Worms from Venus and Mars: Proteomics profiling of sexual differences in Caenorhabditis elegans using in vivo15N isotope labeling

Journal of Proteome Research

Volumn 9, Issue 1, 2010, Pages 341-351

  Tops, Bastiaan B J ^a   Gauci, Sharon ^a   Heck, Albert J R ^a   Krijgsveld, Jeroen ^a  

^a NONE

Author keywords

Fem 1; Fem 3; Female 15N; Isotope; Male; Proteomics; Sex

Indexed keywords

MESSENGER RNA; NITROGEN 15;

ARTICLE; CAENORHABDITIS ELEGANS; ESCHERICHIA COLI; HERMAPHRODITISM; ISOTOPE LABELING; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEOMICS; SEX DIFFERENCE; SPERMATOGENESIS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; ISOTOPE LABELING; LINEAR MODELS; MALE; NITROGEN ISOTOPES; OOGENESIS; PHOSPHOPROTEIN PHOSPHATASES; PROTEOMICS; SEX FACTORS; SPERMATOGENESIS;

ANIMALIA; CAENORHABDITIS ELEGANS; ESCHERICHIA COLI;

EID: 73649137885     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr900678j     Document Type: Article

References (56)

1. Ellis, R. E. Sex determination in the Caenorhabditis elegans germ line. Curr. Top. Dev. Biol. 2008, 83, 41-64.
2. Kimble, J.; Edgar, L.; Hirsh, D. Specification of male development in Caenorhabditis elegans: the fem genes. Dev. Biol. 1984, 105 (1), 234-9.
3. Hodgkin, J. A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev. 1987, 1 (7), 731-45.
4. Doniach, T.; Hodgkin, J. A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev. Biol. 1984, 106 (1), 223-35.
5. Hodgkin, J. Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 1986, 114 (1), 15-52.
6. Ahringer, J.; Kimble, J. Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3′ untranslated region. Nature 1991, 349 (6307), 346-8.
7. Ahringer, J.; Rosenquist, T. A.; Lawson, D. N.; Kimble, J. The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J. 1992, 11 (6), 2303-10.
8. Rosenquist, T. A.; Kimble, J. Molecular cloning and transcript analysis of fem-3, a sex-determination gene in Caenorhabditis elegans. Genes Dev. 1988, 2 (5), 606-16.
9. Barton, M. K.; Schedl, T. B.; Kimble, J. Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 1987, 115 (1), 107-19.
10. Reinke, V.; Gil, I. S.; Ward, S.; Kazmer, K. Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 2004, 131 (2), 311-23.
11. Tabuse, Y.; Nabetani, T.; Tsugita, A. Proteomic analysis of protein expression profiles during Caenorhabditis elegans development using two-dimensional difference gel electrophoresis. Proteomics 2005, 5 (11), 2876-91.
12. Dong, M. Q.; Venable, J. D.; Au, N.; Xu, T.; Park, S. K.; Cociorva, D.; Johnson, J. R.; Dillin, A.; Yates, J. R., III. Quantitative mass spectrometry identifies insulin signaling targets in C. elegans. Science 2007, 317 (5838), 660-3.
13. Krijgsveld, J.; Ketting, R. F.; Mahmoudi, T.; Johansen, J.; Artal-Sanz, M.; Verrijzer, C. P.; Plasterk, R. H.; Heck, A. J. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 2003, 21 (8), 927-31.
14. Mortensen, P.; Gouw, J. W.; Olsen, J. V.; Ong, S. E.; Rigbolt, K. T.; Bunkenborg, J.; Cox, J.; Foster, L. J.; Heck, A. J.; Blagoev, B.; Andersen, J. S.; Mann, M. MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. J. Proteome Res. [Online early access]. DOI: 10.1021/pr900721e. Published online: Nov 18, 2009.
15. Scherl, A.; Shaffer, S. A.; Taylor, G. K.; Kulasekara, H. D.; Miller, S. I.; Goodlett, D. R. Genome-specific gas-phase fractionation strategy for improved shotgun proteomic profiling of proteotypic peptides. Anal. Chem. 2008, 80 (4), 1182-91.
