Affinage

DDI2

Protein DDI1 homolog 2 · UniProt Q5TDH0

Length
399 aa
Mass
44.5 kDa
Annotated
2026-06-09
36 papers in source corpus 15 papers cited in narrative 15 extracted findings
Cross-family judge vs UniProt: Affinage preferred faithfulness: 8/8 claims corpus-supported (100%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

DDI2 is a ubiquitin-directed aspartyl endoprotease that couples recognition of polyubiquitylated substrates to their proteolytic processing, serving as a central effector of the cellular response to proteotoxic stress (PMID:27528193, PMID:32521225). Its ubiquitin-like (UBL) domain binds K11/K48-branched polyubiquitin conjugates and the 26S proteasome, allowing DDI2 to act as a shuttling factor that delivers ubiquitylated cargo for degradation; blocking its endoprotease activity traps it on ubiquitin conjugates and reduces its proteasome association, impairing protein turnover (PMID:35358511). Its best-defined catalytic function is the cleavage of the transcription factor NRF1 (NFE2L1): after NRF1 is retrotranslocated from the ER into the cytosol and rendered highly polyubiquitylated, DDI2 cleaves it to generate the active, nuclear form that drives proteasome subunit gene transcription, providing a compensatory bounce-back when the proteasome is inhibited (PMID:27528193, PMID:32521225, PMID:31947743). This activity requires both the protease and HDD domains and depends on upstream polyubiquitylation by the E3 ligase UBE4A (PMID:35589686, PMID:37084817). Through NRF1 processing, DDI2 governs proteasome recovery in multiple contexts, including bortezomib-treated multiple myeloma cells, ferroptotic stress, and cadmium-induced metallothionein expression in hepatocytes (PMID:34649278, PMID:39384955, PMID:36248746). Beyond NRF1, DDI2 cleaves angiomotin (AMOT) in a poly-ADP-ribosylation/ubiquitination-dependent manner downstream of an NF2–TNKS1/2–RNF146 axis to release a pro-angiogenic AMOT-CT fragment (PMID:37350545), and it forms a complex with p97 that extracts the secretory protein CCN1 from the ER for lysosomal routing, linking the ubiquitin-proteasome system to the autophagy-lysosome pathway (PMID:41809038). DDI2 is essential for development, as germline knockout mice die at E12.5 with proteotoxic stress, ubiquitin conjugate accumulation, and UPR activation (PMID:39328932). The pharmacological inhibitor nelfinavir directly blocks DDI2 activity and sensitizes cells to proteasome inhibitors and ferroptosis (PMID:32916277, PMID:39384955).

Mechanistic history

Synthesis pass · year-by-year structured walk · 14 steps
  1. 2016 High

    Established that DDI2 is the protease responsible for activating the transcription factor NRF1 under proteasome dysfunction, defining its role in the proteasome bounce-back response.

    Evidence DDI2 knockout with wild-type versus protease-dead add-back, Western blot for NRF1 forms and proteasome activity assays

    PMID:27528193

    Open questions at the time
    • Did not establish whether DDI2 cleaves NRF1 directly or via an intermediate
    • Substrate recognition mechanism unresolved
    • Site of cleavage within the cell not localized
  2. 2020 High

    Demonstrated that DDI2 is a ubiquitin-directed endoprotease that cleaves NRF1 only when highly polyubiquitylated, ruling out deubiquitinase activity and defining the substrate signal.

    Evidence In vitro protease assay with purified DDI2 and polyubiquitylated NRF1, KO cells, mass spectrometry

    PMID:32521225

    Open questions at the time
    • Structural basis of ubiquitin-dependent activation not resolved
    • Did not define the minimal ubiquitin chain architecture required
  3. 2020 Medium

    Localized the DDI2-dependent NRF1 cleavage event to the cytosol following complete retrotranslocation from the ER, defining the compartment of activation.

    Evidence Cell fractionation, DDI2 depletion and protease-dead mutant expression, NRF1 cleavage assays in MDA-MB-231 cells

    PMID:31947743

    Open questions at the time
    • Machinery driving complete NRF1 retrotranslocation not identified
    • Single cell line
  4. 2020 Medium

    Identified nelfinavir as a direct pharmacological inhibitor of DDI2, providing a tool to block NRF1 processing and potentiate proteasome inhibitor cytotoxicity.

