PML regulates apoptosis at endoplasmic reticulum by modulating calcium release

The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is currently unknown. We show that extranuclear Pml was specifically enriched at the endoplasmic reticulum (ER) and at the mitochondria-associa...

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Published in:Science (American Association for the Advancement of Science) Vol. 330; no. 6008; p. 1247
Main Authors: Giorgi, Carlotta, Ito, Keisuke, Lin, Hui-Kuan, Santangelo, Clara, Wieckowski, Mariusz R, Lebiedzinska, Magdalena, Bononi, Angela, Bonora, Massimo, Duszynski, Jerzy, Bernardi, Rosa, Rizzuto, Rosario, Tacchetti, Carlo, Pinton, Paolo, Pandolfi, Pier Paolo
Format: Journal Article
Language:English
Published: United States 26.11.2010
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ISSN:1095-9203, 1095-9203
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Abstract The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is currently unknown. We show that extranuclear Pml was specifically enriched at the endoplasmic reticulum (ER) and at the mitochondria-associated membranes, signaling domains involved in ER-to-mitochondria calcium ion (Ca(2+)) transport and in induction of apoptosis. We found Pml in complexes of large molecular size with the inositol 1,4,5-trisphosphate receptor (IP(3)R), protein kinase Akt, and protein phosphatase 2a (PP2a). Pml was essential for Akt- and PP2a-dependent modulation of IP(3)R phosphorylation and in turn for IP(3)R-mediated Ca(2+) release from ER. Our findings provide a mechanistic explanation for the pleiotropic role of Pml in apoptosis and identify a pharmacological target for the modulation of Ca(2+) signals.
AbstractList The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is currently unknown. We show that extranuclear Pml was specifically enriched at the endoplasmic reticulum (ER) and at the mitochondria-associated membranes, signaling domains involved in ER-to-mitochondria calcium ion (Ca(2+)) transport and in induction of apoptosis. We found Pml in complexes of large molecular size with the inositol 1,4,5-trisphosphate receptor (IP(3)R), protein kinase Akt, and protein phosphatase 2a (PP2a). Pml was essential for Akt- and PP2a-dependent modulation of IP(3)R phosphorylation and in turn for IP(3)R-mediated Ca(2+) release from ER. Our findings provide a mechanistic explanation for the pleiotropic role of Pml in apoptosis and identify a pharmacological target for the modulation of Ca(2+) signals.
The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is currently unknown. We show that extranuclear Pml was specifically enriched at the endoplasmic reticulum (ER) and at the mitochondria-associated membranes, signaling domains involved in ER-to-mitochondria calcium ion (Ca(2+)) transport and in induction of apoptosis. We found Pml in complexes of large molecular size with the inositol 1,4,5-trisphosphate receptor (IP(3)R), protein kinase Akt, and protein phosphatase 2a (PP2a). Pml was essential for Akt- and PP2a-dependent modulation of IP(3)R phosphorylation and in turn for IP(3)R-mediated Ca(2+) release from ER. Our findings provide a mechanistic explanation for the pleiotropic role of Pml in apoptosis and identify a pharmacological target for the modulation of Ca(2+) signals.The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is currently unknown. We show that extranuclear Pml was specifically enriched at the endoplasmic reticulum (ER) and at the mitochondria-associated membranes, signaling domains involved in ER-to-mitochondria calcium ion (Ca(2+)) transport and in induction of apoptosis. We found Pml in complexes of large molecular size with the inositol 1,4,5-trisphosphate receptor (IP(3)R), protein kinase Akt, and protein phosphatase 2a (PP2a). Pml was essential for Akt- and PP2a-dependent modulation of IP(3)R phosphorylation and in turn for IP(3)R-mediated Ca(2+) release from ER. Our findings provide a mechanistic explanation for the pleiotropic role of Pml in apoptosis and identify a pharmacological target for the modulation of Ca(2+) signals.
