Small single transmembrane domain (STMD) proteins organize the hydrophobic subunits of large membrane protein complexes

FEBS Letters

Volumn 584, Issue 12, 2010, Pages 2516-2525

  Zickermann, Volker ^a   Angerer, Heike ^a   Ding, Martina G ^a   Nübel, Esther ^a   Brandt, Ulrich ^a  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

Author keywords

Accessory subunit; Assembly; Membrane protein; Mitochondria; Oxidative phosphorylation; Photosystem

Indexed keywords

CYTOCHROME C OXIDASE; MEMBRANE PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

AMINO ACID SEQUENCE; BIOENERGY; GENETIC CONSERVATION; HYDROPHOBICITY; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STABILITY; REVIEW; SACCHAROMYCES CEREVISIAE; YARROWIA LIPOLYTICA;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; FUNGAL PROTEINS; HYDROPHOBICITY; MEMBRANE PROTEINS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; OXIDATIVE PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; STRUCTURAL HOMOLOGY, PROTEIN; YARROWIA;

EID: 77953136730     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.021     Document Type: Review

References (78)

1. Kerscher S., Dröse S., Zwicker K., Zickermann V., Brandt U. Yarrowia lipolytica, a yeast genetic system to study mitochondrial complex I. Biochim. Biophys. Acta 2002, 1555:83-91.
2. Kerscher S. Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim. Biophys. Acta 2000, 1459:274-283.
3. Kerscher S., Dröse S., Zickermann V., Brandt U. The three families of respiratory NADH dehydrogenases. Results Problems Cell Different. 2008, 45:185-222.
4. Morgner N., Zickermann V., Kerscher S., Wittig I., Abdrakhmanova A., Barth H.D., Brutschy B., Brandt U. Subunit mass fingerprinting of mitochondrial complex I. Biochim. Biophys. Acta 2008, 1777:1384-1391.
5. Abdrakhmanova A., Zickermann V., Bostina M., Radermacher M., Schägger H., Kerscher S., Brandt U. Subunit composition of mitochondrial complex I from the yeast Yarrowia lipolytica. Biochim. Biophys. Acta 2004, 1658:148-156.
6. Carroll J., Fearnley I.M., Skehel J.M., Shannon R.J., Hirst J., Walker J.E. Bovine complex I is a complex of 45 different subunits. J. Biol. Chem. 2006, 281:32724-32727.
7. Brandt U., Uribe S., Schägger H., Trumpower B.L. Isolation and characterization of QCR10, the nuclear gene encoding the 8.5-kDa subunit 10 of the Saccharomyces cerevisiae cytochrome bc1 complex. J. Biol. Chem. 1994, 269:12947-12953.
8. Wittig I., Schägger H. Structural organization of mitochondrial ATP synthase. Biochim. Biophys. Acta 2008, 1777:592-598.
9. Geier B.M., Schägger H., Ortwein C., Link T.A., Hagen W.R., Brandt U., von Jagow G. Kinetic properties and ligand binding of the eleven-subunit cytochrome-c oxidase from Saccharomyces cerevisiae isolated with a novel large-scale purification method. Eur. J. Biochem. 1995, 227:296-302.
10. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 1996, 272:1136-1144.
11. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 2006, 75:69-92.
12. Napiwotzki J., Shinzawa-Itoh K., Yoshikawa S., Kadenbach B. ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem. 1997, 378:1013-1021.
13. Ludwig B., Bender E., Arnold S., Huttemann M., Lee I., Kadenbach B. Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem 2001, 2:392-403.
14. Arnold S., Goglia F., Kadenbach B. 3, 5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 1998, 252:325-330.
15. Allen L.A., Zhao X.J., Caughey W.S., Poyton R.O. Isoforms of yeast cytochrome c oxidase subunit V affect the binuclear reaction center and alter the kinetics of interaction with the isoforms of yeast cytochrome c. J. Biol. Chem. 1995, 270:110-118.
16. Cronan J.E., Fearnley I.M., Walker J.E. Mammalian mitochondria contain a soluble acyl carrier protein. FEBS Lett. 2005, 579:4892-4896.
