Ubiquitin is phosphorylated by PINK1 to activate parkin
Ubiquitin, known for its role in post-translational modification of other proteins, undergoes post-translational modification itself; after a decrease in mitochondrial membrane potential, the kinase enzyme PINK1 phosphorylates ubiquitin at Ser 65, and the phosphorylated ubiquitin then interacts with...
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| Published in: | Nature (London) Vol. 510; no. 7503; pp. 162 - 166 |
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| Main Authors: | , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Nature Publishing Group UK
05-06-2014
Nature Publishing Group |
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| Abstract | Ubiquitin, known for its role in post-translational modification of other proteins, undergoes post-translational modification itself; after a decrease in mitochondrial membrane potential, the kinase enzyme PINK1 phosphorylates ubiquitin at Ser 65, and the phosphorylated ubiquitin then interacts with ubiquitin ligase (E3) enzyme parkin, which is also phosphorylated by PINK1, and this process is sufficient for full activation of parkin enzymatic activity.
Phosphorylated ubiquitin is a parkin activator
The small protein ubiquitin, familiar for its role in post-translational modification of other proteins by binding to them and regulating their activity or stability, is shown here to be the substrate of the kinase PINK1, which together with the ubiquitin ligase parkin is a causal gene for hereditary recessive Parkinsonism. Noriyuki Matsuda and colleagues show that following a decrease in mitochondrial membrane potential, PINK1 phosphorylates ubiquitin at serine residue 65; the phosphorylated ubiquitin then interacts with parkin, which is also phosphorylated by PINK1. This interaction allows full activation of parkin enzymatic activity, which involves tagging mitochondrial substrates with ubiquitin.
PINK1
(PTEN induced putative kinase 1) and
PARKIN
(also known as
PARK2
) have been identified as the causal genes responsible for hereditary recessive early-onset Parkinsonism
1
,
2
. PINK1 is a Ser/Thr kinase that specifically accumulates on depolarized mitochondria, whereas parkin is an E3 ubiquitin ligase that catalyses ubiquitin transfer to mitochondrial substrates
3
,
4
,
5
. PINK1 acts as an upstream factor for parkin
6
,
7
and is essential both for the activation of latent E3 parkin activity
8
and for recruiting parkin onto depolarized mitochondria
8
,
9
,
10
,
11
,
12
. Recently, mechanistic insights into mitochondrial quality control mediated by PINK1 and parkin have been revealed
3
,
4
,
5
, and PINK1-dependent phosphorylation of parkin has been reported
13
,
14
,
15
. However, the requirement of PINK1 for parkin activation was not bypassed by phosphomimetic parkin mutation
15
, and how PINK1 accelerates the E3 activity of parkin on damaged mitochondria is still obscure. Here we report that ubiquitin is the genuine substrate of PINK1. PINK1 phosphorylated ubiquitin at Ser 65 both
in vitro
and in cells, and a Ser 65 phosphopeptide derived from endogenous ubiquitin was only detected in cells in the presence of PINK1 and following a decrease in mitochondrial membrane potential. Unexpectedly, phosphomimetic ubiquitin bypassed PINK1-dependent activation of a phosphomimetic parkin mutant in cells. Furthermore, phosphomimetic ubiquitin accelerates discharge of the thioester conjugate formed by UBCH7 (also known as UBE2L3) and ubiquitin (UBCH7∼ubiquitin) in the presence of parkin
in vitro
, indicating that it acts allosterically. The phosphorylation-dependent interaction between ubiquitin and parkin suggests that phosphorylated ubiquitin unlocks autoinhibition of the catalytic cysteine. Our results show that PINK1-dependent phosphorylation of both parkin and ubiquitin is sufficient for full activation of parkin E3 activity. These findings demonstrate that phosphorylated ubiquitin is a parkin activator. |
|---|---|
| AbstractList | Ubiquitin, known for its role in post-translational modification of other proteins, undergoes post-translational modification itself; after a decrease in mitochondrial membrane potential, the kinase enzyme PINK1 phosphorylates ubiquitin at Ser 65, and the phosphorylated ubiquitin then interacts with ubiquitin ligase (E3) enzyme parkin, which is also phosphorylated by PINK1, and this process is sufficient for full activation of parkin enzymatic activity.
