Identification and analysis of residues contained on beta --> alpha loops of the dual-substrate (beta alpha)8 phosphoribosyl isomerase A specific for its phosphoribosyl anthranilate isomerase activity.

alpha loops of the dual-substrate (beta alpha)8 phosphoribosyl isomerase A specific for its phosphoribosyl anthranilate isomerase activity. -->
Autoři: Noda-García L; Evolution of Metabolic Diversity Laboratory, Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), CINVESTAV-IPN, Km 9.6 Libramiento Norte, Carretera Irapuato-León, Irapuato, C.P. 36822, México., Camacho-Zarco AR, Verdel-Aranda K, Wright H, Soberón X, Fülöp V, Barona-Gómez F
Zdroj: Protein science : a publication of the Protein Society [Protein Sci] 2010 Mar; Vol. 19 (3), pp. 535-43.
Způsob vydávání: Journal Article; Research Support, Non-U.S. Gov't
Jazyk: English
Informace o časopise: Publisher: Cold Spring Harbor Laboratory Press Country of Publication: United States NLM ID: 9211750 Publication Model: Print Cited Medium: Internet ISSN: 1469-896X (Electronic) Linking ISSN: 09618368 NLM ISO Abbreviation: Protein Sci Subsets: MEDLINE
Imprint Name(s): Publication: 2001- : Woodbury, NY : Cold Spring Harbor Laboratory Press
Original Publication: New York, N.Y. : Cambridge University Press, c1992-
Výrazy ze slovníku MeSH: Evolution, Molecular*, Aldose-Ketose Isomerases/*chemistry , Streptomyces coelicolor/*enzymology, Aldose-Ketose Isomerases/genetics ; Amino Acid Sequence ; Arginine/chemistry ; Asparagine/chemistry ; Catalytic Domain ; Crystallography, X-Ray ; Kinetics ; Protein Conformation ; Protein Structure, Secondary ; Sequence Analysis, Protein ; Serine/chemistry ; Threonine/chemistry
Abstrakt: A good model to experimentally explore evolutionary hypothesis related to enzyme function is the ancient-like dual-substrate (beta alpha)(8) phosphoribosyl isomerase A (PriA), which takes part in both histidine and tryptophan biosynthesis in Streptomyces coelicolor and related organisms. In this study, we determined the Michaelis-Menten enzyme kinetics for both isomerase activities in wild-type PriA from S. coelicolor and in selected single-residue monofunctional mutants, identified after Escherichia coli in vivo complementation experiments. Structural and functional analyses of a hitherto unnoticed residue contained on the functionally important beta --> alpha loop 5, namely, Arg(139), which was postulated on structural grounds to be important for the dual-substrate specificity of PriA, is presented for the first time. Indeed, enzyme kinetics analyses done on the mutant variants PriA_Ser(81)Thr and PriA_Arg(139)Asn showed that these residues, which are contained on beta --> alpha loops and in close proximity to the N-terminal phosphate-binding site, are essential solely for the phosphoribosyl anthranilate isomerase activity of PriA. Moreover, analysis of the X-ray crystallographic structure of PriA_Arg(139)Asn elucidated at 1.95 A herein strongly implicates the occurrence of conformational changes in this beta --> alpha loop as a major structural feature related to the evolution of the dual-substrate specificity of PriA. It is suggested that PriA has evolved by tuning a fine energetic balance that allows the sufficient degree of structural flexibility needed for accommodating two topologically dissimilar substrates--within a bifunctional and thus highly constrained active site--without compromising its structural stability.
