Structure and Function of the H + -Translocating ATP Synthase of Energy-Coupling Membranes

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1 Module Membrane Biogenesis and Transport Lecture 12 Structure and Function of the H + -Translocating ATP Synthase of Energy-Coupling Membranes Dale Sanders 26 February 2009

2 Aims: By the end of the lecture you should understand The significance of hydropathy analysis; That the F 0 and F 1 sectors of the ATP synthase catalyse H + flow and ATP hydrolysis/synthesis, respectively; The fundamental subunit structure of each sector, and its significance for H + flow and ATP synthesis; The mechanism of ATP synthesis by rotational catalysis; The basic structure and function of Vacuolar H + -pumping ATPases.

3 Reading Lodish et al. (2004) Molecular Cell Biology pp is OK for the basics, but not very detailed. Voet & Voet (2004) Biochemistry pp More detailed account: Nakamoto et al. (2008) The rotary mechanism of the ATP synthase. Arch. Biochem. Biophys. 476:

4 Predicting Transmembrane Domains of Proteins with Hydropathy Analysis For most transport systems where 1 structure known, there are no data on 2 and 3 structure. Therefore use computer algorithm to predict transmembrane spans on the basis of dominantly hydrophobic character: Hydropathy Analysis Principles: 1. Hydrophobic polypeptide in hydrophopic environment adopts - helical conformation. 2. Hydrophobic span of bilayer 3 nm (30Å) 3. 3 nm of -helix 20 residues. 4. Assign a hydropathy index to each amino acid based on its oil: water partition coefficient values range from: (most hydrophobic: Ile) to 4.5 (most hydrophilic: Arg) 5. Search sequence for stretches of 20 residues which have overall hydropathy index >1

5 N C } windows of 20 residues Hydropathy index e.g. M subunit, Rhodopseudomonas Photosynthetic Reaction Centre Residue number calculate mean hydropathy index T/membr. spans

6 ATP Synthase of Energy Coupling Membranes: A Protein of Central Importance in Biology Question: What weight of ATP does a 70 kg human generate in a day? Answer: 75 kg!!!!

7 H + Translocation by the ATP Synthase of Energy Coupling Membranes: Basic Structure ATP synthase is located on N side of membrane. Can be visualised by negative staining or by cryo-em after 2D crystallization. P membrane N 8 nm 4 nm Direction of passive H + flow

8 Cryo-EM of sub-mitochondrial particles

9 Properties of this macromolecular complex in mitochondria: Remove Ca 2+ from solution and head-piece drops off. Find large amount of solublized ATPase activity. Importantly: In these conditions, membranes retain their capacity for electron transport after removal of head-piece. They are uncoupled: - respiratory rate increases - membrane leaky to H +

10 Function: From these results we can conclude that the two sectors of the enzyme have different roles in ATP synthesis Solubilized head-pieces catalysing ATP hydrolysis can be added back to stripped smp s (in presence of Ca 2+ ): 1. in presence of a PMF they synthesize ATP: smp s are coupled. 2. if resp. chain is blocked, and ATP is provided, the whole complex pumps H +.

11 i.e. (1) (2) Driving reaction in red ADP+P i H + ADP+P i H + H + ATP Conclusions: The ATPase is REVERSIBLE: a pump or a synthase The head-piece is involved in ATP synthesis/hydrolysis The head-piece is called F 1 The stalk forms a H + channel, which is open in the absence of F 1. Stalk is called F o Generically known as F-TYPE ATPases Present on all energy-coupling membranes (mitos, thylakoids, prokaryote) H + ATP

12 Structure and Function of Subunits Most work on E. coli enzyme which has fewest sub-unit types: Encoded on unc operon M r = 540 k F 0 sector Subunit a b c Stoichiometry M r (k) Disposition in membrane: evidence from hydropathy analysis models for globular proteins studies with interfacial reagents cryoelectron microscopy

13 N C D/E 61 P N C N N C a b c Mechanism of H + flow: AN INTERESTING FACT ABOUT F 0 : D/E 61 on subunit c is essential Covalently binds inhibitor dicyclohexylcarbodiimide (DCCD) Just 1 DCCD bound per holoenzyme is sufficient for complete inhibition. Implications for H + Flow Through F 0 : H + translocation must involve all c subunits.

14 F 1 sector: Subunit Composition subunit α β γ ε stoichiometry M r (k ) α β γ bind ATP tightly, but non-catalytic: function unknown comprise catalytic binding sites for ATP runs through centre of 3 β 3 hexamer

15 3 β 3 γ complex has been crystallized, and shows alternating β array with γ in centre: β β β Also shows the 3 catalytic nucleotide-binding sites in different states simultaneously on each β subunit Open: Nothing bound Loose: ADP + P i bound Tight: ATP bound

16 Abrahams et al. (1994) Nature 370:

17 Abrahams et al. (1994) Nature 370:

18 Abrahams et al. (1994) Nature 370:

19 Abrahams et al. (1994) Nature 370:

20 How Does H+ Flow Through F0 Energise ATP Synthesis by F1? Putting together kinetic and structural data, the model of rotational catalysis has been developed: 1. H+ flows passively through channels provided jointly by subunit a and 1 of c subunits. 2. Movement of H+ drives rotation of a ring of c subunits [Recall: 1 DCCD bound inhibits catalysis completely] 3. γ is connected indirectly (via ε) to c ring, and also rotates

21 5. Subunits a, α and β are prevented from moving by subunits b (a stator ) 6. Rotation of γ drives each of catalytic sites through conformational change (O L T) The world s smallest motor!! Stator membrane b Rotor c ring a H+

22

23 Rotary Catalysis and Binding Site Conformation in F1 How ATP is Made 1. ADP + Pi bind freely to Loose binding site. 2. Rotation of γ conformational change, making the Loose site Tight. 3. In the Tight site ATP forms spontaneously. 4. The Tight site Opens and ATP is released, again as γ rotates.

24 ADP + Pi Energy ADP+Pi P AT Pi Pi P+ P+ AD AD AT P ADP+Pi ATP Cross (1994) Nature 370: Note: Energy put into driving conformational changes in binding sites especially in Opening the Tight site to get ATP off the surface of the enzyme. Stoichiometry: 4 H+/ATP = 12 H+ for full cycle.

25 H+ Flow and Rotary Catalysis

26 Vacuolar ATPases (V-ATPases) are Distant Cousins of F-ATPases Functions: H+ pumping INTO the lumen of cellular compartments e.g. lysosomes, Golgi, chromaffin granules, plant and fungal Vacuoles Physiological roles: H+ - coupled solute accumulation vesicle trafficking Also H+ pumping OUT of a few cell types e.g. osteoclasts Bone resorption intercalated cells of renal collecting tubule Urinary acidification Stoichiometry Structure 2H+/ATP Vo (= Fo) sector V1 (= F1) sector

27 Many subunit types, amongst which in V0, a 16 kda subunit 6 copies / holoenzyme N C Both N & C halves homologous to subunit c of F0 Evolved from gene duplication and fusion in V1, 70 Catalytic: β homologue & 60 kda subunits non-catalytic: α homologue 3 copies each

28 SUMMARY 1. Hydropathy analysis predicts transmembrane spans in sequences of membrane proteins. 2. ATP synthase composed of 2 sectors: Fo F1 H+-conducting ATP binding 3 subunit types 5 subunit types 3. ATP is synthesized by ROTARY CATALYSIS H+ flow through Fo drives rotation of subunits and conformational energy is transmitted to F1 driving each binding site through a series of affinity changes. 4. Vacuolar H+-ATPases in organelles are distantly related to F ATPases Function solely as PUMPS.

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