publication . Article . 2017

Structural basis for the GTP specificity of the RNA kinase domain of fungal tRNA ligase.

Remus, Barbara S.; Goldgur, Yehuda; Shuman, Stewart;
Open Access
  • Published: 20 Nov 2017 Journal: Nucleic Acids Research, volume 45, pages 12,945-12,953 (issn: 0305-1048, eissn: 1362-4962, Copyright policy)
  • Publisher: Oxford University Press (OUP)
Abstract
Abstract Fungal tRNA ligase (Trl1) is an essential enzyme that repairs RNA breaks with 2′,3′-cyclic-PO4 and 5′-OH ends inflicted during tRNA splicing and non-canonical mRNA splicing in the fungal unfolded protein response. Trl1 is composed of C-terminal cyclic phosphodiesterase and central polynucleotide kinase domains that heal the broken ends to generate the 3′-OH,2′-PO4 and 5′-PO4 termini required for sealing by an N-terminal ligase domain. Trl1 enzymes are found in all human fungal pathogens and are promising targets for antifungal drug discovery because their domain compositions and biochemical mechanisms are unique compared to the mammalian RtcB-type tRNA ...
Subjects
free text keywords: Nucleic Acid Enzymes
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| VACCINIA VIRUS MRNA TRANSCRIPTION TERMINATION
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2R01GM042498-10
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
27 references, page 1 of 2

1.Abelson J., Trotta C.R., Li H.tRNA splicing. J. Biol. Chem.1998; 273:12685–12688.9582290 [OpenAIRE] [PubMed]

2.Sidrauski C., Cox J.S., Walter P.tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell. 1996; 87:405–413.8898194 [OpenAIRE] [PubMed]

3.Greer C.L., Peebles C.L., Gegenheimer P., Abelson J.Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell. 1983; 32:537–546.6297798 [PubMed]

4.Apostol B.L., Westaway S.K., Abelson J., Greer C.L.Deletion analysis of a multifunctional yeast tRNA ligase polypeptide: identification of essential and dispensable functional domains. J. Biol. Chem.1991; 266:7445–7455.1850408 [PubMed]

5.Sawaya R., Schwer B., Shuman S.Genetic and biochemical analysis of the functional domains of yeast tRNA ligase. J. Biol. Chem.2003; 278:43298–43398. [OpenAIRE]

6.Wang L.K., Shuman S.Structure-function analysis of yeast tRNA ligase. RNA. 2005; 11:966–975.15923379 [OpenAIRE] [PubMed]

7.Wang L.K, Schwer B., Englert M., Beier H., Shuman S.Structure-function analysis of the kinase-CPD domain of yeast tRNA ligase (Trl1) and requi rements for complementation of tRNA splicing by a plant Trl1 homolog. Nucleic Acids Res.2006; 34:517–527.16428247 [OpenAIRE] [PubMed]

8.Remus B.S., Shuman S.Distinctive kinetics and substrate specificities of plant and fungal tRNA ligases. RNA. 2014; 20:462–473.24554441 [OpenAIRE] [PubMed]

9.Remus B.S., Schwer B., Shuman S.Characterization of the tRNA ligases of pathogenic fungi Aspergillus fumigatus and Coccidioides immitis. RNA. 2016; 22:1500–1509.27492257 [OpenAIRE] [PubMed]

10.Tanaka N., Shuman S RtcB is the RNA lig ase component of an Escherichia coli RNA repair operon. J. Biol. Chem.2011; 286:7727–7731.21224389 [OpenAIRE] [PubMed]

11.Tanaka N., Chakravarty A.K., Maughan B., Shuman S.A novel mechanism of RNA repair by RtcB via sequential 2’,3’-cyclic phosphodiesterase and 3′-phosphate/5′-hydroxyl ligation reactions. J. Biol. Chem.2011; 286:43134–43143.22045815 [OpenAIRE] [PubMed]

12.Tanaka N., Meineke B., Shuman S.RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J. Biol. Chem.2011; 286:30253–30257.21757685 [OpenAIRE] [PubMed]

13.Chakravarty A.K., Subbotin R., Chait B.T., Shuman S.RNA ligase RtcB splices 3’-phosphate and 5′-OH ends via covalent RtcB-(histidinyl)-GMP and polynucleotide-(3′)pp(5′)G intermediates. Proc. Natl. Acad. Sci. USA. 2012; 109:6072–6077.22474365 [OpenAIRE] [PubMed]

14.Chakravarty A.K., Shuman S.The sequential 2′,3′ cyclic phosphodiesterase and 3′-phosphate/5′-OH ligation steps of the RtcB RNA splicing pathway are GTP-dependent. Nucleic Acids Res.2012; 40:8558–8567.22730297 [OpenAIRE] [PubMed]

15.Englert M., Xia S., Okada C., Nakamura A., Tanavde V., Yao M., Eom S.H., Koningsberg W.H., Söll D., Wang J.Structural and mechanistic insights into guanylylation of RNA-splicing ligase RtcB joining RNA between 3′-terminal phosphate and 5′-OH. Proc. Natl. Acad. Sci. U.S.A.2012; 109:15235–15240.22949672 [OpenAIRE] [PubMed]

