Affinage

NME4

Nucleoside diphosphate kinase D, mitochondrial · UniProt O00746

Length
187 aa
Mass
20.7 kDa
Annotated
2026-04-29
25 papers in source corpus 12 papers cited in narrative 12 extracted findings

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

NME4 (NDPK-D/NM23-H4) is a mitochondrial nucleoside diphosphate kinase that functions as a bifunctional molecular switch governing mitochondrial integrity, lipid signaling, and metastasis suppression. The processed hexameric enzyme resides in the mitochondrial intermembrane space, where it binds the inner membrane via electrostatic interaction between its RRK motif (Arg-90) and cardiolipin; in this membrane-bound state it cross-links membranes and selectively transfers cardiolipin to the outer membrane surface, generating an 'eat-me' signal recognized by LC3 to initiate mitophagy, while also coupling with OPA1-dependent GTP supply to support oxidative phosphorylation (PMID:10799505, PMID:18635542, PMID:23150663, PMID:26742431). Loss of NME4 kinase or membrane-binding function causes mitochondrial fragmentation, a metabolic shift to glycolysis, epithelial–mesenchymal transition, and enhanced metastasis in vivo, establishing NME4 as a metastasis suppressor that operates through JNK-TIMP1-MMP and NFκB2-CCL5 signaling axes (PMID:34674701, PMID:25233933, PMID:39016535). NME4 protein turnover is controlled by RNF6-mediated K48-linked ubiquitination targeting it for proteasomal degradation, while SIRT1-dependent deacetylation regulates its nuclear-cytoplasmic partitioning (PMID:41616518, PMID:26426123).

Mechanistic history

Synthesis pass · year-by-year structured walk · 10 steps
  1. 2000 High

    Establishing that NME4 encodes a mitochondrial NDP kinase resolved its enzymatic identity and organellar context: the full-length precursor is inactive, and import-coupled cleavage of the N-terminal extension activates the hexameric enzyme at mitochondrial membranes.

    Evidence Recombinant expression, X-ray crystallography of hexamer, NDP kinase assays, GFP-fusion confocal microscopy, and subcellular fractionation in HEK293 cells

    PMID:10799505

    Open questions at the time
    • Precise sub-mitochondrial topology (inner vs. outer membrane contact sites) not resolved
    • No identification of the protease responsible for N-terminal cleavage
    • Physiological substrates in vivo not determined
  2. 2008 High

    Demonstrating that Arg-90-dependent cardiolipin binding tethers NME4 to the inner membrane and is required for functional coupling to oxidative phosphorylation answered how the kinase integrates with the respiratory chain.

    Evidence Surface plasmon resonance with model liposomes, R90D mutagenesis, respiration assays and latency measurements in HeLa mitochondria

    PMID:18635542

    Open questions at the time
    • Stoichiometry of NME4–cardiolipin interaction not quantified
    • Whether NME4 contacts other lipid species at physiological ratios unknown
    • Structural basis of hexamer-mediated membrane cross-linking not resolved at atomic level
  3. 2012 High

    Revealing that NME4 selectively transfers cardiolipin from the inner to the outer mitochondrial membrane—while simultaneously forming a complex with the GTPase OPA1—established its dual role as both a lipid transfer protein and a local GTP supplier.

    Evidence LC-MS lipidomics of outer membrane fractions, Co-IP of NME4–OPA1 in rat liver, apoptosis assays (cytochrome c release, caspase 3/7) in HeLa cells with wild-type versus membrane-binding-deficient mutant

    PMID:23150663

    Open questions at the time
    • Whether NME4 directly channels GTP to OPA1 or acts indirectly not distinguished
    • Cardiolipin transfer mechanism (tunnel, flip-flop, or facilitated diffusion) undetermined
    • Reciprocal OPA1-to-NME4 regulation not tested
  4. 2014 Medium

    Placing NME4 upstream of JNK–TIMP1–MMP signaling in oral cancer provided the first pathway-level explanation for its invasion-suppressive function, with miR-196 identified as a direct negative regulator of NME4 mRNA.

    Evidence Luciferase reporter assay confirming miR-196 targeting of NME4 3′ UTR, migration/invasion assays, downstream marker analysis in oral cancer cells

    PMID:25233933

    Open questions at the time
    • Whether JNK activation by NME4 loss is direct or secondary to mitochondrial dysfunction not clarified
    • Single cancer type tested
    • No in vivo metastasis data
  5. 2015 Medium

    Discovering that SIRT1 deacetylates NME4 and that acetylation status controls its nuclear versus cytoplasmic distribution revealed a post-translational regulatory axis beyond mitochondrial function.

