Cell-selective labelling of proteomes in Drosophila melanogaster

Nature Communications

Volumn 6, Issue , 2015, Pages

  Erdmann, Ines ^a,b   Marter, Kathrin ^a,b   Kobler, Oliver ^b   Niehues, Sven ^c,d   Abele, Julia ^a,b   Müller, Anke ^a,b   Bussmann, Julia ^c,d   Storkebaum, Erik ^c,d   Ziv, Tamar ^e   Thomas, Ulrich ^b   Dieterich, Daniela C ^a,b,f  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^f Center for Behavioral Brain Sciences   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYNE; AMINO ACID; AZIDE; AZIDONORLEUCINE; GLYCINE; LEUCINE; METHIONINE; METHIONINE TRANSFER RNA LIGASE; PROTEIN HYDROLYSATE; PROTEOME; UNCLASSIFIED DRUG;

AMINO ACID; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; FLUORESCENCE; FLY; GENE EXPRESSION; LABORATORY METHOD; MUTATION; PROTEIN; PROTEOMICS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BIOORTHOGONAL NONCANONICAL AMINO ACID TAGGING; CELL SELECTION; CELL SPECIFICITY; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DIET SUPPLEMENTATION; DROSOPHILA MELANOGASTER; FLUORESCENT NONCANONICAL AMINO ACID TAGGING; GENE MUTATION; IN VIVO STUDY; NONHUMAN; PROCEDURES CONCERNING CELLS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; TRANSLATION REGULATION; ANIMAL; CHEMISTRY; CLICK CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROCEDURES; STAINING;

DROSOPHILA MELANOGASTER;

ALKYNES; AMINO ACIDS; ANIMALS; CLICK CHEMISTRY; DROSOPHILA MELANOGASTER; GLYCINE; METHIONINE; METHIONINE-TRNA LIGASE; MUTATION; PROTEOME; STAINING AND LABELING;

EID: 84936818255     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8521     Document Type: Article

References (58)

