Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking

Harwardt M-LIE, Young P, Bleymüller W, Meyer T, Karathanasis C, Niemann H, Heilemann M, Dietz MS (2017)
FEBS Open Bio 7(9): 1422-1440.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
The human MET receptor tyrosine kinase contributes to vertebrate development and cell proliferation. As a proto-oncogene, it is a target in cancer therapies. MET is also relevant for bacterial infection by Listeria monocytogenes and is activated by the bacterial protein internalin B. The processes of ligand binding, receptor activation, and the diffusion behavior of MET within the plasma membrane as well as its interconnections with various cell components are not fully understood. We investigated the receptor diffusion dynamics using single-particle tracking and imaging fluorescence correlation spectroscopy and elucidated mobility states of resting and internalin B-bound MET. We show that internalin B-bound MET exhibits lower diffusion coefficients and diffuses in a more confined area in the membrane. We report that the fraction of immobile receptors is larger for internalin B-bound receptors than for resting MET. Results of single-particle tracking in cells treated with various cytotoxins depleting cholesterol from the membrane and disrupting the actin cytoskeleton and microtubules suggest that cholesterol and actin influence MET diffusion dynamics, while microtubules do not have any effect.
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Zeitschriftentitel
FEBS Open Bio
Band
7
Ausgabe
9
Seite(n)
1422-1440
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Harwardt M-LIE, Young P, Bleymüller W, et al. Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking. FEBS Open Bio. 2017;7(9):1422-1440.
Harwardt, M. - L. I. E., Young, P., Bleymüller, W., Meyer, T., Karathanasis, C., Niemann, H., Heilemann, M., et al. (2017). Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking. FEBS Open Bio, 7(9), 1422-1440. doi:10.1002/2211-5463.12285
Harwardt, M. - L. I. E., Young, P., Bleymüller, W., Meyer, T., Karathanasis, C., Niemann, H., Heilemann, M., and Dietz, M. S. (2017). Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking. FEBS Open Bio 7, 1422-1440.
Harwardt, M.-L.I.E., et al., 2017. Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking. FEBS Open Bio, 7(9), p 1422-1440.
M.-L.I.E. Harwardt, et al., “Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking”, FEBS Open Bio, vol. 7, 2017, pp. 1422-1440.
Harwardt, M.-L.I.E., Young, P., Bleymüller, W., Meyer, T., Karathanasis, C., Niemann, H., Heilemann, M., Dietz, M.S.: Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking. FEBS Open Bio. 7, 1422-1440 (2017).
Harwardt, Maria-Lena I.E., Young, Phoebe, Bleymüller, Willem, Meyer, Timo, Karathanasis, Christos, Niemann, Hartmut, Heilemann, Mike, and Dietz, Marina S. “Membrane dynamics of resting and internalin B-bound MET receptor tyrosine kinase studied by single-molecule tracking”. FEBS Open Bio 7.9 (2017): 1422-1440.

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

SPT and Imaging FCS Provide Complementary Information on the Dynamics of Plasma Membrane Molecules.
Harwardt MIE, Dietz MS, Heilemann M, Wohland T., Biophys J 114(10), 2018
PMID: 29650369

49 References

Daten bereitgestellt von Europe PubMed Central.