Phosphorylated ubiquitin is a parkin activator
The small protein ubiquitin, familiar for its role in post-translational modification of other proteins by binding to them and regulating their activity or stability, is shown here to be the substrate of the kinase PINK1, which together with the ubiquitin ligase parkin is a causal gene for hereditary recessive Parkinsonism. Noriyuki Matsuda and colleagues show that following a decrease in mitochondrial membrane potential, PINK1 phosphorylates ubiquitin at serine residue 65; the phosphorylated ubiquitin then interacts with parkin, which is also phosphorylated by PINK1. This interaction allows full activation of parkin enzymatic activity, which involves tagging mitochondrial substrates with ubiquitin.
PINK1
(PTEN induced putative kinase 1) and
PARKIN
(also known as
PARK2
) have been identified as the causal genes responsible for hereditary recessive early-onset Parkinsonism
1
,
2
. PINK1 is a Ser/Thr kinase that specifically accumulates on depolarized mitochondria, whereas parkin is an E3 ubiquitin ligase that catalyses ubiquitin transfer to mitochondrial substrates
3
,
4
,
5
. PINK1 acts as an upstream factor for parkin
6
,
7
and is essential both for the activation of latent E3 parkin activity
8
and for recruiting parkin onto depolarized mitochondria
8
,
9
,
10
,
11
,
12
. Recently, mechanistic insights into mitochondrial quality control mediated by PINK1 and parkin have been revealed
3
,
4
,
5
, and PINK1-dependent phosphorylation of parkin has been reported
13
,
14
,
15
. However, the requirement of PINK1 for parkin activation was not bypassed by phosphomimetic parkin mutation
15
, and how PINK1 accelerates the E3 activity of parkin on damaged mitochondria is still obscure. Here we report that ubiquitin is the genuine substrate of PINK1. PINK1 phosphorylated ubiquitin at Ser 65 both
in vitro
and in cells, and a Ser 65 phosphopeptide derived from endogenous ubiquitin was only detected in cells in the presence of PINK1 and following a decrease in mitochondrial membrane potential. Unexpectedly, phosphomimetic ubiquitin bypassed PINK1-dependent activation of a phosphomimetic parkin mutant in cells. Furthermore, phosphomimetic ubiquitin accelerates discharge of the thioester conjugate formed by UBCH7 (also known as UBE2L3) and ubiquitin (UBCH7∼ubiquitin) in the presence of parkin
in vitro
, indicating that it acts allosterically. The phosphorylation-dependent interaction between ubiquitin and parkin suggests that phosphorylated ubiquitin unlocks autoinhibition of the catalytic cysteine. Our results show that PINK1-dependent phosphorylation of both parkin and ubiquitin is sufficient for full activation of parkin E3 activity. These findings demonstrate that phosphorylated ubiquitin is a parkin activator. PINK1 (PTEN induced putative kinase 1)and PARKIN (also known as PARK2) have been identified as the causal genes responsible for hereditary recessive early-onset Parkinsonism. PINK1 is a Ser/Thr kinase that specifically accumulates on depolarized mitochondria, whereas parkin is an E3 ubiquitin ligase that catalyses ubiquitin transfer to mitochondrial substrates. PINK1 acts as an upstream factor for parkin and is essential both for the activation of latent E3 parkin activity and for recruiting parkin onto depolarized mitochondria. Recently, mechanistic insights into mitochondrial quality control mediated by PINK1 and parkin have been revealed, and PINK1-dependent phosphorylation of parkin has been reported. However, the requirement of PINK1 for parkin activation was not bypassed by phosphomimetic parkin mutation, and how PINK1 accelerates the E3 activity of parkin on damaged mitochondria is still obscure. Here we report that ubiquitin is the genuine substrate of PINK1. PINK1 phosphorylated ubiquitin at Ser 65 both in vitro and in cells, and a Ser 65 phosphopeptide derived from endogenous ubiquitin was only detected in cells in the presence of PINK1 and following a decrease in mitochondrial membrane potential. Unexpectedly, phosphomimetic ubiquitin bypassed PINK1-dependent activation of a phosphomimetic parkin mutant in cells. Furthermore, phosphomimetic ubiquitin accelerates discharge of the thioester conjugate formed by