Affinage

NME4

Nucleoside diphosphate kinase D, mitochondrial · UniProt O00746

Length
187 aa
Mass
20.7 kDa
Annotated
2026-06-10
25 papers in source corpus 12 papers cited in narrative 12 extracted findings
Cross-family judge vs UniProt: tie faithfulness: 5/6 claims corpus-supported (83%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

NME4 (NDPK-D/Nm23-H4) is a mitochondrial nucleoside diphosphate kinase that doubles as a cardiolipin-binding lipid transfer protein, linking nucleotide phosphotransfer to the regulation of mitochondrial membrane lipid composition, apoptosis, mitophagy, and metabolism (PMID:10799505, PMID:23150663). The protein is imported into mitochondria where cleavage of an N-terminal targeting extension relieves an autoinhibitory constraint to activate NDP kinase activity, and the active enzyme assembles into a hexamer that associates peripherally with the inner membrane (PMID:10799505). Membrane binding occurs through electrostatic interaction with cardiolipin via the surface-exposed RRK motif, with Arg90 being essential; this membrane-bound state couples NDPK-D phosphotransfer to oxidative phosphorylation (PMID:18635542). The symmetrical hexamer cross-links anionic-phospholipid membranes and, upon cardiolipin binding, switches from kinase activity to selective intermembrane transfer of cardiolipin, moving it from the inner to the outer membrane where it serves as both a pro-apoptotic and a mitophagy signal; this lipid-transfer function requires the membrane-binding state and is spatially coupled to the dynamin-like GTPase OPA1 (PMID:23150663, PMID:26742431). Consistent with a role in mitochondrial integrity, loss of either NDP kinase activity or membrane binding drives mitochondrial fragmentation, a glycolytic metabolic shift, increased ROS, epithelial-mesenchymal transition, and metastasis, establishing NME4 as a metastasis suppressor (PMID:34674701). NME4 abundance and localization are further controlled post-translationally: SIRT1-mediated deacetylation regulates its acetylation state and nuclear accumulation (PMID:26426123), and RNF6-mediated K48-linked polyubiquitination targets it for proteasomal degradation (PMID:41616518).

Mechanistic history

Synthesis pass · year-by-year structured walk · 9 steps
  1. 2000 High

    Established that NME4 is a mitochondrial NDP kinase whose activity is gated by import-coupled processing, answering how its enzymatic function is spatially and structurally regulated.

    Evidence X-ray crystallography, GFP-fusion confocal microscopy, subcellular fractionation, and in vitro activity assays in HEK293 cells

    PMID:10799505

    Open questions at the time
    • Did not define the lipid determinants of membrane association
    • Did not address functions beyond phosphotransfer
  2. 2008 High

    Identified cardiolipin as the principal membrane anchor of NDPK-D via the Arg90 RRK motif and showed that membrane binding couples the kinase to oxidative phosphorylation, explaining the functional basis of its inner-membrane association.

    Evidence Surface plasmon resonance with liposomes, R90D mutagenesis, mitochondrial respiration assays, and submitochondrial fractionation

    PMID:18635542

    Open questions at the time
    • Did not establish a non-kinase function for the membrane-bound protein
    • Mechanism of respiratory coupling (partner identity) not fully resolved here
  3. 2012 High

    Revealed a moonlighting lipid-transfer function whereby cardiolipin binding switches off kinase activity and enables inner-to-outer membrane cardiolipin transfer that promotes apoptosis, redefining NME4 as a dual-function protein.

    Evidence Co-IP of the OPA1 complex, LC-MS lipid analysis, membrane-binding-deficient mutagenesis, and apoptosis assays in stable cell lines

    PMID:23150663

    Open questions at the time
    • Did not establish the OPA1 interaction as direct versus indirect
    • Did not link the transfer activity to mitophagy
  4. 2016 High

    Demonstrated that the cardiolipin externalized by NDPK-D acts as a mitophagy 'eat-me' signal, connecting the lipid-transfer activity to organelle quality control and OPA1-dependent dynamics.