References: Biochemistry. 1995 Apr 25;34(16):5429-39. (PMID: 7727401)
Biochem Biophys Res Commun. 2008 Jan 4;365(1):16-21. (PMID: 17967415)
Acta Crystallogr D Biol Crystallogr. 2004 Mar;60(Pt 3):534-6. (PMID: 14993684)
Nature. 2008 Aug 7;454(7205):762-5. (PMID: 18594508)
Methods Mol Biol. 2003;235:203-7. (PMID: 12904663)
Biochem Soc Trans. 2009 Aug;37(Pt 4):740-4. (PMID: 19614586)
EMBO Rep. 2005 Feb;6(2):134-9. (PMID: 15654319)
Biochemistry. 2002 Oct 8;41(40):12032-42. (PMID: 12356303)
Nat Chem Biol. 2008 Oct;4(10):617-23. (PMID: 18776889)
Trends Biotechnol. 2007 May;25(5):231-8. (PMID: 17379338)
FEBS Lett. 1999 Jul 2;454(1-2):1-6. (PMID: 10413084)
Science. 2009 Apr 10;324(5924):203-7. (PMID: 19359577)
Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55. (PMID: 15299926)
Chem Biol. 2008 Jun;15(6):607-18. (PMID: 18559271)
Curr Opin Chem Biol. 2009 Feb;13(1):3-9. (PMID: 19249235)
Biochemistry. 2009 Jun 2;48(21):4548-56. (PMID: 19348462)
Methods Enzymol. 1997;276:307-26. (PMID: 27754618)
J Mol Biol. 1999 May 14;288(4):753-63. (PMID: 10329177)
Acta Crystallogr D Biol Crystallogr. 1997 Jul 1;53(Pt 4):448-55. (PMID: 15299911)
Curr Opin Chem Biol. 2006 Oct;10(5):498-508. (PMID: 16939713)
Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9. (PMID: 2025413)
Nat Genet. 2005 Jan;37(1):73-6. (PMID: 15568024)
J Mol Biol. 2009 Apr 10;387(4):949-64. (PMID: 19233201)
Biochemistry. 2009 Aug 4;48(30):7160-8. (PMID: 19588901)
Nat Biotechnol. 2009 Feb;27(2):157-67. (PMID: 19204698)
Science. 2006 Jan 27;311(5760):535-8. (PMID: 16439663)
Annu Rev Microbiol. 1976;30:409-25. (PMID: 791073)
Acta Crystallogr D Biol Crystallogr. 1994 Nov 1;50(Pt 6):869-73. (PMID: 15299354)
J Mol Graph Model. 1997 Apr;15(2):132-4, 112-3. (PMID: 9385560)
Trends Biochem Sci. 2003 Jul;28(7):361-8. (PMID: 12878003)
EMBO Rep. 2003 Mar;4(3):296-300. (PMID: 12634849)
Substance Nomenclature: 2ZD004190S (Threonine)
452VLY9402 (Serine)
7006-34-0 (Asparagine)
94ZLA3W45F (Arginine)
EC 5.3.1.- (Aldose-Ketose Isomerases)
EC 5.3.1.24 (phosphoribosylanthranilate isomerase)
Entry Date(s): Date Created: 20100113 Date Completed: 20100520 Latest Revision: 20211020
Update Code: 20240829
PubMed Central ID: PMC2866278
DOI: 10.1002/pro.331
PMID: 20066665
Autor: Noda-García L; Evolution of Metabolic Diversity Laboratory, Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), CINVESTAV-IPN, Km 9.6 Libramiento Norte, Carretera Irapuato-León, Irapuato, C.P. 36822, México., Camacho-Zarco AR, Verdel-Aranda K, Wright H, Soberón X, Fülöp V, Barona-Gómez F
Jazyk: angličtina
Zdroj: Protein science : a publication of the Protein Society [Protein Sci] 2010 Mar; Vol. 19 (3), pp. 535-43.
DOI: 10.1002/pro.331
Abstrakt: A good model to experimentally explore evolutionary hypothesis related to enzyme function is the ancient-like dual-substrate (beta alpha)(8) phosphoribosyl isomerase A (PriA), which takes part in both histidine and tryptophan biosynthesis in Streptomyces coelicolor and related organisms. In this study, we determined the Michaelis-Menten enzyme kinetics for both isomerase activities in wild-type PriA from S. coelicolor and in selected single-residue monofunctional mutants, identified after Escherichia coli in vivo complementation experiments. Structural and functional analyses of a hitherto unnoticed residue contained on the functionally important beta --> alpha loop 5, namely, Arg(139), which was postulated on structural grounds to be important for the dual-substrate specificity of PriA, is presented for the first time. Indeed, enzyme kinetics analyses done on the mutant variants PriA_Ser(81)Thr and PriA_Arg(139)Asn showed that these residues, which are contained on beta --> alpha loops and in close proximity to the N-terminal phosphate-binding site, are essential solely for the phosphoribosyl anthranilate isomerase activity of PriA. Moreover, analysis of the X-ray crystallographic structure of PriA_Arg(139)Asn elucidated at 1.95 A herein strongly implicates the occurrence of conformational changes in this beta --> alpha loop as a major structural feature related to the evolution of the dual-substrate specificity of PriA. It is suggested that PriA has evolved by tuning a fine energetic balance that allows the sufficient degree of structural flexibility needed for accommodating two topologically dissimilar substrates--within a bifunctional and thus highly constrained active site--without compromising its structural stability.
Databáze: MEDLINE
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