Crosstalk between Akt/GSK3β signaling and dynamin-1 regulates clathrin-mediated endocytosis

EMBO Journal

Volumn 34, Issue 16, 2015, Pages 2132-2146

  Reis, Carlos R ^a   Chen, Ping Hung ^a   Srinivasan, Saipraveen ^a   Aguet, François ^b   Mettlen, Marcel ^a   Schmid, Sandra L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CCP maturation; CME; dynamin; endosomal trafficking; signaling

Indexed keywords

CLATHRIN; DYNAMIN I; DYNAMIN II; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ARTICLE; CANCER CELL CULTURE; CLATHRIN MEDIATED ENDOCYTOSIS; CONTROLLED STUDY; CRISPR CAS SYSTEM; CYTOSOL; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; CELL LINE; CLATHRIN-COATED VESICLE; EPITHELIUM CELL; METABOLISM; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION;

CELL LINE; CLATHRIN-COATED VESICLES; DYNAMIN I; ENDOCYTOSIS; EPITHELIAL CELLS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; PROTEIN INTERACTION MAPS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84939270378     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591518     Document Type: Article

References (48)

1. Aguet F, Antonescu CN, Mettlen M, Schmid SL, Danuser G, (2013) Advances in analysis of low signal-to-noise images link dynamin and AP2 to the functions of an endocytic checkpoint. Dev Cell 26: 279-291
2. Clayton EL, Sue N, Smillie KJ, O'Leary T, Bache N, Cheung G, Cole AR, Wyllie DJ, Sutherland C, Robinson PJ, Cousins MA, (2010) Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat Neurosci 13: 845-851
3. Cocucci E, Gaudin R, Kirchhausen T, (2014) Dynamin recruitment and membrane scission at the neck of a clathrin-coated pit. Mol Biol Cell 25: 3595-3609
4. Damke H, Baba T, Warnock DE, Schmid SL, (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934
5. Di Fiore PP, von Zastrow M, (2014) Endocytosis, signaling, and beyond. Cold Spring Harb Perspect Biol 6: a016865
6. Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, Santiago Y, Lee AH, Vo TD, Doyon Y, Miller JC, Paschon DE, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Drubin DG, (2011) Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13: 331-337
7. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T, (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591-605
8. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, Raimondi A, Gong LW, Ariel P, Paradise S, O'toole E, Flavell R, Cremona O, Meisenböck G, Ryan TA, De Camilli P, (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316: 570-574
9. Ferguson SM, De Camilli P, (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13: 75-88
10. Field MC, Gabernet-Castello C, Dacks JB, (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Expt Med Biol 607: 84-96
11. Forgac M, (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nature Rev Mol Cell Biol 8: 917-929
12. Gorvel JP, Chavrier P, Zerial M, Gruenberg J, (1991) Rab5 controls early endosome fusion in vitro. Cell 64: 915-925
13. Grant BD, Donaldson JG, (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10: 597-608
14. Haferlach T, Kohlmann A, Wieczorek L, Basso G, Kronnie GT, Bene MC, De Vos J, Hernandez JM, Hofmann WK, Mills KI, Gilkes A, Chiaretti S, Shurtleff SA, Kipps TJ, Rassenti LZ, Yeoh AE, Papenhaussen PR, Liu WM, Williams PM, Foa R, (2010) Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: report from the International Microarray Innovations in Leukemia Study Group. J Clin Oncol 28: 2529-2537
15. Hernandez V.J., Weng J., Ly P., Pompey S., Dong H., Mishra L., Schwarz M., Anderson R.G., Michaely P., (2013). Cavin-3 dictates the balance between ERK and Akt signaling. eLife 2: e00905.
16. Hong Y, Downey T, Eu KW, Koh PK, Cheah PY, (2010) A 'metastasis-prone' signature for early-stage mismatch-repair proficient sporadic colorectal cancer patients and its implications for possible therapeutics. Clin Exp Metastasis 27: 83-90
17. Huang F, Khvorova A, Marshall W, Sorkin A, (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279: 16657-16661
