An Engineered Minimal WASP-Myosin Fusion Protein Reveals Essential Functions for Endocytosis

Developmental Cell

Volumn 35, Issue 3, 2015, Pages 281-294

  Lewellyn, Eric B ^a,b   Pedersen, Ross T A ^a   Hong, Jessica ^a   Lu, Rebecca ^a   Morrison, Huntly M ^a   Drubin, David G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; HYBRID PROTEIN; UNCLASSIFIED DRUG; WASP MYOSIN FUSION PROTEIN; ACTIN; MYOSIN; PROTEIN BINDING; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN FILAMENT; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; ANIMAL; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; MYOSINS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 84946750356     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.10.007     Document Type: Article

References (46)

1. Aghamohammadzadeh S., Ayscough K.R. Differential requirements for actin during yeast and mammalian endocytosis. Nat. Cell Biol. 2009, 11:1039-1042.
2. Boettner D.R., Friesen H., Andrews B., Lemmon S.K. Clathrin light chain directs endocytosis by influencing the binding of the yeast Hip1R homologue, Sla2, to F-actin. Mol. Biol. Cell 2011, 22:3699-3714.
3. Boettner D.R., Chi R.J., Lemmon S.K. Lessons from yeast for clathrin-mediated endocytosis. Nat. Cell Biol. 2012, 14:2-10.
4. Boulant S., Kural C., Zeeh J.-C., Ubelmann F., Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13:1124-1131.
5. Burke T.A., Christensen J.R., Barone E., Suarez C., Sirotkin V., Kovar D.R. Homeostatic actin cytoskeleton networks are regulated by assembly factor competition for monomers. Curr. Biol. 2014, 24:579-585.
6. Cheng J., Grassart A., Drubin D.G. Myosin 1E coordinates actin assembly and cargo trafficking during clathrin-mediated endocytosis. Mol. Biol. Cell 2012, 23:2891-2904.
7. Desrivières S., Cooke F.T., Parker P.J., Hall M.N. MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J. Biol. Chem. 1998, 273:15787-15793.
8. Evangelista M., Klebl B.M., Tong A.H., Webb B.A., Leeuw T., Leberer E., Whiteway M., Thomas D.Y., Boone C. A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. J. Cell Biol. 2000, 148:353-362.
9. Feeser E.A., Ignacio C.M.G., Krendel M., Ostap E.M. Myo1e binds anionic phospholipids with high affinity. Biochemistry 2010, 49:9353-9360.
10. Feliciano D., Di Pietro S.M. SLAC, a complex between Sla1 and Las17, regulates actin polymerization during clathrin-mediated endocytosis. Mol. Biol. Cell 2012, 23:4256-4272.
11. Ferguson S.M., Raimondi A., Paradise S., Shen H., Mesaki K., Ferguson A., Destaing O., Ko G., Takasaki J., Cremona O., et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 2009, 17:811-822.
12. 2 and CK2 modulates actin polymerization during endocytic uptake. Dev. Cell 2014, 30:746-758.
13. Friedman A.L., Geeves M.A., Manstein D.J., Spudich J.A. Kinetic characterization of myosin head fragments with long-lived myosin.ATP states. Biochemistry 1998, 37:9679-9687.
14. Galletta B.J., Chuang D.Y., Cooper J.A. Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLoS Biol. 2008, 6:e1.
15. Geli M.I., Lombardi R., Schmelzl B., Riezman H. An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO J. 2000, 19:4281-4291.
16. Greenberg M.J., Lin T., Goldman Y.E., Shuman H., Ostap E.M. Myosin IC generates power over a range of loads via a new tension-sensing mechanism. Proc. Natl. Acad. Sci. USA 2012, 109:E2433-E2440.
17. Grötsch H., Giblin J.P., Idrissi F.-Z., Fernández-Golbano I.-M., Collette J.R., Newpher T.M., Robles V., Lemmon S.K., Geli M.-I. Calmodulin dissociation regulates Myo5 recruitment and function at endocytic sites. EMBO J. 2010, 29:2899-2914.
18. Hokanson D.E., Ostap E.M. Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate. Proc. Natl. Acad. Sci. USA 2006, 103:3118-3123.
19. Hokanson D.E., Laakso J.M., Lin T., Sept D., Ostap E.M. Myo1c binds phosphoinositides through a putative pleckstrin homology domain. Mol. Biol. Cell 2006, 17:4856-4865.
20. Idrissi F.Z., Wolf B.L., Geli M.I. Cofilin, but not profilin, is required for myosin-I-induced actin polymerization and the endocytic uptake in yeast. Mol. Biol. Cell 2002, 13:4074-4087.
