|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online May 15, 2009
Journal of Experimental Biology 212, 1604-1610 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025866
Review Article |
The little we know on the structure and machinery of V-ATPase
Biochemistry Department, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel
* Author for correspondence (e-mail: nelson{at}post.tau.ac.il)
Accepted 21 January 2009
 |
Summary |
|---|
 TOP Summary IntroductionReferences |
|---|
Key words: V-ATPase, secretory pathway, membrane proteins, mechanism of action, structure
|
Introduction |
|---|
|
TOPSummaryIntroductionReferences |
|---|
). In
contrast to F-ATPase, the primary function of which, in eukaryotic cells, is
to form ATP at the expense of the proton motive force (pmf), V-ATPase
functions exclusively as the ATP-dependent proton pump. The pmf generated by
V-ATPase is utilized as a driving force for numerous secondary transport
processes (Beyenbach and Wieczorek,
2006; Hirata et al.,
1997; Nelson and Harvey,
1999). V-ATPase functions in various organelles such as endosomes,
lysosomes, Golgi membranes, several types of secretory granules,
clathrin-coated vesicles and the central vacuoles of plants and yeast
(Anderson and Orci, 1988;
Nelson and Harvey, 1999;
Nishi and Forgac, 2002). Each
of these intracellular compartments has a specific requirement for the
internal pH that is generated by the V-ATPase
(Nelson et al., 2000),
moreover, V-ATPase may act as a sensor of their internal pH
(Hurtado-Lorenzo et al.,
2006). In a single cell, V-ATPases can be involved in a variety of
essential cellular functions such as receptor-mediated endocytosis,
posttranslational secondary transport
(Nelson, 2003;
Nelson and Harvey, 1999;
Sun-Wada et al., 2004) and in
the fusion of certain organelles with the plasma membrane
(Morel, 2003). V-ATPases also
play a major role in the energizing of the plasma membranes, especially apical
plasma membranes of epithelial cells
(Beyenbach and Wieczorek, 2006;
Nelson and Harvey, 1999).
Because of its essential role in many cellular processes, it is expected that
V-ATPase will be present at high quantities in those membranes. However, most
of the isolated organelles and membranes contain small amounts of V-ATPase
(Nelson and Harvey, 1999).
This together with the low specific activity that was measured in
vitro represent a major challenge for the understanding of the function
of V-ATPase in the various organelles.
Eukaryotic V-ATPase can be divided into two structural domains
(Fig. 1): (1) a membrane-bound
260 kDa domain, Vo, composed of subunits a, d, e and the
proteolipids subunits c, c' and c'' with the stoichiometry of a1,
d, e, c4–5, c' and c'', and (2) a soluble domain,
V1, composed of subunits A, B, C, D, E, F, G and H with suggested
stoichiometry of A3, B3, C, D, E, F, G2,
H1–2 and total mass of 600–650 kDa
(Wang et al., 2007). Most of
the structural information about eukaryotic V-ATPase comes from electron
microscopy (Wilkens et al.,
2005) and structures of prokaryotic homologs. To date, only two
subunits of eukaryotic V-ATPase, C and H, have been determined by
high-resolution X-ray crystallography
(Drory et al., 2004a;
Sagermann et al., 2001). It is
the challenge for future research to come up with more high-resolution
structures to get a better view of the architecture of the enzyme so that its
mechanism of activity can be elucidated.
|
) (Fig. 1).
Despite the similarity between the two holoenzymes, their localization,
function and origin are different. In most cases F-ATPase is located in the
plasma membrane of eubacteria, in the thylakoid membrane of chloroplasts and
in the inner membrane of mitochondria. Its primary function is to synthesize
ATP at the expense of the pmf, which is generated by the electron transport
chains. By contrast, V-ATPase functions in eukaryotic plasma membranes as a
membrane energizing system and in the membranes of vesicles and organelles
mostly involved in the secretory pathway, as an interior acidifier
(Nelson and Harvey, 1999). The
origin of the eukaryotic F-ATPase is rooted in the eubacteria that evolved
into chloroplasts and mitochondria. Because its assembly requires gene
products of the organelles, it is confined to these organelles and shows no
contact with the cell cytoplasm (Nelson,
1992). The origin of V-ATPase is related to the F-ATPase of
Archaea (also called A-ATPase), and evolved in eukaryotes concomitantly with
the secretory pathway. In contrast to the F-ATPase, V-ATPase is necessary for
almost every eukaryotic cell, and except for yeast, the consequence of its
destruction is lethality (Nelson and
Harvey, 1999).
