Phosphoproteomic screening identifies Rab GTPases as novel downstream targets of PINK1
Mutations in the PTEN‐induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser 65 ) of the ubiquitin ligase Parkin and ubiquitin to stimulate Park...
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| Published in | The EMBO journal Vol. 34; no. 22; pp. 2840 - 2861 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Blackwell Publishing Ltd
12.11.2015
Nature Publishing Group UK Springer Nature B.V EMBO Press John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Mutations in the PTEN‐induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser
65
) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1‐dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub‐family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser
111
) in response to PINK1 activation. Using phospho‐specific antibodies raised against Ser
111
of each of the Rabs, we demonstrate that Rab Ser
111
phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient‐derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser
111
phosphorylation is not directly regulated by PINK1
in vitro
and demonstrate in cells the time course of Ser
111
phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser
65
. We further show mechanistically that phosphorylation at Ser
111
significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser
111
may represent novel biomarkers of PINK1 activity
in vivo
. Our findings also suggest that disruption of Rab GTPase‐mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease.
Synopsis
The Parkinson's disease‐mutated PINK1 kinase phosphorylates Parkin and ubiquitin. Phosphoproteomic screening reveals Rab8A, Rab8B and Rab13 GTPases as some of only few additional targets whose phosphorylation depends on PINK1 during mitophagy.
Activated PINK1 indirectly controls phosphorylation of serine 111 of Rab8A and closely related Rab GTPases.
Biochemical and cellular analysis imply an unknown intermediate PINK1‐dependent Rab8A Ser111 kinase or phosphatase.
PINK1‐directed activation of Parkin E3 ligase activity is independent of Rab8A Ser111 phosphorylation
Phosphorylation at Ser111 inhibits Rab8A activation by its guanine exchange factor, Rabin8.
Graphical Abstract
Ser111 modification of Rab8A, Rab8B and Rab13 represent some of only few PINK1‐dependent phosphorylation events and may regulate GTPase function during mitophagy. |
|---|---|
| AbstractList | Mutations in the PTEN‐induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser65) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1‐dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub‐family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser111) in response to PINK1 activation. Using phospho‐specific antibodies raised against Ser111 of each of the Rabs, we demonstrate that Rab Ser111 phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient‐derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser111 phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser111 phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser65. We further show mechanistically that phosphorylation at Ser111 significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser111 may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase‐mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease.
Synopsis
The Parkinson's disease‐mutated PINK1 kinase phosphorylates Parkin and ubiquitin. Phosphoproteomic screening reveals Rab8A, Rab8B and Rab13 GTPases as some of only few additional targets whose phosphorylation depends on PINK1 during mitophagy.
Activated PINK1 indirectly controls phosphorylation of serine 111 of Rab8A and closely related Rab GTPases.
Biochemical and cellular analysis imply an unknown intermediate PINK1‐dependent Rab8A Ser111 kinase or phosphatase.
PINK1‐directed activation of Parkin E3 ligase activity is independent of Rab8A Ser111 phosphorylation
Phosphorylation at Ser111 inhibits Rab8A activation by its guanine exchange factor, Rabin8.
Ser111 modification of Rab8A, Rab8B and Rab13 represent some of only few PINK1‐dependent phosphorylation events and may regulate GTPase function during mitophagy. Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser(65)) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1-dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub-family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser(111)) in response to PINK1 activation. Using phospho-specific antibodies raised against Ser(111) of each of the Rabs, we demonstrate that Rab Ser(111) phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient-derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser(111) phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser(111) phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser(65). We further show mechanistically that phosphorylation at Ser(111) significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser(111) may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase-mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease.Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser(65)) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1-dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub-family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser(111)) in response to PINK1 activation. Using phospho-specific antibodies raised against Ser(111) of each of the Rabs, we demonstrate that Rab Ser(111) phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient-derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser(111) phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser(111) phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser(65). We further show mechanistically that phosphorylation at Ser(111) significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser(111) may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase-mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser 65) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1-dependent phosphorylation targets in HEK (human embry-onic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub-family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser 111) in response to PINK1 activation. Using phospho-specific antibodies raised against Ser 111 of each of the Rabs, we demonstrate that Rab Ser 111 phosphoryla-tion occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient-derived fibroblasts stimulated by mitochondrial depolari-sation. We provide evidence that Rab8A GTPase Ser 111 phosphory-lation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser 111 phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser 65. We further show mechanistically that phosphorylation at Ser 111 significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/ 8B/13 at Ser 111 may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase-mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. Mutations in the PTEN‐induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser 65 ) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1‐dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub‐family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser 111 ) in response to PINK1 activation. Using phospho‐specific antibodies raised against Ser 111 of each of the Rabs, we demonstrate that Rab Ser 111 phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient‐derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser 111 phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser 111 phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser 65 . We further show mechanistically that phosphorylation at Ser 111 significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser 111 may represent novel biomarkers of PINK1 activity in vivo . Our findings also suggest that disruption of Rab GTPase‐mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. Synopsis The Parkinson's disease‐mutated PINK1 kinase phosphorylates Parkin and ubiquitin. Phosphoproteomic screening reveals Rab8A, Rab8B and Rab13 GTPases as some of only few additional targets whose phosphorylation depends on PINK1 during mitophagy. Activated PINK1 indirectly controls phosphorylation of serine 111 of Rab8A and closely related Rab GTPases. Biochemical and cellular analysis imply an unknown intermediate PINK1‐dependent Rab8A Ser111 kinase or phosphatase. PINK1‐directed activation of Parkin E3 ligase activity is independent of Rab8A Ser111 phosphorylation Phosphorylation at Ser111 inhibits Rab8A activation by its guanine exchange factor, Rabin8. Graphical Abstract Ser111 modification of Rab8A, Rab8B and Rab13 represent some of only few PINK1‐dependent phosphorylation events and may regulate GTPase function during mitophagy. Mutations in the PTEN ‐induced kinase 1 ( PINK 1) are causative of autosomal recessive Parkinson's disease ( PD ). We have previously reported that PINK 1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser 65 ) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK 1‐dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub‐family of Rab GTP ases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser 111 ) in response to PINK 1 activation. Using phospho‐specific antibodies raised against Ser 111 of each of the Rabs, we demonstrate that Rab Ser 111 phosphorylation occurs specifically in response to PINK 1 activation and is abolished in HeLa PINK 1 knockout cells and mutant PINK 1 PD patient‐derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTP ase Ser 111 phosphorylation is not directly regulated by PINK 1 in vitro and demonstrate in cells the time course of Ser 111 phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser 65 . We further show mechanistically that phosphorylation at Ser 111 significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor ( GEF ), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK 1 is able to regulate the phosphorylation of Rab GTP ases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser 111 may represent novel biomarkers of PINK 1 activity in vivo . Our findings also suggest that disruption of Rab GTP