(The FASEB Journal. 1999;13:S243-S247.)
© 1999 FASEB
Participation of dynamin in the biogenesis of cytoplasmic vesicles
JOHN R. HENLEY,
HONG CAO and
MARK A. MCNIVEN1
Center for Basic Research in Digestive Diseases and Department of Biochemistry and Molecular Biology, Mayo Clinic, Rochester, Minnesota 55905, USA
1Correspondence: Center for Basic Research in Digestive Diseases, Mayo Clinic, Rochester, MN 55905, USA. E-mail: mcniven{at}mayo.edu
 |
ABSTRACT
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Dynamin is a 100-kDa GTPase that has been implicated in endocytosis. To
extend our understanding of its cellular functions, we have
microinjected specific affinity-purified anti-dynamin antibodies into
cultured mammalian epithelial cells. Using this approach, dynamin
function can be inhibited specifically and rapidly in single cells.
Effects of microinjected inhibitory antibodies on distinct endocytic
processes and plasmalemmal morphology were then assayed by
fluorescence microscopy (FM) and ultrastructural analysis.
Microinjected antibodies inhibit the clathrin-mediated
endocytosis of fluorophore-labeled transferrin and cause a marked
invagination of the plasma membrane. Many of these long
plasmalemmal invaginations had clathrin-coated pits along their
cytoplasmic surface. A number of distinct noncoated pits resembling
plasmalemmal caveolae also accumulated in anti-dynamin
antibody-injected cells. Further, the cellular uptake of cholera toxin
B, which normally occurs by the internalization of caveolae, was
inhibited in these cells. In support of these observations,
immunoisolation techniques, double-label immuno-FM, and immunoelectron
microscopy (immuno-EM) provided biochemical and morphological evidence
that dynamin associates with plasmalemmal caveolae. Together, these
observations indicate that dynamin mediates scission from the plasma
membrane of both clathrin-coated pits and caveolae during distinct
endocytic processes. These results demonstrate that dynamin isoforms
are involved in an additional endocytic process that is distinct from
clathrin-mediated endocytosis and provide significant insights into
the molecular mechanisms governing the GTP-mediated internalization of
caveolae. Evidence is provided demonstrating that dynamin isoforms
have a differential distribution in mammalian cells. Targeting
information for these isoforms is provided at least in part by
regions of alternative splicing. Thus, the different dynamin
isoforms may be localized to distinct cellular compartments but provide
a similar scission function during the biogenesis of nascent
cytoplasmic vesicles—Henley, J. R., Cao, H., McNiven, M.
A. Participation of dynamin in the biogenesis of cytoplasmic
vesicles. ;1999>
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CYTOPLASMIC VESICLE FORMATION
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IMPORTANT INSIGHTS INTO the mechanism of cytoplasmic
vesicle formation have come from seminal studies of mutant strains of
Drosophila melanogaster. Temperature-sensitive mutations in
the shibire gene render flies paralyzed at the restrictive
temperature as a result of a marked depletion of
neurotransmitter-containing vesicles from synaptic terminals (1
, 2)
. Ultrastructural studies have shown that this defect occurs
during the endocytic retrieval of recycling synaptic vesicle membrane;
the scission of nascent vesicles from the plasma membrane is disrupted,
causing an accumulation of plasmalemmal invaginations (3
, 4)
.
Subsequent cloning and sequencing showed the shibire gene
product to be nearly identical to dynamin, a 100-kDa GTP-binding enzyme
that is enriched in the mammalian brain (5
6
7)
. In
addition to the three consensus sequence elements for GTP-binding and
hydrolysis within the NH2-terminal domain,
dynamin contains an internal pleckstrin homology domain and a
carboxyl-terminal proline-rich domain. These latter two have been
implicated in mediating molecular interactions with a number of
cellular components in vitro, including microtubules, acidic
phospholipids, certain Src Homology 3 (SH3) domains, and other dynamin
molecules (1
, 2
, 8
9
10
11
12
13
14
15
16)
. These interactions can stimulate
dynamin’s relatively high intrinsic GTPase activity (~2/min) by as
much as 75-fold, although most have been demonstrated in
vitro only (1
, 2)
. More recently, it has been shown
that dynamin function in synaptic vesicle endocytosis can be inhibited
in vivo by disruption of its interaction with the SH3 domain
of amphiphysin (17
, 18)
.
