Probing the mechanisms of DEAD-box proteins as general RNA chaperones: The C-terminal domain of CYT-19 mediates general recognition of RNA

Biochemistry

Volumn 46, Issue 11, 2007, Pages 3013-3022

  Grohman, Jacob K ^a,b   Del Campo, Mark ^a   Bhaskaran, Hari ^a   Tijerina, Pilar ^a   Lambowitz, Alan M ^a   Russell, Rick ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EQUILIBRIUM BINDING EXPERIMENTS; RIBOZYME; RNA-BINDING PROTEINS; TRUNCATED PROTEIN;

AMINO ACIDS; BINDING SITES; MOLECULAR STRUCTURE; PROTEOLYSIS; RNA;

PROTEINS;

AMINO ACID; ARGININE; DEAD BOX PROTEIN; OLIGONUCLEOTIDE; PROTEIN CYT19; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BASE PAIRING; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COVALENT BOND; INTRON; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; RNA BINDING; RNA STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TETRAHYMENA;

ANIMALS; BASE SEQUENCE; BINDING SITES; DEAD-BOX RNA HELICASES; MOLECULAR CHAPERONES; NUCLEIC ACID CONFORMATION; PAPAIN; PROTOZOAN PROTEINS; RNA; RNA, CATALYTIC; TETRAHYMENA THERMOPHILA;

TETRAHYMENA;

EID: 33947362880     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0619472     Document Type: Article

References (57)

