SNX9 Regulates Dynamin Assembly and is Required for Efficient Clathrin-mediated Endocytosis

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2005 Feb 11

PMID 15703209

Citations 103

Authors

Fabienne Soulet

Defne Yarar

Marilyn Leonard

Sandra L Schmid

Affiliations

Soon will be listed here.

Abstract

Dynamin, a central player in clathrin-mediated endocytosis, interacts with several functionally diverse SH3 domain-containing proteins. However, the role of these interactions with regard to dynamin function is poorly defined. We have investigated a recently identified protein partner of dynamin, SNX9, sorting nexin 9. SNX9 binds directly to both dynamin-1 and dynamin-2. Moreover by stimulating dynamin assembly, SNX9 stimulates dynamin's basal GTPase activity and potentiates assembly-stimulated GTPase activity on liposomes. In fixed cells, we observe that SNX9 partially localizes to clathrin-coated pits. Using total internal reflection fluorescence microscopy in living cells, we detect a transient burst of EGFP-SNX9 recruitment to clathrin-coated pits that occurs during the late stages of vesicle formation and coincides spatially and temporally with a burst of dynamin-mRFP fluorescence. Transferrin internalization is inhibited in HeLa cells after siRNA-mediated knockdown of SNX9. Thus, our results establish that SNX9 is required for efficient clathrin-mediated endocytosis and suggest that it functions to regulate dynamin activity.

Citing Articles

Comprehensive Analysis Reveals That ISCA1 Is Correlated with Ferroptosis-Related Genes Across Cancers and Is a Biomarker in Thyroid Carcinoma.

Xiong D, Li Z, Zuo L, Ge J, Gu Y, Zhang E Genes (Basel). 2025; 15(12.

PMID: 39766805 PMC: 11675480. DOI: 10.3390/genes15121538.

Endosome rupture enables enteroviruses from the family Picornaviridae to infect cells.

Ishemgulova A, Mukhamedova L, Trebichalska Z, Rajecka V, Payne P, Smerdova L Commun Biol. 2024; 7(1):1465.

PMID: 39511383 PMC: 11543853. DOI: 10.1038/s42003-024-07147-9.

SNX9 family mediates βarrestin-independent GPCR endocytosis.

Robleto V, Zhuo Y, Crecelius J, Benzow S, Marchese A Commun Biol. 2024; 7(1):1455.

PMID: 39511325 PMC: 11544122. DOI: 10.1038/s42003-024-07157-7.

CHC22 clathrin recruitment to the early secretory pathway requires two-site interaction with SNX5 and p115.

Greig J, Bates G, Yin D, Briant K, Simonetti B, Cullen P EMBO J. 2024; 43(19):4298-4323.

PMID: 39160272 PMC: 11445476. DOI: 10.1038/s44318-024-00198-y.

Dynamin-dependent entry of Chlamydia trachomatis is sequentially regulated by the effectors TarP and TmeA.

Romero M, Carabeo R Nat Commun. 2024; 15(1):4926.

PMID: 38858371 PMC: 11164928. DOI: 10.1038/s41467-024-49350-6.

References

van der Bliek A, Redelmeier T, Damke H, Tisdale E, Meyerowitz E, Schmid S . Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol. 1993; 122(3):553-63. PMC: 2119674. DOI: 10.1083/jcb.122.3.553. View

Wilsbach K, Payne G . Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. EMBO J. 1993; 12(8):3049-59. PMC: 413570. DOI: 10.1002/j.1460-2075.1993.tb05974.x. View

Nakata T, Takemura R, Hirokawa N . A novel member of the dynamin family of GTP-binding proteins is expressed specifically in the testis. J Cell Sci. 1993; 105 ( Pt 1):1-5. DOI: 10.1242/jcs.105.1.1. View

Gout I, Dhand R, Hiles I, Fry M, Panayotou G, Das P . The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell. 1993; 75(1):25-36. View

SEVER S, Muhlberg A, Schmid S . Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature. 1999; 398(6727):481-6. DOI: 10.1038/19024. View

Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov A . Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature. 1999; 401(6749):133-41. DOI: 10.1038/43613. View

Adams M, Matov A, Yarar D, Gupton S, Danuser G, Waterman-Storer C . Signal analysis of total internal reflection fluorescent speckle microscopy (TIR-FSM) and wide-field epi-fluorescence FSM of the actin cytoskeleton and focal adhesions in living cells. J Microsc. 2004; 216(Pt 2):138-52. DOI: 10.1111/j.0022-2720.2004.01408.x. View

Yarar D, Waterman-Storer C, Schmid S . A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell. 2004; 16(2):964-75. PMC: 545926. DOI: 10.1091/mbc.e04-09-0774. View

Sontag J, Fykse E, Ushkaryov Y, Liu J, Robinson P, Sudhof T . Differential expression and regulation of multiple dynamins. J Biol Chem. 1994; 269(6):4547-54. View

10.

Damke H, Baba T, Warnock D, Schmid S . Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994; 127(4):915-34. PMC: 2200053. DOI: 10.1083/jcb.127.4.915. View

11.

Ekena K, Stevens T . The Saccharomyces cerevisiae MVP1 gene interacts with VPS1 and is required for vacuolar protein sorting. Mol Cell Biol. 1995; 15(3):1671-8. PMC: 230391. DOI: 10.1128/MCB.15.3.1671. View

12.

Hinshaw J, Schmid S . Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 1995; 374(6518):190-2. DOI: 10.1038/374190a0. View

13.

Howard L, Nelson K, Maciewicz R, Blobel C . Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J Biol Chem. 1999; 274(44):31693-9. DOI: 10.1074/jbc.274.44.31693. View

14.

Stowell M, Marks B, Wigge P, McMahon H . Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol. 1999; 1(1):27-32. DOI: 10.1038/8997. View

15.

Takei K, Slepnev V, Haucke V, De Camilli P . Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol. 1999; 1(1):33-9. DOI: 10.1038/9004. View

16.

Kranenburg O, Verlaan I, Moolenaar W . Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J Biol Chem. 1999; 274(50):35301-4. DOI: 10.1074/jbc.274.50.35301. View

17.

Kreitzer G, Marmorstein A, Okamoto P, Vallee R, Rodriguez-Boulan E . Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat Cell Biol. 2000; 2(2):125-7. DOI: 10.1038/35000081. View

18.

Cao H, Thompson H, Krueger E, McNiven M . Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin. J Cell Sci. 2000; 113 ( Pt 11):1993-2002. DOI: 10.1242/jcs.113.11.1993. View

19.

Fish K, Schmid S, Damke H . Evidence that dynamin-2 functions as a signal-transducing GTPase. J Cell Biol. 2000; 150(1):145-54. PMC: 2185575. DOI: 10.1083/jcb.150.1.145. View

20.

SEVER S, Damke H, Schmid S . Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol. 2000; 150(5):1137-48. PMC: 2175254. DOI: 10.1083/jcb.150.5.1137. View