    Evidence In vitro DDI2 activity assay with nelfinavir, cellular NFE2L1 cleavage and viability assays

    PMID:32916277

    Open questions at the time
    • Inhibitor is only partially effective and not DDI2-selective
    • Binding mode to DDI2 not structurally defined
  5. 2022 High

    Defined DDI2 as a ubiquitin-shuttling factor whose UBL domain links K11/K48-branched conjugates to the proteasome, explaining how protease activity and substrate delivery are coupled.

    Evidence Affinity co-purification, UBL domain deletion, nelfinavir treatment, purified proteasome binding assays

    PMID:35358511

    Open questions at the time
    • Stoichiometry of DDI2-proteasome engagement unresolved
    • Whether shuttling is general or substrate-restricted not determined
  6. 2022 Medium

    Showed both protease and HDD domains are required for NRF1 activation and that DDI2 upregulation drives bortezomib resistance, establishing therapeutic relevance in multiple myeloma.

    Evidence DDI2 KO in MM cells, domain-mutant add-back, NRF1 cleavage assays, nelfinavir treatment

    PMID:35589686

    Open questions at the time
    • Mechanistic role of the HDD domain not defined
    • Single lab
  7. 2022 High

    Confirmed via reciprocal catalytic-mutant rescue in vitro and in vivo that DDI2 catalytic activity is required for NRF1 nuclear translocation and proteasome recovery after irreversible inhibition.

    Evidence CRISPR KO, wild-type versus catalytically dead add-back, NRF1 immunofluorescence, proteasome activity, in vivo MM models

    PMID:34649278

    Open questions at the time
    • Did not address non-NRF1 substrates in this setting
  8. 2022 Medium

    Established the essential developmental requirement for DDI2, linking its loss to embryonic lethality with proteotoxic stress, UPR, and interferon signatures.

    Evidence Germline/conditional DDI2 KO mice, embryo molecular characterization, surrogate KO cells, transcriptomics

    PMID:39328932

    Open questions at the time
    • Which substrate(s) underlie lethality not pinpointed
    • Origin of the type I interferon signature unresolved
  9. 2022 Medium

    Demonstrated a physiological role for DDI2-NRF1 in hepatic metallothionein induction and cadmium detoxification, distinct from NRF2.

    Evidence Liver-specific Ddi2 KO mice, cadmium exposure, metallothionein and proteasome activity assays

    PMID:36248746

    Open questions at the time
    • Tissue-specificity of this response not broadly mapped
  10. 2023 Medium

    Identified UBE4A as the E3 ligase that polyubiquitylates retrotranslocated NRF1 to license DDI2 cleavage, defining the upstream substrate-priming step.

    Evidence Co-IP, in vitro ubiquitination assay, UBE4A KO and ligase-dead mutant, NRF1 cleavage assays, RT-qPCR

    PMID:37084817

    Open questions at the time
    • Whether other E3 ligases contribute not excluded
    • Chain branching specificity not fully resolved
  11. 2023 High

    Expanded DDI2 substrate repertoire beyond NRF1 by showing it cleaves angiomotin to release a pro-angiogenic fragment downstream of a PARylation/ubiquitination axis.

    Evidence In vitro cleavage assay, genetic KO in zebrafish and mice, AMOT-CT rescue, biochemical epistasis of NF2-TNKS1/2-RNF146

    PMID:37350545

    Open questions at the time
    • Whether AMOT cleavage requires proteasome shuttling like NRF1 not addressed
    • Structural basis of substrate discrimination unknown
  12. 2024 Medium

    Connected DDI2-NRF1 signaling to ferroptosis, showing DDI2 is required for feedback proteasome recovery and that its inhibition sensitizes cells to ferroptotic death.

    Evidence DDI2 KO cells, RSL3-induced ferroptosis, ubiquitylome proteomics, NRF1 cleavage and proteasome activity assays, nelfinavir

    PMID:39384955

    Open questions at the time
    • Mechanistic link between hyperubiquitylation and ferroptosis sensitivity not fully resolved
  13. 2024 Medium

    Dissociated rapid post-inhibitor proteasome recovery from DDI2, showing a transcription-independent, translation-dependent pathway operates before the DDI2-NRF1 program.

