A structure-based approach for targeting the HIV-1 genomic RNA dimerization initiation site

Biochimie

Volumn 89, Issue 10, 2007, Pages 1195-1203

  Ennifar, Eric ^a   Paillart, Jean Christophe ^a   Bernacchi, Serena ^a   Walter, Philippe ^a   Pale, Patrick ^b   Decout, Jean Luc ^c   Marquet, Roland ^a   Dumas, Philippe ^a  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Laboratoire de Pharmacochimie   (France)

Author keywords

Aminoglycoside; Drug design; HIV 1; RNA; Structure

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; GENOMIC RNA; RNA;

ARTICLE; CRYSTAL STRUCTURE; DIMERIZATION; DRUG DESIGN; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; EX VIVO STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOID CELL; PROMOTER REGION; RECEPTOR AFFINITY; RNA STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION SITE; VIRUS GENOME; VIRUS PARTICLE; VIRUS REPLICATION;

AMINOGLYCOSIDES; BASE SEQUENCE; BINDING SITES; DIMERIZATION; GENOME, VIRAL; HIV-1; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; RNA, VIRAL;

BACTERIA (MICROORGANISMS); HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34848831108     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2007.03.003     Document Type: Article

References (42)

1. Bender W., and Davidson N. Mapping of poly(A) sequences in the electron microscope reveals unusual structure of type C oncornavirus RNA molecules. Cell 7 (1976) 595-607
2. Kung H.J., Hu S., Bender W., Bailey J.M., Davidson N., Nicolson M.O., and McAllister R.M. RD-114, baboon, and woolly monkey viral RNA's compared in size and structure. Cell 7 (1976) 609-620
3. Paillart J.C., Dettenhofer M., Yu X.F., Ehresmann C., Ehresmann B., and Marquet R. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem. 279 (2004) 48397-48403
4. Laughrea M., and Jetté L. A 19-nucleotide sequence upstream of the 5′ major splice donor site is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA. Biochemistry 33 (1994) 13464-13474
5. Skripkin E., Paillart J.C., Marquet R., Ehresmann B., and Ehresmann C. Identification of the primary site of the Human Immunodeficiency Virus Type I RNA dimerization in vitro. Proc. Natl. Acad. Sci. USA. 91 (1994) 4945-4949
6. Berkhout B., and van Wamel J.L. Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol. 70 (1996) 6723-6732
7. Clever J.L., and Parslow T.G. Mutant HIV-1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 71 (1997) 3407-3414
8. Laughrea M., Jetté L., Mak J., Kleinman L., Liang C., and Wainberg M.A. Mutations in the kissing-loop hairpin of human immunodeficiency virus type 1 reduce viral infectivity as well as genomic RNA packaging and dimerization. J. Virol. 71 (1997) 3397-3406
9. Paillart J.-C., Berthoux L., Ottmann M., Darlix J.-L., Marquet R., Ehresmann C., and Ehresmann B. A dual role of the dimerization initiation site of HIV-1 in genomic RNA packaging and proviral DNA synthesis. J. Virol. 70 (1996) 8348-8354
10. Clever J.L., Wong M.L., and Parslow T.G. Requirements for kissing-loop-mediated dimerization of human immunodeficiency virus RNA. J. Virol. 70 (1996) 5902-5908
11. Laughrea M., and Jetté L. Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNA can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimer formation. Biochemistry 35 (1996) 1589-1598
12. Muriaux D., Girard P.M., Bonnet-Mathoniere B., and Paoletti J. Dimerization of HIV-1Lai RNA at low ionic strength. An autocomplementary sequence in the 5′ leader region is evidenced by an antisense oligonucleotide. J. Biol. Chem. 270 (1995) 8209-8216
13. Paillart J.C., Marquet R., Skripkin E., Ehresmann B., and Ehresmann C. Mutational analysis of the bipartite dimer linkage structure of HIV-1 genomic RNA. J. Biol. Chem. 269 (1994) 27486-27493
14. Paillart J.C., Skripkin E., Ehresmann B., Ehresmann C., and Marquet R. A loop-loop "kissing" complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc. Natl. Acad. Sci. USA. 93 (1996) 5572-5577
15. Paillart J.C., Westhof E., Ehresmann C., Ehresmann B., and Marquet R. Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA. J. Mol. Biol. 270 (1997) 36-49
16. Lai RNA dimerization process in vitro. Biochemistry 35 (1996) 5075-5082
17. Muriaux D., Rocquigny H.D., Roques B.P., and Paoletti J. NCP7 activates HIV-1 Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J. Biol. Chem. 271 (1996) 33686-33692
18. Rist M.J., and Marino J.P. Mechanism of nucleocapsid protein catalyzed structural isomerization of the dimerization initiation site of HIV-1. Biochemistry 41 (2002) 14762-14770
