Understanding structure, function, and mutations in the mitochondrial ATP synthase

Microbial Cell

Volumn 2, Issue 4, 2015, Pages 105-125

  Xu, Ting ^a   Pagadala, Vijayakanth ^b   Mueller, David M ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNC Hamner Institute for Drug Safety Sciences   (United States)

Author keywords

ATP synthase; F1 ATPase; F1Fo ATP synthase; Mitochondrial diseases; Petite mutations; Uncoupling

Indexed keywords

EID: 84994511808     PISSN: None     EISSN: 23112638     Source Type: Journal    
DOI: 10.15698/mic2015.04.197     Document Type: Review

References (204)

1. Mitchell P. (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type mechanism. Nature 191, 144-148.
2. Boyer PD, Cross RL, and Momsen W. (1973) A new concept for energy coupling in oxidative phosphorylation based on a molecular explanation of the oxygen exchange reactions. Proc Natl Acad Sci USA 70, 2837-2839.
3. Watt IN, Montgomery MG, Runswick MJ, Leslie AG, and Walker JE. (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci USA 107, 16823-16827.
4. Lee CP, Gu Q, Xiong Y, Mitchell RA, and Ernster L. (1996) P/O ratios reassessed: mitochondrial P/O ratios consistently exceed 1.5 with succinate and 2.5 with NAD-linked substrates. FASEB J 10, 345-350.
5. Hinkle PC. (2005) P/O ratios of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1706, 1-11.
6. Kerscher SJ. (2000) Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim Biophys Acta 1459, 274-283.
7. 1 ATPase. EMBO J 25,5433-5442.
8. 10 ring of the yeast mitochondrial ATP synthase in the open conformation. Nat Struct Mol Biol 19, 485-491.
9. Rees DM, Leslie AG, and Walker JE. (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci USA 106, 21597-21601.
10. Kane Dickson V, Silvester JA, Fearnley IM, Leslie AGW, and Walker JE. (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25, 2911-2918.
11. Walker JE, and Dickson VK. (2006) The peripheral stalk of the mitochondrial ATP synthase. Biochim Biophys Acta 1757, 286-296.
12. 1-ATPase from bovine heart mitochondria. Nature 370, 621-628.
13. 1-ATPase from bovine heart mitochondria. Proc Natl Acad Sci USA 109, 11139-11143.
14. 1-ATPase complexed with the peptide antibiotic efrapeptin. Proc Natl Acad Sci USA 93, 9420-9424.
15. 1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc Natl Acad Sci USA 93, 6913-6917.
16. 2+ ADP and aluminium fluoride. Structure Fold Des 8, 567-573.
17. 1-ATPase at 2.4Å resolution. Nat Struct Biol 7, 1055-1061.,
18. 1-ATPase with nucleotide bound to all three catalytic sites. implications for the mechanism of rotary catalysis. Cell 106, 331-341.
19. 1-ATPase inhibited by ADP and beryllium fluoride. EMBO J 23, 2734-2744.
20. Bowler MW, Montgomery MG, Leslie AGW, and Walker JE. (2006) How azide inhibits ATP hydrolysis by the F-ATPases. Proc Natl Acad Sci USA 103, 8646-8649.
21. 1-ATPase from bovine heart mitochondria at 1.9Å resolution. J Biol Chem 282, 14238-14242.
22. 1-ATPase by resveratrol and related polyphenols. Proc Natl Acad Sci USA 104, 13632-13637.
23. 1-ATPase: Configuration of a critical intermediate in ATP synthesis/hydrolysis. Proc Natl Acad Sci USA 95, 11065-11070.
24. 1-ATPase. Residues involved in catalysis and coupling. Ann NY Acad Sci. 671, 335-344.
25. 1-ATPase from yeast. J Biol Chem 269, 9424-9428.
26. 1-ATPase. Biophys J 85, 2253-2266.
27. Komoriya Y, Ariga T, Iino R, and Noji H. (2012) Principal role of the arginine finger in rotary catalysis of F1-ATPase. J Biol Chem 287, 15134-15142.
28. 1-ATPase. Nature 386, 299-302.
29. 1-ATPase. Nature 427, 465-468.
30. Rondelez Y, Tresset G, Nakashima T, Kato-Yamada Y, Fujita H, Takeuchi S, and Noji H. (2005) Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433, 773-777.
31. 1-ATPase. Nature 410, 898-904.,
32. ? steps. Cell 93, 1117-1124.
33. 1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat Struct Mol Biol 11, 142-148.
34. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321.
35. 1-ATPase. Scientific Reports 5, 8773.
36. 1 sector: the e subunit-sensitive rotation. J Biol Chem 281, 4126-4131.
37. 1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc Natl Acad Sci USA 96, 7780-7784.