    Evidence Yeast two-hybrid identification of SIRT1, Co-IP confirmation, acetylation-mimic mutagenesis, confocal localization, apoptosis assays in N1E-115 cells and mouse cortex knockdown

    PMID:26426123

    Open questions at the time
    • Identity of the acetyltransferase is unknown
    • Specific acetylated lysine residues on NME4 not fully mapped by mass spectrometry
    • Nuclear function of NME4 remains uncharacterized
  6. 2016 High

    Showing that NME4-mediated cardiolipin externalization serves as an LC3-recognized 'eat-me' signal for mitophagy unified the lipid-transfer and quality-control roles, with NME4 required across multiple mitophagy inducers and cell types.

    Evidence RNAi knockdown and R90D mutant analysis, CCCP/rotenone/6-OHDA-induced mitophagy assays, proximity ligation assay for NME4–OPA1, in MLE-12, HeLa, and SH-SY5Y cells

    PMID:26742431

    Open questions at the time
    • Whether NME4 cooperates with PINK1/Parkin pathway or acts in parallel not determined
    • Degree of cardiolipin externalization required for LC3 recognition not quantified
    • In vivo relevance in neurodegeneration models not established
  7. 2021 High

    Comprehensive loss-of-function analysis established NME4 as a bona fide metastasis suppressor: loss of either kinase or membrane-binding activity caused mitochondrial fragmentation, metabolic reprogramming to glycolysis, EMT, and metastasis in xenograft models.

    Evidence Kinase-dead and membrane-binding-deficient mutants, RNAi knockdown, in vitro migration/invasion, EMT markers, in vivo xenograft metastasis in immunocompromised mice, metabolic profiling

    PMID:34674701

    Open questions at the time
    • Whether the two functions (kinase and lipid transfer) contribute equally to suppression is unresolved
    • Relevance to immunocompetent tumor microenvironment not addressed in this study
    • Downstream effectors linking metabolic shift to EMT not fully mapped
  8. 2023 Medium

    Hepatic Nme4 knockout revealed an unexpected metabolic role: NME4 interacts with CoA-metabolizing enzymes and its loss suppresses acetyl-CoA/malonyl-CoA accumulation and steatosis, expanding its function beyond cancer biology.

    Evidence Liver-specific Nme4 knockout mice on high-fat diet, proteomics, metabolomics, CoA metabolite quantification

    PMID:38177901

    Open questions at the time
    • Whether NME4 directly phosphorylates CoA pathway enzymes or acts indirectly is unclear
    • Relevance to human NAFLD not yet demonstrated
    • Interaction with CoA enzymes not validated by reciprocal pull-down
  9. 2024 Medium

    In esophageal squamous cell carcinoma, NME4 suppresses NFκB2-CCL5 signaling and thereby limits CD8+ T cell infiltration, connecting its tumor-suppressive function to immune modulation in the tumor microenvironment.

    Evidence Syngeneic C57BL/6 tumor model, single-cell RNA sequencing, quantitative proteomics, protein microarray in murine ESCC cells

    PMID:39016535

    Open questions at the time
    • Mechanism by which NME4 suppresses NFκB2 activity not defined
    • Whether immune modulation is direct or secondary to mitochondrial dysfunction unclear
    • Single tumor type in syngeneic setting
  10. 2026 Medium

    Identification of RNF6 as the E3 ligase that K48-ubiquitinates NME4 for proteasomal degradation, activating JNK/c-JUN, defined the major degradation pathway controlling NME4 protein levels in ovarian cancer.

    Evidence Co-IP of RNF6–NME4, K48-linked ubiquitination assay, cycloheximide chase, rescue experiments, nude mouse xenograft

    PMID:41616518

    Open questions at the time
    • Specific ubiquitinated lysine residues on NME4 not mapped
    • Whether RNF6-NME4 axis operates in non-cancer contexts unknown
    • Deubiquitinase that opposes RNF6 not identified

Open questions

Synthesis pass · forward-looking unresolved questions
  • How NME4's two biochemical activities—NDP kinase and cardiolipin transfer—are coordinately regulated in vivo, and whether its nuclear pool performs distinct functions, remain major open questions.
  • No structural model of NME4 bound to cardiolipin at atomic resolution
  • Nuclear function of NME4 entirely uncharacterized
  • Relationship between NME4-mediated mitophagy and PINK1/Parkin pathway not resolved

