. 2017 Jul;18(7):1077-1089.

doi: 10.15252/embr.201643602. Epub 2017 May 31.

Mitochondrial permeability transition involves dissociation of F₁F_O ATP synthase dimers and C-ring conformation

Massimo Bonora^{1

2}, Claudia Morganti^{1

2}, Giampaolo Morciano^{1

2}, Gaia Pedriali^{1

2}, Magdalena Lebiedzinska-Arciszewska³, Giorgio Aquila⁴, Carlotta Giorgi^{1

2}, Paola Rizzo⁴, Gianluca Campo⁵, Roberto Ferrari⁵, Guido Kroemer^{6

7

8

9

10

11

12}, Mariusz R Wieckowski¹³, Lorenzo Galluzzi^{14

15}, Paolo Pinton^{16

2}

Affiliations

¹ Department of Morphology, Surgery and Experimental Medicine, Section of General Pathology, University of Ferrara, Ferrara, Italy.
² Laboratory for Technologies of Advanced Therapies (LTTA), University of Ferrara, Ferrara, Italy.
³ Department of Biochemistry, Nencki Institute of Experimental Biology, Warsaw, Poland.
⁴ Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Ferrara, Italy.
⁵ Cardiovascular Institute, University of Ferrara, Ferrara, Italy.
⁶ Université Paris Descartes/Paris V, Paris, France.
⁷ Université Pierre et Marie Curie/Paris VI, Paris, France.
⁸ INSERM, U1138, Paris, France.
⁹ Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France.
¹⁰ Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP, Paris, France.
¹¹ Metabolomics and Cell Biology Platforms, Gustave Roussy Cancer Campus, Villejuif, France.
¹² Department of Women's and Children's Health, Karolinska University Hospital, Stockholm, Sweden.
¹³ Department of Biochemistry, Nencki Institute of Experimental Biology, Warsaw, Poland m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.
¹⁴ Université Paris Descartes/Paris V, Paris, France m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.
¹⁵ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
¹⁶ Department of Morphology, Surgery and Experimental Medicine, Section of General Pathology, University of Ferrara, Ferrara, Italy m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.

PMID: 28566520
PMCID: PMC5494524
DOI: 10.15252/embr.201643602

Mitochondrial permeability transition involves dissociation of F₁F_O ATP synthase dimers and C-ring conformation

Massimo Bonora et al. EMBO Rep. 2017 Jul.

. 2017 Jul;18(7):1077-1089.

doi: 10.15252/embr.201643602. Epub 2017 May 31.

Authors

Affiliations

¹ Department of Morphology, Surgery and Experimental Medicine, Section of General Pathology, University of Ferrara, Ferrara, Italy.
² Laboratory for Technologies of Advanced Therapies (LTTA), University of Ferrara, Ferrara, Italy.
³ Department of Biochemistry, Nencki Institute of Experimental Biology, Warsaw, Poland.
⁴ Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Ferrara, Italy.
⁵ Cardiovascular Institute, University of Ferrara, Ferrara, Italy.
⁶ Université Paris Descartes/Paris V, Paris, France.
⁷ Université Pierre et Marie Curie/Paris VI, Paris, France.
⁸ INSERM, U1138, Paris, France.
⁹ Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France.
¹⁰ Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP, Paris, France.
¹¹ Metabolomics and Cell Biology Platforms, Gustave Roussy Cancer Campus, Villejuif, France.
¹² Department of Women's and Children's Health, Karolinska University Hospital, Stockholm, Sweden.
¹³ Department of Biochemistry, Nencki Institute of Experimental Biology, Warsaw, Poland m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.
¹⁴ Université Paris Descartes/Paris V, Paris, France m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.
¹⁵ Department of Radiation Oncology, Weill Cornell Medical College, New York, NY, USA.
¹⁶ Department of Morphology, Surgery and Experimental Medicine, Section of General Pathology, University of Ferrara, Ferrara, Italy m.wieckowski@nencki.gov.pl deadoc@vodafone.it paolo.pinton@unife.it.

