Webb, D. J., Zhang, H. & Horwitz, A. F. Cell migration: an overview. Methods Mol. Biol.294, 3–11 (2005). PubMed Google Scholar
Franz, C. M., Jones, G. E. & Ridley, A. J. Cell migration in development and disease. Dev. Cell2, 153–158 (2002). CASPubMed Google Scholar
Keller, R. Cell migration during gastrulation. Curr. Opin. Cell Biol.17, 533–541 (2005). CASPubMed Google Scholar
Ribeiro, C., Petit, V. & Affolter, M. Signaling systems, guided cell migration, and organogenesis: insights from genetic studies in Drosophila. Dev. Biol.260, 1–8 (2003). CASPubMed Google Scholar
Hatten, M. E. Central nervous system neuronal migration. Annu. Rev. Neurosci.22, 511–539 (1999). CASPubMed Google Scholar
Rossant, J. & Howard, L. Signaling pathways in vascular development. Annu. Rev. Cell Dev. Biol.18, 541–573 (2002). CASPubMed Google Scholar
Raz, E. Guidance of primordial germ cell migration. Curr. Opin. Cell Biol.16, 169–173 (2004). CASPubMed Google Scholar
Santos, A. C. & Lehmann, R. Germ cell specification and migration in Drosophila and beyond. Curr. Biol.14, 578–589 (2004). Google Scholar
Molyneaux, K. & Wylie, C. Primordial germ cell migration. Int. J. Dev. Biol.48, 537–544 (2004). CASPubMed Google Scholar
Kunwar, P. S., Siekhaus, D. E. & Lehmann, R. In vivo migration: a germ cell perspective. Annu. Rev. Cell Dev. Biol.22, 237–265 (2006). CASPubMed Google Scholar
Gobel, U. et al. Germ-cell tumors in childhood and adolescence. GPOH MAKEI and the MAHO study groups. Ann. Oncol.11, 263–271 (2000). CASPubMed Google Scholar
Schneider, D. T. et al. Multipoint imprinting analysis indicates a common precursor cell for gonadal and nongonadal pediatric germ cell tumors. Cancer Res.61, 7268–7276 (2001). CASPubMed Google Scholar
Nakamura, A. & Seydoux, G. Less is more: specification of the germline by transcriptional repression. Development135, 3817–3827 (2008). CASPubMed Google Scholar
Nance, J. & Priess, J. R. Cell polarity and gastrulation in, C. elegans. Development129, 387–397 (2002). CASPubMed Google Scholar
Cinalli, R. M., Rangan, P. & Lehmann, R. Germ cells are forever. Cell132, 559–562 (2008). CASPubMed Google Scholar
Leatherman, J. L., Levin, L., Boero, J. & Jongens, T. A. germ cell-less acts to repress transcription during the establishment of the Drosophila germ cell lineage. Curr. Biol.12, 1681–1685 (2002). CASPubMed Google Scholar
Jongens, T. A., Ackerman, L. D., Swedlow, J. R., Jan, L. Y. & Jan, Y. N. Germ cell-less encodes a cell type-specific nuclear pore-associated protein and functions early in the germ-cell specification pathway of Drosophila. Genes Dev.8, 2123–2136 (1994). CASPubMed Google Scholar
Hanyu-Nakamura, K., Sonobe-Nojima, H., Tanigawa, A., Lasko, P. & Nakamura, A. Drosophila PGC protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. Nature451, 730–733 (2008). CASPubMed CentralPubMed Google Scholar
Nakamura, A., Amikura, R., Mukai, M., Kobayashi, S. & Lasko, P. F. Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science274, 2075–2079 (1996). CASPubMed Google Scholar
Deshpande, G., Calhoun, G. & Schedl, P. Overlapping mechanisms function to establish transcriptional quiescence in the embryonic Drosophila germline. Development131, 1247–1257 (2004). CASPubMed Google Scholar
Martinho, R. G., Kunwar, P. S., Casanova, J. & Lehmann, R. A noncoding RNA is required for the repression of RNApolII-dependent transcription in primordial germ cells. Curr. Biol.14, 159–165 (2004). CASPubMed Google Scholar
Asaoka, M., Sano, H., Obara, Y. & Kobayashi, S. Maternal Nanos regulates zygotic gene expression in germline progenitors of Drosophila melanogaster. Mech. Dev.78, 153–158 (1998). CASPubMed Google Scholar