UBCH7 (also known as UBE2L3) and ubiquitin (UBCH7~ubiquitin) in the presence of parkin invitro, indicating that it acts allosterically. The phosphorylation-dependent interaction between ubiquitin and parkin suggests that phosphorylated ubiquitin unlocks autoinhibition of the catalytic cysteine. Our results show that PINK1-dependent phosphorylation of both parkin and ubiquitin is sufficient for full activation of parkin E3 activity. These findings demonstrate that phosphorylated ubiquitin is a parkin activator. PINK1 (PTEN induced putative kinase 1) and PARKIN (also known as PARK2) have been identified as the causal genes responsible for hereditary recessive early-onset Parkinsonism (1,2). PINK1 is a Ser/Thr kinase that specifically accumulates on depolarized mitochondria, whereas parkin is an E3 ubiquitin ligase that catalyses ubiquitin transfer to mitochondrial substrates (3-5). PINK1 acts as an upstream factor for parkin (6,7) and is essential both for the activation of latent E3 parkin activity (8) and for recruiting parkin onto depolarized mitochondria (8-12). Recently, mechanistic insights into mitochondrial quality control mediated by PINK1 and parkin have been revealed (3-5), and PINK1-dependent phosphorylation of parkin has been reported (13-15). However, the requirement of PINK1 for parkin activation was not bypassed by phosphomimetic parkin mutation (15), and how PINK1 accelerates the E3 activity of parkin on damaged mitochondria is still obscure. Here we report that ubiquitin is the genuine substrate of PINK1. PINK1 phosphorylated ubiquitin at Ser 65 both in vitro and in cells, and a Ser 65 phosphopeptide derived from endogenous ubiquitin was only detected in cells in the presence of PINK1 and following a decrease in mitochondrial membrane potential. Unexpectedly, phosphomimetic ubiquitin bypassed PINK1-dependent activation of a phosphomimetic parkin mutant in cells. Furthermore, phosphomimetic ubiquitin accelerates discharge of the thioester conjugate formed by UBCH7 (also known as UBE2L3) and ubiquitin (UBCH7~ubiquitin) in the presence of parkin invitro, indicating that it acts allosterically. The phosphorylation-dependent interaction between ubiquitin and parkin suggests that phosphorylated ubiquitin unlocks autoinhibition of the catalytic cysteine. Our results show that PINK1-dependent phosphorylation of both parkin and ubiquitin is sufficient for full activation of parkin E3 activity. These findings demonstrate that phosphorylated ubiquitin is a parkin activator. PINK1 (PTEN induced putative kinase 1) and PARKIN (also known as PARK2) have been identified as the causal genes responsible for hereditary recessive early-onset Parkinsonism. PINK1 is a Ser/Thr kinase that specifically accumulates on depolarized mitochondria, whereas parkin is an E3 ubiquitin ligase that catalyses ubiquitin transfer to mitochondrial substrates. PINK1 acts as an upstream factor for parkin and is essential both for the activation of latent E3 parkin activity and for recruiting parkin onto depolarized mitochondria. Recently, mechanistic insights into mitochondrial quality control mediated by PINK1 and parkin have been revealed, and PINK1-dependent phosphorylation of parkin has been reported. However, the requirement of PINK1 for parkin activation was not bypassed by phosphomimetic parkin mutation, and how PINK1 accelerates the E3 activity of parkin on damaged mitochondria is still obscure. Here we report that ubiquitin is the genuine substrate of PINK1. PINK1 phosphorylated ubiquitin at Ser 65 both in vitro and in cells, and a Ser 65 phosphopeptide derived from endogenous ubiquitin was only detected in cells in the presence of PINK1 and following a decrease in mitochondrial membrane potential. Unexpectedly, phosphomimetic ubiquitin bypassed PINK1-dependent activation of a phosphomimetic parkin mutant in cells. Furthermore, phosphomimetic ubiquitin accelerates discharge of the thioester conjugate formed by UBCH7 (also known as UBE2L3) and ubiquitin (UBCH7∼ubiquitin) in the presence of parkin in vitro, indicating that it acts allosterically. The phosphorylation-dependent interaction between ubiquitin and parkin suggests that phosphorylated ubiquitin unlocks autoinhibition of the catalytic cysteine. Our results show that PINK1-dependent phosphorylation of both parkin and ubiquitin is sufficient for full activation of parkin E3 activity. These findings demonstrate that phosphorylated ubiquitin is a parkin activator. |
