Mechanistic insights into the manganese-dependent phosphodiesterase activity of yeast Dbr1 with bis-pnitrophenylphosphate and branched RNA substrates

RNA

Volumn 22, Issue 12, 2016, Pages 1819-1827

  Schwer, Beate ^a   Khalid, Fahad ^a   Shuman, Stewart ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Binuclear metallophosphoesterase; Lariat debranching

Indexed keywords

4 NITROPHENYLPHOSPHATASE; ALANINE; ASPARTIC ACID; CYSTINE; DBR1 ENZYME; ENZYME; FUNGAL ENZYME; HISTIDINE; MANGANESE; MESSENGER RNA; OXYGEN; PHOSPHODIESTERASE; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; RNA DEBRANCHING ENZYME DBR1, S CEREVISIAE; RNA POLYMERASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; ENTAMOEBA; ENZYME ACTIVITY; GENE FUNCTION; GENE IDENTIFICATION; HIGH THROUGHPUT SCREENING; HYDROLYSIS; INTRON; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA BINDING; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; ENZYME ACTIVE SITE; METABOLISM; MUTATION;

CATALYTIC DOMAIN; MANGANESE; MUTATION; PHOSPHORIC DIESTER HYDROLASES; RNA NUCLEOTIDYLTRANSFERASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84999142367     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.058552.116     Document Type: Article

References (32)