38. 1-ATPase. Philos Trans R Soc Lond B Biol Sci 368, 20120023.
39. 1-ATPase molecules. Biochemistry 45, 3117-3124.
40. 1-ATPase powered rotation. Proc Natl Acad Sci USA 111, 3715-3720.
41. 1-ATPase motor. Nat Chem Biol 10, 930-936.
42. Choate GL, Hutton RL, and Boyer PD. (1979) Occurance and significance of oxygen exchange reactions catalyzed by mitochondrial adenosine triphosphatase preparations. J Biol Chem 254, 286-290.
43. Grubmeyer C, Cross RL, and Penefsky HS. (1982) Mechanism of ATP hydrolysis by beef heart mitochondrial ATPase. Rate constants for elementary steps in catlysis at a single site. J Biol Chem 257, 12092-12100.
44. Cross RL, Grubmeyer C, and Penefsky HS. (1982) Mechanism of ATP hydrolysis by beef heart mitochondrial ATPase. Rate enhancements resulting from cooperative interactions between multiple catalytic sites. J Biol Chem 258, 12101-12105.
45. 1-ATPase with the b-subunit Thr197--OpenSPIGreaterThanSPISer mutation. Eur J Biochem 222, 991-999.
46. 1-ATPase: how an ATP-driven molecular machine may work. Annu Rev Biophys Biomol Struct 33, 245-268.
47. 1-ATPase with 1, 2, or 3 incompetent catalytic sites. J Biol Chem 271, 18128-18133.
48. 1-ATPase with one, two, or three altered catalytic sites that bind ATP only slowly. J Biol Chem 277, 24870-24874.
49. Kagawa Y, and Racker E. (1966) Partial resolution of the enzymes catalyzing oxidative phosphorylation. 8. Properties of a factor conferring oligomycin sensitivity on mitochondrial adenosine triphosphatase. J Biol Chem 241, 2461-2466.
50. Racker E. (1964) A reconstituted system of oxidative phosphorylation. Biochem Biophys Res Commun 14, 75-78.
51. Racker E. (1963) A mitochondrial factor conferring oligomycin sensitivity on soluble mitochondrial ATPase. Biochem Biophys Res Commun 10, 435-439.
52. Symersky J, Osowski D, Walters DE, and Mueller DM. (2012) Oligomycin frames a common drug-binding site in the ATP synthase. Proc Natl Acad Sci USA 109, 13961-13965.
53. 1-ATPase. Biochemistry 33, 7971-7978.
54. + transport from each side of the membrane. J Biol Chem 285, 39811-39818.
55. Fillingame RH, Angevine CM, and Dmitriev OY. (2003) Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett 555, 29-34.
56. 0 ATP synthase as determined by labeling of unique cysteine residues. J Biol Chem 273, 16235-16240.
57. Baker LA, Watt IN, Runswick MJ, Walker JE, and Rubinstein JL. (2012) Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc Natl Acad Sci USA 109, 11675-11680.
58. Stock D, Leslie AGW, and Walker JE. (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700-1705.
59. +-ATPase from Ilyobacter tartaricus. Science 308, 659-662.
60. 13 ring from a thermoalkaliphilic ATP synthase reveals an extended diameter due to a special structural region. J Mol Biol 388, 611-618.
61. 14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem 284, 18228-18235.
62. Pogoryelov D, Yildiz Ö, Faraldo-Gómez JD, and Meier T. (2009) High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16, 1068-1073.
63. Vik SB, Long JC, Wada T, and Zhang D. (2000) A model for the structure of subunit a of the Escherichia coli ATP synthase and its role in proton translocation. Biochim Biophys Acta 1458, 457-466.
64. 0 motor. Proc Natl Acad Sci USA 107, 1367-1372.
65. Velours J, Vailler J, Paumard P, Soubannier V, Lai-Zhang J, and Mueller DM. (2001) Bovine coupling fator 6, with just 14.5% shared identity, replaces subunit h in the yeast Saccharomyces cerevisiae ATP synthase. J Biol Chem 276, 8602-8607.
66. 0-ATPase from bovine heart mitochondria. Biochemistry 30, 5369-5378.
67. Spannagel C, Vaillier J, Arselin G, Graves PV, and Velours J. (1997) The subunit f of mitochondrial yeast ATP synthase-Characterization of the protein and disruption of the structural gene ATP17. Eur J Biochem 247, 1111-1117.
68. Vaillier J, Arselin G, Graves PV, Camougrand N, and Velours J. (1999) Isolation of supernumerary yeast ATP synthase subunits e and i. Characterization of subunit i and disruption of its structural gene ATP18. J Biol Chem 274, 543-548.
69. Arnold I, Pfeiffer K, Neupert W, Stuart RA, and Schägger H. (1999) ATP synthase of yeast mitochondria-Isolation of subunit j and disruption of the ATP18 gene. J Biol Chem 274, 36-40.