    Evidence DDI2 KO cells, time-course proteasome activity assays after pulse inhibition, translation inhibitor experiments

    PMID:38619391

    Open questions at the time
    • Identity of the DDI2-independent recovery factors unknown
  14. 2026 Medium

    Revealed a non-NRF1 role for DDI2 as a p97-associated cargo receptor that extracts secretory CCN1 from the ER to lysosomes, bridging the UPS and autophagy-lysosome systems.

    Evidence DDI2 KO in human and murine cells, CCN1 KO rescue, DDI2-p97 co-IP, CCN1-LAMP1 colocalization, ROS and autophagy flux assays

    PMID:41809038

    Open questions at the time
    • Whether CCN1 routing requires DDI2 protease activity not established
    • Structure of the DDI2-p97 complex unknown

Open questions

Synthesis pass · forward-looking unresolved questions
  • The structural basis by which DDI2 recognizes polyubiquitin and selects diverse substrates (NRF1, AMOT, CCN1), and how protease versus shuttling/cargo-receptor functions are partitioned, remains unresolved.
  • No experimental structure of substrate-bound DDI2
  • Rules governing substrate selectivity undefined
  • Determinants distinguishing cleavage from shuttling unknown

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0140096 catalytic activity, acting on a protein 4 GO:0016787 hydrolase activity 2 GO:0038024 cargo receptor activity 1 GO:0060090 molecular adaptor activity 1 GO:0140097 catalytic activity, acting on DNA 1
Localization
GO:0005829 cytosol 2
Pathway
R-HSA-392499 Metabolism of proteins 3 R-HSA-74160 Gene expression (Transcription) 3 R-HSA-8953897 Cellular responses to stimuli 2
Complex memberships
DDI2-p97 complex

