Label-free quantification of proteins in single embryonic cells with neural fate in the cleavage-stage frog (Xenopus laevis) embryo using capillary electrophoresis electrospray ionization high-resolution mass spectrometry (CE-ESI-HRMS)

Molecular and Cellular Proteomics

Volumn 15, Issue 8, 2016, Pages 2756-2768

  Lombard Banek, Camille ^a   Reddy, Sushma ^a,b   Moody, Sally A ^a   Nemes, Peter ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b THOMAS JEFFERSON HIGH SCHOOL FOR SCIENCE AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN CONTAINING TCP1; CREATINE KINASE BRAIN; LIPOVITELLIN; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE 1; NUCLEOSIDE DIPHOSPHATE KINASE; NUCLEOSIDE DIPHOSPHATE KINASE 2; UNCLASSIFIED DRUG; VITELLOGENIN; XENOPUS PROTEIN; YOLK PROTEIN;

ANIMAL CELL; ARTICLE; BLASTOMA; CAPILLARY ELECTROPHORESIS; CELL FATE; CELL HETEROGENEITY; CORRELATION ANALYSIS; CYTOKINESIS; DERIVATIZATION; ELECTROSPRAY MASS SPECTROMETRY; EMBRYO; EMBRYO CELL; LIMIT OF DETECTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; SIGNAL NOISE RATIO; STABLE EXPRESSION; XENOPUS LAEVIS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; FEMALE; MALE; METABOLISM; PROCEDURES; PROTEIN PROTEIN INTERACTION; SINGLE CELL ANALYSIS; TANDEM MASS SPECTROMETRY;

ANIMALS; BLASTOMERES; CELL DIFFERENTIATION; ELECTROPHORESIS, CAPILLARY; FEMALE; MALE; PROTEIN INTERACTION MAPS; PROTEOMICS; SINGLE-CELL ANALYSIS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84982821534     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.057760     Document Type: Article

References (70)

1. Altschuler, S. J., and Wu, L. F. (2010) Cellular heterogeneity: Do differences make a difference? Cell 141, 559-563
2. Singh, D. K., Ku, C. J., Wichaidit, C., Steininger, R. J., Wu, L. F., and Altschuler, S. J. (2010) Patterns of basal signaling heterogeneity can distinguish cellular populations with different drug sensitivities. Mol. Syst. Biol. 6, 1-10
3. Picotti, P., Clement-Ziza, M., Lam, H., Campbell, D. S., Schmidt, A., Deutsch, E. W., Rost, H., Sun, Z., Rinner, O., Reiter, L., Shen, Q., Michaelson, J. J., Frei, A., Alberti, S., Kusebauch, U., Wollscheid, B., Moritz, R. L., Beyer, A., and Aebersold, R. (2013) A complete massspectrometric map of the yeast proteome applied to quantitative trait analysis. Nature 494, 266-270
4. Nagaraj, N., Kulak, N. A., Cox, J., Neuhauser, N., Mayr, K., Hoerning, O., Vorm, O., and Mann, M. (2012) System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top orbitrap. Mol. Cell. Proteomics 11, M111.013722
5. Hebert, A. S., Richards, A. L., Bailey, D. J., Ulbrich, A., Coughlin, E. E., Westphall, M. S., and Coon, J. J. (2014) The one hour yeast proteome. Mol. Cell. Proteomics 13, 339-347
6. McAlister, G. C., Nusinow, D. P., Jedrychowski, M. P., Wuhr, M., Huttlin, E. L., Erickson, B. K., Rad, R., Haas, W., and Gygi, S. P. (2014) Multi- Notch MS3 enables accurate, sensitive, and multiplexed detection of differential expression across cancer cell line proteomes. Anal. Chem. 86, 7150-7158
7. Wuhr, M., Guttler, T., Peshkin, L., McAlister, G. C., Sonnett, M., Ishihara, K., Groen, A. C., Presler, M., Erickson, B. K., Mitchison, T. J., Kirschner, M. W., and Gygi, S. P. (2015) The nuclear proteome of a vertebrate. Curr. Biol. 25, 2663-2671
8. Peshkin, L., Wuhr, M., Pearl, E., Haas, W., Freeman, R. M., Gerhart, J. C., Klein, A. M., Horb, M., Gygi, S. P., and Kirschner, M. W. (2015) On the relationship of protein and mRNA dynamics in vertebrate embryonic development. Dev. Cell 35, 383-394
9. Rubakhin, S. S., Romanova, E. V., Nemes, P., and Sweedler, J. V. (2011) Profiling metabolites and peptides in single cells. Nat. Methods 8, S20-S29