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0008289 lipid binding 3 GO:0016740 transferase activity 3 GO:0098772 molecular function regulator activity 3 GO:0140104 molecular carrier activity 2
Localization
GO:0005739 mitochondrion 4 GO:0005634 nucleus 1
Pathway
R-HSA-1643685 Disease 4 R-HSA-1430728 Metabolism 3 R-HSA-5357801 Programmed Cell Death 2 R-HSA-9612973 Autophagy 2
Partners
Complex memberships
NDPK-D hexamer

Evidence

Reading pass · 12 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
2000 NME4 (Nm23-H4) encodes a mitochondrial nucleoside diphosphate kinase; the full-length protein is inactive due to its N-terminal mitochondrial targeting extension, while the truncated form lacking the extension possesses NDP kinase activity. Import into mitochondria is accompanied by cleavage of the N-terminal extension, restoring activity. X-ray crystallography confirmed the protein forms a hexamer, and submito-chondrial fractionation showed it is associated with mitochondrial membranes, possibly at contact sites between outer and inner membranes. Recombinant protein expression in E. coli, NDP kinase activity assay, X-ray crystallography, site-directed mutagenesis (S129P), GFP-fusion confocal microscopy, Western blot subcellular fractionation in HEK293 cells The Journal of biological chemistry High 10799505
2008 NME4/NDPK-D binds the inner mitochondrial membrane primarily through electrostatic interaction with cardiolipin (the anionic phospholipid most enriched in the inner membrane), mediated by a surface-exposed basic RRK motif (Arg-90). Mutation R90D strongly reduces phospholipid binding in vitro and in vivo. The membrane-bound state of NME4 is required for functional coupling with oxidative phosphorylation (respiration stimulated by TDP only in mitochondria expressing wild-type, not R90D, NME4). NME4's symmetrical hexameric structure allows it to cross-link anionic phospholipid-containing liposomes, suggesting a role in promoting intermembrane contacts. Surface plasmon resonance with recombinant protein and model liposomes, site-directed mutagenesis (R90D), stable expression in HeLa cells, respiration assays, latency assays with isolated mitochondria, antibody binding to mitoplasts The Journal of biological chemistry High 18635542
2012 NME4 has a dual function acting as a mitochondrial switch: (1) phosphotransfer/NDP kinase activity supplying GTP locally, and (2) selective intermembrane cardiolipin transfer from inner to outer mitochondrial membrane. Cardiolipin binding inhibits NDP kinase activity but is required for lipid transfer. Wild-type NME4 (but not a membrane-binding-deficient mutant) selectively increased cardiolipin content in the outer mitochondrial membrane. NME4 forms a complex with the mitochondrial GTPase OPA1 in rat liver, suggesting direct local GTP delivery. Wild-type NME4-expressing HeLa cells showed increased Bax accumulation in mitochondria and were sensitized to rotenone-induced apoptosis (cytochrome c release, caspase 3/7 activation, annexin V binding). Co-immunoprecipitation (NME4-OPA1 complex), LC-MS lipid analysis of HeLa cells expressing wild-type vs. membrane-binding-deficient mutant NME4, apoptosis assays (cytochrome c release, caspase 3/7, annexin V), molecular modeling The Journal of biological chemistry High 23150663
2016 NME4/NDPK-D facilitates translocation of cardiolipin from the inner mitochondrial membrane to the outer mitochondrial membrane surface upon mitophagy induction (CCCP treatment), enabling cardiolipin to serve as an 'eat-me' signal recognized by LC3. RNAi knockdown of NME4 decreased CCCP-induced CL externalization and mitochondrial degradation. The CL-binding deficient mutant R90D was inactive in promoting mitophagy. Proximity ligation assay showed NME4's CL-transfer activity is closely associated with the dynamin-like GTPase OPA1, implicating fission-fusion dynamics. NME4 knockdown also suppressed rotenone- and 6-hydroxydopamine-triggered mitophagy in SH-SY5Y cells. RNAi knockdown, CCCP/rotenone/6-OHDA-induced mitophagy, CL externalization assay, R90D mutant functional analysis, in situ proximity ligation assay (PLA) for NME4-OPA1 association, mitochondrial degradation assays in MLE-12, HeLa, and SH-SY5Y cells Cell death and differentiation High 26742431
