Evidence of proteolipid domain formation in an inner mitochondrial membrane mimicking model

Mouhedine Cheniour, Jonathan R. Brewer, Luis Bagatolli, Olivier Marcillat, Thierry Granjon*

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Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

Background Mitochondrial creatine kinase (mtCK) is highly abundant in mitochondria; its quantity is equimolecular to the Adenylic Nucleotide Translocator and represents 1% of the mitochondrial proteins. It is a multitask protein localized in the mitochondria intermembrane space where it binds to the specific cardiolipin (CL) phospholipid. If mtCK was initially thought to be exclusively implicated in energy transfer between mitochondria and cytosol through a mechanism referred to as the phosphocreatine shuttle, several recent studies suggested an additional role in maintaining mitochondria membrane structure. Methods To further characterized mtCK binding process we used multiphoton excitation fluorescence microscopy coupled with Giant Unilamellar Vesicles (GUV) and laurdan as fluorescence probe. Results We gathered structural and dynamical information on the molecular events occurring during the binding of mtCK to the mitochondria inner membrane. We present the first visualization of mtCK-induced CL segregation on a bilayer model forming micrometer-size proteolipid domains at the surface of the GUV. Those microdomains, which only occurred when CL is included in the lipid mixture, were accompanied by the formation of protein multimolecular assembly, vesicle clamping, and changes in both vesicle curvature and membrane fluidity Conclusion Those results highlighted the importance of the highly abundant mtCK in the lateral organization of the mitochondrial inner membrane. General significance Microdomains were induced in mitochondria-mimicking membranes composed of natural phospholipids without cholesterol and/or sphingolipids differing from the proposed cytoplasmic membrane rafts. Those findings as well as membrane curvature modification were discussed in relation with protein-membrane interaction and protein cluster involvement in membrane morphology.

OriginalsprogEngelsk
TidsskriftBiochimica et Biophysica Acta - General Subjects
Vol/bind1861
Udgave nummer5 Part A
Sider (fra-til)969-976
ISSN0304-4165
DOI
StatusUdgivet - 2017

Fingeraftryk

Mitochondrial Form Creatine Kinase
Proteolipids
Mitochondria
Membranes
Cardiolipins
Unilamellar Liposomes
Multiphoton Fluorescence Microscopy
Phospholipids
Proteins
Membrane Fluidity
Phosphocreatine
Mitochondrial Proteins
Membrane structures
Sphingolipids
Fluidity
Fluorescence microscopy
Constriction
Cytosol
Membrane Proteins
Energy transfer

Citer dette

Cheniour, Mouhedine ; Brewer, Jonathan R. ; Bagatolli, Luis ; Marcillat, Olivier ; Granjon, Thierry. / Evidence of proteolipid domain formation in an inner mitochondrial membrane mimicking model. I: Biochimica et Biophysica Acta - General Subjects. 2017 ; Bind 1861, Nr. 5 Part A. s. 969-976.
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abstract = "Background Mitochondrial creatine kinase (mtCK) is highly abundant in mitochondria; its quantity is equimolecular to the Adenylic Nucleotide Translocator and represents 1{\%} of the mitochondrial proteins. It is a multitask protein localized in the mitochondria intermembrane space where it binds to the specific cardiolipin (CL) phospholipid. If mtCK was initially thought to be exclusively implicated in energy transfer between mitochondria and cytosol through a mechanism referred to as the phosphocreatine shuttle, several recent studies suggested an additional role in maintaining mitochondria membrane structure. Methods To further characterized mtCK binding process we used multiphoton excitation fluorescence microscopy coupled with Giant Unilamellar Vesicles (GUV) and laurdan as fluorescence probe. Results We gathered structural and dynamical information on the molecular events occurring during the binding of mtCK to the mitochondria inner membrane. We present the first visualization of mtCK-induced CL segregation on a bilayer model forming micrometer-size proteolipid domains at the surface of the GUV. Those microdomains, which only occurred when CL is included in the lipid mixture, were accompanied by the formation of protein multimolecular assembly, vesicle clamping, and changes in both vesicle curvature and membrane fluidity Conclusion Those results highlighted the importance of the highly abundant mtCK in the lateral organization of the mitochondrial inner membrane. General significance Microdomains were induced in mitochondria-mimicking membranes composed of natural phospholipids without cholesterol and/or sphingolipids differing from the proposed cytoplasmic membrane rafts. Those findings as well as membrane curvature modification were discussed in relation with protein-membrane interaction and protein cluster involvement in membrane morphology.",
keywords = "Cardiolipin, Fluorescence microscopy, GUVs, Membrane curvature, Mitochondrial creatine kinase, Protein clusters",
author = "Mouhedine Cheniour and Brewer, {Jonathan R.} and Luis Bagatolli and Olivier Marcillat and Thierry Granjon",
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Evidence of proteolipid domain formation in an inner mitochondrial membrane mimicking model. / Cheniour, Mouhedine; Brewer, Jonathan R.; Bagatolli, Luis; Marcillat, Olivier; Granjon, Thierry.

