Synaptic vesicle endocytosis and vesicle regeneration

The retrieval stage of the synaptic vesicle cycle, in which vesicle membrane and resident proteins deposited in the presynaptic plasma membrane by exocytosis are recovered and re-formed into release-competent vesicles at the presynaptic endocytic zone. In the classical clathrin-mediated route, the AP-2 adaptor complex, the neuron-specific assembly protein AP180 and the synaptotagmin-sorting adaptor stonin-2 recognise vesicle cargo and PI(4,5)P2 and nucleate a clathrin coat; BAR-domain proteins (endophilin, amphiphysin, syndapin) shape the invaginating membrane and recruit the GTPase dynamin, which constricts and severs the neck; synaptojanin-1 hydrolyses PI(4,5)P2 and auxilin recruits HSC70 to strip the clathrin coat, yielding a naked vesicle ready for re-acidification and loading. The same coat, curvature, fission and uncoating machinery is reused when membrane is first retrieved by clathrin-independent ultrafast or bulk endocytosis and vesicles are then regenerated by clathrin-dependent budding from a synaptic endosome. The module conforms, with stated deviations, to the generic MODULE:vesicle_coat_budding motif. Exemplars are human. Grounded in GO:0048488 (synaptic vesicle endocytosis).

MODULE:synaptic_vesicle_endocytosisDRAFTCONCRETEBiological Processmodules/synaptic_vesicle_endocytosis.yaml
synaptic vesicle endocytosisGO:0048488
GO:0048488
synaptic vesicle endocytosis
The module is grounded in the GO process for synaptic vesicle endocytosis.
GO:0150007
clathrin-dependent synaptic vesicle endocytosis
The clathrin-mediated route is the elaborated core of the module.
GO:0150008
bulk synaptic vesicle endocytosis
Clathrin-independent bulk/ultrafast retrieval is modeled as the alternative route variant.
PMID:22763746
Synaptic vesicle endocytosis.
Review of the clathrin-mediated synaptic vesicle endocytosis machinery (AP-2, AP180, stonin-2, clathrin, endophilin, amphiphysin, dynamin, synaptojanin, auxilin/HSC70) and of bulk endocytosis.
PMID:24305055
Ultrafast endocytosis at mouse hippocampal synapses.
Establishes clathrin-independent ultrafast endocytosis of membrane at the edge of the active zone within tens of milliseconds, with vesicles later regenerated from endosomes.
PMID:22099461
Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission.
Endophilin couples neck formation to synaptojanin-dependent uncoating at synapses.
PANTHER:PTN000242371
PAINT AP-2 mu subunit clathrin-dependent endocytosis node
Local PAINT IBD node in PTHR10529 seeded by AP2M1 with propagated term P:GO:0072583.
PANTHER:PTN002575694
PAINT stonin synaptic vesicle endocytosis node
Local PAINT IBD node in PTHR10529 seeded by STON2 with propagated term P:GO:0048488.
PANTHER:PTN000170013
PAINT dynamin GTPase node
Local PAINT IBD node in PTHR11566 seeded by DNM1 with propagated term F:GO:0003924.
PANTHER:PTN008570389
PAINT HSC70 clathrin coat disassembly node
Local PAINT IBD node in PTHR19375 seeded by HSPA8 with propagated term P:GO:0072318.
PMID:24015355
Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions.
Ultrafast, clathrin-independent membrane retrieval was first resolved at the C. elegans neuromuscular junction.
PMID:10931870
Mutations in synaptojanin disrupt synaptic vesicle recycling.
C. elegans unc-26 (synaptojanin) mutants accumulate coated and uncoated vesicle intermediates, grounding the worm uncoating step.

