Optical Tweezers Studies on Notch: Single-Molecule Interaction Strength Is Independent of Ligand Endocytosis

Developmental Cell

Volumn 22, Issue 6, 2012, Pages 1313-1320

  Shergill, Bhupinder ^c   Meloty Kapella, Laurence ^a   Musse, Abdiwahab A ^a   Weinmaster, Gerry ^a,b   Botvinick, Elliot ^c,d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e EDWARDS LIFESCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE1 LIGAND; LIGAND; NOTCH RECEPTOR; NOTCH1 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; LIGAND BINDING; LIGAND ENDOCYTOSIS; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN INTERACTION;

ANIMALS; CELL LINE; ENDOCYTOSIS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MICE; OPTICAL TWEEZERS; PROTEIN BINDING; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION;

EID: 84862119187     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.04.007     Document Type: Article

References (48)

1. Ahimou F., Mok L.P., Bardot B., Wesley C. The adhesion force of Notch with Delta and the rate of Notch signaling. J. Cell Biol. 2004, 167:1217-1229.
2. Banks S.M., Cho B., Eun S.H., Lee J.H., Windler S.L., Xie X., Bilder D., Fischer J.A. The functions of auxilin and Rab11 in Drosophila suggest that the fundamental role of ligand endocytosis in notch signaling cells is not recycling. PLoS ONE 2011, 6:e18259.
3. Benhra N., Vignaux F., Dussert A., Schweisguth F., Le Borgne R. Neuralized promotes basal to apical transcytosis of delta in epithelial cells. Mol. Biol. Cell 2010, 21:2078-2086.
4. Chen C., Zhuang X. Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc. Natl. Acad. Sci. USA 2008, 105:11790-11795.
5. Chen H., Ko G., Zatti A., Di Giacomo G., Liu L., Raiteri E., Perucco E., Collesi C., Min W., Zeiss C., et al. Embryonic arrest at midgestation and disruption of Notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proc. Natl. Acad. Sci. USA 2009, 106:13838-13843.
6. Cordle J., Johnson S., Tay J.Z., Roversi P., Wilkin M.B., de Madrid B.H., Shimizu H., Jensen S., Whiteman P., Jin B., et al. A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition. Nat. Struct. Mol. Biol. 2008, 15:849-857.
7. Cordle J., Redfieldz C., Stacey M., van der Merwe P.A., Willis A.C., Champion B.R., Hambleton S., Handford P.A. Localization of the delta-like-1-binding site in human Notch-1 and its modulation by calcium affinity. J. Biol. Chem. 2008, 283:11785-11793.
8. D'Souza B., Meloty-Kapella L., Weinmaster G. Canonical and non-canonical Notch ligands. Curr. Top. Dev. Biol. 2010, 92:73-129.
9. Damke H., Baba T., van der Bliek A.M., Schmid S.L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 1995, 131:69-80.
10. Damke H., Binns D.D., Ueda H., Schmid S.L., Baba T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 2001, 12:2578-2589.
11. Emery G., Hutterer A., Berdnik D., Mayer B., Wirtz-Peitz F., Gaitan M.G., Knoblich J.A. Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 2005, 122:763-773.
12. Fehon R.G., Kooh P.J., Rebay I., Regan C.L., Xu T., Muskavitch M.A., Artavanis-Tsakonas S. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 1990, 61:523-534.
13. 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.
14. Fortini M.E., Bilder D. Endocytic regulation of Notch signaling. Curr. Opin. Genet. Dev. 2009, 19:323-328.
15. Fürthauer M., González-Gaitán M. Endocytic regulation of notch signalling during development. Traffic 2009, 10:792-802.
16. Gordon W.R., Arnett K.L., Blacklow S.C. The molecular logic of Notch signaling-a structural and biochemical perspective. J. Cell Sci. 2008, 121:3109-3119.
17. Heuss S.F., Ndiaye-Lobry D., Six E.M., Israël A., Logeat F. The intracellular region of Notch ligands Dll1 and Dll3 regulates their trafficking and signaling activity. Proc. Natl. Acad. Sci. USA 2008, 105:11212-11217.
18. Hicks C., Ladi E., Lindsell C., Hsieh J.J., Hayward S.D., Collazo A., Weinmaster G. A secreted Delta1-Fc fusion protein functions both as an activator and inhibitor of Notch1 signaling. J. Neurosci. Res. 2002, 68:655-667.
19. Itoh M., Kim C.H., Palardy G., Oda T., Jiang Y.J., Maust D., Yeo S.Y., Lorick K., Wright G.J., Ariza-McNaughton L., et al. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 2003, 4:67-82.
20. Jafar-Nejad H., Andrews H.K., Acar M., Bayat V., Wirtz-Peitz F., Mehta S.Q., Knoblich J.A., Bellen H.J. Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev. Cell 2005, 9:351-363.
