publication . Article . 2019

Structure of tRNA splicing enzyme Tpt1 illuminates the mechanism of RNA 2′-PO4 recognition and ADP-ribosylation

Ankan Banerjee; Annum Munir; Leonora Abdullahu; Masad J. Damha; Yehuda Goldgur; Stewart Shuman;
Open Access English
  • Published: 15 Jan 2019 Journal: Nature Communications, volume 10 (eissn: 2041-1723, Copyright policy)
  • Publisher: Nature Publishing Group UK
Abstract
Tpt1 catalyzes the final essential step in yeast tRNA splicing and is a potential antifungal target. Here the authors provide structural insights into how Tpt1 recognizes a 2’-PO4 RNA splice junction and the mechanism of RNA phospho-ADP-ribosylation.
Subjects
free text keywords: Article, General Biochemistry, Genetics and Molecular Biology, General Physics and Astronomy, General Chemistry, Science, Q
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| New frontiers in extracellular signaling
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM122575-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
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| 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
31 references, page 1 of 3

Culver, GM. An NAD derivative produced during transfer RNA splicing: ADP-ribose 1″-2″ cyclic phosphate. Science. 1993; 261: 206-208 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Kierzek, R, Turner, DH, Phizicky, EM. Transient ADP-ribosylation of a 2′-phosphate implicated in its removal from ligated tRNA during splicing in yeast. J. Biol. Chem.. 1999; 274: 2637-2644 [OpenAIRE] [PubMed] [DOI]

Steiger, MA, Kierzek, R, Turner, DH, Phizicky, EM. Substrate recognition by a yeast 2′-phosphotransferase involved in tRNA splicing and its Escherichia coli homolog. Biochemistry. 2001; 40: 14098-14105 [OpenAIRE] [PubMed] [DOI]

Steiger, MA, Jackman, JE, Phizicky, EM. Analysis of 2′-phosphotransferase (Tpt1p) from Saccharomyces cerevisiae: evidence for a conserved two-step reaction mechanism. RNA. 2005; 11: 99-106 [OpenAIRE] [PubMed] [DOI]

Munir, A, Abdullahu, L, Damha, MJ, Shuman, S. Two-step mechanism and step-arrest mutants of Runella slithyformis NAD+-dependent tRNA 2′-phosphotransferase Tpt1. RNA. 2018; 24: 1144-1157 [OpenAIRE] [PubMed] [DOI]

McCraith, SM, Phizicky, EM. A highly specific phosphatase from Saccharomyces cerevisiae implicated in tRNA splicing. Mol. Cell Biol.. 1990; 10: 1049-1055 [OpenAIRE] [PubMed] [DOI]

McCraith, SM, Phizicky, EM. An enzyme from Saccharomyces cerevisiae uses NAD+ to transfer the splice junction 2′-phosphate from ligated tRNA to an acceptor molecule. J. Biol. Chem.. 1991; 266: 11986-11992 [PubMed]

Culver, GM, McCraith, SM, Consaul, SA, Stanford, DR, Phizicky, EM. A 2′-phosphotransferase implicated in tRNA splicing is essential in Saccharomyces cerevisiae. J. Biol. Chem.. 1997; 272: 13203-13210 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Consaul, SA, Phizicky, EM. A conditional lethal yeast phosphotransferase mutant accumulates tRNA with a 2′-phosphate and an unmodified base at the splice junction. RNA. 1997; 3: 1388-1400 [OpenAIRE] [PubMed]

Greer, CL, Peebles, CL, Gegenheimer, P, Abelson, J. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell. 1983; 32: 537-546 [OpenAIRE] [PubMed] [DOI]

Remus, BS, Shuman, S. A kinetic framework for tRNA ligase and enforcement of a 2′-phosphate requirement for ligation highlights the design logic of an RNA repair machine. RNA. 2013; 19: 659-669 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Malik, HS, Consaul, SA, Phizicky, EM. A functional homolog of a yeast tRNA splicing enzyme is conserved in higher eukaryotes and in Escherichia coli. Proc. Natl. Acad. Sci. USA. 1998; 95: 14136-14141 [OpenAIRE] [PubMed] [DOI]

Popow, J, Schlieffer, A, Martinez, J. Diversity and roles of (t)RNA ligases. Cell Mol. Life Sci.. 2012; 69: 2657-2670 [OpenAIRE] [PubMed] [DOI]

Sawaya, R, Schwer, B, Shuman, S. Structure-function analysis of the yeast NAD+-dependent tRNA 2′-phosphotransferase Tpt1. RNA. 2005; 11: 107-113 [OpenAIRE] [PubMed] [DOI]