21. Idrissi F.-Z., Grötsch H., Fernández-Golbano I.M., Presciatto-Baschong C., Riezman H., Geli M.-I. Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. J. Cell Biol. 2008, 180:1219-1232.
22. Idrissi F.-Z., Blasco A., Espinal A., Geli M.I. Ultrastructural dynamics of proteins involved in endocytic budding. Proc. Natl. Acad. Sci. USA 2012, 109:E2587-E2594.
23. Jonsdottir G.A., Li R. Dynamics of yeast Myosin I: evidence for a possible role in scission of endocytic vesicles. Curr. Biol. 2004, 14:1604-1609.
24. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 2003, 115:475-487.
25. Kaksonen M., Toret C.P., Drubin D.G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
26. Kishimoto T., Sun Y., Buser C., Liu J., Michelot A., Drubin D.G. Determinants of endocytic membrane geometry, stability, and scission. Proc. Natl. Acad. Sci. USA 2011, 108:E979-E988.
27. Krendel M., Osterweil E.K., Mooseker M.S. Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett. 2008, 581:644-650.
28. Kübler E., Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 1993, 12:2855-2862.
29. Kukulski W., Schorb M., Kaksonen M., Briggs J.A. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 2012, 150:508-520.
30. Laakso J.M., Lewis J.H., Shuman H., Ostap E.M. Myosin I can act as a molecular force sensor. Science 2008, 321:133-136.
31. Lechler T., Shevchenko A., Li R. Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J. Cell Biol. 2000, 148:363-373.
32. Longtine M.S., Iii A.M.K., Demarini D.J., Shah N.G. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
33. Merrifield C.J., Perrais D., Zenisek D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 2005, 121:593-606.
34. Okreglak V., Drubin D.G. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J. Cell Biol. 2007, 178:1251-1264.
35. Okreglak V., Drubin D.G. Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway. J. Cell Biol. 2010, 188:769-777.
36. Picco A., Mund M., Ries J., Nédélec F., Kaksonen M. Visualizing the functional architecture of the endocytic machinery. eLife 2015, 4.
37. Skruzny M., Brach T., Ciuffa R., Rybina S., Wachsmuth M., Kaksonen M. Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proc. Natl. Acad. Sci. USA 2012, 109:E2533-E2542.
38. Soulard A., Lechler T., Spiridonov V., Shevchenko A., Shevchenko A., Li R., Winsor B. Saccharomyces cerevisiae Bzz1p is implicated with type I myosins in actin patch polarization and is able to recruit actin-polymerizing machinery in vitro. Mol. Cell. Biol. 2002, 22:7889-7906.
39. Suarez C., Carroll R.T., Burke T.A., Christensen J.R., Bestul A.J., Sees J.A., James M.L., Sirotkin V., Kovar D.R. Profilin regulates F-actin network homeostasis by favoring formin over Arp2/3 complex. Dev. Cell 2015, 32:43-53.
40. Suetsugu S., Kurisu S., Takenawa T. Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins. Physiol. Rev. 2014, 94:1219-1248.
41. Sun Y., Kaksonen M., Madden D.T., Schekman R., Drubin D.G. Interaction of Sla2p's ANTH domain with PtdIns(4,5)P2 is important for actin-dependent endocytic internalization. Mol. Biol. Cell 2005, 16:717-730.
42. Sun Y., Martin A.C., Drubin D.G. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev. Cell 2006, 11:33-46.
43. Sun Y., Leong N.T., Wong T., Drubin D.G. A Pan1/End3/Sla1 complex links Arp2/3-mediated actin assembly to sites of clathrin-mediated endocytosis. Mol. Biol. Cell. 2015, Published online September 2, 2015. mbc.E15-04-0252.
44. Taylor M.J., Perrais D., Merrifield C.J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 2011, 9:e1000604.
45. Tonikian R., Xin X., Toret C.P., Gfeller D., Landgraf C., Panni S., Paoluzi S., Castagnoli L., Currell B., Seshagiri S., et al. Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins. PLoS Biol. 2009, 7:e1000218.
46. Wong M.H., Meng L., Rajmohan R., Yu S., Thanabalu T. Vrp1p-Las17p interaction is critical for actin patch polarization but is not essential for growth or fluid phase endocytosis in S. cerevisiae. Biochim. Biophys. Acta 2010, 1803:1332-1346.