Abstract
Two classes ofSaccharomyces cerevisiae mutants resistant to oligomycin, an inhibitor of mitochondrial membrane bound ATPase are described. Biochemical analysis shows thatin vitro the mitochondrial ATPase of both types of mutant are sensitive to oligomycin.In vivo sensitivity of the mutants to oligomycin can be demonstrated following anaerobic growth of the cells, which grossly alters the mitochondrial membrane and renders the ATPase of the mutants sensitive to oligomycin. It is concluded that the mutation to oligomycin resistance in both mutant types is phenotypically expressed as a change in the mitochondrial membrane. The intact mitochondrial membrane in the wild type cell is freely permeable to oligomycin, whereas the resistant mutant is impermeable to oligomycin; alteration of the mitochondrial membrane during isolation of the organelle or physiological modification of the membranes of the mitochondria by anaerobic growth renders the membranes permeable.
These mitochondrial membrane mutants differ in their cross-reference patterns and their genetics. One is resistant to oligomycin only, and behaves like previously reported cytoplasmic mutants. The other shows cross-resistance to inhibitors of mitochondrial protein synthesis as well as to oligomycin; although the mutant appears to arise from a single step mutation its genetic properties are complex and show part-nuclear and part-cytoplasmic characteristics. The implications of the observations are discussed.
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A. W. Linnane and J. M. Haslam, in:Current Topics in Cellular Regulation, B. L. Horecker and B. R. Stadtman (eds.), Vol. 2, Academic Press, New York, 1970, p. 101.
A. W. Linnane, J. M. Haslam and I. T. Forrester,Biochemistry and Biophysics of Mitochondrial Membranes, G. F. Azzone, E. Carafoli, A. L. Lehninger, E. Quagliariello and N. Siliprandi (eds.), Bressanone, Italy, 1971, Academic Press, New York, in press.
A. A. Andreson and T. J. B. Stier,J. Cell. Comp. Physiol.,41 (1953) 23.
D. K. Bloomfield and K. Bloch,J. Biol. Chem.,235 (1960) 337.
P. G. Wallace, M. Huang and A. W. Linnane,J. Cell. Biol.,37 (1968) 207.
R. S. Criddle and G. Schatz,Biochemistry,8 (1969) 322.
H. Plattner and G. Schatz,Biochemistry,8 (1969) 339.
K. Watson, J. M. Haslam and A. W. Linnane,J. Cell Biol.,46 (1970) 88.
K. Watson, J. M. Haslam, B. Veitch and A. W. Linnane, in:Autonomy and Biogenesis of Mitochondria and Chloroplasts, N. K. Boardman, A. W. Linnane and R. M. Smillie (eds.), North Holland Press, Amsterdam, 1971, p. 162.
K. Bloch, B. Baronowsky, H. Goldfine, W. J. Lennarz, R. Light, A. T. Norris and G. Scheuerbrant,Fed. Proc.,20 (1961) 921.
J. W. Proudlock, L. W. Wheeldon, D. J. Jollow and A. W. Linnane,Biochim. Biophys. Acta,152 (1968) 434.
D. J. Jollow, G. M. Kellerman and A. W. Linnane,J. Cell Biol.,37 (1968) 221.
I. T. Forrester, K. Watson and A. W. Linnane,Biochem. Biophys. Res. Commun.,43 (1971) 409.
K. A. Ward and A. W. Linnane, “Cell Differentiation”, submitted.
I. T. Forrester, K. A. Ward and A. W. Linnane, in preparation.
B. Ephrussi,Harvey Lectures,46 (1950) 45.
J. W. Proudlock, J. M. Haslam and A. W. Linnane,Biochem. Biophys. Res. Commun.,37 (1969) 847.
J. W. Proudlock, J. M. Haslam and A. W. Linnane,J. Bioenergetics,2 (1971) 327.
J. M. Haslam, J. W. Proudlock and A. W. Linnane,J. Bioenergetics,2 (1971) 351.
C. L. Bunn, C. H. Mitchell, H. B. Lukins and A. W. Linnane,Proc. Natl. Acad. Sci. (U.S.) 67 (1970) 1233.
K. Wakabayashi and N. Gunge,FEBS Letters,6 (1970) 302.
K. D. Stuart,Biochem. Biophys. Res. Commun.,39 (1970) 1045.
P. R. Avner and D. E. Griffiths,FEBS Letters,10 (1970) 202.
D. E. Griffiths, P. R. Avner, W. Lancashire and J. R. Turner,Biochemistry and Biophysics of Mitochondrial Membranes, G. F. Azzone, E. Carafoli, A. L. Lehninger, E. Quagliariello, and N. Siliprandi (eds.), Bressanone, Italy, 1971, Academic Press, New York, in press.
