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Acyldepsipeptide analogs dysregulate human mitochondrial ClpP protease activity and cause apoptotic cell death

Acyldepsipeptide analogs dysregulate human mitochondrial ClpP protease activity and cause apoptotic cell death
Acyldepsipeptide analogs dysregulate human mitochondrial ClpP protease activity and cause apoptotic cell death

Acyldepsipeptides (ADEPs) are potential antibiotics that dysregulate the activity of the highly conserved tetradecameric bacterial ClpP protease, leading to bacterial cell death. Here, we identified ADEP analogs that are potent dysregulators of the human mitochondrial ClpP (HsClpP). These ADEPs interact tightly with HsClpP, causing the protease to non-specifically degrade model substrates. Dysregulation of HsClpP activity by ADEP was found to induce cytotoxic effects via activation of the intrinsic, caspase-dependent apoptosis. ADEP-HsClpP co-crystal structure was solved for one of the analogs revealing a highly complementary binding interface formed by two HsClpP neighboring subunits but, unexpectedly, with HsClpP in the compact conformation. Given that HsClpP is highly expressed in multiple cancers and has important roles in cell metastasis, our findings suggest a therapeutic potential for ADEPs in cancer treatment.

Acylation, Anti-Bacterial Agents/adverse effects, Apoptosis/drug effects, Bacterial Infections/drug therapy, Cell Line, Tumor, Depsipeptides/adverse effects, Endopeptidase Clp/chemistry, HEK293 Cells, Humans, Mitochondria/drug effects, Molecular Docking Simulation, Neoplasms/drug therapy
2451-9448
1017-1030.e9
Wong, Keith S
c1a03129-12be-45e7-be1c-6b10c966e53c
Mabanglo, Mark F
389f47da-ecf4-48f3-bf3d-ca10df5ca816
Seraphim, Thiago V
b2f77a83-6b02-48c3-a806-f98f114b5747
Mollica, Antonio
8cfdcaf7-fd8c-4d0b-98c8-45719d05b761
Mao, Yu-Qian
17492790-21cd-4392-95e6-b90bd5db086a
Rizzolo, Kamran
536a53b9-94c8-4dbd-9a88-64424c805d44
Leung, Elisa
89deba98-42d9-449e-9079-d240159c4c04
Moutaoufik, Mohamed T
505c59af-59ea-4e7c-95f5-c5606f962243
Hoell, Larissa
3ef5fa73-db73-41ab-96bf-fabc0b09c295
Phanse, Sadhna
237efb13-805c-4151-98fe-bb656dac3810
Goodreid, Jordan
3c424c0e-62c8-4b9e-ad9c-9d9d1432a92c
Barbosa, Leandro R S
1f14d262-2868-407f-8520-d8b003de4aa4
Ramos, Carlos H I
f7d334d1-1d14-4a12-8a72-2b0af0c5c887
Babu, Mohan
813a9ae5-a8cb-4af4-a245-a1511ef74e1e
Mennella, Vito
43c60e29-c0a7-4ab8-8e5c-fcb59f70a28a
Batey, Robert A
0386bd95-dd8c-4a11-9823-c1e0a70ce6f8
Schimmer, Aaron D
65f83466-bd4b-43eb-aabd-c7534a3aada4
Houry, Walid A
19af9fdf-cdac-4edc-97a4-4b8a722b5fd7
Wong, Keith S
c1a03129-12be-45e7-be1c-6b10c966e53c
Mabanglo, Mark F
389f47da-ecf4-48f3-bf3d-ca10df5ca816
Seraphim, Thiago V
b2f77a83-6b02-48c3-a806-f98f114b5747
Mollica, Antonio
8cfdcaf7-fd8c-4d0b-98c8-45719d05b761
Mao, Yu-Qian
17492790-21cd-4392-95e6-b90bd5db086a
Rizzolo, Kamran
536a53b9-94c8-4dbd-9a88-64424c805d44
Leung, Elisa
89deba98-42d9-449e-9079-d240159c4c04
Moutaoufik, Mohamed T
505c59af-59ea-4e7c-95f5-c5606f962243
Hoell, Larissa
3ef5fa73-db73-41ab-96bf-fabc0b09c295
Phanse, Sadhna
237efb13-805c-4151-98fe-bb656dac3810
Goodreid, Jordan
3c424c0e-62c8-4b9e-ad9c-9d9d1432a92c
Barbosa, Leandro R S
1f14d262-2868-407f-8520-d8b003de4aa4
Ramos, Carlos H I
f7d334d1-1d14-4a12-8a72-2b0af0c5c887
Babu, Mohan
813a9ae5-a8cb-4af4-a245-a1511ef74e1e
Mennella, Vito
43c60e29-c0a7-4ab8-8e5c-fcb59f70a28a
Batey, Robert A
0386bd95-dd8c-4a11-9823-c1e0a70ce6f8
Schimmer, Aaron D
65f83466-bd4b-43eb-aabd-c7534a3aada4
Houry, Walid A
19af9fdf-cdac-4edc-97a4-4b8a722b5fd7

