In vivo</italic> imaging of hematopoietic stem cell development in the zebrafish

doi:10.1007/s11684-011-0123-0

Front Med

2011, Vol. 5

Issue (3) : 239-247 https://doi.org/10.1007/s11684-011-0123-0

REVIEW

In vivo imaging of hematopoietic stem cell development in the zebrafish

Panpan Zhang, Feng Liu(

)

State Key Laboratory of Biomembrane and Membrane Biotechnology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

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Abstract

In vivo imaging is crucial for developmental biology and can further help to follow cell development/differentiation in normal and pathological conditions. Recent advances in optical imaging techniques has facilitated tracing of the developmental dynamics of a specific organ, tissue, or even a single cell. The zebrafish is an excellent model for imaging of hematopoiesis due to its transparent embryo at early stage; moreover, different zebrafish hematopoietic stem cells (HSCs) transgenic lines have been demonstrated as very useful tools for illustrating the details of the HSC developmental process. In this review, we summarize recent studies related to the non-invasive in vivo imaging of HSC transgenics, to show that zebrafish transgenic lines are powerful tools for developmental biology and disease. At the end of the review, the perspective and some open questions in this field will be discussed.

Keywords hematopoietic stem cell hematopoiesis in vivo imaging transgenics zebrafish

Corresponding Author(s): Liu Feng,Email:liuf@ioz.ac.cn

Issue Date: 05 September 2011

Cite this article:

Panpan Zhang,Feng Liu. In vivo imaging of hematopoietic stem cell development in the zebrafish[J]. Front Med, 2011, 5(3): 239-247.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-011-0123-0
https://academic.hep.com.cn/fmd/EN/Y2011/V5/I3/239

Tab.1 A brief summary of primitive and definitive hematopoiesis in zebrafish

Fig.1 Comparison of conventional and confocal microscopy used in zebrafish embryo imaging. (A) Bright-field imaging of a 36 hpf zebrafish embryo. Lateral view, anterior to the left. (B, C) Fluorescent imaging of the same embryos ) showing green blood vessels. Lateral view, anterior to the left. (D, E) Confocal imaging of embryo at day 2 using Zeiss LSM 510 showing 3D structures of blood vessels in green. Lateral view, anterior to the left.

Fig.2 Hematopoiesis is closely associated with vessel development in zebrafish. (A) Whole mount hybridization of , a hemangioblast marker, in lateral plate mesoderm at 5 somite stage. Dorsal view, anterior to the top. (B)-positive cells mark angioblasts migrating to the midline at 18 somite stage. Dorsal view, anterior to the top. (C) staining demarcates artery and vein at 24 hs postfertilization (hpf). Lateral view, anterior to the left. (D) At 36 hpf, positive cells represent hematopoietic stem cells (arrow) which were derived from the dorsal aorta. Lateral view, anterior to the left.

Tab.2 Molecular markers and available transgenic lines in zebrafish hematopoiesis

Fig.3 Bright-field (A) and 3D confocal (B) images of transgenic zebrafish embryo show GFP expression in blood and blood vessels within the whole embryo at 30 h postfertilization (hpf).

