Selection of peptides targeting helix 31 of bacterial 16S ribosomal RNA by screening M13 phage-display libraries

Molecules

Volumn 16, Issue 2, 2011, Pages 1211-1239

  Lamichhane, Tek N ^a,b   Abeydeera, N Dinuka ^a,c   Duc, Anne Cécile E ^a,d   Cunningham, Philip R ^a   Chow, Christine S ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d FOX CHASE CANCER CENTER   (United States)

Author keywords

2 methylguanosine; 5 methylcytidine; Helix 31; Modified nucleotides; Peptides; Phage display

Indexed keywords

HYBRID PROTEIN; PEPTIDE; PEPTIDE LIBRARY; RIBOSOME RNA; RNA 16S;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE M13; CHEMISTRY; CONFORMATION; GENETICS; MOLECULAR GENETICS; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; BACTERIOPHAGE M13; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE LIBRARY; PEPTIDES; RECOMBINANT FUSION PROTEINS; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 16S; SURFACE PLASMON RESONANCE;

EID: 79952139676     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules16021211     Document Type: Article

References (84)

1. Mattaj, I.W.; Nagai, K. Recruiting proteins to the RNA world. Nat. Struct. Biol. 1995, 2, 518-522.
2. Agris, P.F. The importance of being modified: Roles of modified nucleosides and Mg2+ in RNA structure and function. Prog. Nucl. Acid Res. Mol. Biol. 1996, 53, 79-129.
3. Xu, Z.; O'Farrell, H.C.; Rife, J.P.; Culver, G.M. A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat. Struct. Mol. Biol. 2008, 15, 534-536. (Pubitemid 351653583)
4. Demirci, H.; Murphy, F., 4th.; Belardinelli, R.; Kelley, A.C.; Ramakrishnan, V.; Gregory, S.T.; Dahlberg, A.E.; Jogl, G. Modification of 16S ribosomal RNA by the KsgA methyltransferase restructures the 30S subunit to optimize ribosome function. RNA 2010, 16, 2319-2324.
5. Olejniczak, M.; Dale, T.; Fahlman, R.P.; Uhlenbeck, O.C. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat. Struct. Mol. Biol. 2005, 12, 788-793. (Pubitemid 43086253)
6. Chow, C.S.; Lamichhane, T.N.; Mahto, S.K. Expanding the nucleotide repertoire of the ribosome with post-transcriptional modifications. ACS Chem. Biol. 2007, 2, 610-619. (Pubitemid 350019778)
7. Decatur, W.A.; Fournier, M.J. rRNA modifications and ribosome function. Trends Biochem. Sci. 2002, 27, 344-351. (Pubitemid 34756517)
8. Cunningham, P.R.; Richard, R.B.; Weitzmann, C.J.; Nurse, K.; Ofengand, J. The absence of modified nucleotides affects both in vitro assembly and in vitro function of the 30S ribosomal subunit of Escherichia coli. Biochimie 1991, 73, 789-796.
9. Basturea, G.N.; Rudd, K.E.; Deutscher, M.P. Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA 2006, 12, 426-434. (Pubitemid 43290870)
10. Green, R.; Noller, H.F. Reconstitution of functional 50S ribosomes from in vitro transcripts of Bacillus stearothermophilus 23S rRNA. Biochemistry 1999, 38, 1772-1779.
11. Green, R.; Noller, H.F. In vitro complementation analysis localizes 23S rRNA posttranscriptional modifications that are required for Escherichia coli 50S ribosomal subunit assembly and function. RNA 1996, 2, 1011-1021. (Pubitemid 26374191)
12. Baxter-Roshek, J.L.; Petrov, A.N.; Dinman, J.D. Optimization of ribosome structure and function by rRNA base modification. PLoS One 2007, 2, e174.
13. Kehrenberg, C.; Schwarz, S.; Jacobsen, L.; Hansen, L.H.; Vester, B. A new mechanism for chloramphenicol, florfenicol and clindamycin resistance: Methylation of 23S ribosomal RNA at A2503. Mol. Microbiol. 2005, 57, 1064-1073. (Pubitemid 41139866)