Author Lin, Hui-Kuan
Giorgi, Carlotta
Tacchetti, Carlo
Bernardi, Rosa
Pinton, Paolo
Duszynski, Jerzy
Ito, Keisuke
Lebiedzinska, Magdalena
Pandolfi, Pier Paolo
Bonora, Massimo
Rizzuto, Rosario
Santangelo, Clara
Wieckowski, Mariusz R
Bononi, Angela
Author_xml – sequence: 1
  givenname: Carlotta
  surname: Giorgi
  fullname: Giorgi, Carlotta
  organization: Department of Experimental and Diagnostic Medicine, Section of General Pathology, Interdisciplinary Center for the Study of Inflammation (ICSI), Emilia Romagna Laboratory BioPharmaNet, and Laboratory for Technologies of Advanced Therapies (LTTA) University of Ferrara, Ferrara, Italy
– sequence: 2
  givenname: Keisuke
  surname: Ito
  fullname: Ito, Keisuke
– sequence: 3
  givenname: Hui-Kuan
  surname: Lin
  fullname: Lin, Hui-Kuan
– sequence: 4
  givenname: Clara
  surname: Santangelo
  fullname: Santangelo, Clara
– sequence: 5
  givenname: Mariusz R
  surname: Wieckowski
  fullname: Wieckowski, Mariusz R
– sequence: 6
  givenname: Magdalena
  surname: Lebiedzinska
  fullname: Lebiedzinska, Magdalena
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  surname: Bononi
  fullname: Bononi, Angela
– sequence: 8
  givenname: Massimo
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  fullname: Bonora, Massimo
– sequence: 9
  givenname: Jerzy
  surname: Duszynski
  fullname: Duszynski, Jerzy
– sequence: 10
  givenname: Rosa
  surname: Bernardi
  fullname: Bernardi, Rosa
– sequence: 11
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  surname: Rizzuto
  fullname: Rizzuto, Rosario
– sequence: 12
  givenname: Carlo
  surname: Tacchetti
  fullname: Tacchetti, Carlo
– sequence: 13
  givenname: Paolo
  surname: Pinton
  fullname: Pinton, Paolo
– sequence: 14
  givenname: Pier Paolo
  surname: Pandolfi
  fullname: Pandolfi, Pier Paolo
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21030605$$D View this record in MEDLINE/PubMed
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References 21109655 - Science. 2010 Nov 26;330(6008):1183-4. doi: 10.1126/science.1199405.
21145493 - Dev Cell. 2010 Dec 14;19(6):789-90. doi: 10.1016/j.devcel.2010.11.013.
33766887 - Science. 2021 Mar 26;371(6536):eabi4740. doi: 10.1126/science.abi4740.
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– reference: 21145493 - Dev Cell. 2010 Dec 14;19(6):789-90. doi: 10.1016/j.devcel.2010.11.013.
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Snippet The promyelocytic leukemia (PML) tumor suppressor is a pleiotropic modulator of apoptosis. However, the molecular basis for such a diverse proapoptotic role is...
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SubjectTerms Adenosine Triphosphate - metabolism
Animals
Apoptosis
Calcium - metabolism
Calcium Signaling
Cell Line
Cell Nucleus - metabolism
Cells, Cultured
Cytosol - metabolism
Endoplasmic Reticulum - metabolism
Homeostasis
Humans
Inositol 1,4,5-Trisphosphate - metabolism
Inositol 1,4,5-Trisphosphate Receptors - metabolism
Intracellular Membranes - metabolism
Mice
Mitochondria - metabolism
Nuclear Proteins - genetics
Nuclear Proteins - metabolism
Phosphorylation
Promyelocytic Leukemia Protein
Protein Phosphatase 2 - metabolism
Proto-Oncogene Proteins c-akt - metabolism
Recombinant Fusion Proteins - metabolism
Stress, Physiological
Transcription Factors - genetics
Transcription Factors - metabolism
Tumor Suppressor Proteins - genetics
Tumor Suppressor Proteins - metabolism
Title PML regulates apoptosis at endoplasmic reticulum by modulating calcium release
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