Looking closely into the structure of the two enzymes reveals a fundamental
difference in the composition of Vo and Fo. The
multimeric proteolipid subunit c (c-ring) of F-ATPase consists of 10–14
identical subunits (depending on the organism and organelle). Each subunit,
with a molecular mass of 8 kDa, consists of two transmembrane 
-helices.
Helix 2 contains a negatively charged amino acid in position 61 (in
Escherichia coli) that is essential for proton translocation
(Fillingame et al., 2003)
(Fig. 2A). The V-ATPase
proteolipid is homologous to the F-ATPase proteolipid but the former is twice
the size, 16 kDa, with four transmembrane -helices
(Mandel et al., 1988;
Nelson and Nelson, 1989). The
essential negatively charged glutamic acid in position 137 (in
Saccharomyces cerevisiae) which also binds
NN'-dicyclohexylcarbodi-imide (DCCD) is located in helix 4
(Fig. 2B).
|
). Subunits c' and c'' are homologous to subunit c
and consist of four and five transmembrane -helices, respectively
(Hirata et al., 1997). Null
mutation of subunit c'' (vma16
), like most of the null
mutations in yeast, results in a conditionally lethal phenotype
(Nelson and Nelson, 1990). It
was found that Vma16p from lemon fruit and Arabidopsis thaliana was
able to complement the yeast vma16 null mutant. Moreover,
sequence homology of subunit c'' between lemon fruit and yeast, reveals
high identity among -helices 2–5 (56%) but not with helix 1,
which is lacking in plants. These findings led us to suggest that in yeast,
helices 2–5 of subunit c'' are transmembrane and that the first
-helix is a cytoplasmic segment
(Aviezer-Hagai et al., 2003).
Taking into account the orientation of each proteolipid
(Flannery et al., 2004), a
series of gene fusion constructs between pairs of proteolipids was tested for
assembly and activity and the results suggested a particular asymmetric
arrangement of the proteolipid in the c-ring
(Wang et al., 2007). Subunit
c' locates counterclockwise to subunit c'' (as viewed from the
lumen) and the other copies of subunit c form the rest of the c-ring
(Fig. 2C). The question we may
ask is why V-ATPase needs such a large, multi-subunit, c-ring? We suggest that
the constraint that led to gene duplication resulted in a so called proton
slip mechanism (Moriyama and Nelson,
1988; Nelson et al.,
2002; Perzov et al.,
2001). This mechanism enables proton slippage in order to retain a
membrane potential of about 120 mV and avoid thermodynamic equilibrium (about
240 mV). If proton slippage does not occur, the membrane potential will reach
its maxima and ATP hydrolysis will cease.
Proton translocation from one side of the membrane to the other is assigned
to subunit a. In E. coli, F-ATPase subunit a is 30 kDa. It is a
highly hydrophobic protein consisting of five transmembrane -helices
(Vik and Ishmukhametov, 2005).
Eukaryotic V-ATPase subunit a is much larger, about 100 kDa, and consists of
two domains. The hydrophilic N-terminal domain and a large membrane-embedded,
highly hydrophobic domain that spans the membrane with eight -helices
(Wang et al., 2008). S.
cerevisiae contains two isoforms of subunit a, encoded by two genes:
VPH1 and STV1. Their gene products are usually assigned to
the vacuole (Vph1p), and to the Golgi and endosomes (Stv1p)
(Manolson et al., 1994). This
suggests that the isoforms are responsible for enzyme localization. In
contrast to other V-ATPase subunits, VPH1 or STV1 null
mutants can grow on a pH 7.5 medium (the double mutant is lethal). We have
shown that the vph1 mutant has an high levels of STV1 and that
purified vacuoles contain assembled V-ATPase complexes (not contaminated with
endosomal V-ATPase). In addition, the amount of proton pumping was measurable
(Perzov et al., 2002).
