Migration of Zebrafish Primordial Germ Cells: A Role for Myosin Contraction and Cytoplasmic Flow

Developmental Cell

Volumn 11, Issue 5, 2006, Pages 613-627

  Blaser, Heiko ^a   Reichman Fried, Michal ^a   Castanon, Irinka ^b   Dumstrei, Karin ^a   Marlow, Florence L ^c   Kawakami, Koichi ^d   Solnica Krezel, Lilianna ^c   Heisenberg, Carl Philipp ^b   Raz, Erez ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c VANDERBILT UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

CELLBIO; DEVBIO; STEMCELL

Indexed keywords

CALCIUM; CHEMOKINE RECEPTOR CXCR4; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; STROMAL CELL DERIVED FACTOR 1;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; EMBRYO DEVELOPMENT; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; ZEBRA FISH;

ACTINS; ANIMALS; CELL MEMBRANE; CELL POLARITY; CHEMOKINES, CXC; CHEMOTAXIS; CYTOPLASM; CYTOSKELETON; GERM CELLS; MYOSINS; PSEUDOPODIA; RECEPTORS, CXCR4; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 33750491282     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.09.023     Document Type: Article

References (88)

1. Affolter M., and Weijer C.J. Signaling to cytoskeletal dynamics during chemotaxis. Dev. Cell 9 (2005) 19-34
2. 2) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151 (2000) 1067-1080
3. Bear J.E., Loureiro J.J., Libova I., Fassler R., Wehland J., and Gertler F.B. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101 (2000) 717-728
4. Beis D., and Stainier D.Y. In vivo cell biology: following the zebrafish trend. Trends Cell Biol. 16 (2006) 105-112
5. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., and Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 25 (2005) 3995-4003
6. Bereiter-Hahn J. Mechanics of crawling cells. Med. Eng. Phys. 27 (2005) 743-753
7. Bereiter-Hahn J., Strohmeier R., Kunzenbacher I., Beck K., and Voth M. Locomotion of Xenopus epidermis cells in primary culture. J. Cell Sci. 52 (1981) 289-311
8. Betapudi V., Licate L.S., and Egelhoff T.T. Distinct roles of nonmuscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration. Cancer Res. 66 (2006) 4725-4733
9. Blaser H., Eisenbeiss S., Neumann M., Reichman-Fried M., Thisse B., Thisse C., and Raz E. Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J. Cell Sci. 118 (2005) 4027-4038
10. Bleul C.C., Farzan M., Choe H., Parolin C., Clark-Lewis I., Sodroski J., and Springer T.A. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382 (1996) 829-833
11. Brabletz T., Jung A., Spaderna S., Hlubek F., and Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5 (2005) 744-749
12. Bray D., and White J.G. Cortical flow in animal cells. Science 239 (1988) 883-888
13. Burger J.A., and Kipps T.J. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107 (2006) 1761-1767
14. Chard P.S., Bleakman D., Christakos S., Fullmer C.S., and Miller R.J. Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J. Physiol. 472 (1993) 341-357
15. Charras G.T., Yarrow J.C., Horton M.A., Mahadevan L., and Mitchison T.J. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435 (2005) 365-369
16. Chew T.L., Wolf W.A., Gallagher P.J., Matsumura F., and Chisholm R.L. A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156 (2002) 543-553
17. Chisholm R.L., and Firtel R.A. Insights into morphogenesis from a simple developmental system. Nat. Rev. Mol. Cell Biol. 5 (2004) 531-541
18. Doitsidou M., Reichman-Fried M., Stebler J., Koprunner M., Dorries J., Meyer D., Esguerra C.V., Leung T., and Raz E. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111 (2002) 647-659
19. Dumstrei K., Mennecke R., and Raz E. Signaling pathways controlling primordial germ cell migration in zebrafish. J. Cell Sci. 117 (2004) 4787-4795
20. Furukawa R., Maselli A., Thomson S.A., Lim R.W., Stokes J.V., and Fechheimer M. Calcium regulation of actin crosslinking is important for function of the actin cytoskeleton in Dictyostelium. J. Cell Sci. 116 (2003) 187-196
21. Gilmour D., Knaut H., Maischein H.M., and Nusslein-Volhard C. Towing of sensory axons by their migrating target cells in vivo. Nat. Neurosci. 7 (2004) 491-492
22. Hauptmann G., and Gerster T. Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet. 10 (1994) 266
23. 2+ signals. Trends Cell Biol. 14 (2004) 320-330
24. Janson L.W., and Taylor D.L. In vitro models of tail contraction and cytoplasmic streaming in amoeboid cells. J. Cell Biol. 123 (1993) 345-356
25. Jin S.W., Beis D., Mitchell T., Chen J.N., and Stainier D.Y. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132 (2005) 5199-5209
