Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III.

Mitochondria are central to the efficient provision of energy for eukaryotic cells. The oxidative-phosphorylation system of mitochondria consists of a series of five major membrane complexes: NADH-ubiquinone oxidoreductase (commonly known as complex I), succinate-ubiquinone oxidoreductase (complex II), ubiquinol-cytochrome c oxidoreductase (cytochrome bc1 complex or complex III), cytochrome c-O2 oxidoreductase (complex IV), and F1F0-ATP synthase (complex V). Several lines of evidence have recently suggested that complexes I and III-V might interact to form supercomplexes. However, because of their fragility, the structures of these supercomplexes are still unknown. A stable supercomplex consisting of complex I and dimeric complex III was purified from plant mitochondria. Structural characterization by single-particle EM indicates a specific type of interaction between monomeric complex I and dimeric complex III in a 1:1 ratio. We present a model for how complexes I and III are spatially organized within the I+III2 supercomplex.

[1]  N. Dencher,et al.  “Respirasome”-like Supercomplexes in Green Leaf Mitochondria of Spinach* , 2004, Journal of Biological Chemistry.

[2]  M. L. Genova,et al.  The Mitochondrial Respiratory Chain Is Partially Organized in a Supercomplex Assembly , 2004, Journal of Biological Chemistry.

[3]  S. D’haene,et al.  Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. , 2004, Biochemistry.

[4]  A. Brennicke,et al.  Gamma carbonic anhydrases in plant mitochondria , 2004, Plant Molecular Biology.

[5]  H. Braun,et al.  Identification and Characterization of Respirasomes in Potato Mitochondria1 , 2004, Plant Physiology.

[6]  C. Bruno,et al.  Respiratory complex III is required to maintain complex I in mammalian mitochondria. , 2004, Molecular cell.

[7]  J. Smeitink,et al.  Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. , 2004, Human molecular genetics.

[8]  M. Finel,et al.  Assembly of Respiratory Complexes I, III, and IV into NADH Oxidase Supercomplex Stabilizes Complex I in Paracoccus denitrificans* , 2004, Journal of Biological Chemistry.

[9]  B. Böttcher,et al.  The gross structure of the respiratory complex I: a Lego System. , 2004, Biochimica et biophysica acta.

[10]  B. Lemire,et al.  Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis. , 2003, Human molecular genetics.

[11]  Kathy Pfeiffer,et al.  Cardiolipin Stabilizes Respiratory Chain Supercomplexes* , 2003, Journal of Biological Chemistry.

[12]  A. Millar,et al.  Control of Ascorbate Synthesis by Respiration and Its Implications for Stress Responses1 , 2003, Plant Physiology.

[13]  Hans-Peter Braun,et al.  New Insights into the Respiratory Chain of Plant Mitochondria. Supercomplexes and a Unique Composition of Complex II1 , 2003, Plant Physiology.

[14]  M. Bott,et al.  Purification of a cytochrome bc-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunity of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. , 2003, The Journal of biological chemistry.

[15]  E. Boekema,et al.  Plants lacking the main light-harvesting complex retain photosystem II macro-organization , 2003, Nature.

[16]  T. Yagi,et al.  The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. , 2003, Biochemistry.

[17]  William Dowhan,et al.  Gluing the Respiratory Chain Together , 2002, The Journal of Biological Chemistry.

[18]  J. di Rago,et al.  The ATP synthase is involved in generating mitochondrial cristae morphology , 2002, The EMBO journal.

[19]  K. Pfeiffer,et al.  The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. , 2001, The Journal of biological chemistry.

[20]  F. Rébeillé,et al.  The glycine decarboxylase system: a fascinating complex. , 2001, Trends in plant science.

[21]  M. Heel,et al.  Single-particle electron cryo-microscopy: towards atomic resolution , 2000, Quarterly Reviews of Biophysics.

[22]  A. Crofts,et al.  Structure and function of cytochrome bc complexes. , 2000, Annual review of biochemistry.

[23]  K. Pfeiffer,et al.  Supercomplexes in the respiratory chains of yeast and mammalian mitochondria , 2000, The EMBO journal.

[24]  W Chiu,et al.  EMAN: semiautomated software for high-resolution single-particle reconstructions. , 1999, Journal of structural biology.

[25]  Torreão As,et al.  Single-unit implant-supported restoration in the vertically deficient anterior maxilla. , 1999 .

[26]  K. Pfeiffer,et al.  Yeast mitochondrial F1F0‐ATP synthase exists as a dimer: identification of three dimer‐specific subunits , 1998, The EMBO journal.

[27]  T. A. Link,et al.  Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. , 1998, Science.

[28]  N Grigorieff,et al.  Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 A in ice. , 1998, Journal of molecular biology.

[29]  L. Grivell,et al.  The Respiratory Chain in Yeast Behaves as a Single Functional Unit* , 1998, The Journal of Biological Chemistry.

[30]  K. Leonard,et al.  Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). , 1998, Journal of molecular biology.

[31]  T. Oshima,et al.  Resolution of the Aerobic Respiratory System of the Thermoacidophilic Archaeon, Sulfolobus sp. Strain 7: , 1995, The Journal of Biological Chemistry.

[32]  H. Braun,et al.  Are the 'core' proteins of the mitochondrial bc1 complex evolutionary relics of a processing protease? , 1995, Trends in biochemical sciences.

[33]  H. Braun,et al.  Affinity purification of cytochrome c reductase from potato mitochondria. , 1992, European journal of biochemistry.

[34]  H. Braun,et al.  The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. , 1992, The EMBO journal.

[35]  J Frank,et al.  Three-dimensional reconstruction of single particles embedded in ice. , 1992, Ultramicroscopy.

[36]  E. Kutoh,et al.  Identification and properties of a quinol oxidase super-complex composed of a bc1 complex and cytochrome oxidase in the thermophilic bacterium PS3. , 1987, The Journal of biological chemistry.

[37]  Marin van Heel,et al.  Similarity measures between images , 1987 .

[38]  B. Trumpower,et al.  Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa3 complexes. , 1985, The Journal of biological chemistry.

[39]  Y. Hatefi.  The mitochondrial electron transport and oxidative phosphorylation system. , 1985, Annual review of biochemistry.

[40]  H. Weiss,et al.  Isolation of a multiprotein complex containing cytochrome b and c1 from Neurospora crassa mitochondria by affinity chromatography on immobilized cytochrome c. Difference in the binding between ferricytochrome c and ferrocytochrome c to the multiprotein complex. , 1978, European journal of biochemistry.