Cold inactivation
The purification process of the VoV1 complex must be
delicate and fast because of the high sensitivity of the enzyme, in particular
to cold. Incubation of reconstituted VoV1 complexes
purified from chromaffin granules at 0°C in the presence of
Mg2+, Cl– and ATP resulted in a reduction of the
ATPase activity and proton translocation. It was found that 0.1 mmol
l–1 MgATP and 0.2 mol l–1 NaCl cause maximal
inhibition. Similar results were found with V-ATPase of clathrin-coated
vesicles, synaptic vesicles, kidney microsomes, red beet vacuoles and tomato
vacuoles. The reason for the decline of the enzyme activity was the release of
five polypeptides from the complex, which were found to be part of
V1 (Moriyama and Nelson,
1989). Later on, in vivo studies discovered that
depletion of glucose and elevated amount of NaCl in the growth medium (in
yeast) and molting (in insects), results in a reversible dissociation of
V1 (Kane, 1995;
Perzov et al., 2001;
Sumner et al., 1995).
It was suggested that the dissociation of V1 is a result of the
release of the unique subunit C which serves as a link between Vo
and V1 and that this phenomena is part of enzyme regulation
(Beyenbach and Wieczorek,
2006). The dissociated V1 was found to be not active,
furthermore the membrane bound Vo was not able to translocate
protons (Beltran and Nelson,
1992). We suggest that if the Vo were to keep its
proton conductivity intact after the V1 dissociation, the organism
would be doomed under cold and other stress conditions.
Mechanism of action
It is accepted that F-ATPase and V-ATPase share similar mechanisms of
action. Is this correct? Is the conventional mechanism for ATP hydrolysis
correct? These two naive questions arise from the following facts.
The first crystal structure of bovine heart mitochondrial
F1-ATPase was presented by the Walker group
(Abrahams et al., 1994). The
structure revealed a hexagonal, asymmetric catalytic unit, in which each
β-catalytic site had different conformations. One catalytic site was
occupied by AMP-PNP (adenylyl-imidodiphosphate), a non-hydrolysable analogue
of ATP, the second was occupied by ADP and the last was empty. It was
suggested that the conformational change is a consequence of the rotation of
-subunit. This structure fits with Boyer's `binding change mechanism'
which suggests that the three catalytic sites have different nucleotide
affinities (Boyer, 1993). A
series of F1-ATPase structures was published subsequently
supporting these findings, but some of them raise doubt. There are few
F1-ATPase structures that do not have classical binding change
mechanism properties. F1-ATPase from rat liver mitochondria was
found to have a symmetrical hexagonal structure with all three catalytic sites
occupied by nucleotides (Bianchet et al.,
1998). F1-ATPase from the thermophilic
Bacillus PS3 had a symmetrical hexagonal structure with no
nucleotides bound to the catalytic sites
(Shirakihara et al., 1997).
Another example is the F1-ATPase from spinach chloroplasts. Here,
the catalytic sites adopt closed conformation, with no nucleotide binding, to
form a symmetrical hexagonal structure
(Groth and Pohl, 2001).
Collectively, these results may suggest that some of the reported structures
are not well resolved. However, there are other possibilities such as
crystallographic constrains that have to be kept in mind.
|
-subunit or the c-ring
(Noji et al., 1997;
Omote et al., 1999;
Panke et al., 2000).
Amazingly, the fact that less than 1% of the total fixed F-ATPase molecules
exhibited rotation was totally neglected. Is it possible that the rotating
F-ATPase molecules were chemically modified by processes such as proteolytic
digestion of one of the subunits? Even if we take the rotation experiments at
face value, some discrepancies between the structural information and the
rotation mechanism were reported (Sielaff
et al., 2008). Can we adopt the wealth of information obtained for
F-ATPase to explain the mechanism of action of eukaryotic V-ATPase? Only time
will tell.
Structural biology
Studying the structure of the entire VoV1 complex
requires a concerted effort of various analytical methods such as electron
microscopy (EM), small angle X-ray scattering (SAXS), X-ray crystallography,
etc. The combination of these methods in addition to biochemical methods such
as cross linking assays, localization assays and purification processes may
advance our understanding of the structure of V-ATPase.