Human-centric exemplars with family-level descriptors so the module stays reusable. The mechanistic parts (coat assembly, curvature, fission, uncoating) are shared by both retrieval routes; the root variant set records only where the coat forms (plasma membrane vs synaptic endosome). Kiss-and-run retrieval is not modeled. Stonin-2 and AP2M1 both belong to the AP-mu PANTHER family (PTHR10529); the two descriptors are kept as distinct roles, each grounded at family level so that the worm orthologs (unc-41, dpy-23) fit. Loading and release stages are in MODULE:synaptic_vesicle_neurotransmitter_loading and MODULE:synaptic_vesicle_exocytosis; MODULE:synaptic_vesicle_cycle is the umbrella. Caenorhabditis elegans orthologs are listed as second representative members (dpy-23, apb-1, apa-2, aps-2, unc-11, unc-41, chc-1, clic-1, unc-57, amph-1, sdpn-1, dyn-1, unc-26, dnj-25, hsp-1); the worm has one dynamin (dyn-1) and one endophilin (unc-57), and ultrafast endocytosis was first described at its neuromuscular junction. Two caveats from the worm gene reviews: amph-1 and sdpn-1 are grounded here by orthology only, since their worm literature covers intestinal endocytic recycling and nuclear positioning rather than synaptic vesicle retrieval; and the worm has a single beta-adaptin (apb-1) shared between AP-1 and AP-2, so its AP-1 annotations are correct rather than over-propagated.

7Nodes
4Parts
1Variant Sets
2Variants
14Annotons
3Connections

Derived QC

Recommended-field compliance

87.5% recommended fields populated
  • knowledge_gaps[1] · provenance (0/1)
  • knowledge_gaps[2] · provenance (0/1)

Module deep research

✗ none found

No MODULE:synaptic_vesicle_endocytosis deep-research report alongside the module YAML.

Leaf nodes lacking representative members

✓ every leaf node grounds to a representative protein.

Template conformance

4 conformance issue(s):

Reaction chaining (advisory)

✓ every PRECEDES step chains, or its break is acknowledged via chaining_status.

  • dynamin_fission → coat_disassembly [NOT_CHECKED]
    Protein assembly steps, not metabolite chaining.

Gene-review completeness (21/32 grounded genes reviewed)

16 complete review(s) · 18 with deep research · 11 missing review · 3 reviewed but lacking deep research

Gene Review Complete Deep research
amph-1 Q21004 ✓ ✓ ✓
AP2M1 Q96CW1 ✓ 128/184 ✗
AP2S1 P53680 ✓ ✓ ✓
apa-2 Q22601 ✓ ✓ ✓
apb-1 Q9N4F3 ✓ ✓ ✓
aps-2 Q19123 ✓ ✓ ✓
chc-1 P34574 ✓ 31/33 ✓
clic-1 P90961 ✓ ✓ ✓
CLTC Q00610 ✓ ✓ ✓
DNAJC6 O75061 ✓ ✓ ✗
dnj-25 A0A486WXP9 ✓ ✓ ✓
dpy-23 P35603 ✓ 22/23 ✓
dyn-1 P39055 ✓ 45/47 ✓
hsp-1 P09446 ✓ ✓ ✓
HSPA8 P11142 ✓ ✓ ✓
SYNJ1 (Homo sapiens) O43426 ✗ — —
SNAP91 (Homo sapiens) O60641 ✗ — —
AP2A1 (Homo sapiens) O95782 ✗ — —
CLTA (Homo sapiens) P09496 ✗ — —
AMPH (Homo sapiens) P49418 ✗ — —
AP2B1 (Homo sapiens) P63010 ✗ — —
PICALM Q13492 ✓ ✓ ✗
DNM1 (Homo sapiens) Q05193 ✗ — —
STON2 (Homo sapiens) Q8WXE9 ✗ — —
SH3GL2 (Homo sapiens) Q99962 ✗ — —
PACSIN1 (Homo sapiens) Q9BY11 ✗ — —
DNM3 (Homo sapiens) Q9UQ16 ✗ — —
sdpn-1 Q6AHQ8 ✓ ✓ ✓
unc-11 Q9XZI6 ✓ 40/41 ✓
unc-26 G5ECL2 ✓ ✓ ✓
unc-41 P90761 ✓ ✓ ✓
unc-57 B1V8A0 ✓ ✓ ✓

Details

Context
presynaptic endocytic zoneGO:0098833
Coat assembly -> membrane curvature -> dynamin fission -> uncoatingBiological Processsynaptic_vesicle_endocytosis
synaptic vesicle endocytosisGO:0048488
Context
presynaptic endocytic zoneGO:0098833