10. Svatos, A. (2011) Single-cell metabolomics comes of age: New developments in mass spectrometry profiling and imaging. Anal. Chem. 83, 5037-5044
11. Zenobi, R. (2013) Single-cell metabolomics: Analytical and biological perspectives. Science 342, 1201-1212
12. Rubakhin, S. S., Lanni, E. J., and Sweedler, J. V. (2013) Progress toward single cell metabolomics. Curr. Opin. Biotechnol. 24, 95-104
13. Lanni, E. J., Rubakhin, S. S., and Sweedler, J. V. (2012) Mass spectrometry imaging and profiling of single cells. J. Proteomics 75, 5036-5051
14. Sun, L. L., Zhu, G. J., Yan, X. J., Zhang, Z. B., Wojcik, R., Champion, M. M., and Dovichi, N. J. (2016) Capillary zone electrophoresis for bottom-up analysis of complex proteomes. Proteomics 16, 188-196
15. Ye, H., Greer, T., and Li, L. J. (2012) Probing neuropeptide signaling at the organ and cellular domains via imaging mass spectrometry. J. Proteomics 75, 5014-5026
16. Ong, T. H., Kissick, D. J., Jansson, E. T., Comi, T. J., Romanova, E. V., Rubakhin, S. S., and Sweedler, J. V. (2015) Classification of large cellular populations and discovery of rare cells using single cell matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Chem. 87, 7036-7042
17. Buchberger, A., Yu, Q., and Li, L. J. (2015) Advances in mass spectrometric tools for probing neuropeptides. In: Cooks, R. G., and Pemberton, J. E., eds. Annual Review of Analytical Chemistry, Vol 8, pp. 485-509, Annual Reviews, Palo Alto
18. Virant-Klun, I., Leicht, S., Hughes, C., and Krijgsveld, J. (2016) Identification of maturation-specific proteins by single-cell proteomics of human oocytes. Mol. Cell. Proteomics, in print
19. Wuhr, M., Freeman, R. M., Jr., Presler, M., Horb, M. E., Peshkin, L., Gygi, S. P., and Kirschner, M. W. (2014) Deep proteomics of the Xenopus laevis egg using an mRNA-derived reference database. Curr. Biol. 24, 1467-1475
20. Bendall, S. C., Simonds, E. F., Qiu, P., Amir, E. A. D., Krutzik, P. O., Finck, R., Bruggner, R. V., Melamed, R., Trejo, A., Ornatsky, O. I., Balderas, R. S., Plevritis, S. K., Sachs, K., Pe'er, D., Tanner, S. D., and Nolan, G. P. (2011) Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332, 687-696
21. Giesen, C., Wang, H. A. O., Schapiro, D., Zivanovic, N., Jacobs, A., Hattendorf, B., Schuffler, P. J., Grolimund, D., Buhmann, J. M., Brandt, S., Varga, Z., Wild, P. J., Gunther, D., and Bodenmiller, B. (2014) Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat. Methods 11, 417-422
22. Hofstadler, S. A., Swanek, F. D., Gale, D. C., Ewing, A. G., and Smith, R. D. (1995) Capillary electrophoresis electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry for direct analysis of cellular proteins. Anal. Chem. 67, 1477-1480
23. Valaskovic, G. A., Kelleher, N. L., and McLafferty, F. W. (1996) Attomole protein characterization by capillary electrophoresis mass spectrometry. Science 273, 1199-1202
24. Mellors, J. S., Jorabchi, K., Smith, L. M., and Ramsey, J. M. (2010) Integrated microfluidic device for automated single-cell analysis using electrophoretic separation and electrospray ionization mass spectrometry. Anal. Chem. 82, 967-973
25. Nemes, P., Knolhoff, A. M., Rubakhin, S. S., and Sweedler, J. V. (2011) Metabolic differentiation of neuronal phenotypes by single-cell capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 83, 6810-6817
26. Nemes, P., Rubakhin, S. S., Aerts, J. T., and Sweedler, J. V. (2013) Qual itative and quantitative metabolomic investigation of single neurons by capillary electrophoresis electrospray ionization mass spectrometry. Nat. Protoc. 8, 783-799