1. Mohr, S., Stryker, J. M., and Lambowitz, A. M. (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing, Cell 109, 769-779.
2. Tanner, N. K., and Linder, P. (2001) DExD/H box RNA helicases: From generic motors to specific dissociation functions, Mol. Cell 8, 251-262.
3. Silverman, E., Edwalds-Gilbert, G., and Lin, R. J. (2003) DExD/ H-box proteins and their partners: Helping RNA helicases unwind, Gene 312, 1-16.
4. Cordin, O., Banroques, J., Tanner, N. K., and Linder, P. (2006) The DEAD-box protein family of RNA helicases, Gene 367, 17-37.
5. Wang, Y., and Guthrie, C. (1998) PRP16, a DEAH-box RNA helicase, is recruited to the spliceosome primarily via its nonconserved N-terminal domain, RNA 4, 1216-1229.
6. Schneider, S., and Schwer, B. (2001) Functional domains of the yeast splicing factor Prp22p, J. Biol. Chem. 276, 21184-21191.
7. Kossen, K., Karginov, F. V., and Uhlenbeck, O. C. (2002) The carboxy-terminal domain of the DExD/H protein YxiN is sufficient to confer specificity for 23S rRNA, J. Mol. Biol. 324, 625-636.
8. Karginov, F. V., Caruthers, J. M., Hu, Y., McKay, D. B., and Uhlenbeck, O. C. (2005) YxiN is a modular protein combining a DEx(D/H) core and a specific RNA-binding domain, J. Biol. Chem. 280, 35499-35505.
9. Wang, S., Hu, Y., Overgaard, M. T., Karginov, F. V., Uhlenbeck, O. C., and McKay, D. B. (2006) The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold, RNA 12, 959-967.
10. Huang, H. R., Rowe, C. E., Mohr, S., Jiang, Y., Lambowitz, A. M., and Perlman, P. S. (2005) The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function, Proc. Natl. Acad. Sci. U.S.A. 102, 163-168.
11. Tijerina, P., Bhaskaran, H., and Russell, R. (2006) Non-specific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone, Proc. Natl. Acad. Sci. U.S.A. 103, 16698-16703.
12. Mohr, S., Matsuura, M., Perlman, P. S., and Lambowitz, A. M. (2006) A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone, Proc. Natl. Acad. Sci. U.S.A. 103, 3569-3574.
13. Karpel, R. L., Miller, N. S., and Fresco, J. R. (1982) Mechanistic studies of ribonucleic acid renaturation by a helix-destabilizing protein, Biochemistry 21, 2102-2108.
14. Herschlag, D. (1995) RNA chaperones and the RNA folding problem, J. Biol. Chem. 270, 20871-20874.
15. Burd, C. G., and Dreyfuss, G. (1994) Conserved structures and diversity of functions of RNA-binding proteins, Science 265, 615-621.
16. Zaug, A. J., Grosshans, C. A., and Cech, T. R. (1988) Sequence-specific endoribonuclease activity of the Tetrahymena ribozyme: Enhanced cleavage of certain oligonucleotide substrates that form mismatched ribozyme-substrate complexes, Biochemistry 27, 8924-8931.
17. Russell, R., and Herschlag, D. (1999) Specificity from steric restrictions in the guanosine binding pocket of a group I ribozyme, RNA 5, 158-166.
18. Kristelly, R., Earnest, B. T., Krishnamoorthy, L., and Tesmer, J. J. (2003) Preliminary structure analysis of the DH/PH domains of leukemia-associated RhoGEF, Acta Crystallogr., Sect. D: Biol. Crystallogr. 59, 1859-1862.
19. Kapust, R. B., Tozser, J., Fox, J. D., Anderson, D. E., Cherry, S., Copeland, T. D., and Waugh, D. S. (2001) Tobacco etch virus protease: Mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency, Protein Eng. 14, 993-1000.
20. Wong, I., Chao, K. L., Bujalowski, W., and Lohman, T. M. (1992) DNA-induced dimerization of the Escherichia coli rep helicase. Allosteric effects of single-stranded and duplex DNA, J. Biol. Chem. 267, 7596-7610.
21. Russell, R., and Herschlag, D. (2001) Probing the folding landscape of the Tetrahymena ribozyme: Commitment to form the native conformation is late in the folding pathway, J. Mol. Biol. 308, 839-851.
22. Guo, Q. B., Akins, R. A., Garriga, G., and Lambowitz, A. M. (1991) Structural analysis of the Neurospora mitochondrial large rRNA intron and construction of a mini-intron that shows protein-dependent splicing, J. Biol. Chem. 266, 1809-1819.
23. Choe, Y., Leonetti, F., Greenbaum, D. C., Lecaille, F., Bogyo, M., Bromme, D., Ellman, J. A., and Craik, C. S. (2006) Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities, J. Biol. Chem. 281, 12824-12832.
24. Yang, Q., and Jankowsky, E. (2006) The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases, Nat. Struct. Mol. Biol. 13, 981-986.
25. Russell, R., Millett, I. S., Doniach, S., and Herschlag, D. (2000) Small angle X-ray scattering reveals a compact intermediate in RNA folding, Nat. Struct. Biol. 7, 367-370.
26. Russell, R., Das, R., Suh, H., Travers, K., Laederach, A., Engelhardt, M., and Herschlag, D. (2006) The paradoxical behavior of a highly structured misfolded intermediate in RNA folding, J. Mol. Biol. 363, 531-544.
27. Mannella, C. A., Collins, R. A., Green, M. R., and Lambowitz, A. M. (1979) Defective splicing of mitochondrial rRNA in cytochrome-deficient nuclear mutants of Neurospora crassa, Proc. Natl. Acad. Sci. U.S.A. 76, 2635-2639.
