Distinct regulation of the anterior and posterior myeloperoxidase expression by Etv2 and Gata1 during primitive Granulopoiesis in zebrafish

Developmental Biology

Volumn 393, Issue 1, 2014, Pages 149-159

  Glenn, Nicole O ^a   Schumacher, Jennifer A ^a   Kim, Hyon J ^a   Zhao, Emma J ^a   Skerniskyte, Jurate ^a   Sumanas, Saulius ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Er71; Etsrp; Etv2; Gata1; Granulocytes; Myeloid; Neutrophil; Primitive hematopoiesis; Zebrafish

Indexed keywords

MYELOPEROXIDASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETV2; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANTERIOR LATERAL PLATE MESODERM; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GRANULOPOIESIS; HEMATOPOIETIC STEM CELL; MESODERM; NEUTROPHIL; NONHUMAN; POSTERIOR LATERAL PLATE MESODERM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

ER71; ETSRP; ETV2; GATA1; GRANULOCYTES; MYELOID; NEUTROPHIL; PRIMITIVE HEMATOPOIESIS; ZEBRAFISH;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; EMBRYO, NONMAMMALIAN; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HEMATOPOIETIC STEM CELLS; LEUKOPOIESIS; MESODERM; MORPHOLINOS; NEUTROPHILS; PEROXIDASE; PROTO-ONCOGENE PROTEINS; TRANS-ACTIVATORS; TROPONIN T; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84906101188     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.06.011     Document Type: Article

References (55)

