Bcl-xL Retrotranslocates Bax from the Mitochondria into the Cytosol

Edlich, Frank; Banerjee, Soojay; Suzuki, Motoshi; Cleland, Megan M.; Arnoult, Damien; Wang, Chunxin; Neutzner, Albert; Tjandra, Nico; Youle, Richard J.

doi:10.1016/j.cell.2011.02.034

Cited by 634Cell death mechanisms and regulationMitochondrial Function and PathologyAutophagy in Disease and Therapy

Bcl-xL Retrotranslocates Bax from the Mitochondria into the Cytosol

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Edlich, Frank, Banerjee, Soojay, Suzuki, Motoshi, Cleland, Megan M., Arnoult, Damien, Wang, Chunxin, Neutzner, Albert, Tjandra, Nico +1 more·2011·Cell

DOI 10.1016/j.cell.2011.02.034PMC PMC3070914

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Abstract

The Bcl-2 family member Bax translocates from the cytosol to mitochondria, where it oligomerizes and permeabilizes the mitochondrial outer membrane to promote apoptosis. Bax activity is counteracted by prosurvival Bcl-2 proteins, but how they inhibit Bax remains controversial because they neither colocalize nor form stable complexes with Bax. We constrained Bax in its native cytosolic conformation within cells using intramolecular disulfide tethers. Bax tethers disrupt interaction with Bcl-x(L) in detergents and cell-free MOMP activity but unexpectedly induce Bax accumulation on mitochondria. Fluorescence loss in photobleaching (FLIP) reveals constant retrotranslocation of WT Bax, but not tethered Bax, from the mitochondria into the cytoplasm of healthy cells. Bax retrotranslocation depends on prosurvival Bcl-2 family proteins, and inhibition of retrotranslocation correlates with Bax accumulation on the mitochondria. We propose that Bcl-x(L) inhibits and maintains Bax in the cytosol by constant retrotranslocation of mitochondrial Bax.

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In physiological conditions, BAX continuously cycles between the OMM and the cytosol, where it exhibits a quiescent monomeric or inactive dimeric conformation.
“In physiological conditions, BAX continuously cycles between the OMM and the cytosol, where it exhibits a quiescent monomeric or inactive dimeric conformation [48–50].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [48]
Upon induction of apoptosis, BAX retrotranslocation ceases as the mitochondrial pools of BAX and BAK undergo direct or indirect activation by pro-apoptotic BH3-only proteins.
“Upon induction of apoptosis, BAX retrotranslocation ceases as the mitochondrial pools of BAX and BAK undergo direct or indirect activation (see below) by pro-apoptotic BH3-only proteins [48, 56–59].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [48]
In physiological conditions, some anti-apoptotic BCL2 proteins, such as BCL-XL, exert a protective role by promoting the retrotranslocation of BAX and (to a lesser degree) BAK from the mitochondria to the cytoplasm, thus limiting their mitochondrial pool.
“Of note, in physiological conditions, some anti-apoptotic BCL2 proteins, such as BCL-XL, exert a protective role by promoting the retrotranslocation of BAX and (to a lesser degree) BAK from the mitochondria to the cytoplasm, thus limiting their mitochondrial pool [48, 55, 111].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [48]

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Authors: Edlich, F., Banerjee, S., Suzuki, M., Cleland, M. M., Arnoult, D., Wang, C., Neutzner, A., Tjandra, N., & Youle, R. J.
Affiliations: National Institutes of Health (US)
Inserm (FR)
University Hospital of Basel (CH)
Corresponding author: Youle, Richard J.
ORCID: Edlich, Frank
Suzuki, Motoshi
Arnoult, Damien
Wang, Chunxin
Neutzner, Albert
Tjandra, Nico
Youle, Richard J.
Venue: Cell
Publisher: Elsevier BV
Published: 2011-04
Volume: 145
Issue: 1
Pages: 104-116
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2011.02.034
PMC: PMC3070914
OpenAlex: W1995354282
Cited by: 630
References: 50
Citations by year: 2026: 32 · 2025: 28 · 2024: 35 · 2023: 39 · 2022: 41 · 2021: 61 · 2020: 52 · 2019: 58 · 2018: 36 · 2017: 39 · 2016: 41 · 2015: 36 · 2014: 32 · 2013: 43 · 2012: 42
FWCI: 16.99
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 838 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Ligue Contre le Cancer
National Institutes of Health
National Institute of Neurological Disorders and Stroke (ZIANS002859)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords: Bax, Bcl-xL, retrotranslocation, mitochondrial outer membrane permeabilization, apoptosis, Bcl-2 family proteins, mitochondrial membrane potential, Bax oligomerization
MeSH terms: Cytosol, Humans, Mitochondria, Protein Conformation, Apoptosis, Protein Folding, Protein Transport, Cell Line, Tumor, bcl-X Protein, bcl-2-Associated X Protein

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Bcl-xL Retrotranslocates Bax from the Mitochondria into the Cytosol

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