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THE DYNAMIN GENE FAMILY
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To date, three different mammalian dynamin genes have been
identified and each is expressed in a tissue-specific manner
(19)
. Dynamin I (Dyn1) expression appears to be restricted
to neurons and certain neuroendocrine cells (19
20
21
22)
;
dynamin II (Dyn2) is expressed in most cell types (19
, 21
, 22)
; and dynamin III (Dyn3) is expressed primarily in the
testis, with lower expression in the brain, heart, and lung (19
, 23)
. Multiple isoforms of each gene product arise by alternative
splicing, increasing the family size thus far described to 25 different
proteins (19)
. The fundamental questions we have asked are
why are there so many dynamin isoforms, and do they perform distinct or
redundant functions?
|
ROLE OF DYNAMIN IN MULTIPLE ENDOCYTIC PROCESSES
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Multiple endocytic mechanisms are present in many mammalian cells
and include clathrin-mediated endocytosis, internalization by caveolae,
clathrin-independent endocytosis, macropinocytosis, and phagocytosis
(24
25
26
27)
. It has been suggested that dynamin participates
in clathrin-mediated endocytosis exclusively, because heterologous
expression of a mutant Dyn1 construct in epithelial cells inhibits this
process but not pinocytosis (28
29
30
31)
. However, whether a
single mutant Dyn1 isoform can inhibit the multiple forms of endogenous
Dyn2 is unclear. Indeed, the bulk uptake of fluid is inhibited at the
restrictive temperature in cells of D. melanogaster bearing
the mutant shibire gene (3
, 32
33
34)
. To address
this further, we have used single-cell microinjection of inhibitory
antibodies to disrupt dynamin function (35)
.
Peptide-specific antibodies were made to conserved (Pan-dynamin) and
isoform-specific regions of the dynamin family. Cells were injected
with antibodies and then, 2–16 h later, incubated ~20 min with
fluorophore-labeled transferrin. After rinsing with pH 3.5 medium to
remove surface bound ligand, cells were fixed for FM. Using this
approach we determined that ~90% of control cells that were injected
with either heat inactivated or irrelevant anti-kinesin antibodies
internalized transferrin. In contrast, <25% of the anti-dynamin
antibody-injected cells internalized the ligand. Similar results were
obtained using several epithelial cell lines, including HeLa and normal
hepatocyte cultures (Clone 9 and BNL CL.2). When injected cells were
fixed and processed for EM, deep invaginations of the plasma membrane
were found. Bristle-like cytoplasmic coats could be seen on many of
these aberrant invaginations, consistent with a perturbation in the
scission of clathrin-coated pits from the plasma membrane.
Ultrastructurally distinct invaginations also could be found, which
included unbranched and highly fenestrated tubules, large ~0.5-µM
diameter cisternae, and small ~60-nm diameter flask-shaped pits
extending from the plasma membrane deep into the cytoplasm. Strikingly,
these smaller invaginations resembled plasmalemmal vesicles known as
caveolae. Compared with controls, the surface density of these caveolar
profiles increased >2-fold in anti-dynamin antibody-injected cells and
often were arranged in complex clusters and chains, separated by
constrictions or ‘necks’. Both of these observations are consistent
with a disruption in the scission of caveolae from the plasma membrane
of anti-dynamin antibody-injected cells.
To test this more directly, we used cholera toxin B, which, by binding
to the ganglioside GM1, is sequestered and internalized selectively by
plasmalemmal caveolae. Injected cells were incubated 15 min at ~8°C
with either fluorophore or horseradish peroxidase (HRP)-labeled cholera
toxin B and then rinsed and incubated with serum-free growth medium for
2.5 h at 37°C. This method allowed a controlled binding and
internalization of the labeled toxin. Toxin uptake is largely
independent of clathrin-mediated endocytosis in these cells because
depletion of cytoplasmic potassium ions did not inhibit the
accumulation of the labeled toxin within perinuclear compartments but
did block the internalization of fluorophore-labeled transferrin. By FM
we found that the toxin was internalized normally by control cells but
not by anti-dynamin antibody-injected cells. When control cells were
fixed and processed for EM using diaminobenzidine cytochemistry to
detect HRP, little toxin labeling was detected at the plasma membrane
but rather was concentrated within cytoplasmic organelles, including
endocytic vesicles and, suprisingly, elements of the rough ER and
the nuclear envelope. In contrast, the toxin was not detected in these
cytoplasmic compartments in anti-dynamin antibody-injected cells but
instead remained at the cell surface, often concentrated within
clusters of plasmalemmal caveolae. Again, these observations support
the role of dynamin during the scission of caveolae from the plasma
membrane.
