The efficiency of Xenopus primordial germ cell migration depends on the germplasm mRNA encoding the PDZ domain protein Grip2

Differentiation

Volumn 76, Issue 4, 2008, Pages 392-403

  Kirilenko, Pavel ^b   Weierud, Frida K ^a,b   Zorn, Aaron M ^c   Woodland, Hugh R ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Germline; Germplasm; Grip2; PGC migration; Xenopus

Indexed keywords

GENE PRODUCT; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR INTERACTING PROTEIN 2; MESSENGER RNA; PDZ PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; EMBRYO; GERMPLASM; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA TRANSLATION; TADPOLE; XENOPUS;

XENOPUS LAEVIS; XENOPUS TROPICALIS;

EID: 42049117359     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00229.x     Document Type: Article

References (59)

1. Ataman, B., Ashley, J., Gorczyca, D., Gorczyca, M., Mathew, D., Wichmann, C., Sigrist, S.J. Budnik, V. (2006) Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc Natl Acad Sci USA 103 : 7841 7846.
2. Bendel-Stenzel, M., Anderson, R., Heasman, J. Wylie, C. (1998) The origin and migration of primordial germ cells in the mouse. Semin Cell Dev Biol 9 : 393 400.
3. Berekelya, L.A., Mikryukov, A.A., Luchinskaya, N.N., Ponomarev, M.B., Woodland, H.R. Belyavsky, A.V. (2007) The protein encoded by the germ plasm RNA Germes associates with dynein light chains and functions in Xenopus germline development. Differentiation, E. Pub.
4. Bruckner, K., Labrador, J.P., Scheiffele, P., Herb, A., Seeburg, P.H. Klein, R. (1999) EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron 22 : 511 524.
5. Chan, A.P., Kloc, M., Bilinski, S. Etkin, L.D. (2001) The vegetally localized mRNA fatvg is associated with the germ plasm in the early embryo and is later expressed in the fat body. Mech Dev 100 : 137 140.
6. Chang, P., Torres, J., Lewis, R.A., Mowry, K.L., Houliston, E. King, M.L. (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15 : 4669 4681.
7. Clements, D., Cameleyre, I. Woodland, H.R. (2003) Redundant early and overlapping larval roles of Xsox17 subgroup genes in Xenopus endoderm development. Mech Dev 120 : 337 348.
8. Doitsidou, M., Reichman-Fried, M., Stebler, J., Koprunner, M., Dorries, J., Meyer, D., Esguerra, C.V., Leung, T. Raz, E. (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111 : 647 659.
9. Dong, H., O'Brien, R.J., Fung, E.T., Lanahan, A.A., Worley, P.F. Huganir, R.L. (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386 : 279 284.
10. Dong, H.L., Zhang, P.S., Song, I.S., Petralia, R.S., Liao, D.Z. Huganir, R.L. (1999) Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2. J Neurosci 19 : 6930 6941.
11. Farini, D., La Sala, G., Tedesco, M. De Felici, M. (2007) Chemoattractant action and molecular signaling pathways of Kit ligand on mouse primordial germ cells. Dev Biol 306 : 572 583.
12. Forristall, C., Pondel, M., Chen, L.H. King, M.L. (1995) Patterns of localization and cytoskeletal association of 2 vegetally localized RNAs, Vg1 and Xcat-2. Development 121 : 201 208.
13. Harland, R.M. (1991) In situ hybridization - an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36 : 685 695.
14. Hoogenraad, C.C., Milstein, A.D., Ethell, I.M., Henkemeyer, M. Sheng, M. (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 8 : 906 915.
15. Houston, D.W. King, M.L. (2000a) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127 : 447 456.
16. Houston, D.W. King, M.L. (2000b) Germ plasm and molecular determinants of germ cell fate. Curr Topics Dev Biol 50 : 155 181.
17. Hudson, C., Clements, D., Friday, R.V., Stott, D. Woodland, H.R. (1997) Xsox17α and -β mediate endoderm formation in Xenopus. Cell 91 : 397 405.
