Structurefunction relationships of A-, F- and V-ATPases
1 FR 2.5 Biophysik, Universität des Saarlandes, D-66421 Homburg, Germany,
2 Department of Biology, University of Osnabrück, D-49069 Osnabrück, Germany,
3 Whitney Laboratory, University of Florida, St Augustine, FL 32080, USA and
4 Lehrstuhl für Mikrobiologie der Ludwig-Maximilians-Universität München, D-80638, München, Germany
*Author for correspondence (e-mail: ggrueber{at}med-rz.uni-saarland.de)
Accepted May 9, 2001
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Summary |
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Key words: A1Ao-ATPase, archaea-type ATPase, F1Fo-ATPase, H+ translocating vacuolar-type ATPase, V1-ATPase, small-angle X-ray scattering, Escherichia coli, Manduca sexta, Methanosarcina mazei.
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Introduction |
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A-, V- and F-ATPases consist of a mosaic of globular structural units, including domain and secondary structures, which also serve as functional units. Morphologically each of these enzymes has three components: a membrane-bound sector, Ao/Fo/Vo, which contains the ion channel, a central connecting stalk, and an approximately spherical assembly, A1/F1/V1, which contains the catalytic sites (Schäfer et al., 1999; Leslie and Walker, 2000; Forgac, 2000). Side-view projections of the F1Fo- (Wilkens and Capaldi, 1998) and V1Vo-ATPases (Boekema et al., 1997) show a second stalk (stator) as a fourth distinct feature extending from the Fo or Vo portion. In the case of the Escherichia coli F1 moiety the central stalk is composed of ec and
ec, which are the equivalent of
m in mitochondrial F1Fo, and the stator is formed by the
ec and b subunits (Pedersen et al., 2000). The bacterial
subunit (
ec) bears homology to one of the mitochondrial Fo subunits called OSCP (Table1). The mitochondrial F1
subunit (
m) has no counterpart in the bacterial F1Fo enzyme. The central element of the F1 complex, subunit
, has been shown to move relative to the
3ß3 complex during ATP hydrolysis (Capaldi et al., 1996; Junge et al., 1997; Masaike et al., 2000). This rearrangement is proposed to drive the motion of a ring of c914 subunits (Fillingame, 1996; Stock et al., 1999; Seelert et al., 2000; Stahlberg et al., 2001) in the Fo domain (Sambongi et al., 1999; Pänke et al., 2000; Tsunoda et al., 2001), each containing two transmembrane helices (Rastogi and Girvin, 1999).
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F1-ATPase: structure and subunit function |
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Arrangement of the stalk subunits
Neither the structural model of the bovine F1-ATPase (Abrahams et al., 1994) nor the subsequently determined structure of rat liver F1-ATPase (Bianchet et al., 1998), which includes almost all of the residues of the and ß subunits, include either the small subunits
m and
m, or approximately half of the
subunit residues. Subsequently, crystals containing all five subunits of the Escherichia coli F1-ATPase (
3:ß3:
:
ec:
ec) and the
3ß3
ec complex of the same organism have been obtained and diffracted to a resolution of 6.4Å and 4.4Å, respectively (Grüber et al., 1997; Hausrath et al., 1999). Besides the
and ß subunits and the known part of the coiled-coil
-helices of the MF1 the electron-density map at 4.4Å extends 12 and 20 residues, respectively, thereby adding 15Å to the length of the N-terminal
-helix and 23Å to the C-terminal helix of the
subunit (Hausrath et al., 1999). This structure reveals that
extends from the
3ß3 hexagon far enough to traverse the full length of the central stalk, in agreement with the refined crystal structure at 2.4Å resolution of the
ec-
ec complex from E. coli (Rodgers and Wilce, 2000) and the complete bovine F1-ATPase (Fig.1; Gibbons et al., 2000). In these structural models the
subunit is arranged in six
-helices and five ß-stranded ß-sheets (Rodgers and Wilce, 2000; Gibbons et al., 2000). The bottom of
is in contact with the external loops of c subunits (Watts et al., 1995; Watts et al., 1996); the entire
subunit makes up a coupling domain, which couples ATP hydrolysis with ion pumping (Capaldi et al., 1996; Junge et al., 1997). Adjacent to the bottom part of subunit
an additional density has been observed in the map obtained from crystals of the
3ß3
c10 subcomplex of yeast mitochondrial ATP synthase at a 3.9Å resolution (Stock et al., 1999) and the bovine F1 (Gibbons et al., 2000). In these densities the structure of the
ec subunit (Wilkens et al., 1995; Uhlin et al., 1997), the counterpart of the yeast (
ye; Giraud and Velours, 1994) and bovine
subunit (Fig.1;
m), has been modeled. Like subunit
ec, the subunits
ye and
m are composed of a C-terminal helixloophelix structure and an N-terminal 10-stranded ß-sandwich structure. However, the modeling of the
ec subunit indicates that the C terminus of the polypeptide is turned away from the bottom domain of the catalytic ß subunit. This domain is believed to be involved in the coupling of catalytic-site events (Capaldi et al., 1996; Grüber and Capaldi, 1996) along with
and
ec acting as a rotor (reviewed in Junge et al., 1997; Masaike et al., 2000; Tsunoda et al., 2001). This structural feature is in conflict with the model of the
ec-
ec subcomplex (Rodgers and Wilce, 2000), in which the
ec is located in close proximity to ß via its C-terminal
-helix and with its ß-sandwich barrel turned toward the bottom of
. As shown by cryo-electron microscopy (Gogol, 1994) and biochemical studies (Mendel-Hartwig and Capaldi, 1991; Wilkens and Capaldi, 1998), the
ec subunit can exist in different states in the complex depending upon whether ATP, MgATP or MgADP is bound to the enzyme (Mendel-Hartwig and Capaldi, 1991; Wilkens and Capaldi, 1998). Using E. coli F1 mutants with cysteine substitutions in the C termini of the
, ß and
ec subunits it has been shown that in the ATP-conformation, when the
and
ec subunits are linked to
subunits, the high-affinity site is completely closed with nucleotide unable to get in or out. In contrast, in the ADP-conformation, when the small subunits are linked to ß subunits, there is nucleotide exchange in and out from the high catalytic site (Grüber and Capaldi, 1996). Therefore, the question arises as to whether the arrangement of the equivalent to the bacterial
subunit in the yeast and bovine F1Fo complexes reflects a trapped state during its nucleotide-dependent movement.