Evidence

Reading pass · 15 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
2016 DDI2 (aspartyl protease) is required to cleave and activate the transcription factor Nrf1 (NFE2L1) in response to proteasome dysfunction. Deletion of DDI2 reduced the cleaved form of Nrf1 and increased the full-length cytosolic form, resulting in poor upregulation of proteasomes. These defects were restored by wild-type DDI2 but not by protease-defective DDI2, establishing that DDI2's protease activity is essential for Nrf1 processing. DDI2 gene deletion (KO), add-back of wild-type vs. protease-dead DDI2, Western blot for Nrf1 forms, proteasome activity assays eLife High 27528193
2020 DDI2 is a ubiquitin-directed endoprotease: it cleaves NRF1 in vitro only when NRF1 is highly poly-ubiquitylated. Purified DDI2 can cleave high-molecular-weight ubiquitylated proteins in cell extracts. No evidence for DDI2 acting as a de-ubiquitylating enzyme was found. DDI2 KO cells, in vitro protease assay with purified DDI2 and poly-ubiquitylated NRF1, mass spectrometry, cell-based accumulation of ubiquitin conjugates Molecular cell High 32521225
2020 NRF1 can be completely retrotranslocated from the ER into the cytosol, where it is then cleaved and activated by DDI2. Expression of a protease-dead point mutant of DDI2 recapitulates the loss-of-function effects on NRF1 activation, confirming that DDI2's protease activity drives cytosolic NRF1 processing. Cell fractionation, DDI2 depletion (siRNA/KD), protease-dead DDI2 point mutant expression, NRF1 cleavage assays in MDA-MB-231 cells International journal of molecular sciences Medium 31947743
2022 DDI2 functions as a ubiquitin-shuttling factor: its ubiquitin-like (UBL) domain mediates binding to ubiquitin conjugates (K11/K48 branched chains) and to the proteasome. Adding Ub conjugates to cell extracts increases Ddi2 association with proteasomes; adding Ddi2 increases Ub conjugate binding to purified proteasomes. Blocking DDI2 endoprotease activity (genetically or with nelfinavir) increases its binding to Ub conjugates but decreases its binding to proteasomes, reducing protein degradation. Affinity co-purification, deletion of UBL domain, nelfinavir treatment, purified proteasome binding assays, Ub conjugate accumulation assays The Journal of biological chemistry High 35358511
2022 Both the protease domain and the HDD domain of DDI2 are required to activate NRF1 in multiple myeloma cells. DDI2 expression is upregulated upon prolonged bortezomib treatment, contributing to bortezomib resistance via enhanced NRF1 activation. DDI2 KO in MM cells, domain mutant add-back experiments, NRF1 cleavage assays, nelfinavir (partial DDI2 protease inhibitor) treatment Cell death & disease Medium 35589686
2022 DDI2 KO in multiple myeloma cells blocks NRF1 cleavage and nuclear translocation, impairing proteasome activity recovery upon irreversible proteasome inhibition. Add-back of wild-type but not catalytically dead DDI2 fully rescues these phenotypes, confirming DDI2 catalytic activity is necessary. DDI2 KO (CRISPR), wild-type vs. catalytically dead DDI2 add-back, NRF1 localization by immunofluorescence, proteasome activity assays, in vitro and in vivo MM models Blood advances High 34649278
2020 Nelfinavir (an HIV protease inhibitor) directly inhibits DDI2 activity, blocking NFE2L1 (NRF1) proteolysis and potentiating cytotoxicity of proteasome inhibitors in cancer cells. DDI2 protease activity assay with nelfinavir, NFE2L1 cleavage assays in cells, cell viability assays Cellular signalling Medium 32916277
2023 E3 ubiquitin ligase UBE4A catalyzes polyubiquitination of retrotranslocated NRF1 and promotes its cleavage by DDI2. UBE4A interacts with NRF1, and in vitro recombinant UBE4A promotes ubiquitination of retrotranslocated NRF1. Depletion of UBE4A reduces ubiquitin modification on NRF1, shortens polyubiquitin chain length, decreases DDI2-mediated cleavage efficiency, and reduces proteasomal subunit transcription. Co-IP (UBE4A–NRF1 interaction), in vitro ubiquitination assay, UBE4A KO/depletion, ligase-dead mutant expression, NRF1 cleavage assays, RT-qPCR for proteasome subunits Biochimica et biophysica acta. Gene regulatory mechanisms Medium 37084817