70. 1-ATPase in yeast Saccharomyces cerevisiae. EMBO J 18, 58-64.
71. 0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17, 7170-7178.
72. Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, Rycovska A, Zickermann V, and Kuhlbrandt W. (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc Natl Acad Sci USA 108, 14121-14126.
73. Seelert H, and Dencher NA. (2011) ATP synthase superassemblies in animals and plants: two or more are better. Biochim Biophys Acta 1807, 1185-1197.
74. Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, Brethes D, di Rago JP, and Velours J. (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J 21, 221-230.
75. Arselin G, Vaillier J, Salin B, Schaeffer J, Giraud MF, Dautant A, Brethes D, and Velours J. (2004) The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J Biol Chem 279, 40392-40399.
76. 0-ATP synthase, a protein required for maximal activity of cytochrome c oxidase. Eur.J.Biochem. 262, 315-323.
77. 1-cytochrome oxidase supercomplex and its association with the TIM23 machinery. J Biol Chem 283, 6677-6686.
78. Shen H, Walters DE, and Mueller DM. (2008) Introduction of the chloroplast redox regulatory region in the yeast ATP synthase impairs cytochrome c oxidase. J Biol Chem 283, 32937-32943.
79. Pullman ME, and Monroy GC. (1963) A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J Biol Chem 238, 3762-3769.
80. 80.Akashi A, Yoshida Y, Nakagoshi H, Kuroki K, Hashimoto T, Tagawa K, and Imamoto F. (1988) Molecular cloning and expression of a gene for a factor which stabilizes formation of inhibitor-mitochondrial ATPase complex from Saccharomyces cerevisiae. J Biochem 104, 526-530.
81. Ichikawa N, Yoshida Y, Hashimoto T, Ogasawara N, Yoshikawa H, Imamoto F, and Tagawa K. (1990) Activation of ATP hydrolysis by an uncoupler in mutant mitochondria lacking an intrinsic ATPase inhibitor in yeast. J Biol Chem. 265, 6274-6278.
82. Rouslin W, and Broge CW. (1993) Mechanisms of ATP conservation during ischemia in slow and fast heart rate hearts. Am J Physiol 264, C209-216.
83. Rouslin W. (1991) Regulation of the mitochondrial ATPase in situ in cardiac muscle: role of the inhibitor subunit. J Bioenerg Biomembr 23, 873-888.
84. + symport. J Biol Chem 264, 15224-15229.
85. Rouslin W. (1987) Factors affecting the reactivation of the oligomycin-sensitive adenosine 5'-triphosphatase and the release of ATPase inhibitor protein during the re-energization of intact mitochondria from ischemic cardiac muscle. J Biol Chem 262, 3472-3476.
86. Rouslin W, and Erickson JL. (1986) Factors affecting the loss of mitochondrial function in autolyzing cardiac muscle. J Mol Cell Cardiol 18, 1187-1195.
87. o-ATPase inhibitor protein, IF1. Cell Metab 8, 13-25.
88. Rak M, Gokova S, and Tzagoloff A. (2011) Modular assembly of yeast mitochondrial ATP synthase. EMBO J 30, 920-930.
89. Lopez-Martinez G, Rodriguez-Porrata B, Margalef-Catala M, and Cordero-Otero R. (2012) The STF2p hydrophilin from Saccharomyces cerevisiae is required for dehydration stress tolerance. PLoS One 7, e33324.
90. 1, to ATP homeostasis, cell growth, mitochondrial morphology, and cell viability. J Biol Chem 287, 18781-18787.
91. 1-ATPase in complex with its regulatory protein IF1. Nat Struct Biol 10, 744-750.
92. 1-ATPase. Proc Natl Acad Sci USA 111, 11305-11310.
93. 0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme. Proc Natl Acad Sci USA 98, 6560-6564.
94. 1-ATPase activity. J Biol Chem 282, 8521-8532.
95. +-ATPase works in parallel with the HOG pathway to adapt Saccharomyces cerevisiae cells to osmotic stress. Eukaryot Cell 11, 282-291.
96. 1-ATPase biogenesis in mitochondria. Biochim Biophys Acta 1555, 101-105.
97. 1-ATPase in human mitochondria. J Biol Chem 276, 30773-30778.
98. 1-ATPase. J Biol Chem 275, 5767-5772.
99. 1-ATPase in yeast. J Biol Chem 271, 4887-4894.
100. 1-ATPase. Proc Natl Acad Sci USA 87, 4986-4990.
101. 1-ATPase in yeast-Identification of domains important for Atp12p function and oligomerization. J Biol Chem 273, 2993-3002.