19. Takahashi K.I., Baba S., Chattopadhyay P., Koyanagi Y., Yamamoto N., Takaku H., and Kawai G. Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA 6 (2000) 96-102
20. Fu W., Gorelick R.J., and Rein A. Characterization of HIV-1 dimeric RNA from wild-type and protease-defective virions. J. Virol. 68 (1994) 5013-5018
21. Bernacchi S., Ennifar E., Toth K., Walter P., Langowski J., and Dumas P. Mechanism of hairpin-duplex conversion for the HIV-1 dimerization initiation site. J. Biol. Chem. 280 (2005) 40112-40121
22. Rist M., and Marino J. Association of an RNA kissing complex analyzed using 2-aminopurine fluorescence. Nucleic Acids Res. 29 (2001) 2401-2408
23. Theilleux-Delalande V., Girard F., Huynh-Dinh T., Lancelot G., and Paoletti J. The HIV-1(Lai) RNA dimerization. Thermodynamic parameters associated with the transition from the kissing complex to the extended dimer. Eur. J. Biochem. 267 (2000) 2711-2719
24. Ennifar E., Yusupov M., Walter P., Marquet R., Ehresmann B., Ehresmann C., and Dumas P. The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure 7 (1999) 1439-1449
25. Ennifar E., Walter P., and Dumas P. A crystallographic study of the binding of 13 metal ions to two related RNA duplexes. Nucleic Acids Res. 31 (2003) 2671-2682
26. Baba S., Takahashi K., Noguchi S., Takaku H., Koyanagi Y., Yamamoto N., and Kawai G. Solution RNA structures of the HIV-1 dimerization initiation site in the kissing-loop and extended-duplex dimers. J. Biochem. (Tokyo) 138 (2005) 583-592
27. Ulyanov N.B., Mujeeb A., Du Z., Tonelli M., Parslow T.G., and James T.L. NMR structure of the full-length linear dimer of stem-loop-1 RNA in the HIV-1 dimer initiation site. J. Biol. Chem. 281 (2006) 16168-16177
28. Ennifar E., and Dumas P. Polymorphism of bulged-out residues in HIV-1 RNA DIS kissing complex and structure comparison with solution studies. J. Mol. Biol. 356 (2006) 771-782
29. Ennifar E., Walter P., Ehresmann B., Ehresmann C., and Dumas P. Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat. Struct. Biol. 8 (2001) 1064-1068
30. Jossinet F., Paillart J.C., Westhof E., Hermann T., Skripkin E., Lodmell J.S., Ehresmann C., Ehresmann B., and Marquet R. Dimerization of HIV-1 genomic RNA of subtypes A and B: RNA loop structure and magnesium binding. RNA 5 (1999) 1222-1234
31. Kieken F., Paquet F., Brule F., Paoletti J., and Lancelot G. A new NMR solution structure of the SL1 HIV-1Lai loop-loop dimer. Nucleic Acids Res. 34 (2006) 343-352
32. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Wimberly B.T., and Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407 (2000) 340-348
33. Fourmy D., Recht M.I., Blanchard S.C., and Puglisi J.D. Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274 (1996) 1367-1371
34. Lynch S.R., Gonzalez R.L., and Puglisi J.D. Comparison of X-ray crystal structure of the 30S subunit-antibiotic complex with NMR structure of decoding site oligonucleotide-paromomycin complex. Structure (Camb.) 11 (2003) 43-53
35. Vicens Q., and Westhof E. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure Fold Des 9 (2001) 647-658
36. Ennifar E., Paillart J.C., Marquet R., Ehresmann B., Ehresmann C., Dumas P., and Walter P. HIV-1 RNA dimerization initiation site is structurally similar to the ribosomal A site and binds aminoglycoside antibiotics. J. Biol. Chem. 278 (2003) 2723-2730
37. Recht M.I., Fourmy D., Blanchard S.C., Dahlquist K.D., and Puglisi J.D. RNA sequence determinants for aminoglycoside binding to an A-site rRNA model oligonucleotide. J. Mol. Biol. 262 (1996) 421-436
38. Wong C.H., Hendrix M., Priestley E.S., and Greenberg W.A. Specificity of aminoglycoside antibiotics for the A-site of the decoding region of ribosomal RNA. Chem. Biol. 5 (1998) 397-406
39. O'Connor S., Lam L.K., Jones N.D., and Chaney M.O. Apramycin, a unique aminocyclitol antibiotic. J. Org. Chem. 41 (1976) 2087-2092
40. Ennifar E., Paillart J.C., Bodlenner A., Walter P., Weibel J.M., Aubertin A.M., Pale P., Dumas P., and Marquet R. Targeting the dimerization initiation site of HIV-1 RNA with aminoglycosides: from crystal to cell. Nucleic Acids Res. 34 (2006) 2328-2339
41. Francois B., Russell R.J., Murray J.B., Aboul-ela F., Masquida B., Vicens Q., and Westhof E. Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 33 (2005) 5677-5690
42. Shandrick S., Zhao Q., Han Q., Ayida B.K., Takahashi M., Winters G.C., Simonsen K.B., Vourloumis D., and Hermann T. Monitoring molecular recognition of the ribosomal decoding site. Angew. Chem. Int. Ed. Engl. 43 (2004) 3177-3182