Small-angle x-ray scattering analysis of the bifunctional antibiotic resistance enzyme aminoglycoside (6′) acetyltransferase-Ie/aminoglycoside (2″) phosphotransferase-Ia reveals a rigid solution structure

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 4, 2012, Pages 1899-1906

  Caldwell, Shane J ^a   Berghuis, Albert M ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; ACYLTRANSFERASE; AMINOGLYCOSIDE 2'' PHOSPHOTRANSFERASE IA; AMINOGLYCOSIDE 6' ACETYLTRANSFERASE IE; AMINOGLYCOSIDE ANTIBIOTIC AGENT; COENZYME A; GUANOSINE DIPHOSPHATE; GUANYLYLIMIDODIPHOSPHATE; PHOSPHOTRANSFERASE; POLYPEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; R FACTOR; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

ACETYLTRANSFERASES; DATA INTERPRETATION, STATISTICAL; DIALYSIS; DRUG RESISTANCE, BACTERIAL; MODELS, MOLECULAR; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN CONFORMATION; SCATTERING, RADIATION; SUBSTRATE SPECIFICITY; X-RAYS;

EID: 84858690259     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.06378-11     Document Type: Article

References (49)

1. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2009. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME J. 3:243-251.
2. Azucena E, Grapsas I, Mobashery S. 1997. Properties of a bifunctional bacterial antibiotic resistance enzyme that catalyzes ATP-dependent 2″-phosphorylation and acetyl-CoA-dependent 6=-acetylation of aminoglycosides. J. Am. Chem. Soc. 119:2317-2318. (Pubitemid 27160011)
3. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 98:10037-10041. (Pubitemid 32802969)
4. Boehr DD, Lane WS, Wright GD. 2001. Active site labeling of the gentamicin resistance enzyme AAC(6′)-APH(2″) by the lipid kinase inhibitor wortmannin. Chem. Biol. 8:791-800. (Pubitemid 32752458)
5. Boehr DD, Daigle DM, Wright GD. 2004. Domain-domain interactions in the aminoglycoside antibiotic resistance enzyme AAC(6′)-APH(2″). Biochemistry 43:9846-9855. (Pubitemid 38993834)
6. Burk DL, Hon WC, Leung AK, Berghuis AM. 2001. Structural analyses of nucleotide binding to an aminoglycoside phosphotransferase. Biochemistry 40:8756-8764. (Pubitemid 32709507)
7. Centrón D, Roy PH. 2002. Presence of a group II intron in a multiresistant Serratia marcescens strain that harbors three integrons and a novel gene fusion. Antimicrob. Agents Chemother. 46:1402-1409. (Pubitemid 34415321)
8. Chow JW, et al. 2001. Aminoglycoside resistance genes aph(2″)-Ib and aac(6′)-Im detected together in strains of both Escherichia coli and Enterococcus faecium. Antimicrob. Agents Chemother. 45:2691-2694. (Pubitemid 32906658)
9. Cowan-Jacob SW, et al. 2005. The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure 13:861-871. (Pubitemid 40804389)
10. Culebras E, Martínez JL. 1999. Aminoglycoside resistance mediated by the bifunctional enzyme 6′-N-aminoglycoside acetyltransferase-2″- Oaminoglycoside phosphotransferase. Front. Biosci. 4:D1-D8.
11. D'Costa VM, et al. 2011. Antibiotic resistance is ancient. Nature 477:457-461.
12. D'Costa VM, McGrann KM, Hughes DW, Wright GD. 2006. Sampling the antibiotic resistome. Science 311:374-377. (Pubitemid 43132661)
13. Daigle DM, Hughes DW, Wright GD. 1999. Prodigious substrate specificity of AAC(6′)-APH(2″), an aminoglycoside antibiotic resistance determinant in enterococci and staphylococci. Chem. Biol. 6:99-110. (Pubitemid 29363160)
14. Dowding JE. 1977. Mechanisms of gentamicin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 11:47-50. (Pubitemid 8022372)
15. Dubois V, et al. 2002. Molecular characterization of a novel class 1 integron containing blaGES-1 and a fused product of aac3-Ib/aac6′- Ib′ gene cassettes in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 46:638-645. (Pubitemid 34157645)
16. Filippakopoulos P, et al. 2008. Structural coupling of SH2-kinase domains links Fes and Abl substrate recognition and kinase activation. Cell 134:793-803.
17. Fong DH, Lemke CT, Hwang J, Xiong B, Berghuis AM. 2010. Structure of the antibiotic resistance factor spectinomycin phosphotransferase from Legionella pneumophila. J. Biol. Chem. 285:9545-9555.
18. Green KD, Chen W, Garneau-Tsodikova S. 2011. Effects of altering aminoglycoside structures on bacterial resistance enzyme activities. Antimicrob. Agents Chemother. 55:3207-3213.
19. Hon WC, et al. 1997. Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases. Cell 89:887-895.
20. Kim C, Hesek D, Zajícek J, Vakulenko SB, Mobashery S. 2006. Characterization of the bifunctional aminoglycoside-modifying enzyme ANT(3″)-Ii/AAC(6′)-IId from Serratia marcescens. Biochemistry 45:8368-8377. (Pubitemid 44036543)
