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Effects of organic solvents and tentoxin on enzyme-bound ATP synthesis in isolated chloroplast coupling factor 1

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Abstract

Isolated spinach CF1 (chloroplast coupling factor 1) forms enzyme-bound ATP without any supply of energy in the presence of high concentrations of Pi [Feldman and Sigman (1982) J Biol Chem 257: 1676-1683]. The final amount of CF1-bound ATP synthesized was increased greatly by 1,2-propanediol, and moderately by methanol, ethanol, and dimethyl sulfoxide, but decreased by glycerol and octyl glucoside. Methanol and ethanol greatly increased the initial rate of ATP synthesis, while 1,2-propanediol increased it only moderately. Low concentrations (10-8 -10-6 M) of tentoxin, which inhibit ATPase activity of isolated CF1, did not affect enzyme-bound ATP synthesis. However, high concentrations (>10-5 M) of tentoxin, which stimulate ATPase activity of isolated CF1, enhanced the initial rate of CF1-bound ATP synthesis without significant effect on the final amount of ATP synthesized in the presence of medium ADP. The substrate of enzyme-bound ATP synthesized came largely from tightly bound ADP, not medium ADP, and tentoxin did not affect this substrate profile. Tentoxin did not affect the binding of medium ADP to high affinity sites on CF1.

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References

  • Abrahams JP, Leslie AGW, Lutter R and Walker JE (1994) Structure at 2.8Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621-628

    Google Scholar 

  • Arntzen CJ (1972) Inhibition of photophosphorylation by tentoxin, a cyclic tetrapeptide. Biochim Biophys Acta 283: 539-542

    Google Scholar 

  • Avni A, Anderson JD, Holland N, Rochaix J-D, Gromet-Elhanan Z and Edelman M (1992) Tentoxin sensitivity of chloroplasts determined by codon 83 of β subunit of proton-ATPase. Science 257: 1245-1247

    Google Scholar 

  • Boyer PD (1989) A perspective of the binding change mechanism for ATP synthesis. FASEB J 3: 2164-2178

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254

    Google Scholar 

  • Bruist MF and Hammes GG (1981) Further characterization of nucleotide binding sites on chloroplast coupling factor one. Biochemistry 20: 6298-6305

    Google Scholar 

  • Dahse I, Pezennec S, Girault B, Berger B, André F and Liebermann B (1994) The interaction of tentoxin with CF1 and CF1-ε isolated from spinach chloroplast. J Plant Physiol 143: 615-620

    Google Scholar 

  • Durbin RD and Uchytil TF (1977) A survey of plant insensitivity to tentoxin. Phytopathology 67: 602-603

    Google Scholar 

  • Feldman RI and Boyer PD (1985) The role of tightly bound ADP on chloroplast ATPase. J Biol Chem 260: 13088-13094

    Google Scholar 

  • Feldman RI and Sigman DS (1982) The synthesis of enzyme-bound ATP by soluble chloroplast coupling factor 1. J Biol Chem 257: 1676-1683

    Google Scholar 

  • Feldman RI and Sigman DS (1983) The synthesis of ATP by the membrane-bound ATP synthase complex from medium 32Pi under completely uncoupled conditions. J Biol Chem 258: 12178-12183

    Google Scholar 

  • Fromme P, Dahse I and Gräber P (1992) Effect of tentoxin on the activation and on the catalytic reaction of reconstituted H+-ATPase from chloroplasts. Z Naturforsch 47c: 239-244

    Google Scholar 

  • Futai M, Noumi T and Maeda M (1989) ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu Rev Biochem 58: 111-136

    Google Scholar 

  • Girault G, Berger G, Galmiche J-M and Andre F (1988) Characterization of six nucleotide-binding sites on chloroplast coupling factor 1 and one site on its purified β subunit. J Biol Chem 263: 14690-14695

    Google Scholar 

  • Grubmeyer C, Cross RL and Penefsky HS (1982) Mechanism of ATP hydrolysis by beef heart mitochondrial ATPase. J Biol Chem 257: 12092-12100

    Google Scholar 

  • Hansch C, Quinlan JE and Lawrence GL (1968) The linear freeenergy relationship between partition coefficients and the aqueous solubility of organic liquids. J Org Chem 33: 347-350

    Google Scholar 

  • Hisabori T and Sakurai H (1984) Relation between ultra-violet spectral change and nucleotide binding of the chloroplast coupling factor 1. Plant Cell Physiol 25: 483-493

    Google Scholar 

  • Hisabori T and Sakurai H (1985) Effect of methanol on the nucleotide binding to high-affinity sites on chloroplast coupling factor 1. Plant Cell Physiol 26: 505-514

    Google Scholar 

  • Hu D, Fiedler HR, Golan T, Edelman M, Strotmann H, Shavit N and Leu S (1997) Catalytic properties and sensitivity to tentoxin of Chlamydomonas reinhardtii ATP synthases changed in codon 83 of atpB by site-directed mutagenesis. J Biol Chem 272: 5457-5463

    Google Scholar 

  • Hu N, Mills DA, Huchzermeyer B and Richter ML (1993) Inhibition by tentoxin of cooperativity among nucleotide binding sites on chloroplast coupling factor 1. J Biol Chem 268: 8536-8540

    Google Scholar 

  • Krall AR and Purvis MR (1961) A study of nucleotide acceptor specificity of photophosphorylation by spinach chloroplasts. Arch Biochem Biophys 94: 14-19

