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@ARTICLE{Choe:126267,
author = {S. C. Choe$^*$ and A. Hamacher-Brady$^*$ and N. R.
Brady$^*$},
title = {{A}utophagy capacity and sub-mitochondrial heterogeneity
shape {B}nip3-induced mitophagy regulation of apoptosis.},
journal = {Cell communication and signaling},
volume = {13},
number = {1},
issn = {1478-811X},
address = {London},
publisher = {Biomed Central},
reportid = {DKFZ-2017-02382},
pages = {37},
year = {2015},
abstract = {Mitochondria are key regulators of apoptosis. In response
to stress, BH3-only proteins activate pro-apoptotic Bcl2
family proteins Bax and Bak, which induce mitochondrial
outer membrane permeabilization (MOMP). While the
large-scale mitochondrial release of pro-apoptotic proteins
activates caspase-dependent cell death, a limited release
results in sub-lethal caspase activation which promotes
tumorigenesis. Mitochondrial autophagy (mitophagy) targets
dysfunctional mitochondria for degradation by lysosomes, and
undergoes extensive crosstalk with apoptosis signaling, but
its influence on apoptosis remains undetermined. The
BH3-only protein Bnip3 integrates apoptosis and mitophagy
signaling at different signaling domains. Bnip3 inhibits
pro-survival Bcl2 members via its BH3 domain and activates
mitophagy through its LC3 Interacting Region (LIR), which is
responsible for binding to autophagosomes. Previously, we
have shown that Bnip3-activated mitophagy prior to apoptosis
induction can reduce mitochondrial activation of caspases,
suggesting that a reduction to mitochondrial levels may be
pro-survival. An outstanding question is whether organelle
dynamics and/or recently discovered subcellular variations
of protein levels responsible for both MOMP sensitivity and
crosstalk between apoptosis and mitophagy can influence the
cellular apoptosis decision event. To that end, here we
undertook a systems biology analysis of mitophagy-apoptosis
crosstalk at the level of cellular mitochondrial
populations.Based on experimental findings, we developed a
multi-scale, hybrid model with an individually adaptive
mitochondrial population, whose actions are determined by
protein levels, embedded in an agent-based model (ABM) for
simulating subcellular dynamics and local feedback via
reactive oxygen species signaling. Our model, supported by
experimental evidence, identified an emergent regulatory
structure within canonical apoptosis signaling. We show that
the extent of mitophagy is determined by levels and spatial
localization of autophagy capacity, and subcellular
mitochondrial protein heterogeneities. Our model identifies
mechanisms and conditions that alter the mitophagy decision
within mitochondrial subpopulations to an extent sufficient
to shape cellular outcome to apoptotic stimuli.Overall, our
modeling approach provides means to suggest new experiments
and implement findings at multiple scales in order to
understand how network topologies and subcellular
heterogeneities can influence signaling events at individual
organelle level, and hence, determine the emergence of
heterogeneity in cellular decisions due the actions of the
collective intra-cellular population.},
keywords = {BNIP3 protein, human (NLM Chemicals) / BNip3 protein, mouse
(NLM Chemicals) / Membrane Proteins (NLM Chemicals) /
Mitochondrial Proteins (NLM Chemicals) / Proto-Oncogene
Proteins (NLM Chemicals) / Proto-Oncogene Proteins c-bcl-2
(NLM Chemicals) / Reactive Oxygen Species (NLM Chemicals) /
Cytochromes c (NLM Chemicals)},
cin = {B170 / B190},
ddc = {610},
cid = {I:(DE-He78)B170-20160331 / I:(DE-He78)B190-20160331},
pnm = {312 - Functional and structural genomics (POF3-312)},
pid = {G:(DE-HGF)POF3-312},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:26253153},
pmc = {pmc:PMC4528699},
doi = {10.1186/s12964-015-0115-9},
url = {https://inrepo02.dkfz.de/record/126267},
}