CD24 tracks divergent pluripotent states in mouse and human cells

Nature Communications

Volumn 6, Issue , 2015, Pages

  Shakiba, Nika ^a   White, Carl A ^a,b   Lipsitz, Yonatan Y ^a   Yachie Kinoshita, Ayako ^a,b   Tonge, Peter D ^c   Hussein, Samer M I ^c   Puri, Mira C ^b,c   Elbaz, Judith ^c   Morrissey Scoot, James ^a   Li, Mira ^c   Munoz, Javier ^d,e   Benevento, Marco ^d,e   Rogers, Ian M ^b,c   Hanna, Jacob H ^f   Heck, Albert J R ^d,e   Wollscheid, Bernd ^g   Nagy, Andras ^b,c   Zandstra, Peter W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UTRECHT UNIVERSITY   (Netherlands)

^e NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^f WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^g ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; CD24 PROTEIN, HUMAN; CD24A PROTEIN, MOUSE;

BIOMARKER; CELLS AND CELL COMPONENTS; CYTOLOGY; GENE EXPRESSION; PROTEIN; RODENT; THEORETICAL STUDY;

ANIMAL CELL; ARTICLE; CELL SURFACE; CELL TRACKING; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYONIC STEM CELL; EPIBLAST STEM CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PROTEOMICS; STEM CELL CULTURE; STEM CELL RESEARCH; TRANSGENICS; ANIMAL; CYTOLOGY; GERM LAYER; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOUSE EMBRYONIC STEM CELL; STEM CELL;

ANIMALS; ANTIGENS, CD24; CELLULAR REPROGRAMMING; GERM LAYERS; HUMAN EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MOUSE EMBRYONIC STEM CELLS; STEM CELLS;

EID: 84935840469     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8329     Document Type: Article

References (49)

1. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
2. Park, I.-H. et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451, 141-146 (2007).
3. Samavarchi-Tehrani, P. et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7, 64-77 (2010).
4. Polo, J. M. et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151, 1617-1632 (2012).
5. Hansson, J. et al. Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency. Cell Rep. 2, 1579-1592 (2012).
6. O'Malley, J. et al. High-resolution analysis with novel cell-surface markers identifies routes to iPS cells. Nature 499, 88-91 (2013).
7. Woltjen, K. et al. PiggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770 (2009).
8. Golipour, A. et al. A late transition in somatic cell reprogramming requires regulators distinct from the pluripotency network. Stem Cell 11, 769-782 (2012).
9. Tonge, P. D. et al. Divergent reprogramming routes lead to alternative stem cell states. Nature 516, 192-197 (2012).
10. Hussein, S. M. I. et al. Genome-wide characterization of the routes to pluripotency. Nature 516, 198-206 (2012).
11. Gafni, O. et al. Derivation of novel human ground state naive pluripotent stem cells. Nature 504, 282-286 (2013).
12. Wollscheid, B. et al. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat. Biotechnol. 27, 378-386 (2009).
13. Thompson, A. et al. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 75, 1895-1904 (2003).
14. Benevento, M. et al. Proteome adaptation in cell reprogramming proceeds via distinct transcriptional networks. Nature 5, 5613 (2014).
15. Smith, L. M. & Kelleher, N. L. Proteoform: a single term describing protein complexity. Nat. Methods 10, 186-187 (2013).
16. Thomas, P. D. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 13, 2129-2141 (2003).
17. Mi, H. The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res. 33, D284-D288 (2004).
18. Kuhn, R. M. et al. The UCSC Genome Browser Database: update 2009. Nucleic Acids Res. 37, D755-D761 (2009).
19. Fluri, D. A. et al. Derivation, expansion and differentiation of induced pluripotent stem cells in continuous suspension cultures. Nat. Methods 9, 509-516 (2012).
20. Hou, P. et al. Pluripotent stem cells induced from mouse somatic cells by smallmolecule compounds. Science 341, 651-654 (2013).
21. Carey, B. W., Markoulaki, S., Beard, C., Hanna, J. & Jaenisch, R. Single-gene transgenic mouse strains for reprogramming adult somatic cells. Nat. Methods 7, 56-59 (2010).
22. Tonge, P. D. et al. Divergent reprogramming routes lead to alternative stem-cell states. Nature 516, 192-197 (2014).
23. Nishimura, K. et al. Manipulation of KLF4 expression generates iPSCs paused at successive stages of reprogramming. Stem Cell Rep. 3, 915-929 (2014).
24. Rugg-Gunn, P. J. et al. Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells. Dev. Cell 22, 887-901 (2012).
25. Onishi, K., Tonge, P. D., Nagy, A. & Zandstra, P. W. Microenvironmentmediated reversion of epiblast stem cells by reactivation of repressed JAKSTAT signaling. Integr. Biol. (Camb.) 4, 1367-1376 (2012).
26. Toyooka, Y., Shimosato, D., Murakami, K., Takahashi, K. & Niwa, H. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135, 909-918 (2008).
27. Hayashi, K., Lopes, S. M., Tang, F. & Surani, M. A. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3, 391-401 (2008).
28. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
29. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
30. Nichols, J. & Smith, A. Naive and primed pluripotent states. Cell Stem Cell 4, 487-492 (2009).
31. Yan, L. et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1131-1139 (2013).
32. Theunissen, T. W. et al. Systematic identification of culture conditions for induction and maintenanceof naive human pluripotency. Stem Cell 15, 471-487 (2014).
33. Takashima, Y. et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158, 1254-1269 (2014).
34. Sammar, M., Gulbins, E., Hilbert, K., Lang, F. & Altevogt, P. Mouse CD24 as a signaling molecule for integrin-mediated cell binding: functional and physical association with src-kinases. Biochem. Biophys. Res. Commun. 234, 330-334 (1997).
35. Goode, I., Xu, H. & Ildstad, S. T. Regulatory B cells: the new 'it' cell. Transplant. Proc. 46, 3-8 (2014).
36. Quan, M., Wang, P., Cui, J., Gao, Y. & Xie, K. The roles of FOXM1 in pancreatic stem cells and carcinogenesis. Mol. Cancer 12, 159 (2013).
37. Magnaldo, T. & Barrandon, Y. CD24 (heat stable antigen, nectadrin), a novel keratinocyte differentiation marker, is preferentially expressed in areas of the hair follicle containing the colony-forming cells. J. Cell Sci. 109, 3035-3045 (1996).
38. Fang, X., Zheng, P., Tang, J. & Liu, Y. CD24: from A to Z. Cell Mol. Immunol. 7, 100-103 (2010).
39. Shirasawa, T. et al. Gene expression of CD24 core peptide molecule in developing brain and developing non-neural tissues. Dev. Dyn. 198, 1-13 (1993).
40. Lee, T. K. W. et al. CD24(+) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 9, 50-63 (2011).
41. Smith, S. C. et al. The metastasis-associated gene CD24 is regulated by Ral GTPase and is a mediator of cell proliferation and survival in human cancer. Cancer Res. 66, 1917-1922 (2006).
42. Baumann, P. et al. CD24 interacts with and promotes the activity of c-src within lipid rafts in breast cancer cells, thereby increasing integrin-dependent adhesion. Cell Mol. Life Sci. 69, 435-448 (2012).
43. Lee, K.-M. et al. CD24 regulates cell proliferation and transforming growth factor b-induced epithelial to mesenchymal transition through modulation of integrin b1 stability. Cell Signal. 24, 2132-2142 (2012).
44. Wang, L. et al. Intracellular CD24 disrupts the ARF-NPM interaction and enables mutational and viral oncogene-mediated p53 inactivation. Nat. Commun. 6, 5909 (2015).
45. Tesar, P. J. et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199 (2007).
46. Le, T. L., Yap, A. S. & Stow, J. L. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232 (1999).
47. Marelli-Berg, F. M., Peek, E., Lidington, E. A., Stauss, H. J. & Lechler, R. I. Isolation of endothelial cells from murine tissue. J. Immunol. Methods 244, 205-215 (2000).
48. Ware, C. B. et al. Derivation of naive human embryonic stem cells. Proc. Natl Acad. Sci. USA 111, 4484-4489 (2014).
49. Kislinger, T. PRISM, a Generic Large Scale Proteomic Investigation Strategy for Mammals. Mol. Cell. Proteomics 2, 96-106 (2003).