21. Kotlarchyk M.A., Shreim S.G., Alvarez-Elizondo M.B., Estrada L.C., Singh R., Valdevit L., Kniazeva E., Gratton E., Putnam A.J., Botvinick E.L. Concentration independent modulation of local micromechanics in a fibrin gel. PLoS ONE 2011, 6:e20201.
22. Litvinov R.I., Shuman H., Bennett J.S., Weisel J.W. Binding strength and activation state of single fibrinogen-integrin pairs on living cells. Proc. Natl. Acad. Sci. USA 2002, 99:7426-7431.
23. Litvinov S.V., Velders M.P., Bakker H.A., Fleuren G.J., Warnaar S.O. Ep-CAM: a human epithelial antigen is a homophilic cell-cell adhesion molecule. J. Cell Biol. 1994, 125:437-446.
24. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 2006, 10:839-850.
25. McLachlan G., Peel D. Finite Mixture Models 2000, J Wiley, New York.
26. Meloty-Kapella L., Shergill B., Kuon J., Botvinick E., Weinmaster G. Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins and actin. Dev. Cell 2012, 22:1299-1312. this issue.
27. Nichols J.T., Miyamoto A., Olsen S.L., D'Souza B., Yao C., Weinmaster G. DSL ligand endocytosis physically dissociates Notch1 heterodimers before activating proteolysis can occur. J. Cell Biol. 2007, 176:445-458.
28. Nichols J.T., Miyamoto A., Weinmaster G. Notch signaling-constantly on the move. Traffic 2007, 8:959-969.
29. Overstreet E., Chen X., Wendland B., Fischer J.A. Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Curr. Biol. 2003, 13:854-860.
30. Overstreet E., Fitch E., Fischer J.A. Fat facets and liquid facets promote Delta endocytosis and Delta signaling in the signaling cells. Development 2004, 131:5355-5366.
31. Panorchan P., Thompson M.S., Davis K.J., Tseng Y., Konstantopoulos K., Wirtz D. Single-molecule analysis of cadherin-mediated cell-cell adhesion. J. Cell Sci. 2006, 119:66-74.
32. Parks A.L., Klueg K.M., Stout J.R., Muskavitch M.A. Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 2000, 127:1373-1385.
33. Parks A.L., Stout J.R., Shepard S.B., Klueg K.M., Dos Santos A.A., Parody T.R., Vaskova M., Muskavitch M.A. Structure-function analysis of delta trafficking, receptor binding and signaling in Drosophila. Genetics 2006, 174:1947-1961.
34. Rajan A., Tien A.C., Haueter C.M., Schulze K.L., Bellen H.J. The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors. Nat. Cell Biol. 2009, 11:815-824.
35. Rebay I., Fleming R.J., Fehon R.G., Cherbas L., Cherbas P., Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 1991, 67:687-699.
36. Salomo M., Keyser U.F., Struhalla M., Kremer F. Optical tweezers to study single protein A/immunoglobulin G interactions at varying conditions. Eur. Biophys. J. 2008, 37:927-934.
37. Seugnet L., Simpson P., Haenlin M. Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 1997, 192:585-598.
38. Shao J.Y., Hochmuth R.M. Mechanical anchoring strength of L-selectin, beta2 integrins, and CD45 to neutrophil cytoskeleton and membrane. Biophys. J. 1999, 77:587-596.
39. Shimizu K., Chiba S., Kumano K., Hosoya N., Takahashi T., Kanda Y., Hamada Y., Yazaki Y., Hirai H. Mouse jagged1 physically interacts with notch2 and other notch receptors. Assessment by quantitative methods. J. Biol. Chem. 1999, 274:32961-32969.
40. Sprinzak D., Lakhanpal A., Lebon L., Santat L.A., Fontes M.E., Anderson G.A., Garcia-Ojalvo J., Elowitz M.B. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010, 465:86-90.
41. Stout A.L. Detection and characterization of individual intermolecular bonds using optical tweezers. Biophys. J. 2001, 80:2976-2986.
42. Tees D.F., Waugh R.E., Hammer D.A. A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys. J. 2001, 80:668-682.
43. Tian X., Hansen D., Schedl T., Skeath J.B. Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 2004, 131:5807-5815.
44. Ullrich O., Reinsch S., Urbé S., Zerial M., Parton R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 1996, 135:913-924.
45. Wang W., Struhl G. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 2004, 131:5367-5380.
46. Wang W., Struhl G. Distinct roles for Mind bomb, Neuralized and Epsin in mediating DSL endocytosis and signaling in Drosophila. Development 2005, 132:2883-2894.
47. Weisel J.W., Shuman H., Litvinov R.I. Protein-protein unbinding induced by force: single-molecule studies. Curr. Opin. Struct. Biol. 2003, 13:227-235.
48. Windler S.L., Bilder D. Endocytic internalization routes required for delta/notch signaling. Curr. Biol. 2010, 20:538-543.