16. Beausoleil, S. A.; Villen, J.; Gerber, S. A.; Rush, J.; Gygi, S. P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 2006, 24 (10), 1285-92.
17. van Breukelen, B.; van den Toorn, H. W.; Drugan, M. M.; Heck, A. J. StatQuant: a post-quantification analysis toolbox for improving quantitative mass spectrometry. Bioinformatics 2009, 25 (11), 1472-3.
18. Grote, P.; Conradt, B. The PLZF-like protein TRA-4 cooperates with the Gli-like transcription factor TRA-1 to promote female development in C. elegans. Dev Cell 2006, 11 (4), 561-73.
19. Audhya, A.; Hyndman, F.; McLeod, I. X.; Maddox, A. S.; Yates, J. R., III; Desai, A.; Oegema, K. A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J. Cell Biol. 2005, 171 (2), 267-79.
20. Boag, P. R.; Nakamura, A.; Blackwell, T. K. A conserved RNAprotein complex component involved in physiological germline apoptosis regulation in C. elegans. Development 2005, 132 (22), 4975-86.
21. Decker, C. J.; Parker, R. CAR-1 and trailer hitch: driving mRNP granule function at the ER? J. Cell Biol. 2006, 173 (2), 159-63.
22. Hird, S. N.; Paulsen, J. E.; Strome, S. Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation. Development 1996, 122 (4), 1303-12.
23. Kawasaki, I.; Shim, Y. H.; Kirchner, J.; Kaminker, J.; Wood, W. B.; Strome, S. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 1998, 94 (5), 635-45.
24. Kuznicki, K. A.; Smith, P. A.; Leung-Chiu, W. M.; Estevez, A. O.; Scott, H. C.; Bennett, K. L. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 2000, 127 (13), 2907-16.
25. Kelleher, J. F.; Mandell, M. A.; Moulder, G.; Hill, K. L.; L'Hernault, S. W.; Barstead, R.; Titus, M. A. Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Curr. Biol. 2000, 10 (23), 1489-96.
26. L'Hernault, S. W.; Shakes, D. C.; Ward, S. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 1988, 120 (2), 435-52.
27. Mihalik, S. J.; Morrell, J. C.; Kim, D.; Sacksteder, K. A.; Watkins, P. A.; Gould, S. J. Identification of PAHX, a Refsum disease gene. Nat. Genet. 1997, 17 (2), 185-9.
28. Kraemer, B.; Crittenden, S.; Gallegos, M.; Moulder, G.; Barstead, R.; Kimble, J.; Wickens, M. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr. Biol. 1999, 9 (18), 1009-18.
29. Hansen, D.; Wilson-Berry, L.; Dang, T.; Schedl, T. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 2004, 131 (1), 93-104.
30. Kubota, H.; Hynes, G.; Willison, K. The chaperonin containing t-complex polypeptide 1 (TCP-1). Multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol. Eur. J. Biochem. 1995, 230 (1), 3-16.
31. Thulasiraman, V.; Yang, C. F.; Frydman, J. In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 1999, 18 (1), 85-95.
32. Kimble, J.; Sharrock, W. J. Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev. Biol. 1983, 96 (1), 189-96.
33. Hall, D. H.; Winfrey, V. P.; Blaeuer, G.; Hoffman, L. H.; Furuta, T.; Rose, K. L.; Hobert, O.; Greenstein, D. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 1999, 212 (1), 101-23.
34. Grant, B.; Hirsh, D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 1999, 10 (12), 4311-26.
35. Moore, L. L.; Morrison, M.; Roth, M. B. HCP-1, a protein involved in chromosome segregation, is localized to the centromere of mitotic chromosomes in Caenorhabditis elegans. J. Cell Biol. 1999, 147 (3), 471-80.
36. Cheeseman, I. M.; MacLeod, I.; Yates, J. R., III; Oegema, K.; Desai, A. The CENP-F-like proteins HCP-1 and HCP-2 target CLASP to kinetochores to mediate chromosome segregation. Curr. Biol. 2005, 15 (8), 771-7.
