SPKW Apoptosis Subproject

SPKW Apoptosis Subproject

Parent project: SPKW.md

Overview

This subproject identifies human proteins annotated to "apoptotic process" (GO:0006915) or descendants where the only evidence comes from UniProt Keywords mapping (GO_REF:0000043). These annotations lack corroboration from any other source (experimental, computational, or curator statements).

The goal is to review these annotations to determine if they are well-supported by literature or if they represent cases where the UniProt "Apoptosis" keyword was applied but the connection to apoptosis is weak or indirect.

Query Methodology

Using DuckDB on ~/repos/go-db/db/goa_human.ddb:

-- Find proteins with apoptotic process annotations ONLY from UniProt Keywords
WITH all_apoptotic AS (
    SELECT a.db_object_id, a.db_object_symbol, a.supporting_references
    FROM gaf_association a
    INNER JOIN isa_partof_closure ipc ON a.ontology_class_ref = ipc.subject
    WHERE ipc.object = 'GO:0006915'  -- apoptotic process
      AND a.is_negation = false
),
genes_with_other_evidence AS (
    SELECT DISTINCT db_object_id
    FROM all_apoptotic
    WHERE supporting_references != 'GO_REF:0000043'
),
spkw_only_genes AS (
    SELECT DISTINCT db_object_id, db_object_symbol
    FROM all_apoptotic
    WHERE supporting_references = 'GO_REF:0000043'
      AND db_object_id NOT IN (SELECT db_object_id FROM genes_with_other_evidence)
)
SELECT * FROM spkw_only_genes ORDER BY db_object_symbol;

Summary Statistics (Human - goa_human.ddb)

Status

Genes for Review (Sample - Alphabetical)

Gene UniProt Description Status Notes
ADAMTSL4 Q6UY14 ADAMTS-like protein 4 REVIEWED - OVER-ANNOTATION
AIMP1 Q12904 tRNA synthase complex protein 1 REVIEWED - OVER-ANNOTATION Caspase substrate
AIMP2 Q13155 tRNA synthase complex protein 2 REVIEWED - MODIFY Moonlighting; core=MSC scaffold
AKTIP Q9H8T0 AKT-interacting protein REVIEWED - OVER-ANNOTATION
APBB1 O00213 Amyloid beta A4 precursor protein-binding protein REVIEWED - OVER-ANNOTATION
API5 Q9BZZ5 Apoptosis inhibitor 5 REVIEWED - LEGITIMATE Evolved anti-apoptotic
APIP Q96GX9 Methylthioribulose-1-phosphate dehydratase REVIEWED - OVER-ANNOTATION Core=methionine salvage
APLP1 P51693 Amyloid-like protein 1 REVIEWED - OVER-ANNOTATION
AREL1 O15033 Apoptosis-resistant E3 ubiquitin ligase 1 REVIEWED - OVER-ANNOTATION
ARL6IP1 Q15041 ADP-ribosylation factor-like protein 6-interacting protein 1 REVIEWED - OVER-ANNOTATION Core=ER shaping
ASAH2 Q9NR71 Neutral ceramidase REVIEWED - OVER-ANNOTATION Core=ceramide metabolism
ATG4D Q86TL0 Cysteine protease ATG4D REVIEWED - OVER-ANNOTATION Core=autophagy
ATG5 Q9H1Y0 Autophagy protein 5 REVIEWED - OVER-ANNOTATION Core=autophagy
AVEN Q9NQS1 Cell death regulator Aven REVIEWED - LEGITIMATE Evolved anti-apoptotic
AXIN1 O15169 Axin-1 REVIEWED - OVER-ANNOTATION Core=Wnt signaling
BABAM2 Q9NXR7 BRISC and BRCA1-A complex member 2 pending
BAG1 Q99933 BAG family molecular chaperone regulator 1 REVIEWED - OVER-ANNOTATION Core=Hsp70 co-chaperone
BCAP29 Q9UHQ4 B-cell receptor-associated protein 29 pending
BCAP31 P51572 B-cell receptor-associated protein 31 REVIEWED - OVER-ANNOTATION Caspase substrate
BCL2L12 Q9HB09 Bcl-2-like protein 12 REVIEWED - LEGITIMATE Bcl-2 family
BECN1 Q14457 Beclin-1 REVIEWED - OVER-ANNOTATION Core=autophagy
BIRC5 O15392 Baculoviral IAP repeat-containing protein 5 (survivin) REVIEWED - OVER-ANNOTATION Core=mitosis (CPC)
C1QBP Q07021 Complement C1q-binding protein REVIEWED - OVER-ANNOTATION Core=mt-translation
CD47 Q08722 Leukocyte surface antigen CD47 REVIEWED - OVER-ANNOTATION Core=phagocytosis checkpoint
CDK1 P06493 Cyclin-dependent kinase 1 REVIEWED - OVER-ANNOTATION Core=cell cycle

Full list: 280 genes total - see query above to regenerate


Pilot Batch Review Results

Selected 5 genes that appeared suspicious for over-annotation based on names (e.g., "tRNA synthase complex protein").