Receptor tyrosine kinases: mechanisms of activation and signaling.
Hubbard SR, Miller WT., Curr. Opin. Cell Biol. 19(2), 2007
PMID: 17306972
Cell signaling by receptor tyrosine kinases.
Lemmon MA, Schlessinger J., Cell 141(7), 2010
PMID: 20602996
Met, metastasis, motility and more.
Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF., Nat. Rev. Mol. Cell Biol. 4(12), 2003
PMID: 14685170
Degradation of the Met tyrosine kinase receptor by the ubiquitin‐proteasome pathway
AUTHOR UNKNOWN, 1997
Down-regulation of MET, the receptor for hepatocyte growth factor.
Hammond DE, Urbe S, Vande Woude GF, Clague MJ., Oncogene 20(22), 2001
PMID: 11420688
The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells.
Braun L, Ohayon H, Cossart P., Mol. Microbiol. 27(5), 1998
PMID: 9535096
InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase.
Shen Y, Naujokas M, Park M, Ireton K., Cell 103(3), 2000
PMID: 11081636
The Listeria protein internalin B mimics hepatocyte growth factor-induced receptor trafficking.
Li N, Xiang GS, Dokainish H, Ireton K, Elferink LA., Traffic 6(6), 2005
PMID: 15882443
Role of lipid rafts in E-cadherin-- and HGF-R/Met--mediated entry of Listeria monocytogenes into host cells.
Seveau S, Bierne H, Giroux S, Prevost MC, Cossart P., J. Cell Biol. 166(5), 2004
PMID: 15337781
GW domains of the Listeria monocytogenes invasion protein InlB are required for potentiation of Met activation.
Banerjee M, Copp J, Vuga D, Marino M, Chapman T, van der Geer P, Ghosh P., Mol. Microbiol. 52(1), 2004
PMID: 15049825
Single-molecule photobleaching reveals increased MET receptor dimerization upon ligand binding in intact cells.
Dietz MS, Haße D, Ferraris DM, Gohler A, Niemann HH, Heilemann M., BMC Biophys 6(1), 2013
PMID: 23731667
Rotational and translational diffusion in membranes.
Edidin M., Annu. Rev. Biophys. Bioeng. 3(0), 1974
PMID: 4371655
With or without rafts? Alternative views on cell membranes.
Sevcsik E, Schutz GJ., Bioessays 38(2), 2015
PMID: 26666984
Cellular cholesterol efflux mediated by cyclodextrins. Demonstration Of kinetic pools and mechanism of efflux.
Yancey PG, Rodrigueza WV, Kilsdonk EP, Stoudt GW, Johnson WJ, Phillips MC, Rothblat GH., J. Biol. Chem. 271(27), 1996
PMID: 8663188
Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles.
Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K., Mol. Biol. Cell 10(4), 1999
PMID: 10198050
Differential sensitivity to detergents of actin cytoskeleton from nerve endings.
Cubi R, Matas LA, Pou M, Aguilera J, Gil C., Biochim. Biophys. Acta 1828(11), 2013
PMID: 23817010
Lipid rafts are required for GLUT4 internalization in adipose cells.
Ros-Baro A, Lopez-Iglesias C, Peiro S, Bellido D, Palacin M, Zorzano A, Camps M., Proc. Natl. Acad. Sci. U.S.A. 98(21), 2001
PMID: 11593015
Harnessing actin dynamics for clathrin-mediated endocytosis.
Kaksonen M, Toret CP, Drubin DG., Nat. Rev. Mol. Cell Biol. 7(6), 2006
PMID: 16723976
Cell surface organization by the membrane skeleton.
Kusumi A, Sako Y., Curr. Opin. Cell Biol. 8(4), 1996
PMID: 8791449
Effects of cytochalasin and phalloidin on actin.
Cooper JA., J. Cell Biol. 105(4), 1987
PMID: 3312229
Actin-latrunculin A structure and function. Differential modulation of actin-binding protein function by latrunculin A.
Yarmola EG, Somasundaram T, Boring TA, Spector I, Bubb MR., J. Biol. Chem. 275(36), 2000
PMID: 10859320

