Artículos de revistas
Teleost Growth Factor Independence (gfi) Genes Differentially Regulate Successive Waves Of Hematopoiesis
Registro en:
Developmental Biology. , v. 373, n. 2, p. 431 - 441, 2013.
121606
10.1016/j.ydbio.2012.08.015
2-s2.0-84871693252
Autor
Cooney J.D.
Hildick-Smith G.J.
Shafizadeh E.
McBride P.F.
Carroll K.J.
Anderson H.
Shaw G.C.
Tamplin O.J.
Branco D.S.
Dalton A.J.
Shah D.I.
Wong C.
Gallagher P.G.
Zon L.I.
North T.E.
Paw B.H.
Institución
Resumen
Growth Factor Independence (Gfi) transcription factors play essential roles in hematopoiesis, differentially activating and repressing transcriptional programs required for hematopoietic stem/progenitor cell (HSPC) development and lineage specification. In mammals, Gfi1. a regulates hematopoietic stem cells (HSC), myeloid and lymphoid populations, while its paralog, Gfi1. b, regulates HSC, megakaryocyte and erythroid development. In zebrafish, gfi1. aa is essential for primitive hematopoiesis; however, little is known about the role of gfi1. aa in definitive hematopoiesis or about additional gfi factors in zebrafish. Here, we report the isolation and characterization of an additional hematopoietic gfi factor, gfi1. b. We show that gfi1. aa and gfi1. b are expressed in the primitive and definitive sites of hematopoiesis in zebrafish. Our functional analyses demonstrate that gfi1. aa and gfi1. b have distinct roles in regulating primitive and definitive hematopoietic progenitors, respectively. Loss of gfi1. aa silences markers of early primitive progenitors, scl and gata1. Conversely, loss of gfi1. b silences runx-1, c-myb, ikaros and cd41, indicating that gfi1. b is required for definitive hematopoiesis. We determine the epistatic relationships between the gfi factors and key hematopoietic transcription factors, demonstrating that gfi1. aa and gfi1. b join lmo2, scl, runx-1 and c-myb as critical regulators of teleost HSPC. Our studies establish a comparative paradigm for the regulation of hematopoietic lineages by gfi transcription factors. © 2012 Elsevier Inc. 373 2 431 441 Amigo, J.D., Yu, M., Troadec, M.-B., Gwynn, B., Cooney, J.D., Lambert, A.J., Chi, N.C., Paw, B.H., Identification of distal cis-regulatory elements at mouse mitoferrin loci using zebrafish transgenesis (2011) Mol. Cell. Biol., 31, pp. 1344-1356 Amigo, J.D., Ackermann, G.E., Cope, J.J., Yu, M., Cooney, J.D., Ma, D., Langer, N.B., Paw, B.H., The role and regulation of friend of GATA-1 (FOG-1) during blood development in the zebrafish (2009) Blood, 114, pp. 4654-4663 Bolli, N., Payne, E.M., Rhodes, J., Gjini, E., Johnston, A.B., Guo, F., Lee, J.-S., Look, A.T., Cpsf1 is required for definitive HSC survival in zebrafish (2011) Blood, 117, pp. 3996-4007 Burns, C.E., Traver, D., Mayhall, E., Shepard, J.L., Zon, L.I., Hematopoietic stem cell fate is established by the Notch-Runx pathway (2005) Genes Dev., 19, pp. 2331-2342 Bussmann, J., Bakkers, J., Schulte-Merker, S., Early endocardial morphogenesis requires Scl/Tal1 (2007) PLoS Genet., 3, pp. e140 Dan, K., Thrombocytosis in iron deficiency anemia (2005) Intern. Med., 44, pp. 1025-1026 Davidson, A.J., Zon, L.I., The 'definitive' (and "primitive") guide to zebrafish hematopoiesis (2004) Oncogene, 23, pp. 7233-7246 Dooley, K.A., Davidson, A.J., Zon, L.I., Zebrafish scl functions independently in hematopoietic and endothelial development (2005) Dev. Biol., 277, pp. 522-536 Dufourcq, P., Rastegar, S., Strähle, U., Blader, P., Parapineal specific expression of gfi1 in the zebrafish epithalamus (2004) Gene. Expr. Patterns, 4, pp. 53-57 Farr, C.J., Saiki, R.K., Erlich, H.A., McCormick, F., Marshall, C.J., Analysis of RAS gene mutations in acute myeloid leukemia by polymerase chain reaction and oligonucleotide probes (1988) Proc. Natl. Acad. Sci. USA, 85, pp. 1629-1633 