Large-scale transcriptional profiling and functional assays reveal important roles for Rho-GTPase signalling and SCL during haematopoietic differentiation of human embryonic stem cells

Human Molecular Genetics

Volumn 20, Issue 24, 2011, Pages 4932-4946

  Yung, Sun ^a   Ledran, Maria ^a   Moreno gimeno, Inmaculada ^b   Conesa, Ana ^b   Montaner, David ^b   Dopazo, Joaquín ^b,c   Dimmick, Ian ^a   Slater, Nicholas J ^a,d   Marenah, Lamin ^d   Real, Pedro J ^e   Paraskevopoulou, Iliana ^a   Bisbal, Viviana ^b   Burks, Deborah ^b   Santibanez Koref, Mauro ^a   Moreno, Ruben ^b   Mountford, Joanne ^d   Menendez, Pablo ^e   Armstrong, Lyle ^a   Lako, Majlinda ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGONUCLEOTIDE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; ENGRAFTMENT; ERYTHROID CELL; FLOW CYTOMETRY; GENE; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HEMOLYTIC ANEMIA; HUMAN; HUMAN CELL; MESODERM; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCL GENE; UPREGULATION;

ACUTE DISEASE; ANEMIA, HEMOLYTIC; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CLUSTER ANALYSIS; EMBRYONIC STEM CELLS; ERYTHROID CELLS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MYELOID CELLS; PARACRINE COMMUNICATION; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; TRANSCRIPTOME;

EID: 81855183741     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr431     Document Type: Article

References (57)