The increasing use of electron microscopy provides a picture of the
holoenzyme. Low resolution structures of V-ATPase from mammals, yeast and
plants reveal a general architecture resembling F-ATPase. The complex is
cylindrical with overall dimension of 28 nmx14 nmx14 nm. The two
major domains, the 6.5 nm Vo and the 9 nm V1 are
connected by a 6 nm stalk (Domgall et al.,
2002; Harrison et al.,
2003; Wilkens et al.,
1999; Wilkens et al.,
2005; Zhang et al.,
2003). Electron density maps can be used to identify the docking
of high resolution structures of a single subunit (or complexes) from
eukaryotic and prokaryotic V-ATPase, and thus a structural model can be built.
The next level of structure determination is achieved by high resolution
three-dimensional structure. Here we can deduce and understand both the
structure and functionality of the protein. Unlike F-ATPase, there is no
structure evidence of a soluble domain or a membrane embedding domain in the
eukaryotic V-ATPase. Notwithstanding, with the relatively minor structural
information from single subunit structures of the eukaryotic V-ATPase or its
bacterial and archaeal homologs (Table
1), we are trying to learn about the mode of action of the enzyme,
the function of each subunit and the interaction between them (reviewed by
Drory and Nelson, 2006b).
|
Structures related to V1
The crystal structure of the unique V-ATPase subunit C (Vma5p) from S.
cerevisiae was determined at 1.75 Å resolution in our laboratory a
few years ago (Drory et al.,
2004a; Drory et al.,
2004b; Drory and Nelson,
2006b). It has three distinct domains: an upper globular domain,
the `head', an elongated domain, the `neck', and a lower globular domain, the
`foot' (Fig. 3A). We suggest
that the protein head domain is attached to the catalytic sector and the
`foot' and the neck' domains interact with the membrane domain and act as a
stator. Disassembly of the C subunit during glucose depletion or cold
treatment followed by the dissociation of the V1 from
Vo, support the notion of a static connection between the catalytic
and the membrane sectors (Beyenbach and
Wieczorek, 2006). A second crystal structure was determined at 2.9
Å resolution. This structure is highly similar to the first, with the
foot and lower neck domain but a large movement of the head domain was found.
This phenomenon leads us to attribute a flexible ratchet property to this
stator. We also found a remarkable similarity between subunit C foot and head
domains and the actin binding protein from the gelsolin family. Moreover,
V-ATPase was found to bind F and G actin with high affinity and it also leads
to cross linking of actin filaments
(Vitavska et al., 2003).
Taking all together, we modeled the interaction between actin filaments and
subunit C and we found that actin can bind both head and foot domains without
any interference between the two (Drory and
Nelson, 2006a).
The structure of subunit H (S. cerevisiae, Vma13P) was determent
at 2.95 Å resolution (Sagermann et
al., 2001). It is an -helical, elongated structure with two
distinct domains connected by four residues, probably a flexible loop
(Fig. 3B). It has five HEAT
motifs (also called armadillo motifs) similar to the karyopherins family, a
nuclear localization signal (NLS) binding protein. This similarity may suggest
that subunit H binds other proteins using a similar mechanism to the
karyoproteins, and may also provide an indication for the regulation
properties of ATPase activity that are attributed to this subunit.
Prokaryotic V-ATPase subunit F (Vma7p) is known to function in ATPase
activity and in the association of V1 with Vo. The
crystal structure of subunit F was determined at 2.2 Å resolution from
the archaean Thermus thermophilus
(Makyio et al., 2005). The
N-terminal and the C-terminal domains are composed of an /β-fold
and they are connected with a flexible loop
(Fig. 3C). In addition to the
crystal structure, single pair fluorescence resonance energy transfer (FRET)
analysis indicates that subunit F exist in two conformations, `extended' and
`retracted', depending on the presence and absence of ATP, respectively.
Moreover, it supports the idea that only one copy of subunit F exist in the
V-ATPase complex.
Archeal V-ATPase subunit B, the non-catalytic subunit in the catalytic
domain, shares a 58% identity with its S. cerevisiae homolog, subunit
B. Its structure was determined at 1.5 Å resolution from the archaean
Methanosarcina mazei (Schafer et
al., 2006). Subunit B is 80 Å long and 50 Å wide. It
consists of three domains: a six-strand β-barrel N-terminal domain, an
intermediate domain composed of /β-fold and an -helical
C-terminal domain (Fig. 3D). It
has been shown that this regulatory subunit can bind nucleotides, but as in
eukaryotic subunit B the nucleotide binding site, the P-loop, does not exist
in the conserved position as in subunit of F-ATPase, and both
counterparts share identical sequence it the apparent P-loop position. The
question whether this shared identical sequence binds nucleotides in both
prokaryotic and eukaryotic V-ATPase is still open. Co-crystallization of
prokaryotic subunit B with nucleotides may answer this question.
