Artículo

Durrieu, L.; Kirrmaier, D.; Schneidt, T.; Kats, I.; Raghavan, S.; Hufnagel, L.; Saunders, T.E.; Knop, M. "Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis" (2018) Molecular Systems Biology. 14(9)
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Abstract:

Embryogenesis relies on instructions provided by spatially organized signaling molecules known as morphogens. Understanding the principles behind morphogen distribution and how cells interpret locally this information remains a major challenge in developmental biology. Here, we introduce morphogen-age measurements as a novel approach to test models of morphogen gradient formation. Using a tandem fluorescent timer as a protein age sensor, we find a gradient of increasing age of Bicoid along the anterior–posterior axis in the early Drosophila embryo. Quantitative analysis of the protein age distribution across the embryo reveals that the synthesis–diffusion–degradation model is the most likely model underlying Bicoid gradient formation, and rules out other hypotheses for gradient formation. Moreover, we show that the timer can detect transitions in the dynamics associated with syncytial cellularization. Our results provide new insight into Bicoid gradient formation and demonstrate how morphogen-age information can complement knowledge about movement, abundance, and distribution, which should be widely applicable to other systems. © 2018 The Authors. Published under the terms of the CC BY 4.0 license

Registro:

Documento: Artículo
Título:Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis
Autor:Durrieu, L.; Kirrmaier, D.; Schneidt, T.; Kats, I.; Raghavan, S.; Hufnagel, L.; Saunders, T.E.; Knop, M.
Filiación:Zentrum für Molekulare Biologie der Universität Heidelberg (ZMBH), DKFZ-ZMBH Alliance, University of Heidelberg, Heidelberg, Germany
European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
Deutsches Krebsforschungszentrum (DKFZ), DKFZ-ZMBH Alliance, Heidelberg, Germany
Mechanobiology Institute and Department of Biological Sciences, National University of Singapore, Singapore
Institute of Molecular and Cell Biology, A*Star, Biopolis, Singapore
Instituto Leloir, Buenos Aires, Argentina
Departamento de Fisiología, Biología Molecular, y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
p53 Laboratory, A*STAR, Singapore
Palabras clave:Drosophila melanogaster; embryogenesis; fluorescent timers; morphogen gradient; SPIM; morphogen; protein; Article; diffusion coefficient; Drosophila; embryo; embryo development; model; molecular dynamics; nonhuman; priority journal; protein analysis; protein degradation; protein processing; protein synthesis; quantitative analysis; signal transduction
Año:2018
Volumen:14
Número:9
DOI: http://dx.doi.org/10.15252/msb.20188355
Título revista:Molecular Systems Biology
Título revista abreviado:Mol. Syst. Biol.
ISSN:17444292
CAS:protein, 67254-75-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17444292_v14_n9_p_Durrieu

Referencias:

