IF1, a natural inhibitor of mitochondrial ATP synthase, is not essential for the normal growth and breeding of mice

Bioscience Reports

Volumn 33, Issue 5, 2013, Pages 735-741

  Nakamura, Junji ^a,b   Fujikawa, Makoto ^b,c   Yoshida, Masasuke ^a,b  

^a KYOTO SANGYO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

ATP synthesis; FoF1; Knockout mouse

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE INHIBITOR; ATPASE INHIBITORY PROTEIN; PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BREEDING; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; GENOTYPE; GROWTH RATE; HETEROZYGOSITY; IF1 GENE; KNOCKOUT MOUSE; MALE; MITOCHONDRION; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; STARVATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; ENZYMOLOGY; FOOD DEPRIVATION; GENETICS; LIVER MITOCHONDRION; METABOLISM; ULTRASTRUCTURE; WEIGHT GAIN;

ANIMALS; AUTOPHAGY; CELLS, CULTURED; FEMALE; FOOD DEPRIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; PROTEINS; WEIGHT GAIN;

EID: 84884849570     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20130078     Document Type: Article

References (28)

1. Pullman, M. and Monroy, G. (1963) A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J. Biol. Chem. 238, 3762-3769
2. Ichikawa, N., Ushida, S., Kawabata, M. and Masazumi, Y. (1999) Nucleotide sequence of cDNA coding the mitochondrial precursor protein of the ATPase inhibitor from humans. Biosci. Biotechnol. Biochem. 63, 2225-2227 (Pubitemid 129549053)
3. Yamada, E., Ishiguro, N., Miyaishi, O., Takeuchi, A., Nakashima, I., Iwata, H. and Isobe, K. (1997) Differential display analysis of murine collagen-induced arthritis: cloning of the cDNA-encoding murine ATPase inhibitor. Immunology 92, 571-576 (Pubitemid 27525231)
4. Galante, Y.M., Wong, S.Y. and Hatefi, Y. (1981) Mitochondrial adenosinetriphosphatase inhibitor protein: reversible interaction with complex V (ATP synthetase complex). Biochemistry 20, 2671-2678
5. Cabezon, E., Butler, P. J., Runswick, M. J. and Walker, J. E. (2000) Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH. J. Biol. Chem. 275, 25460-25464
6. Aggeler, R., Coons, J., Taylor, S. W., Ghosh, S. S., Garcia, J. J., Capaldi, R. A. and Marusich, M. F. (2002) A functionally active human F1Fo ATPase can be purified by immunocapture from heart tissue and fibroblast cell lines. Subunit structure and activity studies. J. Biol. Chem. 277, 33906-33912
7. Cabezon, E., Montgomery, M. G., Leslie, A. G. and Walker, J. E. (2003) The structure of bovine F1-ATPase in complex with its regulatory protein IF1. Nat. Struct. Biol. 10, 744-750 (Pubitemid 37052414)
8. Hashimoto, T., Yoshida, Y. and Tagawa, K. (1990) Regulatory proteins of F1Fo-ATPase: role of ATPase inhibitor. J. Bioenerg. Biomembr. 22, 27-38 (Pubitemid 20101587)
9. Fujikawa, M, Imamura, H, Nakamura, J and Yoshida, M. (2012) Assessing actual contribution of IF1, inhibitor of mitochondrial FoF1, to ATP homeostasis, cell growth, mitochondrial morphology, and cell viability. J. Biol. Chem. 287, 18781-18787
10. Campanella, M., Casswell, E., Chong, S., Farah, Z., Wieckowski, M. R., Abramov, A. Y., Tinker, A. and Duchen, M. R. (2008) Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab 8, 13-25 (Pubitemid 351859227)
11. Garcia, J. J., Morales-Rios, E., Cortés-Hernandez, P. and Rodriguez-Zavala, J. S. (2006) The inhibitor protein (IF1) promotes dimerization of the mitochondrial F1Fo-ATP synthase. Biochemistry 45, 12695-12703 (Pubitemid 44630855)
12. Buzhynskyy, N., Sens, P., Prima, V., Sturgis, J. N. and Scheuring, S. (2007) Rows of ATP synthase dimers in native mitochondrial inner membranes. Biophys. J. 93, 2870-2876 (Pubitemid 47607823)
