In vivo stable isotope labeling of fruit flies reveals post-transcriptional regulation in the maternal-to-zygotic transition

Molecular and Cellular Proteomics

Volumn 8, Issue 7, 2009, Pages 1566-1578

  Gouw, Joost W ^a   Pinkse, Martijn W H ^a,c   Vos, Harmjan R ^a,d   Moshkin, Yuri ^b   Verrijzer, C Peter ^b   Heck, Albert J R ^a   Krijgsveld, Jeroen ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN L; ISOTOPE; MESSENGER RNA; POLYADENYLIC ACID; STABLE ISOTOPE;

ACCURACY; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; EMBRYO; GENOME; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEOMICS; TRANSCRIPTION REGULATION; ZYGOTE;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, LIQUID; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ISOTOPES; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OOCYTES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; STAINING AND LABELING; TANDEM MASS SPECTROMETRY; TRANSCRIPTIONAL ACTIVATION;

EID: 70350015395     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900114-MCP200     Document Type: Article

References (42)

1. Wieschaus, E., and Gehring, W. (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev. Biol. 50, 249-263
2. Zalokar, M. (1976) Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev. Biol. 49, 425-437
3. Anderson, K. V., and Lengyel, J. A. (1979) Rates of synthesis of major classes of RNA in Drosophila embryos. Dev. Biol. 70, 217-231
4. Newport, J., and Kirschner, M. (1982) A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30, 675-686 (Pubitemid 13204657)
5. Edgar, B. A., and Schubiger, G. (1986) Parameters controlling transcriptional activation during early Drosophila development Cell 44, 871-877
6. De Renzis, S., Elemento, O., Tavazoie, S., and Wieschaus, E. F. (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol. 5, e117 (Pubitemid 46790394)
7. Tadros, W., Goldman, A. L., Babak, T., Menzies, F., Vardy, L., Orr-Weaver, T., Hughes, T. R., Westwood, J. T., Smibert, C. A., and Lipshitz, H. D. (2007) SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev. Cell 12, 143-155 (Pubitemid 46002594)
8. Bashirullah, A., Halsell, S. R., Cooperstock, R. L., Kloc, M., Karaiskakis, A., Fisher, W. W., Fu, W., Hamilton, J. K., Etkin, L. D., and Lipshitz, H. D. (1999) Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 18, 2610-2620 (Pubitemid 29213290)
9. Kloc, M., and Etkin, L. D. (2005) RNA localization mechanisms in oocytes. J. Cell Sci. 118, 269-282
10. St Johnston, D. (2005) Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6, 363-375
11. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22
12. Parker, R., and Sheth, U. (2007) P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646 (Pubitemid 46341926)
13. Gong, L., Puri, M., Unlü, M., Young, M., Robertson, K., Viswanathan, S., Krishnaswamy, A., Dowd, S. R., and Minden, J. S. (2004) Drosophila ventral furrow morphogenesis: a proteomic analysis. Development 131, 643-656 (Pubitemid 38240006)
14. Brunner, E., Ahrens, C. H., Mohanty, S., Baetschmann, H., Loevenich, S., Potthast, F., Deutsch, E. W., Panse, C., de Lichtenberg, U., Rinner, O., Lee, H., Pedrioli, P. G., Malmstrom, J., Koehler, K., Schrimpf, S., Krijgsveld, J., Kregenow, F., Heck, A. J., Hafen, E., Schlapbach, R., and Aebersold, R. (2007) A high-quality catalog of the Drosophila melanogaster proteome. Nat. Biotechnol. 25, 576-583
15. Zhai, B., Villen, J., Beausoleil, S. A., Mintseris, J., and Gygi, S. P. (2008) Phosphoproteome analysis of Drosophila melanogaster embryos. J. Proteome Res. 7, 1675-1682
16. Vardy, L., and Orr-Weaver, T. L. (2007) Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 17, 547-554 (Pubitemid 350087663)
17. Krijgsveld, J., Ketting, R. F., Mahmoudi, T., Johansen, J., Artal-Sanz, M., Verrijzer, C. P., Plasterk, R. H., and Heck, A. J. (2003) Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 21, 927-931
18. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670
