Single-cell mass spectrometry reveals small molecules that affect cell fates in the 16-cell embryo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 21, 2015, Pages 6545-6550

  Onjiko, Rosemary M ^a   Moody, Sally A ^b   Nemes, Peter ^a,b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Embryo development; Mass spectrometry; Metabolomics; Single cell; Xenopus

Indexed keywords

ANIMAL CELL; ARTICLE; CAPILLARY ELECTROPHORESIS; CELL FATE; CELL MOTION; CELL SIZE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EMBRYO; EMBRYO CELL; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL CAPILLARY ELECTROPHORESIS ELECTROSPRAY IONIZATION MASS SPECTROMETRY; XENOPUS LAEVIS; ANIMAL; ANIMAL EMBRYO; BLASTOMA; CYTOLOGY; EMBRYOLOGY; FEMALE; MALE; METABOLISM; METABOLOME; PROCEDURES; SINGLE CELL ANALYSIS;

XENOPUS LAEVIS;

ANIMALS; BLASTOMERES; CELL SIZE; ELECTROPHORESIS, CAPILLARY; EMBRYO, NONMAMMALIAN; FEMALE; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; SINGLE-CELL ANALYSIS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; XENOPUS LAEVIS;

EID: 84930216251     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1423682112     Document Type: Article

References (42)

