A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor

Holger Knaut, Christian Werz, Robert Geisler, E. Busch-Nentwich, R. Dahm, H. G. Frohnhöfer, H. Geiger, D. Gilmour, S. Holley, J. Hooge, D. Jülich, F. Maderspacher, H. M. Maischein, C. Neumann, Teresa Nicolson, H. Roehl, U. Schönberger, C. Seiler, C. Söllner, M. Sonawane & 22 others F. Van Bebber, A. Wehner, C. Weiler, P. Erker, H. Habeck, U. Hagner, C. E Hennen Kapst, A. Kirchner, T. Koblizek, U. Langheinrich, C. Loeschke, C. Metzger, R. Nordin, J. Odenthal, M. Pezzuti, K. Schlombs, J. DeSantana-Stamm, T. Trowe, G. Vacun, B. Walderich, A. Walker, Christiane Nüsslein-Volhard

Research output: Contribution to journalArticle

317 Citations (Scopus)

Abstract

Germ cells preserve an individual's genetic information and transmit it to the next generation. Early in development germ cells are set aside and undergo a specialized developmental programme, a hallmark of which is the migration from their site of origin to the future gonad. In Drosophila, several factors have been identified that control germ-cell migration to their target tissue; however, the germ-cell chemoattractant or its receptor have remained unknown. Here we apply genetics and in vivo imaging to show that odysseus, a zebrafish homologue of the G-protein-coupled chemokine receptor Cxcr4, is required specifically in germ cells for their chemotaxis, odysseus mutant germ cells are able to activate the migratory programme, but fail to undergo directed migration towards their target tissue, resulting in randomly dispersed germ cells. SDF-1, the presumptive cognate ligand for Cxcr4, shows a similar loss-of-function phenotype and can recruit germ cells to ectopic sites in the embryo, thus identifying a vertebrate ligand-receptor pair guiding migratory germ cells at all stages of migration towards their target.

Original languageEnglish (US)
Pages (from-to)279-282
Number of pages4
JournalNature
Volume421
Issue number6920
DOIs
StatePublished - Jan 16 2003
Externally publishedYes

Fingerprint

Chemokine Receptors
Zebrafish
Germ Cells
Ligands
Chemotactic Factors
Gonads
Chemotaxis
G-Protein-Coupled Receptors
Drosophila
Cell Movement
Vertebrates
Embryonic Structures
Phenotype

ASJC Scopus subject areas

  • General

Cite this

Knaut, H., Werz, C., Geisler, R., Busch-Nentwich, E., Dahm, R., Frohnhöfer, H. G., ... Nüsslein-Volhard, C. (2003). A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature, 421(6920), 279-282. https://doi.org/10.1038/nature01338

A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. / Knaut, Holger; Werz, Christian; Geisler, Robert; Busch-Nentwich, E.; Dahm, R.; Frohnhöfer, H. G.; Geiger, H.; Gilmour, D.; Holley, S.; Hooge, J.; Jülich, D.; Maderspacher, F.; Maischein, H. M.; Neumann, C.; Nicolson, Teresa; Roehl, H.; Schönberger, U.; Seiler, C.; Söllner, C.; Sonawane, M.; Van Bebber, F.; Wehner, A.; Weiler, C.; Erker, P.; Habeck, H.; Hagner, U.; Kapst, C. E Hennen; Kirchner, A.; Koblizek, T.; Langheinrich, U.; Loeschke, C.; Metzger, C.; Nordin, R.; Odenthal, J.; Pezzuti, M.; Schlombs, K.; DeSantana-Stamm, J.; Trowe, T.; Vacun, G.; Walderich, B.; Walker, A.; Nüsslein-Volhard, Christiane.

In: Nature, Vol. 421, No. 6920, 16.01.2003, p. 279-282.