Deshpande, G., Calhoun, G., Yanowitz, J. L. & Schedl, P. D. Novel functions of nanos in downregulating mitosis and transcription during the development of the Drosophila germline. Cell99, 271–281 (1999). CASPubMed Google Scholar
Schaner, C. E., Deshpande, G., Schedl, P. D. & Kelly, W. G. A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies. Dev. Cell5, 747–757 (2003). CASPubMed CentralPubMed Google Scholar
Yoon, C., Kawakami, K. & Hopkins, N. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development124, 3157–3165 (1997). CASPubMed Google Scholar
Raz, E. Primordial germ-cell development: the zebrafish perspective. Nature Rev. Genet.4, 690–700 (2003). CASPubMed Google Scholar
Knaut, H., Pelegri, F., Bohmann, K., Schwarz, H. & Nusslein-Volhard, C. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol.149, 875–888 (2000). CASPubMed CentralPubMed Google Scholar
Koprunner, M., Thisse, C., Thisse, B. & Raz, E. A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev.15, 2877–2885 (2001). CASPubMed CentralPubMed Google Scholar
Bontems, F. et al. Bucky ball organizes germ plasm assembly in zebrafish. Curr. Biol.19, 414–422 (2009). CASPubMed Google Scholar
Marlow, F. L. & Mullins, M. C. Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev. Biol.321, 40–50 (2008). CASPubMed CentralPubMed Google Scholar
Li, W. et al. Germ cell-less expression in zebrafish embryos. Dev. Growth Differ.48, 333–338 (2006). CASPubMed Google Scholar
Saga, Y. Mouse germ cell development during embryogenesis. Curr. Opin. Genet. Dev.18, 337–341 (2008). CASPubMed Google Scholar
Saitou, M., Payer, B., O'Carroll, D., Ohinata, Y. & Surani, M. A. Blimp1 and the emergence of the germ line during development in the mouse. Cell Cycle4, 1736–1740 (2005). CASPubMed Google Scholar
Ohinata, Y. et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature436, 207–213 (2005). CASPubMed Google Scholar
Vincent, S. D. et al. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development132, 1315–1325 (2005). CASPubMed Google Scholar
Yamaji, M. et al. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nature Genet.40, 1016–1022 (2008). CASPubMed Google Scholar
Kurimoto, K., Yamaji, M., Seki, Y. & Saitou, M. Specification of the germ cell lineage in mice: a process orchestrated by the PR-domain proteins, Blimp1 and Prdm14. Cell Cycle7, 3514–3518 (2008). CASPubMed Google Scholar
Kunwar, P. S. et al. Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-cadherin. J. Cell Biol.183, 157–168 (2008). Shows a link between G protein-coupled receptor signalling and PGC adhesion and polarity that is mediated by E-cadherin at the initiation of migration inD. melanogaster. CASPubMed CentralPubMed Google Scholar
Jaglarz, M. K. & Howard, K. R. The active migration of Drosophila primordial germ cells. Development121, 3495–3503 (1995). CASPubMed Google Scholar
Callaini, G., Riparbelli, M. G. & Dallai, R. Pole cell migration through the gut wall of the Drosophila embryo: analysis of cell interactions. Dev. Biol.170, 365–375 (1995). CASPubMed Google Scholar
Kunwar, P. S., Starz-Gaiano, M., Bainton, R. J., Heberlein, U. & Lehmann, R. Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells. PLoS Biol.1, E80 (2003). PubMed CentralPubMed Google Scholar
Bainton, R. J. et al. moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell123, 145–156 (2005). CASPubMed Google Scholar
Schwabe, T., Bainton, R. J., Fetter, R. D., Heberlein, U. & Gaul, U. GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell123, 133–144 (2005). CASPubMed Google Scholar
Blaser, H. et al. Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J. Cell Sci.118, 4027–4038 (2005). CASPubMed Google Scholar