37. Tarailo, M.; Tarailo, S.; Rose, A. M. Synthetic lethal interactions identify phenotypic "interologs" of the spindle assembly check-point components. Genetics 2007, 177 (4), 2525-30.
38. Hajeri, V. A.; Stewart, A. M.; Moore, L. L.; Padilla, P. A. Genetic analysis of the spindle checkpoint genes san-1, mdf-2, bub-3 and the CENP-F homologues hcp-1 and hcp-2 in Caenorhabditis elegans. Cell Div. 2008, 3, 6.
39. Su, L. K.; Qi, Y. Characterization of human MAPRE genes and their proteins. Genomics 2001, 71 (2), 142-9.
40. Kozlowski, C.; Srayko, M.; Nedelec, F. Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 2007, 129 (3), 499-510.
41. Blumenthal, T.; Stewart, K. RNA Processing and Gene Structure; Cold Spring Harbor Laboratory Press: New York, 1997.
42. Hastings, K. E. SL trans-splicing: easy come or easy go. Trends Genet. 2005, 21 (4), 240-7.
43. Thomas, J. D.; Conrad, R. C.; Blumenthal, T.; The, C. elegans trans-spliced leader RNA is bound to Sm and has a trimethylguanosine cap. Cell 1988, 54 (4), 533-9.
44. Liou, R. F.; Blumenthal, T. trans-spliced Caenorhabditis elegans mRNAs retain trimethylguanosine caps. Mol. Cell. Biol. 1990, 10 (4), 1764-8.
45. Jankowska-Anyszka, M.; Lamphear, B. J.; Aamodt, E. J.; Harrington, T.; Darzynkiewicz, E.; Stolarski, R.; Rhoads, R. E. Multiple isoforms of eukaryotic protein synthesis initiation factor 4E in Caenorhabditis elegans can distinguish between mono- and trimethylated mRNA cap structures. J. Biol. Chem. 1998, 273 (17), 10538-42.
46. Keiper, B. D.; Lamphear, B. J.; Deshpande, A. M.; Jankowska-Anyszka, M.; Aamodt, E. J.; Blumenthal, T.; Rhoads, R. E. Functional characterization of five eIF4E isoforms in Caenorhabditis elegans. J. Biol. Chem. 2000, 275 (14), 10590-6.
47. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4 (1), 44-57.
48. Giraldez, A. J.; Mishima, Y.; Rihel, J.; Grocock, R. J.; Van Dongen, S.; Inoue, K.; Enright, A. J.; Schier, A. F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312 (5770), 75-9.
49. Taylor, R. C.; Brumatti, G.; Ito, S.; Hengartner, M. O.; Derry, W. B.; Martin, S. J. Establishing a blueprint for CED-3-dependent killing through identification of multiple substrates for this protease. J. Biol. Chem. 2007, 282 (20), 15011-21.
50. Taguchi, A.; Yanagisawa, K.; Tanaka, M.; Cao, K.; Matsuyama, Y.; Goto, H.; Takahashi, T. Identification of hypoxia-inducible factor-1 alpha as a novel target for miR-17-92 microRNA cluster. Cancer Res. 2008, 68 (14), 5540-5.
51. Baek, D.; Villen, J.; Shin, C.; Camargo, F. D.; Gygi, S. P.; Bartel, D. P. The impact of microRNAs on protein output. Nature 2008, 455 (7209), 64-71.
52. Selbach, M.; Schwanhausser, B.; Thierfelder, N.; Fang, Z.; Khanin, R.; Rajewsky, N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455 (7209), 58-63.
53. Yang, Y.; Chaerkady, R.; Beer, M. A.; Mendell, J. T.; Pandey, A. Identification of miR-21 targets in breast cancer cells using a quantitative proteomic approach. Proteomics 2009, 9 (5), 1374-84.
54. Vinther, J.; Hedegaard, M. M.; Gardner, P. P.; Andersen, J. S.; Arctander, P. Identification of miRNA targets with stable isotope labeling by amino acids in cell culture. Nucleic Acids Res. 2006, 34 (No. 16), e107.
55. Gouw, J. W.; Pinkse, M. W.; Vos, H. R.; Moshkin, Y.; Verrijzer, C. P.; Heck, A. J.; Krijgsveld, J. In vivo stable isotope labeling of fruit flies reveals post-transcriptional regulation in the maternal-to-zygotic transition. Mol. Cell. Proteomics 2009, 8, 1566-78.
56. 15N-labeled proteins in comparative proteomics. Anal. Chem. 2008, 80 (20), 7796-803.