27 references, page 1 of 2
Abstract
Abstract Fungal tRNA ligase (Trl1) is an essential enzyme that repairs RNA breaks with 2′,3′-cyclic-PO4 and 5′-OH ends inflicted during tRNA splicing and non-canonical mRNA splicing in the fungal unfolded protein response. Trl1 is composed of C-terminal cyclic phosphodiesterase and central polynucleotide kinase domains that heal the broken ends to generate the 3′-OH,2′-PO4 and 5′-PO4 termini required for sealing by an N-terminal ligase domain. Trl1 enzymes are found in all human fungal pathogens and are promising targets for antifungal drug discovery because their domain compositions and biochemical mechanisms are unique compared to the mammalian RtcB-type tRNA ...
Subjects
free text keywords: Nucleic Acid Enzymes
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| Pixel Array Detector for X-ray Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1S10RR029205-01
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| VACCINIA VIRUS MRNA TRANSCRIPTION TERMINATION
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2R01GM042498-10
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| NE-CAT Center for Advanced Macromolecular Crystallography
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 4P41GM103403-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
27 references, page 1 of 2

1.Abelson J., Trotta C.R., Li H.tRNA splicing. J. Biol. Chem.1998; 273:12685–12688.9582290 [OpenAIRE] [PubMed]

2.Sidrauski C., Cox J.S., Walter P.tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell. 1996; 87:405–413.8898194 [OpenAIRE] [PubMed]

3.Greer C.L., Peebles C.L., Gegenheimer P., Abelson J.Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell. 1983; 32:537–546.6297798 [PubMed]

4.Apostol B.L., Westaway S.K., Abelson J., Greer C.L.Deletion analysis of a multifunctional yeast tRNA ligase polypeptide: identification of essential and dispensable functional domains. J. Biol. Chem.1991; 266:7445–7455.1850408 [PubMed]

5.Sawaya R., Schwer B., Shuman S.Genetic and biochemical analysis of the functional domains of yeast tRNA ligase. J. Biol. Chem.2003; 278:43298–43398. [OpenAIRE]

6.Wang L.K., Shuman S.Structure-function analysis of yeast tRNA ligase. RNA. 2005; 11:966–975.15923379 [OpenAIRE] [PubMed]

7.Wang L.K, Schwer B., Englert M., Beier H., Shuman S.Structure-function analysis of the kinase-CPD domain of yeast tRNA ligase (Trl1) and requi rements for complementation of tRNA splicing by a plant Trl1 homolog. Nucleic Acids Res.2006; 34:517–527.16428247 [OpenAIRE] [PubMed]

8.Remus B.S., Shuman S.Distinctive kinetics and substrate specificities of plant and fungal tRNA ligases. RNA. 2014; 20:462–473.24554441 [OpenAIRE] [PubMed]

9.Remus B.S., Schwer B., Shuman S.Characterization of the tRNA ligases of pathogenic fungi Aspergillus fumigatus and Coccidioides immitis. RNA. 2016; 22:1500–1509.27492257 [OpenAIRE] [PubMed]

10.Tanaka N., Shuman S RtcB is the RNA lig ase component of an Escherichia coli RNA repair operon. J. Biol. Chem.2011; 286:7727–7731.21224389 [OpenAIRE] [PubMed]

11.Tanaka N., Chakravarty A.K., Maughan B., Shuman S.A novel mechanism of RNA repair by RtcB via sequential 2’,3’-cyclic phosphodiesterase and 3′-phosphate/5′-hydroxyl ligation reactions. J. Biol. Chem.2011; 286:43134–43143.22045815 [OpenAIRE] [PubMed]

12.Tanaka N., Meineke B., Shuman S.RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J. Biol. Chem.2011; 286:30253–30257.21757685 [OpenAIRE] [PubMed]

13.Chakravarty A.K., Subbotin R., Chait B.T., Shuman S.RNA ligase RtcB splices 3’-phosphate and 5′-OH ends via covalent RtcB-(histidinyl)-GMP and polynucleotide-(3′)pp(5′)G intermediates. Proc. Natl. Acad. Sci. USA. 2012; 109:6072–6077.22474365 [OpenAIRE] [PubMed]

14.Chakravarty A.K., Shuman S.The sequential 2′,3′ cyclic phosphodiesterase and 3′-phosphate/5′-OH ligation steps of the RtcB RNA splicing pathway are GTP-dependent. Nucleic Acids Res.2012; 40:8558–8567.22730297 [OpenAIRE] [PubMed]

15.Englert M., Xia S., Okada C., Nakamura A., Tanavde V., Yao M., Eom S.H., Koningsberg W.H., Söll D., Wang J.Structural and mechanistic insights into guanylylation of RNA-splicing ligase RtcB joining RNA between 3′-terminal phosphate and 5′-OH. Proc. Natl. Acad. Sci. U.S.A.2012; 109:15235–15240.22949672 [OpenAIRE] [PubMed]

27 references, page 1 of 2
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