  • Abu-Arish, A., Porcher, A., Czerwonka, A., Dostatni, N., Fradin, C., High mobility of Bicoid captured by fluorescence correlation spectroscopy: implication for the rapid establishment of its gradient (2010) Biophys J, 99, pp. L33-L35
  • Alexandre, C., Baena-Lopez, A., Vincent, J.-P., Patterning and growth control by membrane-tethered Wingless (2014) Nature, 505, pp. 180-185
  • Barry, J.D., Dona, E., Gilmour, D., Huber, W., TimerQuant: a modelling approach to tandem fluorescent timer design and data interpretation for measuring protein turnover in embryos (2016) Development, 143, pp. 174-179
  • Baumgart, E., Kubitscheck, U., Scanned light sheet microscopy with confocal slit detection (2012) Opt Express, 20, pp. 21805-21814
  • Bergmann, S., Sandler, O., Sberro, H., Shnider, S., Schejter, E., Shilo, B.-Z., Barkai, N., Pre-steady-state decoding of the Bicoid morphogen gradient (2007) PLoS Biol, 5
  • Bergmann, S., Tamari, Z., Schejter, E., Shilo, B.-Z., Barkai, N., Re-examining the stability of the Bicoid morphogen gradient (2008) Cell, 132, pp. 15-17
  • Berleth, T., Burri, M., Thoma, G., Bopp, D., Richstein, S., Frigerio, G., Noll, M., Nüsslein-Volhard, C., The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo (1988) EMBO J, 7, pp. 1749-1756
  • Bialek, W., Gregor, T., Tank, D.W., Wieschaus, E.F., Response: can we fit all of the data? (2008) Cell, 132, pp. 17-18
  • Bothma, J.P., Norstad, M.R., Alamos, S., Garcia, H.G., LlamaTags: a versatile tool to image transcription factor dynamics in live embryos (2018) Cell, 173, pp. 1810-1822. , e16
  • Castle, B.T., Howard, S.A., Odde, D.J., Assessment of transport mechanisms underlying the bicoid morphogen gradient (2011) Cel Mol Bioeng, 4, pp. 116-121
  • Chen, B.-C., Legant, W.R., Wang, K., Shao, L., Milkie, D.E., Davidson, M.W., Janetopoulos, C., Reymann, A.-C., Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution (2014) Science, 346, p. 1257998
  • Coppey, M., Berezhkovskii, A.M., Kim, Y., Boettiger, A.N., Shvartsman, S.Y., Modeling the bicoid gradient: diffusion and reversible nuclear trapping of a stable protein (2007) Dev Biol, 312, pp. 623-630
  • Dalessi, S., Neves, A., Bergmann, S., Modeling morphogen gradient formation from arbitrary realistically shaped sources (2012) J Theor Biol, 294, pp. 130-138
  • Dickinson, M.E., Bearman, G., Tille, S., Lansford, R., Fraser, S.E., Multi-spectral imaging and linear unmixing add a whole new dimension to laser scanning fluorescence microscopy (2001) Biotechniques, 31, pp. 1272-1278
  • Dilão, R., Muraro, D., mRNA diffusion explains protein gradients in Drosophila early development (2010) J Theor Biol, 264, pp. 847-853
  • Donà, E., Barry, J.D., Valentin, G., Quirin, C., Khmelinskii, A., Kunze, A., Durdu, S., Gilmour, D., Directional tissue migration through a self-generated chemokine gradient (2014) Nature, 503, pp. 285-289
  • Driever, W., Nüsslein-Volhard, C., A gradient of bicoid protein in Drosophila embryos (1988) Cell, 54, pp. 83-93
  • Driever, W., Nüsslein-Volhard, C., The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner (1988) Cell, 54, pp. 95-104
  • Drocco, J.A., Grimm, O., Tank, D.W., Wieschaus, E., Measurement and perturbation of morphogen lifetime: effects on gradient shape (2011) Biophys J, 101, pp. 1807-1815
  • Erdmann, T., Howard, M., ten Wolde, P.R., Role of spatial averaging in the precision of gene expression patterns (2009) Phys Rev Lett, 103, p. 258101
  • Frigerio, G., Burri, M., Bopp, D., Baumgartner, S., Noll, M., Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network (1986) Cell, 47, pp. 735-746
