Family-wide analysis of poly(ADP-ribose) polymerase activity

The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as substrate. Based on the composition of three NAD + coordinating amino acids, the H-Y-E motif, each PARP is predicted to generate either poly(ADP...

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Published in	Nature communications Vol. 5; no. 1; p. 4426
Main Authors	Vyas, Sejal, Matic, Ivan, Uchima, Lilen, Rood, Jenny, Zaja, Roko, Hay, Ronald T., Ahel, Ivan, Chang, Paul
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 21.07.2014 Nature Publishing Group
Subjects	38 38/109 631/45/173 631/80/458/2389 82 82/16 82/29 82/80 82/83 Adenosine Diphosphate Ribose - metabolism Amino Acid Motifs Cells, Cultured Cysteine - metabolism Humanities and Social Sciences Humans Lysine - metabolism multidisciplinary Poly Adenosine Diphosphate Ribose - metabolism Poly(ADP-ribose) Polymerases - chemistry Poly(ADP-ribose) Polymerases - genetics Poly(ADP-ribose) Polymerases - metabolism Science Science (multidisciplinary)
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Abstract	The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as substrate. Based on the composition of three NAD + coordinating amino acids, the H-Y-E motif, each PARP is predicted to generate either poly(ADPr) (PAR) or mono(ADPr) (MAR). However, the reaction product of each PARP has not been clearly defined, and is an important priority since PAR and MAR function via distinct mechanisms. Here we show that the majority of PARPs generate MAR, not PAR, and demonstrate that the H-Y-E motif is not the sole indicator of PARP activity. We identify automodification sites on seven PARPs, and demonstrate that MAR and PAR generating PARPs modify similar amino acids, suggesting that the sequence and structural constraints limiting PARPs to MAR synthesis do not limit their ability to modify canonical amino-acid targets. In addition, we identify cysteine as a novel amino-acid target for ADP-ribosylation on PARPs. The poly(ADP-ribose) polymerase family of enzymes control many aspects of cellular signalling by covalently modifying proteins with either poly- or mono-(ADP-ribose). Vyas et al. catalogue the catalytic specificity of this family, and reveal that the majority of these enzymes generate only mono(ADP-ribose).
AbstractList	The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as substrate. Based on the composition of three NAD + coordinating amino acids, the H-Y-E motif, each PARP is predicted to generate either poly(ADPr) (PAR) or mono(ADPr) (MAR). However, the reaction product of each PARP has not been clearly defined, and is an important priority since PAR and MAR function via distinct mechanisms. Here we show that the majority of PARPs generate MAR, not PAR, and demonstrate that the H-Y-E motif is not the sole indicator of PARP activity. We identify automodification sites on seven PARPs, and demonstrate that MAR and PAR generating PARPs modify similar amino acids, suggesting that the sequence and structural constraints limiting PARPs to MAR synthesis do not limit their ability to modify canonical amino-acid targets. In addition, we identify cysteine as a novel amino-acid target for ADP-ribosylation on PARPs. The poly(ADP-ribose) polymerase family of enzymes control many aspects of cellular signalling by covalently modifying proteins with either poly- or mono-(ADP-ribose). Vyas et al. catalogue the catalytic specificity of this family, and reveal that the majority of these enzymes generate only mono(ADP-ribose). The poly(ADP-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as substrate. Based on the composition of three NAD + coordinating amino acids, the H-Y-E motif, each PARP is predicted to generate either poly(ADP-ribose) (PAR) or mono(ADP-ribose) (MAR). However, the reaction product of each PARP has not been clearly defined, and is an important priority since PAR and MAR function via distinct mechanisms. Here we show that the majority of PARPs generate MAR, not PAR, and demonstrate that the H-Y-E motif is not the sole indicator of PARP activity. We identify automodification sites on seven PARPs, and demonstrate that MAR and PAR generating PARPs modify similar amino acids, suggesting that the sequence and structural constraints limiting PARPs to MAR synthesis do not limit their ability to modify canonical amino acid targets. In addition, we identify cysteine as a novel amino acid target for ADP-ribosylation on PARPs. The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD+ as substrate. Based on the composition of three NAD+ coordinating amino acids, the H-Y-E motif, each PARP is predicted to generate either poly(ADPr) (PAR) or mono(ADPr) (MAR). However, the reaction product of each PARP has not been clearly defined, and is an important priority since PAR and MAR function via distinct mechanisms. Here we show that the majority of PARPs generate MAR, not PAR, and demonstrate that the H-Y-E motif is not the sole indicator of PARP activity. We identify automodification sites on seven PARPs, and demonstrate that MAR and PAR generating PARPs modify similar amino acids, suggesting that the sequence and structural constraints limiting PARPs to MAR synthesis do not limit their ability to modify canonical amino-acid targets. In addition, we identify cysteine as a novel amino-acid target for ADP-ribosylation on PARPs.