14. Long, K.S.; Poehlsgaard, J.; Kehrenberg, C.; Schwarz, S.; Vester, B. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrob. Agents Chemother. 2006, 50, 2500-2505. (Pubitemid 43993192)
15. Wright, G.D. The antibiotic resistome: The nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 2007, 5, 175-186. (Pubitemid 46291277)
16. Anderson, A.D.; Nelson, J.M.; Rossiter, S.; Angulo, F.J. Public health consequences of use of antimicrobial agents in food animals in the United States. Microb. Drug Resist. 2003, 9, 373-379. (Pubitemid 38168194)
17. Tomasz, A. Multiple-antibiotic-resistant pathogenic bacteria. A report on the Rockefeller University Workshop. N. Engl. J. Med. 1994, 330, 1247-1251.
18. Gregory, S.T.; Carr, J.F.; Dahlberg, A.E. A mutation in the decoding center of Thermus thermophilus 16S rRNA suggests a novel mechanism of streptomycin resistance. J. Bacteriol. 2005, 187, 2200-2202. (Pubitemid 40316251)
19. Thompson, J.; Skeggs, P.A.; Cundliffe, E. Methylation of 16S ribosomal RNA and resistance to the aminoglycoside antibiotics gentamicin and kanamycin determined by DNA from the gentamicin-producer, Micromonospora purpurea. Mol. Gen. Genet. 1985, 201, 168-173. (Pubitemid 16232771)
20. Pfister, P.; Hobbie, S.; Vicens, Q.; Böttger, E.C.; Westhof, E. The molecular basis for A-site mutations conferring aminoglycoside resistance: Relationship between ribosomal susceptibility and X-ray crystal structures. ChemBioChem 2003, 4, 1078-1088. (Pubitemid 37267597)
21. Cannone, J.J.; Subramanian, S.; Schnare, M.N.; Collett, J.R.; D'Souza, L.M.; Du, Y.; Feng, B.; Lin, N.; Madabusi, L.V.; Müller, K.M.; Pande, N.; Shang, Z.; Yu, N.; Gutell, R.R. The comparative RNA web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 2002, 3, 2.
22. Kowalak, J.A.; Bruenger, E.; Crain, P.F.; McCloskey, J.A. Identities and phylogenetic comparisons of posttranscriptional modifications in 16S ribosomal RNA from Haloferax volcanii. J. Biol. Chem. 2000, 275, 24484-24489. (Pubitemid 30626541)
23. Maden, B.E. The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucl. Acid Res. Mol. Biol. 1990, 39, 241-303.
24. Woese, C.R.; Gupta, R.; Hahn, C.M.; Zillig, W.; Tu, J. The phylogenetic relationships of three sulfur dependent archaebacteria. Syst. Appl. Microbiol. 1984, 5, 97-105.
25. Youvan, D.C.; Hearst, J.E. A sequence from Drosophila melanogaster 18S rRNA bearing the conserved hypermodified nucleoside am psi: Analysis by reverse transcription and highperformance liquid chromatography. Nucl. Acid. Res. 1981, 9, 1723-1741.
26. Lesnyak, D.V.; Osipiuk, J.; Skarina, T.; Sergiev, P.V.; Bogdanov, A.A.; Edwards, A.; Savchenko, A.; Joachimiak, A.; Dontsova, O.A. Methyltransferase that modifies guanine 966 of the 16S rRNA: Functional identification and tertiary structure. J. Biol. Chem. 2007, 282, 5880-5887. (Pubitemid 47093721)
27. Gu, X.R.; Gustafsson, C.; Ku, J.; Yu, M.; Santi, D.V. Identification of the 16S rRNA m5C967 methyltransferase from Escherichia coli. Biochemistry 1999, 38, 4053-4057.
28. Saraiya, A.A.; Lamichhane, T.N.; Chow, C.S.; SantaLucia, J., Jr.; Cunningham, P.R. Identification and role of functionally important motifs in the 970 loop of Escherichia coli 16S ribosomal RNA. J. Mol. Biol. 2008, 376, 645-657.
29. Schuwirth, B.S.; Borovinskaya, M.A.; Hau, C.W.; Zhang, W.; Vila-Sanjurjo, A.; Holton, J.M.; Cate, J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310, 827-834. (Pubitemid 41567336)