2015 NME4/NDPK-D is acetylated, and its acetylation state regulates its subcellular localization between nucleus and cytoplasm, as well as cell survival. SIRT1 was identified as a binding partner of NME4 by yeast two-hybrid screening, confirmed by co-immunoprecipitation. SIRT1 inhibition increases NME4 acetylation. Overexpression of NME4 with SIRT1, or mutation of acetylated lysine residues in NME4, increases nuclear accumulation. Acetylation-mimic mutant NME4 increased apoptosis in N1E-115 cells. NME4 knockdown induced apoptosis in neuroblastoma cells and mouse cortex. Yeast two-hybrid screening, co-immunoprecipitation, site-directed mutagenesis (acetylation-mimic), SIRT1 inhibitor treatment, confocal microscopy, apoptosis assays, in vivo knockdown in mouse cortex PloS one Medium 26426123
2014 NME4 suppresses cell migration and invasion in oral cancer through the NME4-JNK-TIMP1-MMP signaling pathway; miR-196 inhibits NME4 expression, thereby activating p-JNK, suppressing TIMP1, and augmenting MMP1/9, promoting invasive phenotype. miR-196 overexpression/inhibition, RT-qPCR, Western blot, luciferase reporter assay for miR-196 targeting of NME4 3'UTR, cell migration and invasion assays, confocal microscopy Molecular cancer Medium 25233933
2021 NME4 acts as a metastasis suppressor in cancer cells. Loss-of-function mutations (lacking either NDP kinase activity or membrane interaction) or RNAi depletion of NME4 promoted epithelial-mesenchymal transition, increased migratory and invasive potential, and increased metastasis formation in immunocompromised mice. Mechanistically, NME4 loss caused mitochondrial fragmentation and loss, metabolic switch from respiration to glycolysis, and increased ROS generation, triggering pro-metastatic signaling cascades. Loss-of-function mutants (kinase-dead and membrane interaction-deficient), RNAi knockdown, in vitro migration/invasion assays, EMT marker analysis, in vivo xenograft metastasis model in immunocompromised mice, metabolic profiling BMC biology High 34674701
2023 NME4 interacts with key enzymes in coenzyme A (CoA) metabolism and increases the levels of acetyl-CoA and malonyl-CoA in the liver, promoting triglyceride accumulation and NAFLD progression. Hepatic deletion of Nme4 in mice suppressed hepatic steatosis progression. Hepatic-specific Nme4 knockout in mice (high-fat diet model), proteomics, metabolomics, CoA metabolite measurements EMBO reports Medium 38177901
2024 NME4 negatively regulates the NFκB2-CCL5 signaling axis in esophageal squamous cell carcinoma, preventing CD8+ T cell infiltration into the tumor microenvironment. Mechanistically, NME4 suppresses NFκB2 activity, which controls CCL5 chemokine expression. Syngeneic tumor model in C57BL/6 mice, single-cell RNA sequencing, quantitative proteomics, protein microarray screening, NME4 modulation in murine ESCC cell line AKR Immunology Medium 39016535
2021 Let-7f-5p miRNA directly targets the 3' UTR of Nme4 mRNA and negatively regulates Nme4 expression in mouse bone marrow-derived mesenchymal stem cells (BM-MSCs). TNF-α upregulates let-7f-5p (via NF-κB), reducing Nme4 and impairing osteogenic differentiation. Ectopic Nme4 expression reversed the inhibitory effects of let-7f-5p on osteogenesis in vitro and restored bone formation in ovariectomized mice in vivo. miRNA mimic/inhibitor transfection, luciferase reporter assay (let-7f-5p targeting Nme4 3'UTR), NME4 overexpression rescue, in vivo ovariectomized mouse model, osteogenic differentiation assays (ALP, Alizarin Red staining) Biochemistry and cell biology Medium 34297624
2026 E3 ubiquitin ligase RNF6 directly binds NME4 and promotes its K48-linked polyubiquitination, leading to proteasomal degradation of NME4. NME4 degradation by RNF6 activates the JNK/c-JUN signaling pathway, promoting ovarian cancer malignancy. Co-immunoprecipitation (RNF6-NME4 interaction), cycloheximide chase assay, ubiquitination assay (K48-linked), RNF6/NME4 co-modulation rescue experiments, in vivo nude mouse xenograft model Pathology, research and practice Medium 41616518
2024 Conserved Arg27 across group I NDPKs (NME1-4) is a key residue for hexamer assembly; Arg27 mutation leads to decreased binding affinity, altered dynamics, and complex destabilization. For NME4 specifically, double and triple Arg mutations destabilize the hexamer into a dimer, partly due to its shorter C-terminal region. Molecular dynamics simulations, structural modeling, binding affinity calculations with mutant NME4 constructs bioRxivpreprint Low bio_10.1101_2024.09.19.613900

