Radical-mediated ring contraction in the biosynthesis of 7-deazapurines

Current Opinion in Structural Biology

Volumn 35, Issue , 2015, Pages 116-124

  Bandarian, Vahe ^a   Drennan, Catherine L ^b  

^a UNIVERSITY OF UTAH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 CARBOXY 7 DEAZAGUANINE; 7 CARBOXY 7 DEAZAGUANINE SYNTHASE; 7 DEAZAPURINE DERIVATIVE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; PYRROLOPYRIMIDINE DERIVATIVE; QUEUOSINE; SANGIVAMYCIN; SYNTHETASE; TETRAHYDROFOLIC ACID; TOYOCAMYCIN; UNCLASSIFIED DRUG; 7-DEAZAPURINE; FREE RADICAL; LIGASE; PURINE DERIVATIVE;

ACINETOBACTER CALCOACETICUS; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL METABOLISM; BIOTRANSFORMATION; BURKHOLDERIA MULTIVORANS; CATALYSIS; CHEMICAL REACTION; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE CLUSTER; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RADICAL MEDIATED RING CONTRACTION; REVIEW; STREPTOMYCES RIMOSUS; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; METABOLISM;

BIOCATALYSIS; FREE RADICALS; LIGASES; PURINES;

EID: 84948775336     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.11.005     Document Type: Review

References (45)