Connections

The growing coat and its accessory proteins recruit BAR-domain proteins to the pit neck.
BAR-protein SH3 domains recruit dynamin to the constricted neck, driving scission.
Fission exposes the coated vesicle to synaptojanin, auxilin and HSC70 for uncoating.
Part 1: cargo recognition and clathrin coat assembly
AP-2 / AP180 / stonin-2 cargo recognition and clathrin coat nucleationRegulatory Stepadaptor_and_coat_assembly

Adaptors bind PI(4,5)P2 and vesicle cargo (synaptotagmin, VAMP2, SV2) on the plasma membrane and recruit clathrin triskelia, which polymerise into the coat of the forming pit.

synaptic vesicle coatingGO:0016183

Annotons

AP-2 adaptor complex
ap2_adaptor_complex
Participant: Protein Complex: AP-2 clathrin adaptor complex
Protein Complex:
AP-2 clathrin adaptor complexGO:0030122
Active units:
AP-2 mu subunit
Participant: Family: AP-2 mu subunit (AP2M1 / DPY-23) orthologs in the AP-mu family
Family:
AP-2 mu subunit (AP2M1 / DPY-23) orthologs in the AP-mu familyPANTHER:PTHR10529
Representative Members: AP2M1 (Homo sapiens)UniProtKB:Q96CW1 dpy-23 (Caenorhabditis elegans)UniProtKB:P35603
Role: Binds YxxPhi cargo motifs and PI(4,5)P2 after phosphorylation-dependent opening.
Function:
clathrin-cargo adaptor activityGO:0035615
AP-2 beta subunit
Participant: Family: AP complex beta subunit family (AP2B1)
Family:
AP complex beta subunit family (AP2B1)PANTHER:PTHR11134
Representative Members: AP2B1 (Homo sapiens)UniProtKB:P63010 apb-1 (Caenorhabditis elegans)UniProtKB:Q9N4F3
Role: Binds clathrin through its hinge/appendage and dileucine cargo motifs with sigma.
Function:
clathrin bindingGO:0030276
AP-2 alpha subunit
Participant: Family: AP complex alpha/gamma/epsilon subunit family (AP2A1)
Family:
AP complex alpha/gamma/epsilon subunit family (AP2A1)PANTHER:PTHR22780
Representative Members: AP2A1 (Homo sapiens)UniProtKB:O95782 apa-2 (Caenorhabditis elegans)UniProtKB:Q22601
Role: Binds PI(4,5)P2 and, via its appendage, accessory proteins such as AP180, amphiphysin and synaptojanin.
Function:
phosphatidylinositol-4,5-bisphosphate bindingGO:0005546
AP-2 sigma subunit
Participant: Family: AP complex small (sigma) subunit family (AP2S1)
Family:
AP complex small (sigma) subunit family (AP2S1)PANTHER:PTHR11753
Representative Members: AP2S1 (Homo sapiens)UniProtKB:P53680 aps-2 (Caenorhabditis elegans)UniProtKB:Q19123
Role: Small subunit that, with beta, forms the dileucine cargo-binding site.
file:human/AP2S1/AP2S1-ai-review.yaml
Gene review places AP2S1 in clathrin-dependent endocytosis at the clathrin-coated pit.

Function

clathrin-cargo adaptor activityGO:0035615
Cargo: synaptic vesicle membrane proteins (synaptotagmin, VAMP2, SV2)

Processes

clathrin-dependent synaptic vesicle endocytosisGO:0150007

Locations

presynaptic endocytic zone membraneGO:0098835

Hub adaptor that links PI(4,5)P2, vesicle cargo, accessory proteins and clathrin.