  • Gregor, T., Tank, D.W., Wieschaus, E.F., Bialek, W., Probing the limits to positional information (2007) Cell, 130, pp. 153-164
  • Gregor, T., Wieschaus, E.F., McGregor, A.P., Bialek, W., Tank, D.W., Stability and nuclear dynamics of the bicoid morphogen gradient (2007) Cell, 130, pp. 141-152
  • Grimm, O., Coppey, M., Wieschaus, E., Modelling the Bicoid gradient (2010) Development, 137, pp. 2253-2264
  • Hecht, I., Rappel, W.-J., Levine, H., Determining the scale of the Bicoid morphogen gradient (2009) Proc Natl Acad Sci USA, 106, pp. 1710-1715
  • Houchmandzadeh, B., Wieschaus, E., Leibler, S., Establishment of developmental precision and proportions in the early Drosophila embryo (2002) Nature, 415, pp. 798-802
  • Huang, A., Amourda, C., Zhang, S., Tolwinski, N.S., Saunders, T.E., Decoding temporal interpretation of the morphogen Bicoid in the early Drosophila embryo (2017) Elife, 6, p. 197
  • Jaeger, J., A matter of timing and precision (2010) Mol Sys Biol, 6, p. 427
  • Kavousanakis, M.E., Kanodia, J.S., Kim, Y., Kevrekidis, I.G., Shvartsman, S.Y., A compartmental model for the bicoid gradient (2010) Dev Biol, 345, pp. 12-17
  • Khmelinskii, A., Keller, P.J., Bartosik, A., Meurer, M., Barry, J.D., Mardin, B.R., Kaufmann, A., Knop, M., Tandem fluorescent protein timers for in vivo analysis of protein dynamics (2012) Nat Biotechnol, 30, pp. 708-714
  • Khmelinskii, A., Knop, M., Analysis of protein dynamics with tandem fluorescent protein timers (2014) Computational systems biology, pp. 195-210. , Ireton R, Montgomery K, Bumgarner R, Samudrala R, McDermott J, (eds), pp, New York, NY, Springer New York
  • Khmelinskii, A., Meurer, M., Ho, C.-T., Besenbeck, B., Füller, J., Lemberg, M.K., Bukau, B., Knop, M., Incomplete proteasomal degradation of green fluorescent proteins in the context of tandem fluorescent protein timers (2016) Mol Biol Cell, 27, pp. 360-370
  • Kicheva, A., Bollenbach, T., Ribeiro, A., Valle, H.P., Lovell-Badge, R., Episkopou, V., Briscoe, J., Coordination of progenitor specification and growth in mouse and chick spinal cord (2014) Science, 345, p. 1254927
  • Kraus, B., Ziegler, M., Wolff, H., Linear fluorescence unmixing in cell biological research (2007) Modern Res Educ Topics Microsc, 3, pp. 863-872
  • Krzic, U., Gunther, S., Saunders, T.E., Streichan, S.J., Hufnagel, L., Multiview light-sheet microscope for rapid in toto imaging (2012) Nat Meth, 9, pp. 730-733
  • de Lachapelle, A.M., Bergmann, S., Precision and scaling in morphogen gradient read-out (2010) Mol Sys Biol, 6, p. 351
  • de Lachapelle, A.M., Bergmann, S., Pre-steady and stable morphogen gradients: can they coexist? (2010) Mol Sys Biol, 6, p. 428
  • Lander, A.D., Pattern, growth, and control (2011) Cell, 144, pp. 955-969
  • Liang, H.-L., Nien, C.-Y., Liu, H.-Y., Metzstein, M.M., Kirov, N., Rushlow, C., The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila (2008) Nature, 456, pp. 400-403
  • Little, S.C., Tkačik, G., Kneeland, T.B., Wieschaus, E.F., Gregor, T., The formation of the bicoid morphogen gradient requires protein movement from anteriorly localized mRNA (2011) PLoS Biol, 9
  • Little, S.C., Tikhonov, M., Gregor, T., Precise developmental gene expression arises from globally stochastic transcriptional activity (2013) Cell, 154, pp. 789-800
  • Liu, J., Ma, J., Fates-shifted is an F-box protein that targets Bicoid for degradation and regulates developmental fate determination in Drosophila embryos (2011) Nat Cell Biol, 13, pp. 22-29
  • Liu, J., He, F., Ma, J., Morphogen gradient formation and action (2011) Fly, 5, pp. 242-246