1. Macaulay IC, Voet T (2014) Single cell genomics: Advances and future perspectives. PLoS Genet 10(1):e1004126.
2. Shapiro E, Biezuner T, Linnarsson S (2013) Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat Rev Genet 14(9):618-630.
3. Grant PA, Yan B, Johnson MA, Johnson DLE, Moody SA (2014) Novel animal pole-enriched maternal mRNAs are preferentially expressed in neural ectoderm. Dev Dyn 243(3):478-496.
4. Xanthos JB, Kofron M, Wylie C, Heasman J (2001) Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128(2):167-180.
5. White JA, Heasman J (2008) Maternal control of pattern formation in Xenopus laevis. J Exp Zoolog B Mol Dev Evol 310(1):73-84.
6. Hainski AM, Moody SA (1992) Xenopus maternal RNAs from a dorsal animal blastomere induce a secondary axis in host embryos. Development 116(2):347-355.
7. Yan B, Moody SA (2007) The competence of Xenopus blastomeres to produce neural and retinal progeny is repressed by two endo-mesoderm promoting pathways. Dev Biol 305(1):103-119.
8. Collart C, et al. (2014) High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141(9):1927-1939.
9. Flachsova M, Sindelka R, Kubista M (2013) Single blastomere expression profiling of Xenopus laevis embryos of 8 to 32-cells reveals developmental asymmetry. Scientific Reports 3:2278.
10. Sindelka R, Sidova M, Svec D, Kubista M (2010) Spatial expression profiles in the Xenopus laevis oocytes measured with qPCR tomography. Methods 51(1):87-91.
11. Sun LL, et al. (2014) Quantitative proteomics of Xenopus laevis embryos: Expression kinetics of nearly 4000 proteins during early development. Scientific Reports 4:4365.
12. Vastag L, et al. (2011) Remodeling of the metabolome during early frog development. PLoS ONE 6(2):e16881.
13. Shrestha B, et al. (2014) Subcellular metabolite and lipid analysis of Xenopus laevis eggs by LAESI mass spectrometry. PLoS ONE 9(12):e115173.
14. Anderson JL, Carten JD, Farber SA (2011) Zebrafish lipid metabolism: From mediating early patterning to the metabolism of dietary fat and cholesterol. Zebrafish: Cellular and Developmental Biology, Methods in Cell Biology, eds Detrich HW, Westerfield M, Zon LI (Elsevier, San Diego), Vol 101, 3rd Ed, pp 111-141.
15. Baskin JM, Dehnert KW, Laughlin ST, Amacher SL, Bertozzi CR (2010) Visualizing enveloping layer glycans during zebrafish early embryogenesis. Proc Natl Acad Sci USA 107(23):10360-10365.
16. Moody SA (1987) Fates of the blastomeres of the 16-cell stage Xenopus embryo. Dev Biol 119(2):560-578.
17. Rubakhin SS, Romanova EV, Nemes P, Sweedler JV (2011) Profiling metabolites and peptides in single cells. Nat Methods 8(4, Suppl):S20-S29.
18. Svatoš A (2011) Single-cell metabolomics comes of age: New developments in mass spectrometry profiling and imaging. Anal Chem 83(13):5037-5044.
19. Ye H, Greer T, Li L (2012) Probing neuropeptide signaling at the organ and cellular domains via imaging mass spectrometry. J Proteomics 75(16):5014-5026.
20. Zenobi R (2013) Single-cell metabolomics: Analytical and biological perspectives. Science 342(6163):1243259.
21. Rubakhin SS, Lanni EJ, Sweedler JV (2013) Progress toward single cell metabolomics. Curr Opin Biotechnol 24(1):95-104.
22. Ibáñez AJ, et al. (2013) Mass spectrometry-based metabolomics of single yeast cells. Proc Natl Acad Sci USA 110(22):8790-8794.
23. Stolee JA, Shrestha B, Mengistu G, Vertes A (2012) Observation of subcellular metabolite gradients in single cells by laser ablation electrospray ionization mass spectrometry. Angew Chem Int Ed Engl 51(41):10386-10389.
24. Date S, Mizuno H, Tsuyama N, Harada T, Masujima T (2012) Direct drug metabolism monitoring in a live single hepatic cell by video mass spectrometry. Anal Sci 28(3):201-203.
25. Pan N, et al. (2014) The single-probe: A miniaturized multifunctional device for single cell mass spectrometry analysis. Anal Chem 86(19):9376-9380.
26. Hofstadler SA, Severs JC, Smith RD, Swanek FD, Ewing AG (1996) Analysis of single cells with capillary electrophoresis electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Rapid Commun Mass Spectrom 10(8):919-922.
27. Valaskovic GA, Kelleher NL, McLafferty FW (1996) Attomole protein characterization by capillary electrophoresis-mass spectrometry. Science 273(5279):1199-1202.
28. Mellors JS, Jorabchi K, Smith LM, Ramsey JM (2010) Integrated microfluidic device for automated single cell analysis using electrophoretic separation and electrospray ionization mass spectrometry. Anal Chem 82(3):967-973.
29. Nemes P, Rubakhin SS, Aerts JT, Sweedler JV (2013) Qualitative and quantitative metabolomic investigation of single neurons by capillary electrophoresis electrospray ionization mass spectrometry. Nat Protoc 8(4):783-799.
30. Kanehisa M, et al. (2014) Data, information, knowledge and principle: Back to metabolism in KEGG. Nucleic Acids Res 42(Database issue, D1):D199-D205.
31. Fukumoto T, Kema IP, Levin M (2005) Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr Biol 15(9):794-803.
32. Adams DS, et al. (2006) Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133(9):1657-1671.
33. Harland R, Gerhart J (1997) Formation and function of Spemann's organizer. Annu Rev Cell Dev Biol 13:611-667.
34. Klein SL, King ML (1988) Correlations between cell fate and the distribution of proteins that are synthesized before the midblastula transition in Xenopus. Rouxs Arch Dev Biol 197(5):275-281.
35. Dale L, Slack JMW (1987) Fate map for the 32-cell stage of Xenopus laevis. Development 99(4):527-551.
36. Moody SA, Kline MJ (1990) Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. Anat Embryol (Berl) 182(4):347-362.
37. Moody SA (1987) Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev Biol 122(2):300-319.
38. Kalhan SC, Hanson RW (2012) Resurgence of serine: An often neglected but indispensable amino Acid. J Biol Chem 287(24):19786-19791.
39. Wang J, et al. (2009) Dependence of mouse embryonic stem cells on threonine catabolism. Science 325(5939):435-439.
40. Luu N, et al. (2013) Differential regulation of two histidine ammonia-lyase genes during Xenopus development implicates distinct functions during thyroid hormone-induced formation of adult stem cells. Cell Biosci 3(1):43.
41. Laihia JK, et al. (1998) Urocanic acid binds to GABA but not to histamine (H1, H2, or H3) receptors. J Invest Dermatol 111(4):705-706.
42. Aerts JT, et al. (2014) Patch clamp electrophysiology and capillary electrophoresis-mass spectrometry metabolomics for single cell characterization. Anal Chem 86(6):3203-3208.