Structures related to Vo
Prokaryotic subunit C shares low but significant sequence similarity (18%)
with its yeast homologous subunit d (Vma6p). It is solely ascribed to
V-ATPase, and it is located at the central stalk. The structure of subunit C
was determined first from the eubacterium T. thermophilus at 1.95
Å resolution (Iwata et al.,
2004) and subsequently, at 1.85 Å resolution
(Numoto et al., 2004). Subunit
C is funnel shaped with dimensions of 45 Åx50 Åx50
Å. It is mainly -helical and consists of three similarly
structured domains (Fig. 3E).
The lower central region of the protein is about 30 Å in diameter, which
matches the 30 Å diameter cavity of the c-ring of E. coli.
Moreover, the structure reveals a positively charged amino acid region, mainly
lysine, at the lower central region, which may interact with the negatively
charged glutamic acid of the L subunit (part of the membrane embedded L-ring,
the homolog of F-ATPase and V-ATPase subunit c). Recently a low resolution
structure of subunit d from S. cerevisiae V-ATPase was determined
from solution X-ray scattering data. According to these findings, subunit d is
a boxing glove shape with two distinct domains
(Thaker et al., 2007). These
data contradict the suggested structural similarity between subunit C of
T. thermophilus and subunit d from S. cerevisiae. Therefore,
the question of whether prokaryotic subunit C and eukaryotic subunit d are
homologous and share similar function remains unanswered.
Na+-dependent vacuolar ATPase is a close relative of the
eukaryotic V-ATPase. The structure of its ring (K-ring) was determined from
the prokaryotic Enterococcus hire at 2.1 Å resolution
(Murata et al., 2005). The
ring consists of 10 similar subunits, encoded by the same gene, NtpK.
Each subunit contains five -helices, H0–H4. The first
-helix (H0) is cytoplasmic and the other four -helices
(H1–H4) are transmembrane. Similar to its eukaryotic homolog, the
essential negatively charged glutamic acid is placed in H4 in position 137,
which blocks the Na+ atom within the binding pocket
(Fig. 3F). The ring dimensions
are 68 Å in length and 83 Å maximal diameter. As expected from
sequence similarity, the ring length is similar to the S. cerevisiae
and Ilyobacter tartaricus F-ATPase c-ring, 58 Å and 70 Å,
respectively (Meier et al.,
2005; Stock et al.,
1999). Interestingly, the ring maximal diameter is much larger the
F-ATPase homologs, 55 Å and 50 Å, respectively). These differences
may reflect differences in the association of the ring with the central
stalk.
Despite the primary structure similarity and the apparent resemblance in architecture, the understanding of the exact structure and the mode of action of each subunit within the eukaryotic V-ATPase c-ring is yet to be determined.
At this point we would like to emphasize that at the time of submission of this review, the high resolution structure of the membrane-embedded proton channel (subunit a in V-ATPase and F-ATPase) has not been determined. Such structural information will facilitate the understanding of the proton translocation mechanism and as a consequence the clarification of the mechanism of energy conversion by the mechano-chemical machines of F- and V-ATPases.
|
Footnotes |
|---|
|
References |
|---|
|
TOPSummaryIntroductionReferences |
|---|
Abrahams, J. P., Leslie, A. G., Lutter, R. and Walker, J. E. (1994). Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370,621 -628.[CrossRef][Medline]
Anderson, R. G. and Orci, L. (1988). A view of
acidic intracellular compartments. J. Cell Biol.
106,539
-543.
Aviezer-Hagai, K., Padler-Karavani, V. and Nelson, N.
(2003). Biochemical support for the V-ATPase rotary mechanism:
antibody against HA-tagged Vma7p or Vma16p but not Vma10p inhibits activity.
J. Exp. Biol. 206,3227
-3237.
Beltran, C. and Nelson, N. (1992). The membrane sector of vacuolar H(+)-ATPase by itself is impermeable to protons. Acta Physiol. Scand. Suppl. 607, 41-47.[Medline]
Beyenbach, K. W. and Wieczorek, H. (2006). The
V-type H+ ATPase: molecular structure and function, physiological
roles and regulation. J. Exp. Biol.