Key Principle Applied: Over-annotation occurs when a protein is annotated to "apoptotic process" based on:
- Being a substrate/target of apoptosis machinery (not participating IN apoptosis)
- Having causal downstream effects on apoptosis through pleiotropic mechanisms
- Having effects at pharmacological concentrations rather than physiological
- Performing a different core function where apoptotic effects are secondary

An evolved regulatory mechanism is different - this requires evidence that the gene product specifically evolved to regulate apoptosis as part of its function.

Gene Core Function Apoptosis Relationship Assessment
AIMP1 MSC scaffold, tRNA binding Cleaved BY caspase-7 → releases EMAP-II; EMAP-II "induces apoptosis at high concentrations" OVER-ANNOTATION - being a caspase substrate ≠ participating in apoptosis; EMAP-II effect is pharmacological
AIMP2 MSC scaffold Proapoptotic via p53 stabilization (blocks MDM2); stress-responsive nuclear translocation MODIFYGO:0043065 (positive regulation of apoptotic process). Genuine evolved moonlighting function, but AIMP2 REGULATES apoptosis via p53, doesn't participate IN apoptotic process
APIP Methionine salvage enzyme (MtnB) Moonlighting: binds Apaf-1, inhibits apoptosis; enzymatic activity dispensable for anti-apoptotic effect OVER-ANNOTATION - core function is metabolic; apoptosis effect is moonlighting; INHIBITS not participates
ARL6IP1 ER membrane shaping (reticulon-like) Named "ARMER"; inhibits CASP9-dependent apoptosis OVER-ANNOTATION - anti-apoptotic effect likely secondary to ER homeostasis; deep research is all about ER morphology
ASAH2 Neutral ceramidase (sphingolipid metabolism) Reduces ceramide → shifts ceramide/S1P balance toward survival OVER-ANNOTATION - metabolic enzyme; apoptotic effect is downstream of ceramide catabolism, not an evolved regulatory function

Results: 5 of 5 genes have issues with GO:0006915. AIMP2 has a genuine apoptosis-related function but requires MODIFY to regulatory term.


Detailed Gene Analysis

AIMP1 (Q12904) - tRNA synthase complex protein 1

Core evolved function: Scaffold/organizing subunit of the multi-aminoacyl tRNA synthetase complex (MSC); has OB-fold for tRNA binding.

Apoptosis connection:
- Cleaved BY caspase-7 during apoptosis → releases EMAP-II cytokine
- EMAP-II has proinflammatory effects and "induces apoptosis at high concentrations"

Why OVER-ANNOTATION:
- Being cleaved BY caspases makes you a target/substrate of apoptosis, not a participant IN the apoptotic process
- EMAP-II inducing apoptosis "at high concentrations" is a pharmacological effect, not a physiological evolved function
- 2024 literature focuses on EMAP-II as a stress/inflammation signal, not as having an evolved proapoptotic role
- Core function is clearly the MSC scaffold role


AIMP2 (Q13155) - tRNA synthase complex protein 2

Core evolved function: MSC scaffold (multi-aminoacyl-tRNA synthetase complex).

Apoptosis connection:
- Moonlighting function: upon DNA damage, AIMP2 is phosphorylated, dissociates from MSC, translocates to nucleus
- Mechanism: blocks MDM2-mediated ubiquitination of p53, thereby stabilizing p53
- p53 then activates apoptotic genes
- Evidence (PMID:18695251): AIMP2 depletion → resistance to apoptosis; reintroduction → susceptibility restored

Why MODIFY (not LEGITIMATE for GO:0006915):
- The evidence is phenotypic: cells ± AIMP2 differ in apoptosis susceptibility
- The mechanism is regulatory: AIMP2 → blocks MDM2 → stabilizes p53 → p53 activates apoptosis
- AIMP2 does NOT directly participate in apoptotic process execution (caspase cascades, MOMP, DNA fragmentation)
- This is a genuine evolved moonlighting function, but the correct term is GO:0043065 (positive regulation of apoptotic process)
- Analogous to APBB1 - both regulate apoptosis but don't participate IN apoptosis


APIP (Q96GX9) - Methylthioribulose-1-phosphate dehydratase

Core evolved function: Enzyme in the methionine salvage pathway (MtnB step). Catalyzes dehydration of MTRu-1-P.