1. Bennett C.M., Kanki J.P., Rhodes J., Liu T.X., Paw B.H., Kieran M.W., Langenau D.M., Delahaye-Brown A., Zon L.I., Fleming M.D., Look A.T. Myelopoiesis in the zebrafish, Danio rerio. Blood 2001, 98:643-651.
2. Bertrand J.Y., Kim A.D., Violette E.P., Stachura D.L., Cisson J.L., Traver D. Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development 2007, 134:4147-4156.
3. Bradbury J. Small fish, big science. PLoS Biol. 2004, 2:E148.
4. Brownlie A., Hersey C., Oates A.C., Paw B.H., Falick A.M., Witkowska H.E., Flint J., Higgs D., Jessen J., Bahary N., Zhu H., Lin S., Zon L. Characterization of embryonic globin genes of the zebrafish. Dev. Biol. 2003, 255:48-61.
5. Burns C.E., Galloway J.L., Smith A.C., Keefe M.D., Cashman T.J., Paik E.J., Mayhall E.A., Amsterdam A.H., Zon L.I. A genetic screen in zebrafish defines a hierarchical network of pathways required for hematopoietic stem cell emergence. Blood 2009, 113:5776-5782.
6. Clay H., Davis J.M., Beery D., Huttenlocher A., Lyons S.E., Ramakrishnan L. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2007, 2:29-39.
7. Davidson A.J., Zon L.I. The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene 2004, 23:7233-7246.
8. Detrich H.W., Kieran M.W., Chan F.Y., Barone L.M., Yee K., Rundstadler J.A., Pratt S., Ransom D., Zon L.I. Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. USA 1995, 92:10713-10717.
9. Dooley K.A., Davidson A.J., Zon L.I. Zebrafish scl functions independently in hematopoietic and endothelial development. Dev. Biol. 2005, 277:522-536.
10. Ferdous A., Caprioli A., Iacovino M., Martin C.M., Morris J., Richardson J.A., Latif S., Hammer R.E., Harvey R.P., Olson E.N., Kyba M., Garry D.J. Nkx2-5 transactivates the Ets-related protein 71 gene and specifies an endothelial/endocardial fate in the developing embryo. Proc. Natl. Acad. Sci. USA 2009, 106:814-819.
11. Fujiwara Y., Browne C.P., Cunniff K., Goff S.C., Orkin S.H. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc. Natl. Acad. Sci. USA 1996, 93:12355-12358.
12. Galloway J.L., Wingert R.A., Thisse C., Thisse B., Zon L.I. Loss of gata1 but not gata2 converts erythropoiesis to myelopoiesis in zebrafish embryos. Dev. Cell 2005, 8:109-116.
13. Galloway J.L., Zon L.I. Ontogeny of hematopoiesis: examining the emergence of hematopoietic cells in the vertebrate embryo. Curr. Top. Dev. Biol. 2003, 53:139-158.
14. Hall C., Crosier P. Editorial: maintaining the balance-fishing for drugs to treat persistent neutrophilic inflammation. J. Leukoc. Biol. 2010, 87:189-191.
15. Herbomel P., Thisse B., Thisse C. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 1999, 126:3735-3745.
16. Hsia N., Zon L.I. Transcriptional regulation of hematopoietic stem cell development in zebrafish. Exp. Hematol. 2005, 33:1007-1014.
17. Jin H., Li L., Xu J., Zhen F., Zhu L., Liu P.P., Zhang M., Zhang W., Wen Z. Runx1 regulates embryonic myeloid fate choice in zebrafish through a negative feedback loop inhibiting Pu.1 expression. Blood 2012, 119:5239-5249.
18. Jowett T. Analysis of protein and gene expression. Methods Cell Biol. 1999, 59:63-85.
19. Kataoka H., Hayashi M., Nakagawa R., Tanaka Y., Izumi N., Nishikawa S., Jakt M.L., Tarui H., Nishikawa S. Etv2/ER71 induces vascular mesoderm from Flk1+PDGFRalpha+ primitive mesoderm. Blood 2011, 118:6975-6986.
20. Kimmel C.B., Warga R.M., Schilling T.F. Origin and organization of the zebrafish fate map. Development 1990, 108:581-594.
21. Kohli V., Schumacher J.A., Desai S.P., Rehn K., Sumanas S. Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev. Cell 2013, 25:196-206.
22. Lakshman R., Finn A. Neutrophil disorders and their management. J. Clin. Pathol. 2001, 54:7-19.
23. Lawson N.D., Weinstein B.M. in vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
24. Le Guyader D., Redd M.J., Colucci-Guyon E., Murayama E., Kissa K., Briolat V., Mordelet E., Zapata A., Shinomiya H., Herbomel P. Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 2008, 111:132-141.
25. Lee D., Kim T., Lim D.S. The Er71 is an important regulator of hematopoietic stem cells in adult mice. Stem Cells 2011, 29:539-548.
26. Lee D., Park C., Lee H., Lugus J.J., Kim S.H., Arentson E., Chung Y.S., Gomez G., Kyba M., Lin S., Janknecht R., Lim D.S., Choi K. ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2008, 2:497-507.
27. Li L., Jin H., Xu J., Shi Y., Wen Z. Irf8 regulates macrophage versus neutrophil fate during zebrafish primitive myelopoiesis. Blood 2011, 117:1359-1369.
28. Liao E.C., Paw B.H., Oates A.C., Pratt S.J., Postlethwait J.H., Zon L.I. SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev. 1998, 12:621-626.
