Characterization of transcriptional networks in blood stem and progenitor cells using high-throughput single-cell gene expression analysis (original) (raw)
Orkin, S. H. & Zon, L. I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell132, 631–644 (2008). ArticleCAS Google Scholar
Ottersbach, K., Smith, A., Wood, A. & Gottgens, B. Ontogeny of haematopoiesis: recent advances and open questions. Br. J. Haematol.148, 343–355 (2010). Article Google Scholar
Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell126, 663–676 (2006). CAS Google Scholar
Davis, R. L., Weintraub, H. & Lassar, A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell51, 987–1000 (1987). ArticleCAS Google Scholar
Gering, M., Yamada, Y., Rabbitts, T. H. & Patient, R. K. Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development130, 6187–6199 (2003). ArticleCAS Google Scholar
Di Tullio, A. et al. CCAAT/enhancer binding protein alpha (C/EBP(α))-induced transdifferentiation of pre-B cells into macrophages involves no overt retrodifferentiation. Proc. Natl Acad. Sci. USA108, 17016–17021 (2011). ArticleCAS Google Scholar
Basso, K. et al. Reverse engineering of regulatory networks in human B cells. Nat. Genet.37, 382–390 (2005). ArticleCAS Google Scholar
Pimanda, J. E. & Gottgens, B. Gene regulatory networks governing haematopoietic stem cell development and identity. Int. J. Dev. Biol.54, 1201–1211 (2010). ArticleCAS Google Scholar
Pimanda, J. E. et al. Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc. Natl Acad. Sci. USA104, 17692–17697 (2007). ArticleCAS Google Scholar
Wilson, N. K., Calero-Nieto, F. J., Ferreira, R. & Gottgens, B. Transcriptional regulation of haematopoietic transcription factors. Stem Cell Res. Ther.2, 6 (2011). ArticleCAS Google Scholar
Wilson, N. K. et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell7, 532–544 (2010). ArticleCAS Google Scholar
Wilson, N. K. et al. The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood113, 5456–5465 (2009). ArticleCAS Google Scholar
Sieburg, H. B. et al. The hematopoietic stem compartment consists of a limited number of discrete stem cell subsets. Blood107, 2311–2316 (2006). ArticleCAS Google Scholar
Dykstra, B. et al. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell1, 218–229 (2007). ArticleCAS Google Scholar
Copley, M. R., Beer, P. A. & Eaves, C. J. Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell10, 690–697 (2012). ArticleCAS Google Scholar
Ramos, C. A. et al. Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet.2, e159 (2006). Article Google Scholar
Glotzbach, J. P. et al. An information theoretic, microfluidic-based single cell analysis permits identification of subpopulations among putatively homogeneous stem cells. PLoS One6, e21211 (2011). ArticleCAS Google Scholar
Hu, M. et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev.11, 774–785 (1997). ArticleCAS Google Scholar
Citri, A., Pang, Z. P., Sudhof, T. C., Wernig, M. & Malenka, R. C. Comprehensive qPCR profiling of gene expression in single neuronal cells. Nat. Protoc.7, 118–127 (2012). ArticleCAS Google Scholar
Guo, G. et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell18, 675–685 (2010). ArticleCAS Google Scholar
Dalerba, P. et al. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol.29, 1120–1127 (2011). ArticleCAS Google Scholar
Pina, C. et al. Inferring rules of lineage commitment in haematopoiesis. Nat. Cell Biol.14, 287–294 (2012). ArticleCAS Google Scholar
Kiel, M. J., Yilmaz, O. H., Iwashita, T., Terhorst, C. & Morrison, S. J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell121, 1109–1121 (2005). ArticleCAS Google Scholar
Adolfsson, J. et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell121, 295–306 (2005). ArticleCAS Google Scholar
Pronk, C. J. et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell1, 428–442 (2007). ArticleCAS Google Scholar
Akashi, K., Traver, D., Miyamoto, T. & Weissman, I. L. A clonogenic commonmyeloid progenitor that gives rise to all myeloid lineages. Nature404, 193–197 (2000). ArticleCAS Google Scholar
