ZFIN ID: ZDB-LAB-980414-2
Robert Ho Lab
PI/Director: Ho, Robert K.
Contact Person:
Email: dmjonesm@midway.uchicago.edu
Address: Department of Organismal Biology and Anatomy University of Chicago 1027 East 57th Street Chicago, IL 60637 USA
Country: United States
Phone: (773) 834-8422
Fax: (773) 834-3028
Line Designation: ch

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Embryonic development of the zebrafish, Danio rerio.

The embryo of the zebrafish is an excellent preparation in which to study many aspects of development. Cells of zebrafish are relatively large, optically clear, and accessible at all stages of development to experimental manipulations such as the microinjection of lineage tracer molecules, cell ablations, and cell transplantations. The zebrafish embryo also has a strong background of genetic analyses, and several interesting mutations have been isolated. In addition, many molecular techniques are becoming increasingly routine in the zebrafish system.

Because zebrafish embryos are optically transparent, it is easy to label individual cells with fluorescent lineage tracers
and follow their development using low light level video time-lapse techniques. By using these methods, Kimmel and his coworkers were able to construct a "fate map" for the zebrafish at gastrulation. A fate map, which is a puzzling together of the various cell lineages of an organism, allows one to accurately predict the identity of the progeny cells produced by a given precursor cell, and therefore is a useful reference model for normal development.

We are interested in understanding how and when individual cells of the early embryo become "committed," that is, irreversibly restricted to expressing a particular cellular identity. The elucidation of the zebrafish fate map has allowed us to perform precise and reproducible
experimental manipulations for the purpose of disturbing the normal cellular processes in defined ways. By studying the effects of these
manipulations on development, we hope to gain insights into the manner by which cellular identity is specified and maintained.

For instance, we now have techniques to transplant individual embryonic cells from one fate map region of a labeled donor embryo to a different region within an unlabeled host. The purpose of these manipulations is to see if the transplanted cell would later express a fate appropriate for its new position (in which case it was still pluripotent and uncomitted to any particular fate), or if it would retain the fate of its original position even though moved to a new location (in which case it could be characterized as committed to its original fate). By extending these types of analyses to later and later stages in development and by proceeding in a flow-chart like manner from very general cases(commitment between mesoderm and ectoderm), to very specific distinctions (commitment between different types of neurons), an organized pattern of differentiation can be conceptualized. By systematically testing the in vivo responses of cells to various conditions at different times in development, we hope to better understand how cell identity is conferred and how a vertebrate, such as the zebrafish, organizes the emergence of its complex body plan.

Another tool we can use in the study of cell identity is the isolation and characterization of mutations that affect the patterning of the zebrafish body plan. For example, the spadetail mutant specifically lacks segmented somites in the trunk region; the no tail mutant fails to form a differentiated notochord; and the cyclops mutantlacks a specialized group of ventral cells in the neural tube called floor plate cells. We plan to further characterize these and similar mutations using a variety of embryological and molecular techniques in order to better understand the cellular and biochemical interactions that lead to the expression of definitive cell fates.

Ahn, Dae-gwon Post-Doc Byrd, Shannon Graduate Student Vickers, Sarah Graduate Student