ase‐mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser65) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1-dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub-family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser111) in response to PINK1 activation. Using phospho-specific antibodies raised against Ser111 of each of the Rabs, we demonstrate that Rab Ser111 phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient-derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser111 phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser111 phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser65. We further show mechanistically that phosphorylation at Ser111 significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser111 may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase-mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. Synopsis The Parkinson's disease-mutated PINK1 kinase phosphorylates Parkin and ubiquitin. Phosphoproteomic screening reveals Rab8A, Rab8B and Rab13 GTPases as some of only few additional targets whose phosphorylation depends on PINK1 during mitophagy. Activated PINK1 indirectly controls phosphorylation of serine 111 of Rab8A and closely related Rab GTPases. Biochemical and cellular analysis imply an unknown intermediate PINK1-dependent Rab8A Ser111 kinase or phosphatase. PINK1-directed activation of Parkin E3 ligase activity is independent of Rab8A Ser111 phosphorylation Phosphorylation at Ser111 inhibits Rab8A activation by its guanine exchange factor, Rabin8. Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is activated by mitochondrial depolarisation and phosphorylates serine 65 (Ser(65)) of the ubiquitin ligase Parkin and ubiquitin to stimulate Parkin E3 ligase activity. Here, we have employed quantitative phosphoproteomics to search for novel PINK1-dependent phosphorylation targets in HEK (human embryonic kidney) 293 cells stimulated by mitochondrial depolarisation. This led to the identification of 14,213 phosphosites from 4,499 gene products. Whilst most phosphosites were unaffected, we strikingly observed three members of a sub-family of Rab GTPases namely Rab8A, 8B and 13 that are all phosphorylated at the highly conserved residue of serine 111 (Ser(111)) in response to PINK1 activation. Using phospho-specific antibodies raised against Ser(111) of each of the Rabs, we demonstrate that Rab Ser(111) phosphorylation occurs specifically in response to PINK1 activation and is abolished in HeLa PINK1 knockout cells and mutant PINK1 PD patient-derived fibroblasts stimulated by mitochondrial depolarisation. We provide evidence that Rab8A GTPase Ser(111) phosphorylation is not directly regulated by PINK1 in vitro and demonstrate in cells the time course of Ser(111) phosphorylation of Rab8A, 8B and 13 is markedly delayed compared to phosphorylation of Parkin at Ser(65). We further show mechanistically that phosphorylation at Ser(111) significantly impairs Rab8A activation by its cognate guanine nucleotide exchange factor (GEF), Rabin8 (by using the Ser111Glu phosphorylation mimic). These findings provide the first evidence that PINK1 is able to regulate the phosphorylation of Rab GTPases and indicate that monitoring phosphorylation of Rab8A/8B/13 at Ser(111) may represent novel biomarkers of PINK1 activity in vivo. Our findings also suggest that disruption of Rab GTPase-mediated signalling may represent a major mechanism in the neurodegenerative cascade of Parkinson's disease. |
| Author | Corvol, Jean‐Christophe Woodroof, Helen I Corti, Olga Trost, Matthias Gourlay, Robert Campbell, David G Kondapalli, Chandana Macartney, Thomas J Dill, Brian D Peggie, Mark Lai, Yu‐Chiang Lehneck, Ronny Muqit, Miratul MK Itzen, Aymelt Procter, James B |
| AuthorAffiliation | 4 Division of Signal Transduction Therapy College of Life Sciences University of Dundee Dundee UK 10 AP‐HP Département des maladies du système nerveux Hôpital de la Pitié‐Salpêtrière Paris France 7 Sorbonne Universités UPMC Paris 06 UMR S 1127 Paris France 1 MRC Protein Phosphorylation and Ubiquitylation Unit College of Life Sciences University of Dundee Dundee UK 2 Centre for Integrated Protein Science Munich Department Chemistry Technische Universität München Garching Germany 3 Division of Computational Biology College of Life Sciences University of Dundee Dundee UK 5 Inserm U 1127 Paris France 8 Institut du Cerveau et de la Moelle épinière ICM Paris France 9 Inserm Centre d'Investigation Clinique (CIC) Paris France 11 College of Medicine, Dentistry & Nursing University of Dundee Dundee UK 6 CNRS UMR 7225 Paris France |
| AuthorAffiliation_xml | – name: 1 MRC Protein Phosphorylation and Ubiquitylation Unit College of Life Sciences University of Dundee Dundee UK – name: 11 College of Medicine, Dentistry & Nursing University of Dundee Dundee UK – name: 6 CNRS UMR 7225 Paris France – name: 7 Sorbonne Universités UPMC Paris 06 UMR S 1127 Paris France – name: 10 AP‐HP Département des maladies du système nerveux Hôpital de la Pitié‐Salpêtrière Paris France – name: 4 Division of Signal Transduction Therapy College of Life Sciences University of Dundee Dundee UK – name: 5 Inserm U 1127 Paris France – name: 9 Inserm Centre d'Investigation Clinique (CIC) Paris France – name: 3 Division of Computational Biology College of Life Sciences University of Dundee Dundee UK – name: 8 Institut du Cerveau et de la Moelle épinière ICM Paris France – name: 2 Centre for Integrated Protein Science Munich Department Chemistry Technische Universität München Garching Germany |
