., Arai T., Akiyama H., Hasegawa M. Truncation and pathogenic mutations facilitate the formation of intracellular aggregates of TDP-43. Hum. Mol. Genet. 2009, 18:3353-3364.
30. Shiina Y., Arima K., Tabunoki H., Satoh J. TDP-43 dimerizes in human cells in culture. Cell. Mol. Neurobiol. 2010, 30:641-652.
31. Shamoo Y., Abdul-Manan N., Williams K.R. Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res. 1995, 23:725-728.
32. Swarup V., Phaneuf D., Dupre N., Petri S., Strong M., Kriz J., Julien J.P. Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor kappaB-mediated pathogenic pathways. J. Exp. Med. 2011, 208:2429-2447.
33. Auweter S.D., Oberstrass F.C., Allain F.H.-T. Sequence-specific binding of single-stranded RNA: is there a code for recognition?. Nucleic Acids Res. 2006, 34:4943-4959.