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In particular, whether stochasticity in subcellular protein distributions and interactions across cytosol and mitochondria can realistically contribute to mitochondrial MOMP heterogeneity has not yet been studied. To assess this, we sequentially built and experimentally parameterized a particle-based, cell-sized model including cytosolic and mitochondrial compartments, and that featured a reduced interactome of MCL-1, BAK and tBID. High-performance computing enabled cell-scale simulations of protein distributions and interactions to understand how and under which conditions stochasticity could contribute to heterogeneity in MOMP susceptibility. Our results show that stochastic effects strongly predispose sub-pools of fragmented mitochondria to MOMP under low apoptotic stress. At higher apoptotic stress, fractions of small mitochondria were more likely to escape MOMP than large mitochondria. Retrospective quantification of mitochondrial sizes in experimental scenarios of minority and majority MOMP confirmed these findings. We therefore conclude that stochasticity substantially contributes to enabling small or fragmented mitochondria to undergo MOMP in minority MOMP scenarios and to escape MOMP in majority MOMP scenarios.","annote":"","author":[{"family":"Geiger","given":"Jenny"},{"family":"Klötzer","given":"Fabian"},{"family":"Pollak","given":"Nadine"},{"family":"Fullstone","given":"Gavin"},{"family":"Rehm","given":"Markus"}],"citation-label":"geiger2025stochasticity","collection-editor":[],"collection-title":"","container-author":[],"container-title":"Cell Death & Disease","documents":[],"edition":"","editor":[],"event-date":{"date-parts":[["2025"]],"literal":"2025"},"event-place":"","id":"13d070ca717db4ad910b6f698ff75056simtechpuma","interhash":"f4e9c4247e6172bfe4a2c1d3d3b1202b","intrahash":"13d070ca717db4ad910b6f698ff75056","issue":"1","issued":{"date-parts":[["2025"]],"literal":"2025"},"keyword":"PN2 EXC2075 PN2-1A 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A key event during apoptosis is mitochondrial outer membrane permeabilization (MOMP), which typically proceeds in a rapid all-or-none fashion. If MOMP occurs only in a subset of mitochondria (minority MOMP), it can be sublethal and contribute to tumorigenesis and cancer progression. Similarly, individual mitochondria escaping widespread MOMP (majority MOMP) can allow cancer cells to recover if apoptosis execution fails. How such heterogeneities in mitochondrial MOMP responsiveness arise within cells is incompletely understood. In particular, whether stochasticity in subcellular protein distributions and interactions across cytosol and mitochondria can realistically contribute to mitochondrial MOMP heterogeneity has not yet been studied. To assess this, we sequentially built and experimentally parameterized a particle-based, cell-sized model including cytosolic and mitochondrial compartments, and that featured a reduced interactome of MCL-1, BAK and tBID. High-performance computing enabled cell-scale simulations of protein distributions and interactions to understand how and under which conditions stochasticity could contribute to heterogeneity in MOMP susceptibility. Our results show that stochastic effects strongly predispose sub-pools of fragmented mitochondria to MOMP under low apoptotic stress. At higher apoptotic stress, fractions of small mitochondria were more likely to escape MOMP than large mitochondria. Retrospective quantification of mitochondrial sizes in experimental scenarios of minority and majority MOMP confirmed these findings. We therefore conclude that stochasticity substantially contributes to enabling small or fragmented mitochondria to undergo MOMP in minority MOMP scenarios and to escape MOMP in majority MOMP scenarios.","annote":"","author":[{"family":"Geiger","given":"Jenny"},{"family":"Klötzer","given":"Fabian"},{"family":"Pollak","given":"Nadine"},{"family":"Fullstone","given":"Gavin"},{"family":"Rehm","given":"Markus"}],"citation-label":"geiger2025stochasticity","collection-editor":[],"collection-title":"","container-author":[],"container-title":"Cell Death & Disease","documents":[],"edition":"","editor":[],"event-date":{"date-parts":[["2025"]],"literal":"2025"},"event-place":"","id":"13d070ca717db4ad910b6f698ff75056simtech","interhash":"f4e9c4247e6172bfe4a2c1d3d3b1202b","intrahash":"13d070ca717db4ad910b6f698ff75056","issue":"1","issued":{"date-parts":[["2025"]],"literal":"2025"},"keyword":"PN2 curated EXC2075 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As chemotherapy primarily eliminates cancer cells by apoptosis, we here evaluated if the expression of key apoptosis regulators (Bax, Bak, Bcl-2, Bcl-xL, Smac, Procaspase-9, Apaf-1, Procaspase-3 and XIAP) allows prognosticating PFS in stage III/IV melanoma patients. Following antibody validation, marker expression was determined by automated and manual scoring of immunohistochemically stained tissue microarrays (TMAs) constructed from treatment-naive metastatic melanoma biopsies. Interestingly and counter-intuitively, low expression of the pro-apoptotic proteins Bax, Bak and Smac indicated better prognosis (log-rank p \\textless 0.0001, p = 0.0301 and p = 0.0227 for automated and p = 0.0422, p = 0.0410 and p = 0.0073 for manual scoring). These findings were independently validated in the cancer genome atlas (TCGA) metastatic melanoma cohort (TCGA-SKCM) at transcript level (log-rank p = 0.0004, p = 0.0104 and p = 0.0377). Taking expression heterogeneity between the markers in individual tumour samples into account allowed defining combinatorial Bax, Bak, Smac signatures that were associated with significantly increased PFS (p = 0.0002 and p = 0.0028 at protein and transcript level, respectively). Furthermore, combined low expression of Bax, Bak and Smac allowed predicting prolonged PFS (\\textgreater 12 months) on a case-by-case basis (area under the receiver operating characteristic curve (ROC AUC) = 0.79). 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