Ganis, J.J., Hsia, N., Trompouki, E., de Jong, J.L.O., Dibiase, A., Lambert, J.S., Jia, Z., Zon, L.I., Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR (2012) Dev. Biol., 366, pp. 185-194 Gering, M., Rodaway, A.R., Göttgens, B., Patient, R.K., Green, A.R., The SCL gene specifies haemangioblast development from early mesoderm (1998) EMBO J., 17, pp. 4029-4045 Gilks, C.B., Bear, S.E., Grimes, H.L., Tsichlis, P.N., Progression of interleukin-2 (IL-2)-dependent rat T cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein (1993) Mol. Cell. Biol., 13, pp. 1759-1768 Grimes, H.L., Chan, T.O., Zweidler-Mckay, P.A., Tong, B., Tsichlis, P.N., The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal (1996) Mol. Cell. Biol., 16, pp. 6263-6272 Hock, H., Hamblen, M.J., Rooke, H.M., Schindler, J.W., Saleque, S., Fujiwara, Y., Orkin, S.H., Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells (2004) Nature, 431, pp. 1002-1007 Hock, H., Hamblen, M.J., Rooke, H.M., Traver, D., Bronson, R.T., Cameron, S., Orkin, S.H., Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation (2003) Immunity, 18, pp. 109-120 Hsu, K., Traver, D., Kutok, J.L., Hagen, A., Liu, T.-X., Paw, B.H., Rhodes, J., Look, A.T., The pu.1 promoter drives myeloid gene expression in zebrafish (2004) Blood, 104, pp. 1291-1297 Karsunky, H., Zeng, H., Schmidt, T., Zevnik, B., Kluge, R., Schmid, K.W., Dührsen, U., Möröy, T., Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1 (2002) Nat. Genet., 30, pp. 295-300 Khandanpour, C., Sharif-Askari, E., Vassen, L., Gaudreau, M.-C., Zhu, J., Paul, W.E., Okayama, T., Möröy, T., Evidence that growth factor independence 1b regulates dormancy and peripheral blood mobilization of hematopoietic stem cells (2010) Blood, 116, pp. 5149-5161 Liao, E.C., Trede, N.S., Ransom, D., Zapata, A., Kieran, M., Zon, L.I., Non-cell autonomous requirement for the bloodless gene in primitive hematopoiesis of zebrafish (2002) Development, 129, pp. 649-659 Lieschke, G.J., Oates, A.C., Paw, B.H., Thompson, M.A., Hall, N.E., Ward, A.C., Ho, R.K., Layton, J.E., Zebrafish SPI-1 (PU.1) marks a site of myeloid development independent of primitive erythropoiesis: implications for axial patterning (2002) Dev. Biol., 246, pp. 274-295 Lin, H.-F., Traver, D., Zhu, H., Dooley, K., Paw, B.H., Zon, L.I., Handin, R.I., Analysis of thrombocyte development in CD41-GFP transgenic zebrafish (2005) Blood, 106, pp. 3803-3810 Liu, F., Walmsley, M., Rodaway, A., Patient, R., Fli1 acts at the top of the transcriptional network driving blood and endothelial development (2008) Curr. Biol., 18, pp. 1234-1240 Long, Q., Meng, A., Wang, H., Jessen, J.R., Farrell, M.J., Lin, S., GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene (1997) Development, 124, pp. 4105-4111 Lyons, S.E., Lawson, N.D., Lei, L., Bennett, P.E., Weinstein, B.M., Liu, P.P., A nonsense mutation in zebrafish gata1 causes the bloodless phenotype in vlad tepes (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 5454-5459 Ma, D., Zhang, J., Lin, H.-F., Italiano, J., Handin, R.I., The identification and characterization of zebrafish hematopoietic stem cells (2011) Blood, 118, pp. 289-297 Meeker, N.D., Hutchinson, S.A., Ho, L., Trede, N.S., Method for isolation of PCR-ready genomic DNA from zebrafish tissues (2007) BioTechniques, 43, pp. 610-614 Nilsson, R., Schultz, I.J., Pierce, E.L., Soltis, K.A., Naranuntarat, A., Ward, D.M., Baughman, J.M., Mootha, V.K., Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis (2009) Cell Metab., 10, pp. 119-130 Patterson, L.J., Gering, M., Patient, R., Scl is required for dorsal aorta as well as blood formation in zebrafish embryos (2005) Blood, 105, pp. 3502-3511 Patterson, L.J., Gering, M., Eckfeldt, C.E., Green, A.R., Verfaillie, C.M., Ekker, S.C., Patient, R., The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish (2007) Blood, 109, pp. 2389-2398 Paw, B.H., Moskowitz, S.M., Uhrhammer, N., Wright, N., Kaback, M.M., Neufeld, E.F., Juvenile GM2 gangliosidosis caused by substitution of histidine for arginine at position 499 or 504 of the alpha-subunit of beta-hexosaminidase (1990) J. Biol. Chem., 265, pp. 9452-9457 Pelster, B., Burggren, W.W., Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio) (1996) Circ. Res., 79, pp. 358-362 Person, R.E., Li, F.