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Structure and mechanism of the V1-ATPase |
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Two major advances have been made toward elucidating the quaternary structure of V1 during the past two years. First, the gross structure of the M. sexta midgut V1-ATPase was investigated by SAXS (Svergun et al., 1998b). The enzyme is highly elongated with a maximal length of about 220Å. The solution scattering data define a hydrated complex with a headpiece approximately 145Å in diameter and a stalk approximately 110Å in length (Fig.5). Second, image processing of electron micrographs of negatively stained V-ATPases from Clostridium fervidus (Boekema et al., 1998) and V1-ATPase from M. sexta (Radermacher et al., 1999) yielded two-dimensional structures at a resolution of 18Å and 24Å, respectively. A comparison of the independently identified structures (Boekema et al., 1998; Svergun et al., 1998b; Radermacher et al., 1999) revealed that the headpiece consists of a pseudo-hexagonal arrangement of six masses, surrounding a seventh mass. These six masses, which are assumed to consist of the major subunits A and B, are arranged in an alternating manner (Boekema et al., 1998; Svergun et al., 1998b). The first three-dimensional reconstruction of the V1 complex was determined at 32Å resolution from negatively stained preparations of the M. sexta V1-ATPase (Fig.2) (Grüber et al., 2000a). A striking feature of the reconstruction is the presence of six elongated lobes, approximately 20Å in diameter and 90Å in length, which are parallel to the threefold axis (Fig.2B). These lobes, which represent the alternating three copies each of subunits A and B, can be traced for most of the length of the V1-ATPase. The hexagonal barrel of subunits A and B encloses a core of approximately 40Å. In this model the V1 complex is barrel-shaped, being approximately 110Å high and 135Å wide. At both ends of the hexagonal barrel extensions can be observed. The extensions on one side (Fig.2A) are consistent with published two-dimensional average images of the V1Vo-ATPase from bovine brain clathrin-coated vesicles, where elongated features (Fig.2FH; as, ce) can be seen at the very top of the V1 domain (Wilkens et al., 1999). The extensions on the opposite side can be attributed to traces of the stalk, e.g. the extension visible in Fig.2B,C. The correspondence of dimensions of the hexagonal domain as determined by SAXS (see above) and electron microscopy indicate that the stalk is not completely resolved in the three-dimensional reconstruction, presumably due to absorption and drying of the V1 particle on the carbon film. However, a striking fact is that the shape and interdigitation of the A3B3 subunits, located around the periphery of the barrel, are in agreement with the three-dimensional model of the related F1-ATPase, derived from two- (Capaldi et al., 1992; Gogol, 1994) and three-dimensional crystals of this complex (Abrahams et al., 1994; Bianchet et al., 1998; Hausrath et al., 1999), in which the alternating subunits and ß interdigitate for the full length surrounding the
subunit.
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Copper chloride-mediated disulfide formation yielded further insight into the proximity of the M. sexta V1 subunits to each other and into their functional relationships. When the enzyme was incubated with 2mmoll-1 CaADP on ice before Cu2+ treatment, two bands with apparent molecular masses of 120 and 110kDa, consisting of the subunits A,E,F and B,H, respectively, were obtained. A B,H product did not occur when cross-linking was conducted in 2mmoll-1 CaATP on ice to slow down ATP hydrolysis, implying that subunit H moves away from B to the A,B interface (Fig.3). This interpretation is consistent with the model of the yeast V1-ATPase, in which subunit H was located at an interface of the nucleotide-binding subunits A and B (Tomashek et al., 1997). Moreover, in the presence of CaATP, two new bands with apparent molecular masses of 42 and 44kDa, and composed of the subunits E,G and E,F, respectively, were observed. A homologous cross-linked product consisting of subunits E and G was also been generated using dimethyl sulfoxide (Thomashek et al., 1997) and disuccinimidyl glutarate (Xu et al., 1999) as cross-linking reagents.