28. Akins, R. A., and Lambowitz, A. M. (1987) A protein required for splicing group I introns in Neurospora mitochondria is mitochondrial tyrosyl-tRNA synthetase or a derivative thereof, Cell 50, 331-345.
29. Gibson, T. J., and Thompson, J. D. (1994) Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: Implications for monomeric RNA helicases, Nucleic Acids Res. 22, 2552-2556.
30. Zhang, S., and Grosse, F. (1997) Domain structure of human nuclear DNA helicase II (RNA helicase A), J. Biol. Chem. 272, 11487-11494.
31. Lorkovic, Z. J., Herrmann, R. G., and Oelmuller, R. (1997) PRH75, a new nucleus-localized member of the DEAD-box protein family from higher plants, Mol. Cell. Biol. 17, 2257-2265.
32. Kiledjian, M., and Dreyfuss, G. (1992) Primary structure and binding activity of the hnRNP U protein: Binding RNA through RGG box, EMBO J. 11, 2655-2664.
33. Lohman, T. M., and Bjornson, K. P. (1996) Mechanisms of helicase-catalyzed DNA unwinding, Annu. Rev. Biochem. 65, 169-214.
34. Ha, T., Rasnik, I., Cheng, W., Babcock, H. P., Gauss, G. H., Lohman, T. M., and Chu, S. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase, Nature 419, 638-641.
35. Talavera, M. A., Matthews, E. E., Eliason, W. K., Sagi, I., Wang, J., Henn, A., and de la Cruz, E. M. (2006) Hydrodynamic characterization of the DEAD-box RNA helicase DbpA, J. Mol. Biol. 355, 697-707.
36. Rogers, G. W., Jr., Lima, W. F., and Merrick, W. C. (2001) Further characterization of the helicase activity of eIF4A. Substrate specificity, J. Biol. Chem. 276, 12598-12608.
37. Bizebard, T., Ferlenghi, I., Iost, I., and Dreyfus, M. (2004) Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases, Biochemistry 43, 7857-7866.
38. Jankowsky, E., Gross, C. H., Shuman, S., and Pyle, A. M. (2000) The DExH protein NPH-II is a processive and directional motor for unwinding RNA, Nature 403, 447-451.
39. Jankowsky, E., Gross, C. H., Shuman, S., and Pyle, A. M. (2001) Active disruption of an RNA-protein interaction by a DExH/D RNA helicase, Science 291, 121-125.
40. Fairman, M. E., Maroney, P. A., Wang, W., Bowers, H. A., Gollnick, P., Nilsen, T. W., and Jankowsky, E. (2004) Protein displacement by DExH/D RNA helicases without duplex unwinding, Science 304, 730-734.
41. Sengoku, T., Nureki, O., Nakamura, A., Kobayashi, S., and Yokoyama, S. (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa, Cell 125, 287-300.
42. Walstrum, S. A., and Uhlenbeck, O. C. (1990) The self-splicing RNA of Tetrahymena is trapped in a less active conformation by gel purification, Biochemistry 29, 10573-10576.
43. Woodson, S. A., and Cech, T. R. (1991) Alternative secondary structures in the 5′ exon affect both forward and reverse self-splicing of the Tetrahymena intervening sequence RNA, Biochemistry 30, 2042-2050.
44. Pan, T., and Sosnick, T. R. (1997) Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity, Nat. Struct. Biol. 4, 931-938.
45. Treiber, D. K., Rook, M. S., Zarrinkar, P. P., and Williamson, J. R. (1998) Kinetic intermediates trapped by native interactions in RNA folding, Science 279, 1943-1946.
46. Russell, R., and Herschlag, D. (1999) New pathways in folding of the Tetrahymena group I RNA enzyme, J. Mol. Biol. 291, 1155-1167.
47. Schroeder, R., Barta, A., and Semrad, K. (2004) Strategies for RNA folding and assembly, Nat. Rev. Mol. Cell. Biol. 5, 908-919.
48. Chuang, R. Y., Weaver, P. L., Liu, Z., and Chang, T. H. (1997) Requirement of the DEAD-box protein Ded1p for messenger RNA translation, Science 275, 1468-1471.
49. de la Cruz, J., Iost, I., Kressler, D., and Linder, P. (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. U.S.A. 94, 5201-5206.
50. Marsden, S., Nardelli, M., Linder, P., and McCarthy, J. E. (2006) Unwinding single RNA molecules using helicases involved in eukaryotic translation initiation, J. Mol. Biol. 361, 327-335.
51. Zapp, M. L., and Green, M. R. (1989) Sequence-specific RNA binding by the HIV-1 Rev protein, Nature 342, 714-716.
52. Dingwall, C., Ernberg, I., Gait, M. J., Green, S. M., Heaphy, S., Karn, J., Lowe, A. D., Singh, M., Skinner, M. A., and Valerio, R. (1989) Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro, Proc. Natl. Acad. Sci. U.S.A. 86, 6925-6929.
53. Weeks, K. M., Ampe, C., Schultz, S. C., Steitz, T. A., and Crothers, D. M. (1990) Fragments of the HIV-1 Tat protein specifically bind TAR RNA, Science 249, 1281-1285.
54. Austin, R. J., Xia, T., Ren, J., Takahashi, T. T., and Roberts, R. W. (2002) Designed arginine-rich RNA-binding peptides with picomolar affinity, J. Am. Chem. Soc. 124, 10966-10967.
55. Bayer, T. S., Booth, L. N., Knudsen, S. M., and Ellington, A. D. (2005) Arginine-rich motifs present multiple interfaces for specific binding by RNA, RNA 11, 1848-1857.
56. Svitkin, Y. V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G. J., and Sonenberg, N. (2001) The requirement for eukaryotic initiation factor 4A (e1F4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure, RNA 7, 382-394.
57. Linder, P. (2003) Yeast RNA helicases of the DEAD-box family involved in translation initiation, Biol. Cell 95, 157-167.