26. Jowett T., and Lettice L. Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin- and fluorescein-labelled probes. Trends Genet. 10 (1994) 73-74
27. Kaksonen M., Peng H.B., and Rauvala H. Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J. Cell Sci. 113 (2000) 4421-4426
28. Kawakami K., Takeda H., Kawakami N., Kobayashi M., Matsuda N., and Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 7 (2004) 133-144
29. Kimmel C., Ballard W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
30. Knaut H., Werz C., Geisler R., and Nusslein-Volhard C. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421 (2003) 279-282
31. Kovacs M., Toth J., Hetenyi C., Malnasi-Csizmadia A., and Sellers J.R. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279 (2004) 35557-35563
32. Kunwar P.S., Siekhaus D.E., and Lehmann R. In vivo migration: a germ cell perspective. Annu. Rev. Cell Dev. Biol. 22 (2006) 237-265
33. Kuo J.C., Wang W.J., Yao C.C., Wu P.R., and Chen R.H. The tumor suppressor DAPK inhibits cell motility by blocking the integrin-mediated polarity pathway. J. Cell Biol. 172 (2006) 619-631
34. Köprunner M., Thisse C., Thisse B., and Raz E. A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev. 15 (2001) 2877-2885
35. Langridge P.D., and Kay R.R. Blebbing of Dictyostelium cells in response to chemoattractant. Exp. Cell Res. 312 (2006) 2009-2017
36. Lapidot T., Dar A., and Kollet O. How do stem cells find their way home?. Blood 106 (2005) 1901-1910
37. 2+ influx. Curr. Biol. 15 (2005) 1235-1241
38. Luster A.D., Alon R., and von Andrian U.H. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6 (2005) 1182-1190
39. Marlow F., Topczewski J., Sepich D., and Solnica-Krezel L. Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12 (2002) 876-884
40. Matsumura F. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15 (2005) 371-377
41. Mejillano M.R., Kojima S., Applewhite D.A., Gertler F.B., Svitkina T.M., and Borisy G.G. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118 (2004) 363-373
42. Moussavi R.S., Kelley C.A., and Adelstein R.S. Phosphorylation of vertebrate nonmuscle and smooth muscle myosin heavy chains and light chains. Mol. Cell. Biochem. 127-128 (1993) 219-227
43. Murdoch C. CXCR4: chemokine receptor extraordinaire. Immunol. Rev. 177 (2000) 175-184
44. Oberlin E., Amara A., Bachelerie F., Bessia C., Virelizier J.L., Arenzana-Seisdedos F., Schwartz O., Heard J.M., Clark-Lewis I., Legler D.F., et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382 (1996) 833-835
45. Paluch E., Piel M., Prost J., Bornens M., and Sykes C. Cortical actomyosin breakage triggers shape oscillations in cells and cell fragments. Biophys. J. 89 (2005) 724-733
46. Paluch E., Sykes C., Prost J., and Bornens M. Dynamic modes of the cortical actomyosin gel during cell locomotion and division. Trends Cell Biol. 16 (2006) 5-10
47. Pechere J.F., Derancourt J., and Haiech J. The participation of parvalbumins in the activation-relaxation cycle of vertebrate fast skeletal-muscle. FEBS Lett. 75 (1977) 111-114
48. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 (2003) 453-465
49. Rafelski S.M., and Theriot J.A. Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73 (2004) 209-239
50. Raucher D., Stauffer T., Chen W., Shen K., Guo S., York J.D., Sheetz M.P., and Meyer T. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100 (2000) 221-228
51. Raz E. Primordial germ-cell development: the zebrafish perspective. Nat. Rev. Genet. 4 (2003) 690-700
52. Raz E., and Reichman-Fried M. Attraction rules: germ cell migration in zebrafish. Curr. Opin. Genet. Dev. 16 (2006) 355-359
53. Reichman-Fried M., Minina S., and Raz E. Autonomous modes of behavior in primordial germ cell migration. Dev. Cell 6 (2004) 589-596
54. Rhyner J.A., Durussel I., Cox J.A., Ilg E.C., Schafer B.W., and Heizmann C.W. Human recombinant alpha-parvalbumin and nine mutants with individually inactivated calcium- and magnesium-binding sites: biochemical and immunological properties. Biochim. Biophys. Acta 1313 (1996) 179-186
55. 2+ channel function. J. Cell Biol. 169 (2005) 435-445
56. Sahai E., and Marshall C.J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5 (2003) 711-719
57. Sepich D.S., Calmelet C., Kiskowski M., and Solnica-Krezel L. Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation. Dev. Dyn. 234 (2005) 279-292
58. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., and Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22 (2004) 1567-1572
