Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling

@article{Boissan2014NucleosideDK,
  title={Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling},
  author={Mathieu Boissan and Guillaume Montagnac and Qinfang Shen and Lorena Gripari{\'c} and J{\'e}r{\^o}me Guitton and Maryse Romao and Nathalie Sauvonnet and Thibault Lagache and Ioan Lascu and Graça Raposo and C{\'e}line Desbourdes and Uwe Schlattner and M. L. Lacombe and Simona Polo and Alexander M. van der Bliek and Aur{\'e}lien Roux and Philippe Chavrier},
  journal={Science},
  year={2014},
  volume={344},
  pages={1510 - 1515}
}
Supplying power: Right time, right place Cell membranes are very flexible and easily molded to shape; however, to physically pinch off a membrane vesicle from a membrane tube still requires power. A type of molecular machine known as dynamin is involved in this sort of membrane remodeling. Dynamins use guanosine triphosphate (GTP) rather than the more commonly used cellular energy source adenosine triphosphate to work. Boissan et al. now show that two separate dynamins found in the cytoplasm or… 

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References

SHOWING 1-10 OF 34 REFERENCES

The mechanism of GTP hydrolysis by dynamin II: a transient kinetic study.

The results are interpreted as showing that mantdGTP binds to dynamin in a two-step mechanism that more closely resembles that of the Ras family of proteins involved in cell signaling than the myosin ATPase involved in cellular motility.

GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission

Monitoring the effect of nucleotides on dynamin-coated lipid tubules in real time demonstrates a mechanoenzyme activity of dynamin in endocytosis, but also implies that constriction is not sufficient for fission.

Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals

These findings demonstrate that dynamin and clathrin act at different sites in the formation of endocytic vesicles and suggest that stabilization of the GTP-bound conformation of dynamin leads to tubule formation by progressive elongation of the vesicle stalk.

Dual Function of Mitochondrial Nm23-H4 Protein in Phosphotransfer and Intermembrane Lipid Transfer

It is proposed that Nm23-H4 acts as a lipid-dependent mitochondrial switch with dual function in phosphotransfer serving local GTP supply and cardiolipin transfer for apoptotic signaling and putative other functions.

The Nucleoside Diphosphate Kinase D (NM23-H4) Binds the Inner Mitochondrial Membrane with High Affinity to Cardiolipin and Couples Nucleotide Transfer with Respiration*

In HeLa cells, stable expression of wild type but not of the R90D mutant led to membrane-bound enzyme in vivo, which indicates local ADP regeneration in the mitochondrial intermembrane space and a tight functional coupling of NDPK-D with oxidative phosphorylation that depends on its membrane- bound state.