2023 DDI2 proteolytically cleaves angiomotin (AMOT) to generate an AMOT-CT fragment that promotes angiogenesis. AMOT cleavage by DDI2 is regulated upstream by a signaling axis: NF2 controls AMOT membrane localization, TNKS1/2 catalyzes poly-ADP ribosylation of AMOT, and RNF146 catalyzes AMOT ubiquitination — all required for DDI2-mediated AMOT cleavage. Genetic inactivation of AMOT cleavage regulators in zebrafish and mice causes defective angiogenesis rescued by AMOT-CT overexpression. In vitro cleavage assay (DDI2 + AMOT), genetic KO in zebrafish and mice, rescue with AMOT-CT, co-IP/biochemical epistasis for NF2-TNKS1/2-RNF146-DDI2 axis The EMBO journal High 37350545
2024 DDI2-mediated NRF1 (NFE2L1) proteolytic cleavage is critical for ferroptosis-induced feedback regulation of proteasome function. Cells lacking DDI2 cannot activate NFE2L1 in response to RSL3-induced ferroptosis, showing global hyperubiquitylation and diminished proteasomal activity. Nelfinavir (DDI2 inhibitor) sensitizes cells to ferroptosis. DDI2 KO cells, RSL3-induced ferroptosis, ubiquitylome proteomics, NRF1 cleavage assays, proteasome activity assays, nelfinavir treatment Cell death and differentiation Medium 39384955
2022 DDI2 KO mice die at embryonic day E12.5 with severe developmental failure, characterized by insufficient proteasome expression, proteotoxic stress, accumulation of high-molecular-weight ubiquitin conjugates, induction of the unfolded protein response, and activation of cell death pathways. In DDI2 surrogate KO cells, proteotoxic stress activates the integrated stress response and induces a type I interferon signature. Conditional/germline DDI2 KO in mice, molecular characterization of embryos (ubiquitin conjugates, UPR markers, proteasome activity), surrogate KO cell lines, transcriptomics iScience Medium 39328932
2022 Liver-specific DDI2 KO mice demonstrate that DDI2 contributes to metallothionein (MT) expression in hepatocytes at baseline and upon cadmium (Cd) exposure through DDI2-mediated NRF1 proteolytic maturation. Cd exposure inhibits proteasome activity, resulting in DDI2-mediated NRF1 cleavage; DDI2 deficiency sensitizes cells to Cd toxicity. NRF2 does not contribute to MT production in this context. Liver-specific Ddi2 KO mice, cadmium exposure, MT expression assays, proteasome activity assays, genetic analysis comparing NRF1 vs NRF2 contribution iScience Medium 36248746
2024 Early recovery of proteasome activity after pulse treatment with proteasome inhibitors is DDI2-independent: it occurs before transcription of proteasomal genes is upregulated but requires protein translation. This establishes a DDI2- and transcription-independent pathway for rapid proteasome activity recovery. DDI2 KO cells, time-course proteasome activity assays after pulse treatment with proteasome inhibitors, translation inhibitor experiments eLife Medium 38619391
2026 Loss of DDI2 leads to proteotoxic accumulation of the secretory protein CCN1, which is normally extracted from the ER by a DDI2-p97 complex and directed to lysosomes. In the absence of DDI2, CCN1 builds up, generates reactive oxygen species, and triggers compensatory autophagy. DDI2 functions as a selective cargo receptor linking the UPS and the autophagy-lysosome pathway. DDI2 KO in human and murine cells, CCN1 KO rescue, DDI2-p97 co-IP complex identification, CCN1-LAMP1 colocalization (immunofluorescence), ROS measurement, autophagy flux assays iScience Medium 41809038
2020 Comparative structural analysis of retroviral and retroviral-like protease domains shows that DDI2 contains a retroviral protease-like domain and that the mode of dimerization and density of intermonomeric contacts differ between DDI1/DDI2 and canonical retroviral proteases, correlating with evolutionary relationships. Structural bioinformatics analysis of PDB entries, multiple sequence and structure alignments International journal of molecular sciences Low 32079302