If dynamin participates directly in the scission of caveolae to form
discrete endocytic vesicles, then it should be possible to detect it in
association with plasmalemmal caveolae. To provide biochemical support
for this, a Pan-dynamin antibody coupled to magnetic beads was used to
immunoisolate caveolar membranes from a cultured hepatocyte postnuclear
membrane fraction. By immunoblot analysis, most of the caveolar marker
protein caveolin/VIP21 that was detected in the starting fraction was
found with the immunoisolated fraction, and very little could be
detected in the remaining nonbound fraction. To provide morphological
support for this association, double-label immuno-FM was used to show a
significant colocalization of dynamin and caveolin/VIP21. By EM, double
immunogold labeling of ultrathin cryo-sections also showed a
significant colocalization of these 2 proteins on plasmalemmal caveolae
in cultured hepatocytes and the continuous endothelium of the lung
(R.-V. Stan and J. M. McCafferey, unpublished results). Thus,
functional assays in combination with FM and ultrastructural and
biochemical analyses provide strong evidence that Dyn2 participates in
the scission of caveolae from the plasma membrane in addition to a role
in clathrin-mediated endocytosis. These results are supported by a
recent study that used an in vitro assay for the budding of
caveolae from an isolated plasmalemmal fraction (36)
.
To test the role of dynamin in other endocytic processes, markers for
fluid-phase endocytosis, such as dextran, have been used. Importantly,
we have determined that microinjected anti-dynamin antibodies greatly
attenuate the cellular uptake of fluorophore-labeled dextran when
assayed under serum-free conditions (unpublished results). Whether
constitutive pinocytosis in these cells involves an endocytic process
that is independent of clathrin-mediated endocytosis or internalization
by caveolae is being investigated. This result supports the earlier
observations made on cells of D. melanogaster bearing a
mutation in the shibire gene, although it is in contrast to
the lack of inhibition seen in cells overexpressing a mutant Dyn1
construct. Importantly, epidermal growth factor (EGF) induced
macropinocytosis of fluorophore-labeled dextran is not inhibited in
cells microinjected with anti-dynamin antibodies (unpublished results).
Likewise, EGF-induced phagocytosis of latex beads continues in these
cells. Thus, not all endocytic processes are inhibited in anti-dynamin
antibody-injected cells.
|
ROLE OF DYNAMIN IN BIOSYNTHETIC PROCESSES
|
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In addition to a plasmalemmal distribution, multiple antibodies
have localized dynamin to the Golgi complex of many cell types, as
determined by double-label immuno-FM and immuno-EM (19
, 37
38
39)
. Also, a Pan-dynamin antibody coupled to magnetic beads
has been used to immunoisolate membranes of the Golgi complex, as
confirmed both ultrastructurally and by immunoblot analysis
(37)
. Studies using isoform-specific antibodies have
supported the original proposal that Dyn2 associates with the Golgi
apparatus (19
, 37
38
39)
. Further support for this has come
from studies on epithelial cells expressing a cDNA fusion construct of
Dyn2 and green fluorescent protein (Dyn2-GFP) (19, 38). By confocal
microscopy, Dyn2-GFP is prominent in a juxtanuclear region that
overlaps significantly with TGN-38, 
-adaptin, and clathrin. Thus,
dynamin isoforms localize to the Golgi complex in addition to an
association with endocytic structures.
In addition to these localization studies, functional support for the
role of dynamin in biosynthetic processes has come from a cell-free
assay that reconstitutes the budding of vesicles from the trans-Golgi
network in vitro (38)
. When Golgi complex
membranes are immobilized on magnetic beads and incubated with a
cytosolic fraction and ATP-regenerating system, distinct classes of
vesicles are formed. These include clathrin-coated vesicles, which
contain nascent hydrolytic enzymes destined for the lysosomes, and also
constitutive secretory vesicles, which are nonclathrin-coated.