209,577
-589.
Bianchet, M. A., Hullihen, J., Pedersen, P. L. and Amzel, L.
M. (1998). The 2.8-A structure of rat liver F1-ATPase:
configuration of a critical intermediate in ATP synthesis/hydrolysis.
Proc. Natl. Acad. Sci. USA
95,11065
-11070.
Boyer, P. D. (1993). The binding change mechanism for ATP synthase-some probabilities and possibilities. Biochim. Biophys. Acta 1140,215 -250.[Medline]
Domgall, I., Venzke, D., Luttge, U., Ratajczak, R. and Bottcher,
B. (2002). Three-dimensional map of a plant V-ATPase based on
electron microscopy. J. Biol. Chem.
277,13115
-13121.
Drory, O. and Nelson, N. (2006a). The emerging structure of vacuolar ATPases. Physiology (Bethesda) 21,317 -325.[CrossRef][Medline]
Drory, O. and Nelson, N. (2006b). Structural and functional features of yeast V-ATPase subunit C. Biochim. Biophys. Acta 1757,297 -303.[Medline]
Drory, O., Frolow, F. and Nelson, N. (2004a). Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5,1148 -1152.[CrossRef][Medline]
Drory, O., Mor, A., Frolow, F. and Nelson, N. (2004b). Expression, crystallization and phasing of vacuolar H(+)-ATPase subunit C (Vma5p) of Saccharomyces cerevisiae. Acta Crystallogr. D Biol. Crystallogr. 60,1906 -1909.[CrossRef][Medline]
Fillingame, R. H., Angevine, C. M. and Dmitriev, O. Y. (2003). Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 555, 29-34.[CrossRef][Medline]
Flannery, A. R., Graham, L. A. and Stevens, T. H.
(2004). Topological characterization of the c, c', and c"
subunits of the vacuolar ATPase from the yeast Saccharomyces cerevisiae.
J. Biol. Chem. 279,39856
-39862.
Girvin, M. E., Rastogi, V. K., Abildgaard, F., Markley, J. L. and Fillingame, R. H. (1998). Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry 37,8817 -8824.[CrossRef][Medline]
Groth, G. and Pohl, E. (2001). The structure of
the chloroplast F1-ATPase at 3.2 A resolution. J. Biol.
Chem. 276,1345
-1352.
Harrison, M., Durose, L., Song, C. F., Barratt, E., Trinick, J., Jones, R. and Findlay, J. B. (2003). Structure and function of the vacuolar H+-ATPase: moving from low-resolution models to high-resolution structures. J. Bioenerg. Biomembr. 35,337 -345.[CrossRef][Medline]
Hirata, R., Graham, L. A., Takatsuki, A., Stevens, T. H. and
Anraku, Y. (1997). VMA11 and VMA16 encode second and third
proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane
H+-ATPase. J. Biol. Chem.
272,4795
-4803.
Hurtado-Lorenzo, A., Skinner, M., El Annan, J., Futai, M., Sun-Wada, G. H., Bourgoin, S., Casanova, J., Wildeman, A., Bechoua, S., Ausiello, D. A. et al. (2006). V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 8,124 -136.[CrossRef][Medline]
Iwata, M., Imamura, H., Stambouli, E., Ikeda, C., Tamakoshi, M.,
Nagata, K., Makyio, H., Hankamer, B., Barber, J., Yoshida, M. et al.
(2004). Crystal structure of a central stalk subunit C and
reversible association/dissociation of vacuole-type ATPase. Proc.
Natl. Acad. Sci. USA 101,59
-64.
Kane, P. M. (1995). Disassembly and reassembly
of the yeast vacuolar H(+)-ATPase in vivo. J. Biol.
Chem. 270,17025
-17032.
Makyio, H., Iino, R., Ikeda, C., Imamura, H., Tamakoshi, M., Iwata, M., Stock, D., Bernal, R. A., Carpenter, E. P., Yoshida, M. et al. (2005). Structure of a central stalk subunit F of prokaryotic V-type ATPase/synthase from Thermus thermophilus. EMBO J. 24,3974 -3983.[CrossRef][Medline]
Mandel, M., Moriyama, Y., Hulmes, J. D., Pan, Y. C., Nelson, H.
and Nelson, N. (1988). cDNA sequence encoding the 16-kDa
proteolipid of chromaffin granules implies gene duplication in the evolution
of H+-ATPases. Proc. Natl. Acad. Sci. USA
85,5521
-5524.