1	Zon LI. Developmental biology of hematopoiesis. Blood 1995; 86(8): 2876–2891 pmid:7579378
2	Ingham PW. The power of the zebrafish for disease analysis. Hum Mol Genet 2009; 18(R1): R107–R112 doi: 10.1093/hmg/ddp091 pmid:19297397
3	de Jong JL, Zon LI. Use of the zebrafish system to study primitive and definitive hematopoiesis. Annu Rev Genet 2005; 39(1): 481–501 doi: 10.1146/annurev.genet.39.073003.095931 pmid:16285869
4	Amatruda JF, Zon LI. Dissecting hematopoiesis and disease using the zebrafish. Dev Biol 1999; 216(1): 1–15 doi: 10.1006/dbio.1999.9462 pmid:10588859
5	Ciau-Uitz A, Liu F, Patient R. Genetic control of hematopoietic development in Xenopus and zebrafish. Int J Dev Biol 2010; 54(6-7): 1139–1149 doi: 10.1387/ijdb.093055ac pmid:20711991
6	Chen AT, Zon LI. Zebrafish blood stem cells. J Cell Biochem 2009; 108(1): 35–42 doi: 10.1002/jcb.22251 pmid:19565566
7	Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 2010; 464(7285): 108–111 doi: 10.1038/nature08738 pmid:20154733
8	Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010; 464(7285): 116–120 doi: 10.1038/nature08764 pmid:20154729
9	Kissa K, Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 2010; 464(7285): 112–115 doi: 10.1038/nature08761 pmid:20154732
10	Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, Lin HF, Handin RI, Herbomel P. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 2006; 25(6): 963–975 doi: 10.1016/j.immuni.2006.10.015 pmid:17157041
11	Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008; 132(4): 631–644 doi: 10.1016/j.cell.2008.01.025 pmid:18295580
12	Ntziachristos V. Going deeper than microscopy: the optical imaging frontier in biology. Nat Methods 2010; 7(8): 603–614 doi: 10.1038/nmeth.1483 pmid:20676081
13	Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 1990; 248(4951): 73–76 doi: 2321027" target="_blank">10.1126/science. pmid:2321027 pmid:2321027
14	Shi X, Teo LS, Pan X, Chong SW, Kraut R, Korzh V, Wohland T. Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy. Dev Dyn 2009; 238(12): 3156–3167 doi: 10.1002/dvdy.22140 pmid:19882725
15	Kimmel CB, Warga RM, Schilling TF. Origin and organization of the zebrafish fate map. Development 1990; 108(4): 581–594 pmid:2387237
16	Warga RM, Kimmel CB. Cell movements during epiboly and gastrulation in zebrafish. Development 1990; 108(4): 569–580 pmid:2387236
17	Vogeli KM, Jin SW, Martin GR, Stainier DY. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 2006; 443(7109): 337–339 doi: 10.1038/nature05045 pmid:16988712
18	Hatta K, Tsujii H, Omura T. Cell tracking using a photoconvertible fluorescent protein. Nat Protoc 2006; 1(2): 960–967 doi: 10.1038/nprot.2006.96 pmid:17406330
19	Collins RT, Linker C, Lewis J. MAZe: a tool for mosaic analysis of gene function in zebrafish. Nat Methods 2010; 7(3): 219–223 doi: 10.1038/nmeth.1423 pmid:20139970
20	Detrich HW 3rd, Kieran MW, Chan FY, Barone LM, Yee K, Rundstadler JA, Pratt S, Ransom D, Zon LI. Intraembryonic hematopoietic cell migration during vertebrate development. Proc Natl Acad Sci USA 1995; 92(23): 10713–10717 doi: 10.1073/pnas.92.23.10713 pmid:7479870
21	Davidson AJ, Ernst P, Wang Y, Dekens MP, Kingsley PD, Palis J, Korsmeyer SJ, Daley GQ, Zon LI. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 2003; 425(6955): 300–306 doi: 10.1038/nature01973 pmid:13679919
22	Kalev-Zylinska ML, Horsfield JA, Flores MV, Postlethwait JH, Vitas MR, Baas AM, Crosier PS, Crosier KE. Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis. Development 2002; 129(8): 2015–2030 doi: 10.1016/j.devcel.2005.01.010 pmid:15737934
23	Liu F, Wen Z. Cloning and expression pattern of the lysozyme C gene in zebrafish. Mech Dev 2002; 113(1): 69–72 doi: 10.1016/S0925-4773(01)00658-X pmid:11900976
24	Patterson LJ, Gering M, Eckfeldt CE, Green AR, Verfaillie CM, Ekker SC, Patient R. The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish. Blood 2007; 109(6): 2389–2398 doi: 10.1182/blood-2006-02-003087 pmid:17090656
25	Fouquet B, Weinstein BM, Serluca FC, Fishman MC. Vessel patterning in the embryo of the zebrafish: guidance by notochord. Dev Biol 1997; 183(1): 37–48 doi: 10.1006/dbio.1996.8495 pmid:9119113
26	Gering M, Patient R. Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev Cell 2005; 8(3): 389–400 doi: 10.1016/j.devcel.2005.01.010 pmid:15737934
27	Wilkinson RN, Pouget C, Gering M, Russell AJ, Davies SG, Kimelman D, Patient R. Hedgehog and Bmp polarize hematopoietic stem cell emergence in the zebrafish dorsal aorta. Dev Cell 2009; 16(6): 909–916 doi: 10.1016/j.devcel.2009.04.014 pmid:19531361
28	Liu F, Walmsley M, Rodaway A, Patient R. Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 2008; 18(16): 1234–1240 doi: 10.1016/j.cub.2008.07.048 pmid:18718762
29	Lawson ND, Vogel AM, Weinstein BM. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell 2002; 3(1): 127–136 doi: 10.1016/S1534-5807(02)00198-3 pmid:12110173
30	Burns CE, Galloway JL, Smith AC, Keefe MD, Cashman TJ, Paik EJ, Mayhall EA, Amsterdam AH, Zon LI. A genetic screen in zebrafish defines a hierarchical network of pathways required for hematopoietic stem cell emergence. Blood 2009; 113(23): 5776–5782 doi: 10.1182/blood-2008-12-193607 pmid:19332767
