Side scatter intensity is highly heterogeneous in undifferentiated pluripotent stem cells and predicts clonogenic self-renewal

Stem Cells and Development

Volumn 22, Issue 12, 2013, Pages 1851-1860

  Ramirez, Jean Marie ^a,b   Bai, Qiang ^a,b,c   Péquignot, Marie ^b,d   Becker, Fabienne ^a   Kassambara, Alboukadel ^a,b   Bouin, Alexandra ^a,b   Kalatzis, Vasiliki ^b,d   Dijon Grinand, Marilyne ^a,b   De Vos, John ^a,b,c,e  

^a HÔPITAL SAINT ELOI   (France)

^b INSERM   (France)

^c UNIV MONTPELLIER   (France)

^d Montpellier University Medical Center   (France)

^e MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; CELL SURFACE MARKER; PROTEIN SSEA3; PROTEIN SSEA4; PROTEIN TRA 1-60; PROTEIN TRA 1-81; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GRANULE; CELL HETEROGENEITY; CELL RENEWAL; CELLULAR DISTRIBUTION; CLONOGENESIS; CORRELATION ANALYSIS; FLOW CYTOMETRY; GERM LAYER; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD24; ANTIGENS, SURFACE; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CLONE CELLS; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC HETEROGENEITY; GERM LAYERS; HUMANS; MICE; MICE, SCID; PLURIPOTENT STEM CELLS; PROTEOGLYCANS; STAGE-SPECIFIC EMBRYONIC ANTIGENS; TERATOMA;

EID: 84881094559     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0658     Document Type: Article

References (32)

