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The energy transmission in ATP synthase: From the γ-c rotor to the α3β3 oligomer fixed by OSCP-b stator via the βDELSEED sequence

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Abstract

ATP synthase (F0F1) is driven by an electrochemical potential of H+ (δΜH+). F0F1 is composed of an ion-conducting portion (F0) and a catalytic portion (F1). The subunit composition of F1 is α3β3γδε. The active α3β3 oligomer, characterized by X-ray crystallography, has been obtained only from thermnophilic F1 (TF1). We proposed in 1984 that ATP is released from the catalytic site (C site) by a conformational change induced by the βDELSEED sequence via γδε-F0. In fact, cross-linking of βDELSEED to γ stopped the ATP-driven rotation of γ in the center of α3β3. The torque of the rotation is estimated to be 420 pN·å from the δΜH+ and H+-current through F0F1. The angular velocity (Ω) of γ is the rate-limiting step, because δΜH+ increased theV max of H+ current through F0, but not theK m (ATP). The rotational unit of F0 (=ab2c10) is π/5, while that in α3β3 is 2π/3. This difference is overcome by an analog-digital conversion via elasticity around βDELSEED with a threshold to release ATP. The αβ distance at the C site is about 9.6 å (2,8-diN3-ATP), and tight Mg-ATP binding in α3β3γ was shown by ESR. The rotational relaxation of TF1 is too rapid (Φ=100 nsec), but the rate of AT(D)P-induced conformational change of α3β3 measured with a synchrotron is close to Ω. The ATP bound between the P-loop and βE188 is released by the shift of βDELSEED from γRGL. Considering the viscosity resistance and inertia of the free rotor (γ-c), there may be a stator containing OSCP (=δ of TF1) and F0-d to hold free rotation of α3β3.

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Abbreviations

F0F1 :

ATP synthase

F1 :

catalytic portion of F0F1

F0 :

ion-conducting portion of F0F1

α3β3γδε:

subunit composition of F1

C:

catalytic site

NC:

noncatalytic site

I:

ion-binding site in the c subunit of F0

DELSEED:

Asp-Glu-Leu-Ser-Glu-Glu-Asp- sequence in the N-terminal region of the β subunit of F1

P-loop:

-Gly-X-X-X-X-Gly-Lys-Thr- sequence of both the α and β subunit of F1

2-N3-AT(D)P:

2-azido-AT(D)P

2-N3-SL-AT(D)P:

2-azido-spin label AT(D)P

AMPPNP:

5′-adenylyl-imino diphosphate

BzAT(D)P:

3′-o-(4-benzoyl)benzoyl-AT(D)P

c10 :

decamer of the c subunit of F0

δΜH+ :

electrochemical potential difference of protons across the membrane

δψ:

electric potential difference (voltage) across the membrane

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  1. Department of Biochemistry, Jichi Medical School, 329-04, Tochigi-ken, Japan

    Yasuo Kagawa & Toshiro Hamamoto

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  1. Yasuo Kagawa
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  2. Toshiro Hamamoto
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Kagawa, Y., Hamamoto, T. The energy transmission in ATP synthase: From the γ-c rotor to the α3β3 oligomer fixed by OSCP-b stator via the βDELSEED sequence. J Bioenerg Biomembr 28, 421–431 (1996). https://doi.org/10.1007/BF02113984

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