ArticleNumber	4426
Author	Rood, Jenny Vyas, Sejal Zaja, Roko Hay, Ronald T. Matic, Ivan Ahel, Ivan Chang, Paul Uchima, Lilen
AuthorAffiliation	6 Division for Marine and Environmental Research, Rudjer Boskovic Institute, Zagreb 10002, Croatia 1 Koch Institute for Integrative Cancer Research, Cambridge, MA 02139, USA 2 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 3 Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Dow Street, Dundee DD1 5EH, UK 5 Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford, OX1 3RE, UK
AuthorAffiliation_xml	– name: 1 Koch Institute for Integrative Cancer Research, Cambridge, MA 02139, USA – name: 3 Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Dow Street, Dundee DD1 5EH, UK – name: 2 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – name: 6 Division for Marine and Environmental Research, Rudjer Boskovic Institute, Zagreb 10002, Croatia – name: 5 Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford, OX1 3RE, UK
Author_xml	– sequence: 1 givenname: Sejal surname: Vyas fullname: Vyas, Sejal organization: Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology – sequence: 2 givenname: Ivan surname: Matic fullname: Matic, Ivan organization: Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre, Present address: Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Street 9b, D-50931 Köln/Cologne, Germany – sequence: 3 givenname: Lilen surname: Uchima fullname: Uchima, Lilen organization: Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology – sequence: 4 givenname: Jenny surname: Rood fullname: Rood, Jenny organization: Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology – sequence: 5 givenname: Roko surname: Zaja fullname: Zaja, Roko organization: Sir William Dunn School of Pathology, University of Oxford, Division for Marine and Environmental Research, Rudjer Boskovic Institute – sequence: 6 givenname: Ronald T. surname: Hay fullname: Hay, Ronald T. organization: Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Sir James Black Centre – sequence: 7 givenname: Ivan surname: Ahel fullname: Ahel, Ivan organization: Sir William Dunn School of Pathology, University of Oxford – sequence: 8 givenname: Paul surname: Chang fullname: Chang, Paul email: pchang2@mit.edu organization: Koch Institute for Integrative Cancer Research, Department of Biology, Massachusetts Institute of Technology
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25043379$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Str.9b, D-50931 Köln / Cologne, Germany Author Contributions: PC, SV and IA wrote the manuscript. PC and SV conceived the experiments. SV performed in vitro NAD+ incorporation assays, enzymatic and chemical treatment analysis and Donor/acceptor chimera and mutant assays, purified PARPs for mass spectrometry analysis and performed validation of cysteine modifications. IM and RH performed mass spectrometry experiments. RZ expressed and purified MacroD1, TARG1, PARP3 and 16 proteins and prepared proteins for mass spectrometry analysis. LU helped optimize running conditions for TLC analysis. JR determined effect of having GFP tag on the N vs C terminus of PARP1.
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Snippet	The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as... The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD(+) as... The poly(adenosine diphosphate (ADP)-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD+ as... The poly(ADP-ribose) polymerase (PARP) protein family generates ADP-ribose (ADPr) modifications onto target proteins using NAD + as substrate. Based on the...
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SubjectTerms	38 38/109 631/45/173 631/80/458/2389 82 82/16 82/29 82/80 82/83 Adenosine Diphosphate Ribose - metabolism Amino Acid Motifs Cells, Cultured Cysteine - metabolism Humanities and Social Sciences Humans Lysine - metabolism multidisciplinary Poly Adenosine Diphosphate Ribose - metabolism Poly(ADP-ribose) Polymerases - chemistry Poly(ADP-ribose) Polymerases - genetics Poly(ADP-ribose) Polymerases - metabolism Science Science (multidisciplinary)
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Title	Family-wide analysis of poly(ADP-ribose) polymerase activity
URI	https://link.springer.com/article/10.1038/ncomms5426 https://www.ncbi.nlm.nih.gov/pubmed/25043379 https://www.proquest.com/docview/1546235919 https://search.proquest.com/docview/1547518852 https://pubmed.ncbi.nlm.nih.gov/PMC4123609
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