Apoptosis connection:
- Named "APAF1-interacting protein" because it binds Apaf-1
- Competes with procaspase-9 for Apaf-1 binding, thereby inhibiting apoptosome
- Key finding: "APIP's enzymatic activity is dispensable for anti-apoptotic effects" - this is a moonlighting function

Why OVER-ANNOTATION:
- Primary evolved function is methionine salvage (metabolic)
- The Apaf-1 binding is a real moonlighting function, but:
- It INHIBITS apoptosis, doesn't participate in it
- "Apoptotic process" (GO:0006915) implies direct participation
- The regulatory annotation (GO:0043066) is more accurate


ARL6IP1 (Q15041) - ADP-ribosylation factor-like protein 6-interacting protein 1

Core evolved function: ER membrane-shaping protein with reticulon-like hairpins that generate positive membrane curvature and promote tubular ER formation.

Apoptosis connection:
- Named "ARMER" (Apoptotic regulator in the membrane of the ER)
- Has IDA evidence for GO:0043066 (negative regulation of apoptotic process)
- Inhibits CASP9-dependent apoptosis

Why OVER-ANNOTATION:
- Deep research is entirely about ER morphology, not apoptosis
- Loss of protein → disrupted ER structure → ER stress → cell death
- This is a downstream consequence of ER dysfunction, not an evolved apoptosis regulatory function
- Anti-apoptotic effect likely reflects the importance of proper ER structure for cell viability
- Linked to hereditary spastic paraplegia (HSP) via ER dysfunction, not apoptosis dysregulation


ASAH2 (Q9NR71) - Neutral ceramidase

Core evolved function: Neutral ceramidase enzyme (EC 3.5.1.23). Hydrolyzes ceramide → sphingosine + fatty acid. Primary role in intestinal digestion of dietary sphingolipids.

Apoptosis connection:
- Ceramide is generally proapoptotic; sphingosine-1-phosphate (S1P) is pro-survival
- By breaking down ceramide, ASAH2 shifts the balance toward survival signaling
- Has IMP evidence for GO:2001234 (negative regulation of apoptotic signaling pathway)

Why OVER-ANNOTATION:
- This is exactly the "causal downstream effect" pattern
- Core function is ceramide metabolism (especially dietary sphingolipids in intestine)
- The anti-apoptotic effect is a metabolic consequence of reducing ceramide levels
- The enzyme didn't evolve TO regulate apoptosis - it evolved to metabolize ceramides, and ceramides happen to be involved in apoptotic signaling
- Deep research emphasizes intestinal brush border function and dietary sphingolipid catabolism


Batch 2 Review Results

Expanded review to 15 additional genes using the strict over-annotation criteria established in the pilot batch.

Gene UniProt Core Function Assessment Rationale
ADAMTSL4 Q6UY14 ECM/microfibril organization for lens zonules OVER-ANNOTATION No apoptosis function in literature; core function is extracellular matrix assembly
AKTIP Q9H8T0 Telomere replication support, ESCRT function OVER-ANNOTATION No apoptosis function; UEV-domain protein for telomere/cytokinesis
API5 Q9BZZ5 Anti-apoptotic scaffold LEGITIMATE Evolved anti-apoptotic mechanisms: binds caspase-2 CARD, protects Acinus from cleavage
ATG4D Q86TL0 Autophagy protease (LC3/GABARAP processing) OVER-ANNOTATION Core function is autophagy; no evolved apoptosis function
ATG5 Q9H1Y0 Autophagy E3-like (ATG12-ATG5-ATG16L1) OVER-ANNOTATION Core function is autophagosome biogenesis; apoptosis effects are secondary
AVEN Q9NQS1 Anti-apoptotic (BCL-XL/Apaf-1 binding) LEGITIMATE Evolved anti-apoptotic function: binds BCL-XL, inhibits Apaf-1/apoptosome, has BH3-like motif
AXIN1 O15169 Wnt signaling scaffold (β-catenin destruction) OVER-ANNOTATION Core function is Wnt/β-catenin pathway; no apoptosis mentioned in research
BAG1 Q99933 Hsp70 co-chaperone/nucleotide exchange factor OVER-ANNOTATION Core function is proteostasis/chaperoning; BCL2 binding is secondary
BCAP31 P51572 ER cargo receptor/quality control OVER-ANNOTATION Core function is ER QC; is a caspase-8 substrate (like AIMP1)
BCL2L12 Q9HB09 Anti-apoptotic (caspase/p53 inhibition) LEGITIMATE Evolved function: directly inhibits caspase-7, antagonizes p53, Bcl-2 family member
BECN1 Q14457 Autophagy (PI3KC3 scaffold) OVER-ANNOTATION Core function is autophagy; BCL2 interaction regulates autophagy, not apoptosis
BIRC5 O15392 Mitosis (CPC component) OVER-ANNOTATION "survivin's best-established function is mitotic CPC"; anti-apoptotic effects are indirect
C1QBP Q07021 Mitochondrial RNA binding, complement receptor OVER-ANNOTATION Core functions are mt-translation and C1q binding; no apoptosis core function
CD47 Q08722 Phagocytosis checkpoint ("don't eat me") OVER-ANNOTATION Core function is innate immune checkpoint (SIRPα); not apoptosis
CDK1 P06493 Cell cycle kinase (G2/M transition) OVER-ANNOTATION Core function is cell cycle; phosphorylates apoptosis substrates but that's not its evolved function