21. Kim C, Villegas-Estrada A, Hesek D, Mobashery S. 2007. Mechanistic characterization of the bifunctional aminoglycoside-modifying enzyme AAC(3)-Ib/AAC(6′)-Ib′ from Pseudomonas aeruginosa. Biochemistry 46:5270-5282. (Pubitemid 46683023)
22. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36:1277-1282.
23. Kozin MB, Svergun DI. 2001. Automated matching of high-and low-resolution structural models. J. Appl. Crystallogr. 34:33-41. (Pubitemid 32151714)
24. Llano-Sotelo B, Azucena EF, Jr, Kotra LP, Mobashery S, Chow CS. 2002. Aminoglycosides modified by resistance enzymes display diminished binding to the bacterial ribosomal aminoacyl-tRNA site. Chem. Biol. 9:455-463. (Pubitemid 34439764)
25. Martel A, Masson M, Moreau N, Le Goffic F. 1983. Kinetic studies of aminoglycoside acetyltransferase and phosphotransferase from Staphylococcus aureus RPAL. Relationship between the two activities. Eur. J. Biochem. 133:515-521. (Pubitemid 13060120)
26. Martel A, Moreau N, Capmau ML, Soussy CJ, Duval J. 1977. 2″-O-phosphorylation of gentamicin components by a Staphylococcus aureus strain carrying a plasmid. Antimicrob. Agents Chemother. 12:26-30. (Pubitemid 8143079)
27. Matsuo H, Kobayashi M, Kumagai T, Kuwabara M, Sugiyama M. 2003. Molecular mechanism for the enhancement of arbekacin resistance in a methicillin- resistant Staphylococcus aureus. FEBS Lett. 546:401-406. (Pubitemid 36782447)
28. Maurice F, et al. 2008. Enzyme structural plasticity and the emergence of broad-spectrum antibiotic resistance. EMBO Rep. 9:344-349.
29. Mendes RE, et al. 2004. Integron carrying a novel metallo-betalactamase gene, blaIMP-16, and a fused form of aminoglycosideresistant gene aac(6′)-30/aac(6′)-Ib′: report from the SENTRY Antimicrobial Surveillance Program. Antimicrob. Agents Chemother. 48: 4693-4702. (Pubitemid 39577674)
30. Nagar B, et al. 2003. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112:859-871. (Pubitemid 36378887)
31. Petoukhov MV, Svergun DI. 2005. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J. 89:1237-1250. (Pubitemid 41099005)
32. Ramirez MS, Tolmasky ME. 2010. Aminoglycoside modifying enzymes. Drug Resist. Updat. 13:151-171.
33. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815. (Pubitemid 24007801)
34. Shaw KJ, Rather PN, Hare RS, Miller GH. 1993. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57:138-163. (Pubitemid 23078440)
35. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41:207-234.
36. Svergun DI, Petoukhov MV, Koch MH. 2001. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80:2946-2953. (Pubitemid 32521666)
37. Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25:495-503. (Pubitemid 23564996)
38. Svergun D, Barberato C, Koch MHJ. 1995. CRYSOL-a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28:768-773. (Pubitemid 3014671)
39. Tan RC, Truong TN, McCammon JA, Sussman JL. 1993. Acetylcholinesterase: electrostatic steering increases the rate of ligand binding. Biochemistry 32:401-403. (Pubitemid 23034875)
40. Thompson PR, Schwartzenhauer J, Hughes DW, Berghuis AM, Wright GD. 1999. The COOH terminus of aminoglycoside phosphotransferase (3′)-IIIa is critical for antibiotic recognition and resistance. J. Biol. Chem. 274:30697-30706.
41. Vetting MW, et al. 2008. Mechanistic and structural analysis of aminoglycoside N-acetyltransferase AAC(6′)-Ib and its bifunctional, fluoroquinolone-active AAC(6′)-Ib-cr variant. Biochemistry 47:9825-9835.
42. Volkov VV, Svergun DI. 2003. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36:860-864.
43. Wade RC, Gabdoulline RR, Lüdemann SK, Lounnas V. 1998. Electrostatic steering and ionic tethering in enzyme-ligand binding: insights from simulations. Proc. Natl. Acad. Sci. U. S. A. 95:5942-5949. (Pubitemid 28248943)
44. Waksman SA, Lechevalier HA. 1949. Neomycin, a new antibiotic active against streptomycin-resistant bacteria, including tuberculosis organisms. Science 109:305-307.
45. Wright GD. 1999. Aminoglycoside-modifying enzymes. Curr. Opin. Microbiol. 2:499-503. (Pubitemid 29477176)
46. Wright GD. 2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5:175-186. (Pubitemid 46291277)
47. Young PG, et al. 2009. The crystal structures of substrate and nucleotide complexes of Enterococcus faecium aminoglycoside-2″-phosphotransferase- IIa [APH(2″)-IIa] provide insights into substrate selectivity in the APH(2″) subfamily. J. Bacteriol. 191:4133-4143.
48. Yuan M, et al. 2011. Susceptibility of vertilmicin to modifications by three types of recombinant aminoglycoside-modifying enzymes. Antimicrob. Agents Chemother. 55:3950-3953.
49. Zhang W, Fisher JF, Mobashery S. 2009. The bifunctional enzymes of antibiotic resistance. Curr. Opin. Microbiol. 12:505-511.