Kondo, M., Weissman, I. L. & Akashi, K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell91, 661–672 (1997). ArticleCAS Google Scholar
Katayama, N. et al. Stage-specific expression of c-kit protein by murine hematopoietic progenitors. Blood82, 2353–2360 (1993). CASPubMed Google Scholar
Donaldson, I. J. et al. Genome-wide identification of cis-regulatory sequences controlling blood and endothelial development. Hum. Mol. Genet.14, 595–601 (2005). ArticleCAS Google Scholar
Gottgens, B. et al. Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J.21, 3039–3050 (2002). ArticleCAS Google Scholar
Pimanda, J. E. et al. The SCL transcriptional network and BMP signaling pathway interact to regulate RUNX1 activity. Proc. Natl Acad. Sci. USA104, 840–845 (2007). ArticleCAS Google Scholar
Tanaka, Y. et al. The transcriptional programme controlled by Runx1 during early embryonic blood development. Dev. Biol.366, 404–419 (2012). ArticleCAS Google Scholar
Wilson, N. K. et al. Gfi1 expression is controlled by five distinct regulatory regions spread over 100 kilobases, with Scl/Tal1, Gata2, PU.1, Erg, Meis1, and Runx1 acting as upstream regulators in early hematopoietic cells. Mol. Cell Biol.30, 3853–3863 (2010). ArticleCAS Google Scholar
Yamamoto, M., Takahashi, S., Onodera, K., Muraosa, Y. & Engel, J. D. Upstream and downstream of erythroid transcription factor GATA-1. Genes Cells2, 107–115 (1997). ArticleCAS Google Scholar
Mouthon, M. A. et al. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood81, 647–655 (1993). CASPubMed Google Scholar
Orlic, D., Anderson, S., Biesecker, L. G., Sorrentino, B. P. & Bodine, D. M. Pluripotent hematopoietic stem cells contain high levels of mRNA for c-kit, GATA-2, p45 NF-E2, and c-myb and low levels or no mRNA for c-fms and the receptors for granulocyte colony-stimulating factor and interleukins 5 and 7. Proc. Natl Acad. Sci. USA92, 4601–4605 (1995). ArticleCAS Google Scholar
Doan, L. L. et al. Targeted transcriptional repression of Gfi1 by GFI1 and GFI1B in lymphoid cells. Nucleic Acids Res.32, 2508–2519 (2004). ArticleCAS Google Scholar
Vassen, L., Okayama, T. & Moroy, T. Gfi1b: green fluorescent protein knock-in mice reveal a dynamic expression pattern of Gfi1b during hematopoiesis that is largely complementary to Gfi1. Blood109, 2356–2364 (2007). ArticleCAS Google Scholar
Luc, S. et al. The earliest thymic T cell progenitors sustain B cell and myeloid lineage potential. Nat. Immunol.13, 412–419 (2012). ArticleCAS Google Scholar
Lawrence, N. D. ICML Proceedings of the 23rd International Conference on Machine Learning 513–520 (2006). Book Google Scholar
Buettner, F. & Theis, F. J. A novel approach for resolving differences in single-cell gene expression patterns from zygote to blastocyst. Bioinformatics28, i626–i632 (2012). ArticleCAS Google Scholar
Shivdasani, R. A. & Orkin, S. H. Erythropoiesis and globin gene expression in mice lacking the transcription factor NF-E2. Proc. Natl Acad. Sci. USA92, 8690–8694 (1995). ArticleCAS Google Scholar
Shivdasani, R. A. et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell81, 695–704 (1995). ArticleCAS Google Scholar
Hall, M. A. et al. The critical regulator of embryonic hematopoiesis, SCL, is vital in the adult for megakaryopoiesis, erythropoiesis, and lineage choice in CFU-S12. Proc. Natl Acad. Sci. USA100, 992–997 (2003). ArticleCAS Google Scholar
Huang, Z. et al. GATA-2 reinforces megakaryocyte development in the absence of GATA-1. Mol. Cell Biol.29, 5168–5180 (2009). ArticleCAS Google Scholar
Ikonomi, P. et al. Overexpression of GATA-2 inhibits erythroid and promotes megakaryocyte differentiation. Exp. Hematol.28, 1423–1431 (2000). ArticleCAS Google Scholar
Porcher, C. et al. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell86, 47–57 (1996). ArticleCAS Google Scholar
Schuh, A. H. et al. ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol. Cell Biol.25, 10235–10250 (2005). ArticleCAS Google Scholar