Research output: Contribution to journalArticle

Knaut, H, Werz, C, Geisler, R, Busch-Nentwich, E, Dahm, R, Frohnhöfer, HG, Geiger, H, Gilmour, D, Holley, S, Hooge, J, Jülich, D, Maderspacher, F, Maischein, HM, Neumann, C, Nicolson, T, Roehl, H, Schönberger, U, Seiler, C, Söllner, C, Sonawane, M, Van Bebber, F, Wehner, A, Weiler, C, Erker, P, Habeck, H, Hagner, U, Kapst, CEH, Kirchner, A, Koblizek, T, Langheinrich, U, Loeschke, C, Metzger, C, Nordin, R, Odenthal, J, Pezzuti, M, Schlombs, K, DeSantana-Stamm, J, Trowe, T, Vacun, G, Walderich, B, Walker, A & Nüsslein-Volhard, C 2003, 'A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor', Nature, vol. 421, no. 6920, pp. 279-282. https://doi.org/10.1038/nature01338
Knaut H, Werz C, Geisler R, Busch-Nentwich E, Dahm R, Frohnhöfer HG et al. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature. 2003 Jan 16;421(6920):279-282. https://doi.org/10.1038/nature01338
Knaut, Holger ; Werz, Christian ; Geisler, Robert ; Busch-Nentwich, E. ; Dahm, R. ; Frohnhöfer, H. G. ; Geiger, H. ; Gilmour, D. ; Holley, S. ; Hooge, J. ; Jülich, D. ; Maderspacher, F. ; Maischein, H. M. ; Neumann, C. ; Nicolson, Teresa ; Roehl, H. ; Schönberger, U. ; Seiler, C. ; Söllner, C. ; Sonawane, M. ; Van Bebber, F. ; Wehner, A. ; Weiler, C. ; Erker, P. ; Habeck, H. ; Hagner, U. ; Kapst, C. E Hennen ; Kirchner, A. ; Koblizek, T. ; Langheinrich, U. ; Loeschke, C. ; Metzger, C. ; Nordin, R. ; Odenthal, J. ; Pezzuti, M. ; Schlombs, K. ; DeSantana-Stamm, J. ; Trowe, T. ; Vacun, G. ; Walderich, B. ; Walker, A. ; Nüsslein-Volhard, Christiane. / A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. In: Nature. 2003 ; Vol. 421, No. 6920. pp. 279-282.
@article{3ef1036fb1814d3ca211740e111adf8b,
title = "A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor",
abstract = "Germ cells preserve an individual's genetic information and transmit it to the next generation. Early in development germ cells are set aside and undergo a specialized developmental programme, a hallmark of which is the migration from their site of origin to the future gonad. In Drosophila, several factors have been identified that control germ-cell migration to their target tissue; however, the germ-cell chemoattractant or its receptor have remained unknown. Here we apply genetics and in vivo imaging to show that odysseus, a zebrafish homologue of the G-protein-coupled chemokine receptor Cxcr4, is required specifically in germ cells for their chemotaxis, odysseus mutant germ cells are able to activate the migratory programme, but fail to undergo directed migration towards their target tissue, resulting in randomly dispersed germ cells. SDF-1, the presumptive cognate ligand for Cxcr4, shows a similar loss-of-function phenotype and can recruit germ cells to ectopic sites in the embryo, thus identifying a vertebrate ligand-receptor pair guiding migratory germ cells at all stages of migration towards their target.",
author = "Holger Knaut and Christian Werz and Robert Geisler and E. Busch-Nentwich and R. Dahm and Frohnh{\"o}fer, {H. G.} and H. Geiger and D. Gilmour and S. Holley and J. Hooge and D. J{\"u}lich and F. Maderspacher and Maischein, {H. M.} and C. Neumann and Teresa Nicolson and H. Roehl and U. Sch{\"o}nberger and C. Seiler and C. S{\"o}llner and M. Sonawane and {Van Bebber}, F. and A. Wehner and C. Weiler and P. Erker and H. Habeck and U. Hagner and Kapst, {C. E Hennen} and A. Kirchner and T. Koblizek and U. Langheinrich and C. Loeschke and C. Metzger and R. Nordin and J. Odenthal and M. Pezzuti and K. Schlombs and J. DeSantana-Stamm and T. Trowe and G. Vacun and B. Walderich and A. Walker and Christiane N{\"u}sslein-Volhard",
year = "2003",
month = "1",
day = "16",
doi = "10.1038/nature01338",
language = "English (US)",
volume = "421",
pages = "279--282",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "6920",

}

TY - JOUR

T1 - A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor

AU - Knaut, Holger

AU - Werz, Christian

AU - Geisler, Robert

AU - Busch-Nentwich, E.