1. McCarty R.M., Bandarian V. Biosynthesis of pyrrolopyrimidines. Bioorg Chem 2012, 43:15-25.
2. Nishimura H., Katagiri K., Sato K., Mayama M., Shimoka N. Toyocamycin, a new anti-candida antibiotics. J Antibiot 1956, 9:60-62.
3. RajBhandary U., Chang H.J., Gross F., Harada F., Kimura S., Nishimura S. E. coli tyrosine transfer RNA-primary sequence and direct evidence for base pairing between terminal sequences. Fed Proc Fed Amer Soc Exp Biol 1969, 28:409.
4. Harada F., Nishimura S. Possible anticodon sequences of tRNA His, tRNA Asn, and tRNA Asp from Escherichia coli B. Universal presence of nucleoside Q in the first postion of the anticondons of these transfer ribonucleic acids. Biochemistry 1972, 11:301-308.
5. Kasai H., Oashi Z., Harada F., Nishimura S., Oppenheimer N.J., Crain P.F., Liehr J.G., von Minden D.L., McCloskey J.A. Structure of the modified nucleoside Q isolated from Escherichia coli transfer ribonucleic acid. 7-(4,5-cis-dihydroxy-1-cyclopenten-3-ylaminomethyl)-7-deazaguanosine. Biochemistry 1975, 14:4198-4208.
6. Suhadolnik R.J., Uematsu T. Biosynthesis of the pyrrolopyrimidine nucleoside antibiotic, toyocamycin. VII. Origin of the pyrrole carbons and the cyano carbon. J Biol Chem 1970, 245:4365-4371.
7. Uematsu T., Suhadolnik R.J. Nucleoside antibiotics. VI. Biosynthesis of the pyrrolopyrimidine nucleoside antibiotic toyocamycin by Streptomyces rimosus. Biochemistry 1970, 9:1260-1266.
8. Kuchino Y., Kasai H., Nihei K., Nishimura S. Biosynthesis of the modified nucleoside Q in transfer RNA. Nucleic Acids Res 1976, 3:393-398.
9. Guroff G., Strenkoski C.A. Biosynthesis of pteridines and of phenylalanine hydroxylase cofactor in cell-free extracts of Pseudomonas species (ATCC 11299a). J Biol Chem 1966, 241:2220-2227.
10. Reynolds J.J., Brown G.M. The biosynthesis of folic acid. IV. Enzymatic synthesis of dihydrofolic acid from guanine and ribose compounds. J Biol Chem 1964, 239:317-325.
11. Reynolds J.J., Brown G.M. Enzymatic formation of the pteridine moiety of folic acid from guanine compounds. J Biol Chem 1962, 237:2713-2715.
12. Burg A.W., Brown G.M. The biosynthesis of folic acid. 8. Purification and properties of the enzyme that catalyzes the production of formate from carbon atom 8 of guanosine triphosphate. J Biol Chem 1968, 243:2349-2358.
13. Foor F., Brown G.M. Purification and properties of guanosine triphosphate cyclohydrolase II from Escherichia coli. J Biol Chem 1975, 250:3545-3551.
14. McCarty R.M., Bandarian V. Deciphering deazapurine biosynthesis: pathway for pyrrolopyrimidine nucleosides toyocamycin and sangivamycin. Chem Biol 2008, 15:790-798.
15. Reader J.S., Metzgar D., Schimmel P., de Crécy-Lagard V. Identification of four genes necessary for biosynthesis of the modified nucleoside queuosine. J Biol Chem 2004, 279:6280-6285.
16. McCarty R.M., Somogyi A., Lin G., Jacobsen N.E., Bandarian V. The deazapurine biosynthetic pathway revealed: in vitro enzymatic synthesis of PreQ(0) from guanosine 5'-triphosphate in four steps. Biochemistry 2009, 48:3847-3852.
17. McCarty R.M., Somogyi A., Bandarian V. Escherichia coli QueD is a 6-carboxy-5,6,7,8-tetrahydropterin synthase. Biochemistry 2009, 48:2301-2303.
18. Phillips G., El Yacoubi B., Lyons B., Alvarez S., Iwata-Reuyl D., de Crécy-Lagard V. Biosynthesis of 7-deazaguanosine-modified tRNA nucleosides: a new role for GTP cyclohydrolase I. J Bacteriol 2008, 190:7876-7884.
19. Takikawa S., Curtius H.C., Redweik U., Ghisla S. Purification of 6-pyruvoyl-tetrahydropterin synthase from human liver. Biochem Biophys Res Commun 1986, 134:646-651.
20. Miles Z.D., Roberts S.A., McCarty R.M., Bandarian V. Biochemical and structural studies of 6-carboxy-5,6,7,8-tetrahydropterin synthase reveal the molecular basis of catalytic promiscuity within the tunnel-fold superfamily. J Biol Chem 2014, 289:23641-23652.
21. McCarty R.M., Krebs C., Bandarian V. Spectroscopic, steady-state kinetic, and mechanistic characterization of the radical SAM enzyme QueE, which catalyzes a complex cyclization reaction in the biosynthesis of 7-deazapurines. Biochemistry 2013, 52:188-198.
22. Dowling D.P., Bruender N.A., Young A.P., McCarty R.M., Bandarian V., Drennan C.L. Radical SAM enzyme QueE defines a new minimal core fold and metal-dependent mechanism. Nat Chem Biol 2014, 10:106-112.
23. Nelp M.T., Bandarian V. A single enzyme transforms a carboxylic acid into a nitrile through an amide intermediate. Angew Chem Int Ed Engl 2015, 54:10627-10629.