-Q., Duan, Z., Benson, K.F., Wechsler, J., Papadaki, H.A., Eliopoulos, G., Horwitz, M., Mutations in proto-oncogene GFI1 cause human neutropenia and target ELA2 (2003) Nat. Genet., 34, pp. 308-312 Postlethwait, J., Woods, I., Ngo-Hazelett, P., Yan, Y., Kelly, P., Chu, F., Huang, H., Talbot, W., Zebrafish comparative genomics and the origins of vertebrate chromosomes (2000) Genome Res., 10, p. 1890 Randrianarison-Huetz, V., Laurent, B., Bardet, V., Blobe, G.C., Huetz, F., Duménil, D., Gfi-1B controls human erythroid and megakaryocytic differentiation by regulating TGF-beta signaling at the bipotent erythro-megakaryocytic progenitor stage (2010) Blood, 115, pp. 2784-2795 Rhodes, J., Hagen, A., Hsu, K., Deng, M., Liu, T.-X., Look, A.T., Kanki, J.P., Interplay of pu.1 and gata1 determines myelo-erythroid progenitor cell fate in zebrafish (2005) Dev. Cell, 8, pp. 97-108 Saleque, S., Cameron, S., Orkin, S.H., The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages (2002) Genes Dev., 16, pp. 301-306 Schmidt, T., Karsunky, H., Gau, E., Zevnik, B., Elsässer, H.P., Möröy, T., Zinc finger protein GFI-1 has low oncogenic potential but cooperates strongly with pim and myc genes in T-cell lymphomagenesis (1998) Oncogene, 17, pp. 2661-2667 Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative C(T) method (2008) Nat. Protoc., 3, pp. 1101-1108 Shaw, G.C., Cope, J.J., Li, L., Corson, K., Hersey, C., Ackermann, G.E., Gwynn, B., Paw, B.H., Mitoferrin is essential for erythroid iron assimilation (2006) Nature, 440, pp. 96-100 Sood, R., English, M.A., Belele, C.L., Jin, H., Bishop, K., Haskins, R., McKinney, M.C., Liu, P.P., Development of multilineage adult hematopoiesis in the zebrafish with a runx1 truncation mutation (2010) Blood, 115, pp. 2806-2809 Spooner, C.J., Cheng, J.X., Pujadas, E., Laslo, P., Singh, H., A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates (2009) Immunity, 31, pp. 576-586 Stainier, D.Y., Weinstein, B.M., Detrich, H.W., Zon, L.I., Fishman, M.C., Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages (1995) Development, 121, pp. 3141-3150 Thompson, M.A., Ransom, D.G., Pratt, S.J., MacLennan, H., Kieran, M.W., Detrich, H.W., Vail, B., Zon, L.I., The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis (1998) Dev. Biol., 197, pp. 248-269 van der Meer, L.T., Jansen, J.H., van der Reijden, B.A., Gfi1 and Gfi1b: key regulators of hematopoiesis (2010) Leukemia, 24, pp. 1834-1843 Wallis, D., Hamblen, M., Zhou, Y., Venken, K.J.T., Schumacher, A., Grimes, H.L., Zoghbi, H.Y., Bellen, H.J., The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival (2003) Development, 130, pp. 221-232 Wei, W., Wen, L., Huang, P., Zhang, Z., Chen, Y., Xiao, A., Huang, H., Lin, S., Gfi1.1 regulates hematopoietic lineage differentiation during zebrafish embryogenesis (2008) Cell Res., 18, pp. 677-685 Wilson, N.K., Timms, R.T., Kinston, S.J., Cheng, Y.-H., Oram, S.H., Landry, J.-R., Mullender, J., Gottgens, B., 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 (2010) Mol. Cell. Biol., 30, pp. 3853-3863 Woods, I., Kelly, P., Chu, F., Ngo-Hazelett, P., Yan, Y., Huang, H., Postlethwait, J., Talbot, W., A comparative map of the zebrafish genome (2000) Genome Res., 10, p. 1903 Zeng, H., Yücel, R., Kosan, C., Klein-Hitpass, L., Möröy, T., Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells (2004) EMBO J., 23, pp. 4116-4125