31	Burns CE, Traver D, Mayhall E, Shepard JL, Zon LI. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev 2005; 19(19): 2331–2342 doi: 10.1101/gad.1337005 pmid:16166372
32	Kissa K, Murayama E, Zapata A, Cortés A, Perret E, Machu C, Herbomel P. Live imaging of emerging hematopoietic stem cells and early thymus colonization. Blood 2008; 111(3): 1147–1156 doi: 10.1182/blood-2007-07-099499 pmid:17934068
33	Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 2009; 457(7231): 887–891 doi: 10.1038/nature07619 pmid:19129762
34	Lin HF, Traver D, Zhu H, Dooley K, Paw BH, Zon LI, Handin RI. Analysis of thrombocyte development in CD41-GFP transgenic zebrafish. Blood 2005; 106(12): 3803–3810 doi: 10.1182/blood-2005-01-0179 pmid:16099879
35	Bertrand JY, Kim AD, Teng S, Traver D. CD41+ cmyb+ precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis. Development 2008; 135(10): 1853–1862 doi: 10.1242/dev.015297 pmid:18417622
36	North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang IH, Grosser T, Fitzgerald GA, Daley GQ, Orkin SH, Zon LI. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 2007; 447(7147): 1007–1011 doi: 10.1038/nature05883 pmid:17581586
37	Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 2002; 248(2): 307–318 doi: 10.1006/dbio.2002.0711 pmid:12167406
38	Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 2005; 132(23): 5199–5209 doi: 10.1242/dev.02087 pmid:16251212
39	Long Q, Meng A, Wang H, Jessen JR, Farrell MJ, Lin S. GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. Development 1997; 124(20): 4105–4111 pmid:9374406
40	Jessen JR, Meng A, McFarlane RJ, Paw BH, Zon LI, Smith GR, Lin S. Modification of bacterial artificial chromosomes through chi-stimulated homologous recombination and its application in zebrafish transgenesis. Proc Natl Acad Sci USA 1998; 95(9): 5121–5126 doi: 10.1073/pnas.95.9.5121 pmid:9560239
41	Bajoghli B, Ramialison M, Aghaallaei N, Czerny T, Wittbrodt J. Identification of starmaker-like in medaka as a putative target gene of Pax2 in the otic vesicle. Dev Dyn 2009; 238(11): 2860–2866 doi: 10.1002/dvdy.22093 pmid:19795520
42	Bertrand JY, Kim AD, Violette EP, Stachura DL, Cisson JL, Traver D. Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development 2007; 134(23): 4147–4156 doi: 10.1016/j.ydbio.2005.01.034 pmid:15893977
43	Hsu K, Traver D, Kutok JL, Hagen A, Liu TX, Paw BH, Rhodes J, Berman JN, Zon LI, Kanki JP, Look AT. The pu.1 promoter drives myeloid gene expression in zebrafish. Blood 2004; 104(5): 1291–1297 doi: 10.1182/blood-2003-09-3105 pmid:14996705
44	Lam EY, Chau JY, Kalev-Zylinska ML, Fountaine TM, Mead RS, Hall CJ, Crosier PS, Crosier KE, Flores MV. Zebrafish runx1 promoter-EGFP transgenics mark discrete sites of definitive blood progenitors. Blood 2009; 113(6): 1241–1249 doi: 10.1182/blood-2008-04-149898 pmid:18927441
45	Zhang XY, Rodaway AR. SCL-GFP transgenic zebrafish: in vivo imaging of blood and endothelial development and identification of the initial site of definitive hematopoiesis. Dev Biol 2007; 307(2): 179–194 doi: 10.1016/j.ydbio.2007.04.002 pmid:17559829
46	Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J, Joly JS. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 2002; 118(1-2): 91–98 doi: 10.1016/S0925-4773(02)00218-6 pmid:12351173
47	Kawakami K, Shima A, Kawakami N. Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc Natl Acad Sci USA 2000; 97(21): 11403–11408 doi: 10.1073/pnas.97.21.11403 pmid:11027340
48	Kawakami K. Transposon tools and methods in zebrafish. Dev Dyn 2005; 234(2): 244–254 doi: 10.1002/dvdy.20516 pmid:16110506
49	Liu F, Patient R. Genome-wide analysis of the zebrafish ETS family identifies three genes required for hemangioblast differentiation or angiogenesis. Circ Res 2008; 103(10): 1147–1154 doi: 10.1161/CIRCRESAHA.108.179713 pmid:18832752
50	Jin H, Xu J, Wen Z. Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development. Blood 2007; 109(12): 5208–5214 doi: 10.1182/blood-2007-01-069005 pmid:17327398
51	Ng CE, Yokomizo T, Yamashita N, Cirovic B, Jin H, Wen Z, Ito Y, Osato M. A Runx1 intronic enhancer marks hemogenic endothelial cells and hematopoietic stem cells. Stem Cells 2010; 28(10): 1869–1881 doi: 10.1002/stem.507 pmid:20799333
52	Zhu H, Traver D, Davidson AJ, Dibiase A, Thisse C, Thisse B, Nimer S, Zon LI. Regulation of the lmo2 promoter during hematopoietic and vascular development in zebrafish. Dev Biol 2005; 281(2): 256–269 doi: 10.1016/j.ydbio.2005.01.034 pmid:15893977
53	Bertrand JY, Giroux S, Golub R, Klaine M, Jalil A, Boucontet L, Godin I, Cumano A. Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc Natl Acad Sci USA 2005; 102(1): 134–139 doi: 10.1073/pnas.0402270102 pmid:15623562
54	Finley KR, Davidson AE, Ekker SC. Three-color imaging using fluorescent proteins in living zebrafish embryos. Biotechniques 2001; 31(1): 66–70 pmid:11464522
55	Beis D, Stainier DY. In vivo cell biology: following the zebrafish trend. Trends Cell Biol 2006; 16(2): 105–112 doi: 10.1016/j.tcb.2005.12.001 pmid:16406520

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