    Evidence RNAi knockdown, R90D mutagenesis, in situ proximity ligation assay, and mitophagy assays across MLE-12, HeLa, and SH-SY5Y cells with multiple triggers

    PMID:26742431

    Open questions at the time
    • Did not identify the receptor recognizing externalized cardiolipin in all contexts
    • Did not resolve how fission-fusion and CL transfer are mechanistically coupled
  5. 2015 Medium

    Uncovered acetylation as a regulatory layer controlling NDPK-D localization, showing SIRT1 binds and deacetylates NDPK-D to govern its nuclear accumulation and apoptotic output.

    Evidence Yeast two-hybrid, co-IP, acetylation-mimic mutagenesis, SIRT1 inhibition, and apoptosis assays in neuroblastoma cells and mouse cortex

    PMID:26426123

    Open questions at the time
    • Specific acetylated lysines not definitively mapped
    • Functional role of nuclear NDPK-D not defined
    • Single-lab interaction evidence
  6. 2021 High

    Established NME4 as a metastasis suppressor by showing that loss of either kinase or membrane-binding activity drives mitochondrial fragmentation, glycolytic switching, and EMT, tying its molecular functions to a cancer phenotype.

    Evidence Loss-of-function mutagenesis, RNAi, in vivo xenograft metastasis assay, and metabolic/ROS/morphology readouts

    PMID:34674701

    Open questions at the time
    • Did not separate the contributions of kinase versus lipid-transfer activity to the metastasis phenotype
    • Upstream regulators of NME4 loss in tumors not defined here
  7. 2023 Medium

    Extended NME4 function into hepatic lipid metabolism, showing it interacts with CoA-metabolism enzymes and promotes lipid accumulation, with hepatic deletion protecting against steatosis.

    Evidence Proteomics, metabolomics, and hepatic Nme4 knockout in a high-fat-diet mouse model

    PMID:38177901

    Open questions at the time
    • Direct enzymatic partners in CoA metabolism not biochemically validated
    • Mechanistic link to mitochondrial cardiolipin transfer not established
    • Single lab
  8. 2024 Medium

    Placed NME4 in tumor immune evasion by showing it suppresses the NFkB2-CCL5 axis to restrict CD8+ T cell infiltration, broadening its role beyond cell-intrinsic mitochondrial functions.

    Evidence Syngeneic murine tumor model with single-cell RNA sequencing, quantitative proteomics, and protein microarray in esophageal squamous cell carcinoma

    PMID:39016535

    Open questions at the time
    • Mechanism connecting mitochondrial NME4 to NFkB2-CCL5 signaling unresolved
    • Direct molecular target in the pathway not identified
    • Single lab
  9. 2026 Medium

    Identified RNF6 as an E3 ligase that controls NME4 stability via K48-linked polyubiquitination, defining a degradative regulatory mechanism with downstream JNK/c-JUN consequences in ovarian cancer.

    Evidence Co-IP, CHX chase, ubiquitination assay, co-modulation rescue, and nude mouse xenograft

    PMID:41616518

    Open questions at the time
    • Ubiquitinated lysine residues not mapped
    • Whether degradation is regulated under physiological signals not addressed
    • Single lab

Open questions

Synthesis pass · forward-looking unresolved questions
  • How NME4's two activities (phosphotransfer versus cardiolipin transfer) are switched in vivo, and how its post-translational regulation integrates with its metabolic and immune-modulatory roles, remains unresolved.
  • No unified model linking acetylation, ubiquitination, and lipid-transfer regulation
  • Structural basis of the kinase-to-transferase switch not solved
  • Physiological triggers governing the switch unknown

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0008289 lipid binding 2 GO:0016740 transferase activity 2 GO:0140104 molecular carrier activity 2 GO:0140098 catalytic activity, acting on RNA 1
Localization
GO:0005739 mitochondrion 2
Pathway
R-HSA-1430728 Metabolism 2 R-HSA-5357801 Programmed Cell Death 1 R-HSA-9612973 Autophagy 1
Partners

