Hotspots Organize Clathrin-Mediated Endocytosis by Efficient Recruitment and Retention of Nucleating Resources

Traffic

Volumn 12, Issue 12, 2011, Pages 1868-1878

  Nunez, Daniel ^a,b   Antonescu, Costin ^b   Mettlen, Marcel ^b   Liu, Allen ^b   Schmid, Sandra L ^b   Loerke, Dinah ^b,c   Danuser, Gaudenz ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF DENVER   (United States)

Author keywords

Clathrin; Endocytosis; FCHo1; FCHo2; Hotspot; SNX9

Indexed keywords

ACTIN; CLATHRIN; PHOSPHOLIPID; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

ACTINS; ADAPTOR PROTEIN COMPLEX 2; ANIMALS; CELL LINE; CELL MEMBRANE; CLATHRIN; CLATHRIN-COATED VESICLES; COATED PITS, CELL-MEMBRANE; COMPUTER SIMULATION; ENDOCYTOSIS; HAPLORHINI; KINETICS; RATS; RECEPTORS, TRANSFERRIN;

EID: 81055147607     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01273.x     Document Type: Article

References (43)

1. Brett TJ, Traub LM. Molecular structures of coat and coat-associated proteins: function follows form. Curr Opin Cell Biol 2006;18:395-406.
2. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003;422:37-44.
3. Kirchhausen T. Clathrin. Annu Rev Biochem 2000;69:699-727.
4. Schoch S, Gundelfinger ED. Molecular organization of the presynaptic active zone. Cell Tissue Res 2006;326:379-391.
5. Owald D, Sigrist SJ. Assembling the presynaptic active zone. Curr Opin Neurobiol 2009;19:311-318.
6. Bai J, Hu Z, Dittman JS, Pym EC, Kaplan JM. Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 2010;143:430-441.
7. Brodin L, Shupliakov O. Giant reticulospinal synapse in lamprey: molecular links between active and periactive zones. Cell Tissue Res 2006;326:301-310.
8. Gaidarov I, Santini F, Warren RA, Keen JH. Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1999;1:1-7.
9. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004;118:591-605.
10. Saffarian S, Cocucci E, Kirchhausen T. Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 2009;7:e1000191.
11. Keyel PA, Watkins SC, Traub LM. Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy. J Biol Chem 2004;279:13190-13204.
12. Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H, Danuser G, Schmid SL. Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 2009;7:e57.
13. Merrifield CJ, Feldman ME, Wan L, Almers W. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 2002;4:691-698.
14. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, Danuser G. Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods 2008;5:695-702.
15. Haase P. Spatial pattern-analysis in ecology based on Ripley k-function: introduction and methods of edge correction. J Veg Sci 1995;6:575-582.
16. Ripley BD. 2nd-order analysis of stationary point processes. J Appl Probab 1976;13:255-266.
17. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 2010;328:1281-1284.
18. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 2002;157:1071-1081.
19. Boucrot E, Saffarian S, Massol R, Kirchhausen T, Ehrlich M. Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 2006;312:4036-4048.
20. Coue M, Brenner SL, Spector I, Korn ED. Inhibition of actin polymerization by latrunculin A. FEBS Lett 1987;213:316-318.
21. Yarar D, Waterman-Storer CM, Schmid SL. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 2005;16:964-975.
22. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 1994;269:14869-14871.
23. Ponti A, Matov A, Adams M, Gupton S, Waterman-Storer CM, Danuser G. Periodic patterns of actin turnover in lamellipodia and lamellae of migrating epithelial cells analyzed by quantitative fluorescent speckle microscopy. Biophys J 2005;89:3456-3469.
24. Antonescu CN, Aguet F, Danuser G, Schmid SL. Phosphatidylinositol-(4, 5)-bisphosphate regulates clathrin-coated pit initiation, stabilization and size. Mol Biol Cell 2011;22:2588-2600.
25. Padron D, Wang YJ, Yamamoto M, Yin H, Roth MG. Phosphatidylinositol phosphate 5-kinase Ibeta recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol 2003;162:693-701.
26. Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol 1999;15:705-732.
27. Mettlen M, Stoeber M, Loerke D, Antonescu CN, Danuser G, Schmid SL. Endocytic accessory proteins are functionally distinguished by their differential effects on the maturation of clathrin-coated pits. Mol Biol Cell 2009;20:3251-3260.
28. Worby CA, Dixon JE. Sorting out the cellular functions of sorting nexins. Nat Rev Mol Cell Biol 2002;3:919-931.
29. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004;303:495-499.
30. Soulet F, Yarar D, Leonard M, Schmid SL. SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 2005;16:2058-2067.
31. Lundmark R, Carlsson SR. The beta-appendages of the four adaptor-protein (AP) complexes: structure and binding properties, and identification of sorting nexin 9 as an accessory protein to AP-2. Biochem J 2002;362:597-607.
32. Lundmark R, Carlsson SR. Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 2003;278:46772-46781.
33. Shin N, Ahn N, Chang-Ileto B, Park J, Takei K, Ahn SG, Kim SA, Di Paolo G, Chang S. SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J Cell Sci 2008;121:1252-1263.
34. Yarar D, Surka MC, Leonard MC, Schmid SL. SNX9 activities are regulated by multiple phosphoinositides through both PX and BAR domains. Traffic 2008;9:133-146.
35. Yarar D, Waterman-Storer CM, Schmid SL. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev Cell 2007;13:43-56.
36. Badour K, McGavin MK, Zhang J, Freeman S, Vieira C, Filipp D, Julius M, Mills GB, Siminovitch KA. Interaction of the Wiskott-Aldrich syndrome protein with sorting nexin 9 is required for CD28 endocytosis and cosignaling in T cells. Proc Natl Acad Sci U S A 2007;104:1593-1598.
37. Shin N, Lee S, Ahn N, Kim SA, Ahn SG, YongPark Z, Chang S. Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J Biol Chem 2007;282:28939-28950.
38. Taylor MJ, Perrais D, Merrifield CJ. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 2011;9:e1000604.
39. Loerke D, Mettlen M, Schmid SL, Danuser G. Measuring the hierarchy of molecular events during clathrin-mediated endocytosis. Traffic 2011;12:815-825.
40. Liu AP, Aguet F, Danuser G, Schmid SL. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 2010;191:1381-1393.
41. Scita G, Di Fiore PP. The endocytic matrix. Nature 2010;463:464-473.
42. Motley A, Bright NA, Seaman MN, Robinson MS. Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 2003;162(5):909-918.
43. Lu Q. Seamless cloning and gene fusion. Trends Biotechnol 2005;23:199-207.