Results Summary: 12 OVER-ANNOTATION, 3 LEGITIMATE


Detailed Analysis - Batch 2 Legitimate Genes

API5 (Q9BZZ5) - Apoptosis inhibitor 5

Core evolved function: Anti-apoptotic scaffold protein with HEAT/ARM-like helical repeat architecture.

Why LEGITIMATE:
- Direct caspase-2 inhibition: Binds the CARD domain of caspase-2, preventing dimerization/activation
- Acinus protection: Binds Acinus and protects it from caspase-3 cleavage, blocking DNA fragmentation
- E2F1 axis modulation: Suppresses E2F1-dependent apoptosis
- All mechanisms are specific, evolved anti-apoptotic functions, not pleiotropic effects


AVEN (Q9NQS1) - Cell death regulator Aven

Core evolved function: Anti-apoptotic regulator.

Why LEGITIMATE:
- BCL-XL binding: Direct interaction with BCL-XL, stabilizing it and potentiating its anti-apoptotic function
- Apaf-1 inhibition: Binds Apaf-1, preventing apoptosome assembly and caspase-9 activation
- BH3-like motif: Predicted BH3-like sequence (aa 141-153) for BCL-XL interaction
- Proteolytic regulation: Cathepsin D cleaves N-terminus to release potent anti-apoptotic C-terminal fragment
- Specific evolved mechanisms, not downstream/metabolic effects


BCL2L12 (Q9HB09) - Bcl-2-like protein 12

Core evolved function: Anti-apoptotic Bcl-2 family member.

Why LEGITIMATE:
- Direct caspase inhibition: Inhibits effector caspase-7 (and possibly caspase-3)
- p53 antagonism: Binds and neutralizes p53 transcriptional activity
- Bcl-2 family member: Has BH3-like motif, part of the evolved apoptosis regulatory network
- Named appropriately - this is a bona fide anti-apoptotic protein with evolved mechanisms


Detailed Analysis - Batch 2 Over-Annotations (Selected)

BIRC5/Survivin (O15392)

Why OVER-ANNOTATION despite "Apoptosis inhibitor" name:
- Deep research states: "survivin's best-established function is as an essential CPC component regulating mitotic progression"
- "Anti-apoptotic effects are context-dependent and likely mediated by networks (XIAP, SMAC) rather than direct caspase inhibition"
- Core evolved function is mitosis (Chromosomal Passenger Complex), not apoptosis
- This is a case where the gene NAME is misleading - the protein evolved for cell division, with indirect anti-apoptotic effects

ATG5 (Q9H1Y0)

Why OVER-ANNOTATION despite "Apoptosis-specific protein" alias:
- Core function is autophagy: E3-like activity in ATG12-ATG5-ATG16L1 complex for LC3 lipidation
- While autophagy and apoptosis have crosstalk, ATG5's evolved function is autophagosome biogenesis
- The UniProt alias "Apoptosis-specific protein" reflects early naming, not current functional understanding

CDK1 (P06493)

Why OVER-ANNOTATION:
- Core function is cell cycle control (essential G2/M transition kinase)
- 2023 review notes CDK1 phosphorylates "caspase-9, Bcl-2 family, survivin" among its 1000+ substrates
- Phosphorylating apoptosis-related proteins as part of cell cycle doesn't make apoptosis its evolved function
- This is like annotating a transcription factor to all processes its target genes are involved in


Cumulative Results

Batch Total Genes Over-Annotation/Modify Legitimate Issue Rate
Pilot (5) 5 5 0 100%
Batch 2 (15) 15 12 3 80%
Additional (3) 3 3 0 100%
Combined 23 20 3 87%