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 truncated form (lacking the N-terminal mitochondrial targeting extension) possesses NDP kinase activity, while the full-length protein is inactive, indicating the N-terminal extension prevents enzyme folding/activity. X-ray crystallography showed the active form is a hexamer. The naturally occurring Ser129 (equivalent to K-pn mutation) weakens subunit interactions, and the S129P mutant is greatly stabilized. Confocal microscopy and subcellular fractionation of HEK293 cells showed mitochondrial localization with association to mitochondrial membranes, likely at contact sites between outer and inner membranes. Import into mitochondria is accompanied by cleavage of the N-terminal extension, which enables NDP kinase activity. X-ray crystallography, site-directed mutagenesis, GFP-fusion confocal microscopy, Western blot subcellular fractionation, in vitro enzymatic activity assay The Journal of biological chemistry High 10799505
2008 NDPK-D/NME4 is a peripheral protein of the mitochondrial inner membrane, binding primarily via electrostatic interaction with cardiolipin (highest affinity among anionic phospholipids) as shown by surface plasmon resonance with recombinant protein and model liposomes. Mutation of Arg90 in the surface-exposed RRK motif strongly reduced phospholipid interaction in vitro and in vivo. Due to its symmetrical hexameric structure, NDPK-D can cross-link anionic phospholipid-containing liposomes. Respiration was significantly stimulated by NDPK substrate TDP in mitochondria expressing wild-type NDPK-D but not the R90D mutant, demonstrating functional coupling to oxidative phosphorylation that depends on membrane-bound state. Surface plasmon resonance, site-directed mutagenesis (R90D), stable cell expression, liposome cross-linking assay, mitochondrial respiration assay, submitochondrial fractionation The Journal of biological chemistry High 18635542
2012 NME4/NDPK-D forms a complex with mitochondrial GTPase OPA1 in rat liver, suggesting direct local GTP delivery. Cardiolipin binding inhibits NDP kinase activity but enables a second function: selective intermembrane lipid transfer. Wild-type NME4, but not a membrane-binding-deficient mutant, selectively increased cardiolipin content in the outer mitochondrial membrane (analyzed by LC-MS), while other phospholipids (e.g., phosphatidylcholine) were unaffected. Cells expressing wild-type NME4 showed increased Bax accumulation in mitochondria and were sensitized to rotenone-induced apoptosis (cytochrome c release, caspase 3/7 activity, annexin V binding), demonstrating that cardiolipin transfer promotes apoptotic signaling. Co-immunoprecipitation (OPA1 complex), LC-MS lipid analysis, site-directed mutagenesis (membrane-binding-deficient mutant), apoptosis assays (cytochrome c release, caspase activity, annexin V), stable cell expression The Journal of biological chemistry High 23150663
2016 NME4/NDPK-D facilitates cardiolipin externalization from the inner mitochondrial membrane to the outer mitochondrial membrane surface as a mitophagy signal. CCCP-induced mitophagy caused CL externalization in MLE-12 and HeLa cells; RNAi knockdown of NDPK-D decreased CL externalization and mitochondrial degradation. The R90D mutant (which does not bind CL) was inactive in promoting mitophagy. Proximity ligation assay showed that CL-transfer activity of NDPK-D is closely associated with dynamin-like GTPase OPA1, implicating fission-fusion dynamics. NDPK-D knockdown also suppressed rotenone- and 6-hydroxydopamine-triggered mitophagy in SH-SY5Y cells. RNAi knockdown, site-directed mutagenesis (R90D), in situ proximity ligation assay (PLA), flow cytometry/imaging of CL externalization, mitophagy assays in multiple cell lines Cell death and differentiation High 26742431
2015 NDPK-D/NME4 is acetylated, and this modification is regulated by the NAD+-dependent deacetylase SIRT1, which was identified as a binding partner of NDPK-D by yeast two-hybrid screening and confirmed by co-immunoprecipitation. SIRT1 inhibition increases NDPK-D acetylation. Overexpression of NDPK-D with SIRT1, or mutation of the acetylated lysine residues, increases NDPK-D nuclear accumulation. An acetylation-mimic mutant of NDPK-D increased apoptosis in N1E-115 cells. NDPK-D knockdown induces apoptosis in neuroblastoma cells and in mouse cortex. Yeast two-hybrid screening, co-immunoprecipitation, site-directed mutagenesis (acetylation-mimic), confocal microscopy (co-localization), SIRT1 inhibitor treatment, RNAi knockdown, apoptosis assay PloS one Medium 26426123