A. W. Linnane, G. W. Saunders, E. B. Gingold and H. B. Lukins,Proc. Natl. Acad. Sci. (U.S.),59 (1968) 903.
G. W. Saunders, E. B. Gingold, M. K. Trembath, H. B. Lukins and A. W. Linnane, in:Autonomy and Biogenesis of Mitochondria and Chloroplasts, N. K. Boardman, A. W. Linnane and R. M. Smillie (eds.), Amsterdam, North Holland Press, 1971, p. 185.
E. B. Gingold, G. W. Saunders, H. B. Lukins and A. W. Linnane,Genetics,62 (1969) 735.
P. Nagley and A. W. Linnane,Biochem. Biophys. Res. Commun.,39 (1970) 989.
E. S. Goldring, L. I. Grossman, D. Krupnick, D. R. Cryer and J. Marmur,J. Mol. Biol.,52 (1970) 323.
G. Michaelis, S. Douglass, M. Tsai and R. S. Criddle,Biochem. Genet.,5 (1971) 487.
A. J. Lamb, G. D. Clark-Walker and A. W. Linnane,Biochem. Biophys. Acta,161 (1968) 415.
M. Somlo,European J. Biochem.,5 (1968) 276.
G. Gomori,J. Lab. Clin. Med.,27 (1942) 955.
G. C. Monroy and M. E. Pullman, in:Methods in Enzymology, Vol. 10, R. W. Estabrook and M. E. Pullman (eds.), Academic Press, New York, 1967, p. 510.
L. Kovac, H. Bednarova, and M. Greksak,Biochim. Biophys. Acta,153 (1968) 32.
B. Ephrussi, H. Jakob and S. Grandchamp,Genetics,54 (1966) 1.
D. Coen, J. Deutsch, P. Netter, E. Petrochilo and P. P. Slonimski, in:The Control of Organelle Development, P. L. Miller (ed.), p. 449, Cambridge University Press, 1970.
J. Subik, S. Kuzela, J. Kolorov, L. Kovac and T. M. Lachowicz,Biochim. Biophys. Acta,205 (1970) 513.
A. Tzagaloff,J. Biol. Chem.,246 (1971) 3050.
D. Plummer, A. A. Green, K. Watson, K. A. Ward and A. W. Linnane, in preparation.
C. L. Bunn, H. B. Lukins and A. W. Linnane, in preparation.
R. E. Monro and D. Vazquez,J. Mol. Biol.,28 (1967) 161.
H. Teraoka, M. Tamaki and K. Tanaka,Biochem. Biophys. Res. Commun.,38 (1970) 328.
J. C. H. Mao and E. R. Robishaw,Biochemistry,10 (1971) 2054.
D. Wilkie, inThe Control of Organelle Development, P. L. Miller (ed.), Cambridge University Press, 1970, p. 71.
A. W. Linnane, A. J. Lamb, C. Christodoulou and H. B. Lukins,Proc. Natn. Acad. Sci. (U.S.),59 (1968) 1288.
L. A. Grivell, L. Reijanders and H. de Vries,FEBS Letters,16 (1971) 159.
J. H. Parker, I. R. Trimble and J. R. Mattoon,Biochem. Biophys. Res. Commun.,33 (1968) 590.
T. M. Sonneborn, in:The Nature of Biological Diversity, J. M. Allen (ed.), McGraw-Hill, New York, 1963, p. 165.
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Mitchell, C.H., Bunn, C.L., Lukins, H.B. et al. Biogenesis of mitochondria 23. The biochemical and genetic characteristics of two different oligomycin resistant mutants ofSaccharomyces cerevisiae under the influence of cytoplasmic genetic modification. J Bioenerg Biomembr 4, 161–177 (1973). https://doi.org/10.1007/BF01516054
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DOI: https://doi.org/10.1007/BF01516054