Manolson, M. F., Wu, B., Proteau, D., Taillon, B. E., Roberts,
B. T., Hoyt, M. A. and Jones, E. W. (1994). STV1 gene encodes
functional homologue of 95-kDa yeast vacuolar H(+)-ATPase subunit Vph1p.
J. Biol. Chem. 269,14064
-14074.
Meier, T., Polzer, P., Diederichs, K., Welte, W. and Dimroth,
P. (2005). Structure of the rotor ring of F-Type
Na+-ATPase from Ilyobacter tartaricus.
Science 308,659
-662.
Morel, N. (2003). Neurotransmitter release: the dark side of the vacuolar-H+ATPase. Biol. Cell 95,453 -457.[CrossRef][Medline]
Moriyama, Y. and Nelson, N. (1988). The vacuolar H+-ATPase, a proton pump controlled by a slip. Prog. Clin. Biol. Res. 273,387 -394.[Medline]
Moriyama, Y. and Nelson, N. (1989). Cold
inactivation of vacuolar proton-ATPases. J. Biol.
Chem. 264,3577
-3582.
Murata, T., Yamato, I., Kakinuma, Y., Leslie, A. G. and Walker,
J. E. (2005). Structure of the rotor of the V-Type
Na+-ATPase from Enterococcus hirae. Science
308,654
-659.
Nelson, H. and Nelson, N. (1989). The progenitor of ATP synthases was closely related to the current vacuolar H+-ATPase. FEBS Lett. 247,147 -153.[CrossRef][Medline]
Nelson, H. and Nelson, N. (1990). Disruption of
genes encoding subunits of yeast vacuolar H(+)-ATPase causes conditional
lethality. Proc. Natl. Acad. Sci. USA
87,3503
-3507.
Nelson, N. (1992). Evolution of organellar proton-ATPases. Biochim. Biophys. Acta 1100,109 -124.[CrossRef][Medline]
Nelson, N. (2003). A journey from mammals to yeast with vacuolar H+-ATPase (V-ATPase). J. Bioenerg. Biomembr. 35,281 -289.[CrossRef][Medline]
Nelson, N. and Harvey, W. R. (1999). Vacuolar
and plasma membrane proton-adenosine triphosphatases. Physiol.
Rev. 79,361
-385.
Nelson, N., Perzov, N., Cohen, A., Hagai, K., Padler, V. and Nelson, H. (2000). The cellular biology of proton-motive force generation by V-ATPases. J. Exp. Biol. 203, 89-95.[Abstract]
Nelson, N., Sacher, A. and Nelson, H. (2002). The significance of molecular slips in transport systems. Nat. Rev. Mol. Cell Biol. 3,876 -881.[CrossRef][Medline]
Nishi, T. and Forgac, M. (2002). The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3,94 -103.[CrossRef][Medline]
Noji, H., Yasuda, R., Yoshida, M. and Kinosita, K., Jr (1997). Direct observation of the rotation of F1-ATPase. Nature 386,299 -302.[CrossRef][Medline]
Numoto, N., Kita, A. and Miki, K. (2004). Structure of the C subunit of V-type ATPase from Thermus thermophilus at 1.85 A resolution. Acta Crystallogr. D Biol. Crystallogr. 60,810 -815.[CrossRef][Medline]
Omote, H., Sambonmatsu, N., Saito, K., Sambongi, Y.,
Iwamoto-Kihara, A., Yanagida, T., Wada, Y. and Futai, M.
(1999). The gamma-subunit rotation and torque generation in
F1-ATPase from wild-type or uncoupled mutant Escherichia coli.Proc. Natl. Acad. Sci. USA
96,7780
-7784.
Panke, O., Gumbiowski, K., Junge, W. and Engelbrecht, S. (2000). F-ATPase: specific observation of the rotating c subunit oligomer of EF(o)EF(1). FEBS Lett. 472, 34-38.[CrossRef][Medline]
Perzov, N., Padler-Karavani, V., Nelson, H. and Nelson, N. (2001). Features of V-ATPases that distinguish them from F-ATPases. FEBS Lett. 504,223 -228.[CrossRef][Medline]
Perzov, N., Padler-Karavani, V., Nelson, H. and Nelson, N.