Significantly, Pan-dynamin and Dyn2-specific antibodies inhibit the
formation of these distinct vesicle classes. Further, immunodepletion
of dynamin proteins from the cytosolic fraction also inhibits the
formation of these vesicles and readdition of a dynamin-enriched
fraction restores the budding activity to control levels. Thus, taken
together, these studies strongly suggest that dynamin participates in
the formation of distinct cytoplasmic vesicles at the Golgi complex.
|
DIFFERENTIAL LOCALIZATION OF DYNAMIN ISOFORMS
|
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How might dynamin be directed to participate in such a
variety of biosynthetic and endocytic processes? At least 25 different
transcripts arise by alternative splicing of the 3 dynamin genes
(19)
. Thus, the unique peptide sequences that are inserted
into the various dynamin isoforms could provide targeting information,
directing each to a specific membrane compartment. To test this
hypothesis, cDNA fusion constructs of GFP and at least 2 spliced
variants of each dynamin gene product were expressed in a normal
hepatocyte cell line (Clone 9) (19, 38). Confocal microscopy of these
transfected epithelial cells confirmed that certain spliced variants
[Dyn1(ab) and Dyn2(ab)] are indeed localized to clathrin-coated pits
at the plasma membrane, whereas another [Dyn2(aa)] is also localized
to the Golgi complex. One isoform [Dyn1(bb)] does not associate with
plasmalemmal clathrin-coated pits but is found at the Golgi apparatus.
Other isoforms seem to associate either additionally [Dyn1(ab) and
Dyn2(ab)] or exclusively [Dyn3(baa)] with nonclathrin-coated
vesicles. Thus, multiple dynamin isoforms are localized to a variety of
cellular compartments, and targeting information seems to be encoded at
least partly by as few as 4 amino acid insertions at regions of
alternative splicing.
|
MOLECULAR MACHINERY REGULATING VESICLE BIOGENESIS
|
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Recently, it has been demonstrated that dynamin alone can mediate
membrane tubulation and scission, although other molecules may
participate in these processes in vivo
(40
41
42)
. It now seems likely that differentially spliced
isoforms of dynamin are targeted to distinct cellular compartments to
provide a similar function in the biogenesis of nascent vesicles
(Fig. 1
). Multiple binding proteins or lipids may associate either directly or
indirectly with distinct isoforms and thereby mediate their
intracellular localization. Furthermore, these molecular components may
also differentially regulate the function of each dynamin isoform.
Certainly, determining the nature of the molecular machinery that
regulates the function and cellular localization of the multiple
dynamin isoforms will be key to a more complete understanding of the
biogenesis of cytoplasmic vesicles.
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Figure 1. Model illustrating the participation of dynamin isoforms in the
biogenesis of distinct cytoplasmic vesicles during multiple endocytic
and biosynthetic processes. Targeting information that is provided by
insertions at sites of alternative splicing direct dynamin ‘collars’
to specific locations at the plasma membrane and the Golgi apparatus.
The different isoforms then mediate a similar function, the scission of
nascent vesicles from the appropriate donor membrane. These processes
include the formation of both clathrin and nonclathrin-coated vesicles
from the trans-Golgi network and the separation of caveolae,
clathrin-coated, and possibly nonclathrin-coated vesicles from the
plasma membrane.
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ACKNOWLEDGMENTS
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R.-V. Stan and J. M. McCafferey performed the immuno-EM and
shared unpublished results. This research was supported by National
Institutes of Health grants to M.A.M. J.R.H. is the recipient of
an American Liver Foundation Postdoctoral Research Fellowship Award. We
are grateful to the following people for expert technical assistance:
F. Garcia for making cDNA constructs, E. W. A. Krueger for
performing single-cell microinjections and EM, and B. J. Oswald
for purifying anti-dynamin antibodies and doing the immunoisolation
experiments. We thank H. Thompson for critical comments about the
manuscript.
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TOP
ABSTRACT
CYTOPLASMIC VESICLE FORMATION