Source papers

Stage 0 corpus · 36 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
2016 The aspartyl protease DDI2 activates Nrf1 to compensate for proteasome dysfunction. eLife 152 27528193
2020 DDI2 Is a Ubiquitin-Directed Endoprotease Responsible for Cleavage of Transcription Factor NRF1. Molecular cell 68 32521225
2005 Mice without the regulator gene Rsc1A1 exhibit increased Na+-D-glucose cotransport in small intestine and develop obesity. Molecular and cellular biology 50 15601832
2006 RS1 (RSC1A1) regulates the exocytotic pathway of Na+-D-glucose cotransporter SGLT1. American journal of physiology. Renal physiology 36 16788146
2020 Disabling the Protease DDI2 Attenuates the Transcriptional Activity of NRF1 and Potentiates Proteasome Inhibitor Cytotoxicity. International journal of molecular sciences 35 31947743
2003 Downregulation of the Na(+)- D-glucose cotransporter SGLT1 by protein RS1 (RSC1A1) is dependent on dynamin and protein kinase C. The Journal of membrane biology 35 14724758
2022 Multiple myeloma cells depend on the DDI2/NRF1-mediated proteasome stress response for survival. Blood advances 28 34649278
2007 Tripeptides of RS1 (RSC1A1) inhibit a monosaccharide-dependent exocytotic pathway of Na+-D-glucose cotransporter SGLT1 with high affinity. The Journal of biological chemistry 28 17686765
2006 Transporter regulator RS1 (RSC1A1) coats the trans-Golgi network and migrates into the nucleus. American journal of physiology. Renal physiology 27 16788147
2022 The aspartyl protease DDI2 drives adaptation to proteasome inhibition in multiple myeloma. Cell death & disease 21 35589686
2020 Nelfinavir inhibits human DDI2 and potentiates cytotoxicity of proteasome inhibitors. Cellular signalling 21 32916277
2015 Phosphorylation of RS1 (RSC1A1) Steers Inhibition of Different Exocytotic Pathways for Glucose Transporter SGLT1 and Nucleoside Transporter CNT1, and an RS1-Derived Peptide Inhibits Glucose Absorption. Molecular pharmacology 21 26464324
2024 Activating the NFE2L1-ubiquitin-proteasome system by DDI2 protects from ferroptosis. Cell death and differentiation 18 39384955
2015 Two duplicated genes DDI2 and DDI3 in budding yeast encode a cyanamide hydratase and are induced by cyanamide. The Journal of biological chemistry 17 25847245
2019 MicroRNA-3607 inhibits the tumorigenesis of colorectal cancer by targeting DDI2 and regulating the DNA damage repair pathway. Apoptosis : an international journal on programmed cell death 15 31134446
2022 LncRNA FAM13A-AS1 Regulates Proliferation and Apoptosis of Cervical Cancer Cells by Targeting miRNA-205-3p/DDI2 Axis. Journal of oncology 14 35783157
2022 Mammalian Ddi2 is a shuttling factor containing a retroviral protease domain that influences binding of ubiquitylated proteins and proteasomal degradation. The Journal of biological chemistry 13 35358511
2018 RS1 (Rsc1A1) deficiency limits cerebral SGLT1 expression and delays brain damage after experimental traumatic brain injury. Journal of neurochemistry 13 30022488
2009 Novel shuttling domain in a regulator (RSC1A1) of transporter SGLT1 steers cell cycle-dependent nuclear location. Traffic (Copenhagen, Denmark) 13 19765263
2023 Proteolytic activation of angiomotin by DDI2 promotes angiogenesis. The EMBO journal 11 37350545
2020 Dimer Interface Organization is a Main Determinant of Intermonomeric Interactions and Correlates with Evolutionary Relationships of Retroviral and Retroviral-Like Ddi1 and Ddi2 Proteases. International journal of molecular sciences 10 32079302
2019 Fine-tuning the expression of target genes using a DDI2 promoter gene switch in budding yeast. Scientific reports 10 31467340
2023 UBE4A catalyzes NRF1 ubiquitination and facilitates DDI2-mediated NRF1 cleavage. Biochimica et biophysica acta. Gene regulatory mechanisms 9 37084817
2016 Protein RS1 (RSC1A1) Downregulates the Exocytotic Pathway of Glucose Transporter SGLT1 at Low Intracellular Glucose via Inhibition of Ornithine Decarboxylase. Molecular pharmacology 9 27555600
2022 The protease DDI2 regulates NRF1 activation in response to cadmium toxicity. iScience 8 36248746
2019 Structure of Ddi2, a highly inducible detoxifying metalloenzyme from Saccharomyces cerevisiae. The Journal of biological chemistry 8 31152065
2023 In-silico identification of novel DDI2 inhibitor in glioblastoma via repurposing FDA approved drugs using molecular docking and MD simulation study. Journal of biomolecular structure & dynamics 6 37139547
2015 The tomato DDI2, a PCNA ortholog, associating with DDB1-CUL4 complex is required for UV-damaged DNA repair and plant tolerance to UV stress. Plant science : an international journal of experimental plant biology 6 25900570
2024 DDI2 protease controls embryonic development and inflammation via TCF11/NRF1. iScience 5 39328932
2022 DDI2 promotes tumor metastasis and resists antineoplastic drugs-induced apoptosis in colorectal cancer. Apoptosis : an international journal on programmed cell death 5 36520320
2022 Transcriptional activation of budding yeast DDI2/3 through chemical modifications of Fzf1. Cell biology and toxicology 4 35809138
2018 A Modified Tripeptide Motif of RS1 (RSC1A1) Down-Regulates Exocytotic Pathways of Human Na+-d-glucose Cotransporters SGLT1, SGLT2, and Glucose Sensor SGLT3 in the Presence of Glucose. Molecular pharmacology 3 30355744
2025 Deficiency of DDI2 suppresses liver cancer progression by worsening cell survival conditions. Free radical biology & medicine 1 40049338
2024 Early recovery of proteasome activity in cells pulse-treated with proteasome inhibitors is independent of DDI2. eLife 1 38619391
2026 Loss of DDI2 rewires proteostasis through CCN1-driven compensatory autophagy. iScience 0 41809038
2023 Early recovery of proteasome activity in cells pulse-treated with proteasome inhibitors is independent of DDI2. bioRxiv : the preprint server for biology 0 37577495

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