(2002). Characterization of yeast V-ATPase mutants lacking Vph1p
or Stv1p and the effect on endocytosis. J. Exp. Biol.
205,1209
-1219.
Powell, B., Graham, L. A. and Stevens, T. H.
(2000). Molecular characterization of the yeast vacuolar
H+-ATPase proton pore. J. Biol. Chem.
275,23654
-23660.
Sagermann, M., Stevens, T. H. and Matthews, B. W.
(2001). Crystal structure of the regulatory subunit H of the
V-type ATPase of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci.
USA 98,7134
-7139.
Schafer, I. B., Bailer, S. M., Duser, M. G., Borsch, M., Bernal, R. A., Stock, D. and Gruber, G. (2006). Crystal structure of the archaeal A1Ao ATP synthase subunit B from Methanosarcina mazei Go1: Implications of nucleotide-binding differences in the major A1Ao subunits A and B. J. Mol. Biol. 358,725 -740.[CrossRef][Medline]
Shirakihara, Y., Leslie, A. G., Abrahams, J. P., Walker, J. E., Ueda, T., Sekimoto, Y., Kambara, M., Saika, K., Kagawa, Y. and Yoshida, M. (1997). The crystal structure of the nucleotide-free alpha 3 beta 3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer. Structure 5,825 -836.[Medline]
Sielaff, H., Rennekamp, H., Engelbrecht, S. and Junge, W. (2008). Functional halt positions of rotary FOF1-ATPase correlated with crystal structures. Biophys. J. 95,4979 -4987.[CrossRef][Medline]
Stock, D., Leslie, A. G. and Walker, J. E.
(1999). Molecular architecture of the rotary motor in ATP
synthase. Science 286,1700
-1705.
Sumner, J. P., Dow, J. A., Earley, F. G., Klein, U., Jager, D.
and Wieczorek, H. (1995). Regulation of plasma membrane
V-ATPase activity by dissociation of peripheral subunits. J. Biol.
Chem. 270,5649
-5653.
Sun-Wada, G. H., Wada, Y. and Futai, M. (2004). Diverse and essential roles of mammalian vacuolar-type proton pump ATPase: toward the physiological understanding of inside acidic compartments. Biochim. Biophys. Acta 1658,106 -114.[Medline]
Thaker, Y. R., Roessle, M. and Gruber, G. (2007). The boxing glove shape of subunit d of the yeast V-ATPase in solution and the importance of disulfide formation for folding of this protein. J. Bioenerg. Biomembr. 39,275 -289.[CrossRef][Medline]
Vik, S. B. and Ishmukhametov, R. R. (2005). Structure and function of subunit a of the ATP synthase of Escherichia coli. J. Bioenerg. Biomembr. 37,445 -449.[CrossRef][Medline]
Vitavska, O., Wieczorek, H. and Merzendorfer, H.
(2003). A novel role for subunit C in mediating binding of the
H+-V-ATPase to the actin cytoskeleton. J. Biol.
Chem. 278,18499
-18505.
Wang, Y., Cipriano, D. J. and Forgac, M.
(2007). Arrangement of subunits in the proteolipid ring of the
V-ATPase. J. Biol. Chem.
282,34058
-34065.
Wang, Y., Toei, M. and Forgac, M. (2008).
Analysis of the membrane topology of transmembrane segments in the C-terminal
hydrophobic domain of the yeast vacuolar ATPase subunit a (Vph1p) by chemical
modification. J. Biol. Chem.
283,20696
-20702.
Wilkens, S., Vasilyeva, E. and Forgac, M.
(1999). Structure of the vacuolar ATPase by electron microscopy.
J. Biol. Chem. 274,31804
-31810.
Wilkens, S., Zhang, Z. and Zheng, Y. (2005). A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 36,109 -126.[CrossRef][Medline]
Zhang, Z., Charsky, C., Kane, P. M. and Wilkens, S.
(2003). Yeast V1-ATPase: affinity purification and structural
features by electron microscopy. J. Biol. Chem.
278,47299
-47306.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  W. W. C. Shum, N. Da Silva, D. Brown, and S. Breton Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk J. Exp. Biol., June 1, 2009; 212(11): 1753 - 1761. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