30. Yusupov, M.M.; Yusupova, G.Z.; Baucom, A.; Lieberman, K.; Earnest, T.N.; Cate, J.H.; Noller, H.F. Crystal structure of the ribosome at 5.5 Å resolution. Science 2001, 292, 883-896. (Pubitemid 32422479)
31. Johnson, R.M.; Harrison, S.D.; Maclean, D. Therapeutic applications of cell-penetrating peptides. Methods Mol. Biol. 2011, 683, 535-551.
32. Huther, A.; Dietrich, U. The emergence of peptides as therapeutic drugs for the inhibition of HIV- 1. AIDS Rev. 2007, 9, 208-217. (Pubitemid 351181619)
33. Sato, A.K.; Viswanathan, M.; Kent, R.B.; Wood, C.R. Therapeutic peptides: Technological advances driving peptides into development. Curr. Opin. Biotechnol. 2006, 17, 638-642. (Pubitemid 44791908)
34. Gentilucci, L.; De Marco, R.; Cerisoli, L. Chemical modifications designed to improve peptide stability: Incorporation of non-natural amino acids, pseudo-peptide bonds, and cyclization. Curr. Pharm. Des. 2010, 16, 3185-3203.
35. Adessi, C.; Soto, C. Converting a peptide into a drug: Strategies to improve stability and bioavailability. Curr. Med. Chem. 2002, 9, 963-978. (Pubitemid 34498572)
36. Smith, G.P.; Scott, J.K. Libraries of peptides and proteins displayed on filamentous phage. Methods Enzymol. 1993, 217, 228-257.
37. Smith, G.P.; Petrenko, V.A. Phage Display. Chem. Rev. 1997, 97, 391-410. (Pubitemid 127659250)
38. Calcutt, M.J.; Kremer, M.T.; Giblin, M.F.; Quinn, T.P.; Deutscher, S.L. Isolation and characterization of nucleic acid-binding antibody fragments from autoimmune mice-derived bacteriophage display libraries. Gene 1993, 137, 77-83. (Pubitemid 24053735)
39. Laird-Offringa, I.A.; Belasco, J.G. In vitro genetic analysis of RNA-binding proteins using phage display libraries. Methods Enzymol. 1996, 267, 149-168.
40. Frankel, A.D. Peptide models of the Tat-TAR protein-RNA interaction. Protein Sci. 1992, 1, 1539-1542. (Pubitemid 23047470)
41. Grate, D.; Wilson, C. Role REVersal: Understanding how RRE RNA binds its peptide ligand. Structure 1997, 5, 7-11. (Pubitemid 27102853)
42. Patel, D.J. Adaptive recognition in RNA complexes with peptides and protein modules. Curr. Opin. Struct. Biol. 1999, 9, 74-87. (Pubitemid 29471978)
43. Calnan, B.J.; Biancalana, S.; Hudson, D.; Frankel, A.D. Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition. Genes Dev. 1991, 5, 201-210. (Pubitemid 21905945)
44. Powers, J.E.; Marchbank, M.T.; Deutscher, S.L. The isolation of U1 RNA-binding antibody fragments from autoimmune human-derived bacteriophage display libraries. Nucl. Acid. Symp. Ser. 1995, 240-243.
45. Hoet, R.M.; Pieffers, M.; Stassen, M.H.; Raats, J.; de Wildt, R.; Pruijn, G.J.; van den Hoogen, F.; van Venrooij, W.J. The importance of the light chain for the epitope specificity of human anti-U1 small nuclear RNA autoantibodies present in systemic lupus erythematosus patients. J. Immunol. 1999, 163, 3304-3312. (Pubitemid 29431832)
46. Pustowka, A.; Dietz, J.; Ferner, J.; Baumann, M.; Landersz, M.; Königs, C.; Schwalbe, H.; Dietrich, U. Identification of peptide ligands for target RNA structures derived from the HIV-1 packaging signal psi by screening phage-displayed peptide libraries. ChemBioChem 2003, 4, 1093-1097. (Pubitemid 37267599)
47. Dietz, J.; Koch, J.; Kaur, A.; Raja, C.; Stein, S.; Grez, M.; Pustowka, A.; Mensch, S.; Ferner, J.; Möller, L.; Bannert, N.; Tampé, R.; Divita, G.; Mély, Y.; Schwalbe, H.; Dietrich, U. Inhibition of HIV-1 by a peptide ligand of the genomic RNA packaging signal Psi. ChemMedChem 2008, 3, 749-755.
