Development, Vol 126, Issue 23 5295-5307, Copyright © 1999 by Company of Biologists

JOURNAL ARTICLES

Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells

G Weidinger, U Wolke, M Koprunner, M Klinger and E Raz
Department of Developmental Biology, Institute of Biology I, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany.

In many organisms, the primordial germ cells have to migrate from the position where they are specified towards the developing gonad where they generate gametes. Extensive studies of the migration of primordial germ cells in Drosophila, mouse, chick and Xenopus have identified somatic tissues important for this process and demonstrated a role for specific molecules in directing the cells towards their target. In zebrafish, a unique situation is found in that the primordial germ cells, as marked by expression of vasa mRNA, are specified in random positions relative to the future embryonic axis. Hence, the migrating cells have to navigate towards their destination from various starting positions that differ among individual embryos. Here, we present a detailed description of the migration of the primordial germ cells during the first 24 hours of wild-type zebrafish embryonic development. We define six distinct steps of migration bringing the primordial germ cells from their random positions before gastrulation to form two cell clusters on either side of the midline by the end of the first day of development. To obtain information on the origin of the positional cues provided to the germ cells by somatic tissues during their migration, we analyzed the migration pattern in mutants, including spadetail, swirl, chordino, floating head, cloche, knypek and no isthmus. In mutants with defects in axial structures, paraxial mesoderm or dorsoventral patterning, we find that certain steps of the migration process are specifically affected. We show that the paraxial mesoderm is important for providing proper anteroposterior information to the migrating primordial germ cells and that these cells can respond to changes in the global dorsoventral coordinates. In certain mutants, we observe accumulation of ectopic cells in different regions of the embryo. These ectopic cells can retain both morphological and molecular characteristics of primordial germ cells, suggesting that, in zebrafish at the early stages tested, the vasa-expressing cells are committed to the germ cell lineage.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				X. Sang, M. S. Curran, and A. W. Wood Paracrine Insulin-Like Growth Factor Signaling Influences Primordial Germ Cell Migration: In Vivo Evidence from the Zebrafish Model Endocrinology, October 1, 2008; 149(10): 5035 - 5042. [Abstract] [Full Text] [PDF]

				H. Sano, A. D. Renault, and R. Lehmann Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2 J. Cell Biol., November 21, 2005; 171(4): 675 - 683. [Abstract] [Full Text] [PDF]

				H. Blaser, S. Eisenbeiss, M. Neumann, M. Reichman-Fried, B. Thisse, C. Thisse, and E. Raz Transition from non-motile behaviour to directed migration during early PGC development in zebrafish J. Cell Sci., September 1, 2005; 118(17): 4027 - 4038. [Abstract] [Full Text] [PDF]

				K. Dumstrei, R. Mennecke, and E. Raz Signaling pathways controlling primordial germ cell migration in zebrafish J. Cell Sci., September 15, 2004; 117(20): 4787 - 4795. [Abstract] [Full Text] [PDF]

				J. M. Spitsbergen and M. L. Kent The State of the Art of the Zebrafish Model for Toxicology and Toxicologic Pathology Research--Advantages and Current Limitations Toxicol Pathol, January 1, 2003; 31(1_suppl): 62 - 87. [Abstract] [PDF]

				B. Ciruna, G. Weidinger, H. Knaut, B. Thisse, C. Thisse, E. Raz, and A. F. Schier Production of maternal-zygotic mutant zebrafish by germ-line replacement PNAS, November 12, 2002; 99(23): 14919 - 14924. [Abstract] [Full Text] [PDF]

				Y. Takeuchi, G. Yoshizaki, T. Kobayashi, and T. Takeuchi Mass Isolation of Primordial Germ Cells from Transgenic Rainbow Trout Carrying the Green Fluorescent Protein Gene Driven by the vasa Gene Promoter Biol Reprod, October 1, 2002; 67(4): 1087 - 1092. [Abstract] [Full Text] [PDF]

				C. Thisse and L. I. Zon Organogenesis--Heart and Blood Formation from the Zebrafish Point of View Science, January 18, 2002; 295(5554): 457 - 462. [Abstract] [Full Text] [PDF]

				G. Weidinger, U. Wolke, M. Koprunner, C. Thisse, B. Thisse, and E. Raz Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target Development, January 1, 2002; 129(1): 25 - 36. [Abstract] [Full Text] [PDF]

				M. Koprunner, C. Thisse, B. Thisse, and E. Raz A zebrafish nanos-related gene is essential for the development of primordial germ cells Genes & Dev., November 1, 2001; 15(21): 2877 - 2885. [Abstract] [Full Text] [PDF]

				Y. Ying, X. Qi, and G.-Q. Zhao Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways PNAS, June 20, 2001; (2001) 151242798. [Abstract] [Full Text] [PDF]

				Y. Ying, X.-M. Liu, A. Marble, K. A. Lawson, and G.-Q. Zhao Requirement of Bmp8b for the Generation of Primordial Germ Cells in the Mouse Mol. Endocrinol., July 1, 2000; 14(7): 1053 - 1063. [Abstract] [Full Text]

				H. Knaut, F. Pelegri, K. Bohmann, H. Schwarz, and C. Nusslein-Volhard Zebrafish vasa RNA but Not Its Protein Is a Component of the Germ Plasm and Segregates Asymmetrically before Germline Specification J. Cell Biol., May 15, 2000; 149(4): 875 - 888. [Abstract] [Full Text] [PDF]

				M. Tanaka, M. Kinoshita, D. Kobayashi, and Y. Nagahama Establishment of medaka (Oryzias latipes) transgenic lines with the expression of green fluorescent protein fluorescence exclusively in germ cells: A useful model to monitor germ cells in a live vertebrate PNAS, February 27, 2001; 98(5): 2544 - 2549. [Abstract] [Full Text] [PDF]

				Y. Ying, X. Qi, and G.-Q. Zhao Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways PNAS, July 3, 2001; 98(14): 7858 - 7862. [Abstract] [Full Text] [PDF]