Weidinger, G. et al. dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr. Biol.13, 1429–1434 (2003). CASPubMed Google Scholar
Kedde, M. et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell131, 1273–1286 (2007). CASPubMed Google Scholar
Anderson, R., Copeland, T. K., Scholer, H., Heasman, J. & Wylie, C. The onset of germ cell migration in the mouse embryo. Mech. Dev.91, 61–68 (2000). Describes the first in-depth analysis of PGC migration in mice, using live imaging. CASPubMed Google Scholar
Tanaka, S. S., Yamaguchi, Y. L., Tsoi, B., Lickert, H. & Tam, P. P. IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev. Cell9, 745–756 (2005). CASPubMed Google Scholar
Lange, U. C. et al. Normal germ line establishment in mice carrying a deletion of the Ifitm/Fragilis gene family cluster. Mol. Cell. Biol.28, 4688–4696 (2008). CASPubMed CentralPubMed Google Scholar
Youngren, K. K. et al. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature435, 360–364 (2005). CASPubMed CentralPubMed Google Scholar
Gu, Y., Runyan, C., Shoemaker, A., Surani, A. & Wylie, C. Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development136, 1295–1303 (2009). Clarifies the role of the steel–c-kit signalling pathway in regulating PGC migration in mice, using a PGC-specific reporter line in live embryos. This study shows that steel expression continuously surrounds PGCs throughout their migration and promotes general motility, but does not provide directional information. CASPubMed Google Scholar
Warrior, R. Primordial germ cell migration and the assembly of the Drosophila embryonic gonad. Dev. Biol.166, 180–194 (1994). CASPubMed Google Scholar
Moore, L. A., Broihier, H. T., Van Doren, M., Lunsford, L. B. & Lehmann, R. Identification of genes controlling germ cell migration and embryonic gonad formation in Drosophila. Development125, 667–678 (1998). CASPubMed Google Scholar
Wang, J., Wu, X., Simonavicius, N., Tian, H. & Ling, L. Medium-chain fatty acids as ligands for orphan G protein-coupled receptor GPR84. J. Biol. Chem.281, 34457–34464 (2006). CASPubMed Google Scholar
Zhang, N., Zhang, J., Purcell, K. J., Cheng, Y. & Howard, K. The Drosophila protein Wunen repels migrating germ cells. Nature385, 64–67 (1997). CASPubMed Google Scholar
Zhang, N., Zhang, J., Cheng, Y. & Howard, K. Identification and genetic analysis of wunen, a gene guiding Drosophila melanogaster germ cell migration. Genetics143, 1231–1241 (1996). CASPubMed CentralPubMed Google Scholar
Starz-Gaiano, M., Cho, N. K., Forbes, A. & Lehmann, R. Spatially restricted activity of a Drosophila lipid phosphatase guides migrating germ cells. Development128, 983–991 (2001). CASPubMed Google Scholar
Hanyu-Nakamura, K., Kobayashi, S. & Nakamura, A. Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development131, 4545–4553 (2004). CASPubMed Google Scholar
Sano, H., Renault, A. D. & Lehmann, R. Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J. Cell Biol.171, 675–683 (2005). CASPubMed CentralPubMed Google Scholar
Renault, A. D., Sigal, Y. J., Morris, A. J. & Lehmann, R. Soma-germ line competition for lipid phosphate uptake regulates germ cell migration and survival. Science305, 1963–1966 (2004). Along with reference 61, this study shows thatD. melanogasterPGCs and somatic cells compete for a phospholipid that is required for PGC migration and survival. CASPubMed Google Scholar
Burnett, C. & Howard, K. Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep.4, 793–799 (2003). CASPubMed CentralPubMed Google Scholar
Burnett, C., Makridou, P., Hewlett, L. & Howard, K. Lipid phosphate phosphatases dimerise, but this interaction is not required for in vivo activity. BMC Biochem.5, 2 (2004). PubMed CentralPubMed Google Scholar