AP180 clathrin assembly protein
ap180_assembly_protein
Participant: Family: AP180/CALM (SNAP91/PICALM) clathrin assembly protein family
Family:
AP180/CALM (SNAP91/PICALM) clathrin assembly protein familyPANTHER:PTHR22951
Representative Members: SNAP91 (Homo sapiens)UniProtKB:O60641 unc-11 (Caenorhabditis elegans)UniProtKB:Q9XZI6 PICALM (Homo sapiens)UniProtKB:Q13492

Function

clathrin bindingGO:0030276
Cargo: synaptobrevin-2 / VAMP2

Processes

clathrin coat assemblyGO:0048268

Locations

presynaptic endocytic zone membraneGO:0098835

ANTH-domain PI(4,5)P2 binder that sorts VAMP2 into the pit and sets the size of the regenerated vesicle.

file:human/PICALM/PICALM-ai-review.yaml
Gene review accepts clathrin binding, PI(4,5)P2 binding and SNARE (VAMP) cargo sorting for the AP180 paralog PICALM.
Stonin-2 synaptotagmin sorting adaptor
stonin2_synaptotagmin_adaptor
Participant: Family: stonin (STON2 / UNC-41) orthologs in the AP-mu-homology family
Family:
stonin (STON2 / UNC-41) orthologs in the AP-mu-homology familyPANTHER:PTHR10529
Representative Members: STON2 (Homo sapiens)UniProtKB:Q8WXE9 unc-41 (Caenorhabditis elegans)UniProtKB:P90761

Function

clathrin-cargo adaptor activityGO:0035615
Cargo: synaptotagmin-1

Processes

synaptic vesicle endocytosisGO:0048488

mu-homology-domain adaptor dedicated to retrieving synaptotagmin into the pit via AP-2.

Clathrin triskelion
clathrin_triskelion
Participant: Protein Complex: clathrin triskelion (heavy + light chains)
Protein Complex:
clathrin triskelion (heavy + light chains)GO:0071439
Active units:
Clathrin heavy chain
Participant: Family: clathrin heavy chain (CLTC/CLTCL1) family
Family:
clathrin heavy chain (CLTC/CLTCL1) familyPANTHER:PTHR10292
Representative Members: CLTC (Homo sapiens)UniProtKB:Q00610 chc-1 (Caenorhabditis elegans)UniProtKB:P34574
Role: Three heavy chains form the triskelion legs that polymerise into the lattice.
Function:
structural molecule activityGO:0005198
file:human/CLTC/CLTC-ai-review.yaml
Gene review accepts structural molecule activity in clathrin coat assembly as a core function of CLTC.
Clathrin light chain
Participant: Family: clathrin light chain (CLTA/CLTB) family
Family:
clathrin light chain (CLTA/CLTB) familyPANTHER:PTHR10639
Representative Members: CLTA (Homo sapiens)UniProtKB:P09496 clic-1 (Caenorhabditis elegans)UniProtKB:P90961
Role: Binds the heavy-chain hub and regulates lattice assembly and disassembly.
Function:
structural molecule activityGO:0005198

Function

structural molecule activityGO:0005198

Processes

clathrin coat assemblyGO:0048268

Locations

clathrin-coated pitGO:0005905

Polymerises into the polyhedral lattice that stabilises the budding pit.

Part 2: membrane curvature and neck formation
BAR-domain shaping of the invaginating membraneRegulatory Stepmembrane_curvature

N-BAR (endophilin, amphiphysin) and F-BAR (syndapin/PACSIN) proteins bind and bend the membrane, generating and stabilising the tubular neck of the pit, and their SH3 domains recruit dynamin and synaptojanin to it.

Annotons

Endophilin-A N-BAR protein
endophilin_a_bar_protein
Participant: Family: endophilin-A (SH3GL1/2/3) family
Family:
endophilin-A (SH3GL1/2/3) familyPANTHER:PTHR14167
Representative Members: SH3GL2 (Homo sapiens)UniProtKB:Q99962 unc-57 (Caenorhabditis elegans)UniProtKB:B1V8A0

Function

phospholipid binding (N-BAR membrane bending)GO:0005543

Processes

membrane bendingGO:0097753

Locations

presynaptic endocytic zone membraneGO:0098835

Senses/induces neck curvature and recruits dynamin and synaptojanin-1 through its SH3 domain, coupling fission to uncoating.

PMID:22099461
Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission.
Endophilin recruitment to pit necks couples fission to synaptojanin-dependent uncoating.
Amphiphysin N-BAR protein
amphiphysin_bar_protein
Participant: Family: amphiphysin (AMPH/BIN1) family
Family:
amphiphysin (AMPH/BIN1) familyPANTHER:PTHR46514
Representative Members: AMPH (Homo sapiens)UniProtKB:P49418 amph-1 (Caenorhabditis elegans)UniProtKB:Q21004

Function

phospholipid binding (N-BAR membrane bending)GO:0005543

Processes

membrane bendingGO:0097753

Binds AP-2 and clathrin and recruits dynamin to the neck via its SH3 domain.

