Cross-talk between prion protein and quadruplex-forming nucleic acids: A dynamic complex formation

Nucleic Acids Research

Volumn 41, Issue 1, 2013, Pages

  Cavaliere, Paola ^a,d   Pagano, Bruno ^a   Granata, Vincenzo ^b   Prigent, Stephanie ^c   Rezaei, Human ^c   Giancola, Concetta ^a   Zagari, Adriana ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c INRA Institut National de la Recherche Agronomique   (France)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; GUANINE; ISOPROTEIN; NUCLEIC ACID; OLIGOMER; PRION PROTEIN; QUADRUPLEX FORMING NUCLEIC ACID; THYMINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; ISOTHERMAL TITRATION CALORIMETRY; KINETICS; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; THERMODYNAMICS;

BINDING SITES; CALORIMETRY; CIRCULAR DICHROISM; DNA; G-QUADRUPLEXES; KINETICS; PRIONS; PROTEIN BINDING; RNA; SURFACE PLASMON RESONANCE; THERMODYNAMICS;

EID: 84871747710     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks970     Document Type: Article

References (52)

1. Prusiner, S.B. (1982) Novel proteinaceous infectious particles cause scrapie. Science, 216, 136-144.
2. Prusiner, S.B. (1998) Prions. Proc. Natl Acad. Sci. USA, 95, 13363-13383.
3. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M.A., Brentani, R.R., Foguel, D. and Silva, J.L. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J. Biol. Chem., 276, 49400-49409.
4. Nandi, P.K. and Leclerc, E. (1999) Polymerization of murine recombinant prion protein in nucleic acid solution. Arch. Virol., 144, 1751-1763.
5. Telling, G.C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F.E., Dearmond, S.J. and Prusiner, S.B. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell, 83, 79-90.
6. Ma, J., Wollmann, R. and Lindquist, S. (2002) Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science, 298, 1781-1785.
7. Jimenez, J.S. (2010) Protein-DNA interaction at the origin of neurological diseases: a hypothesis. J. Alzheimers Dis., 22, 375-391.
8. Mange, A., Crozet, C., Lehmann, S. and Beranger, F. (2004) Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin. J. Cell Sci., 117, 2411-2416.
9. Mironov, A.J., Latawiec, D., Wille, H., Bouzamondo-Bernstein, E., Legname, G., Williamson, R.A., Burton, D., DeArmond, S.J., Prusiner, S.B. and Peters, P.J. (2003) Cytosolic prion protein in neurons. J. Neurosci., 23, 7183-7193.
10. Strom, A., Wang, G.S., Picketts, D.J., Reimer, R., Stuke, A.W. and Scott, F.W. (2011) Cellular prion protein localizes to the nucleus of endocrine and neuronal cells and interacts with structural chromatin components. Eur. J. Cell Biol., 90, 414-419.
11. Yamasaki, T., Suzuki, A., Shimizu, T., Watarai, M., Hasebe, R. and Horiuchi, M. (2012) Characterization of intracellular localization of PrPSc in prion-infected cells using a mAb that recognizes the region consisting of aa 119-127 of mouse PrP. J. Gen. Virol., 93, 668-680.
12. Takemura, K., Wang, P., Vorberg, I., Surewicz, W., Priola, S.A., Kanthasamy, A., Pottathil, R., Chen, S.G. and Sreevatsan, S. (2006) DNA aptamers that bind to PrP(C) and not PrP(Sc) show sequence and structure specificity. Exp. Biol. Med. (Maywood), 231, 204-214.
13. Adler, V., Zeiler, B., Kryukov, V., Kascsak, R., Rubenstein, R. and Grossman, A. (2003) Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J. Mol. Biol., 332, 47-57.
14. Gabus, C., Auxilien, S., Pechoux, C., Dormont, D., Swietnicki, W., Morillas, M., Surewicz, W., Nandi, P. and Darlix, J.L. (2001) The prion protein has DNA strand transfer properties similar to retroviral nucleocapsid protein. J. Mol. Biol., 307, 1011-1021.
