Defining the Minimal Factors Required for Erythropoiesis through Direct Lineage Conversion

Cell Reports

Volumn 15, Issue 11, 2016, Pages 2550-2562

  Capellera Garcia, Sandra ^a   Pulecio, Julian ^b   Dhulipala, Kishori ^a   Siva, Kavitha ^a   Rayon Estrada, Violeta ^c   Singbrant, Sofie ^a   Sommarin, Mikael N E ^a   Walkley, Carl R ^d   Soneji, Shamit ^a   Karlsson, Göran ^a   Raya, Ángel ^b,e,f   Sankaran, Vijay G ^g,h   Flygare, Johan ^a  

^a LUND UNIVERSITY   (Sweden)

^b Barcelona Biomedical Research Park   (Spain)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 1; MYC PROTEIN; PROTEIN MYB; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR LMO2; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG; GLOBIN;

ADULT; ANIMAL CELL; ARTICLE; BURST FORMING UNIT; CELL FATE; CELL LINEAGE; CELL STRUCTURE; COLONY FORMATION; CONTROLLED STUDY; ERYTHROBLAST; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; AGING; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CFU COUNTING; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLULAR REPROGRAMMING; COLONY-FORMING UNITS ASSAY; ERYTHROBLASTS; ERYTHROPOIESIS; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLOBINS; HUMANS; MICE, INBRED C57BL; TRANSCRIPTION FACTORS;

EID: 84974678251     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.05.027     Document Type: Article

References (47)