Harding, HP. An intact unfolded protein response in Trpt1 knockout mice reveals phylogenetic divergence in pathways for RNA ligation. RNA. 2008; 14: 225-232 [OpenAIRE] [PubMed] [DOI]

31 references, page 1 of 3
Abstract
Tpt1 catalyzes the final essential step in yeast tRNA splicing and is a potential antifungal target. Here the authors provide structural insights into how Tpt1 recognizes a 2’-PO4 RNA splice junction and the mechanism of RNA phospho-ADP-ribosylation.
Subjects
free text keywords: Article, General Biochemistry, Genetics and Molecular Biology, General Physics and Astronomy, General Chemistry, Science, Q
Funded by
NIH| MOUSE GENETICS
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2P30CA008748-43
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| New frontiers in extracellular signaling
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R35GM122575-01
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
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| 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
31 references, page 1 of 3

Culver, GM. An NAD derivative produced during transfer RNA splicing: ADP-ribose 1″-2″ cyclic phosphate. Science. 1993; 261: 206-208 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Kierzek, R, Turner, DH, Phizicky, EM. Transient ADP-ribosylation of a 2′-phosphate implicated in its removal from ligated tRNA during splicing in yeast. J. Biol. Chem.. 1999; 274: 2637-2644 [OpenAIRE] [PubMed] [DOI]

Steiger, MA, Kierzek, R, Turner, DH, Phizicky, EM. Substrate recognition by a yeast 2′-phosphotransferase involved in tRNA splicing and its Escherichia coli homolog. Biochemistry. 2001; 40: 14098-14105 [OpenAIRE] [PubMed] [DOI]

Steiger, MA, Jackman, JE, Phizicky, EM. Analysis of 2′-phosphotransferase (Tpt1p) from Saccharomyces cerevisiae: evidence for a conserved two-step reaction mechanism. RNA. 2005; 11: 99-106 [OpenAIRE] [PubMed] [DOI]

Munir, A, Abdullahu, L, Damha, MJ, Shuman, S. Two-step mechanism and step-arrest mutants of Runella slithyformis NAD+-dependent tRNA 2′-phosphotransferase Tpt1. RNA. 2018; 24: 1144-1157 [OpenAIRE] [PubMed] [DOI]

McCraith, SM, Phizicky, EM. A highly specific phosphatase from Saccharomyces cerevisiae implicated in tRNA splicing. Mol. Cell Biol.. 1990; 10: 1049-1055 [OpenAIRE] [PubMed] [DOI]

McCraith, SM, Phizicky, EM. An enzyme from Saccharomyces cerevisiae uses NAD+ to transfer the splice junction 2′-phosphate from ligated tRNA to an acceptor molecule. J. Biol. Chem.. 1991; 266: 11986-11992 [PubMed]

Culver, GM, McCraith, SM, Consaul, SA, Stanford, DR, Phizicky, EM. A 2′-phosphotransferase implicated in tRNA splicing is essential in Saccharomyces cerevisiae. J. Biol. Chem.. 1997; 272: 13203-13210 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Consaul, SA, Phizicky, EM. A conditional lethal yeast phosphotransferase mutant accumulates tRNA with a 2′-phosphate and an unmodified base at the splice junction. RNA. 1997; 3: 1388-1400 [OpenAIRE] [PubMed]

Greer, CL, Peebles, CL, Gegenheimer, P, Abelson, J. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell. 1983; 32: 537-546 [OpenAIRE] [PubMed] [DOI]

Remus, BS, Shuman, S. A kinetic framework for tRNA ligase and enforcement of a 2′-phosphate requirement for ligation highlights the design logic of an RNA repair machine. RNA. 2013; 19: 659-669 [OpenAIRE] [PubMed] [DOI]

Spinelli, SL, Malik, HS, Consaul, SA, Phizicky, EM. A functional homolog of a yeast tRNA splicing enzyme is conserved in higher eukaryotes and in Escherichia coli. Proc. Natl. Acad. Sci. USA. 1998; 95: 14136-14141 [OpenAIRE] [PubMed] [DOI]

Popow, J, Schlieffer, A, Martinez, J. Diversity and roles of (t)RNA ligases. Cell Mol. Life Sci.. 2012; 69: 2657-2670 [OpenAIRE] [PubMed] [DOI]

Sawaya, R, Schwer, B, Shuman, S. Structure-function analysis of the yeast NAD+-dependent tRNA 2′-phosphotransferase Tpt1. RNA. 2005; 11: 107-113 [OpenAIRE] [PubMed] [DOI]

Harding, HP. An intact unfolded protein response in Trpt1 knockout mice reveals phylogenetic divergence in pathways for RNA ligation. RNA. 2008; 14: 225-232 [OpenAIRE] [PubMed] [DOI]

31 references, page 1 of 3
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