2014 miR-196 promotes oral cancer cell migration and invasion by inhibiting NME4 expression, which leads to activation of p-JNK, suppression of TIMP1, and augmentation of MMP1/9, placing NME4 upstream of the JNK-TIMP1-MMP signaling axis. RT-qPCR, Western blot, luciferase reporter assay (target validation), confocal microscopy, cell migration/invasion assays Molecular cancer Medium 25233933
2021 Loss-of-function mutations in NME4 (lacking either NDP kinase activity or membrane interaction) and RNAi-mediated depletion of NME4 both promoted epithelial-mesenchymal transition, increased migratory and invasive potential, and caused mitochondrial fragmentation, loss of mitochondria, metabolic switch from respiration to glycolysis, and increased ROS generation. Immunocompromised mice developed more metastases when injected with cells expressing mutant NDPK-D versus wild-type, establishing NME4 as a metastasis suppressor acting via mitochondrial integrity. Loss-of-function mutagenesis, RNAi knockdown, in vivo xenograft metastasis assay, EMT marker analysis, mitochondrial morphology imaging, metabolic assays (respiration, glycolysis), ROS measurement BMC biology High 34674701
2023 NME4 interacts with key enzymes in coenzyme A (CoA) metabolism and increases levels of acetyl-CoA and malonyl-CoA, leading to increased triglyceride levels and lipid accumulation in the liver. Hepatic deletion of Nme4 in mice suppressed hepatic steatosis progression, establishing NME4 as a regulator of mitochondrial lipid metabolism in NAFLD. Proteomics (interaction partners), metabolomics, hepatic Nme4 knockout (in vivo), high-fat diet mouse model, lipid quantification EMBO reports Medium 38177901
2024 NME4 suppresses the NFκB2-CCL5 signaling axis in esophageal squamous cell carcinoma cells, thereby restricting CD8+ T cell infiltration into the tumor microenvironment. This was demonstrated using a syngeneic murine tumor model with single-cell RNA sequencing showing reduced CD8+ T cell infiltration upon NME4 expression, and quantitative proteomics/protein microarray mapping the NFκB2-CCL5 pathway as negatively regulated by NME4. Syngeneic murine tumor model, single-cell RNA sequencing, quantitative proteomics, protein microarray, in vivo tumor experiments Immunology Medium 39016535
2026 RNF6 E3 ubiquitin ligase directly binds NME4 and facilitates its K48-linked polyubiquitination, leading to proteasomal degradation of NME4. NME4 depletion reverses the tumor-suppressive effects of RNF6 knockdown and reinstates JNK/c-JUN pathway activation, establishing an RNF6/NME4/JNK axis in ovarian cancer. Co-immunoprecipitation, cycloheximide (CHX) chase assay, ubiquitination assay, RNF6/NME4 co-modulation rescue experiments, nude mouse xenograft model Pathology, research and practice Medium 41616518
2021 let-7f-5p directly targets the 3' UTR of Nme4 mRNA and negatively regulates Nme4 expression in mouse bone marrow-derived mesenchymal stem cells. Ectopic Nme4 expression completely reversed the inhibitory effects of let-7f-5p on osteogenic differentiation, and overexpression of Nme4 in BM-MSCs restored in vivo bone formation in an ovariectomized mouse model, placing Nme4 downstream of TNF-α/let-7f-5p in osteogenesis regulation. Luciferase reporter assay (3' UTR targeting), miRNA mimic/inhibitor transfection, ectopic Nme4 expression (rescue), in vivo ovariectomized animal model, ALP/alizarin red staining Biochemistry and cell biology Medium 34297624
2024 Computational modeling (molecular dynamics simulations) identified conserved Arg27 in NME4 (and other group I NDPKs, NME1-4) as a key residue for hexamer assembly, mediating inter- and intra-molecular monomer interactions. Arg27 mutation decreased binding affinity and destabilized the complex. Double and triple Arg mutations in NME4, combined with a shorter C-terminal region, destabilize the hexamer into a dimer, highlighting the role of the C-terminal region in hexamer stabilization. Molecular dynamics simulation, computational modeling of hexameric assembly, mutation analysis (computational) 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 165 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 96 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 84 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 31 29035377
2021 The mitochondrially-localized nucleoside diphosphate kinase D (NME4) is a novel metastasis suppressor. BMC biology 27 34674701
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
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 14 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

Missed literature

Know a paper Affinage missed for NME4? Flag it for the maintainers and the community.

No submissions yet.