Syndapin/PACSIN F-BAR protein
syndapin_fbar_protein
Participant: Family: syndapin/PACSIN F-BAR family
Family:
syndapin/PACSIN F-BAR familyPANTHER:PTHR23065
Representative Members: PACSIN1 (Homo sapiens)UniProtKB:Q9BY11 sdpn-1 (Caenorhabditis elegans)UniProtKB:Q6AHQ8

Function

phospholipid binding (F-BAR membrane tubulation)GO:0005543

Processes

plasma membrane tubulationGO:0097320

Neuronal F-BAR protein that tubulates membrane and recruits dynamin; also implicated in bulk retrieval.

Part 3: dynamin fission
Dynamin GTP-dependent scission of the vesicle neckReactiondynamin_fission

Dynamin polymerises around the neck; GTP hydrolysis drives constriction and membrane fission, releasing the coated vesicle.

Annotons

Dynamin GTPase
dynamin_gtpase
Participant: Family: dynamin (DNM1/2/3) family
Family:
dynamin (DNM1/2/3) familyPANTHER:PTHR11566
Representative Members: DNM1 (Homo sapiens)UniProtKB:Q05193 dyn-1 (Caenorhabditis elegans)UniProtKB:P39055 DNM3 (Homo sapiens)UniProtKB:Q9UQ16

Function

GTPase activityGO:0003924
Substrates: GTP
Products: GDP + phosphate

Processes

membrane fissionGO:0090148 synaptic vesicle budding from presynaptic endocytic zone membraneGO:0016185

Locations

presynaptic endocytic zone membraneGO:0098835

Mechanochemical scission of the neck for both clathrin-coated pits and ultrafast/bulk invaginations.

Part 4: uncoating
Synaptojanin / auxilin / HSC70 uncoatingReactioncoat_disassembly

Synaptojanin-1 dephosphorylates PI(4,5)P2 to release adaptors from the membrane; auxilin binds the clathrin lattice and recruits HSC70, whose ATP hydrolysis disassembles the coat, leaving a naked vesicle that can re-acidify and be reloaded.

synaptic vesicle uncoatingGO:0016191

Annotons

Synaptojanin-1 PI(4,5)P2 5-phosphatase
synaptojanin_pip2_phosphatase
Participant: Family: synaptojanin (SYNJ1/2) inositol 5-phosphatase family
Family:
synaptojanin (SYNJ1/2) inositol 5-phosphatase familyPANTHER:PTHR11200
Representative Members: SYNJ1 (Homo sapiens)UniProtKB:O43426 unc-26 (Caenorhabditis elegans)UniProtKB:G5ECL2

Function

phosphatidylinositol-4,5-bisphosphate 5-phosphatase activityGO:0004439
Substrates: phosphatidylinositol 4,5-bisphosphate
Products: phosphatidylinositol 4-phosphate

Processes

synaptic vesicle uncoatingGO:0016191

Locations

presynaptic endocytic zone membraneGO:0098835

Removes the PI(4,5)P2 anchor of AP-2/AP180 so that adaptors dissociate after fission.

Auxilin J-domain co-chaperone
auxilin_cochaperone
Participant: Family: auxilin/GAK (DNAJC6/GAK) family
Family:
auxilin/GAK (DNAJC6/GAK) familyPANTHER:PTHR23172
Representative Members: DNAJC6 (Homo sapiens)UniProtKB:O75061 dnj-25 (Caenorhabditis elegans)UniProtKB:A0A486WXP9

Function

clathrin heavy chain bindingGO:0032050

Processes

clathrin coat disassemblyGO:0072318

Locations

extrinsic component of presynaptic endocytic zone membraneGO:0098894

Binds the clathrin lattice after fission and, through its J domain, targets HSC70 to it.

