Fine modulation of the respiratory syncytial virus M2-1 protein quaternary structure by reversible zinc removal from its Cys3- His1 motif

Biochemistry

Volumn 52, Issue 39, 2013, Pages 6779-6789

  Esperante, Sebastián A ^a   Noval, María G ^a   Altieri, Tamara A ^a   De Oliveira, Guilherme A P ^b   Silva, Jerson L ^b   De Prat Gay, Gonzalo ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR CONTEXTS; EUKARYOTIC PROTEINS; POLYMERASE COMPLEX; PROTEIN FUNCTIONS; PROTEIN QUATERNARY STRUCTURE; RESPIRATORY SYNCYTIAL VIRUS; SECONDARY STRUCTURES; TRYPTOPHAN RESIDUES;

AMINO ACIDS; DISSOCIATION; MONOMERS; OLIGOMERS; RNA; VIRUSES; ZINC;

PROTEINS;

CYSTEINE; GLUTATHIONE; HISTIDINE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN M2-1; RNA POLYMERASE; TETRAMER; THIONEINE; TRYPTOPHAN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC;

ARTICLE; METAPNEUMOVIRUS; PH; PNEUMOVIRINAE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTON TRANSPORT; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RNA BINDING; VIRION; VIRUS PARTICLE; VIRUS RELEASE;

AMINO ACID MOTIFS; CYSTEINE; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; PROTEIN STRUCTURE, QUATERNARY; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VIRAL PROTEINS; ZINC;

EID: 84885005412     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401029q     Document Type: Article

References (42)