Mao, L.M.F., Boyle Anderson, E.A.T., Ho, R.K. (2021) Anterior lateral plate mesoderm gives rise to multiple tissues and requires tbx5a function in left-right asymmetry, migration dynamics, and cell specification of late-addition cardiac cells. Developmental Biology. 472:52-66
Quintanilla, C.A., Ho, R.K. (2020) The Cdx transcription factors and retinoic acid play parallel roles in antero-posterior position of the pectoral fin field during gastrulation. Mechanisms of Development. 164:103644
Boyle Anderson, E.A.T., Ho, R.K. (2018) A transcriptomics analysis of the Tbx5 paralogues in zebrafish. PLoS One. 13:e0208766
Steimle, J.D., Rankin, S.A., Slagle, C.E., Bekeny, J., Rydeen, A.B., Chan, S.S., Kweon, J., Yang, X.H., Ikegami, K., Nadadur, R.D., Rowton, M., Hoffmann, A.D., Lazarevic, S., Thomas, W., Boyle Anderson, E.A.T., Horb, M.E., Luna-Zurita, L., Ho, R.K., Kyba, M., Jensen, B., Zorn, A.M., Conlon, F.L., Moskowitz, I.P. (2018) Evolutionarily conserved Tbx5-Wnt2/2b pathway orchestrates cardiopulmonary development.. Proceedings of the National Academy of Sciences of the United States of America. 115(45):E10615-E10624
Zhao, B.S., Wang, X., Beadell, A.V., Lu, Z., Shi, H., Kuuspalu, A., Ho, R.K., He, C. (2017) m6A-dependent maternal mRNA clearance facilitates zebrafish maternal-to-zygotic transition.. Nature. 542(7642):475-478
Chang, J., Skromne, I., Ho, R.K. (2016) CDX4 and retinoic acid interact to position the hindbrain-spinal cord transition. Developmental Biology. 410(2):178-89
Mao, Q., Stinnett, H.K., Ho, R.K. (2015) Asymmetric cell convergence-driven fin bud initiation and pre-pattern requires Tbx5a control of a mesenchymal Fgf signal. Development (Cambridge, England). 142(24):4329-39
Warga, R.M., Mueller, R.L., Ho, R.K., and Kane, D.A. (2013) Zebrafish Tbx16 regulates intermediate mesoderm cell fate by attenuating Fgf activity. Developmental Biology. 383(1):75-89
Ahn, D., You, K.H., and Kim, C.H. (2012) Evolution of the Tbx6/16 Subfamily Genes in Vertebrates: Insights from Zebrafish. Mol. Biol. Evol.. 29(12):3959-3983
Green, M.H., Ho, R.K., and Hale, M.E. (2011) Movement and function of the pectoral fins of the larval zebrafish (Danio rerio) during slow swimming. The Journal of experimental biology. 214(18):3111-3123
Kim, H.T., So, J.H., Jung, S.H., Ahn, D.G., Koh, W., Kim, N.S., Kim, S.H., Lee, S., and Kim, C.H. (2011) Cug2 is essential for normal mitotic control and CNS development in zebrafish. BMC Developmental Biology. 11(1):49
Kim, H.T., Lee, M.S., Choi, J.H., Jung, J.Y., Ahn, D.G., Yeo, S.Y., Choi, D.K., and Kim, C.H. (2011) The microcephaly gene aspm is involved in brain development in zebrafish. Biochemical and Biophysical Research Communications. 409(4):640-4
Mueller, R.L., Huang, C., and Ho, R.K. (2010) Spatio-temporal regulation of Wnt and retinoic acid signaling by tbx16/spadetail during zebrafish mesoderm differentiation. BMC Genomics. 11:492
Elsen, G.E., Choi, L.Y., Prince, V.E., and Ho, R.K. (2009) The autism susceptibility gene met regulates zebrafish cerebellar development and facial motor neuron migration. Developmental Biology. 335(1):78-92
Warga, R.M., Kane, D.A., and Ho, R.K. (2009) Fate mapping embryonic blood in zebrafish: multi- and unipotential lineages are segregated at gastrulation. Developmental Cell. 16(5):744-755
Ahn, D., and Ho, R.K. (2008) Tri-phasic expression of posterior Hox genes during development of pectoral fins in zebrafish: Implications for the evolution of vertebrate paired appendages. Developmental Biology. 322(1):220-233
Skromne, I., Thorsen, D., Hale, M., Prince, V.E., and Ho, R.K. (2007) Repression of the hindbrain developmental program by Cdx factors is required for the specification of the vertebrate spinal cord. Development (Cambridge, England). 134(11):2147-2158
Walton, R.Z., Bruce, A.E., Olivey, H.E., Najib, K., Johnson, V., Earley, J.U., Ho, R.K., and Svensson, E.C. (2006) Fog1 is required for cardiac looping in zebrafish. Developmental Biology. 289(2):482-493
Oates, A.C., Rohde, L.A., and Ho, R.K. (2005) Generation of segment polarity in the paraxial mesoderm of the zebrafish through a T-box-dependent inductive event. Developmental Biology. 283(1):204-214