| Audience | Academic |
| Author | Tamura, Yasushi Okatsu, Kei Tsuchiya, Hikaru Kosako, Hidetaka Kimura, Mayumi Kimura, Yoko Go, Etsu Endo, Toshiya Trempe, Jean-François Tanaka, Keiji Koyano, Fumika Hirokawa, Takatsugu Fon, Edward A. Matsuda, Noriyuki Yoshihara, Hidehito Saeki, Yasushi |
| Author_xml | – sequence: 1 givenname: Fumika surname: Koyano fullname: Koyano, Fumika organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba 277-8561, Japan – sequence: 2 givenname: Kei surname: Okatsu fullname: Okatsu, Kei organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba 277-8561, Japan – sequence: 3 givenname: Hidetaka surname: Kosako fullname: Kosako, Hidetaka organization: Division of Cell Signaling, Fujii Memorial Institute of Medical Sciences, The University of Tokushima, Tokushima 770-8503, Japan – sequence: 4 givenname: Yasushi surname: Tamura fullname: Tamura, Yasushi organization: Research Center for Materials Science, Nagoya University, Nagoya, Aichi 464-8602, Japan – sequence: 5 givenname: Etsu surname: Go fullname: Go, Etsu organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 6 givenname: Mayumi surname: Kimura fullname: Kimura, Mayumi organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 7 givenname: Yoko surname: Kimura fullname: Kimura, Yoko organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan, Graduate School of Agriculture, Shizuoka University, 836 Ohya, Shizuoka 422-8529, Japan – sequence: 8 givenname: Hikaru surname: Tsuchiya fullname: Tsuchiya, Hikaru organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 9 givenname: Hidehito surname: Yoshihara fullname: Yoshihara, Hidehito organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 10 givenname: Takatsugu surname: Hirokawa fullname: Hirokawa, Takatsugu organization: Molecular Profiling Research Center for Drug Discovery, National Institute of Advanced Industrial Science and Technology, 2-4-7 Aomi, Koto-ku, Tokyo 135-0064, Japan – sequence: 11 givenname: Toshiya surname: Endo fullname: Endo, Toshiya organization: JST-CREST/Department of Chemistry, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan, JST-CREST/Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo-motoyama, Kita-ku, Kyoto 603-8555, Japan – sequence: 12 givenname: Edward A. surname: Fon fullname: Fon, Edward A. organization: Department of Neurology and Neurosurgery, McGill Parkinson Program, Montreal Neurological Institute and Hospital, McGill University, Montréal, Québec H3A 2B4, Canada – sequence: 13 givenname: Jean-François surname: Trempe fullname: Trempe, Jean-François organization: Department of Pharmacology & Therapeutics, McGill University, Montréal, Québec H3G 1Y6, Canada – sequence: 14 givenname: Yasushi surname: Saeki fullname: Saeki, Yasushi organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 15 givenname: Keiji surname: Tanaka fullname: Tanaka, Keiji email: tanaka-kj@igakuken.or.jp organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan – sequence: 16 givenname: Noriyuki surname: Matsuda fullname: Matsuda, Noriyuki email: matsuda-nr@igakuken.or.jp organization: Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan, Protein Metabolism Project, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24784582$$D View this record in MEDLINE/PubMed |
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| Snippet | Ubiquitin, known for its role in post-translational modification of other proteins, undergoes post-translational modification itself; after a decrease in... PINK1 (PTEN induced putative kinase 1) and PARKIN (also known as PARK2) have been identified as the causal genes responsible for hereditary recessive... PINK1 (PTEN induced putative kinase 1)and PARKIN (also known as PARK2) have been identified as the causal genes responsible for hereditary recessive... |
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| Title | Ubiquitin is phosphorylated by PINK1 to activate parkin |
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