1. Chadwick, K., Wang, L., Li, L., Menendez, P., Murdoch, B., Rouleau, A. and Bhatia, M. (2003) Cytokines and BMP-4 Promote Hematopoietic Differentiation of Human Embryonic Stem Cells. Blood, 102, 906-915.
2. Choi, K.D., Yu, J., Smuga-Otto, K., Salvagiotto, G., Rehrauer, W., Vodyanik, M., Thomson, J. and Slukvin, I. (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells, 27, 559-567.
3. Karlsson, K.R., Cowley, S., Martinez, F.O., Shaw, M., Minger, S.L. and James, W. (2008) Homogeneous monocytes and macrophages from human embryonic stem cells following coculture-free differentiation in M-CSF and IL-3. Exp. Hematol., 36, 1167-1175.
4. Kaufman, D.S., Hanson, E.T., Lewis, R.L., Auerbach, R. and Thomson, J.A. (2001) Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc. Natl Acad. Sci. USA, 98, 10716-10721.
5. Kennedy, M., D'Souza, S.L., Lynch-Kattman, M., Schwantz, S. and Keller, G. (2007) Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood, 109, 2679-2687.
6. Ma, F., Wang, D., Hanada, S., Ebihara, Y., Kawasaki, H., Zaike, Y., Heike, T., Nakahata, T. and Tsuji, K. (2007) Novel method for efficient production of multipotential hematopoietic progenitors from human embryonic stem cells. Int. J. Hematol., 85, 371-379.
7. Martin, C.H., Woll, P.S., Ni, Z., Zuniga-Pflucker, J.C. and Kaufman, D.S. (2008) Differences in lymphocyte developmental potential between human embryonic stem cell and umbilical cord blood-derived hematopoietic progenitor cells. Blood, 112, 2730-2737.
8. Ng, E.S., Davis, R.P., Hatzistavrou, T., Stanley, E.G. and Elefanty, A.G. (2008) Directed differentiation of human embryonic stem cells as spin embryoid bodies and a description of the hematopoietic blast colony forming assay. Curr. Protoc. Stem Cell Biol., Chapter 1, Unit 1D.3.
9. Pick, M., Azzola, L., Mossman, A., Stanley, E.G. and Elefanty, A.G. (2007) Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells, 25, 2206-2214.
10. Schenke-Layland, K., Rhodes, K.E., Angelis, E., Butylkova, Y., Heydarkhan-Hagvall, S., Gekas, C., Zhang, R., Goldhaber, J.I., Mikkola, H.K., Plath, K. et al. (2008) Reprogrammed mouse fibroblasts differentiate into cells of the cardiovascular and hematopoietic lineages. Stem Cells, 26, 1537-1546.
11. Tabatabaei-Zavareh, N., Vlasova, A., Greenwood, C.P. and Takei, F. (2007) Characterization of developmental pathway of natural killer cells from embryonic stem cells in vitro. PLoS One, 2, e232.
12. Timmermans, F., Velghe, I., Vanwalleghem, L., De Smedt, M., Van Coppernolle, S., Taghon, T., Moore, H.D., Leclercq, G., Langerak, A.W., Kerre, T. et al. (2009) Generation of T cells from human embryonic stem cell-derived hematopoietic zones. J. Immunol., 182, 6879-6888.
13. Woll, P.S., Morris, J.K., Painschab, M.S., Marcus, R.K., Kohn, A.D., Biechele, T.L., Moon, R.T. and Kaufman, D.S. (2008) Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood, 111, 122-131.
14. Yu, C., Liu, Y., Miao, Z., Yin, M., Lu, W., Lv, Y., Ding, M. and Deng, H. (2010) Retinoic acid enhances the generation of hematopoietic progenitors from human embryonic stem cell-derived hemato-vascular precursors. Blood, 116, 4786-4794.
15. Ledran, M.H., Krassowska, A., Armstrong, L., Dimmick, I., Renstrom, J., Lang, R., Yung, S., Santibanez-Koref, M., Dzierzak, E., Stojkovic, M. et al. (2008) Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell, 3, 85-98.
16. Bowles, K.M., Vallier, L., Smith, J.R., Alexander, M.R. and Pedersen, R.A. (2006) HOXB4 overexpression promotes hematopoietic development by human embryonic stem cells. Stem Cells, 24, 1359-1369.
17. Lee, G.S., Kim, B.S., Sheih, J.H. and Moore, M. (2008) Forced expression of HoxB4 enhances hematopoietic differentiation by human embryonic stem cells. Mol. Cells, 25, 487-493.
18. Unger, C., Karner, E., Treschow, A., Stellan, B., Felldin, U., Concha, H., Wendel, M., Hovatta, O., Aints, A., Ahrlund-Richter, L. et al. (2008) Lentiviral-mediated HoxB4 expression in human embryonic stem cells initiates early hematopoiesis in a dose-dependent manner but does not promote myeloid differentiation. Stem Cells, 26, 2455-2466.