AUTHOR UNKNOWN, 2000
Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain.
Ravelli RB, Gigant B, Curmi PA, Jourdain I, Lachkar S, Sobel A, Knossow M., Nature 428(6979), 2004
PMID: 15014504
Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density.
Giannone G, Hosy E, Levet F, Constals A, Schulze K, Sobolevsky AI, Rosconi MP, Gouaux E, Tampe R, Choquet D, Cognet L., Biophys. J. 99(4), 2010
PMID: 20713016
Electron multiplying charge-coupled device camera based fluorescence correlation spectroscopy.
Kannan B, Har JY, Liu P, Maruyama I, Ding JL, Wohland T., Anal. Chem. 78(10), 2006
PMID: 16689548
Structure of the human receptor tyrosine kinase met in complex with the Listeria invasion protein InlB.
Niemann HH, Jager V, Butler PJ, van den Heuvel J, Schmidt S, Ferraris D, Gherardi E, Heinz DW., Cell 130(2), 2007
PMID: 17662939
Advanced methods of microscope control using μManager software.
Edelstein AD, Tsuchida MA, Amodaj N, Pinkard H, Vale RD, Stuurman N., J Biol Methods 1(2), 2014
PMID: 25606571
Mean square displacement analysis of single‐particle trajectories with localization error
AUTHOR UNKNOWN, 2010
Integrins β1 and β3 exhibit distinct dynamic nanoscale organizations inside focal adhesions.
Rossier O, Octeau V, Sibarita JB, Leduc C, Tessier B, Nair D, Gatterdam V, Destaing O, Albiges-Rizo C, Tampe R, Cognet L, Choquet D, Lounis B, Giannone G., Nat. Cell Biol. 14(10), 2012
PMID: 23023225
Single-molecule imaging of transcription factor binding to DNA in live mammalian cells.
Gebhardt JC, Suter DM, Roy R, Zhao ZW, Chapman AR, Basu S, Maniatis T, Xie XS., Nat. Methods 10(5), 2013
PMID: 23524394
ImFCS: a software for imaging FCS data analysis and visualization.
Sankaran J, Shi X, Ho LY, Stelzer EH, Wohland T., Opt Express 18(25), 2010
PMID: 21164894
The ImageJ ecosystem: An open platform for biomedical image analysis.
Schindelin J, Rueden CT, Hiner MC, Eliceiri KW., Mol. Reprod. Dev. 82(7-8), 2015
PMID: 26153368
Calibration and limits of camera-based fluorescence correlation spectroscopy: a supported lipid bilayer study.
Bag N, Sankaran J, Paul A, Kraut RS, Wohland T., Chemphyschem 13(11), 2012
PMID: 22615144
Ganglioside embedded in reconstituted lipoprotein binds cholera toxin with elevated affinity.
Bricarello DA, Mills EJ, Petrlova J, Voss JC, Parikh AN., J. Lipid Res. 51(9), 2010
PMID: 20472870
GPI-anchored proteins do not reside in ordered domains in the live cell plasma membrane.
Sevcsik E, Brameshuber M, Folser M, Weghuber J, Honigmann A, Schutz GJ., Nat Commun 6(), 2015
PMID: 25897971
Spatial control of EGF receptor activation by reversible dimerization on living cells.
Chung I, Akita R, Vandlen R, Toomre D, Schlessinger J, Mellman I., Nature 464(7289), 2010
PMID: 20208517
Ligand signature in the membrane dynamics of single TrkA receptor molecules.
Marchetti L, Callegari A, Luin S, Signore G, Viegi A, Beltram F, Cattaneo A., J. Cell. Sci. 126(Pt 19), 2013
PMID: 23886941
A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family.
Ponzetto C, Bardelli A, Zhen Z, Maina F, dalla Zonca P, Giordano S, Graziani A, Panayotou G, Comoglio PM., Cell 77(2), 1994
PMID: 7513258
Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis.
Weidner KM, Di Cesare S, Sachs M, Brinkmann V, Behrens J, Birchmeier W., Nature 384(6605), 1996
PMID: 8906793
Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development.
Maina F, Casagranda F, Audero E, Simeone A, Comoglio PM, Klein R, Ponzetto C., Cell 87(3), 1996
PMID: 8898205
Hepatocyte growth factor-induced Ras activation requires ERM proteins linked to both CD44v6 and F-actin.
Orian-Rousseau V, Morrison H, Matzke A, Kastilan T, Pace G, Herrlich P, Ponta H., Mol. Biol. Cell 18(1), 2006
PMID: 17065554
Regulated migration of epidermal growth factor receptor from caveolae.
Mineo C, Gill GN, Anderson RG., J. Biol. Chem. 274(43), 1999
PMID: 10521449
Ligand-mediated dimerization of the Met receptor tyrosine kinase by the bacterial invasion protein InlB.
Ferraris DM, Gherardi E, Di Y, Heinz DW, Niemann HH., J. Mol. Biol. 395(3), 2009
PMID: 19900460

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