1. Anstee D.J., Gampel A., Toye A.M. Ex-vivo generation of human red cells for transfusion. Curr. Opin. Hematol. 2012, 19:163-169.
2. Batta K., Florkowska M., Kouskoff V., Lacaud G. Direct reprogramming of murine fibroblasts to hematopoietic progenitor cells. Cell Rep. 2014, 9:1871-1884.
3. Cantor A.B., Orkin S.H. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 2002, 21:3368-3376.
4. Chen K., Liu J., Heck S., Chasis J.A., An X., Mohandas N. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc. Natl. Acad. Sci. USA 2009, 106:17413-17418.
5. Doulatov S., Vo L.T., Chou S.S., Kim P.G., Arora N., Li H., Hadland B.K., Bernstein I.D., Collins J.J., Zon L.I., Daley G.Q. Induction of multipotential hematopoietic progenitors from human pluripotent stem cells via respecification of lineage-restricted precursors. Cell Stem Cell 2013, 13:459-470.
6. Dubois N.C., Adolphe C., Ehninger A., Wang R.A., Robertson E.J., Trumpp A. Placental rescue reveals a sole requirement for c-Myc in embryonic erythroblast survival and hematopoietic stem cell function. Development 2008, 135:2455-2465.
7. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
8. Heinrich A.C., Pelanda R., Klingmüller U. A mouse model for visualization and conditional mutations in the erythroid lineage. Blood 2004, 104:659-666.
9. Hodge D., Coghill E., Keys J., Maguire T., Hartmann B., McDowall A., Weiss M., Grimmond S., Perkins A. A global role for EKLF in definitive and primitive erythropoiesis. Blood 2006, 107:3359-3370.
10. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
11. Huang W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
12. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
13. Huang P., He Z., Ji S., Sun H., Xiang D., Liu C., Hu Y., Wang X., Hui L. Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 2011, 475:386-389.
14. Ieda M., Fu J.D., Delgado-Olguin P., Vedantham V., Hayashi Y., Bruneau B.G., Srivastava D. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142:375-386.
15. Jopling C., Boue S., Izpisua Belmonte J.C. Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat. Rev. Mol. Cell Biol. 2011, 12:79-89.
16. Kingsley P.D., Malik J., Emerson R.L., Bushnell T.P., McGrath K.E., Bloedorn L.A., Bulger M., Palis J. "Maturational" globin switching in primary primitive erythroid cells. Blood 2006, 107:1665-1672.
17. Kingsley P.D., Greenfest-Allen E., Frame J.M., Bushnell T.P., Malik J., McGrath K.E., Stoeckert C.J., Palis J. Ontogeny of erythroid gene expression. Blood 2013, 121:e5-e13.
18. Kulessa H., Frampton J., Graf T. GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev. 1995, 9:1250-1262.
19. Lang S., Ugale A., Erlandsson E., Karlsson G., Bryder D., Soneji S. SCExV: a webtool for the analysis and visualisation of single cell qRT-PCR data. BMC Bioinformatics 2015, 16:320.
20. Li L., Freudenberg J., Cui K., Dale R., Song S.H., Dean A., Zhao K., Jothi R., Love P.E. Ldb1-nucleated transcription complexes function as primary mediators of global erythroid gene activation. Blood 2013, 121:4575-4585.
21. Love P.E., Warzecha C., Li L. Ldb1 complexes: the new master regulators of erythroid gene transcription. Trends Genet. 2014, 30:1-9.
22. McGrath K.E., Frame J.M., Fromm G.J., Koniski A.D., Kingsley P.D., Little J., Bulger M., Palis J. A transient definitive erythroid lineage with unique regulation of the β-globin locus in the mammalian embryo. Blood 2011, 117:4600-4608.
23. Mead P.E., Deconinck A.E., Huber T.L., Orkin S.H., Zon L.I. Primitive erythropoiesis in the Xenopus embryo: the synergistic role of LMO-2, SCL and GATA-binding proteins. Development 2001, 128:2301-2308.
24. Osada H., Grutz G.G., Axelson H., Forster A., Rabbitts T.H. LIM-only protein Lmo2 forms a protein complex with erythroid transcription factor GATA-1. Leukemia 1997, 11(Suppl 3):307-312.
25. Palis J. Primitive and definitive erythropoiesis in mammals. Front. Physiol. 2014, 5:3.
26. Pereira C.F., Chang B., Qiu J., Niu X., Papatsenko D., Hendry C.E., Clark N.R., Nomura-Kitabayashi A., Kovacic J.C., Ma'ayan A., et al. Induction of a hemogenic program in mouse fibroblasts. Cell Stem Cell 2013, 13:205-218.
27. Pulecio J., Nivet E., Sancho-Martinez I., Vitaloni M., Guenechea G., Xia Y., Kurian L., Dubova I., Bueren J., Laricchia-Robbio L., Izpisua Belmonte J.C. Conversion of human fibroblasts into monocyte-like progenitor cells. Stem Cells 2014, 32:2923-2938.
28. Riddell J., Gazit R., Garrison B.S., Guo G., Saadatpour A., Mandal P.K., Ebina W., Volchkov P., Yuan G.C., Orkin S.H., Rossi D.J. Reprogramming committed murine blood cells to induced hematopoietic stem cells with defined factors. Cell 2014, 157:549-564.
29. Sadahira K., Fukuchi Y., Kunimono H., Sakurai M., Ikeda Y., Okamoto S., Nakajima H. Direct reprogramming of terminally differentiated B cells into erythroid lineage. FEBS Lett. 2012, 586:3645-3652.
30. Sankaran V.G., Xu J., Ragoczy T., Ippolito G.C., Walkley C.R., Maika S.D., Fujiwara Y., Ito M., Groudine M., Bender M.A., et al. Developmental and species-divergent globin switching are driven by BCL11A. Nature 2009, 460:1093-1097.
31. Sankaran V.G., Menne T.F., Šćepanović D., Vergilio J.A., Ji P., Kim J., Thiru P., Orkin S.H., Lander E.S., Lodish H.F. MicroRNA-15a and -16-1 act via MYB to elevate fetal hemoglobin expression in human trisomy 13. Proc. Natl. Acad. Sci. USA 2011, 108:1519-1524.
32. Sekiya S., Suzuki A. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 2011, 475:390-393.
33. Shivdasani R.A., Orkin S.H. The transcriptional control of hematopoiesis. Blood 1996, 87:4025-4039.
34. Singbrant S., Russell M.R., Jovic T., Liddicoat B., Izon D.J., Purton L.E., Sims N.A., Martin T.J., Sankaran V.G., Walkley C.R. Erythropoietin couples erythropoiesis, B-lymphopoiesis, and bone homeostasis within the bone marrow microenvironment. Blood 2011, 117:5631-5642.
35. Song S.H., Hou C., Dean A. A positive role for NLI/Ldb1 in long-range beta-globin locus control region function. Mol. Cell 2007, 28:810-822.
36. Sridharan R., Tchieu J., Mason M.J., Yachechko R., Kuoy E., Horvath S., Zhou Q., Plath K. Role of the murine reprogramming factors in the induction of pluripotency. Cell 2009, 136:364-377.
37. Szabo E., Rampalli S., Risueño R.M., Schnerch A., Mitchell R., Fiebig-Comyn A., Levadoux-Martin M., Bhatia M. Direct conversion of human fibroblasts to multilineage blood progenitors. Nature 2010, 468:521-526.
38. Takahashi K. Cellular reprogramming--lowering gravity on Waddington's epigenetic landscape. J. Cell Sci. 2012, 125:2553-2560.
39. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
40. Tober J., McGrath K.E., Palis J. Primitive erythropoiesis and megakaryopoiesis in the yolk sac are independent of c-myb. Blood 2008, 111:2636-2639.
41. Trakarnsanga K., Wilson M.C., Lau W., Singleton B.K., Parsons S.F., Sakuntanaga P., Kurita R., Nakamura Y., Anstee D.J., Frayne J. Induction of adult levels of β-globin in human erythroid cells that intrinsically express embryonic or fetal globin by transduction with KLF1 and BCL11A-XL. Haematologica 2014, 99:1677-1685.
42. Tsiftsoglou A.S., Vizirianakis I.S., Strouboulis J. Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life 2009, 61:800-830.
43. Vierbuchen T., Wernig M. Direct lineage conversions: unnatural but useful?. Nat. Biotechnol. 2011, 29:892-907.
44. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Südhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
45. Weng W., Sheng G. Five transcription factors and FGF pathway inhibition efficiently induce erythroid differentiation in the epiblast. Stem Cell Reports 2014, 2:262-270.
46. Yi Z., Cohen-Barak O., Hagiwara N., Kingsley P.D., Fuchs D.A., Erickson D.T., Epner E.M., Palis J., Brilliant M.H. Sox6 directly silences epsilon globin expression in definitive erythropoiesis. PLoS Genet. 2006, 2:e14.
47. Zhou D., Liu K., Sun C.W., Pawlik K.M., Townes T.M. KLF1 regulates BCL11A expression and gamma- to beta-globin gene switching. Nat. Genet. 2010, 42:742-744.