Hamlett, I. et al. Characterization of megakaryocyte GATA1-interacting proteins: the corepressor ETO2 and GATA1 interact to regulate terminal megakaryocyte maturation. Blood112, 2738–2749 (2008). ArticleCAS Google Scholar
Huang, S., Guo, Y. P., May, G. & Enver, T. Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol.305, 695–713 (2007). ArticleCAS Google Scholar
Nerlov, C. & Graf, T. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev.12, 2403–2412 (1998). ArticleCAS Google Scholar
Bonadies, N. et al. Genome-wide analysis of transcriptional reprogramming in mouse models of acute myeloid leukaemia. PLoS One6, e16330 (2011). ArticleCAS Google Scholar
Khandanpour, C. et al. The human GFI136N variant induces epigenetic changes at the Hoxa9 locus and accelerates K-RAS driven myeloproliferative disorder in mice. Blood120, 4006–4017 (2012). ArticleCAS Google Scholar
Grass, J. A. et al. Distinct functions of dispersed GATA factor complexes at an endogenous gene locus. Mol. Cell Biol.26, 7056–7067 (2006). ArticleCAS Google Scholar
Pinto do, O. P., Kolterud, A. & Carlsson, L. Expression of the LIM-homeobox gene LH2 generates immortalized steel factor-dependent multipotent hematopoietic precursors. EMBO J.17, 5744–5756 (1998). ArticleCAS Google Scholar
Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y. & Orkin, S. H. Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol.210, 305–321 (1999). ArticleCAS Google Scholar
Bee, T. et al. The mouse Runx1 +23 hematopoietic stem cell enhancer confers hematopoietic specificity to both Runx1 promoters. Blood113, 5121–5124 (2009). ArticleCAS Google Scholar
Gottgens, B. et al. cis-regulatory remodeling of the SCL locus during vertebrate evolution. Mol. Cell Biol.30, 5741–5751 (2010). ArticleCAS Google Scholar
Foster, S. D., Oram, S. H., Wilson, N. K. & Gottgens, B. From genes to cells to tissues-modelling the haematopoietic system. Mol. Biosyst.5, 1413–1420 (2009). ArticleCAS Google Scholar
Narula, J., Smith, A. M., Gottgens, B. & Igoshin, O. A. Modeling reveals bistability and low-pass filtering in the network module determining blood stem cell fate. PLoS Comput. Biol.6, e1000771 (2010). Article Google Scholar
Alon, U. Network motifs: theory and experimental approaches. Nat. Rev. Genet.8, 450–461 (2007). ArticleCAS Google Scholar
Tipping, A. J. et al. High GATA-2 expression inhibits human hematopoietic stem and progenitor cell function by effects on cell cycle. Blood113, 2661–2672 (2009). ArticleCAS Google Scholar
Monteiro, R., Pouget, C. & Patient, R. The gata1/pu.1 lineage fate paradigm varies between blood populations and is modulated by tif1gamma. EMBO J.30, 1093–1103 (2011). ArticleCAS Google Scholar
Hahn, C. N. et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat. Genet.43, 1012–1017 (2011). ArticleCAS Google Scholar
Phelan, J. D. et al. Growth factor independent-1 (Gfi1) is critically required for T-cell acute lymphoblastic leukemia (T-ALL) tumor initiation and maintenance. Blood (ASH Annual Meeting Abstracts)116, 3156 (2010). Google Scholar
Szklarczyk, D. et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res.39, D561–D568 (2011). ArticleCAS Google Scholar
Kim, W. K., Krumpelman, C. & Marcotte, E. M. Inferring mouse gene functions from genomic-scale data using a combined functional network/classification strategy. Genome Biol.9 (Suppl. 1), S5 (2008). Article Google Scholar
Milasevic, P. a. D. & Ducharme, G. R. Uniqueness of the spatial median. Ann. Stat.15, 1332–1333 (1987). Article Google Scholar
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods9, 357–359 (2012). ArticleCAS Google Scholar
Bockamp, E. O. et al. Transcriptional regulation of the stem cell leukemia gene by PU.1 and Elf-1. J. Biol. Chem.273, 29032–29042 (1998). ArticleCAS Google Scholar
Landry, J. R. et al. Fli1, Elf1, and Ets1 regulate the proximal promoter of the LMO2 gene in endothelial cells. Blood106, 2680–2687 (2005). ArticleCAS Google Scholar