17. Dobrynin K., Abdrakhmanova A., Richers S., Hunte C., Kerscher S., Brandt U. Characterization of two different acyl carrier proteins in complex I from Yarrowia lipolytica. Biochim. Biophys. Acta 2010, 1797:152-159.
18. Gueguen V., Macherel D., Jaquinod M., Douce R., Bourguignon J. Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J. Biol. Chem. 2000, 275:5016-5025.
19. Jordan S.W., Cronan J.E. A new metabolic link. The acyl carrier protein of lipid synthesis donates lipoic acid to the pyruvate dehydrogenase complex in Escherichia coli and mitochondria. J. Biol. Chem. 1997, 272:17903-17906.
20. Braun H.P., Zabaleta E. Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiol. Plant. 2007, 129:114-122.
21. Zara V., Conte L., Trumpower B.L. Biogenesis of the yeast cytochrome bc1 complex. Biochim. Biophys. Acta 2009, 1793:89-96.
22. Hunte C., Koepke J., Lange C., Michel H. Structure at 2.3 Ångstrom resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure 2000, 8:669-684.
23. Fontanesi F., Soto I.C., Horn D., Barrientos A. Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am. J. Physiol. Cell Physiol. 2006, 291:C1129-C1147.
24. Au H.C., Seo B.B., Matsuno-Yagi A., Yagi T., Scheffler I.E. The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria. Proc. Natl. Acad. Sci. USA 1999, 96:4354-4359.
25. Potluri P., Yadava N., Scheffler I.E. The role of the ESSS protein in the assembly of a functional and stable mammalian mitochondrial complex I (NADH-ubiquinone oxidoreductase). Eur. J. Biochem. 2004, 271:3265-3273.
26. Marques I., Duarte M., Assuncao J., Ushakova A.V., Videira A. Composition of complex I from Neurospora crassa and disruption of two " accessory" subunits. Biochim. Biophys. Acta 2005, 1707:211-220.
27. Chen R.M., Fearnley I.M., Peak-Chew S.Y., Walker J.E. The phosphorylation of subunits of complex I from bovine heart mitochondria. J. Biol. Chem. 2004, 279:26036-26045.
28. Yadava N., Potluri P., Scheffler I.E. Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly. Int. J Biochem. Cell Biol. 2008, 40:447-460.
29. Brandt U., Abdrakhmanova A., Zickermann V., Galkin A., Dröse S., Zwicker K., Kerscher S. Structure-function relationships in mitochondrial complex I of the strictly aerobic yeast Yarrowia lipolytica. Biochem. Soc. Trans. 2005, 33:840-844.
30. Iwata S., Lee J.W., Okada K., Lee J.K., Iwata M., Rasmussen B., Link T.A., Ramaswamy S., Jap B.K. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 1998, 281:64-71.
31. Tusnady G.E., Simon I. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 1998, 283:489-506.
32. McCaldon P., Argos P. Oligopeptide biases in protein sequences and their use in predicting protein coding regions in nucleotide-sequences. Proteins Struct. Funct. Genetics 1988, 4:99-122.
33. Fearnley I.M., Walker J.E. Two overlapping genes in bovine mitochondrial-DNA encode membrane-components of ATP Synthase. EMBO J. 1986, 5:2003-2008.
34. Velours J., Guerin B. Localization of the hydrophilic C-terminal part of the ATP synthase subunit 8 of Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 1986, 138:78-86.
35. von Heijne G. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature 1990, 341:456-458.
36. Tso S.C., Shenoy S.K., Quinn B.N., Yu L. Subunit IV of cytochrome bc1 complex from Rhodobacter sphaeroides. Localization of regions essential for interaction with the three-subunit core complex. J. Biol. Chem. 2000, 275:15287-15294.
37. Tso S.C., Yin Y., Yu C.A., Yu L. Identification of amino acid residues essential for reconstitutive activity of subunit IV of the cytochrome bc1 complex from Rhodobacter sphaeroides. Biochim. Biophys. Acta 2006, 1757:1561-1567.
38. Yin Y., Tso S.C., Yu C.A., Yu L. Effect of subunit IV on superoxide generation by Rhodobacter sphaeroides cytochrome bc1 complex. Biochim. Biophys. Acta 2009, 1787:913-919.
39. Shi L.X., Schroder W.P. The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta 2004, 1608:75-96.