18. Hudson, C. Woodland, H.R. (1998) Xpat, a gene expressed specifically in germ plasm and primordial germ cells of Xenopus laevis. Mech Dev 73 : 159 168.
19. Ikenishi, K. (1998) Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev Growth Diff 40 : 1 10.
20. Ikenishi, K., Nishiumi, F. Komiya, T. (2006) The Xdsg protein in presumptive primordial germ cells (pPGCs) is essential to their differentiation into PGCs in Xenopus. Dev Biol 297 : 483 492.
21. Ikenishi, K., Ohno, T. Komiya, T. (2007) Ectopic germline cells in embryos of Xenopus laevis. Dev Growth Differ 49 : 561 570.
22. Irino, Y., Ichinohe, M., Nakamura, Y., Nakahara, M. Fukami, K. (2005) Phospholipase Cdelta4 associates with glutamate receptor interacting protein 1 in testis. J Biochem (Tokyo) 138 : 451 456.
23. Jonason, A.S., Baker, S.M. Sweasy, J.B. (2001) Interaction of DNA polymerase beta with GRIP1 during meiosis. Chromosoma 110 : 402 410.
24. Kaneshiro, K., Miyauchi, M., Tanigawa, Y., Ikenishi, K. Komiya, T. (2007) The mRNA coding for Xenopus glutamate receptor interacting protein 2 (XGRIP2) is maternally transcribed, transported through the late pathway and localized to the germ plasm. Biochem Biophys Res Commun 355 : 902 906.
25. Kloc, M., Bilinski, S. Etkin, L.D. (2004) The Balbiani body and germ cell determinants: 150 years later. In : Schatten, G.P. ed). Current topics in developmental biology, Vol. 29. Elsevier Inc., San Diego, pp. 1 36.
26. Kloc, M. Etkin, L.D. (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121 : 287 297.
27. Kloc, M. Etkin, L.D. (1998) Apparent continuity between the messenger transport organizer and late RNA localization pathways during oogenesis in Xenopus. Mech Dev 73 : 95 106.
28. Kurokawa, H., Aoki, Y., Nakamura, S., Ebe, Y., Kobayashi, D. Tanaka, M. (2006) Time-lapse analysis reveals different modes of primordial germ cell migration in the medaka Oryzias latipes. Dev Growth Diff 48 : 209 221.
29. Lasko, P. (1999) RNA sorting in Drosophila oocytes and embryos. FASEB J 13 : 421 433.
30. Lin, S.H., Arai, A.C., Wang, Z., Nothacker, H.P. Civelli, O. (2001) The carboxyl terminus of the prolactin-releasing peptide receptor interacts with PDZ domain proteins involved in alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor clustering. Mol Pharmacol 60 : 916 923.
31. Lopes, S., van den Driesche, S., Carvalho, R.L.C., Larsson, J., Eggen, B., Surani, M.A. Mummery, C.L. (2005) Altered primordial germ cell migration in the absence of transforming growth factor beta signaling via ALK5. Dev Biol 284 : 194 203.
32. Nakata, A., Ito, T., Nagata, M., Hori, S. Sekimizu, K. (2004) GRIP1tau, a novel PDZ domain-containing transcriptional activator, cooperates with the testis-specific transcription elongation factor SII-T1. Genes Cells 9 : 1125 1135.
33. Nishiumi, F., Komiya, T. Ikenishi, K. (2005) The mode and molecular mechanisms of the migration of presumptive PGC in the endoderm cell mass of Xenopus embryos. Dev Growth Diff 47 : 37 48.
34. Quaas, J. Wylie, C. (2002) Surface contraction waves (SCWs) in the Xenopus egg are required for the localization of the germ plasm and are dependent upon maternal stores of the kinesin-like protein Xklp1. Dev Biol 243 : 272 280.
35. Raz, E. (2002) Primordial germ cell development in zebrafish. Seminars in Cell Dev Biol 13 : 489 495.
36. Richardson, J.C., Gatherer, D. Woodland, H.R. (1995) Developmental effects of over-expression of normal and mutated forms of a Xenopus NF-kB homolog. Mech Dev 52 : 165 177.
37. Robb, D.L., Heasman, J., Raats, J. Wylie, C. (1996) A kinesin-like protein is required for germ plasm aggregation in Xenopus. Cell 87 : 823 831.
38. Saffman, E.E. Lasko, P. (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55 : 1141 1163.