18. Kasprowicz J, Kuenen S, Swerts J, Miskiewicz K, Verstreken P, (2014) Dynamin photoinactivation blocks Clathrin and alpha-adaptin recruitment and induces bulk membrane retrieval. J Cell Biol 204: 1141-1156
19. Le Roy C, Wrana JL, (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6: 112-126
20. Liberali P, Snijder B, Pelkmans L, (2014) A hierarchical map of regulatory genetic interactions in membrane trafficking. Cell 157: 1473-1487
21. Liu AP, Aguet F, Danuser G, Schmid SL, (2010) Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191: 1381-1393
22. Liu YW, Neumann S, Ramachandran R, Ferguson SM, Pucadyil TJ, Schmid SL, (2011) Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. Proc Natl Acad Sci USA 108: E234-E242
23. Liu YW, Su AI, Schmid SL, (2012) The evolution of dynamin to regulate clathrin-mediated endocytosis: speculations on the evolutionarily late appearance of dynamin relative to clathrin-mediated endocytosis. BioEssays 34: 643-647
24. Liu YW, Surka MC, Schroeter T, Lukiyanchuk V, Schmid SL, (2008) Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol Biol Cell 19: 5347-5359
25. Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H, Danuser G, Schmid SL, (2009) Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7: e57
26. Maxfield FR, McGraw TE, (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5: 121-132
27. McMahon HT, Boucrot E, (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533
28. Mellman I, (1996) Endocytosis and molecular sorting. Ann Rev Cell Dev Biol 12: 575-625
29. Mellman I, Yarden Y, (2013) Endocytosis and cancer. Cold Spring Harb Perspect Biol 5: a016949
30. Mettlen M, Pucadyil T, Ramachandran R, Schmid SL, (2009a) Dissecting dynamin's role in clathrin-mediated endocytosis. Biochem Soc Trans 37: 1022-1026
31. Mettlen M, Stoeber M, Loerke D, Antonescu CN, Danuser G, Schmid SL, (2009b) Endocytic accessory proteins are functionally distinguished by their differential effects on the maturation of clathrin-coated pits. Mol Biol Cell 20: 3251-3260
32. Mosesson Y, Mills GB, Yarden Y, (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8: 835-850
33. Motley AM, Berg N, Taylor MJ, Sahlender DA, Hirst J, Owen DJ, Robinson MS, (2006) Functional analysis of AP-2 alpha and mu2 subunits. Mol Biol Cell 17: 5298-5308
34. Palfy M, Remenyi A, Korcsmaros T, (2012) Endosomal crosstalk: meeting points for signaling pathways. Trends Cell Biol 22: 447-456
35. Platta HW, Stenmark H, (2011) Endocytosis and signaling. Curr Opin Cell Biol 23: 393-403
36. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F, (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389
37. Rink J, Ghigo E, Kalaidzidis Y, Zerial M, (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749
38. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B, Brand M, Zerial M, (2008) The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133: 486-497
39. Schmid EM, McMahon HT, (2007) Integrating molecular and network biology to decode endocytosis. Nature 448: 883-888
40. Schmid SL, Smythe E, (1991) Stage-specific assays for coated pit formation and coated vesicle budding in vitro. J Cell Biol 114: 869-880
41. Sever S, Damke H, Schmid SL, (2000) Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol 150: 1137-1148
42. Sever S, Muhlberg AB, Schmid SL, (1999) Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398: 481-486
43. Smillie KJ, Cousin MA, (2011) The role of GSK3 in presynaptic function. Int J Alzheimer's Dis 2011: 263673
44. Sorkin A, von Zastrow M, (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10: 609-622
45. Taylor MJ, Lampe M, Merrifield CJ, (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10: e1001302
46. Traub LM, (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10: 583-596
47. Villasenor R., Nonaka H., Del Conte-Zerial P., Kalaidzidis Y., Zerial M., (2015). Regulation of EGFR signal transduction by analogue-to-digital conversion in endosomes. eLife 4: e06156
48. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P, (2009) A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136: 1110-1121