40. Baena-Gonzalez E., Aro E.M. Biogenesis, assembly and turnover of photosystem II units. Philos. Trans. R Soc. Lond. B Biol. Sci. 2002, 357:1451-1459.
41. Mandon E.C., Trueman S.F., Gilmore R. Translocation of proteins through the Sec61 and SecYEG channels. Curr. Opin. Cell Biol. 2009, 21:501-507.
42. Dempski R.E., Imperiali B. Oligosaccharyl transferase: gatekeeper to the secretory pathway. Curr. Opin. Chem. Biol. 2002, 6:844-850.
43. Kim H., Yan Q., von Heijne G., Caputo G.A., Lennarz W.J. Determination of the membrane topology of Ost4p and its subunit interactions in the oligosaccharyl-transferase complex in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2003, 100:7460-7464.
44. Lazarou M., Thorburn D.R., Ryan M.T., McKenzie M. Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta 2009, 1793:78-88.
45. Vogel R.O., Smeitink J.A., Nijtmans L.G. Human mitochondrial complex I assembly: a dynamic and versatile process. Biochim. Biophys. Acta 2007, 1767:1215-1227.
46. Küffner R., Rohr A., Schmiede A., Krüll C., Schulte U. Involvement of two novel chaperones in the assembly of mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Mol. Biol. 1998, 283:409-417.
47. Chothia C., Levitt M., Richardson D. Structure of proteins: packing of α-helices and pleated sheets. Proc. Natl. Acad. Sci. USA 1977, 74:4130-4134.
48. Arnold I., Pfeiffer K., Neupert W., Stuart R.A., Schägger H. Yeast F1F0-ATPSynthase exists as a dimer: identification of three dimer specific subunits. EMBO J. 1998, 17:7170-7178.
49. Das J., Miller S.T., Stern D.L. Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome c oxidase suggests conservation of structure underlies evolving functional sites. Mol. Biol. Evol. 2004, 21:1572-1582.
50. Gross J., Bhattacharya D. Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective. Nat. Rev. Genetics 2009, 10:495-505.
51. Little A.G., Kocha K.M., Lougheed S.C., Moyes C.D. Evolution of the nuclear-encoded cytochrome oxidase subunits in vertebrates. Physiol. Genomics 2010, 10.1152/physiolgenomics.00015.2010.
52. Ardail D., Privat J.P., Egretcharlier M., Levrat C., Lerme F., Louisot P. Mitochondrial contact sites - lipid-composition and dynamics. J. Biol. Chem. 1990, 265:18797-18802.
53. Mannella C.A. The relevance of mitochondrial membrane topology to mitochondrial function. Biochim. Biophys. Acta 2006, 1762:140-147.
54. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., Brethes D., di Rago J.P., Velours J. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 2002, 21:221-230.
55. Aoyama H., Muramoto K., Shinzawa-Itoh K., Hirata K., Yamashita E., Tsukihara T., Ogura T., Yoshikawa S. A peroxide bridge between Fe and Cu ions in the O2 reduction site of fully oxidized cytochrome c oxidase could suppress the proton pump. Proc. Natl. Acad. Sci. USA 2009, 106:2165-2169.
56. Potterton L., McNicholas S., Krissinel E., Gruber J., Cowtan K., Emsley P., Murshudov G.N., Cohen S., Perrakis A., Noble M. Developments in the CCP4 molecular-graphics project. Acta Cryst. D 2004, 60:2288-2294.
57. Carroll J., Shannon R.J., Fearnley I.M., Walker J.E., Hirst J. Definition of the nuclear encoded protein composition of bovine heart mitochondrial complex I - identification of two new subunits. J. Biol. Chem. 2002, 277:50311-50317.
58. Walker J.E., Arizmendi J.M., Dupuis A., Fearnley I.M., Finel M., Medd S.M., Pilkington S.J., Runswick M.J., Skehel J.M. Sequences of 20 Subunits of NADH - ubiquinone oxidoreductase from bovine heart-mitochondria - application of a novel strategy for sequencing proteins using the polymerase chain-reaction. J. Mol. Biol. 1992, 226:1051-1072.
59. Fearnley I.M., Carroll J., Shannon R.J., Runswick M.J., Walker J.E., Hirst J. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 2001, 276:38345-38348.
60. Arizmendi J.M., Skehel J.M., Runswick M.J., Fearnley I.M., Walker J.E. Complementary DNA sequences of two 14.5 kDa subunits of NADH:ubiquinone oxidoreductase from bovine heart mitochondria. FEBS Lett. 1992, 313:80-84.