48. Li, M.; Duc, A.C.; Klosi, E.; Pattabiraman, S.; Spaller, M.R.; Chow, C.S. Selection of peptides that target the aminoacyl-tRNA site of bacterial 16S ribosomal RNA. Biochemistry 2009, 48, 8299-8311.
49. Llano-Sotelo, B.; Klepacki, D.; Mankin, A.S. Selection of small peptides, inhibitors of translation. J. Mol. Biol. 2009, 391, 813-819.
50. Mucha, P.; Szyk, A.; Rekowski, P.; Agris, P.F. Sequence-altered peptide adopts optimum conformation for modification-dependent binding of the yeast tRNAPhe anticodon domain. Protein J. 2004, 23, 33-38. (Pubitemid 41399344)
51. Mucha, P.; Szyk, A.; Rekowski, P.; Weiss, P.A.; Agris, P.F. Anticodon domain methylated nucleosides of yeast tRNA(Phe) are significant recognition determinants in the binding of a phage display selected peptide. Biochemistry 2001, 40, 14191-14199. (Pubitemid 33081622)
52. Eshete, M.; Marchbank, M.T.; Deutscher, S.L.; Sproat, B.; Leszczynska, G.; Malkiewicz, A.; Agris, P.F. Specificity of phage display selected peptides for modified anticodon stem and loop domains of tRNA. Protein J. 2007, 26, 61-73. (Pubitemid 46292259)
53. Agris, P.F.; Marchbank, M.T.; Newman, W.; Guenther, R.; Ingram, P.; Swallow, J.; Mucha, P.; Szyk, A.; Rekowski, P.; Peletskaya, E.; Deutscher, S.L. Experimental models of protein-RNA interaction: Isolation and analyses of tRNA(Phe) and U1 snRNA-binding peptides from bacteriophage display libraries. J. Protein Chem. 1999, 18, 425-435. (Pubitemid 29382096)
54. Abeydeera, N.D.; Chow, C.S. Synthesis and characterization of modified nucleotides in the 970 hairpin loop of Escherichia coli 16S ribosomal RNA. Bioorg. Med. Chem. 2009, 17, 5887-5893.
55. Devlin, J.J.; Panganiban, L.C.; Devlin, P.E. Random peptide libraries: A source of specific protein binding molecules. Science 1990, 249, 404-406.
56. Mandava, S.; Makowski, L.; Devarapalli, S.; Uzubell, J.; Rodi, D.J. RELIC-a bioinformatics server for combinatorial peptide analysis and identification of protein-ligand interaction sites. Proteomics 2004, 4, 1439-1460. (Pubitemid 38648034)
57. Korostelev, A.; Trakhanov, S.; Laurberg, M.; Noller, H.F. Crystal structure of a 70S ribosometRNA complex reveals functional interactions and rearrangements. Cell 2006, 126, 1065-1077. (Pubitemid 44380300)
58. Berk, V.; Zhang, W.; Pai, R.D.; Cate, J.H. Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl. Acad. Sci. USA 2006, 103, 15830-15834. (Pubitemid 44657552)
59. Berk, V.; Cate, J.H. Insights into protein biosynthesis from structures of bacterial ribosomes. Curr. Opin. Struct. Biol. 2007, 17, 302-309. (Pubitemid 47021363)
60. Sidhu, S.S.; Koide, S. Phage display for engineering and analyzing protein interaction interfaces. Curr. Opin. Struct. Biol. 2007, 17, 481-487. (Pubitemid 47451773)
61. Park, H.Y.; Kim, J.; Cho, J.H.; Moon, J.Y.; Lee, S.J.; Yoon, M.Y. Phage display screen for peptides that bind bcl-2 protein. J. Biomol. Screen. 2011, 16, 82-89.
62. Llano-Sotelo, B.; Azucena, E.F., Jr.; Kotra, L.P.; Mobashery, S.; Chow, C.S. Aminoglycosides modified by resistance enzymes display diminished binding to the bacterial ribosomal aminoacyltRNA site. Chem. Biol. 2002, 9, 455-463. (Pubitemid 34439764)
63. Cooper, J.P.; Hagerman, P.J. Analysis of fluorescence energy transfer in duplex and branched DNA molecules. Biochemistry 1990, 29, 9261-9268. (Pubitemid 20320893)