    Google Scholar 

  • Leckband D and Hammes GG (1987) Interactions between nucleotide binding sites on chloroplast coupling factor 1 during ATP hydrolysis. Biochemistry 26: 2306-2312

    Google Scholar 

  • Mal'yan AN (1981) Chloroplasts ATPase (CF1): allosteric regulation by ADP and Mg2C ions. Photosynthetica 15: 474-483

    Google Scholar 

  • McCarty RE and Moroney JV (1985) Functions of the subunits and regulation of chloroplast coupling factor 1. In: Martonosi A (ed) The Enzymes of Biological Membranes, 2nd ed, pp 383-413. Plenum Publishing Corp., New York

    Google Scholar 

  • Mochimaru M and Sakurai H (1997) Threee kinds of binding site for tentoxin on isolated chloroplast coupling factor 1. FEBS Lett 419: 23-26

    Google Scholar 

  • Ohta Y, Yoshioka T, Mochimaru M, Hisabori T and Sakurai H (1993) Tentoxin inhibits both photophosphorylation in thylakoids and the ATPase activity of isolated coupling factor F1 from the cyanobacterium Anacystis nidulans. Plant Cell Physiol 34: 523-529

    Google Scholar 

  • Pedersen PL and Amzel LM (1993) ATP synthases. J Biol Chem 268: 9937-9940

    Google Scholar 

  • Penefsky HS (1977) Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase. J Biol Chem 252: 2891-2899

    Google Scholar 

  • Pick U and Bassilian S (1982) Activation of magnesium ion specific adenosinetriphosphatase in chloroplast coupling factor 1 by octyl glucoside. Biochemistry 21: 6144-6152

    Google Scholar 

  • Reimer S and Selman BR (1979) Tentoxin-induced binding of adenine nucleotides to soluble spinach chloroplast coupling factor 1. Biochim Biophys Acta 545: 415-423

    Google Scholar 

  • Richter ML, Gromet-Elhanan Z and McCarty RE (1986) Reconstitution of the H+-ATPase complex of Rhodospirillum rubrum by the β subunit of the chloroplast coupling factor 1. J Biol Chem 261: 12109-12113

    Google Scholar 

  • Sakamoto J and Tonomura Y (1983) Synthesis of enzyme-bound ATP by mitochondrial soluble F1-ATPase in the presence of dimethylsulfoxide. J Biochem 93: 1601-1614

    Google Scholar 

  • Sakurai H and Hisabori T (1987) Effects of organic solvents on the enzyme-bound ATP synthesis by isolated CF1. In: Biggins J (ed) Progress in Photosynthesis Research, Vol III, pp 13-16. Martinus Nijhoff Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Sakurai H, Hosoda T and Hisabori T (1990) Properties of the nucleotide-binding sites on isolated CF1. In: Baltscheffsky M (ed) Current Research in Photosynthesis Vol III, pp 73-76. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Sakurai H, Shinohara K, Hisabori T and Shinohara K (1981) Enhancement of adenosine triphosphatase activity of purified chloroplast coupling factor 1 in an aqueous organic solvent. J Biochem 90: 95-102

    Google Scholar 

  • Selman-Reimer S, Merchant S and Selman BR (1981) Isolation, purification, and characterization of coupling factor 1 from Chlamydomonas reinhardi. Biochemistry 20: 5476-5482

    Google Scholar 

  • Shapiro AB, Huber AH and McCarty RE (1991) Four tight nucleotide binding sites of chloroplast coupling factor 1. J Biol Chem 266: 4194-4200

    Google Scholar 

  • Sigalat C, Pitard B and Haraux F (1995) Proton coupling is preserved in membrane-bound chloroplast ATPase activated by high concentrations of tentoxin. FEBS Lett 368: 253-256

    Google Scholar 

  • Sokolov M and Gromet-Elhanan Z (1996) Spinach chloroplast coupling factor CF1-α3β3 core complex: Structure, stability, and catalytic properties. Biochemistry 35: 1242-1248

    Google Scholar 

  • Steele JA, Durbin RD, Uchytil TF and Rich DH (1978) An uncompetitive inhibitor of lettuce chloroplast coupling factor 1. Biochim Biophys Acta 501: 72-82

    Google Scholar 

  • Steele JA, Uchytil TF and Durbin RD (1978) The stimulation of coupling factor 1 ATPase by tentoxin. Biochim Biophys Acta 504: 136-141

    Google Scholar 

  • Vambutas VK and Racker E (1965) Partial resolution of the enzymes catalyzing photophosphorylation. J Biol Chem 240: 2660-2667

    Google Scholar 

  • Younis HM, Winget GD and Racker E (1977) Requirement of the δ subunit of chloroplast coupling factor 1 for photophosphorylation. J Biol Chem 252: 1814-1818

    Google Scholar 

  • Zhang S and Jagendorf AT (1995) Some unique characteristics of thylakoid unisite ATPase. J Biol Chem 270: 6607-6614

    Google Scholar 

Download references

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  1. Department of Biology, School of Education, Waseda University Nishiwaseda 1, Shinjuku, Tokyo 169-8050, Japan

    Mari Mochimaru & Hidehiro Sakurai

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  1. Mari Mochimaru
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  2. Hidehiro Sakurai
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Mochimaru, M., Sakurai, H. Effects of organic solvents and tentoxin on enzyme-bound ATP synthesis in isolated chloroplast coupling factor 1. Photosynthesis Research 57, 305–315 (1998). https://doi.org/10.1023/A:1005973801028

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