Legitimate genes for GO:0006915 (3/23):
1. API5 - evolved anti-apoptotic (caspase-2, Acinus)
2. AVEN - evolved anti-apoptotic (BCL-XL, Apaf-1)
3. BCL2L12 - Bcl-2 family member (caspase-7, p53)

MODIFY to regulatory term (1/23):
1. AIMP2 - genuine proapoptotic moonlighting function via p53/MDM2, but should be GO:0043065 (positive regulation of apoptotic process)

Common issue patterns:
1. Regulatory vs participatory conflation (AIMP2, APBB1) - gene regulates apoptosis but doesn't participate IN the process → MODIFY to regulatory term
2. Autophagy proteins (ATG4D, ATG5, BECN1) - autophagy/apoptosis crosstalk ≠ apoptosis function
3. Cell cycle proteins (CDK1, BIRC5) - core function is cell cycle, not apoptosis
4. Caspase substrates (AIMP1, BCAP31) - being cleaved BY apoptosis ≠ participating IN apoptosis
5. Metabolic enzymes (ASAH2, APIP) - metabolic effects on apoptosis ≠ evolved function
6. Core functions elsewhere (ADAMTSL4=ECM, C1QBP=mt-translation, CD47=phagocytosis, AXIN1=Wnt, ARL6IP1=ER shaping, AKTIP=telomeres, BAG1=chaperoning)


Key Findings

  1. Stricter criteria for legitimate GO:0006915 (apoptotic process) annotation:
  2. Must directly participate in apoptotic process execution (caspase cascades, MOMP, DNA fragmentation)
  3. Being a caspase substrate ≠ participating in apoptosis
  4. Regulating apoptosis (even via genuine evolved mechanisms) ≠ participating IN apoptosis
  5. Effects at pharmacological concentrations ≠ physiological function
  6. Downstream metabolic effects ≠ evolved function

  7. Regulatory vs participatory distinction is critical:

  8. AIMP2 has a genuine evolved proapoptotic function (p53 stabilization) but REGULATES apoptosis
  9. The phenotypic evidence (cells ± gene = differential apoptosis susceptibility) supports regulatory annotation
  10. Correct term is GO:0043065 (positive regulation of apoptotic process), not GO:0006915

  11. UniProt "Apoptosis" keyword is too broad:

  12. Applied to anything that affects apoptosis (participates, regulates, is a substrate, has downstream effects)
  13. GO term "apoptotic process" implies direct participation, which is inappropriate for most of these

Recommendations:
- Genes with genuine regulatory functions: MODIFY to regulatory term (GO:0043065/GO:0043066)
- Genes with different core functions: Mark as OVER-ANNOTATED or REMOVE
- Only genes that directly execute apoptosis should retain GO:0006915


Notes

2026-01-31

APLP1 Review Completed

APLP1 is classified as an OVER-ANNOTATION for GO:0006915 (apoptotic process):

Follow-up adjustment
- Changed GO:0006915 review action to MARK_AS_OVER_ANNOTATED (fragment-specific, by-similarity evidence); removed the proposed replacement to GO:0043065.

AREL1 Review Completed

AREL1 is classified as an OVER-ANNOTATION for GO:0006915 (apoptotic process):

2026-01-19

APBB1 Review Completed

APBB1 (Fe65) is classified as an OVER-ANNOTATION for GO:0006915 (apoptotic process):

This continues the pattern: APBB1 has a genuine role in apoptosis regulation but is incorrectly annotated to "apoptotic process" instead of the more specific regulatory term.

2026-01-18

Apoptosis Subproject Initialization

Created subproject to review apoptotic process annotations on human proteins that have ONLY UniProt Keyword (SPKW) evidence via GO_REF:0000043, with no corroborating evidence from any other method.

Key findings from DuckDB analysis:
- 280 human genes have apoptotic process (GO:0006915 or descendants) annotations derived SOLELY from UniProt Keywords
- These annotations have no corroboration from:
- Experimental evidence (IDA, IMP, IGI, etc.)
- Curator statements (TAS, NAS, IC)
- Computational methods (ISS, ISO, IBA)
- Other IEA pipelines (InterPro, Reactome, etc.)

Source breakdown of ALL IEA apoptotic annotations (for context):
- GO_REF:0000043 (UniProtKB-KW): 539 annotations
- GO_REF:0000107 (Reactome): 458 annotations
- GO_REF:0000117 (UniProt): 71 annotations
- GO_REF:0000002 (InterPro2GO): 44 annotations