A PERK–miR-211 axis suppresses circadian regulators and protein synthesis to promote cancer cell survival
The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR a...
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| Vydáno v: | Nature cell biology Ročník 20; číslo 1; s. 104 - 115 |
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| Hlavní autoři: | , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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London
Nature Publishing Group UK
01.01.2018
Nature Publishing Group |
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| ISSN: | 1465-7392, 1476-4679, 1476-4679 |
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| Abstract | The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt’s lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression.
PERK regulates tumour cell survival. Bu et al. show that the unfolded protein response protein PERK induces miR-211 repression of the circadian factor Bmal1 to regulate protein synthesis and stress responses, contributing to tumour progression. |
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| AbstractList | The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt's lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression. PERK regulates tumour cell survival. Bu et al. show that the unfolded protein response protein PERK induces miR-211 repression of the circadian factor Bmal1 to regulate protein synthesis and stress responses, contributing to tumour progression. The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt's lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression. The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt's lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression.The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt's lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression. The unfolded protein response (UPR) is a stress-activated signalling pathway that regulates cell proliferation, metabolism and survival. The circadian clock coordinates metabolism and signal transduction with light/dark cycles. We explore how UPR signalling interfaces with the circadian clock. UPR activation induces a 10 h phase shift in circadian oscillations through induction of miR-211, a PERK-inducible microRNA that transiently suppresses both Bmal1 and Clock, core circadian regulators. Molecular investigation reveals that miR-211 directly regulates Bmal1 and Clock via distinct mechanisms. Suppression of Bmal1 and Clock has the anticipated impact on expression of select circadian genes, but we also find that repression of Bmal1 is essential for UPR-dependent inhibition of protein synthesis and cell adaptation to stresses that disrupt endoplasmic reticulum homeostasis. Our data demonstrate that c-Myc-dependent activation of the UPR inhibits Bmal1 in Burkitt’s lymphoma, thereby suppressing both circadian oscillation and ongoing protein synthesis to facilitate tumour progression. PERK regulates tumour cell survival. Bu et al. show that the unfolded protein response protein PERK induces miR-211 repression of the circadian factor Bmal1 to regulate protein synthesis and stress responses, contributing to tumour progression. |
| Audience | Academic |
| Author | Ruggero, Davide Oran, Amanda Koumenis, Constantinos Diehl, J. Alan Tameire, Feven Yoshida, Akihiro Altman, Brian J. Wertheim, Gerald B. Chitnis, Nilesh Armeson, Kent E. Dang, Chi V. Bu, Yiwen McMahon, Steven B. Gennaro, Victoria Fuchs, Serge Y. |
| Author_xml | – sequence: 1 givenname: Yiwen surname: Bu fullname: Bu, Yiwen organization: Department of Biochemistry and Molecular Biology and Hollings Cancer Center, Medical University of South Carolina – sequence: 2 givenname: Akihiro surname: Yoshida fullname: Yoshida, Akihiro organization: Department of Biochemistry and Molecular Biology and Hollings Cancer Center, Medical University of South Carolina – sequence: 3 givenname: Nilesh surname: Chitnis fullname: Chitnis, Nilesh organization: Department of Biochemistry and Molecular Biology and Hollings Cancer Center, Medical University of South Carolina – sequence: 4 givenname: Brian J. orcidid: 0000-0002-3954-4916 surname: Altman fullname: Altman, Brian J. organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 5 givenname: Feven surname: Tameire fullname: Tameire, Feven organization: Department of Radiation Oncology, Perelman School of Medicine, University of Pennsylvania – sequence: 6 givenname: Amanda surname: Oran fullname: Oran, Amanda organization: Department of Cancer Biology, Sidney Kimmel Medical College, Thomas Jefferson University – sequence: 7 givenname: Victoria surname: Gennaro fullname: Gennaro, Victoria organization: Department of Cancer Biology, Sidney Kimmel Medical College, Thomas Jefferson University – sequence: 8 givenname: Kent E. surname: Armeson fullname: Armeson, Kent E. organization: Department of Public Health Sciences and Hollings Cancer Center, Medical University of South Carolina – sequence: 9 givenname: Steven B. surname: McMahon fullname: McMahon, Steven B. organization: Department of Cancer Biology, Sidney Kimmel Medical College, Thomas Jefferson University – sequence: 10 givenname: Gerald B. surname: Wertheim fullname: Wertheim, Gerald B. organization: Department of Pathology and Laboratory Medicine, Children’s Hospital of Philadelphia – sequence: 11 givenname: Chi V. surname: Dang fullname: Dang, Chi V. organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 12 givenname: Davide surname: Ruggero fullname: Ruggero, Davide organization: Departments of Urology and Cellular and Molecular Pharmacology, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco – sequence: 13 givenname: Constantinos surname: Koumenis fullname: Koumenis, Constantinos organization: Department of Radiation Oncology, Perelman School of Medicine, University of Pennsylvania – sequence: 14 givenname: Serge Y. surname: Fuchs fullname: Fuchs, Serge Y. organization: Department of Biomedical Sciences, School of Veterinary Medicine – sequence: 15 givenname: J. Alan orcidid: 0000-0001-9854-5049 surname: Diehl fullname: Diehl, J. Alan email: diehl@musc.edu organization: Department of Biochemistry and Molecular Biology and Hollings Cancer Center, Medical University of South Carolina |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29230015$$D View this record in MEDLINE/PubMed |
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| Title | A PERK–miR-211 axis suppresses circadian regulators and protein synthesis to promote cancer cell survival |
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