27. Onjiko, R. M., Moody, S. A., and Nemes, P. (2015) Single-cell mass spectrometry reveals small molecules that affect cell fates in the 16-cell embryo. Proc. Natl. Acad. Sci. U.S.A. 112, 6545-6550
28. Hofstadler, S. A., Severs, J. C., Smith, R. D., Swanek, F. D., and Ewing, A. G. (1996) Analysis of single cells with capillary electrophoresis electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Rapid Commun. Mass Spectrom. 10, 919-922
29. Wang, Y., Fonslow, B. R., Wong, C. C. L., Nakorchevsky, A., and Yates, J. R. (2012) Improving the comprehensiveness and sensitivity of sheathless capillary electrophoresis tandem mass spectrometry for proteomic analysis. Anal. Chem. 84, 8505-8513
30. Sun, L. L., Zhu, G. J., and Dovichi, N. J. (2013) Integrated capillary zone electrophoresis electrospray ionization tandem mass spectrometry system with an immobilized trypsin microreactor for online digestion and analysis of picogram amounts of RAW 264.7 cell lysate. Anal. Chem. 85, 4187-4194
31. Moini, M. (2007) Simplifying CE-MS operation. 2. Interfacing low-flow separation techniques to mass spectrometry using a porous tip. Anal. Chem. 79, 4241-4246
32. Sun, L. L., Zhu, G. J., Zhang, Z. B., Mou, S., and Dovichi, N. J. (2015) Third-generation electrokinetically pumped sheath-flow nanospray interface with improved stability and sensitivity for automated capillary zone electrophoresis mass spectrometry analysis of complex proteome digests. J. Proteome Res. 14, 2312-2321
33. Bonvin, G., Schappler, J., and Rudaz, S. (2012) Capillary electrophoresiselectrospray ionization-mass spectrometry interfaces: Fundamental concepts and technical developments. J. Chromatogr., A 1267, 17-31
34. Lindenburg, P. W., Haselberg, R., Rozing, G., and Ramautar, R. (2015) Developments in interfacing designs for CE-MS: Towards enabling tools for proteomics and metabolomics. Chromatographia 78, 367-377
35. Sun, L. L., Hebert, A. S., Yan, X. J., Zhao, Y. M., Westphall, M. S., Rush, M. J. P., Zhu, G. J., Champion, M. M., Coon, J. J., and Dovichi, N. J. (2014) Over 10000 peptide identifications from the HeLa proteome by using single-shot capillary zone electrophoresis combined with tandem mass spectrometry. Angew. Chem. Int. Ed. 53, 13931-13933
36. Lombard-Banek, C., Moody, S. A., and Nemes, P. (2016) Single-cell mass spectrometry for discovery proteomics: Quantifying translational cell heterogeneity in the 16-cell frog (Xenopus) embryo. Angew. Chem. Int. Ed. 55, 2454-2458
37. Ludwig, K. R., Sun, L. L., Zhu, G. J., Dovichi, N. J., and Hummon, A. B. (2015) Over 2300 phosphorylated peptide identifications with single-shot capillary zone electrophoresis tandem mass spectrometry in a 100 min separation. Anal. Chem. 87, 9532-9537
38. Sun, L. L., Zhu, G. J., Zhao, Y. M., Yan, X. J., Mou, S., and Dovichi, N. J. (2013) Ultrasensitive and fast bottom-up analysis of femtogram amounts of complex proteome digests. Angew. Chem. Int. Ed. 52, 13661-13664
39. Onjiko, R. M., Morris, S. E., Moody, S. A., and Nemes, P. (2016) Single-cell mass spectrometry with multi-solvent extraction identifies metabolic differences between left and right blastomeres in the 8-cell frog (Xenopus) embryo. Analyst 141, 3648-3656
40. Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., and Mann, M. (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13, 2513-2526
41. Moody, S. A. (1987) Fates of the blastomeres of the 16-cell stage Xenopus embryo. Dev. Biol. 119, 560-578
42. Grant, P. A., Herold, M. B., and Moody, S. A. (2013) Blastomere explants to test for cell fate commitment during embryonic development. J. Visualized Exp. 71, 4458