file:human/DNAJC6/DNAJC6-ai-review.yaml
Gene review accepts clathrin heavy chain binding and heat shock protein binding in clathrin coat disassembly as core functions of DNAJC6.
HSC70 uncoating ATPase
hsc70_uncoating_atpase
Participant: Family: HSC70 (HSPA8 / HSP-1) orthologs in the HSP70 family
Family:
HSC70 (HSPA8 / HSP-1) orthologs in the HSP70 familyPANTHER:PTHR19375
Representative Members: HSPA8 (Homo sapiens)UniProtKB:P11142 hsp-1 (Caenorhabditis elegans)UniProtKB:P09446

Function

ATP hydrolysis activityGO:0016887
Substrates: ATP
Products: ADP + phosphate

Processes

clathrin coat disassemblyGO:0072318

Locations

presynaptic cytosolGO:0099523

ATP-driven disassembly of the clathrin lattice, directed by auxilin.

file:human/HSPA8/HSPA8-ai-review.yaml
Gene review accepts an ATP-dependent chaperone role of HSPA8 in clathrin coat disassembly.
Variant set: Membrane retrieval route by route (One Or More)

Both routes reuse the coat, curvature, fission and uncoating parts above; they differ in whether the clathrin coat forms directly on the plasma membrane or on a synaptic endosome after clathrin-independent uptake.

Direct clathrin-mediated endocytosis from the plasma membraneBiological Processdirect_clathrin_mediated_retrieval

The classical route: a clathrin-coated pit forms in the presynaptic endocytic zone and buds a vesicle directly from the plasma membrane over seconds to tens of seconds.

Annotons

AP-2-dependent plasma-membrane pit
cme_ap2_route_marker
Participant: Family: AP-2 mu subunit (AP2M1 / DPY-23) orthologs in the AP-mu family
Family:
AP-2 mu subunit (AP2M1 / DPY-23) orthologs in the AP-mu familyPANTHER:PTHR10529
Representative Members: AP2M1 (Homo sapiens)UniProtKB:Q96CW1 dpy-23 (Caenorhabditis elegans)UniProtKB:P35603

Function

clathrin-cargo adaptor activityGO:0035615

Processes

clathrin-dependent synaptic vesicle endocytosisGO:0150007

Locations

presynaptic endocytic zone membraneGO:0098835

The coat forms on the plasma membrane and the budded vesicle is uncoated directly.

Ultrafast / bulk endocytosis with endosomal regenerationBiological Processultrafast_bulk_retrieval

Clathrin-independent, dynamin- and actin-dependent invagination at the edge of the active zone retrieves membrane within tens of milliseconds (ultrafast) or as large cisternae after strong stimulation (bulk); synaptic vesicles are then regenerated by clathrin-dependent budding from the resulting synaptic endosome.

Annotons

Dynamin-dependent clathrin-independent invagination
ultrafast_dynamin_retrieval
Participant: Family: dynamin (DNM1/2/3) family
Family:
dynamin (DNM1/2/3) familyPANTHER:PTHR11566
Representative Members: DNM1 (Homo sapiens)UniProtKB:Q05193 dyn-1 (Caenorhabditis elegans)UniProtKB:P39055

Function

GTPase activityGO:0003924

Processes

bulk synaptic vesicle endocytosisGO:0150008

Locations

presynaptic endocytic zone membraneGO:0098835

Severs the clathrin-independent invagination to form a synaptic endosome.

PMID:24305055
Ultrafast endocytosis at mouse hippocampal synapses.
Ultrafast endocytosis is clathrin-independent but dynamin-dependent.
Clathrin-dependent vesicle regeneration from the synaptic endosome
endosomal_clathrin_regeneration
Participant: Family: clathrin heavy chain (CLTC/CLTCL1) family
Family:
clathrin heavy chain (CLTC/CLTCL1) familyPANTHER:PTHR10292
Representative Members: CLTC (Homo sapiens)UniProtKB:Q00610 chc-1 (Caenorhabditis elegans)UniProtKB:P34574

Function

structural molecule activityGO:0005198

Processes

synaptic vesicle budding from endosomeGO:0016182 synaptic vesicle recycling via endosomeGO:0036466

Locations

presynaptic endosomeGO:0098830

Clathrin coats bud uniform synaptic vesicles from the endosomal intermediate.