19. (n): technical design and applications to peptide and protein analysis. J. Sep. Sci. 25, 557-568
20. Zhang, B., Chambers, M. C., and Tabb, D. L. (2007) Proteomic parsimony through bipartite graph analysis improves accuracy and transparency. J. Proteome Res. 6, 3549-3557 (Pubitemid 47522746)
21. Kuyumcu-Martinez, N. M., Joachims, M., and Lloyd, R. E. (2002) Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J. Virol. 76, 2062-2074 (Pubitemid 34150674)
22. 15N-labeled proteins in comparative proteomics. Anal. Chem. 80, 7796-7803
23. Moshkin, Y. M., Mohrmann, L., van Ijcken, W. F., and Verrijzer, C. P. (2007) Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol. Cell. Biol. 27, 651-661
24. Schulze, W. X., and Mann, M. (2004) A novel proteomic screen for peptide-protein interactions. J. Biol. Chem. 279, 10756-10764
25. Lécuyer, E., Yoshida, H., Parthasarathy, N., Aim, C., Babak, T., Cerovina, T., Hughes, T. R., Tomancak, P., and Krause, H. M. (2007) Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131, 174-187 (Pubitemid 47498530)
26. Hosack, D. A., Dennis, G., Jr., Sherman, B. T., Lane, H. C., and Lempicki, R. A. (2003) Identifying biological themes within lists of genes with EASE. Genome Biol. 4, R70
27. Yamamoto, Y., Kurata, M., Watabe, S., Murakami, R., and Takahashi, S. Y. (2002) Novel cysteine proteinase inhibitors homologous to the prorogions of cysteine proteinases. Curr. Protein Pept. Sci. 3, 231-238
28. Mangus, D. A., Evans, M. C., and Jacobson, A. (2003) Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4, 223
29. Arthur, C. G., Weide, C. M., Vincent, W. S., 3rd, and Goldstein, E. S. (1979) mRNA sequence diversity during early embryogenesis in Drosophila melanogaster. Exp. Cell Res. 121, 87-94
30. Trumbly, R. J., and Jarry, B. (1983) Stage-specific protein synthesis during early embryogenesis in Drosophila melanogaster. EMBO J. 2, 1281-1290
31. Nakamura, A., Sato, K., and Hanyu-Nakamura, K. (2004) Drosophila cup is an elF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6, 69-78 (Pubitemid 38089206)
32. Dahanukar, A., Walker, J. A., and Wharton, R. P. (1999) Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol. Cell 4, 209-218 (Pubitemid 29456889)
33. Smibert, C. A., Lie, Y. S., Shillinglaw, W., Henzel, W. J., and Macdonald, P. M. (1999) Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 5, 1535-1547
34. Zaessinger, S., Busseau, I., and Simonelig, M. (2006) Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 133, 4573-4583 (Pubitemid 46017831)
35. Semotok, J. L., Cooperstock, R. L., Pinder, B. D., Vari, H. K., Lipshitz, H. D., and Smibert, C. A. (2005) Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr. Biol. 15, 284-294
36. Nakahara, K., Kim, K., Sciulli, C., Dowd, S. R., Minden, J. S., and Carthew, R. W. (2005) Targets of microRNA regulation in the Drosophila oocyte proteome. Proc. Natl. Acad. Sci. U.S.A. 102, 12023-12028
37. Barrett, A. J., Rawlings, N. D., and Woessner, J. F. (eds) (2003) Handbook of Proteolytic Enzymes, 2nd Ed., Academic Press, New York
38. Goulet, B., Baruch, A., Moon, N. S., Poirier, M., Sansregret, L. L., Erickson, A., Bogyo, M., and Nepveu, A. (2004) A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor. Mol. Cell 14, 207-219 (Pubitemid 38515648)
39. Duncan, E. M., Muratore-Schroeder, T. L., Cook, R. G., Garcia, B. A., Shabanowitz, J., Hunt, D. F., and Allis, C. D. (2008) Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 135, 284-294
40. Jacobson, A., and Favreau, M. (1983) Possible involvement of poly(A) in protein synthesis. Nucleic Acids Res. 11, 6353-6368
41. de Moor, C. H., Meijer, H., and Lissenden, S. (2005) Mechanisms of translational control by the 3′ UTR in development and differentiation. Semin. Cell Dev. Biol. 16, 49-58
42. Joachims, M., Van Breugel, P. C., and Lloyd, R. E. (1999) Cleavage of poly(A)-binding protein by enterovirus proteases concurrent with inhibition of translation in vitro. J. Virol. 73, 718-727 (Pubitemid 28565417)