PMID: 28566520
PMCID: PMC5494524
DOI: 10.15252/embr.201643602

Abstract

The impact of the mitochondrial permeability transition (MPT) on cellular physiology is well characterized. In contrast, the composition and mode of action of the permeability transition pore complex (PTPC), the supramolecular entity that initiates MPT, remain to be elucidated. Specifically, the precise contribution of the mitochondrial F₁F_O ATP synthase (or subunits thereof) to MPT is a matter of debate. We demonstrate that F₁F_O ATP synthase dimers dissociate as the PTPC opens upon MPT induction. Stabilizing F₁F_O ATP synthase dimers by genetic approaches inhibits PTPC opening and MPT Specific mutations in the F₁F_O ATP synthase c subunit that alter C-ring conformation sensitize cells to MPT induction, which can be reverted by stabilizing F₁F_O ATP synthase dimers. Destabilizing F₁F_O ATP synthase dimers fails to trigger PTPC opening in the presence of mutants of the c subunit that inhibit MPT The current study does not provide direct evidence that the C-ring is the long-sought pore-forming subunit of the PTPC, but reveals that PTPC opening requires the dissociation of F₁F_O ATP synthase dimers and involves the C-ring.

Keywords: CYPD; ATP synthasome; ATP5G1; cyclosporine A; regulated necrosis.

PubMed Disclaimer

Figures

**Figure 1. MPT is associated with dissociation of F₁F_O ATP synthase dimers**
A–C
Representative traces of mouse liver mitochondria undergoing MPT in response to 100 μM CaCl₂ alone or in the presence of 1 μM cyclosporine A (CsA) (A). Representative in‐gel activity assay after blue‐native PAGE (B) and quantification (C) of F₁F_O ATP synthase dimers (D) and monomers (M) in mouse liver mitochondria in basal conditions or after MPT induction as in panel (F). *P = 0.0001, **P = 0.0011 (ANOVA plus unpaired Student's t‐test). Results are representative of five independent experiments.
D–F
Representative calcein/Co²⁺ quenching traces in HEK293T cells treated with 1 μM ionomycin (Iono), alone or in the presence of 1.6 μM CsA (D). Representative images (E) and quantification (F; n = 3) of PLA assays for F₁F_O ATP synthase dimers in HEK293T cells maintained in basal conditions or driven in MPT as in panel (D). *P = 0.0106, **P = 0.0137 (ANOVA plus unpaired Student's t‐test). Results are representative of three independent experiments.
Data information: All results are expressed as mean ± SEM. Scale bar = 10 μm. Source data are available online for this figure.

**Figure EV1. Validation of F₁F_O ATP synthase dimerization status**
A
High‐resolution image of F₁F_O ATP synthase dimers and monomers isolated from rat heart mitochondria (HM) by the use of n‐dodecyl β‐D‐maltoside (DM) or digitonin (DIG), upon separation by blue‐native PAGE and immunostaining for ATP5A.
B
Schematic representation of PLA assay setting in physiological conditions (left) or in the course of MPT (right).
C
Immunoreactivity of the ATP5H‐specific antibody used in the PLA assay as compared to an antibody specific for the mitochondrial marker TOMM20.
D
Maximum intensity projection of z‐stack from a representative HEK293T cell stained for the (immuno)fluorescence microscopy‐based detection of DNA (DAPI, blue), mitochondria (TOMM20, red), and F₁F_O ATP synthase dimers (PLA, green). Quantification of the PLA signal colocalizing with TOMM20 is reported (whiskers: max and min; box: 10^th and 90^th percentile; line: median).
E
Assessment of transfection efficiency in HEK293T cells transfected with a control siRNA (siCTR) or a siRNA targeting ATP5H (siATP5H) for 96 h. GAPDH levels were monitored to ensure equal lane loading.
F, G
Representative images (F) and quantification (G) of PLA assays for F₁F_O ATP synthase dimers in HEK293T cells transfected with siCTR or siATP5H for 96 h. The results are representative of three independent experiments. *P = 0.0001 (unpaired Student's t‐test).
H, I
Representative images (H) and quantification (I) of PLA assays for F₁F_O ATP synthase dimers in ρ⁰ cells and their wt counterpart HPA11. The results are representative of three independent experiments. ****P = 0.0001 (unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM. Scale bar = 10 μm.