102. Xiao Y, Metzl M, and Mueller DM. (2000) Partial uncoupling of the mitochondrial membrane by a heterozygous null mutation in the gene encoding the g-or d-subunit of the yeast mitochondrial ATPase. J Biol Chem 275, 6963-6968.
103. Duvezin-Caubet S, Caron M, Giraud MF, Velours J, and di Rago JP. (2003) The two rotor components of yeast mitochondrial ATP synthase are mechanically coupled by subunit d. Proc Natl Acad Sci USA 100, 13235-13240.
104. Mueller DM. (2000) Partial assembly of the yeast ATP synthase. J Bioener Biomem 32, 391-400.
105. Beasley EM, Wachter C, and Schatz G. (1992) Putting energy into mitochondrial protein import. Curr Opin Cell Biol 4, 646-651.
106. Gasser SM, Daum G, and Schatz G. (1982) Import of proteins into mitochondria. Energy-dependent uptake of precursors by isolated mitochondria. J Biol Chem 257, 13034-13041.
107. Klingenberg M, and Rottenberg H. (1977) Relation between the gradient of the ATP/ADP ratio and the membrane potential across the mitochondrial membrane. Eur J Biochem 73, 125-130.
108. 0 strains of Saccharomyces cerevisiae. Biochem Biophys Res Commun 132, 1116-1123.
109. Kominsky DJ, Brownson MP, Updike DL, and Thorsness PE. (2002) Genetic and biochemical basis for viability of yeast lacking mitochondrial genomes. Genetics 162, 1595-1604.
110. 1-ATPase by expression of the corresponding bovine subunits in yeast S. cerevisiae. Eur J Biochem 267, 2409-2418.
111. Guélin E, Chevallier J, Rigoulet M, Guérin B, and Velours J. (1993) ATP synthase of yeast mitochondria. Isolation and disruption of the ATPe gene. J Biol Chem 268, 161-167.
112. 0. Mol Biol Cell 25, 791-799.
113. Clark-Walker GD, and Chen XJ. (1996) A vital function for mitochondrial DNA in the petite-negative yeast Kluyveromyces lactis. Mol Gen Genet 252, 746-750.
114. 0. Mol Gen Genet 259, 457-467.
115. 1-ATPase d-subunit gene in Kluyveromyces lactis. Curr Genet 33, 46-51.
116. 1-ATPase are required for survival of petite mutants in Saccharomyces cerevisiae. Mol Gen Genet 262, 898-908.
117. 1-ATPase. Biochim Biophys Acta 1478, 125-137.
118. Fernet CS, Clark-Walker GD, and Claisse ML. (2002) The mitochondrial genome can be altered or lost without lethal effect in the petite-negative yeast Debaryomyces (Schwanniomyces) occidentalis. Curr Genet 42, 94-102.
119. Kominsky DJ, and Thorsness PE. (2000) Expression of the Saccharomyces cerevisiae gene YME1 in the petite-negative yeast Schizosaccharomyces pombe converts it to petite-positive. Genetics 154, 147-154.
120. Weber ER, Rooks RS, Shafer KS, Chase JW, and Thorsness PE. (1995) Mutations in the mitochondrial ATP synthase g subunit suppress a slow-growth phenotype of yme1 yeast lacking mitochondrial DNA. Genetics 140, 435-442.
121. 1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24, 4029-4040.
122. Dean S, Gould MK, Dewar CE, and Schnaufer AC. (2013) Single point mutations in ATP synthase compensate for mitochondrial genome loss in trypanosomes. Proc Natl Acad Sci USA 110, 14741-14746.
123. Wang Y, Singh U, and Mueller DM. (2007) Mitochondrial genome integrity mutations uncouple the yeast Saccharomyces cerevisiae ATP synthase. J Biol Chem 282, 8228-8236.
124. 1 ATPase reveal two modes of uncoupling. J Biol Chem 285, 36561-36569.
125. Gumbiowski K, Cherepanov D, Muller M, Panke O, Promto P, Winkler S, Junge W, and Engelbrecht S. (2001) F-ATPase: forced full rotation of the rotor despite covalent cross-link with the stator. J Biol Chem 276, 42287-42292.
126. Muller M, Gumbiowski K, Cherepanov DA, Winkler S, Junge W, Engelbrecht S, and Panke O. (2004) Rotary F1-ATPase. Is the C-terminus of subunit g fixed or mobile? Eur J Biochem 271, 3914-3922.
127. Hilbers F, Junge W, and Sielaff H. (2013) The torque of rotary F-ATPase can unfold subunit g if rotor and stator are cross-linked. PLoS One 8, e53754.
128. Ichida M, Endo H, Ikeda U, Matsuda C, Ueno E, Shimada K, and Kagawa Y. (1998) MyoD is indispensable for muscle-specific alternative splicing in mouse mitochondrial ATP synthase g-subunit pre-mRNA. J Biol Chem 273, 8492-8501.