1. Acharya S, Földesi A, Chattopadhyaya J. 2003. The pKa of the internucleotide 2′-hydroxyl group in diribobucleoside (3′-5′) monophosphates. J Org Chem 68: 1906-1910.
2. Arenas J, Hurwitz J. 1987. Purification of a RNA debranching activity from HeLa cells. J Biol Chem 262: 4274-4279.
3. Armakola M, Higgins MJ, Figley MD, Barmada SJ, Scarborough EA, Diaz Z, Fang X, Shorter J, Krogan NJ, Finkbeiner S, et al. 2012. Inhibition of RNA lariat debranching enzyme suppresses TDP-43 toxicity in ALS disease models. Nat Genet 44: 1302-1309.
4. Bitton DA, Rallis C, Jeffares DC, Smith GC, Chen YYC, Codlin S, Marguerat S, Bähler J. 2014. LaSSO, a strategy for genome-wide mapping of intronic lariats and branch points using RNA-seq. Genome Res 24: 1169-1179.
5. Buratti E. 2015. Functional significance of TDP-43 mutations in disease. Adv Genetics 91: 1-53.
6. Carriero S, Damha MJ. 2002. Solid-phase synthesis of branched oligonucleotides. Curr Protoc Nucleic Acid Chem 4: 14.
7. Chapman KB, Boeke JD. 1991. Isolation and characterization of the gene encoding yeast debranching enzyme. Cell 65: 483-492.
8. Garrey SM, Katolik A, Prekeris M, Li X, York K, Bernards S, Fields S, Zhao R, Damha MJ, Hesselberth JR. 2014. A homolog of lariatdebranching enzyme modulates turnover of branched RNA. RNA 20: 1337-1348.
9. Herrick D, Parker R, Jacobson A. 1990. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 10: 2269-2284.
10. Hopfner KP, Karcher A, Craig L, Woo TT, Carney JP, Tainer JA. 2001. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105: 473-485.
11. Katolik A, Johnsson R, Montemayor E, Lackey JG, Hart PJ, Damha MJ. 2014. Regiospecific solid-phase synthesis of branched oligoribonucleotides that mimic intronic lariat RNA intermediates. J Org Chem 79: 963-975.
12. Keppetipola N, Shuman S. 2006. Distinct enzymic functional groups are required for the phosphomonoesterase and phosphodiesterase activities of Clostridium thermocellum polynucleotide kinase/phosphatase. J Biol Chem 281: 19251-19259.
13. Keppetipola N, Shuman S. 2007. Characterization of the 2′, 3′-cyclic phosphodiesterase activities of Clostridium thermocellum polynucleotide kinase-phosphatase and bacteriophage λ phosphatase. Nucleic Acids Res 35: 7721-7732.
14. Keppetipola N, Shuman S. 2008. A phosphate-binding histidine of binuclear metallophosphodiesterase enzymes is a determinant of 2′, 3′- cyclic nucleotide phosphodiesterase activity. J Biol Chem 283: 30942-30949.
15. Khalid F, Damha MJ, Shuman S, Schwer B. 2005. Structure-function analysis of yeast RNA debranching enzyme (Dbr1), a manganese-dependent phosphodiesterase. Nucleic Acids Res 33: 6349-6360.
16. Matange N, Podobnik M, Visweswariah SS. 2015. Metallophosphoesterases: structural fidelity with functional promiscuity. Biochem J 467: 201-216.
17. Montemayor EJ, Katolik A, Clark NE, Taylor AB, Scheurmann JP, Combs DJ, Johnsson R, Holloway SP, Stevens SW, Damha MJ, et al. 2014. Structural basis of lariat RNA recognition by the intron debranching enzyme Dbr1. Nucleic Acid Res 42: 10845-10855.
18. Nam K, Hudson RH, Chapman KB, Ganeshan K, Damha MJ, Boeke JD. 1994. Yeast lariat debranching enzyme. Substrate and sequence specificity. J Biol Chem 269: 20613-20621.
19. Nam K, Lee G, Trambley J, Devine SE, Boeke JD. 1997. Severe growth defect in a Schizosaccharomyces pombe mutant defective in intron lariat degradation. Mol Cell Biol 17: 809-818.
20. Padgett RA, Konarska MM, Grabowski PJ, Hardy SF, Sharp PA. 1984. Lariat RNAs as intermediates and products in the splicing of messenger RNA precursors. Science 225: 898-903.
21. Podobnik M, Tyagi R, Matange N, Dermol U, Gupta AK, Mattoo R, Seshadri K, Visweswariah SS. 2009. A mycobacterial cyclic AMP phosphodiesterase that moonlights as a modifier of cell wall permeability. J Biol Chem 284: 32846-32857.
22. Qin D, Huang L, Wlodaver A, Andrade J, Staley JP. 2016. Sequencing of lariat termini in S. cerevisiae reveals 5′ splice sites, branch points, and novel splicing events. RNA 22: 237-253.
23. Ruskin B, Green MR. 1985. An RNA processing activity that debranches RNA lariats. Science 229: 135-140.
24. Ruskin B, Krainer AR, Maniatis T, Green MR. 1984. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell 38: 317-331.
25. Shenoy AR, Capuder M, Draskovic P, Lamba D, Visweswariah SS, Podobnik M. 2007. Structural and biochemical analysis of the Rv0805 cyclic nucleotide phosphodiesterase from Mycobacterium tuberculosis. J Mol Biol 365: 211-225.
26. Stepankiw N, Raghavan M, Fogarty EA, Grimson A, Pleiss JA. 2015. Widespread alternative and aberrant splicing revealed by lariat sequencing. Nucleic Acids Res 43: 8488-8501.
27. Tago N, Katolik A, Clark NE, Montemayor EJ, Seio K, Sekine M, Hart PJ, Damha MJ. 2015. Design, synthesis, and properties of phosphoramidate 2′, 5′-linked branched RNA: Toward the rational design of inhibitors of the RNA lariat debranching enzyme. J Org Chem 80: 10108-10118.
28. Tanaka N, Schwer B. 2005. Characterization of the NTPase, RNA-binding, and RNA helicase activities of the DEAH-box splicing factor Prp22. Biochemistry 44: 9795-9803.
29. Velikyan I, Acharya S, Trifonova A, Földesi A, Chattopadhyaya J. 2001. The pKas of 2′-hydroxyl group in nucleosides and nucleotides. J Am Chem Soc 123: 2893-2894.
30. Wang LK, Smith P, Shuman S. 2013. Structure and mechanism of the 2′, 3′ phosphatase component of the bacterial Pnkp-Hen1 RNA repair system. Nucleic Acids Res 41: 5864-5873.
31. Wong I, Lohman TM. 1993. A double-filter method for nitrocellulosefilter binding: Application to protein-nucleic acid interactions. Proc Natl Acad Sci 90: 5428-5432.
32. Zheng S, Vuong BQ, Vaidyanathan B, Lin JY, Huang FT, Chaudhuri J. 2015. Non-coding RNA generated following lariat debranching mediates targeting of AID to DNA. Cell 161: 762-773.