Renault, A. D. & Lehmann, R. Follow the fatty brick road: lipid signaling in cell migration. Curr. Opin. Genet. Dev.16, 348–354 (2006). CASPubMed Google Scholar
Steinhauer, J. et al. Drosophila lysophospholipid acyltransferases are specifically required for germ cell development. Mol. Biol. Cell 28 Oct 2009 (doi:10.1091/mbc.E09-05-0382). CASPubMed CentralPubMed Google Scholar
Van Doren, M., Broihier, H. T., Moore, L. A. & Lehmann, R. HMG-CoA reductase guides migrating primordial germ cells. Nature396, 466–469 (1998). CASPubMed Google Scholar
Goldstein, J. L. & Brown, M. S. Regulation of the mevalonate pathway. Nature343, 425–430 (1990). CASPubMed Google Scholar
Santos, A. C. & Lehmann, R. Isoprenoids control germ cell migration downstream of HMGCoA reductase. Dev. Cell6, 283–293 (2004). CASPubMed Google Scholar
Ricardo, S. & Lehmann, R. An ABC transporter controls export of a Drosophila germ cell attractant. Science323, 943–946 (2009). Identifies the ABC transporter MDR49 as being important for PGC migration inD. melanogaster, presumably through export of an HMGCR-modified chemoattractant, and proves the ability of MDR49 to promote PGC attraction using sorted PGCs in anin vitrochemotaxis assay. CASPubMed CentralPubMed Google Scholar
Li, J., Xia, F. & Li, W. X. Coactivation of STAT and Ras is required for germ cell proliferation and invasive migration in Drosophila. Dev. Cell5, 787–798 (2003). CASPubMed CentralPubMed Google Scholar
Brown, S., Zeidler, M. P. & Hombria, J. E. JAK/STAT signalling in Drosophila controls cell motility during germ cell migration. Dev. Dyn.235, 958–966 (2006). CASPubMed Google Scholar
Weidinger, G., Wolke, U., Koprunner, M., Klinger, M. & Raz, E. Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development126, 5295–5307 (1999). CASPubMed Google Scholar
Reichman-Fried, M., Minina, S. & Raz, E. Autonomous modes of behavior in primordial germ cell migration. Dev. Cell6, 589–596 (2004). CASPubMed Google Scholar
Blaser, H. et al. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev. Cell11, 613–627 (2006). Provides a detailed cellular analysis of PGC migration in zebrafish and determines that PGCs migrate by extending bleb-like protrusions that are regulated by myosin contraction in response to an increase in local Ca2+concentration. CASPubMed Google Scholar
Knaut, H., Werz, C., Geisler, R. & Nusslein-Volhard, C. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature421, 279–282 (2003). CASPubMed Google Scholar
Doitsidou, M. et al. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell111, 647–659 (2002). CASPubMed Google Scholar
Dumstrei, K., Mennecke, R. & Raz, E. Signaling pathways controlling primordial germ cell migration in zebrafish. J. Cell Sci.117, 4787–4795 (2004). CASPubMed Google Scholar
Boldajipour, B. et al. Control of chemokine-guided cell migration by ligand sequestration. Cell132, 463–473 (2008). Identifies a role for CXCR7B, a GPCR, in sequestering SDF1A in somatic cells and promoting the proper distribution of this chemokine and PGC migration. CASPubMed Google Scholar
Mahabaleshwar, H., Boldajipour, B. & Raz, E. Killing the messenger: The role of CXCR7 in regulating primordial germ cell migration. Cell Adh. Migr.2, 69–70 (2008). PubMed CentralPubMed Google Scholar
Thorpe, J. L., Doitsidou, M., Ho, S. Y., Raz, E. & Farber, S. A. Germ cell migration in zebrafish is dependent on HMGCoA reductase activity and prenylation. Dev. Cell6, 295–302 (2004). CASPubMed Google Scholar
Mulligan, T., Blaser, H., Raz, E. & Farber, S. A. Prenylation-deficient G protein γ subunits disrupt GPCR signaling in the zebrafish. Cell Signal. 26 Sep 2009 (http://dx.doi.org/10.1016/j.cellsig.2009.09.017).