1. Yu J and JA Thomson. (2008). Pluripotent stem cell lines. Genes Dev 22:1987-1997.
2. Chambers I, J Silva, D Colby, J Nichols, B Nijmeijer, M Robertson, J Vrana, K Jones, L Grotewold and A Smith. (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450:1230-1234.
3. Guo G, M Huss, GQ Tong, C Wang, L Li Sun, ND Clarke and P Robson. (2010). Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18:675-685.
4. Halley JD, K Smith-Miles, DA Winkler, T Kalkan, S Huang and A Smith. (2012). Self-organizing circuitry and emergent computation in mouse embryonic stem cells. Stem Cell Res 8:324-333.
5. Gu B, J Zhang, Q Chen, B Tao, W Wang, Y Zhou, L Chen, Y Liu and M Zhang. (2010). Aire regulates the expression of differentiation-associated genes and self-renewal of embryonic stem cells. Biochem Biophys Res Commun 394:418-423.
6. Gu B, J Zhang, W Wang, L Mo, Y Zhou, L Chen, Y Liu and M Zhang. (2010). Global expression of cell surface proteins in embryonic stem cells. PLoS One 5:e15795.
7. Gu B, J Zhang, Y Wu, X Zhang, Z Tan, Y Lin, X Huang, L Chen, K Yao and M Zhang. (2011). Proteomic analyses reveal common promiscuous patterns of cell surface proteins on human embryonic stem cells and sperms. PLoS One 6:e19386.
8. Cui L, K Johkura, F Yue, N Ogiwara, Y Okouchi, K Asa-numa and K Sasaki. (2004). Spatial distribution and initial changes of SSEA-1 and other cell adhesion-related molecules on mouse embryonic stem cells before and during differentiation. J Histochem Cytochem 52:1447-1457.
9. Enver T, S Soneji, C Joshi, J Brown, F Iborra, T Orntoft, T Thykjaer, E Maltby, K Smith, et al. (2005). Cellular differentiation hierarchies in normal and culture-adapted human embryonic stem cells. Hum Mol Genet 14:3129-3140.
10. Hong SH, S Rampalli, JB Lee, J McNicol, T Collins, JS Draper and M Bhatia. (2011). Cell fate potential of human pluripo-tent stem cells is encoded by histone modifications. Cell Stem Cell 9:24-36.
11. Ramirez JM, S Gerbal-Chaloin, O Milhavet, B Qiang, F Becker, S Assou, JM Lemaitre, S Hamamah and J De Vos. (2011). Brief report: benchmarking human pluripotent stem cell markers during differentiation into the three germ layers unveils a striking heterogeneity: all markers are not equal. Stem Cells 29:1469-1474.
12. Stewart MH, M Bosse, K Chadwick, P Menendez, SC Bendall and M Bhatia. (2006). Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem cell compartment. Nat Methods 3:807-815.
13. Hayashi K, SM Lopes, F Tang and MA Surani. (2008). Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3:391-401.
14. Tanasijevic B, B Dai, T Ezashi, K Livingston, RM Roberts and TP Rasmussen. (2009). Progressive accumulation of epigenetic heterogeneity during human ES cell culture. Epigenetics 4:330-338.
15. Hough SR, AL Laslett, SB Grimmond, G Kolle and MF Pera. (2009). A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells. PLoS One 4:e7708.
16. Martinez Arias A and JM Brickman. (2011). Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr Opin Cell Biol 23:650-656.
17. Eldar A and MB Elowitz. (2010). Functional roles for noise in genetic circuits. Nature 467:167-173.
18. Ho MS, A Fryga and AL Laslett. (2011). Flow cytometric analysis of human pluripotent stem cells. Methods Mol Biol 767:221-230.
19. Cowan CA, I Klimanskaya, J McMahon, J Atienza, J Witmyer, JP Zucker, S Wang, CC Morton, AP McMahon, D Powers and DA Melton. (2004). Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 350:1353-1356.
20. Assou S, D Cerecedo, S Tondeur, V Pantesco, O Hovatta, B Klein, S Hamamah and J De Vos. (2009). A gene expression signature shared by human mature oocytes and embryonic stem cells. BMC Genomics 10:10.
21. Yu J, MA Vodyanik, K Smuga-Otto, J Antosiewicz-Bourget, JL Frane, S Tian, J Nie, GA Jonsdottir, V Ruotti, et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920.
22. D'Amour KA, AD Agulnick, S Eliazer, OG Kelly, E Kroon and EE Baetge. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23:1534-1541.
23. Chambers SM, CA Fasano, EP Papapetrou, M Tomishima, M Sadelain and L Studer. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275-280.
24. Klimchenko O, M Mori, A Distefano, T Langlois, F Larbret, Y Lecluse, O Feraud, W Vainchenker, F Norol and N Debili. (2009). A common bipotent progenitor generates the ery-throid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood 114:1506-1517.
25. Gentleman RC, VJ Carey, DM Bates, B Bolstad, M Dettling, S Dudoit, B Ellis, L Gautier, Y Ge, et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80.
26. Hahne F, N LeMeur, RR Brinkman, B Ellis, P Haaland, D Sarkar, J Spidlen, E Strain and R Gentleman. (2009). flow-Core: a Bioconductor package for high throughput flow cytometry. BMC Bioinformatics 10:106.
27. Assou S, T Le Carrour, S Tondeur, S Strom, A Gabelle, S Marty, L Nadal, V Pantesco, T Reme, et al. (2007). A meta-analysis of human embryonic stem cells transcriptome integrated into a web-based expression atlas. Stem Cells 25:961-973.
28. Lensch MW, TM Schlaeger, LI Zon and GQ Daley. (2007). Teratoma formation assays with human embryonic stem cells: a rationale for one type of human-animal chimera. Cell Stem Cell 1:253-258.
29. Prokhorova TA, LM Harkness, U Frandsen, N Ditzel, HD Schroder, JS Burns and M Kassem. (2009). Teratoma formation by human embryonic stem cells is site dependent and enhanced by the presence of Matrigel. Stem Cells Dev 18:47-54.
30. Narsinh KH, N Sun, V Sanchez-Freire, AS Lee, P Almeida, S Hu, T Jan, KD Wilson, D Leong, et al. (2011). Single cell transcriptional profiling reveals heterogeneity of human induced pluripotent stem cells. J Clin Invest 121:1217-1221.
31. das Neves RP, NS Jones, L Andreu, R Gupta, T Enver and FJ Iborra. (2010). Connecting variability in global transcription rate to mitochondrial variability. PLoS Biol 8:e1000560.
32. Chang HH, M Hemberg, M Barahona, DE Ingber and S Huang. (2008). Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453:544-547.