1. Schickli, J. H., Dubovsky, F., and Tang, R. S. (2009) Challenges in developing a pediatric RSV vaccine Hum. Vaccines 5, 582-591
2. Murata, Y. and Falsey, A. R. (2007) Respiratory syncytial virus infection in adults Antiviral Ther. 12, 659-670
3. Meissner, H. C., Rennels, M. B., Pickering, L. K., and Hall, C. B. (2004) Risk of severe respiratory syncytial virus disease, identification of high risk infants and recommendations for prophylaxis with palivizumab Pediatr. Infect. Dis. J. 23, 284-285
4. Ventre, K. and Randolph, A. G. (2007) Ribavirin for respiratory syncytial virus infection of the lower respiratory tract in infants and young children Cochrane Database Syst. Rev. CD000181
5. Collins, P. L., Chanock, R. M., and Murphy, B. R. (2001) Respiratory Syncytial Virus. in Fields Virology, (Fields, B. N., Knipe, D. M., Griffin, D. E., Lamb, R. A., Martin, M. A., Roizman, B, and Straus, S. E., Eds.) 4 th ed., Lippincott Williams & Wilkins Publishers, Philadelphia, PA.
6. Collins, P. L., Hill, M. G., Cristina, J., and Grosfeld, H. (1996) Transcription elongation factor of respiratory syncytial virus, a nonsegmented negative-strand RNA virus Proc. Natl. Acad. Sci. U.S.A. 93, 81-85
7. Fearns, R. and Collins, P. L. (1999) Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription J. Virol. 73, 5852-5864
8. Hardy, R. W., Harmon, S. B., and Wertz, G. W. (1999) Diverse gene junctions of respiratory syncytial virus modulate the efficiency of transcription termination and respond differently to M2-mediated antitermination J. Virol. 73, 170-176
9. Garcia, J., Garcia-Barreno, B., Vivo, A., and Melero, J. A. (1993) Cytoplasmic inclusions of respiratory syncytial virus-infected cells: formation of inclusion bodies in transfected cells that coexpress the nucleoprotein, the phosphoprotein, and the 22K protein Virology 195, 243-247
10. Li, D., Jans, D. A., Bardin, P. G., Meanger, J., Mills, J., and Ghildyal, R. (2008) Association of respiratory syncytial virus M protein with viral nucleocapsids is mediated by the M2-1 protein J. Virol. 82, 8863-8870
11. Tran, T. L., Castagne, N., Dubosclard, V., Noinville, S., Koch, E., Moudjou, M., Henry, C., Bernard, J., Yeo, R. P., and Eleouet, J. F. (2009) The respiratory syncytial virus M2-1 protein forms tetramers and interacts with RNA and P in a competitive manner J. Virol. 83, 6363-6374
12. Esperante, S. A., Chemes, L. B., Sanchez, I. E., and de Prat-Gay, G. (2011) The respiratory syncytial virus transcription antiterminator M(2-1) is a highly stable, zinc binding tetramer with strong pH-dependent dissociation and a monomeric unfolding intermediate Biochemistry 50, 8529-8539
13. Hardy, R. W. and Wertz, G. W. (2000) The Cys(3)-His(1) motif of the respiratory syncytial virus M2-1 protein is essential for protein function J. Virol. 74, 5880-5885
14. Tang, R. S., Nguyen, N., Cheng, X., and Jin, H. (2001) Requirement of cysteines and length of the human respiratory syncytial virus M2-1 protein for protein function and virus viability J. Virol. 75, 11328-11335
15. Zhou, H., Cheng, X., and Jin, H. (2003) Identification of amino acids that are critical to the processivity function of respiratory syncytial virus M2-1 protein J. Virol. 77, 5046-5053
16. Cuesta, I., Geng, X., Asenjo, A., and Villanueva, N. (2000) Structural phosphoprotein M2-1 of the human respiratory syncytial virus is an RNA binding protein J. Virol. 74, 9858-9867
17. Hartlieb, B., Muziol, T., Weissenhorn, W., and Becker, S. (2007) Crystal structure of the C-terminal domain of Ebola virus VP30 reveals a role in transcription and nucleocapsid association Proc. Natl. Acad. Sci. U.S.A. 104, 624-629
18. Blondot, M. L., Dubosclard, V., Fix, J., Lassoued, S., Aumont-Nicaise, M., Bontems, F., Eleouet, J. F., and Sizun, C. (2012) Structure and functional analysis of the RNA- and viral phosphoprotein-binding domain of respiratory syncytial virus M2-1 protein PLoS Pathog. 8, e1002734
19. Esperante, S. A., Paris, G., and de Prat-Gay, G. (2012) Modular unfolding and dissociation of the human respiratory syncytial virus phosphoprotein p and its interaction with the m(2-1) antiterminator: a singular tetramer-tetramer interface arrangement Biochemistry 51, 8100-8110
20. Hall, T. M. (2005) Multiple modes of RNA recognition by zinc finger proteins Curr. Opin. Struct. Biol. 15, 367-373
21. Brown, R. S. (2005) Zinc finger proteins: getting a grip on RNA Curr. Opin. Struct. Biol. 15, 94-98
22. Sun, L., Liu, A., and Georgopoulos, K. (1996) Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development EMBO J. 15, 5358-5369
23. Brooks, S. A. and Blackshear, P. J. (2013) Tristetraprolin (TTP): Interactions with mRNA and proteins, and current thoughts on mechanisms of action Biochim. Biophys. Acta 1829, 666-679
24. Michel, S. L., Guerrerio, A. L., and Berg, J. M. (2003) Selective RNA binding by a single CCCH zinc-binding domain from Nup475 (Tristetraprolin) Biochemistry 42, 4626-4630
25. Amann, B. T., Worthington, M. T., and Berg, J. M. (2003) A Cys3His zinc-binding domain from Nup475/tristetraprolin: a novel fold with a disklike structure Biochemistry 42, 217-221
26. Hudson, B. P., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d Nat. Struct. Mol. Biol. 11, 257-264
27. Lu, P., Lu, G., Yan, C., Wang, L., Li, W., and Yin, P. (2012) Structure of the mRNA splicing complex component Cwc2: insights into RNA recognition Biochem. J. 441, 591-597
28. John, S. P., Wang, T., Steffen, S., Longhi, S., Schmaljohn, C. S., and Jonsson, C. B. (2007) Ebola virus VP30 is an RNA binding protein J. Virol. 81, 8967-8976
29. Modrof, J., Becker, S., and Muhlberger, E. (2003) Ebola virus transcription activator VP30 is a zinc-binding protein J. Virol. 77, 3334-3338
30. Hartlieb, B., Modrof, J., Muhlberger, E., Klenk, H. D., and Becker, S. (2003) Oligomerization of Ebola virus VP30 is essential for viral transcription and can be inhibited by a synthetic peptide J. Biol. Chem. 278, 41830-41836
31. Hunt, J. B., Neece, S. H., and Ginsburg, A. (1985) The use of 4-(2-pyridylazo)resorcinol in studies of zinc release from Escherichia coli aspartate transcarbamoylase Anal. Biochem. 146, 150-157
32. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131, 266-280
33. Uversky, V. N. (2002) Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11, 739-756
34. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4, 2138-2148
35. Mason, S. W., Aberg, E., Lawetz, C., DeLong, R., Whitehead, P., and Liuzzi, M. (2003) Interaction between human respiratory syncytial virus (RSV) M2-1 and P proteins is required for reconstitution of M2-1-dependent RSV minigenome activity J. Virol. 77, 10670-10676
36. Krezel, A. and Bal, W. (2004) Studies of zinc(II) and nickel(II) complexes of GSH, GSSG and their analogs shed more light on their biological relevance Bioinorg. Chem. Appl. 293-305
37. Bixby, K. A., Nanao, M. H., Shen, N. V., Kreusch, A., Bellamy, H., Pfaffinger, P. J., and Choe, S. (1999) Zn2+-binding and molecular determinants of tetramerization in voltage-gated K+ channels Nat. Struct. Biol. 6, 38-43
38. Okorokov, A. L., Waugh, A., Hodgkinson, J., Murthy, A., Hong, H. K., Leo, E., Sherman, M. B., Stoeber, K., Orlova, E. V., and Williams, G. H. (2007) Hexameric ring structure of human MCM10 DNA replication factor EMBO Rep. 8, 925-930
39. Cook, C. R., Kung, G., Peterson, F. C., Volkman, B. F., and Lei, M. (2003) A novel zinc finger is required for Mcm10 homocomplex assembly J. Biol. Chem. 278, 36051-36058
40. Zheng, R., Jenkins, T. M., and Craigie, R. (1996) Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity Proc. Natl. Acad. Sci. U.S.A. 93, 13659-13664
41. Lee, S. P., Xiao, J., Knutson, J. R., Lewis, M. S., and Han, M. K. (1997) Zn2+ promotes the self-association of human immunodeficiency virus type-1 integrase in vitro Biochemistry 36, 173-180
42. Cherepanov, P., Maertens, G., Proost, P., Devreese, B., Van Beeumen, J., Engelborghs, Y., De Clercq, E., and Debyser, Z. (2003) HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells J. Biol. Chem. 278, 372-381