Bruce, A.E., Howley, C., Dixon Fox, M., and Ho, R.K. (2005) T-box gene eomesodermin and the homeobox-containing Mix/Bix gene mtx2 regulate epiboly movements in the zebrafish. Developmental dynamics : an official publication of the American Association of Anatomists. 233(1):105-114
Oates, A.C., Mueller, C., and Ho, R.K. (2005) Cooperative function of deltaC and her7 in anterior segment formation. Developmental Biology. 280(1):133-149
Byrd, S.M. (2005) Post-transcriptional regulation of maternal RNA in zebrafish : restriction of nanos1 to the primordial germ cells via an EDEN/EDEN-BP-like mechanism. Ph.D. Thesis. :107p
Rohde, L.A., Oates, A.C., and Ho, R.K. (2004) A Crucial Interaction between Embryonic Red Blood Cell Progenitors and Paraxial Mesoderm Revealed in spadetail Embryos. Developmental Cell. 7(2):251-262
Bruce, A.E., Howley, C., Zhou, Y., Vickers, S.L., Silver, L.M., King, M.L., and Ho, R.K. (2003) The maternally expressed zebrafish T-box gene eomesodermin regulates organizer formation. Development (Cambridge, England). 130(22):5503-5517
Piotrowski, T., Ahn, D.-G., Schilling, T.F., Nair, S., Ruvinsky, I., Geisler, R., Rauch, G.-J., Haffter, P., Zon, L.I., Zhou, Y., Foott, H., Dawid, I.B., and Ho, R.K. (2003) The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development (Cambridge, England). 130(20):5043-5052
Byrd, S.M. and Ho, R.K. (2002) The role of bruno-like in early zebrafish development. Developmental Biology. 247(2):466-467
Oates, A.C. and Ho, R.K. (2002) Redundancy between components of the segmentation oscillator and the Delta/Notch pathway protects the anterior somites of zebrafish from genetic perturbation. Developmental Biology. 247(2):516
Skromne, I., Kikuchi, Y., Stainier, D., and Ho, R.K. (2002) The para-hox gene caudal is required for tail formation in zebrafish. Developmental Biology. 247(2):472-473
Lieschke, G.J., Oates, A.C., Paw, B.H., Thompson, M.A., Hall, N.E., Ward, A.C., Ho, R.K., Zon, L.I., and Layton, J.E. (2002) Zebrafish SPI-1 (PU.1) marks a site of myeloid development independent of primitive erythropoiesis: implications for axial patterning. Developmental Biology. 246(2):274-295
Ahn, D.-G., Kourakis, M.J., Rohde, L.A., Silver, L.M., and Ho, R.K. (2002) T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature. 417(6890):754-758
Oates, A.C. and Ho, R.K. (2002) Hairy/E(spl)-related (Her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish. Development (Cambridge, England). 129(12):2929-2946
Keegan, B.R., Feldman, J.L., Lee, D.H., Koos, D.S., Ho, R.K., Stainier, D.Y., and Yelon, D. (2002) The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo. Development (Cambridge, England). 129(7):1623-1632
Oates, A.C., Pratt, S.J., Vail, B., Yan, Y.-L., Ho, R.K., Johnson, S.L., Postlethwait, J.H., and Zon, L.I. (2001) The zebrafish klf gene family. Blood. 98(6):1792-1801
Prince, V.E., Holley, S.A., Bally-Cuif, L., Prabhakaran, B., Oates, A.C., Ho, R.K., and Vogt, T.F. (2001) Zebrafish lunatic fringe demarcates segmental boundaries. Mechanisms of Development. 105(1-2):175-180
Bruce, A.E., Oates, A.C., Prince, V.E., and Ho, R.K. (2001) Additional hox clusters in the zebrafish: divergent expression patterns belie equivalent activities of duplicate hoxB5 genes. Evolution & development. 3(3):127-144
Oates, A.C., Bruce, A.E., and Ho, R.K. (2000) Too much interference: injection of double-stranded RNA has nonspecific effects in the zebrafish embryo. Developmental Biology. 224(1):20-28
Ahn, D., Ruvinsky, I., Oates, A.C., Silver, L.M., and Ho, R.K. (2000) tbx20, a new vertebrate T-box gene expressed in the cranial motor neurons and developing cardiovascular structures in zebrafish. Mechanisms of Development. 95(1-2):253-258
Yelon, D., Ticho, B., Halpern, M.E., Ruvinsky, I., Ho, R.K., Silver, L.M., and Stainier, D.Y. (2000) The bHLH transcription factor Hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development (Cambridge, England). 127(12):2573-2582
Howley, C. and Ho, R.K. (2000) mRNA localization patterns in zebrafish oocytes. Mechanisms of Development. 92(2):305-309
Ruvinsky, I., Oates, A.C., Silver, L.M., and Ho, R.K. (2000) The evolution of paired appendages in vertebrates: T-box genes in the zebrafish. Development genes and evolution. 210(2):82-91
Koos, D.S. and Ho, R.K. (1999) The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula. Developmental Biology. 215(2):190-207