**Figure 2. Stabilization of F₁F_O ATP synthase dimers by ATPIF1 inhibits MPT**
A
Assessment of transfection efficiency in HEK293T cells transfected with a control siRNA (siCTR) or a siRNA targeting ATPIF1 (siATPIF1) for 96 h. GAPDH levels were monitored to ensure equal lane loading.
B, C
Representative calcein/Co²⁺ quenching traces (B) and quenching rate quantification (C) in HEK293T cells transfected with siCTR or siATPIF1 for 96 h, and then treated with 1 μM ionomycin (Iono). Results are representative of three independent experiments. *P = 0.0135 (unpaired Student's t‐test).
D
Representative colocalization of ATPIF1 with TOMM20 in HEK293T cells transfected with a plasmid for ATPIF1 overexpression.
E, F
Representative images (E) and quantification (F) of PLA assays for F₁F_O ATP synthase dimers in HEK293T cells co‐transfected with a plasmid coding for mtGFP and with pcDNA3 or a plasmid for the overexpression of ATPIF1. Results are representative of five independent experiments. *P = 0.0001 (unpaired Student's t‐test).
G, H
Representative calcein/Co²⁺ quenching traces (G) and quenching rate quantification (H) in HEK293T cells transfected as in (E, F) and treated with 1 μM Iono. Results are representative of five independent experiments. *P = 0.0001 (unpaired Student's t‐test).
I, J
Representative mitochondrial transmembrane potential (Δψ_m) recordings (I) and depolarization rate quantification (J; n = 3) in HEK293T cells transiently as in (E, F) and exposed to 500 μM H₂O₂. 1 μM carbonyl cyanide p‐trifluoromethoxyphenylhydrazone (FCCP) was employed as control for depolarization. Results are representative of five independent experiments. *P = 0.0001 (unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM. Scale bars = 10 μm.Source data are available online for this figure.

**Figure EV2. Mitochondrial parameters in ATPIF1‐overexpressing HEK293T cells**
A–D
Representative rendering (A) and quantification of morphological parameters (count, B; average volume, C; total volume, D) in HEK293T cells transiently transfected with pcDNA3 or with a plasmid for the overexpression of ATPIF1. The results are representative of three independent experiments. Scale bar = 10 μm.
E, F
Representative images (E) and quantification (F) of TMRM staining in HEK293T cells transiently transfected with pcDNA3 or with a plasmid for the overexpression of ATPIF1. The results are representative of five independent experiments. *P = 0.0001 (unpaired Student's t‐test). Scale bar = 10 μm.
G, H
Representative traces (G) and quantification (H) of mitochondrial ATP‐dependent light emission in HEK293T cells transiently transfected with pcDNA3 or with a plasmid for the overexpression of ATPIF1. 75 μM *N,N*‐dicyclohexylcarbodiimide (DCCD) was employed to completely inhibit mitochondrial ATP synthesis. The results are representative of five independent experiments.
I, J
Representative traces (I) and quantification (J) of mtAlphi/ECFP ratio in HEK293T cells transiently co‐transfected with pcDNA3 or with a plasmid for the overexpression of ATPIF1. 30 mM Na acetate or 30 mM NH₄Cl was employed to detect the minimum and maximum ratio, respectively. The results are representative of four independent experiments.
K, L
Representative immunoblotting for the detection of the ATP5A1 subunit after blue‐native PAGE (K) and quantification (L) of F₁F_O ATP synthase dimers (D) and monomers (M) in HEK293T cells transiently transfected with pcDNA3 or with a plasmid for the overexpression of ATPIF1. The results are representative of three independent experiments. *P = 0.0095 (unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM.