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Redox modulation as a regulation of V-ATPases
There is abundant evidence that V-ATPase activity is modulated by disulfide-bond formation (Feng and Forgac, 1992; Forgac, 2000). A mechanism of reversible disulfide-bond formation between cysteine residues (Cys254 and Cys532) of the catalytic A subunit was proposed to regulate the V-ATPase in vivo (Oluwatosin and Kane, 1995; Forgac, 2000). A mechanism was proposed in which disulfide bond formation is quickly followed by dissociation of the V1 and Vo complexes (Dschida and Bowman, 1995), implying that nucleotide-binding and hydrolysis in the A subunit of the V1 domain have to be linked by the stalk region to ion translocation in the membrane-bound Vo domain. Recently SAXS experiments showed that reducing the V1-ATPase of M. sexta leads to significant changes in the overall dimensions of the complex. The radius of gyration of the oxidized and reduced enzyme are 62±6Å and 58±6Å, respectively, whereas the maximum dimension of both complexes remains constant at 220±10Å (Grüber et al., 2000b). The shapes of both complexes (Fig.4) were determined ab initio at a resolution of 27Å by a simulated annealing procedure, based on a representation of the structure in terms of dummy atoms (Svergun, 1999). Both low-resolution structures have a characteristic mushroom-like shape with a central stalk of significant length, similar to the identified structures of the V1-ATPase from Clostridium fervidus (Boekema et al., 1998) and M. sexta (Svergun et al., 1998), using electron microscopy and SAXS, respectively. Comparison of the oxidized and reduced models indicates that the main conformational changes upon reduction take place in both the crown-like region at the very top of the globular headpiece, where the major subunits A and B are located, and in the elongated stalk. Both regions evolve into an arrow-like shape after reduction (Grüber et al., 2000b). Based on homology of the subunits A and B to the related F-ATPase subunits ß and , respectively (Nelson, 1992), whose N termini form a ß-barrel domain in a crown-like fashion (Bakhtiari et al., 1999), the conformational changes at the top of the V1-ATPase are presumably due to rearrangements in the N termini of the A and B subunits. As shown more recently by three-dimensional reconstructions of the related F1Fo-ATPase from E. coli, a crown-like shape, which is missing in the absence of the nucleotide (Böttcher et al., 2000), evolves upon binding of the non-cleavable nucleotide analogue AMP-PNP into the catalytic ß subunit. The appearance of the crown has been attributed to rearrangements in the N-terminal domains of the
and ß subunits, located at the very top of F1. Moreover, when AMP-PNP or ADP are bound to the catalytic site, subunit ß assumes its closed conformation, in which the adenine-binding pocket moves into close proximity with the phosphate-binding domain, the P-loop; it moves away when the binding-site is empty (open conformation), as shown by the crystallographic model of the
3ß3
subcomplex of bovine heart mitochondrial F1-ATPase (Abrahams et al., 1994). There is a striking similarity between the crown structure of the E. coli F1Fo-ATPase (Böttcher et al., 2000) that evolves after binding of AMP-PNP (closed conformation) and the crown-like feature that is observed in the oxidized V1-ATPase (Grüber et al., 2000b). In this state, the catalytic A subunit is proposed to be in a closed conformation (Forgac, 2000), and alters into a wedge-like shape after reduction of V1. In summary, the structural changes in the headpiece, upon reduction of the enzyme, correspond with alterations of the protuberance of the stalk into a wedge-like feature, which enables the enzyme to transmit the activating movements that take place in the V1 headpiece to the Vo complex.
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The archaeal A1-ATPase |
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Conclusions and future perspectives |
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Further evidence for a closer relationship between A- and V-ATPases than either has to F-ATPase is found by comparing Ao and Vo to Fo domains. Unlike the Fo domain (see above) the Vo and Ao domains contain only two membrane integral subunits, a (I in A1Ao-ATPases) and c (the so called proteolipid). There is a surprising variation in the number of proteolipid subunits: two additional proteolipid subunits, c' and c'', both of which have homology to subunit c (Stevens and Forgac, 1997) are found in some V-ATPases, the F-ATPase from the bacterium Acetobacterium woodii contains two 8-kDa proteolipid subunits, c2 and c3, and the A-ATPase from the archaeon Archeoglobus fulgidus contains two 8kDa proteolipids (Müller et al., 1999; Müller et al., 2001). Moreover, there is an astonishing variability in the size of the proteolipids in archaeal A-ATPases with two, four or six transmembrane helices and a variable number of conserved ionizable groups per monomer (Müller et al., 1999). A proteolipid with four transmembrane helices but only one ionizable group has recently been described in the bacterial F1Fo-ATPase from A. woodii (Aufurth et al., 2000). Regarding these remarkably complex machines there still remains the question of how the energy coupling between the proposed ion-gradient-driven motion within the Ao and Vo domains is coupled by their stalks to the reversal of the ATP-driven motion in A1 and V1 domains.
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Acknowledgments |
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