Molyneaux, K. A., Stallock, J., Schaible, K. & Wylie, C. Time-lapse analysis of living mouse germ cell migration. Dev. Biol.240, 488–498 (2001). CASPubMed Google Scholar
Hara, K. et al. Evidence for crucial role of hindgut expansion in directing proper migration of primordial germ cells in mouse early embryogenesis. Dev. Biol.330, 427–439 (2009). CASPubMed Google Scholar
Ara, T. et al. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc. Natl Acad. Sci. USA100, 5319–5323 (2003). CASPubMedPubMed Central Google Scholar
Molyneaux, K. A. et al. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development130, 4279–4286 (2003). Along with references 77, 78 and 86, this study shows that the CXCR4–SDF1 signalling pathway is essential for PGC migration in zebrafish and mice. CASPubMed Google Scholar
McCoshen, J. A. & McCallion, D. J. A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia31, 589–590 (1975). CASPubMed Google Scholar
Buehr, M., McLaren, A., Bartley, A. & Darling, S. Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev. Dyn.198, 182–189 (1993). CASPubMed Google Scholar
Mahakali Zama, A., Hudson, F. P., & Bedell, M. A. Analysis of hypomorphic KitlSl mutants suggests different requirements for KITL in proliferation and migration of mouse primordial germ cells. Biol. Reprod.73, 639–647 (2005). PubMed Google Scholar
Runyan, C. et al. Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development133, 4861–4869 (2006). CASPubMed Google Scholar
Di Carlo, A. & De Felici, M. A role for E-cadherin in mouse primordial germ cell development. Dev. Biol.226, 209–219 (2000). CASPubMed Google Scholar
Bendel-Stenzel, M. R., Gomperts, M., Anderson, R., Heasman, J. & Wylie, C. The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech. Dev.91, 143–152 (2000). CASPubMed Google Scholar
Anderson, R. et al. Mouse primordial germ cells lacking β1 integrins enter the germline but fail to migrate normally to the gonads. Development126, 1655–1664 (1999). CASPubMed Google Scholar
Ding, J. et al. Inhibition of HMG CoA reductase reveals an unexpected role for cholesterol during PGC migration in the mouse. BMC Dev. Biol.8, 120 (2008). PubMed CentralPubMed Google Scholar
Jenkins, A. B., McCaffery, J. M. & Van Doren, M. Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis. Development130, 4417–4426 (2003). CASPubMed Google Scholar
Van Doren, M. et al. fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development130, 2355–2364 (2003). CASPubMed Google Scholar
Mathews, W. R., Ong, D., Milutinovich, A. B. & Van Doren, M. Zinc transport activity of Fear of Intimacy is essential for proper gonad morphogenesis and DE-cadherin expression. Development133, 1143–1153 (2006). CASPubMed Google Scholar
Coffman, C. R. Cell migration and programmed cell death of Drosophila germ cells. Ann. N. Y. Acad. Sci.995, 117–126 (2003). CASPubMed Google Scholar
Yamada, Y., Davis, K. D. & Coffman, C. R. Programmed cell death of primordial germ cells in Drosophila is regulated by p53 and the Outsiders monocarboxylate transporter. Development135, 207–216 (2008). CASPubMed Google Scholar
Matsui, Y. et al. Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature353, 750–752 (1991). CASPubMed Google Scholar
Godin, I. et al. Effects of the steel gene product on mouse primordial germ cells in culture. Nature352, 807–809 (1991). CASPubMed Google Scholar
Dolci, S. et al. Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature352, 809–811 (1991). CASPubMed Google Scholar
Stallock, J., Molyneaux, K., Schaible, K., Knudson, C. M. & Wylie, C. The pro-apoptotic gene Bax is required for the death of ectopic primordial germ cells during their migration in the mouse embryo. Development130, 6589–6597 (2003). CASPubMed Google Scholar
Cook, M. S., Coveney, D., Batchvarov, I., Nadeau, J. H. & Capel, B. BAX-mediated cell death affects early germ cell loss and incidence of testicular teratomas in Dnd1Ter/Ter mice. Dev. Biol.328, 377–383 (2009). Examines the formation of teratomas in mice with disrupted DND function caused by theTermutation and finds that apoptosis mediated by BAX is responsible for both germ cell loss and protection from tumour formation in these mutants. CASPubMed CentralPubMed Google Scholar
Hartsock, A. & Nelson, W. J. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta1778, 660–669 (2008). CASPubMed Google Scholar
Alvarez-Buylla, A. & Merchant-Larios, H. Mouse primordial germ cells use fibronectin as a substrate for migration. Exp. Cell Res.165, 362–368 (1986). CASPubMed Google Scholar
Devenport, D. & Brown, N. H. Morphogenesis in the absence of integrins: mutation of both Drosophila β subunits prevents midgut migration. Development131, 5405–5415 (2004). CASPubMed Google Scholar
Kardash, E. et al. A role for Rho GTPases and cell–cell adhesion in single-cell motility in vivo. Nature Cell Biol. 13 Dec 2009 (doi:10.1038/ncb2003). PubMed Google Scholar
Friedl, P. & Wolf, K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nature Rev. Cancer3, 362–374 (2003). CAS Google Scholar
Sahai, E. Mechanisms of cancer cell invasion. Curr. Opin. Genet. Dev.15, 87–96 (2005). CASPubMed Google Scholar
Starz-Gaiano, M. & Lehmann, R. Moving towards the next generation. Mech. Dev.105, 5–18 (2001). CASPubMed Google Scholar