43. Zhang, Y. Y., Fonslow, B. R., Shan, B., Baek, M. C., and Yates, J. R. (2013) Protein analysis by shotgun/bottom-up proteomics. Chem. Rev. 113, 2343-2394
44. Nemes, P., Marginean, I., and Vertes, A. (2007) Spraying mode effect on droplet formation and ion chemistry in electrosprays. Anal. Chem. 79, 3105-3116
45. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The proteomics identifications (PRIDE) database and associated tools: Status in 2013. Nucleic Acids Res. 41, D1063-D1069
46. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
47. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
48. Bateman, A., Martin, M. J., O'Donovan, C., Magrane, M., Apweiler, R., Alpi, E., Antunes, R., Ar-Ganiska, J., Bely, B., Bingley, M., Bonilla, C., Britto, R., Bursteinas, B., Chavali, G., Cibrian-Uhalte, E., Da Silva, A., De Giorgi, M., Dogan, T., Fazzini, F., Gane, P., Cas-Tro, L. G., Garmiri, P., Hatton- Ellis, E., Hieta, R., Huntley, R., Legge, D., Liu, W. D., Luo, J., MacDougall, A., Mutowo, P., Nightin-Gale, A., Orchard, S., Pichler, K., Poggioli, D., Pundir, S., Pureza, L., Qi, G. Y., Rosanoff, S., Saidi, R., Sawford, T., Shypitsyna, A., Turner, E., Volynkin, V., Wardell, T., Watkins, X., Watkins, Cowley, A., Figueira, L., Li, W. Z., McWilliam, H., Lopez, R., Xenarios, I., Bougueleret, L., Bridge, A., Poux, S., Redaschi, N., Aimo, L., Argoud- Puy, G., Auchincloss, A., Axelsen, K., Bansal, P., Baratin, D., Blatter, M. C., Boeckmann, B., Bolleman, J., Boutet, E., Breuza, L., Casal-Casas, C., De Castro, E., Coudert, E., Cuche, B., Doche, M., Dornevil, D., Duvaud, S., Estreicher, A., Famiglietti, L., Feuermann, M., Gasteiger, E., Gehant, S., Gerritsen, V., Gos, A., Gruaz-Gumowski, N., Hinz, U., Hulo, C., Jungo, F., Keller, G., Lara, V., Lemercier, P., Lieberherr, D., Lombardot, T., Martin, X., Masson, P., Morgat, A., Neto, T., Nouspikel, N., Paesano, S., Pedruzzi, I., Pilbout, S., Pozzato, M., Pruess, M., Rivoire, C., Roechert, B., Schneider, M., Sigrist, C., Sonesson, K., Staehli, S., Stutz, A., Sundaram, S., Tognolli, M., Verbregue, L., Veuthey, A. L., Wu, C. H., Arighi, C. N., Arminski, L., Chen, C. M., Chen, Y. X., Garavelli, J. S., Huang, H. Z., Laiho, K. T., McGarvey, P., Natale, D. A., Suzek, B. E., Vinayaka, C. R., Wang, Q. H., Wang, Y. Q., Yeh, L. S., Yerramalla, M. S., Zhang, J., and UniProt, C. (2015) UniProt: A hub for protein information. Nucleic Acids Res. 43, D204-D212
49. James-Zorn, C., Ponferrada, V. G., Burns, K. A., Fortriede, J. D., Lotay, V. S., Liu, Y., Karpinka, J. B., Karimi, K., Zorn, A. M., and Vize, P. D. (2015) Xenbase: Core features, data acquisition, and data processing. Genesis 53, 486-497
50. Karpinka, J. B., Fortriede, J. D., Burns, K. A., James-Zorn, C., Ponferrada, V. G., Lee, J., Karimi, K., Zorn, A. M., and Vize, P. D. (2015) Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Res. 43, D756-D763
51. Beck, S., Michalski, A., Raether, O., Lubeck, M., Kaspar, S., Goedecke, N., Baessmann, C., Hornburg, D., Meier, F., Paron, I., Kulak, N. A., Cox, J., and Mann, M. (2015) The Impact II, a very high-resolution quadrupole time-of-flight instrument (QTOF) for deep shotgun proteomics. Mol. Cell. Proteomics 14, 2014-2029
52. Szklarczyk, D., Franceschini, A., Wyder, S., Forslund, K., Heller, D., Huerta- Cepas, J., Simonovic, M., Roth, A., Santos, A., Tsafou, K. P., Kuhn, M., Bork, P., Jensen, L. J., and von Mering, C. (2015) STRING v10: Proteinprotein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447-D452
53. Jorgensen, P., Steen, J. A., Steen, H., and Kirschner, M. W. (2009) The mechanism and pattern of yolk consumption provide insight into embryonic nutrition in Xenopus. Development 136, 1539-1548