13. De los Rios Castillo, D., Zarco-Zavala, M., Olvera-Sanchez, S., Pardo, J. P., Juarez, O., Martinez, F., Mendoza-Hernandez, G., Garcia-Trejo, J. J. and Flores-Herrera, O. (2011) Atypical cristae morphology of human syncytiotrophoblast mitochondria: role for complex V. J. Biol Chem. 286, 23911-23919
14. Dienhart, M., Pfeiffer, K., Schagger, H. and Stuart, R. A. (2002) Formation of the yeast F1Fo-ATP synthase dimeric complex does not require the ATPase inhibitor protein, Inh1. J. Biol. Chem. 277, 39289-39295 (Pubitemid 35190900)
15. Tomasetig, L., Di Pancrazio, F., Harris, D. A., Mavelli, I. and Lippe, G. (2002) Dimerization of F1Fo-ATP synthase from bovine heart is independent from the binding of the inhibitor protein IF1. Biochim. Biophys. Acta 1556, 133-141 (Pubitemid 35379671)
16. Campanella, M., Seraphim, A., Abeti, R., Casswell, E., Echave, P. and Duchen, M. R. (2009) IF1, the endogenous regulator of the F1Fo-ATPsynthase, defines mitochondrial volume fraction in HeLa cells by regulating autophagy. Biochim. Biophys. Acta 1787, 393-401
17. Sánchez-Cenizo, L., Formentini, L., Aldea, M., Ortega, A. D., Garcia-Huerta, P., Sánchez-Aragó, M. and Cuezva, J. M. (2010) Up-regulation of the ATPase inhibitory factor 1 (IF1) of the mitochondrial H+ -ATP synthase in human tumors mediates the metabolic shift of cancer cells to a Warburg phenotype. J. Biol. Chem. 285, 25308-25313
18. Domenis, R., Comelli, M., Bisetto, E. and Mavelli, I. (2011) Mitochondrial bioenergetic profile and responses to metabolic inhibition in human hepatocarcinoma cell lines with distinct differentiation characteristics. J. Bioenerg. Biomembr. 43, 493-505
19. Shah, D. I., Takahashi-Makise, N., Cooney, J. D., Li, L., Schultz, I. J., Pierce, E. L., Narla, A., Seguin, A., Hattangadi, S. M., Medlock, A. E. et al. (2012) Mitochondrial Atpif1 regulates haem synthesis in developing erythroblasts. Nature 491, 608-612
20. Giorgio, V., Bisetto, E., Franca, R., Harris, D.A., Passamonti, S. and Lippe, G. (2010) The ectopic F(O)F(1) ATP synthase of rat liver is modulated in acute cholestasis by the inhibitor protein IF1. J. Bioenerg. Biomembr. 42, 117-123
21. Genoux, A., Pons, V., Radojkovic, C., Roux-Dalvai, F., Combes, G., Rolland, C., Malet, N., Monsarrat, B., Lopez, F., Ruidavets, J.B. et al. (2011) Mitochondrial inhibitory factor 1 (IF1) is present in human serum and is positively correlated with HDL-cholesterol. PLoS ONE 6, e23949
22. Frezza, C., Cipolat, S. and Scorrano, L. (2007) Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc. 2, 287-295 (Pubitemid 47040043)
23. Ko, Y. H., Hullihen, J., Hong, S. and Pedersen, P. L. (2000) Mitochondrial F1Fo-ATP synthase. Subunit regions on the F1 motor shielded by Fo, functional significance, and evidence for an involvement of the unique Fo subunit F6. J. Biol. Chem. 275, 32931-32939
24. Zanotti, F., Raho, G., Gaballo, A. and Papa, S. (2004) Inhibitory and anchoring domains in the ATPase inhibitor protein IF1 of bovine heart mitochondrial ATP synthase. J. Bioenerg. Biomembr. 36, 447-457 (Pubitemid 39491330)
25. Wittig, I., Karas, M. and Schägger, H. (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell Proteomics. 6, 1215-1225 (Pubitemid 47099231)
26. Mizushima, N., Yoshimori, T. and Levine, B. (2010) Methods in mammalian autophagy research. Cell 140, 313-326
27. Sönnichsen, B., Koski, L. B., Walsh, A., Marschall, P., Neumann, B., Brehm, M., Alleaume, A. M., Artelt, J., Bettencourt, P., Cassin, E. et al. (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434, 462-469 (Pubitemid 40477050)
28. Lu, Y. M., Miyazawa, K., Yamaguchi, K., Nowaki, K., Iwatsuki, H., Wakamatsu, Y., Ichikawa, N. and Hashimoto, T. (2001) Deletion of mitochondrial ATPase inhibitor in the yeast Saccharomyces cerevisiae decreased cellular and mitochondrial ATP levels under non-nutritional conditions and induced a respiration-deficient cell-type. J. Biochem. 130, 873-878 (Pubitemid 34024139)