Authors

Ivan Lebedev

Type

Text

Type

Dissertation

Advisor

Seeliger, Markus A | Glynn, Steven E | Moll, Ute | Bowen, Mark E | Bogenhagen, Daniel | .

Date

2016-12-01

Keywords

CypD, mPTP, Necrosis, p53, Stroke | Biology

Department

Department of Biochemistry and Structural Biology

Language

en_US

Source

This work is sponsored by the Stony Brook University Graduate School in compliance with the requirements for completion of degree.

Identifier

http://hdl.handle.net/11401/76942

Publisher

The Graduate School, Stony Brook University: Stony Brook, NY.

Format

application/pdf

Abstract

Tissue necrosis as a consequence of ischemia-reperfusion injury and oxidative damage is a leading cause of permanent disability and death worldwide. The complete mechanism by which cells undergo necrosis upon oxidative stress is not understood. In response to an oxidative insult, wildtype p53 has been implicated as a central regulatory component of the mitochondrial permeability transition (mPT), triggering necrosis. This process is associated with cellular stabilization and translocation of p53 into the mitochondrial matrix. I explore the mechanism by which p53 activates the key mPT regulator cyclophilin D (CypD); how the stability of p53 affects its ability to interact with CypD; and how Trap1, an Hsp90-related mitochondrial matrix chaperone protein and member of the mitochondrial unfolded protein response (mtUPR), is able to suppress mPT in a p53-dependent manner. I find that p53 needs to be structurally destabilized in order to interact with CypD and that catalytically active CypD causes strong aggregation of wildtype p53 protein (both full length and isolated DNA binding domain) into amyloid-type fibrils in vitro. NMR studies of CypD reveal slow exchange behavior, characteristic of a dynamic process such as isomerization. Moreover, I find that inhibition of Trap1 by the mitochondria-specific HSP90 ATPase antagonist gamitrinib strongly sensitizes primary mouse embryonic fibroblasts (MEFs) to mPT and permeability transition pore (mPTP) opening in a p53- and CypD-dependent manner. The result of my work proposes a model by which influx of unfolded p53 into the mitochondrial matrix in response to oxidative stress indirectly activates the normally inhibited CypD by displacing it from Trap1 complexes. This activates CypD’s isomerase activity. Liberated CypD then isomerizes multiple proteins including p53 (causing p53 aggregation) and the structural components of the mPTP pore, inducing pore opening. | Tissue necrosis as a consequence of ischemia-reperfusion injury and oxidative damage is a leading cause of permanent disability and death worldwide. The complete mechanism by which cells undergo necrosis upon oxidative stress is not understood. In response to an oxidative insult, wildtype p53 has been implicated as a central regulatory component of the mitochondrial permeability transition (mPT), triggering necrosis. This process is associated with cellular stabilization and translocation of p53 into the mitochondrial matrix. I explore the mechanism by which p53 activates the key mPT regulator cyclophilin D (CypD); how the stability of p53 affects its ability to interact with CypD; and how Trap1, an Hsp90-related mitochondrial matrix chaperone protein and member of the mitochondrial unfolded protein response (mtUPR), is able to suppress mPT in a p53-dependent manner. I find that p53 needs to be structurally destabilized in order to interact with CypD and that catalytically active CypD causes strong aggregation of wildtype p53 protein (both full length and isolated DNA binding domain) into amyloid-type fibrils in vitro. NMR studies of CypD reveal slow exchange behavior, characteristic of a dynamic process such as isomerization. Moreover, I find that inhibition of Trap1 by the mitochondria-specific HSP90 ATPase antagonist gamitrinib strongly sensitizes primary mouse embryonic fibroblasts (MEFs) to mPT and permeability transition pore (mPTP) opening in a p53- and CypD-dependent manner. The result of my work proposes a model by which influx of unfolded p53 into the mitochondrial matrix in response to oxidative stress indirectly activates the normally inhibited CypD by displacing it from Trap1 complexes. This activates CypD’s isomerase activity. Liberated CypD then isomerizes multiple proteins including p53 (causing p53 aggregation) and the structural components of the mPTP pore, inducing pore opening. | 154 pages

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