Cytoplasmic Inheritance of Oligomycin Resistance in Chinese Hamster Ovary Cells

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1980 Sep 1

PMID 6447704

Citations 8

Authors

G A Breen

I E Scheffler

Affiliations

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Abstract

Oligomycin-resistant clones were isolated from Chinese hamster ovary cells by treatment of cells with ethidium bromide, followed by mutagenesis with ethylmethane sulfonate and selection in oligomycin. One clone (Olir 8.1) was chosen for further study. Olir 8.1 cells grow with doubling time similar to that of wild-type cells, whether grown in the presence or absence of drug (doubling time of 13-14 h). In plating efficiency experiments, Olir 8.1 cells are approximately 100-fold more resistant to oligomycin than are wild-type cells. There is approximately a 32-fold increase in the resistance to inhibition by oligomycin of the mitochondrial ATPase from Olir 8.1 cells. The electron transport chain is functional in Olir 8.1 cells. Oligomycin resistance is stable in the absence of selective pressure. There is little or no cross-resistance of Olir 8.1 cells to venturicidin and dicyclohexylcarbodiimide, other inhibitors of the mitochondrial ATPase, or to chloramphenicol, an inhibitor of mitochondrial protein synthesis. Oligomycin resistance is dominant in hybrids between Olir 8.1 cells and wild-type cells. Fusions of enucleated Olir 8.1 cells with sensitive cells and characterization of the resulting "cybrid" clones indicates that oligomycin resistance in Olir 8.1 cells is cytoplasmically inherited.

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References

Horstman L, RACKER E . Partial resolution of the enzyme catalyzing oxidative phosphorylation. XXII. Interaction between mitochondrial adenosine triphosphatase inhibitor and mitochondrial adenosine triphosphatase. J Biol Chem. 1970; 245(6):1336-44. View

Tzagoloff A, Meagher P . Assesmbly of the mitochondrial membrane system. VI. Mitochondrial synthesis of subunit proteins of the rutamycin-sensitive adenosine triphosphatase. J Biol Chem. 1972; 247(2):594-603. View

Cattell K, Lindop C, Knight I, Beechey R . The identification of the site of action of NN'-dicyclohexylcarbodi-imide as a proteolipid in mitochondrial membranes. Biochem J. 1971; 125(1):169-77. PMC: 1178037. DOI: 10.1042/bj1250169. View

Stekhovan F, Waitkus R, van Moerkerk H . Identification of the dicyclohexylcarbodiimide-binding protein in the oligomycin-sensitive adenosine triphosphatase from bovine heart mitochondria. Biochemistry. 1972; 11(7):1144-50. DOI: 10.1021/bi00757a005. View

Avner P, Griffiths D . Studies on energy-linked reactions. Genetic analysis of oligomycin-resistant mutants of Saccharomyces cerevisiae. Eur J Biochem. 1973; 32(2):312-21. DOI: 10.1111/j.1432-1033.1973.tb02612.x. View

Shannon C, Enns R, Wheels L, Burchiel K, Criddle R . Alterations in mitochondrial adenosine triphosphatase activity resulting from mutation of mitochondrial deoxyribonucleic acid. J Biol Chem. 1973; 248(9):3004-11. View

Mitchell C, Bunn C, Lukins H, Linnane A . Biogenesis of mitochondria. 23. The biochemical and genetic characteristics of two different oligomycin resistant mutants of Saccharomyces cerevisiae under the influence of cytoplasmic genetic modification. J Bioenerg. 1973; 4(1):161-77. DOI: 10.1007/BF01516054. View

Bunn C, Wallace D, Eisenstadt J . Cytoplasmic inheritance of chloramphenicol resistance in mouse tissue culture cells. Proc Natl Acad Sci U S A. 1974; 71(5):1681-5. PMC: 388302. DOI: 10.1073/pnas.71.5.1681. View

Gillham N . Genetic analysis of the chloroplast and mitochondrial genomes. Annu Rev Genet. 1974; 8:347-91. DOI: 10.1146/annurev.ge.08.120174.002023. View

10.

Wigler M, Weinstein I . A preparative method for obtaining enucleated mammalian cells. Biochem Biophys Res Commun. 1975; 63(3):669-74. DOI: 10.1016/s0006-291x(75)80436-0. View

11.

Jackl G, Sebald W . Identification of two products of mitochondrial protein synthesis associated with mitochondrial adenosine triphosphatase from Neurospora crassa. Eur J Biochem. 1975; 54(1):97-106. DOI: 10.1111/j.1432-1033.1975.tb04118.x. View

12.

Foury F, Tzagoloff A . Localization on mitochondrial DNA of mutations leading to a loss of rutamycin-sensitive adenosine triphosphatase. Eur J Biochem. 1976; 68(1):113-9. DOI: 10.1111/j.1432-1033.1976.tb10769.x. View

13.

Koch G . Synthesis of the mitochondrial inner membrane in cultured Xenopus laevis oocytes. J Biol Chem. 1976; 251(19):6097-107. View

14.

Juliano R, Ling V . A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta. 1976; 455(1):152-62. DOI: 10.1016/0005-2736(76)90160-7. View

15.

Soderberg K, Ditta G, Scheffler I . Mammalian cells with defective mitochondrial functions: a Chinese hamster mutant cell line lacking succinate dehydrogenase activity. Cell. 1977; 10(4):697-702. DOI: 10.1016/0092-8674(77)90103-9. View

16.

Ditta G, Soderberg K, Landy F, Scheffler I . The selection of Chinese hamster cells deficient in oxidative energy metabolism. Somatic Cell Genet. 1976; 2(4):331-44. DOI: 10.1007/BF01538838. View

17.

Norwood T, Zeigler C, Martin G . Dimethyl sulfoxide enhances polyethylene glycol-mediated somatic cell fusion. Somatic Cell Genet. 1976; 2(3):263-70. DOI: 10.1007/BF01538964. View

18.

Ditta G, Soderberg K, Scheffler I . Chinese hamster cell mutant with defective mitochondrial protein synthesis. Nature. 1977; 268(5615):64-7. DOI: 10.1038/268064a0. View

19.

Sebald W . Biogenesis of mitochondrial ATPase. Biochim Biophys Acta. 1977; 463(1):1-27. DOI: 10.1016/0304-4173(77)90002-7. View

20.

Bunn C, Eisenstadt J . Carbomycin resistance in mouse L cells. Somatic Cell Genet. 1977; 3(6):611-27. DOI: 10.1007/BF01539069. View