39. Schlueter, P.J., Sang, X., Duan, C. Wood, A.W. (2007) Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev Biol 305 : 377 387.
40. Schnorrer, F., Kalchhauser, I. Dickson, B.J. (2007) The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev Cell 12 : 751 766.
41. Setou, M., Seog, D.H., Tanaka, Y., Kanai, Y., Takei, Y., Kawagishi, M. Hirokawa, N. (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417 : 83 87.
42. Sinner, D., Kirilenko, P., Rankin, S., Wei, E., Howard, L., Kofron, M., Heasman, J., Woodland, H.R. Zorn, A.M. (2006) Global analysis of the transcriptional network controlling Xenopus endoderm formation. Development 133 : 1955 1966.
43. Smyth, I. Scambler, P. (2005) The genetics of Fraser syndrome and the blebs mouse mutants. Hum Mol Genet 14 : R269 R274.
44. Smyth, I., Xin, D., Taylor, M.S., Justice, M.J., Beutler, B. Jackson, I.J. (2004) The extracellular matrix gene Frem1 is essential for the normal adhesion of the embryonic epidermis. Proc Natl Acad Sci USA 101 : 13560 13565.
45. Stebler, J., Spieler, D., Slanchev, K., Molyneaux, K.A., Richter, U., Cojocaru, V., Tarabykin, V., Wylie, C., Kessel, M. Raz, E. (2004) Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev Biol 272 : 351 361.
46. Swan, L.E., Schmidt, M., Schwarz, T., Ponimaskin, E., Prange, U., Boeckers, T., Thomas, U. Sigrist, S.J. (2006) Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J 25 : 3640 3651.
47. Swan, L.E., Wichmann, C., Prange, U., Schmid, A., Schmidt, M., Schwarz, T., Ponimaskin, E., Madeo, F., Vorbruggen, G. Sigrist, S.J. (2004) A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev 18 : 223 237.
48. Takamiya, K., Kostourou, V., Adams, S., Jadeja, S., Chalepakis, G., Scambler, P.J., Huganir, R.L. Adams, R.H. (2004) A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1. Nat Genet 36 : 172 177.
49. Tunstall, M.J., Roberts, A. Soffe, S.R. (2002) Modelling inter-segmental coordination of neuronal oscillators: synaptic mechanisms for uni-directional coupling during swimming in Xenopus tadpoles. J Comput Neurosci 13 : 143 158.
50. Wilk, K., Bilinski, S., Dougherty, M.T. Kloc, M. (2005) Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. Int J Dev Biol 49 : 17 21.
51. Wylie, C. (1999) Germ cells. Cell 96 : 165 174.
52. Wyszynski, M., Kim, E., Yang, F.C. Sheng, M. (1998) Biochemical and immunocytochemical characterization of GRIP, a putative AMPA receptor anchoring protein, in rat brain. Neuropharmacology 37 : 1335 1344.
53. Wyszynski, M., Valtschanoff, J.G., Naisbitt, S., Dunah, A.W., Kim, E., Standaert, D.G., Weinberg, R. Sheng, M. (1999) Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J Neurosci 19 : 6528 6537.
54. Ye, B., Liao, D., Zhang, X., Zhang, P., Dong, H. Huganir, R.L. (2000) GRASP-1: a neuronal RasGEF associated with the AMPA receptor/GRIP complex. Neuron 26 : 603 617.
55. Yu, G.Y., Zerucha, T., Ekker, M. Rubenstein, J.L.R. (2001) Evidence that GRIP, a PDZ-domain protein which is expressed in the embryonic forebrain, co-activates transcription with DLX homeodomain proteins. Dev Brain Res 130 : 217 230.
56. Zearfoss, N.R., Chan, A.P., Wu, C.F., Kloc, M. Etkin, L.D. (2004) Hermes is a localized factor regulating cleavage of vegetal blastomeres in Xenopus laevis. Dev Biol 267 : 60 71.
57. Zhao, F.Y., Wolf, E. Roberts, A. (1998) Longitudinal distribution of components of excitatory synaptic input to motoneurones during swimming in young Xenopus tadpoles: experiments with antagonists. J Physiol 511 (Pt 3) : 887 901.
58. Zhou, Y. King, M.L. (1996) RNA transport to the vegetal cortex of Xenopus oocytes. Dev Biol 179 : 173 183.
59. Zhou, Y. King, M.L. (2004) Sending RNAs into the future: RNA localization and germ cell fate. Iubmb Life 56 : 19 27.