24. Van Lanen S.G., Reader J.S., Swairjo M.A., de Crécy-Lagard V., Lee B., Iwata-Reuyl D. From cyclohydrolase to oxidoreductase: discovery of nitrile reductase activity in a common fold. Proc Natl Acad Sci USA 2005, 102:4264-4269.
25. Okada N., Noguchi S., Kasai H., Shindo-Okada N., Ohgi T., Goto T., Nishimura S. Novel mechanism of post-transcriptional modification of tRNA. Insertion of bases of Q precursors into tRNA by a specific tRNA transglycosylase reaction. J Biol Chem 1979, 254:3067-3073.
26. Okada N., Nishimura S. Isolation and characterization of a guanine insertion enzyme, a specific tRNA transglycosylase, from Escherichia coli. J Biol Chem 1979, 254:3061-3066.
27. Xie W., Liu X., Huang R.H. Chemical trapping and crystal structure of a catalytic tRNA guanine transglycosylase covalent intermediate. Nat Struct Biol 2003, 10:781-788.
28. Kittendorf J.D., Sgraja T., Reuter K., Klebe G., Garcia G.A. An essential role for aspartate 264 in catalysis by tRNA-guanine transglycosylase from Escherichia coli. J Biol Chem 2003, 278:42369-42376.
29. Garcia G.A., Chervin S.M., Kittendorf J.D. Identification of the rate-determining step of tRNA-guanine transglycosylase from Escherichia coli. Biochemistry 2009, 48:11243-11251.
30. Slany R.K., Bösl M., Kersten H. Transfer and isomerization of the ribose moiety of AdoMet during the biosynthesis of queuosine tRNAs, a new unique reaction catalyzed by the QueA protein from Escherichia coli. Biochimie 1994, 76:389-393.
31. Slany R.K., Bösl M., Crain P.F., Kersten H. A new function of S-adenosylmethionine: the ribosyl moiety of AdoMet is the precursor of the cyclopentenediol moiety of the tRNA wobble base queuine. Biochemistry 1993, 32:7811-7817.
32. Miles Z.D., McCarty R.M., Molnar G., Bandarian V. Discovery of epoxyqueuosine (oQ) reductase reveals parallels between halorespiration and tRNA modification. Proc Natl Acad Sci USA 2011, 108:7368-7372.
33. 12-dependent dehalogenation. Nature 2015, 517:513-516.
34. Bommer M., Kunze C., Fesseler J., Schubert T., Diekert G., Dobbek H. Structural basis for organohalide respiration. Science 2014, 346:455-458.
35. Miles Z.D., Myers W.K., Kincannon W.M., Britt R.D., Bandarian V. Biochemical and spectroscopic studies of epoxyqueuosine reductase: a novel iron-sulfur cluster- and cobalamin-containing protein involved in the biosynthesis of queuosine. Biochemistry 2015, 54:4927-4935.
36. Nelp M.T., Astashkin A.V., Breci L.A., McCarty R.M., Bandarian V. The alpha subunit of nitrile hydratase is sufficient for catalytic activity and post-translational modification. Biochemistry 2014, 53:3990-3994.
37. Sofia H.J., Chen G., Hetzler B.G., Reyes-Spindola J.F., Miller N.E. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 2001, 29:1097-1106.
38. Walsby C.J., Ortillo D., Broderick W.E., Broderick J.B., Hoffman B.M. An anchoring role for FeS clusters: chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe-4S] cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 2002, 124:11270-11271.
39. Akiva E., Brown S., Almonacid D.E., Barber A.E., Custer A.F., Hicks M.A., Huang C.C., Lauck F., Mashiyama S.T., Meng E.C., et al. The structure-function linkage database. Nucleic Acids Res 2014, 42:D521-D530.
40. Vey J.L., Drennan C.L. Structural insights into radical generation by the radical SAM superfamily. Chem Rev 2011, 111:2487-2506.
41. Lanz N.D., Grove T.L., Gogonea C.B., Lee K-HH, Krebs C., Booker S.J. RlmN and AtsB as models for the overproduction and characterization of radical SAM proteins. Meth Enzymol 2012, 516:125-152.
42. Bruender N.A., Young A.P., Bandarian V. Chemical and biological reduction of the radical SAM enzyme CDG synthase. Biochemistry 2015, 54:2903-2910.
43. Zhou W., Liu Y. Ring contraction catalyzed by the metal-dependent radical SAM enzyme: 7-carboxy-7-deazaguanine synthase from B. multivorans. Theoretical insights into the reaction mechanism and the influence of metal ions. ACS Catal 2015, 5:3953-3965.
44. Horitani M., Byer A.S., Shisler K.A., Chandra T., Broderick J.B., Hoffman B.M. Why nature uses radical sam enzymes so widely: electron nuclear double resonance studies of lysine 2,3-aminomutase show the 5'-dAdo J Am Chem Soc 2015, 137:7111-7121.
45. Lees N.S., Chen D., Walsby C.J., Behshad E., Frey P.A., Hoffman B.M. How an enzyme tames reactive intermediates: positioning of the active-site components of lysine 2,3-aminomutase during enzymatic turnover as determined by ENDOR spectroscopy. J Am Chem Soc 2006, 128:10145-10154.