Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose)

Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that th...

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Published in:	Nature communications Vol. 6; no. 1; p. 8088
Main Authors:	Altmeyer, Matthias, Neelsen, Kai J., Teloni, Federico, Pozdnyakova, Irina, Pellegrino, Stefania, Grøfte, Merete, Rask, Maj-Britt Druedahl, Streicher, Werner, Jungmichel, Stephanie, Nielsen, Michael Lund, Lukas, Jiri
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 19.08.2015 Nature Publishing Group Nature Pub. Group
Subjects:	14/1 14/28 14/35 14/63 631/337/1427 631/45 631/57/2269 Adenosine diphosphate Biopolymers Cell Line, Tumor Cloning, Molecular Deoxyribonucleic acid DNA DNA Damage Gene Expression Regulation - physiology Humanities and Social Sciences Humans multidisciplinary Nucleic acids Poly Adenosine Diphosphate Ribose - chemistry Protein Conformation Protein Structure, Tertiary Proteins - chemistry Proteins - genetics Proteins - metabolism Science Science (multidisciplinary)
ISSN:	2041-1723, 2041-1723
Online Access:	Get full text
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Abstract	Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing. PAR levels are markedly induced at sites of DNA damage, and we provide evidence that PAR-seeded liquid demixing results in rapid, yet transient and fully reversible assembly of various intrinsically disordered proteins at DNA break sites. Demixing, which relies on electrostatic interactions between positively charged RGG repeats and negatively charged PAR, is amplified by aggregation-prone prion-like domains, and orchestrates the earliest cellular responses to DNA breakage. We propose that PAR-seeded liquid demixing is a general mechanism to dynamically reorganize the soluble nuclear space with implications for pathological protein aggregation caused by derailed phase separation. Intrinsically disordered proteins can phase separate from the soluble intracellular space. Here the authors show that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing and orchestrates the earliest cellular responses to DNA breakage.
AbstractList	Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing. PAR levels are markedly induced at sites of DNA damage, and we provide evidence that PAR-seeded liquid demixing results in rapid, yet transient and fully reversible assembly of various intrinsically disordered proteins at DNA break sites. Demixing, which relies on electrostatic interactions between positively charged RGG repeats and negatively charged PAR, is amplified by aggregation-prone prion-like domains, and orchestrates the earliest cellular responses to DNA breakage. We propose that PAR-seeded liquid demixing is a general mechanism to dynamically reorganize the soluble nuclear space with implications for pathological protein aggregation caused by derailed phase separation. Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing. PAR levels are markedly induced at sites of DNA damage, and we provide evidence that PAR-seeded liquid demixing results in rapid, yet transient and fully reversible assembly of various intrinsically disordered proteins at DNA break sites. Demixing, which relies on electrostatic interactions between positively charged RGG repeats and negatively charged PAR, is amplified by aggregation-prone prion-like domains, and orchestrates the earliest cellular responses to DNA breakage. We propose that PAR-seeded liquid demixing is a general mechanism to dynamically reorganize the soluble nuclear space with implications for pathological protein aggregation caused by derailed phase separation. Intrinsically disordered proteins can phase separate from the soluble intracellular space. Here the authors show that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing and orchestrates the earliest cellular responses to DNA breakage. Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing. PAR levels are markedly induced at sites of DNA damage, and we provide evidence that PAR-seeded liquid demixing results in rapid, yet transient and fully reversible assembly of various intrinsically disordered proteins at DNA break sites. Demixing, which relies on electrostatic interactions between positively charged RGG repeats and negatively charged PAR, is amplified by aggregation-prone prion-like domains, and orchestrates the earliest cellular responses to DNA breakage. We propose that PAR-seeded liquid demixing is a general mechanism to dynamically reorganize the soluble nuclear space with implications for pathological protein aggregation caused by derailed phase separation. Intrinsically disordered proteins can phase separate from the soluble intracellular space. Here the authors show that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing and orchestrates the earliest cellular responses to DNA breakage. Intrinsically disordered proteins can phase separate from the soluble intracellular space, and tend to aggregate under pathological conditions. The physiological functions and molecular triggers of liquid demixing by phase separation are not well understood. Here we show in vitro and in vivo that the nucleic acid-mimicking biopolymer poly(ADP-ribose) (PAR) nucleates intracellular liquid demixing. PAR levels are markedly induced at sites of DNA damage, and we provide evidence that PAR-seeded liquid demixing results in rapid, yet transient and fully reversible assembly of various intrinsically disordered proteins at DNA break sites. Demixing, which relies on electrostatic interactions between positively charged RGG repeats and negatively charged PAR, is amplified by aggregation-prone prion-like domains, and orchestrates the earliest cellular responses to DNA breakage. We propose that PAR-seeded liquid demixing is a general mechanism to dynamically reorganize the soluble nuclear space with implications for pathological protein aggregation caused by derailed phase separation.
ArticleNumber	8088
Author	Jungmichel, Stephanie Pellegrino, Stefania Streicher, Werner Lukas, Jiri Grøfte, Merete Pozdnyakova, Irina Teloni, Federico Neelsen, Kai J. Rask, Maj-Britt Druedahl Nielsen, Michael Lund Altmeyer, Matthias
Author_xml	– sequence: 1 givenname: Matthias surname: Altmeyer fullname: Altmeyer, Matthias email: matthias.altmeyer@uzh.ch organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen, Institute of Veterinary Biochemistry and Molecular Biology, University of Zurich – sequence: 2 givenname: Kai J. surname: Neelsen fullname: Neelsen, Kai J. organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 3 givenname: Federico orcidid: 0000-0003-0953-8010 surname: Teloni fullname: Teloni, Federico organization: Institute of Veterinary Biochemistry and Molecular Biology, University of Zurich – sequence: 4 givenname: Irina surname: Pozdnyakova fullname: Pozdnyakova, Irina organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 5 givenname: Stefania surname: Pellegrino fullname: Pellegrino, Stefania organization: Institute of Veterinary Biochemistry and Molecular Biology, University of Zurich – sequence: 6 givenname: Merete surname: Grøfte fullname: Grøfte, Merete organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 7 givenname: Maj-Britt Druedahl surname: Rask fullname: Rask, Maj-Britt Druedahl organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 8 givenname: Werner surname: Streicher fullname: Streicher, Werner organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen, Present address: Novozymes A/S, Krogshoejvej 36, DK-2880 Bagsverd, Denmark – sequence: 9 givenname: Stephanie surname: Jungmichel fullname: Jungmichel, Stephanie organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 10 givenname: Michael Lund surname: Nielsen fullname: Nielsen, Michael Lund organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 11 givenname: Jiri surname: Lukas fullname: Lukas, Jiri email: jiri.lukas@cpr.ku.dk organization: Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26286827$$D View this record in MEDLINE/PubMed
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SubjectTerms	14/1 14/28 14/35 14/63 631/337/1427 631/45 631/57/2269 Adenosine diphosphate Biopolymers Cell Line, Tumor Cloning, Molecular Deoxyribonucleic acid DNA DNA Damage Gene Expression Regulation - physiology Humanities and Social Sciences Humans multidisciplinary Nucleic acids Poly Adenosine Diphosphate Ribose - chemistry Protein Conformation Protein Structure, Tertiary Proteins - chemistry Proteins - genetics Proteins - metabolism Science Science (multidisciplinary)
Title	Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose)
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