19. Wang, L., Menendez, P., Shojaei, F., Li, L., Mazurier, F., Dick, J.E., Cerdan, C., Levac, K. and Bhatia, M. (2005) Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J. Exp. Med., 201, 1603-1614.
20. Kaufman, D.S. (2009) Toward clinical therapies using hematopoietic cells derived from human pluripotent stem cells. Blood, 114, 3513-3523.
21. Chen, D., Wang, P., Lewis, R.L., Daigh, C.A., Ho, C., Chen, X., Thomson, J.A. and Kendziorski, C. (2007) A microarray analysis of the emergence of embryonic definitive hematopoiesis. Exp. Hematol., 35, 1344-1357.
22. Lu, S.J., Hipp, J.A., Feng, Q., Hipp, J.D., Lanza, R. and Atala, A. (2007) GeneChip analysis of human embryonic stem cell differentiation into hemangioblasts: an in silico dissection of mixed phenotypes. Genome Biol., 8, R240.
23. Player, A., Wang, Y., Bhattacharya, B., Rao, M., Puri, R.K. and Kawasaki, E.S. (2006) Comparisons between transcriptional regulation and RNA expression in human embryonic stem cell lines. Stem Cells Dev., 15, 315-323.
24. Senju, S., Haruta, M., Matsunaga, Y., Fukushima, S., Ikeda, T., Takahashi, K., Okita, K., Yamanaka, S. and Nishimura, Y. (2009) Characterization of dendritic cells and macrophages generated by directed differentiation from mouse induced pluripotent stem cells. Stem Cells, 27, 1021-1031.
25. Sun, B.W., Yang, A.C., Feng, Y., Sun, Y.J., Zhu, Y., Zhang, Y., Jiang, H., Li, C.L., Gao, F.R., Zhang, Z.H. et al. (2006) Temporal and parental-specific expression of imprinted genes in a newly derived Chinese human embryonic stem cell line and embryoid bodies. Hum. Mol. Genet., 15, 65-75.
26. Wang, L., Li, L., Shojaei, F., Levac, K., Cerdan, C., Menendez, P., Martin, T., Rouleau, A. and Bhatia, M. (2004) Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity, 21, 31-41.
27. Nueda, M.J., Conesa, A., Westerhuis, J.A., Hoefsloot, H.C., Smilde, A.K., Talon, M. and Ferrer, A. (2007) Discovering gene expression patterns in time course microarray experiments by ANOVA-SCA. Bioinformatics, 23, 1792-1800.
28. Nueda, M.J., Sebastian, P., Tarazona, S., Garcia-Garcia, F., Dopazo, J., Ferrer, A. and Conesa, A. (2009) Functional assessment of time course microarray data. BMC Bioinform., 10(Suppl. 6), S9.
29. Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M. and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
30. Ghiaur, G., Ferkowicz, M.J., Milsom, M.D., Bailey, J., Witte, D., Cancelas, J.A., Yoder, M.C. and Williams, D.A. (2008) Rac1 is essential for intraembryonic hematopoiesis and for the initial seeding of fetal liver with definitive hematopoietic progenitor cells. Blood, 111, 3313-3321.
31. Konstantinidis, D.G., George, A. and Kalfa, T.A. (2010) Rac GTPases in erythroid biology. Transf. Clin. Biol., 17, 126-130.
32. Kalfa, T.A., Pushkaran, S., Zhang, X., Johnson, J.F., Pan, D., Daria, D., Geiger, H., Cancelas, J.A., Williams, D.A. and Zheng, Y. (2010) Rac1 and Rac2 GTPases are necessary for early erythropoietic expansion in the bone marrow but not in the spleen. Haematologica, 95, 27-35.
33. Yang, L., Wang, L., Kalfa, T.A., Cancelas, J.A., Shang, X., Pushkaran, S., Mo, J., Williams, D.A. and Zheng, Y. (2007) Cdc42 critically regulates the balance between myelopoiesis and erythropoiesis. Blood, 110, 3853-3861.
34. Guo, F., Velu, C.S., Grimes, H.L. and Zheng, Y. (2009) Rho GTPase Cdc42 is essential for B-lymphocyte development and activation. Blood, 114, 2909-2916.
35. Chae, H.D., Lee, K.E., Williams, D.A. and Gu, Y. (2008) Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood, 111, 2597-2605.
36. Fonseca, A.V., Freund, D., Bornhauser, M. and Corbeil, D. (2010) Polarization and migration of hematopoietic stem and progenitor cells rely on the RhoA/ROCK I pathway and an active reorganization of the microtubule network. J. Biol. Chem., 285, 31661-31671.
37. Geiger, H., Koehler, A. and Gunzer, M. (2007) Stem cells, aging, niche, adhesion and Cdc42: a model for changes in cell-cell interactions and hematopoietic stem cell aging. Cell Cycle, 6, 884-887.