Source papers

Stage 0 corpus · 25 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
2016 NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy. Cell death and differentiation 164 26742431
2005 Cation [M = H+, Li+, Na+, K+, Ca2+, Mg2+, NH4+, and NMe4+] interactions with the aromatic motifs of naturally occurring amino acids: a theoretical study. The journal of physical chemistry. A 152 16834293
2000 The human nm23-H4 gene product is a mitochondrial nucleoside diphosphate kinase. The Journal of biological chemistry 126 10799505
1997 nm23-H4, a new member of the family of human nm23/nucleoside diphosphate kinase genes localised on chromosome 16p13. Human genetics 115 9099850
2012 Dual function of mitochondrial Nm23-H4 protein in phosphotransfer and intermembrane lipid transfer: a cardiolipin-dependent switch. The Journal of biological chemistry 95 23150663
2014 OncomiR-196 promotes an invasive phenotype in oral cancer through the NME4-JNK-TIMP1-MMP signaling pathway. Molecular cancer 84 25233933
2008 The nucleoside diphosphate kinase D (NM23-H4) binds the inner mitochondrial membrane with high affinity to cardiolipin and couples nucleotide transfer with respiration. The Journal of biological chemistry 83 18635542
2009 Interaction of NDPK-D with cardiolipin-containing membranes: Structural basis and implications for mitochondrial physiology. Biochimie 36 19254751
2017 NME4/nucleoside diphosphate kinase D in cardiolipin signaling and mitophagy. Laboratory investigation; a journal of technical methods and pathology 30 29035377
2018 The mitochondrial nucleoside diphosphate kinase (NDPK-D/NME4), a moonlighting protein for cell homeostasis. Laboratory investigation; a journal of technical methods and pathology 27 29491425
2021 The mitochondrially-localized nucleoside diphosphate kinase D (NME4) is a novel metastasis suppressor. BMC biology 26 34674701
2005 Expression of the nm23 homologues nm23-H4, nm23-H6, and nm23-H7 in human gastric and colon cancer. The Journal of pathology 25 15726650
2015 Acetylation of NDPK-D Regulates Its Subcellular Localization and Cell Survival. PloS one 20 26426123
2011 Probing Lewis acidity of Y(BH4)3 via its reactions with MBH4 (M = Li, Na, K, NMe4). Dalton transactions (Cambridge, England : 2003) 19 22052250
2019 NME4 may enhance non‑small cell lung cancer progression by overcoming cell cycle arrest and promoting cellular proliferation. Molecular medicine reports 17 31257488
2014 Mitochondrial NM23-H4/NDPK-D: a bifunctional nanoswitch for bioenergetics and lipid signaling. Naunyn-Schmiedeberg's archives of pharmacology 15 25231795
2024 NME4 suppresses NFκB2-CCL5 axis, restricting CD8+ T cell tumour infiltration in oesophageal squamous cell carcinoma. Immunology 12 39016535
2001 Overexpression of nm23-H4 RNA in colorectal and renal tumours. Anticancer research 12 11724361
2020 NME4 modulates PD-L1 expression via the STAT3 signaling pathway in squamous cell carcinoma. Biochemical and biophysical research communications 11 32192776
2023 NME4 mediates metabolic reprogramming and promotes nonalcoholic fatty liver disease progression. EMBO reports 8 38177901
2020 Widely targeted metabolomic analyses unveil the metabolic variations after stable knock-down of NME4 in esophageal squamous cell carcinoma cells. Molecular and cellular biochemistry 6 32504364
2023 Differential Expression of NME4 in Trophoblast Stem-Like Cells and Peripheral Blood Mononuclear Cells of Normal Pregnancy and Preeclampsia. Journal of Korean medical science 3 37096311
2021 The let-7f-5p-Nme4 pathway mediates tumor necrosis factor α-induced impairment in osteogenesis of bone marrow-derived mesenchymal stem cells. Biochemistry and cell biology = Biochimie et biologie cellulaire 2 34297624
2026 RNF6 activates JNK/c-JUN pathway in ovarian cancer by promoting K48-linked NME4 ubiquitination. Pathology, research and practice 0 41616518
2024 Creatine kinase elevation in chronic hepatitis B patients with telbivudine therapy: influence of telbivudine plasma concentration and single nucleotide polymorphisms of TK2, RRM2B, and NME4. European journal of clinical pharmacology 0 38502357