AU - Dahm, R.

AU - Frohnhöfer, H. G.

AU - Geiger, H.

AU - Gilmour, D.

AU - Holley, S.

AU - Hooge, J.

AU - Jülich, D.

AU - Maderspacher, F.

AU - Maischein, H. M.

AU - Neumann, C.

AU - Nicolson, Teresa

AU - Roehl, H.

AU - Schönberger, U.

AU - Seiler, C.

AU - Söllner, C.

AU - Sonawane, M.

AU - Van Bebber, F.

AU - Wehner, A.

AU - Weiler, C.

AU - Erker, P.

AU - Habeck, H.

AU - Hagner, U.

AU - Kapst, C. E Hennen

AU - Kirchner, A.

AU - Koblizek, T.

AU - Langheinrich, U.

AU - Loeschke, C.

AU - Metzger, C.

AU - Nordin, R.

AU - Odenthal, J.

AU - Pezzuti, M.

AU - Schlombs, K.

AU - DeSantana-Stamm, J.

AU - Trowe, T.

AU - Vacun, G.

AU - Walderich, B.

AU - Walker, A.

AU - Nüsslein-Volhard, Christiane

PY - 2003/1/16

Y1 - 2003/1/16

N2 - Germ cells preserve an individual's genetic information and transmit it to the next generation. Early in development germ cells are set aside and undergo a specialized developmental programme, a hallmark of which is the migration from their site of origin to the future gonad. In Drosophila, several factors have been identified that control germ-cell migration to their target tissue; however, the germ-cell chemoattractant or its receptor have remained unknown. Here we apply genetics and in vivo imaging to show that odysseus, a zebrafish homologue of the G-protein-coupled chemokine receptor Cxcr4, is required specifically in germ cells for their chemotaxis, odysseus mutant germ cells are able to activate the migratory programme, but fail to undergo directed migration towards their target tissue, resulting in randomly dispersed germ cells. SDF-1, the presumptive cognate ligand for Cxcr4, shows a similar loss-of-function phenotype and can recruit germ cells to ectopic sites in the embryo, thus identifying a vertebrate ligand-receptor pair guiding migratory germ cells at all stages of migration towards their target.

AB - Germ cells preserve an individual's genetic information and transmit it to the next generation. Early in development germ cells are set aside and undergo a specialized developmental programme, a hallmark of which is the migration from their site of origin to the future gonad. In Drosophila, several factors have been identified that control germ-cell migration to their target tissue; however, the germ-cell chemoattractant or its receptor have remained unknown. Here we apply genetics and in vivo imaging to show that odysseus, a zebrafish homologue of the G-protein-coupled chemokine receptor Cxcr4, is required specifically in germ cells for their chemotaxis, odysseus mutant germ cells are able to activate the migratory programme, but fail to undergo directed migration towards their target tissue, resulting in randomly dispersed germ cells. SDF-1, the presumptive cognate ligand for Cxcr4, shows a similar loss-of-function phenotype and can recruit germ cells to ectopic sites in the embryo, thus identifying a vertebrate ligand-receptor pair guiding migratory germ cells at all stages of migration towards their target.

UR - http://www.scopus.com/inward/record.url?scp=0037448598&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037448598&partnerID=8YFLogxK

U2 - 10.1038/nature01338

DO - 10.1038/nature01338

M3 - Article

VL - 421

SP - 279

EP - 282

JO - Nature

JF - Nature

SN - 0028-0836

IS - 6920

ER -