Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning

Nature Cell Biology

Volumn 14, Issue 5, 2012, Pages 488-501

  Umasankar, P K ^a   Sanker, Subramaniam ^a   Thieman, James R ^a   Chakraborty, Souvik ^a   Wendland, Beverly ^b   Tsang, Michael ^a   Traub, Linton M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 8; BONE MORPHOGENETIC PROTEIN RECEPTOR; FCH DOMAIN ONLY 1 PROTEIN; FCH DOMAIN ONLY 2 PROTEIN; MEMBRANE PROTEIN; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CLATHRIN MEDIATED ENDOCYTOSIS; CONTROLLED STUDY; DORSOVENTRAL PATTERNING; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENDOCYTOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ADAPTOR PROTEIN COMPLEX 2; BODY PATTERNING; CLATHRIN; EMBRYONIC DEVELOPMENT; ENDOCYTOSIS; GENE SILENCING; HELA CELLS; HUMANS; PROTEINS;

DANIO RERIO;

EID: 84860513160     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2473     Document Type: Article

References (69)

1. Conner, S. D. & Schmid, S. L. Regulated portals of entry into the cell. Nature 422, 37-44 (2003). (Pubitemid 36323287)
2. McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533 (2011).
3. Kirchhausen, T. Imaging endocytic clathrin structures in living cells. Trends Cell Biol. 19, 596-605 (2009).
4. Kelly, B. T. & Owen, D. J. Endocytic sorting of transmembrane protein cargo. Curr. Opin. Cell Biol. 23, 404-412 (2011).
5. Reider, A. & Wendland, B. Endocytic adaptors-social networking at the plasma membrane. J. Cell Sci. 124, 1613-1622 (2011).
6. Traub, L. M. Tickets to ride: Selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596 (2009).
7. Taylor, M. J., Perrais, D. & Merri-eld, C. J. A high precision survery of the molecular dynamics of mammalian clathrin mediated endocytosis. PLoS Biol. 9, e1000604 (2011).
8. Schmid, E. M. & McMahon, H. T. Integrating molecular and network biology to decode endocytosis. Nature 448, 883-888 (2007). (Pubitemid 47312770)
9. 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. 312, 4036-4048 (2006). (Pubitemid 44828048)
10. Zoncu, R. et al. Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4, 5-bisphosphate. Proc. Natl Acad. Sci. USA 104, 3793-3798 (2007). (Pubitemid 47181533)
11. Jackson, L. P. et al. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141, 1220-1229 (2010).
12. Henne, W. M. et al. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284 (2010).
13. Little, S. C. & Mullins, M. C. Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis. Nat. Cell Biol. 11, 637-643 (2009).
14. Mintzer, K. A. et al. Lost-a-n encodes a type I BMP receptor, Alk8, acting maternally and zygotically in dorsoventral pattern formation. Development 128, 859-869 (2001). (Pubitemid 32288197)
15. Reider, A. et al. Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation. EMBO J. 28, 3103-3016 (2009).
16. Katoh, M. Identi-cation and characterization of human FCHO2 and mouse Fcho2 genes in silico. Int. J. Mol Med. 14, 327-331 (2004).
17. Stimpson, H. E., Toret, C. P., Cheng, A. T., Pauly, B. S. & Drubin, D. G. Early-arriving Syp1p and Ede1p function in endocytic site placement and formation in budding yeast. Mol. Biol. Cell 20, 4640-4651 (2009).
18. Boettner, D. R. et al. The F-BAR protein Syp1 negatively regulates WASp-Arp2/3 complex activity during endocytic patch formation. Curr. Biol. 19, 1979-1987 (2009).
19. Uezu, A. et al. Characterization of the EFC/F-BAR domain protein, FCHO2. Genes Cells 16, 868-878 (2011).
20. Zoncu, R. et al. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136, 1110-1121 (2009).
21. Henne, W. M. et al. Structure and analysis of FCHo2 F-BAR domain: A dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852 (2007). (Pubitemid 47042426)