**Figure 3. Modulation of F₁F_O ATP synthase dimers via ATP5I impacts on MPT**
A
Assessment of transfection efficiency in HEK293T cells transfected with a control siRNA (siCTR) or a siRNA targeting ATP5I (siATP5I) for 96 h. GAPDH levels were monitored to ensure equal lane loading.
B, C
Representative calcein/Co²⁺ quenching traces (B) and quenching rate quantification (C) in HEK293T cells transfected with siCTR or siATP5I for 96 h, and then treated with 1 μM ionomycin (Iono). Results are representative of five independent experiments. *P = 0.0001 (unpaired Student's t‐test).
D
Representative colocalization of ATP5I or ATP5I^G26L with TOMM20 in HEK293T cells transfected with constructs for ATP5I or ATP5I^G26L overexpression, respectively.
E, F
Representative images (E) and quantification (F) of PLA assays for F₁F_O ATP synthase dimers in HEK293T cells co‐transfected with a plasmid coding for mtGFP and with constructs for the overexpression of ATP5I or ATP5I^G26L. Results are representative of three independent experiments. *P = 0.0001 (unpaired Student's t‐test).
G, H
Representative calcein/Co²⁺ quenching traces (G) and quenching rate quantification (H) in HEK293T cells co‐transfected with an ATP5G1‐encoding construct and pcDNA or with plasmids for the overexpression of ATP5I or ATP5I^G26L and treated with 1 μM Iono. Results are representative of five independent experiments. *P = 0.0007, **P = 0.0007 (ANOVA plus unpaired Student's t‐test).
I, J
Representative mitochondrial transmembrane potential (Δψ_m) recordings (I) and depolarization rate quantification (J) in HEK293T cells transfected as in (G, H) and exposed to 500 μM H₂O₂. 1 μM carbonyl cyanide p‐trifluoromethoxyphenylhydrazone (FCCP) was added as control for depolarization. Results are representative of 3–5 independent experiments. *P = 0.0001, **P = 0.0191 (ANOVA plus unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM. Scale bars = 10 μm.Source data are available online for this figure.

**Figure EV3. Dimerization status during ATP5I overexpression**
A, B
Representative immunoblotting for the detection of the ATP5A1 subunit after blue‐native PAGE (A) and quantification (B) of F₁F_O ATP synthase dimers (D) and monomers (M) in HEK293T cells transiently transfected with pcDNA3 or with a plasmid for the overexpression of ATP5G1. The results are representative of three independent experiments and expressed as mean ± SEM.

**Figure EV4. Mitochondrial parameters in ATP5G1‐ and ATP5I‐co‐overexpressing HEK293T cells**
A–D
Representative rendering (A) and quantification of morphological parameters (count, B; average volume, C; total volume, D) in HEK293T cells transiently transfected with a construct for the overexpression of ATP5G1 plus pcDNA3 or a plasmid for the overexpression of ATP5I or ATP5I^G26L. The results are representative of three independent experiments. Scale bar = 10 μm.
E, F
Representative images (E) and quantification (F) of TMRM staining in HEK293T cells transiently transfected with a construct for the overexpression of ATP5G1 plus pcDNA3 or a plasmid for the overexpression of ATP5I or ATP5I^G26L. The results are representative of three independent experiments. *P = 0.0060, **P = 0.0345 (Kruskal–Wallis test with Dunn's correction for multiple comparison). Scale bar = 10 μm.
G, H
Representative traces (G) and quantification (H) of mitochondrial ATP‐dependent light emission in HEK293T cells transiently transfected with a construct for the overexpression of ATP5G1 plus pcDNA3 or a plasmid for the overexpression of ATP5I or ATP5I^G26L. 75 μM DCCD was employed to completely inhibit mitochondrial ATP synthesis at the end of the assay. The results are representative of three independent experiments.
Data information: All results are expressed as mean ± SEM.