  • Liu, F., Morrison, A.H., Gregor, T., Dynamic interpretation of maternal inputs by the Drosophila segmentation gene network (2013) Proc Natl Acad Sci USA, 110, pp. 6724-6729
  • de Medeiros, G., Norlin, N., Gunther, S., Albert, M., Panavaite, L., Fiuza, U.-M., Peri, F., Hufnagel, L., Confocal multiview light-sheet microscopy (2015) Nat Commun, 6, p. 8881
  • Mir, M., Reimer, A., Haines, J.E., Li, X.-Y., Stadler, M., Garcia, H., Eisen, M.B., Darzacq, X., Dense Bicoid hubs accentuate binding along the morphogen gradient (2017) Genes Dev, 31, pp. 1784-1794
  • Muller, P., Rogers, K.W., Yu, S.R., Brand, M., Schier, A.F., Morphogen transport (2013) Development, 140, pp. 1621-1638
  • Ribes, V., Briscoe, J., Establishing and interpreting graded sonic hedgehog signaling during vertebrate neural tube patterning: the role of negative feedback (2009) CSH Persp Biol, 1, p. a002014
  • Rogers, K.W., Schier, A.F., Morphogen gradients: from generation to interpretation (2011) Annu Rev Cell Dev Biol, 27, pp. 377-407
  • Saunders, T., Howard, M., When it pays to rush: interpreting morphogen gradients prior to steady-state (2009) Phys Biol, 6, p. 046020
  • Schmid, B., Shah, G., Scherf, N., Weber, M., Thierbach, K., Campos, C.P.E.R., Roeder, I., Huisken, J., High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics (2013) Nat Commun, 4, p. 2207
  • Sigaut, L., Pearson, J.E., Colman-Lerner, A., Ponce Dawson, S., Messages do diffuse faster than messengers: reconciling disparate estimates of the morphogen Bicoid diffusion coefficient (2014) PLoS Comput Biol, 10
  • Sommer, C., Straehle, C., Kothe, U., ilastik: interactive learning and segmentation toolkit (2011) 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro, pp. 230-233. , https://doi.org/10.1109/ISBI.2011.5872394, pp, Chicago, IL
  • Spirov, A., Fahmy, K., Schneider, M., Frei, E., Noll, M., Baumgartner, S., Formation of the bicoid morphogen gradient: an mRNA gradient dictates the protein gradient (2009) Development, 136, pp. 605-614
  • Stelzer, E.H.K., Light-sheet fluorescence microscopy for quantitative biology (2015) Nat Meth, 12, pp. 23-26
  • Tomer, R., Khairy, K., Amat, F., Keller, P.J., Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy (2012) Nat Meth, 9, pp. 755-763
  • Wieschaus, E., Wassarman, P.M., Positional information and cell fate determination in the early Drosophila embryo (2016) Essays on developmental biology, part B, 117, pp. 567-579. , (ed), Chapter 33, pp, Cambridge, MA, Academic Press
  • Wolpert, L., Positional information and the spatial pattern of cellular differentiation (1969) J Theor Biol, 25, pp. 1-47

Citas:

---------- APA ----------
Durrieu, L., Kirrmaier, D., Schneidt, T., Kats, I., Raghavan, S., Hufnagel, L., Saunders, T.E.,..., Knop, M. (2018) . Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis. Molecular Systems Biology, 14(9).
http://dx.doi.org/10.15252/msb.20188355
---------- CHICAGO ----------
Durrieu, L., Kirrmaier, D., Schneidt, T., Kats, I., Raghavan, S., Hufnagel, L., et al. "Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis" . Molecular Systems Biology 14, no. 9 (2018).
http://dx.doi.org/10.15252/msb.20188355
---------- MLA ----------
Durrieu, L., Kirrmaier, D., Schneidt, T., Kats, I., Raghavan, S., Hufnagel, L., et al. "Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis" . Molecular Systems Biology, vol. 14, no. 9, 2018.
http://dx.doi.org/10.15252/msb.20188355
---------- VANCOUVER ----------
Durrieu, L., Kirrmaier, D., Schneidt, T., Kats, I., Raghavan, S., Hufnagel, L., et al. Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis. Mol. Syst. Biol. 2018;14(9).
http://dx.doi.org/10.15252/msb.20188355