Wong, Keith S, Mabanglo, Mark F, Seraphim, Thiago V, Mollica, Antonio, Mao, Yu-Qian, Rizzolo, Kamran, Leung, Elisa, Moutaoufik, Mohamed T, Hoell, Larissa, Phanse, Sadhna, Goodreid, Jordan, Barbosa, Leandro R S, Ramos, Carlos H I, Babu, Mohan, Mennella, Vito, Batey, Robert A, Schimmer, Aaron D and Houry, Walid A (2018) Acyldepsipeptide analogs dysregulate human mitochondrial ClpP protease activity and cause apoptotic cell death. Cell Chemical Biology, 25 (8), 1017-1030.e9. (doi:10.1016/j.chembiol.2018.05.014).

Record type: Article

Abstract

Acyldepsipeptides (ADEPs) are potential antibiotics that dysregulate the activity of the highly conserved tetradecameric bacterial ClpP protease, leading to bacterial cell death. Here, we identified ADEP analogs that are potent dysregulators of the human mitochondrial ClpP (HsClpP). These ADEPs interact tightly with HsClpP, causing the protease to non-specifically degrade model substrates. Dysregulation of HsClpP activity by ADEP was found to induce cytotoxic effects via activation of the intrinsic, caspase-dependent apoptosis. ADEP-HsClpP co-crystal structure was solved for one of the analogs revealing a highly complementary binding interface formed by two HsClpP neighboring subunits but, unexpectedly, with HsClpP in the compact conformation. Given that HsClpP is highly expressed in multiple cancers and has important roles in cell metastasis, our findings suggest a therapeutic potential for ADEPs in cancer treatment.

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More information

Accepted/In Press date: 18 May 2018
e-pub ahead of print date: 28 June 2018
Published date: 16 August 2018
Keywords: Acylation, Anti-Bacterial Agents/adverse effects, Apoptosis/drug effects, Bacterial Infections/drug therapy, Cell Line, Tumor, Depsipeptides/adverse effects, Endopeptidase Clp/chemistry, HEK293 Cells, Humans, Mitochondria/drug effects, Molecular Docking Simulation, Neoplasms/drug therapy

Identifiers

Local EPrints ID: 434162
URI: http://eprints.soton.ac.uk/id/eprint/434162
ISSN: 2451-9448
PURE UUID: 68b79c72-a434-4daa-a352-ae91b4581f9e
ORCID for Vito Mennella: ORCID iD orcid.org/0000-0002-4842-9012

Catalogue record

Date deposited: 13 Sep 2019 16:30
Last modified: 16 Mar 2024 04:03

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Contributors

Author: Keith S Wong
Author: Mark F Mabanglo
Author: Thiago V Seraphim
Author: Antonio Mollica
Author: Yu-Qian Mao
Author: Kamran Rizzolo
Author: Elisa Leung
Author: Mohamed T Moutaoufik
Author: Larissa Hoell
Author: Sadhna Phanse
Author: Jordan Goodreid
Author: Leandro R S Barbosa
Author: Carlos H I Ramos
Author: Mohan Babu
Author: Vito Mennella ORCID iD
Author: Robert A Batey
Author: Aaron D Schimmer
Author: Walid A Houry

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