129. Endo H, Matsuda C, and Kagawa Y. (1994) Exclusion of an alternatively spliced exon in human ATP synthase g-subunit pre-mRNA requires de novo protein synthesis. J Biol Chem 269, 12488-12493.
130. Hayakawa M, Endo H, Hamamoto T, and Kagawa Y. (1998) Acidic stimulation induces a negative regulatory factor that affects alternative exon selection in vitro in human ATP synthase g-subunit pre-mRNA. Biochem Biophys Res Commun. 251, 603-608.
131. Hayakawa M, Sakashita E, Ueno E, Tominaga S, Hamamoto T, Kagawa Y, and Endo H. (2002) Muscle-specific exonic splicing silencer for exon exclusion in human ATP synthase g-subunit pre-mRNA. J Biol Chem 277, 6974-6984.
132. Matsuda C, Endo H, Hirata H, Morosawa H, Nakanishi M, and Kagawa Y. (1993) Tissue-specific isoforms of the bovine mitochondrial ATP synthase g-subunit. FEBS Lett. 325, 281-284.
133. Matsuda C, Muneyuki E, Endo H, Yoshida M, and Kagawa Y. (1994) Comparison of the ATPase activities of bovine heart and liver mitochondrial ATP synthases with different tissue-specific g subunit isoforms. Biochem Biophys Res Commun 200, 671-678.
134. 2+-adenosine triphosphatase-deficient mutant of Escherichia coli. J Bacteriol 116, 1124-1129.
135. 1 assembly on membranes. Arch Biochem Biophys 241, 364-370.
136. 1-ATPase rotates in the correct direction. Science 319, 955-958.
137. Mnatsakanyan N, Hook JA, Quisenberry L, and Weber J. (2009) ATP synthase with its g subunit reduced to the N-terminal helix can still catalyze ATP synthesis. J Biol Chem 284, 26519-26525.
138. 1-ATPase plays a significant role in torque production. Biophys J 95, 4837-4844.
139. 1-ATPase is dispensable for torque generation. Biophys J 90, 4195-4203.
140. 1. J Biol Chem 287, 1884-1891.
141. 1 e subunit. Hum Mol Genet 19, 3430-3439.
142. Lieber DS, Calvo SE, Slate NG, Liu S, Hershman SG, Gold NB, Borowsky ML, Thorburn DR, Berry GT, Schmahmann JD, Mueller DM, Sims KB, and Mootha VK. (2013) Targeted exome sequencing of suspected mitochondrial disorders. Neurology 80, 1762-1770.
143. Jonckheere AI, Renkema GH, Bras M, van den Heuvel LP, Hoischen A, Gilissen C, Nabuurs SB, Huynen MA, de Vries MC, Smeitink JA, and Rodenburg RJ. (2013) A complex V ATP5A1 defect causes fatal neonatal mitochondrial encephalopathy. Brain 136, 1544-1554.
144. Holt IJ, Harding AE, Petty RK, and Morgan-Hughes JA. (1990) A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am J Hum Genet 46, 428-433. PMID: 2137962.
145. Vik SB, and Ishmukhametov RR. (2005) Structure and function of subunit a of the ATP synthase of Escherichia coli. J Bioenerg Biomembr 37, 445-449.
146. DeLeon-Rangel J, Ishmukhametov RR, Jiang W, Fillingame RH, and Vik SB. (2013) Interactions between subunits a and b in the rotary ATP synthase as determined by cross-linking, FEBS Lett 587, 892-897.
147. Long JC, DeLeon-Rangel J, and Vik SB. (2002) Characterization of the first cytoplasmic loop of subunit a of the Escherichia coli ATP synthase by surface labeling, cross-linking, and mutagenesis. J Biol Chem 277, 27288-27293.
148. Moore KJ, and Fillingame RH. (2008) Structural interactions between transmembrane helices 4 and 5 of subunit a and the subunit c ring of Escherichia coli ATP synthase. J Biol Chem 283, 31726-31735.
149. 0: a study based on cysteine mutants, thiol modification and cross-linking reagents. Biochim Biophys Acta 1458, 443-456.
150. Angevine CM, Herold KA, Vincent OD, and Fillingame RH. (2007) Aqueous access pathways in ATP synthase subunit a. Reactivity of cysteine substituted into transmembrane helices 1, 3, and 5, J Biol Chem 282, 9001-9007.
151. Moslemi AR, Darin N, Tulinius M, Oldfors A, and Holme E. (2005) Two new mutations in the MTATP6 gene associated with Leigh syndrome, Neuropediatrics 36, 314-318.
152. Childs AM, Hutchin T, Pysden K, Highet L, Bamford J, Livingston J, and Crow YJ. (2007) Variable phenotype including Leigh syndrome with a 9185TOpenSPIGreaterThanSPIC mutation in the MTATP6 gene. Neuropediatrics 38, 313-316.