22. Edeling, M. A., Smith, C. & Owen, D. Life of a clathrin coat: Insights from clathrin and AP structures. Nat. Rev. Mol. Cell Biol. 7, 32-44 (2006). (Pubitemid 43361570)
23. Edeling, M. A. et al. Molecular switches involving the AP-2-2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 10, 329-342 (2006).
24. Schmid, E. M. et al. Role of the AP2-appendage hub in recruiting partners for clathrin coated vesicle assembly. PLoS Biol. 4, e262 (2006).
25. Mishra, S. K. et al. Dual-engagement regulation of protein interactions with the AP-2 adaptor-appendage. J. Biol. Chem. 279, 46191-46203 (2004). (Pubitemid 39491614)
26. Praefcke, G. J. et al. Evolving nature of the AP2-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 23, 4371-4383 (2004). (Pubitemid 39601962)
27. Hinrichsen, L., Harborth, J., Andrees, L., Weber, K. & Ungewickell, E. J. Effect of clathrin heavy chain-and-adaptin speci-c small interfering RNAs on endocytic accessory proteins and receptor traf-cking in HeLa cells. J. Biol. Chem. 278, 45160-45170 (2003). (Pubitemid 37432649)
28. Motley, A., Bright, N. A., Seaman, M. N. & Robinson, M. S. Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162, 909-918 (2003). (Pubitemid 37087730)
29. Uezu, A. et al. SGIP1-is an endocytic protein that directly interacts with phospholipids and Eps15. J. Biol. Chem. 282, 26481-26489 (2007). (Pubitemid 47443791)
30. Yamabhai, M. et al. Intersectin, a novel adaptor protein with two Eps15 homology and-ve Src homology 3 domains. J. Biol. Chem. 273, 31401-31407 (1998). (Pubitemid 28533159)
31. Koh, T. W. et al. Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J. Cell Biol. 178, 309-322 (2007).
32. Sengar, A. S., Wang, W., Bishay, J., Cohen, S. & Egan, S. E. The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J. 18, 1159-1171 (1999). (Pubitemid 29110301)
33. Imai, Y. & Talbot, W. S. Morpholino phenocopies of the bmp2b/swirl and bmp7/snailhouse mutations. Genesis 30, 160-163 (2001). (Pubitemid 32730765)
34. Mullins, M. C. et al. Genes establishing dorsoventral pattern formation in the zebra-sh embryo: The ventral specifying genes. Development 123, 81-93 (1996). (Pubitemid 27056738)
35. Schier, A. F. & Talbot, W. S. Molecular genetics of axis formation in zebra-sh. Annu. Rev. Genet. 39, 561-613 (2005). (Pubitemid 43011127)
36. Tucker, J. A., Mintzer, K. A. & Mullins, M. C. The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev. Cell 14, 108-119 (2008).
37. Robu, M. E. et al. p53 activation by knockdown technologies. PLoS Genet. 3, e78 (2007).
38. Schulte-Merker, S., Lee, K. J., McMahon, A. P. & Hammerschmidt, M. The zebra-sh organizer requires chordino. Nature 387, 862-863 (1997).
39. von der Hardt, S. et al. The Bmp gradient of the zebra-sh gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 17, 475-487 (2007).
40. Bauer, H., Lele, Z., Rauch, G. J., Geisler, R. & Hammerschmidt, M. The type I serine/threonine kinase receptor Alk8/Lost-a-n is required for Bmp2b/7 signal transduction during dorsoventral patterning of the zebra-sh embryo. Development 128, 849-858 (2001). (Pubitemid 32288196)
41. Payne, T. L., Postlethwait, J. H. & Yelick, P. C. Functional characterization and genetic mapping of alk8. Mech. Dev. 100, 275-289 (2001). (Pubitemid 32109336)
42. Solnica-Krezel, L. Gastrulation in zebra-sh-all just about adhesion? Curr. Opin. Genet. Dev. 16, 433-441 (2006).
43. Borner, G. H. et al. CVAK104 is a novel regulator of clathrin-mediated SNARE sorting. Traf-c 8, 893-903 (2007). (Pubitemid 46971635)
44. Tsang, M. et al. A role for MKP3 in axial patterning of the zebra-sh embryo. Development 131, 2769-2779 (2004). (Pubitemid 38997268)
45. Yu, S. R. et al. Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536 (2009).