I: Biochimica et Biophysica Acta - General Subjects, Bind 1861, Nr. 5 Part A, 2017, s. 969-976.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Evidence of proteolipid domain formation in an inner mitochondrial membrane mimicking model

AU - Cheniour, Mouhedine

AU - Brewer, Jonathan R.

AU - Bagatolli, Luis

AU - Marcillat, Olivier

AU - Granjon, Thierry

PY - 2017

Y1 - 2017

N2 - Background Mitochondrial creatine kinase (mtCK) is highly abundant in mitochondria; its quantity is equimolecular to the Adenylic Nucleotide Translocator and represents 1% of the mitochondrial proteins. It is a multitask protein localized in the mitochondria intermembrane space where it binds to the specific cardiolipin (CL) phospholipid. If mtCK was initially thought to be exclusively implicated in energy transfer between mitochondria and cytosol through a mechanism referred to as the phosphocreatine shuttle, several recent studies suggested an additional role in maintaining mitochondria membrane structure. Methods To further characterized mtCK binding process we used multiphoton excitation fluorescence microscopy coupled with Giant Unilamellar Vesicles (GUV) and laurdan as fluorescence probe. Results We gathered structural and dynamical information on the molecular events occurring during the binding of mtCK to the mitochondria inner membrane. We present the first visualization of mtCK-induced CL segregation on a bilayer model forming micrometer-size proteolipid domains at the surface of the GUV. Those microdomains, which only occurred when CL is included in the lipid mixture, were accompanied by the formation of protein multimolecular assembly, vesicle clamping, and changes in both vesicle curvature and membrane fluidity Conclusion Those results highlighted the importance of the highly abundant mtCK in the lateral organization of the mitochondrial inner membrane. General significance Microdomains were induced in mitochondria-mimicking membranes composed of natural phospholipids without cholesterol and/or sphingolipids differing from the proposed cytoplasmic membrane rafts. Those findings as well as membrane curvature modification were discussed in relation with protein-membrane interaction and protein cluster involvement in membrane morphology.

AB - Background Mitochondrial creatine kinase (mtCK) is highly abundant in mitochondria; its quantity is equimolecular to the Adenylic Nucleotide Translocator and represents 1% of the mitochondrial proteins. It is a multitask protein localized in the mitochondria intermembrane space where it binds to the specific cardiolipin (CL) phospholipid. If mtCK was initially thought to be exclusively implicated in energy transfer between mitochondria and cytosol through a mechanism referred to as the phosphocreatine shuttle, several recent studies suggested an additional role in maintaining mitochondria membrane structure. Methods To further characterized mtCK binding process we used multiphoton excitation fluorescence microscopy coupled with Giant Unilamellar Vesicles (GUV) and laurdan as fluorescence probe. Results We gathered structural and dynamical information on the molecular events occurring during the binding of mtCK to the mitochondria inner membrane. We present the first visualization of mtCK-induced CL segregation on a bilayer model forming micrometer-size proteolipid domains at the surface of the GUV. Those microdomains, which only occurred when CL is included in the lipid mixture, were accompanied by the formation of protein multimolecular assembly, vesicle clamping, and changes in both vesicle curvature and membrane fluidity Conclusion Those results highlighted the importance of the highly abundant mtCK in the lateral organization of the mitochondrial inner membrane. General significance Microdomains were induced in mitochondria-mimicking membranes composed of natural phospholipids without cholesterol and/or sphingolipids differing from the proposed cytoplasmic membrane rafts. Those findings as well as membrane curvature modification were discussed in relation with protein-membrane interaction and protein cluster involvement in membrane morphology.

KW - Cardiolipin

KW - Fluorescence microscopy

KW - GUVs

KW - Membrane curvature

KW - Mitochondrial creatine kinase

KW - Protein clusters

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U2 - 10.1016/j.bbagen.2017.02.001

DO - 10.1016/j.bbagen.2017.02.001

M3 - Journal article

VL - 1861

SP - 969

EP - 976

JO - B B A - General Subjects

JF - B B A - General Subjects

SN - 0304-4165

IS - 5 Part A

ER -