153. Castagna AE, Addis J, McInnes RR, Clarke JT, Ashby P, Blaser S, and Robinson BH. (2007) Late onset Leigh syndrome and ataxia due to a T to C mutation at bp 9,185 of mitochondrial DNA. Am J Med Genet A 143A, 808-816.
154. Verity CM, Winstone AM, Stellitano L, Krishnakumar D, Will R, and McFarland R. (2010) The clinical presentation of mitochondrial diseases in children with progressive intellectual and neurological deterioration: a national, prospective, population-based study. Dev Med Child Neurol 52, 434-440.
155. Gigarel N, Hesters L, Samuels DC, Monnot S, Burlet P, Kerbrat V, Lamazou F, Benachi A, Frydman R, Feingold J, Rotig A, Munnich A, Bonnefont JP, Frydman N, and Steffann J. (2011) Poor correlations in the levels of pathogenic mitochondrial DNA mutations in polar bodies versus oocytes and blastomeres in humans. Am J Hum Genet 88, 494-498.
156. Pereira L, Soares P, Radivojac P, Li B, and Samuels DC. (2011) Comparing phylogeny and the predicted pathogenicity of protein variations reveals equal purifying selection across the global human mtDNA diversity. Am J Hum Genet 88, 433-439.
157. Pfeffer G, Blakely EL, Alston CL, Hassani A, Boggild M, Horvath R, Samuels DC, Taylor RW, and Chinnery PF. (2012) Adult-onset spinocerebellar ataxia syndromes due to MTATP6 mutations. J Neurol Neurosurg Psychiatry 83, 883-886.
158. Aure K, Dubourg O, Jardel C, Clarysse L, Sternberg D, Fournier E, Laforet P, Streichenberger N, Petiot P, Gervais-Bernard H, Vial C, Bedat-Millet AL, Drouin-Garraud V, Bouillaud F, Vandier C, Fontaine B, and Lombes A. (2013) Episodic weakness due to mitochondrial DNA MT-ATP6/8 mutations. Neurology 81, 1810-1818.
159. Saneto RP, and Singh KK. (2010) Illness-induced exacerbation of Leigh syndrome in a patient with the MTATP6 mutation, m.9185 TOpenSPIGreaterThanSPIC. Mitochondrion 10, 567-572.
160. Carrozzo R, Murray J, Capuano O, Tessa A, Chichierchia G, Neglia MR, Capaldi RA, and Santorelli FM. (2000) A novel mtDNA mutation in the ATPase6 gene studied by E. coli modeling. Neurol Sci 21, S983-984.
161. Carrozzo R, Murray J, Santorelli FM, and Capaldi RA. (2000) The T9176G mutation of human mtDNA gives a fully assembled but inactive ATP synthase when modeled in Escherichia coli. FEBS Lett 486, 297-299.
162. Alvarez-Iglesias V, Barros F, Carracedo A, and Salas A. (2008) Minisequencing mitochondrial DNA pathogenic mutations. BMC Med Genet 9, 26.
163. Thyagarajan D, Shanske S, Vazquez-Memije M, De Vivo D, and DiMauro S. (1995) A novel mitochondrial ATPase 6 point mutation in familial bilateral striatal necrosis. Ann Neurol 38, 468-472.
164. Campos Y, Martin MA, Rubio JC, Solana LG, Garcia-Benayas C, Terradas JL, and Arenas J. (1997) Leigh syndrome associated with the T9176C mutation in the ATPase 6 gene of mitochondrial DNA. Neurology 49, 595-597.
165. Dionisi-Vici C, Seneca S, Zeviani M, Fariello G, Rimoldi M, Bertini E, and De Meirleir L. (1998) Fulminant Leigh syndrome and sudden unexpected death in a family with the T9176C mutation of the mitochondrial ATPase 6 gene. J Inherit Metab Dis 21, 2-8.
166. Makino M, Horai S, Goto Y, and Nonaka I. (1998) Confirmation that a T-to-C mutation at 9176 in mitochondrial DNA is an additional candidate mutation for Leigh's syndrome. Neuromuscul Disord 8, 149-151.
167. Rubio-Gozalbo ME, Dijkman KP, van den Heuvel LP, Sengers RC, Wendel U, and Smeitink JA. (2000) Clinical differences in patients with mitochondriocytopathies due to nuclear versus mitochondrial DNA mutations. Hum Mutat 15, 522-532.
168. Mishmar D, and Zhidkov I. (2010) Evolution and disease converge in the mitochondrion. Biochim Biophys Acta 1797, 1099-1104.