46. Scholpp, S. & Brand, M. Endocytosis controls spreading and effective signaling range of Fgf8 protein. Curr. Biol 14, 1834-1841 (2004). (Pubitemid 39408773)
47. Molina, G. A., Watkins, S. C. & Tsang, M. Generation of FGF reporter transgenic zebra-sh and their utility in chemical screens. BMC Dev. Biol. 7, 62 (2007).
48. Furthauer, M., Van Celst, J., Thisse, C. & Thisse, B. Fgf signalling con-trols the dorsoventral patterning of the zebra-sh embryo. Development 131, 2853-2864 (2004). (Pubitemid 38997274)
49. Sorkin, A. & von Zastrow, M. Endocytosis and signalling: Intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-922 (2009).
50. Belenkaya, T. Y. et al. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119, 231-244 (2004). (Pubitemid 39360905)
51. O'Connor-Giles, K. M., Ho, L. L. & Ganetzky, B. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58, 507-518 (2008). (Pubitemid 351672350)
52. Wang, W. & Struhl, G. Distinct roles for Mind bomb, Neuralized and Epsin in mediating DSL endocytosis and signaling in Drosophila. Development 132, 2883-2894 (2005). (Pubitemid 40932876)
53. Hartung, A. et al. Different routes of bone morphogenic protein (BMP) receptor endocytosis in-uence BMP signaling. Mol. Cell Biol. 26, 7791-7805 (2006). (Pubitemid 44547724)
54. Heining, E., Bhushan, R., Paarmann, P., Henis, Y. I. & Knaus, P. Spatial segregation of BMP/Smad signaling affects osteoblast differentiation in C2C12 cells. PLoS One 6, e25163 (2011).
55. Zhou, Y. et al. Receptor internalization-independent activation of Smad2 in activin signaling. Mol. Endocrinol. 18, 1818-1826 (2004). (Pubitemid 38859587)
56. Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L. & Wrana, J. L. SARA, a FYVE domain protein that recruits Smad2 to the TGFb receptor. Cell 95, 779-791 (1998). (Pubitemid 29014458)
57. Lin, H. K., Bergmann, S. & Pandol-, P. P. Cytoplasmic PML function in TGF-signalling. Nature 431, 205-211 (2004).
58. Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F. & Wrana, J. L. Distinct endocytic pathways regulate TGF-receptor signalling and turnover. Nat. Cell Biol. 5, 410-421 (2003). (Pubitemid 36592263)
59. Hayes, S., Chawla, A. & Corvera, S. TGF-receptor internalization into EEA1-enriched early endosomes: Role in signaling to Smad2. J. Cell Biol. 158, 1239-1249 (2002).
60. Shi, W. et al. Endo-n acts as a Smad anchor for receptor activation in BMP signaling. J. Cell Sci. 120, 1216-1224 (2007). (Pubitemid 46711840)
61. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. Stages of embryonic development of the zebra-sh. Dev. Dyn. 203, 253-310 (1995).
62. Barrios-Rodiles, M. et al. High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307, 1621-1625 (2005). (Pubitemid 40354744)
63. Jullien, J. & Gurdon, J. Morphogen gradient interpretation by a regulated traf-cking step during ligand-receptor transduction. Genes Dev. 19, 2682-2694 (2005). (Pubitemid 41627935)
64. Mitsunari, T. et al. Clathrin adaptor AP-2 is essential for early embryonal development. Mol. Cell. Biol. 25, 9318-9323 (2005). (Pubitemid 41507833)
65. Hart, N. H. & Collins, G. C. An electron-microscope and freeze-fracture study of the egg cortex of Brachydanio rerio. Cell Tissue Res. 265, 317-328 (1991).
66. Feng, B., Schwarz, H. & Jesuthasan, S. Furrow-speci-c endocytosis during cytokinesis of zebra-sh blastomeres. Exp. Cell Res. 279, 14-20 (2002).
67. von Kleist, L. et al. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146, 471-484 (2011).
68. Thieman, J. R. et al. Clathrin regulates the association of PIPKI 661 with the AP-2 adaptor-2 appendage. J. Biol. Chem. 284, 13924-13939 (2009).
69. Edeling, M. A. et al. Structural requirements for PACSIN/Syndapin operation during zebra-sh embryonic notochord development. PLoS One 4, e8150 (2009).