64. Maruyama, T.; Shinohara, T.; Ichinose, H.; Kitaoka, M.; Okamura, N.; Kamiya, N.; Goto, M. Mutation detection in DNA oligonucleotides based on a guanine quenching method coupled with enzymatic digestion of single-stranded DNA. Biotechnol. Lett. 2005, 27, 1349-1354. (Pubitemid 41805627)
65. Selmer, M.; Dunham, C.M.; Murphy, F.V., 4th.; Weixlbaumer, A.; Petry, S.; Kelley, A.C.; Weir, J.R.; Ramakrishnan, V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313, 1935-1942. (Pubitemid 44497996)
66. Fourmy, D.; Recht, M.I.; Blanchard, S.C.; Puglisi, J.D. Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 1996, 274, 1367-1371. (Pubitemid 26391459)
67. Fourmy, D.; Yoshizawa, S.; Puglisi, J.D. Paromomycin binding induces a local conformational change in the A-site of 16S rRNA. J. Mol. Biol. 1998, 277, 333-345. (Pubitemid 28174972)
68. Hanahan, D. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 1983, 166, 557-580. (Pubitemid 13027898)
69. Luria, S.E.; Burrous, J.W. Hybridization between Escherichia coli and Shigella. J. Bacteriol. 1957, 74, 461-476.
70. Dower, W.J.; Miller, J.F.; Ragsdale, C.W. High efficiency transformation of E. coli by high voltage electroporation. Nucl. Acid. Res. 1988, 16, 6127-6145.
71. Porath, J.; Carlsson, J.; Olsson, I.; Belfrage, G. Metal chelate affinity chromatography, a new approach to protein fractionation. Nature 1975, 258, 598-599.
72. Gorman, J.J. Fluorescent labeling of cysteinyl residues to facilitate electrophoretic isolation of proteins suitable for amino-terminal sequence analysis. Anal. Biochem. 1987, 160, 376-387. (Pubitemid 17022068)
73. Qin, P.Z.; Pyle, A.M. Site-specific labeling of RNA with fluorophores and other structural probes. Methods 1999, 18, 60-70. (Pubitemid 29440537)
74. Kaiser, E.; Colescott, R.L.; Bossinger, C.D.; Cook, P.I. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides. Anal. Biochem. 1970, 34, 595-598.
75. Mac, F.D.; Fowler, N. On the mechanism of the reaction of ninhydrin with amino acids. II. A spectrophotometric study of hydrindantin reactions. J. Biol. Chem. 1950, 186, 13-22.
76. Custom peptide synthesis: Concentration calculation. http://www. sigmaaldrich.com/life-science/ custom-oligos/custom-peptides/learning-center/ concentration-calculation.html. Accessed on 26 January 2011.
77. Protein assays: Micro BCA Protein Assay Kit. http://www.piercenet.com/ products /browse.cfm?fldID=02020102. Accessed on 26 January 2011
78. Carpino, L.A.; Han, G.Y. The 9-fluorenylmethoxycarbonyl function, a new base-sensitive aminoprotecting group. J. Am. Chem. Soc. 1970, 92, 5748-5749.
79. Rink, H. Solid-phase synthesis of protected peptide fragments using a trialkoxy-diphenyl-methyl ester resin. Tetrahedron Lett. 1987, 28, 3787-3790.
80. Greenfield, L.; Boone, T.; Wilcox, G. DNA sequence of the araBAD promoter in Escherichia coli B/r. Proc. Natl. Acad. Sci. USA 1978, 75, 4724-4728. (Pubitemid 9121257)
81. Kaplan, D.A.; Greenfield, L.; Boone, T.; Wilcox, G. Hybrid plasmids containing the araBAD genes of Escherichia coli B/r. Gene 1978, 3, 177-189. (Pubitemid 9017105)
82. Moazed, D.; Stern, S.; Noller, H.F. Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension. J. Mol. Biol. 1986, 187, 399-416. (Pubitemid 16083780)
83. Davis, T.M.; Wilson, W.D. Surface plasmon resonance biosensor analysis of RNA-small molecule interactions. Methods Enzymol. 2001, 340, 22-51. (Pubitemid 32751695)
84. Marquart, A. SPR pages. Access online http://www.sprpages.nl/Index.php. Accessed on 26 January 2011.