61. Schägger H., Borchart U., Aquila H., Link T.A., von Jagow G. Isolation and amino acid sequence of the smallest subunit of beef heart bc1 complex. FEBS Lett. 1985, 190:89-94.
62. Schägger H., von Jagow G., Borchart U., Machleidt W. Amino acid sequence of the smallest protein of the cytochrome c1 subcomplex from beef heart mitochondria. Hoppe-Seyler's Z Physiol. Chem. 1983, 364:307-311.
63. Phillips J.D., Schmitt M.E., Brown T.A., Beckmann J.D., Trumpower B.L. Isolation and characterization of QCR9, a nuclear gene encoding the 7.3-kDa subunit 9 of the Saccharomyces cerevisae ubiquinol-cytochrome c oxidoreductase complex - an intron-containing gene with a conserved sequence occurring in the intron of COX4. J. Biol. Chem. 1990, 265:20813-20821.
64. Borchart U., Machleidt W., Schägger H., Link T.A., von Jagow G. Isolation and amino acid sequence of the 9.5 kDa protein of beef heart ubiquinol:cytochrome c reductase. FEBS Lett. 1986, 200:81-86.
65. Hemrika W., Berden J.A., Grivell L.A. A region of the C-terminal part of the 11-kDa subunit of ubiquinol-cytochrome-c oxidoreductase of the yeast Saccharomyces cerevisiae contributes to the structure of the Qout reaction domain. Eur. J. Biochem. 1993, 215:601-609.
66. Boumans H., Berden J.A., Grivell L.A. The role of subunit VIII is the structural stability of the bc1 complex from Saccharomyces cerevisiae studied using hybrid complexes. Eur. J. Biochem. 1997, 249:762-769.
67. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyoma H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. USA 2003, 100:15304-15309.
68. Lee I., Salomon A.R., Yu K.B., Samavati L., Pecina P., Pecinova A., Huttemann M. Isolation of regulatory-competent, phosphorylated cytochrome c oxidase. Mitochondrial function, part b mitochondrial protein kinases, protein phosphatases and mitochondrial diseases. Methods Enzymol. 2009, 457:193-210.
69. Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem. J. 2007, 405:1-9.
70. Belogrudov G.I., Tomich J.M., Hatefi Y. Membrane topography and near-neighbor relationships of the mitochondrial ATP synthase subunits e, f, and g. J. Biol. Chem. 1996, 271:20340-20345.
71. Schägger H., Pfeiffer K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 2000, 19:1777-1783.
72. Hong S.J., Pedersen P.L. Mitochondrial ATP synthase: A bioinformatic approach reveals new insights about the roles of supernumerary subunits g and A6L. J. Bioenerg. Biomembr. 2004, 36:515-523.
73. Roudeau S., Spannagel C., Vaillier J., Arselin G., Graves P.V., Velours J. Subunit f of the yeast mitochondrial ATP synthase: topological and functional studies. J. Bioenerg. Biomembr. 1999, 31:85-94.
74. Grandiervazeille X., Ouhabi R., Guerin M. Antibodies against subunits of F-0 sector of ATP synthase from Saccharomyces cerevisiae - stimulation of ATP synthase by subunit-8-reactive antibodies and inhibition by subunit-9-reactive antibodies. Eur. J. Biochem. 1994, 223:521-528.
75. Macreadie I.G., Novitski C.E., Maxwell R.J., John U., Ooi B.G., Mcmullen G.L., Lukins H.B., Linnane A.W., Nagley P. Biogenesis of mitochondria - the mitochondrial gene (aapl) coding for mitochondrial ATPase subunit-8 in Saccharomyces cerevisiae. Nucleic Acids Res. 1983, 11:4435-4451.
76. Meyer B., Wittig I., Trifilieff E., Karas M., Schägger H. Identification of two proteins associated with mammalian ATP synthase. Mol. Cell Proteomics 2007, 6:1690-1699.
77. Arnold I., Pfeiffer K., Neupert W., Stuart R.A., Schägger H. ATP synthase of yeast mitochondria: isolation of subunit j and disruption of the ATP18 gene. J. Biol. Chem. 1999, 274:36-40.
78. Vaillier J., Arselin G., Graves P.V., Camougrand N., Velours J. Isolation of supernumerary yeast ATP synthase subunits e and i - Characterization of subunit i and disruption of its structural gene ATP18. J. Biol. Chem. 1999, 274:543-548.