| Author_xml | – sequence: 1 givenname: Yu-Chiang surname: Lai fullname: Lai, Yu-Chiang organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 2 givenname: Chandana surname: Kondapalli fullname: Kondapalli, Chandana organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 3 givenname: Ronny surname: Lehneck fullname: Lehneck, Ronny organization: Centre for Integrated Protein Science Munich, Department Chemistry, Technische Universität München, Garching, Germany – sequence: 4 givenname: James B surname: Procter fullname: Procter, James B organization: Division of Computational Biology, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 5 givenname: Brian D surname: Dill fullname: Dill, Brian D organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 6 givenname: Helen I surname: Woodroof fullname: Woodroof, Helen I organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 7 givenname: Robert surname: Gourlay fullname: Gourlay, Robert organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 8 givenname: Mark surname: Peggie fullname: Peggie, Mark organization: Division of Signal Transduction Therapy, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 9 givenname: Thomas J surname: Macartney fullname: Macartney, Thomas J organization: Division of Signal Transduction Therapy, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 10 givenname: Olga surname: Corti fullname: Corti, Olga organization: Inserm U 1127, Paris, France – sequence: 11 givenname: Jean-Christophe surname: Corvol fullname: Corvol, Jean-Christophe organization: Inserm U 1127, Paris, France – sequence: 12 givenname: David G surname: Campbell fullname: Campbell, David G organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 13 givenname: Aymelt surname: Itzen fullname: Itzen, Aymelt organization: Centre for Integrated Protein Science Munich, Department Chemistry, Technische Universität München, Garching, Germany – sequence: 14 givenname: Matthias surname: Trost fullname: Trost, Matthias email: Corresponding author. Tel: +44 1382 386402; , m.trost@dundee.ac.uk, Corresponding author. Tel: +44 1382 388377; , m.muqit@dundee.ac.uk organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK – sequence: 15 givenname: Miratul MK surname: Muqit fullname: Muqit, Miratul MK email: Corresponding author. Tel: +44 1382 386402; , m.trost@dundee.ac.uk, Corresponding author. Tel: +44 1382 388377; , m.muqit@dundee.ac.uk organization: MRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26471730$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-01285599$$DView record in HAL |
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| Copyright | The Author(s) 2015 2015 The Authors. Published under the terms of the CC BY 4.0 license 2015 The Authors. Published under the terms of the CC BY 4.0 license. 2015 EMBO Attribution |
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| DOI | 10.15252/embj.201591593 |
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| Genre | article Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural |
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| ISSN | 0261-4189 1460-2075 |
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| Issue | 22 |
| Keywords | phosphoproteomics PINK1 Parkinson's disease Rab GTPases Rab GTPases Subject Categories Membrane & Intracellular Transport Post-translational Modifications Methods & Resources Proteolysis & Proteomics |
| Language | English |
| License | Attribution 2015 The Authors. Published under the terms of the CC BY 4.0 license. Attribution: http://creativecommons.org/licenses/by This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Notes | GlaxoSmithKline Wellcome/MRC PD consortium Pfizer Investissements d'avenir - No. ANR-10-IAIHU-06 ark:/67375/WNG-0BRGKZC1-T Medical Research Council (MRC) - No. MC_UU_12016/5 BBSRC BBR - No. BB/L020742/1 istex:CC0F73DA46D8E73497F7BFC1EAC49A505D8D7E2B ArticleID:EMBJ201591593 Boehringer-Ingelheim German Research Foundation - No. DFG: SFB1035, project B05 Janssen Pharmaceutica Michael J. Fox Foundation for Parkinson's disease research AppendixExpanded View Figures PDFTable EV1Table EV2Table EV3Review Process File Merck KGaA Tenovus Scotland AstraZeneca MRC-PPU of University of Dundee Wellcome Trust Senior Research Fellowship - No. 101022/Z/13/Z NIGMS - No. P41-GM103311 Parkinson's UK ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally to this work |
| ORCID | 0000-0001-9733-2404 |
| OpenAccessLink | https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201591593 |
| PMID | 26471730 |
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| PublicationCentury | 2000 |