**Figure 4. C‐ring conformation affects PTPC opening and consequent MPT**
A
Bioinformatic prediction of the alterations imposed by the G83S and the 4GL mutations on ATP5G1 structure.
B
Representative colocalization of ATP5G1, ATP5G1^G83S or ATP5G1^4GL with TOMM20 in HEK293T cells transfected with constructs for ATP5G1, ATP5G1^G83S or ATP5G1^4GL overexpression, respectively. Scale bar = 10 μm.
C, D
Representative images (C) and quantification (D) of PLA assays for F₁F_O ATP synthase dimers in HEK293T cells co‐transfected with a plasmid coding for mtGFP and constructs for the overexpression of ATP5G1, ATP5G1^G83S or ATP5G1^4GL. Results are representative of three independent experiments. Scale bar = 10 μm.
E, F
Representative calcein/Co²⁺ quenching recordings (E) and quenching rate quantification (F) in HEK293T cells transfected as in (C, D) and then treated with 1 μM ionomycin (Iono). Results are representative of three independent experiments. *P = 0.0352, **P = 0.0453 (ANOVA plus unpaired Student's t‐test).
G, H
Representative mitochondrial transmembrane potential (Δψ_m) readings (G) and depolarization rate quantification (H) in HEK293T cells transfected as in (C, D) and then exposed to 500 μM H₂O₂. 1 μM carbonyl cyanide p‐trifluoromethoxyphenylhydrazone (FCCP) was employed at the end of the assay as a positive control for depolarization. Results are representative of five independent experiments. *P = 0.0006, **P = 0.0270 (ANOVA plus unpaired Student's t‐test).
I, J
Representative calcein/Co²⁺ quenching traces (I) and quenching rate quantification (J) in HEK293T cells pre‐treated with 1.6 μM cyclosporine A (CsA), 10 μM oligomycin, 15 μM *N,N*‐dicyclohexylcarbodiimide (DCCD) or 10 μM venturicidin, and then exposed to 1 μM Iono. The results are representative of three independent experiments. *P = 0.0001, **P = 0.0033 (ANOVA plus unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM.

Figure 5. Critical role of C‐rings in MPT *in cellula* and *ex vivo*
A, B
Representative calcein/Co²⁺ quenching recordings (A) and quenching rate quantification (B) in HEK293T cells transfected with an empty plasmid or with a construct for the overexpression of ATPIF1, combined with an ATP5G1‐ or an ATP5G1^4GL‐encoding plasmid, and exposed to 1 μM ionomycin (Iono). Results are representative of three independent experiments. *P = 0.0030, **P = 0.0035, ***P = 0.0078 (ANOVA plus unpaired Student's t‐test).
C, D
Representative calcein/Co²⁺ quenching recordings (C) and quenching rate quantification (D) in HEK293T cells transfected with a control siRNA (siCTR) or with a siRNA specific for ATP5I (siATP5I), combined with an ATP5G1‐ or an ATP5G1^G83S‐encoding plasmid, and then treated with 1 μM Iono. Results are representative of three independent experiments. *P = 0.0001, **P = 0.00001, ***P = 0.0235 (ANOVA plus unpaired Student's t‐test).
E
Design of the experimental approach to study cardiac ischemia/reperfusion damage *ex vixo*. P, pressure readings. T, TUNEL assay.
F
Quantification of LVEDP in rat hearts subjected to ischemia *ex vivo* and then reperfused with vehicle only (black), or with vehicle supplemented with 0.2 μM cyclosporine A (CsA; green) or 0.2 μM *N,N*‐dicyclohexylcarbodiimide (DCCD; blue), as detailed in panel (E). Results are representative of four independent experiments and expressed as individual readings. *P = 0.0001, **P = 0.0032 (ANOVA plus unpaired Student's t‐test).
G, H
Representative images (G) and quantification (H) of TUNEL assays in rat hearts subjected to ischemia *ex vivo* and then reperfused with vehicle only, or with vehicle supplemented with 0.2 μM CsA or 0.2 μM DCCD, as detailed in panel (E). TO‐PRO^®‐3 was employed as a nuclear counterstain. Results are representative of three independent experiments. *P = 0.0054, **P = 0.0006 (ANOVA plus unpaired Student's t‐test).
Data information: All results are expressed as mean ± SEM. Scale bar = 100 μm.

See this image and copyright information in PMC

Comment in

ATP synthase complex and the mitochondrial permeability transition pore: poles of attraction.
Chinopoulos C. Chinopoulos C. EMBO Rep. 2017 Jul;18(7):1041-1042. doi: 10.15252/embr.201744412. Epub 2017 Jun 19. EMBO Rep. 2017. PMID: 28630136 Free PMC article.