59. Sheetz M.P., Sable J.E., and Dobereiner H.G. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 417-434
60. Shohat G., Shani G., Eisenstein M., and Kimchi A. The DAP-kinase family of proteins: study of a novel group of calcium-regulated death-promoting kinases. Biochim. Biophys. Acta 1600 (2002) 45-50
61. Small J.V., and Resch G.P. The comings and goings of actin: coupling protrusion and retraction in cell motility. Curr. Opin. Cell Biol. 17 (2005) 517-523
62. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., and Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299 (2003) 1743-1747
63. Strohmeier R., and Bereiter-Hahn J. Control of cell shape and locomotion by external calcium. Exp. Cell Res. 154 (1984) 412-420
64. Strohmeier R., and Bereiter-Hahn J. Hydrostatic pressure in epidermal cells is dependent on Ca-mediated contractions. J. Cell Sci. 88 (1987) 631-640
65. Svitkina T.M., Verkhovsky A.B., McQuade K.M., and Borisy G.G. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139 (1997) 397-415
66. Taylor D.L., Blinks J.R., and Reynolds G. Contractile basis of ameboid movement. VII. Aequorin luminescence during ameboid movement, endocytosis, and capping. J. Cell Biol. 86 (1980) 599-607
67. Taylor D.L., Wang Y.L., and Heiple J.M. Contractile basis of ameboid movement. VII. The distribution of fluorescently labeled actin in living amebas. J. Cell Biol. 86 (1980) 590-598
68. Torres-Vazquez J., Gitler A.D., Fraser S.D., Berk J.D., Van N.P., Fishman M.C., Childs S., Epstein J.A., and Weinstein B.M. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 7 (2004) 117-123
69. Totsukawa G., Wu Y., Sasaki Y., Hartshorne D.J., Yamakita Y., Yamashiro S., and Matsumura F. Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J. Cell Biol. 164 (2004) 427-439
70. Tsukita S., and Yonemura S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J. Biol. Chem. 274 (1999) 34507-34510
71. Ulrich F., Krieg M., Schotz E.M., Link V., Castanon I., Schnabel V., Taubenberger A., Mueller D., Puech P.H., and Heisenberg C.P. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9 (2005) 555-564
72. Van Haastert P.J., and Devreotes P.N. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5 (2004) 626-634
73. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J. Cell Biol. 131 (1995) 989-1002
74. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Self-polarization and directional motility of cytoplasm. Curr. Biol. 9 (1999) 11-20
75. Vicente-Manzanares M., Webb D.J., and Horwitz A.R. Cell migration at a glance. J. Cell Sci. 118 (2005) 4917-4919
76. Wadgaonkar R., Nurmukhambetova S., Zaiman A.L., and Garcia J.G. Mutation analysis of the non-muscle myosin light chain kinase (MLCK) deletion constructs on CV1 fibroblast contractile activity and proliferation. J. Cell. Biochem. 88 (2003) 623-634
77. Weed S.A., Karginov A.V., Schafer D.A., Weaver A.M., Kinley A.W., Cooper J.A., and Parsons J.T. Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J. Cell Biol. 151 (2000) 29-40
78. Weidinger G., Wolke U., Koprunner M., Klinger M., and Raz E. Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126 (1999) 5295-5307
79. Weidinger G., Wolke U., Koprunner M., Thisse C., Thisse B., and Raz E. Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target. Development 129 (2002) 25-36
80. Westerfield M. The Zebrafish Book (1995), University of Oregon Press, Oregon
81. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., and Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160 (2003) 267-277
82. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., Takuwa Y., Sugimoto N., Mitchison T., and Bourne H.R. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114 (2003) 201-214
83. Yamada A., Hirose K., Hashimoto A., and Iino M. Real-time imaging of myosin II regulatory light-chain phosphorylation using a new protein biosensor. Biochem. J. 385 (2005) 589-594
84. Yamaguchi H., Wyckoff J., and Condeelis J. Cell migration in tumors. Curr. Opin. Cell Biol. 17 (2005) 559-564
85. Yanai M., Kenyon C.M., Butler J.P., Macklem P.T., and Kelly S.M. Intracellular pressure is a motive force for cell motion in Amoeba proteus. Cell Motil. Cytoskeleton 33 (1996) 22-29
86. Yoon C., Kawakami K., and 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. Development 124 (1997) 3157-3165
87. 2+ store to the plasma membrane. Nature 437 (2005) 902-905
88. Zlotnik A. Involvement of chemokine receptors in organ-specific metastasis. Contrib. Microbiol. 13 (2006) 191-199