| PublicationDate | 12 November 2015 |
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| PublicationTitle | The EMBO journal |
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| PublicationYear | 2015 |
| Publisher | Blackwell Publishing Ltd Nature Publishing Group UK Springer Nature B.V EMBO Press John Wiley and Sons Inc |
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496 Kazlauskaite, Martinez‐Torres, Wilkie, Kumar, Peltier, Gonzalez, Johnson, Zhang, Hope, Peggie, Trost, van Aalten, Alessi, Prescott, Knebel, Walden, Muqit (CR38) 2015; 16 Kazlauskaite, Kelly, Johnson, Baillie, Hastie, Peggie, Macartney, Woodroof, Alessi, Pedrioli, Muqit (CR36) 2014; 4 Poole, Thomas, Andrews, McBride, Whitworth, Pallanck (CR71) 2008; 105 Wauer, Swatek, Wagstaff, Gladkova, Pruneda, Michel, Gersch, Johnson, Freund, Komander (CR93) 2015; 34 Ibanez, Lesage, Lohmann, Thobois, De, Borg, Agid, Durr, Brice (CR30) 2006; 129 Ritorto, Cook, Tyagi, Pedrioli, Trost (CR74) 2013; 12 Kitada, Asakawa, Hattori, Matsumine, Yamamura, Minoshima, Yokochi, Mizuno, Shimizu (CR42) 1998; 392 Kamp, Exner, Lutz, Wender, Hegermann, Brunner, Nuscher, Bartels, Giese, Beyer, Eimer, Winklhofer, Haass (CR34) 2010; 29 MacLeod, Rhinn, Kuwahara, Zolin, Di Paolo, McCabe, Marder, Honig, Clark, Small, Abeliovich (CR50) 2013; 77 Matsuda, Sato, Shiba, Okatsu, Saisho, Gautier, Sou, Saiki, Kawajiri, Sato, Kimura, Komatsu, Hattori, Tanaka (CR51) 2010; 189 Valente, Abou‐Sleiman, Caputo, Muqit, Harvey, Gispert, Ali, Del Turco, Bentivoglio, Healy, Albanese, Nussbaum, Gonzalez‐Maldonado, Deller, Salvi, Cortelli, Gilks, Latchman, Harvey, Dallapiccola (CR86) 2004; 304 Wang, Winter, Ashrafi, Schlehe, Wong, Selkoe, Rice, Steen, LaVoie, Schwarz (CR91) 2011; 147 Koyano, Matsuda (CR44) 2015; 1853 Sklan, Serrano, Einav, Pfeffer, Lambright, Glenn (CR82) 2007; 282 Ericsson, Hallberg, Detitta, Dekker, Nordlund (CR18) 2006; 357 Gitler, Bevis, Shorter, Strathearn, Hamamichi, Su, Caldwell, Caldwell, Rochet, McCaffery, Barlowe, Lindquist (CR24) 2008; 105 Kettenbach, Schweppe, Faherty, Pechenick, Pletnev, Gerber (CR40) 2011; 4 Larsen, Thingholm, Jensen, Roepstorff, Jorgensen (CR46) 2005; 4 Liu, Sawada, Lee, Yu, Silverio, Alapatt, Millan, Shen, Saxton, Kanao, Takahashi, Hattori, Imai, Lu (CR47) 2012; 8 Shiromizu, Adachi, Watanabe, Murakami, Kuga, Muraoka, Tomonaga (CR81) 2013; 12 Chen, Xie, Turkson, Zhuang (CR8) 2015; 35 Choi, Zhang, Deng, Hatcher, Patricelli, Zhao, Alessi, Gray (CR9) 2012; 3 Ordureau, Sarraf, Duda, Heo, Jedrychowski, Sviderskiy, Olszewski, Koerber, Xie, Beausoleil, Wells, Gygi, Schulman, Harper (CR63) 2014; 56 Powell, Forslund, Szklarczyk, Trachana, Roth, Huerta‐Cepas, Gabaldon, Rattei, Creevey, Kuhn, Jensen, von Mering, Bork (CR72) 2014; 42 2015; 35 2010; 12 2015; 34 2014; 70 2013; 4 2011; 117 2002; 52 2013; 22 2010; 107 2004; 25 2002; 158 2002; 13 2010; 189 2013; 288 2008; 7 2008; 105 2012; 13 2014; 23 2014b; 460 1998; 392 2009; 48 2008; 183 2013; 9 2003; 12 2013b; 125 2014; 127 2014a; 4 2014; 205 2014; 3 2010; 29 2013; 12 2015; 85 2013; 52 2011; 20 2008; 26 2010; 430 2003; 4 1999; 96 2009; 284 2014; 96 2010; 3 2003; 126 2010; 191 2014; 8 2014; 95 2006; 129 2012; 22 2014; 6 2014; 56 2006; 441 2010; 8 2014; 289 2015; 282 2009; 25 2015; 14 2015; 16 2009; 65 2011; 1 2007; 282 2015; 11 2013; 41 2008; 58 2011; 30 2010; 285 2014; 46 2015; 1853 2011; 4 2006; 357 2004; 304 2014; 510 2014; 42 2009; 33 2011; 147 2013a; 20 2012; 2 2009; 30 2012; 3 2013; 77 2013; 339 2000; 301 2011; 91 2005; 4 2010; 133 2013; 496 2014; 33 2012; 8 27115692 - Curr Biol. 2016 Apr 25;26(8):R332-4. doi: 10.1016/j.cub.2016.03.001. |
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| Snippet | Mutations in the PTEN‐induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is... Mutations in the PTEN-induced kinase 1 (PINK1) are causative of autosomal recessive Parkinson's disease (PD). We have previously reported that PINK1 is... Mutations in the PTEN ‐induced kinase 1 ( PINK 1) are causative of autosomal recessive Parkinson's disease ( PD ). We have previously reported that PINK 1 is... |
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| SubjectTerms | Amino Acid Substitution Biochemistry, Molecular Biology EMBO20 EMBO22 EMBO31 Enzyme Activation - genetics Enzymes Germinal Center Kinases HEK293 Cells HeLa Cells Humans Life Sciences Mutation Mutation, Missense Oncogene Proteins - genetics Oncogene Proteins - metabolism Parkinson's disease Parkinsonian Disorders - genetics Parkinsonian Disorders - metabolism Parkinsonian Disorders - pathology phosphoproteomics Phosphorylation Phosphorylation - genetics PINK1 Protein Kinases - genetics Protein Kinases - metabolism Protein Serine-Threonine Kinases - genetics Protein Serine-Threonine Kinases - metabolism Proteomics rab GTP-Binding Proteins - genetics rab GTP-Binding Proteins - metabolism Rab GTPases Resource |
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| Title | Phosphoproteomic screening identifies Rab GTPases as novel downstream targets of PINK1 |
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