Cited by

Peptides Targeting the IF1-ATP Synthase Complex Modulate the Permeability Transition Pore in Cancer HeLa Cells.
Grandi M, Fabbian S, Solaini G, Baracca A, Bellanda M, Giorgio V. Grandi M, et al. Int J Mol Sci. 2024 Apr 25;25(9):4655. doi: 10.3390/ijms25094655. Int J Mol Sci. 2024. PMID: 38731874 Free PMC article.
Mitochondrial Calcium Uniporter (MCU) is Involved in an Ischemic Postconditioning Effect Against Ischemic Reperfusion Brain Injury in Mice.
Sasaki H, Nakagawa I, Furuta T, Yokoyama S, Morisaki Y, Saito Y, Nakase H. Sasaki H, et al. Cell Mol Neurobiol. 2024 Apr 3;44(1):32. doi: 10.1007/s10571-024-01464-7. Cell Mol Neurobiol. 2024. PMID: 38568450 Free PMC article.
Mitochondria: A Promising Convergent Target for the Treatment of Amyotrophic Lateral Sclerosis.
Cunha-Oliveira T, Montezinho L, Simões RF, Carvalho M, Ferreiro E, Silva FSG. Cunha-Oliveira T, et al. Cells. 2024 Jan 29;13(3):248. doi: 10.3390/cells13030248. Cells. 2024. PMID: 38334639 Free PMC article. Review.
Pharmaceutical Manipulation of Mitochondrial F0F1-ATP Synthase Enables Imaging and Protection of Myocardial Ischemia/Reperfusion Injury Through Stress-induced Selective Enrichment.
Chen Z, Tan X, Jin T, Wang Y, Dai L, Shen G, Zhang C, Qu L, Long L, Shen C, Cao X, Wang J, Li H, Yue X, Shi C. Chen Z, et al. Adv Sci (Weinh). 2024 Mar;11(9):e2307880. doi: 10.1002/advs.202307880. Epub 2023 Dec 14. Adv Sci (Weinh). 2024. PMID: 38093654 Free PMC article.
The mitochondrial ATP synthase is a negative regulator of the mitochondrial permeability transition pore.
Pekson R, Liang FG, Axelrod JL, Lee J, Qin D, Wittig AJH, Paulino VM, Zheng M, Peixoto PM, Kitsis RN. Pekson R, et al. Proc Natl Acad Sci U S A. 2023 Dec 19;120(51):e2303713120. doi: 10.1073/pnas.2303713120. Epub 2023 Dec 13. Proc Natl Acad Sci U S A. 2023. PMID: 38091291 Free PMC article.

See all "Cited by" articles

References

1. Bonora M, Wieckowski MR, Chinopoulos C, Kepp O, Kroemer G, Galluzzi L, Pinton P (2015) Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition. Oncogene 34: 1475–1486 - PubMed
1. Galluzzi L, Bravo‐San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, Alnemri ES, Altucci L, Andrews D, Annicchiarico‐Petruzzelli M et al (2015) Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 22: 58–73 - PMC - PubMed
1. Sharpe JC, Arnoult D, Youle RJ (2004) Control of mitochondrial permeability by Bcl‐2 family members. Biochim Biophys Acta 1644: 107–113 - PubMed
1. Izzo V, Bravo‐San Pedro JM, Sica V, Kroemer G, Galluzzi L (2016) Mitochondrial permeability transition: new findings and persisting uncertainties. Trends Cell Biol 26: 655–667 - PubMed
1. Morciano G, Giorgi C, Bonora M, Punzetti S, Pavasini R, Wieckowski MR, Campo G, Pinton P (2015) Molecular identity of the mitochondrial permeability transition pore and its role in ischemia‐reperfusion injury. J Mol Cell Cardiol 78: 142–153 - PubMed

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions
Actions
Actions
Actions

LinkOut - more resources

Full Text Sources
Other Literature Sources
- The Lens - Patent Citations
- scite Smart Citations

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Mitochondrial permeability transition involves dissociation of F₁F_O ATP synthase dimers and C-ring conformation

Affiliations

Mitochondrial permeability transition involves dissociation of F₁F_O ATP synthase dimers and C-ring conformation

Authors

Affiliations

Abstract

Figures

Comment in

Similar articles

Cited by

References

Publication types

MeSH terms

Substances

LinkOut - more resources

Full Text Sources

Other Literature Sources

Abstract

Figures

Comment in

Similar articles

Cited by

References

Publication types

MeSH terms

Substances

Related information

LinkOut - more resources

Full Text Sources

Other Literature Sources