169. Nakano K, Ohsawa I, Yamagata K, Nakayama T, Sasaki K, Tarashima M, Saito K, Osawa M, and Ohta S. (2003) Continuous culture of novel mitochondrial cells lacking nuclei. Mitochondrion 3, 21-27.
170. Dobrowolski SF, Hendrickx AT, van den Bosch BJ, Smeets HJ, Gray J, Miller T, and Sears M. (2009) Identifying sequence variants in the human mitochondrial genome using high-resolution melt (HRM) profiling. Hum Mutat 30, 891-898.
171. Nishigaki Y, Ueno H, Coku J, Koga Y, Fujii T, Sahashi K, Nakano K, Yoneda M, Nonaka M, Tang L, Liou CW, Paquis-Flucklinger V, Harigaya Y, Ibi T, Goto Y, Hosoya H, DiMauro S, Hirano M, and Tanaka M. (2010) Extensive screening system using suspension array technology to detect mitochondrial DNA point mutations. Mitochondrion 10, 300-308.
172. Kucharczyk R, Ezkurdia N, Couplan E, Procaccio V, Ackerman SH, Blondel M, and di Rago JP. (2010) Consequences of the pathogenic T9176C mutation of human mitochondrial DNA on yeast mitochondrial ATP synthase. Biochim Biophys Acta 1797, 1105-1112.
173. Shidara Y, Yamagata K, Kanamori T, Nakano K, Kwong JQ, Manfredi G, Oda H, and Ohta S. (2005) Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65, 1655-1663.
174. Verny C, Guegen N, Desquiret V, Chevrollier A, Prundean A, Dubas F, Cassereau J, Ferre M, Amati-Bonneau P, Bonneau D, Reynier P, and Procaccio V. (2011) Hereditary spastic paraplegia-like disorder due to a mitochondrial ATP6 gene point mutation. Mitochondrion 11, 70-75.
175. Ronchi D, Bordoni A, Cosi A, Rizzuti M, Fassone E, Di Fonzo A, Servida M, Sciacco M, Collotta M, Ronzoni M, Lucchini V, Mattioli M, Moggio M, Bresolin N, Corti S, and Comi GP. (2011) Unusual adult-onset Leigh syndrome presentation due to the mitochondrial m.9176TOpenSPIGreaterThanSPIC mutation. Biochem Biophys Res Commun 412, 245-248.
176. Ciafaloni E, Santorelli FM, Shanske S, Deonna T, Roulet E, Janzer C, Pescia G, and DiMauro S. (1993) Maternally inherited Leigh syndrome. J Pediatr 122, 419-422.
177. Vazquez-Memije ME, Shanske S, Santorelli FM, Kranz-Eble P, DeVivo DC, and DiMauro S. (1998) Comparative biochemical studies of ATPases in cells from patients with the T8993G or T8993C mitochondrial DNA mutations. J Inherit Metab Dis 21, 829-836.
178. de Vries DD, van Engelen BG, Gabreels FJ, Ruitenbeek W, and van Oost BA. (1993) A second missense mutation in the mitochondrial ATPase 6 gene in Leigh's syndrome. Ann Neurol 34, 410-412.
179. Santorelli FM, Shanske S, Jain KD, Tick D, Schon EA, and DiMauro S. (1994) A T--OpenSPIGreaterThanSPIC mutation at nt 8993 of mitochondrial DNA in a child with Leigh syndrome. Neurology 44, 972-974.
180. Pallotti F, Baracca A, Hernandez-Rosa E, Walker WF, Solaini G, Lenaz G, Melzi D'Eril GV, Dimauro S, Schon EA, and Davidson MM. (2004) Biochemical analysis of respiratory function in cybrid cell lines harbouring mitochondrial DNA mutations. Biochem J 384, 287-293.
181. Morava E, Rodenburg RJ, Hol F, de Vries M, Janssen A, van den Heuvel L, Nijtmans L, and Smeitink J. (2006) Clinical and biochemical characteristics in patients with a high mutant load of the mitochondrial T8993G/C mutations. Am J Med Genet A 140, 863-868.
182. Rantamaki MT, Soini HK, Finnila SM, Majamaa K, and Udd B. (2005) Adult-onset ataxia and polyneuropathy caused by mitochondrial 8993T--OpenSPIGreaterThanSPIC mutation. Ann Neurol 58, 337-340.
183. Harding AE, Holt IJ, Sweeney MG, Brockington M, and Davis MB. (1992) Prenatal diagnosis of mitochondrial DNA8993 T----G disease. Am J Hum Genet 50, 629-633.
184. Pastores GM, Santorelli FM, Shanske S, Gelb BD, Fyfe B, Wolfe D, and Willner JP. (1994) Leigh syndrome and hypertrophic cardiomyopathy in an infant with a mitochondrial DNA point mutation (T8993G). Am J Med Genet 50, 265-271.