15. Gabus, C., Derrington, E., Leblanc, P., Chnaiderman, J., Dormont, D., Swietnicki, W., Morillas, M., Surewicz, W.K., Marc, D., Nandi, P. et al. (2001) The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J. Biol. Chem., 276, 19301-19309.
16. Gomes, M.P., Vieira, T.C., Cordeiro, Y. and Silva, J.L. (2012) The role of RNA in mammalian prion protein conversion. Wiley Interdiscip. Rev. RNA, 3, 415-428.
17. Guichard, C., Ivanyi-Nagy, R., Sharma, K.K., Gabus, C., Marc, D., Mely, Y. and Darlix, J.L. (2011) Analysis of nucleic acid chaperoning by the prion protein and its inhibition by oligonucleotides. Nucleic Acids Res., 39, 8544-8558.
18. Lima, L.M., Cordeiro, Y., Tinoco, L.W., Marques, A.F., Oliveira, C.L., Sampath, S., Kodali, R., Choi, G., Foguel, D., Torriani, I. et al. (2006) Structural insights into the interaction between prion protein and nucleic acid. Biochemistry, 45, 9180-9187.
19. Deleault, N.R., Harris, B.T., Rees, J.R. and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc. Natl Acad. Sci. USA, 104, 9741-9746.
20. Wang, F., Wang, X., Yuan, C.G. and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science, 327, 1132-1135.
21. Mashima, T., Matsugami, A., Nishikawa, F., Nishikawa, S. and Katahira, M. (2009) Unique quadruplex structure and interaction of an RNA aptamer against bovine prion protein. Nucleic Acids Res., 37, 6249-6258.
22. Mercey, R., Lantier, I., Maurel, M.C., Grosclaude, J., Lantier, F. and Marc, D. (2006) Fast, reversible interaction of prion protein with RNA aptamers containing specific sequence patterns. Arch. Virol., 151, 2197-2214.
23. Murakami, K., Nishikawa, F., Noda, K., Yokoyama, T. and Nishikawa, S. (2008) Anti-bovine prion protein RNA aptamer containing tandem GGA repeat interacts both with recombinant prion protein and its b isoform with high affinity. Prion, 2, 73-78.
24. Sekiya, S., Noda, K., Nishikawa, F., Yokoyama, T., Kumar, P.K. and Nishikawa, S. (2006) Characterization and application of a novel RNA aptamer against the mouse prion protein. J. Biochem., 139, 383-390.
25. Weiss, S., Proske, D., Neumann, M., Groschup, M.H., Kretzschmar, H.A., Famulok, M. and Winnacker, E.L. (1997) RNA aptamers specifically interact with the prion protein PrP. J. Virol., 71, 8790-8797.
26. Proske, D., Gilch, S., Wopfner, F., Schatzl, H.M., Winnacker, E.L. and Famulok, M. (2002) Prion-protein-specific aptamer reduces PrPSc formation. Chembiochem., 3, 717-725.
27. Matsugami, A., Ouhashi, K., Kanagawa, M., Liu, H., Kanagawa, S., Uesugi, S. and Katahira, M. (2001) An intramolecular quadruplex of (GGA)(4) triplet repeat DNA with a G:G:G:G tetrad and a G(:A):G(:A):G(:A):G heptad, and its dimeric interaction. J. Mol. Biol., 19, 255-269.
28. Pagano, B., Mattia, C.A., Cavallo, L., Uesugi, S., Giancola, C. and Fraternali, F. (2008) Stability and cations coordination of DNA and RNA 14-mer G-quadruplexes: a multiscale computational approach. J. Phys. Chem. B, 112, 12115-12123.
29. Heller, M., Flemington, E., Kieff, E. and Deininger, P. (1985) Repeat arrays in cellular DNA related to the Epstein-Barr virus IR3 repeat. Mol. Cell Biol., 5, 457-465.
30. Eddy, J. and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res., 36, 1321-1333.
31. Huppert, J.L. and Balasubramanian, S. (2001) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 35, 406-413.
32. Patel, D.J., Phan, A.T. and Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 5′-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res., 35, 7429-7455.
33. Laughlan, G., Murchie, A.I.H., Norman, D.G., Moore, M.H., Moody, P.C., Lilley, D.M. and Luisi, B. (1994) The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science, 265, 520-524.