38. Sengupta, A., Arnett, J., Dunn, S., Williams, D.A. and Cancelas, J.A. (2010) Rac2 GTPase deficiency depletes BCR-ABL+ leukemic stem cells and progenitors in vivo. Blood, 116, 81-84.
39. Christian, S., Ahorn, H., Novatchkova, M., Garin-Chesa, P., Park, J.E., Weber, G., Eisenhaber, F., Rettig, W.J. and Lenter, M.C. (2001) Molecular cloning and characterization of EndoGlyx-1, an EMILIN-like multisubunit glycoprotein of vascular endothelium. J. Biol. Chem., 276, 48588-48595.
40. Kim, I., Saunders, T.L. and Morrison, S.J. (2007) Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell, 130, 470-483.
41. Zhang, M., Bohlson, S.S., Dy, M. and Tenner, A.J. (2005) Modulated interaction of the ERM protein, moesin, with CD93. Immunology, 115, 63-73.
42. Gandillet, A., Serrano, A.G., Pearson, S., Lie, A.L.M., Lacaud, G. and Kouskoff, V. (2009) Sox7-sustained expression alters the balance between proliferation and differentiation of hematopoietic progenitors at the onset of blood specification. Blood, 114, 4813-4822.
43. Albrecht, I., Niesner, U., Janke, M., Menning, A., Loddenkemper, C., Kuhl, A.A., Lepenies, I., Lexberg, M.H., Westendorf, K., Hradilkova, K. et al. (2010) Persistence of effector memory Th1 cells is regulated by Hopx. Eur. J. Immunol., 40, 2993-3006.
44. Lawrence, H.J., Christensen, J., Fong, S., Hu, Y.L., Weissman, I., Sauvageau, G., Humphries, R.K. and Largman, C. (2005) Loss of expression of the Hoxa-9 homeobox gene impairs the proliferation and repopulating ability of hematopoietic stem cells. Blood, 106, 3988-3994.
45. Wilson, N.K., Miranda-Saavedra, D., Kinston, S., Bonadies, N., Foster, S.D., Calero-Nieto, F., Dawson, M.A., Donaldson, I.J., Dumon, S., Frampton, J. et al. (2009) The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood, 113, 5456-5465.
46. Liu, F. and Patient, R. (2008) Genome-wide analysis of the zebrafish ETS family identifies three genes required for hemangioblast differentiation or angiogenesis. Circ. Res., 103, 1147-1154.
47. Pimanda, J.E., Ottersbach, K., Knezevic, K., Kinston, S., Chan, W.Y., Wilson, N.K., Landry, J.R., Wood, A.D., Kolb-Kokocinski, A., Green, A.R. et al. (2007) Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc. Natl Acad. Sci. USA, 104, 17692-17697.
48. Klimchenko, O., Mori, M., Distefano, A., Langlois, T., Larbret, F., Lecluse, Y., Feraud, O., Vainchenker, W., Norol, F. and Debili, N. (2009) A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood, 114, 1506-1517.
49. Tsiftsoglou, A.S., Vizirianakis, I.S. and Strouboulis, J. (2009) Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life, 61, 800-830.
50. Savill, N.J., Chadwick, W. and Reece, S.E. (2009) Quantitative analysis of mechanisms that govern red blood cell age structure and dynamics during anaemia. PLoS Comput. Biol., 5, e1000416.
51. Baum, K.J. and Ren, R. (2008) Effect of Ras inhibition in hematopoiesis and BCR/ABL leukemogenesis. J. Hematol. Oncol., 1, 5.
52. Mulloy, J.C., Cancelas, J.A., Filippi, M.D., Kalfa, T.A., Guo, F. and Zheng, Y. (2010) Rho GTPases in hematopoiesis and hemopathies. Blood, 115, 936-947.
53. Cancelas, J.A. and Williams, D.A. (2009) Rho GTPases in hematopoietic stem cell functions. Curr. Opin. Hematol., 16, 249-254.
54. Robb, L. and Begley, C.G. (1997) The SCL/TAL1 gene: roles in normal and malignant haematopoiesis. Bioessays, 19, 607-613.
55. Shibuya, K., Akahori, H., Takahashi, K., Tahara, E., Kato, T. and Miyazaki, H. (1998) Multilineage hematopoietic recovery by a single injection of pegylated recombinant human megakaryocyte growth and development factor in myelosuppressed mice. Blood, 91, 37-45.
56. Stojkovic, M., Lako, M., Stojkovic, P., Stewart, R., Przyborski, S., Armstrong, L., Evans, J., Herbert, M., Hyslop, L., Ahmad, S. et al. (2004) Derivation of human embryonic stem cells from day-8 blastocysts recovered after three-step in vitro culture. Stem Cells, 22, 790-797.
57. Yang, C., Atkinson, S.P., Vilella, F., Lloret, M., Armstrong, L., Mann, D.A. and Lako, M. (2010) Opposing putative roles for canonical and noncanonical NFkappaB signaling on the survival, proliferation, and differentiation potential of human embryonic stem cells. Stem Cells, 28, 1970-1980.