185. Santorelli FM, Shanske S, Macaya A, DeVivo DC, and DiMauro S. (1993) The mutation at nt 8993 of mitochondrial DNA is a common cause of Leigh's syndrome. Ann Neurol 34, 827-834.
186. Shoffner JM, Fernhoff PM, Krawiecki NS, Caplan DB, Holt PJ, Koontz DA, Takei Y, Newman NJ, Ortiz RG, Polak M, and et al. (1992) Subacute necrotizing encephalopathy: oxidative phosphorylation defects and the ATPase 6 point mutation. Neurology 42, 2168-2174.
187. Sgarbi G, Baracca A, Lenaz G, Valentino LM, Carelli V, and Solaini G. (2006) Inefficient coupling between proton transport and ATP synthesis may be the pathogenic mechanism for NARP and Leigh syndrome resulting from the T8993G mutation in mtDNA. Biochem J 395, 493-500.
188. Baracca A, Sgarbi G, Mattiazzi M, Casalena G, Pagnotta E, Valentino ML, Moggio M, Lenaz G, Carelli V, and Solaini G. (2007) Biochemical phenotypes associated with the mitochondrial ATP6 gene mutations at nt8993. Biochim Biophys Acta 1767, 913-919.
189. Mak SC, Chi CS, Liu CY, Pang CY, and Wei YH. (1996) Leigh syndrome associated with mitochondrial DNA 8993 T--OpenSPIGreaterThanSPIG mutation and ragged-red fibers. Pediatr Neurol 15, 72-75.
190. Schon EA, Santra S, Pallotti F, and Girvin ME. (2001) Pathogenesis of primary defects in mitochondrial ATP synthesis. Semin Cell Dev Biol 12, 441-448.
191. Kucharczyk R, Zick M, Bietenhader M, Rak M, Couplan E, Blondel M, Caubet SD, and di Rago JP. (2009) Mitochondrial ATP synthase disorders: molecular mechanisms and the quest for curative therapeutic approaches. Biochim Biophys Acta 1793, 186-199.
192. Houstek J, Mracek T, Vojtiskova A, and Zeman J. (2004) Mitochondrial diseases and ATPase defects of nuclear origin. Biochim Biophys Acta 1658, 115-121.
193. Rak M, Tetaud E, Godard F, Sagot I, Salin B, Duvezin-Caubet S, Slonimski PP, Rytka J, and di Rago JP. (2007) Yeast cells lacking the mitochondrial gene encoding the ATP synthase subunit 6 exhibit a selective loss of complex IV and unusual mitochondrial morphology. J Biol Chem 282, 10853-10864.
194. 0-ATP synthase. Biochim Biophys Acta 1793, 1776-1786.
195. 0-ATP synthase from Escherichia coli. A model for human mitochondrial disease. J Biol Chem 268, 12250-12252. PMID:8509361
196. 0-ATP synthase without preventing enzyme assembly and oligomerization. J Biol Chem 282, 1051-1058.
197. Kucharczyk R, Rak M, and di Rago JP. (2009) Biochemical consequences in yeast of the human mitochondrial DNA 8993TOpenSPIGreaterThanSPIC mutation in the ATPase6 gene found in NARP/MILS patients. Biochim Biophys Acta 1793, 817-824.
198. Rak M, Tetaud E, Duvezin-Caubet S, Ezkurdia N, Bietenhader M, Rytka J, and di Rago JP. (2007) A yeast model of the neurogenic ataxia retinitis pigmentosa (NARP) T8993G mutation in the mitochondrial ATP synthase-6 gene. J Biol Chem 282, 34039-34047.
199. Jonckheere AI, Hogeveen M, Nijtmans LG, van den Brand MA, Janssen AJ, Diepstra JH, van den Brandt FC, van den Heuvel LP, Hol FA, Hofste TG, Kapusta L, Dillmann U, Shamdeen MG, Smeitink JA, and Rodenburg RJ. (2008) A novel mitochondrial ATP8 gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J Med Genet 45, 129-133.
200. Ware SM, El-Hassan N, Kahler SG, Zhang Q, Ma YW, Miller E, Wong B, Spicer RL, Craigen WJ, Kozel BA, Grange DK, and Wong LJ. (2009) Infantile cardiomyopathy caused by a mutation in the overlapping region of mitochondrial ATPase 6 and 8 genes. J Med Genet 46, 308-314.
201. 386 segment in energy coupling. Biochem J 330, 707-712.
202. 1-ATP synthase: The uncoupling mutation, gM23K, disrupts the use of binding energy to drive catalysis. Biochemistry 36, 12954-12960.
203. i. Transition state analysis of this mutant and others reveals that synthesis and hydrolysis utilize the same kinetic pathway. Biochemistry 36, 12961-12969.
204. 0 ATP synthase. J Biol Chem 284, 23243-23250.