54. Lomeli, S. H., Peng, I. X., Yin, S., Loo, R. R., and Loo, J. A. (2010) New reagents for increasing ESI multiple charging of proteins and protein complexes. J. Am. Soc. Mass Spectrom. 21, 127-131
55. Sterling, H. J., Prell, J. S., Cassou, C. A., and Williams, E. R. (2011) Protein conformation and supercharging with DMSO from aqueous solution. J. Am. Soc. Mass Spectrom. 22, 1178-1186
56. Flachsova, M., Sindelka, R., and Kubista, M. (2013) Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry. Sci. Rep. 3, 2278
57. Collart, C., Owens, N. D. L., Bhaw-Rosun, L., Cooper, B., De Domenico, E., Patrushev, I., Sesay, A. K., Smith, J. N., Smith, J. C., and Gilchrist, M. J. (2014) High-resolution analysis of gene activity during the Xenopus midblastula transition. Development 141, 1927-1939
58. Domenico, E. D., Owens, N. D. L., Grant, I. M., Gomes-Faria, R., and Gilchrist, M. J. (2015) Molecular asymmetry in the 8-cell stage Xenopus tropicalis embryo described by single blastomere transcript sequencing. Dev. Biol. 408, 252-268
59. Eisenberg, E., and Levanon, E. Y. (2003) Human housekeeping genes are compact. Trends Genet. 19, 362-365
60. Abe, H., Obinata, T., Minamide, L. S., and Bamburg, J. R. (1996) Xenopus laevis actin-depolymerizing factor cofilin: A phosphorylation-regulated protein essential for development. J. Cell Biol. 132, 871-885
61. Sun, L. L., Bertke, M. M., Champion, M. M., Zhu, G. J., Huber, P. W., and Dovichi, N. J. (2014) Quantitative proteomics of Xenopus laevis embryos: Expression kinetics of nearly 4000 proteins during early development. Sci. Rep. 4, 4365
62. Aerts, J. T., Louis, K. R., Crandall, S. R., Govindaiah, G., Cox, C. L., and Sweedler, J. V. (2014) Patch clamp electrophysiology and capillary electrophoresis mass spectrometry metabolomics for single cell characterization. Anal. Chem. 86, 3203-3208
63. Pan, N., Rao, W., Kothapalli, N. R., Liu, R., Burgett, A. W. G., and Yang, Z. (2014) The single-probe: A miniaturized multifunctional device for single cell mass spectrometry analysis. Anal. Chem. 86, 9376-9380
64. Zhang, Z., Sun, L., Zhu, G., Cox, O. F., Huber, P. W., and Dovichi, N. J. (2016) Nearly 1000 protein identifications from 50 ng of Xenopus laevis zygote homogenate using online sample preparation on a strong cation exchange monolith based microreactor coupled with capillary zone electrophoresis. Anal. Chem. 88, 877-882
65. Breadmore, M. C., Tubaon, R. M., Shallan, A. I., Phung, S. C., Keyon, A. S. A., Gstoettenmayr, D., Prapatpong, P., Alhusban, A. A., Ranjbar, L., See, H. H., Dawod, M., and Quirino, J. P. (2015) Recent advances in enhancing the sensitivity of electrophoresis and electrochromatography in capillaries and microchips (2012-2014). Electrophoresis 36, 36-61
66. Kitagawa, F., and Otsuka, K. (2014) Recent applications of on-line sample preconcentration techniques in capillary electrophoresis. J. Chromatogr. 1335, 43-60
67. Kler, P. A., Sydes, D., and Huhn, C. (2015) Column-coupling strategies for multidimensional electrophoretic separation techniques. Anal. Bioanal. Chem. 407, 119-138
68. Whitt, J. T., and Moini, M. (2003) Capillary electrophoresis to mass spectrometry interface using a porous junction. Anal. Chem. 75, 2188-2191
69. Han, X., Wang, Y., Aslanian, A., Bern, M., Lavallee-Adam, M., and Yates, J. R. (2014) Sheathless capillary electrophoresis tandem mass spectrometry for top-down characterization of Pyrococcus furiosus proteins on a proteome scale. Anal. Chem. 86, 11006-11012
70. Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., Trombetta, J. J., Weitz, D. A., Sanes, J. R., Shalek, A. K., Regev, A., and McCarroll, S. A. (2015) Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202-1214