34. Rezaei, H., Marc, D., Choiset, Y., Takahashi, M., Hui Bon Hoa, G., Haertle, T., Grosclaude, J. and Debey, P. (2000) High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility. Eur. J. Biochem., 267, 2833-2839.
35. Eghiaian, F., Daubenfeld, T., Quenet, Y., van Audenhaege, M., Bouin, A.P., van der Rest, G., Grosclaude, J. and Rezaei, H. (2007) Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage. Proc. Natl Acad. Sci. USA, 104, 7414-7419.
36. Cantor, C.R., Warshaw, M.M. and Shapiro, H. (1970) Oligonucleotide interactions. III Circular dichroism studies of the conformation of deoxyoligonucleotides. Biopolymers, 9, 1059-1077.
37. Pagano, B., Mattia, C.A. and Giancola, C. (2009) Applications of isothermal titration calorimetry in biophysical studies of G-quadruplexes. Int. J. Mol. Sci., 10, 2935-2957.
38. Rhie, A., Kirby, L., Sayer, N., Wellesley, R., Disterer, P., Sylvester, I., Gill, A., Hope, J., James, W. and Tahiri-Alaoui, A. (2003) Characterization of 2′-fluoro-RNA aptamers that bind preferentially to disease-associated conformations of prion protein and inhibit conversion. J. Biol. Chem., 278, 39697-39705.
39. Gomes, M.P., Millen, T.A., Ferreira, P.S., e Silva, N.L., Vieira, T.C., Almeida, M.S., Silva, J.L. and Cordeiro, Y. (2008) Prion protein complexed to N2a cellular RNAs through its N-terminal domain forms aggregates and is toxic to murine neuroblastoma cells. J. Biol. Chem., 283, 19616-19625.
40. Bera, A., Roche, A.C. and Nandi, P.K. (2007) Bending and unwinding of nucleic acid by prion protein. Biochemistry, 46, 1320-1328.
41. Nandi, P.K., Leclerc, E., Nicole, J.C. and Takahashi, M. (2002) DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J. Mol. Biol., 322, 153-161.
42. Nandi, P.K. and Nicole, J.C. (2004) Nucleic acid and prion protein interaction produces spherical amyloids which can function in vivo as coats of spongiform encephalopathy agent. J. Mol. Biol., 344, 827-837.
43. Vuzman, D. and Levy, Y. (2010) DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail. Proc. Natl Acad. Sci. USA, 107, 21004-21009.
44. Darnell, J.C., Jensen, K.B., Jin, P., Brown, V., Warren, S.T. and Darnell, R.B. (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell, 107, 489-499.
45. Giraldo, R. and Rhodes, D. (1994) The yeast telomere-binding protein RAP1 binds to and promotes the formation of DNA quadruplexes in telomeric DNA. EMBO J., 13, 2411-2420.
46. Pagano, B., Martino, L., Randazzo, A. and Giancola, C. (2008) Stability and binding properties of a modified thrombin binding aptamer. Biophys. J., 94, 562-569.
47. Simonsson, T. (2001) G-quadruplex DNA structures-variations on a theme. Biol. Chem., 382, 621-628.
48. Giri, B., Smaldino, P.J., Thys, R.G., Creacy, S.D., Routh, E.D., Hantgan, R.R., Lattmann, S., Nagamine, Y., Akman, S.A. and Vaughn, J.P. (2011) G4 resolvase 1 tightly binds and unwinds unimolecular G4-DNA. Nucleic Acids Res., 39, 7161-7178.
49. Harrington, C., Lan, Y. and Akman, S.A. (1997) The identification and characterization of a G4-DNA resolvase activity. J. Biol. Chem., 272, 24631-24636.
50. Paramasivam, M., Membrino, A., Cogoi, S., Fukuda, H., Nakagama, H. and Xodo, L.E. (2009) Protein hnRNP A1 and its derivative Up1 unfold quadruplex DNA in the human KRAS promoter: implications for transcription. Nucleic Acids Res., 37, 2841-2853.
51. Marc, D. (2010) Aptamers to explore prion protein interactions with nucleic acids. Front. Biosci., 15, 550-563.
52. Harris, D.A. (2003) Trafficking, turnover and membrane topology of PrP. Br. Med. Bull., 66, 71-85.