Ahn, D. and Gibson, G. (1999) Expression patterns of threespine stickleback hox genes and insights into the evolution of the vertebrate body axis. Development genes and evolution. 209(8):482-494
Roy, M.N., Prince, V.E., and Ho, R.K. (1999) Heat shock produces periodic somitic disturbances in the zebrafish embryo. Mechanisms of Development. 85(1-2):27-34
Bruce, A.E.E., Prince, V.E., and Ho, R.K. (1999) Comparison of expression and function of two hoxb5 paralogues in the zebrafish. Developmental Biology. 210:188
Amores, A., Force, A., Yan, Y.-L. Joly, L., Amemiya, C., Fritz, A., Ho, R., Langeland, J., Prince, V., Wang, Y.-L., Westerfield, M., Ekker, M., and Postlethwait, J.H. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science (New York, N.Y.). 282:1711-1714
Koos, D.S. and Ho, R.K. (1998) The nieuwkoid gene characterizes and mediates a Nieuwkoop-center-like activity in the zebrafish. Current biology : CB. 8:1199-1206
Prince, V.E., Price, A.L., and Ho, R.K. (1998) Hox gene expression reveals regionalization along the anteroposterior axis of the zebrafish notochord. Development genes and evolution. 208:517-522
Bally-Cuif, L., Schatz, W.J., and Ho, R.K. (1998) Characterization of the zebrafish Orb/CPEB-related RNA-binding protein and localization of maternal components in the zebrafish oocyte. Mechanisms of Development. 77:31-47
Ruvinsky, I., Silver, L.M., and Ho, R.K. (1998) Characterization of the zebrafish tbx16 gene and evolution of the vertebrate T-box family. Development genes and evolution. 208:94-99
Prince, V.E., Joly, L., Ekker, M., and Ho, R.K. (1998) Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk. Development (Cambridge, England). 125:407-420
Prince, V.E., Moens, C.B., Kimmel, C.B., and Ho, R.K. (1998) Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene valentino. Development (Cambridge, England). 125:393-406
Kanki, J.P. and Ho, R.K. (1997) The development of the posterior body in zebrafish. Development (Cambridge, England). 124(4):881-893
Kozlowski, D.J., Murakami, T., Ho, R.K., and Weinberg, E.S. (1997) Regional cell movement and tissue patterning in the zebrafish embryo revealed by fate mapping with caged fluorescein. Biochemistry and cell biology = Biochimie et biologie cellulaire. 75:551-562
Halpern, M.E., Thisse, C., Ho, R.K., Thisse, B., Riggleman, B., Trevarrow, B., Weinberg, E.S., Postlethwait, J.H., and Kimmel, C.B. (1995) Cell-autonomous shift from axial to paraxial mesodermal development in zebrafish floating head mutants. Development (Cambridge, England). 121:4257-4264
Sepich, D.S., Ho, R.K., and Westerfield, M. (1994) Autonomous expression of the nic1 acetylcholine receptor mutation in zebrafish muscle cells. Developmental Biology. 161:84-90
Halpern, M.E., Ho, R.K., Walker, C., and Kimmel, C.B. (1993) Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell. 75:99-111
Ho, R.K. and Kimmel, C.B. (1993) Commitment of cell fate in the early zebrafish embryo. Science (New York, N.Y.). 261:109-111
Kimmel, C.B., Molven, A., Ellis, T.J., Hatta, K., Ho, R.K., Kane, D.A., Schilling, T.F., Walker, C., and Warga, R.M. (1993) Developmental and mutational analysis of body pattern formation: the zebrafish model. In Physiological and Biochemical Aspects of Fish Development, Walther-B-T. and Fyhn-H-J., eds., Bergen, Norway: University of Bergen Press. :22-29
Schulte-Merker, S., Ho, R.K., Herrmann, B.G., and Nüsslein-Volhard, C. (1992) The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development (Cambridge, England). 116:1021-1032
Ho, R.K. (1992) Cell movements and cell fate during zebrafish gastrulation. Development (Cambridge, England). (Suppl.) 116:65-73
Ho, R.K. (1992) Axis formation in the embryo of the zebrafish, Brachydanio rerio. Sem. Dev. Biol.. 3:53-64
Hatta, K., Kimmel, C.B., Ho, R.K., and Walker, C. (1991) The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system. Nature. 350:339-341
Kimmel, C.B., Kane, D.A., and Ho, R.K. (1991) Lineage specification during early embryonic development of the zebrafish. In Cell-Cell Interactions in Early Development, J. Gerhart, ed., Wiley, N.Y.. :203-225
Ho, R.K. and Kane, D.A. (1990) Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors. Nature. 348:728-730