1. Pandey, A. & Mann, M. Proteomics to study genes and genomes. Nature 405, 837-846 (2000).
2. Burkhart, J. M. et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120, e73-e82 (2012).
3. Grant, M. M., Scheel-Toellner, D. & Griffiths, H. R. Contributions to our understanding of T cell physiology through unveiling the T cell proteome. Clin. Exp. Immunol. 149, 9-15 (2007).
4. Lonnberg, T., Chen, Z. & Lahesmaa, R. From a gene-centric to whole-proteome view of differentiation of T helper cell subsets. Brief. Funct. Genomics 12, 471-482 (2013).
5. Wasbrough, E. R. et al. The Drosophila melanogaster sperm proteome-II (DmSP-II). J. Proteomics 73, 2171-2185 (2010).
6. Wilkins, M. R. et al. High-throughput mass spectrometric discovery of protein post-translational modifications. J. Mol. Biol. 289, 645-657 (1999).
7. Peng, J. et al. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926 (2003).
8. Panse, V. G., Hardeland, U., Werner, T., Kuster, B. & Hurt, E. A proteomewide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279, 41346-41351 (2004).
9. Cohen, L. D. et al. Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS ONE 8, e63191 (2013).
10. Dieterich, D. C. Chemical reporters for the illumination of protein and cell dynamics. Curr. Opin. Neurobiol. 20, 623-630 (2010).
11. Ong, S. E. et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386 (2002).
12. Link, A. J., Mock, M. L. & Tirrell, D. A. Non-canonical amino acids in protein engineering. Curr. Opin. Biotechnol. 14, 603-609 (2003).
13. Liu, J., Xu, Y., Stoleru, D. & Salic, A. Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. Proc. Natl Acad. Sci. USA 109, 413-418 (2012).
14. Dieterich, D. C. et al. Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat. Protoc. 2, 532-540 (2007).
15. Dieterich, D. C., Link, A. J., Graumann, J., Tirrell, D. A. & Schuman, E. M. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc. Natl Acad. Sci. USA 103, 9482-9487 (2006).
16. Beatty, K. E. et al. Fluorescence visualization of newly synthesized proteins in mammalian cells. Angew. Chem. Int. Ed. Engl. 45, 7364-7367 (2006).
17. Dieterich, D. C. et al. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13, 897-905 (2010).
18. Tom Dieck, S. et al. Metabolic labeling with noncanonical amino acids and visualization by chemoselective fluorescent tagging. Curr. Protoc. Cell. Biol. 1, 7.11 (2012).
19. Link, A. J. & Tirrell, D. A. Cell surface labeling of Escherichia coli via copper(I)- catalyzed [3+2] cycloaddition. J. Am. Chem. Soc. 125, 11164-11165 (2003).
20. Tcherkezian, J., Brittis, P. A., Thomas, F., Roux, P. P. & Flanagan, J. G. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141, 632-644 (2010).
21. Yoon, B. C. et al. Local translation of extranuclear lamin B promotes axon maintenance. Cell 148, 752-764 (2012).
22. Hinz, F. I., Dieterich, D. C., Tirrell, D. A. & Schuman, E. M. Non-canonical amino acid labelling in vivo to visualize and affinity purify newly synthesized proteins in larval zebrafish. ACS Chem. Neurosci. 3, 40-49 (2012).
23. Link, A. J. et al. Discovery of aminoacyl-tRNA synthetase activity through cell-surface display of noncanonical amino acids. Proc. Natl Acad. Sci. USA 103, 10180-10185 (2006).
24. Tanrikulu, I. C., Schmitt, E., Mechulam, Y., Goddard, W. A., 3rd & Tirrell, D. A. Discovery of Escherichia coli methionyl-tRNA synthetase mutants for efficient labeling of proteins with azidonorleucine in vivo. Proc. Natl Acad. Sci. USA 106, 15285-15290 (2009).
25. Ngo, J. T. et al. Cell-selective metabolic labeling of proteins. Nat. Chem. Biol. 5, 715-717 (2009).
26. Ngo, J. T., Schuman, E. M. & Tirrell, D. A. Mutant methionyl-tRNA synthetase from bacteria enables site-selective N-terminal labelling of proteins expressed in mammalian cells. Proc. Natl Acad. Sci. USA 110, 4992-4997 (2013).
27. Fukuyama, H. et al. Landscape of protein-protein interactions in Drosophila immune deficiency signaling during bacterial challenge. Proc. Natl Acad. Sci. USA 110, 10717-10722 (2013).
28. Kwon, Y. et al. The Hippo signaling pathway interactome. Science 342, 737-740 (2013).
29. Owald, D. et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J. Cell Biol. 188, 565-579 (2010).
30. Guruharsha, K. G. et al. A protein complex network of Drosophila melanogaster. Cell 147, 690-703 (2011).
31. Loevenich, S. N. et al. The Drosophila melanogaster PeptideAtlas facilitates the use of peptide data for improved fly proteomics and genome annotation. BMC Bioinformatics 10, 59 (2009).
32. Mahdavi, A. et al. Identification of secreted bacterial proteins by noncanonical amino acid tagging. Proc. Natl Acad. Sci. USA 111, 433-438 (2014).
33. Bachmann, A. et al. A perisynaptic menage a trois between Dlg, DLin-7, and Metro controls proper organization of Drosophila synaptic junctions. J. Neurosci. 30, 5811-5824 (2010).
34. Hu, Y., Ye, Y. & Fortini, M. E. Nicastrin is required for gamma-secretase cleavage of the Drosophila Notch receptor. Dev. Cell 2, 69-78 (2002).
35. Nichols, C. D., Becnel, J. & Pandey, U. B. Methods to assay Drosophila behavior. J. Vis. Exp. 61, e3795 (2012).
36. Ali, Y. O., Escala, W., Ruan, K. & Zhai, R. G. Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. J. Vis. Exp. 49, e2504 (2011).
37. Schmidt, I. et al. Kinesin heavy chain function in Drosophila glial cells controls neuronal activity. J. Neurosci. 32, 7466-7476 (2012).
38. Maples, T. & Rothenfluh, A. A simple way to measure ethanol sensitivity in flies. J. Vis. Exp. 48, e2541 (2011).
39. Tissot, M. & Stocker, R. F. Metamorphosis in drosophila and other insects: the fate of neurons throughout the stages. Prog. Neurobiol. 62, 89-111 (2000).
40. Deal, R. B., Henikoff, J. G. & Henikoff, S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328, 1161-1164 (2010).
41. Zhang, M. M., Tsou, L. K., Charron, G., Raghavan, A. S. & Hang, H. C. Tandem fluorescence imaging of dynamic S-acylation and protein turnover. Proc. Natl Acad. Sci. USA 107, 8627-8632 (2010).
42. Hodas, J. J. et al. Dopaminergic modulation of the hippocampal neuropil proteome identified by bioorthogonal noncanonical amino acid tagging (BONCAT). Proteomics 12, 2464-2476 (2012).
43. Eichelbaum, K. & Krijgsveld, J. Rapid temporal dynamics of transcription, protein synthesis and secretion during macrophage activation. Mol. Cell. Proteomics 13, 792-810 (2014).
44. Eichelbaum, K., Winter, M., Berriel Diaz, M., Herzig, S. & Krijgsveld, J. Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat. Biotechnol. 30, 984-990 (2012).
45. Howden, A. J. et al. QuaNCAT: quantitating proteome dynamics in primary cells. Nat. Methods 10, 343-346 (2013).
46. Somasekharan, S. P. et al. Identification and quantification of newly synthesized proteins translationally regulated by YB-1 using a novel Click-SILAC approach. J. Proteomics 77, e1-10 (2012).
47. Brown, J. L. The N-terminal region of soluble proteins from procaryotes and eucaryotes. Biochim. Biophys. Acta 221, 480-488 (1970).
48. Matheson, A. T., Yaguchi, M. & Visentin, L. P. The conservation of amino acids in the n-terminal position of ribosomal and cytosol proteins from Escherichia coli, Bacillus stearothermophilus, and Halobacterium cutirubrum. Can. J. Biochem. 53, 1323-1327 (1975).
49. Waller, J. P. The Nh2-terminal residues of the proteins from cell-free extracts of E. Coli. J. Mol. Biol. 7, 483-496 (1963).
50. Yuet, K. P. et al. Cell-specific proteomic analysis in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 112, 2705-2710 (2015).
51. Link, A. J., Vink, M. K. & Tirrell, D. A. Preparation of the functionalizable methionine surrogate azidohomoalanine via copper-catalyzed diazo transfer. Nat. Protoc. 2, 1879-1883 (2007).
52. Lin, D. M. & Goodman, C. S. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13, 507-523 (1994).
53. Halter, D. A. et al. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332 (1995).
54. Mahr, A. & Aberle, H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene. Expr. Patterns. 6, 299-309 (2006).
55. Thomas, U. et al. Synaptic targeting and localization of discs-large is a stepwise process controlled by different domains of the protein. Curr. Biol. 10, 1108-1117 (2000).
56. Hinz, U., Giebel, B. & Campos-Ortega, J. A. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77-87 (1994).
57. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
58. Blum, H., Beier, H. & Gross, H. J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93-99 (1987).