29. Lieschke G.J., Oates A.C., Crowhurst M.O., Ward A.C., Layton J.E. Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 2001, 98:3087-3096.
30. Lieschke G.J., Oates A.C., Paw B.H., Thompson M.A., Hall N.E., Ward A.C., Ho R.K., Zon L.I., Layton J.E. Zebrafish SPI-1 (PU.1) marks a site of myeloid development independent of primitive erythropoiesis: implications for axial patterning. Dev. Biol. 2002, 246:274-295.
31. Liu F., Wen Z. Cloning and expression pattern of the lysozyme C gene in zebrafish. Mechan. Dev. 2002, 113:69-72.
32. Lyons S.E., Shue B.C., Lei L., Oates A.C., Zon L.I., Liu P.P. Molecular cloning, genetic mapping, and expression analysis of four zebrafish c/ebp genes. Gene 2001, 281:43-51.
33. Mathias J.R., Perrin B.J., Liu T.X., Kanki J., Look A.T., Huttenlocher A. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 2006, 80:1281-1288.
34. McKercher S.R., Torbett B.E., Anderson K.L., Henkel G.W., Vestal D.J., Baribault H., Klemsz M., Feeney A.J., Wu G.E., Paige C.J., Maki R.A. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 1996, 15:5647-5658.
35. Meijer A.H., van der Sar A.M., Cunha C., Lamers G.E., Laplante M.A., Kikuta H., Bitter W., Becker T.S., Spaink H.P. Identification and real-time imaging of a myc-expressing neutrophil population involved in inflammation and mycobacterial granuloma formation in zebrafish. Dev. Comp. Immunol. 2008, 32:36-49.
36. Murayama E., Kissa K., Zapata A., Mordelet E., Briolat V., Lin H.F., Handin R.I., Herbomel P. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 2006, 25:963-975.
37. Pase L., Layton J.E., Wittmann C., Ellett F., Nowell C.J., Reyes-Aldasoro C.C., Varma S., Rogers K.L., Hall C.J., Keightley M.C., Crosier P.S., Grabher C., Heath J.K., Renshaw S.A., Lieschke G.J. Neutrophil-delivered myeloperoxidase dampens the hydrogen peroxide burst after tissue wounding in zebrafish. Curr. Biol. 2012, 22:1818-1824.
38. Patterson L.J., Gering M., Patient R. Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 2005, 105:3502-3511.
39. Pham V.N., Lawson N.D., Mugford J.W., Dye L., Castranova D., Lo B., Weinstein B.M. Combinatorial function of ETS transcription factors in the developing vasculature. Dev. Biol. 2007, 303:772-783.
40. Proulx K., Lu A., Sumanas S. Cranial vasculature in zebrafish forms by angioblast cluster-derived angiogenesis. Dev. Biol. 2010, 348:34-46.
41. 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. Dev. Cell 2005, 8:97-108.
42. Robb L., Lyons I., Li R., Hartley L., Kontgen F., Harvey R.P., Metcalf D., Begley C.G. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci.USA 1995, 92:7075-7079.
43. Scott E.W., Simon M.C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 1994, 265:1573-1577.
44. Sehnert A.J., Huq A., Weinstein B.M., Walker C., Fishman M., Stainier D.Y. Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 2002, 31:106-110.
45. Shivdasani R.A., Mayer E.L., Orkin S.H. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 1995, 373:432-434.
46. Sumanas S., Gomez G., Zhao Y., Park C., Choi K., Lin S. Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 2008, 111:4500-4510.
47. Sumanas S., Jorniak T., Lin S. Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants. Blood 2005, 106:534-541.
48. Sumanas S., Lin S. Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol. 2006, 4:e10.
49. Thompson M.A., Ransom D.G., Pratt S.J., MacLennan H., Kieran M.W., Detrich H.W., Vail B., Huber T.L., Paw B., Brownlie A.J., Oates A.C., Fritz A., Gates M.A., Amores A., Bahary N., Talbot W.S., Her H., Beier D.R., Postlethwait J.H., Zon L.I. The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev. Biol. 1998, 197:248-269.
50. Trinh le A., McCutchen M.D., Bonner-Fraser M., Fraser S.E., Bumm L.A., McCauley D.W. Fluorescent in situ hybridization employing the conventional NBT/BCIP chromogenic stain. Biotechniques 2007, 42:756-759.
51. Vogeli K.M., Jin S.W., Martin G.R., Stainier D.Y. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 2006, 443:337-339.
52. Warga R.M., Kane D.A., Ho R.K. Fate mapping embryonic blood in zebrafish: multi- and unipotential lineages are segregated at gastrulation. Dev. Cell 2009, 16:744-755.
53. Westerfield M. The Zebrafish Book 2007, Monte Westerfield, Eugene, OR. 5th ed.
54. Xu J., Du L., Wen Z. Myelopoiesis during zebrafish early development. J. Genet. Genom.=Yi chuan xue bao 2012, 39:435-442.
55. Zhang P., Behre G., Pan J., Iwama A., Wara-Aswapati N., Radomska H.S., Auron P.E., Tenen D.G., Sun Z. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc. Natl. Acad. Sci. USA 1999, 96:8705-8710.