Intermolecular interactions of homologs of germ plasm components in mammalian germ cells

Developmental Biology

Volumn 301, Issue 2, 2007, Pages 417-431

  Fox, Mark S ^a,b   Clark, Amander T ^a,b   El Majdoubi, Mohammed ^a,b   Vigne, Jean Louis ^a,b   Urano, Jun ^a,b   Hostetler, Chris E ^c   Griswold, Michael D ^c   Weiner, Richard I ^a,b   Reijo Pera, Renee A ^a,b  

^a Department of Obstetrics Gynecology and Reproductive Sciences   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

DAZ; DAZL; Germ cell development; Germ cells; Germ plasm; NANOS; PUM1; PUM2; RNA binding proteins

Indexed keywords

PROTEIN; RNA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; EMBRYONIC STEM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GERM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANURA; MAMMALIA;

EID: 33846119708     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.08.047     Document Type: Article

References (73)

1. Abeyta M., Clark A.T., Rodriguez R., Bodnar M., Reijo Pera R.A., and Firpo M. Unique gene expression signatures of independently-derived human embryonic stem cell lines. Hum. Mol. Genet. 13 (2004) 601-608
2. Asaoka-Taguchi M., Yamada M., Nakamura A., Hanyu K., and Kobayashi S. Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat. Cell Biol. 1 (1999) 431-437
3. Ascoli M. Regulation of gonadotropin receptors and gonadotropin responses in a clonal strain of Leydig tumor cells by epidermal growth factor. J. Biol. Chem. 256 (1981) 179-183
4. Buehr M., and Smith A. Genesis of embryonic stem cells. Philos. Trans. R. Soc. Lond., B Biol. Sci. 358 (2003) 1397-1402
5. Campbell R., Tour O., Palmer A., Steinbach P., Baird G., Zacharias D., and Tsien R. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. 99 (2002) 7877-7882
6. Castrillon D.H., Quade B.J., Wang T.Y., Quigley C., and Crum C.P. The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl. Acad. Sci. 97 (2000) 9585-9590
7. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., and Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113 (2003) 643-655
8. Chiquoine A. The identification, origin and migration of the primordial germ cells in the mouse embryo. Anat. Rec. 118 (1954) 135-146
9. Clark A.T., Bodnar M.S., Fox M.S., Rodriquez R.T., Abeyta M.J., Firpo M.T., and Reijo Pera R.A. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum. Mol. Genet. 13 (2004) 727-739
10. Clark A.T., Rodriguez R., Bodnar M., Abeyta M., Turek P., Firpo M., and Reijo Pera R.A. Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hot-spot for teratocarcinoma. Stem Cells 22 (2004) 169-179
11. Collier B., Gorgoni B., Loveridge C., Cooke H., and Gray N. The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 24 (2005) 2656-2666
12. D'Agostino I., Merritt C., Chen P., Seydoux G., and Subramaniam K. Translational repression restricts expression of the C. elegans Nanos homolog NOS-2 to the embryonic germline. Dev. Biol. 292 (2006) 244-252
13. Day R., and Schaufele F. Imaging molecular interactions in living cells. Mol. Endocrinol. 19 (2005) 1675-1686
14. Eberhart C.G., Maines J.Z., and Wasserman S.A. Meiotic cell cycle requirement for a fly homologue of human Deleted in AZoospermia. Nature 381 (1996) 783-785
15. Evans M., and Hunter S. Source and nature of embryonic stem cells. C. R. Biol. 325 (2002) 1003-1007
16. Feng L.X., Chen Y., Dettin L., Reijo Pera R.A., Herr J.C., Goldberg E., and Dym M. Generation and in vitro differentiation of a spermatogonial cell line. Science 297 (2002) 392-395
17. Forbes A., and Lehmann R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125 (1998) 679-690
18. Fox M., Urano J., and Reijo Pera R.A. Identification and characterization of RNA sequences to which human PUMILIO-2 (PUM2) and Deleted in Azoospermia-Like (DAZL) bind. Genomics 85 (2005) 92-105
19. Fujiwara T., Dunn N.R., and Hogan B.L. Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc. Natl. Acad. Sci. 98 (2001) 13739-13744
20. Geijsen N., Horoschak M., Kim K., Gribnau J., Eggan K., and Daley G.Q. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427 (2004) 148-154
21. Houston D.W., and King M.L. A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127 (2000) 447-456
22. Howley C., and Ho R.K. mRNA localization patterns in zebrafish oocytes. Mech. Dev. 92 (2000) 305-309
23. Hubner K., Fuhrmann G., Christenson L., Kehler J., Reinbold R., De La Fuente R., Wood J., Strauss III J., Boiani M., and Scholer H. Derivation of oocytes from mouse embryonic stem cells. Science 300 (2003) 1251-1256
24. Ikenishi K. Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev. Growth Differ. 40 (1998) 1-10
25. Jaruzelska J., Kotecki M., Kusz K., Spik A., Firpo M., and Reijo Pera R.A. Conservation of a Pumilio-Nanos complex from Drosophila germ plasm to human germ cells. Dev. Genes Evol. 213 (2003) 120-126
26. Jiao X., Trifillis P., and Kiledjian M. Identification of target messenger RNA substrates for the murine Deleted in Azoospermia-Like RNA-binding Protein. Biol. Reprod. 66 (2002) 475-485
27. Johnson A.D., Bachvarova R.F., Drum M., and Masi T. Expression of axolotl dazl rna, a marker of germ plasm: widespread maternal rna and onset of expression in germ cells approaching the gonad. Dev. Biol. 234 (2001) 402-415
28. Karashima T., Sugimoto A., and Yamamoto M. Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127 (2000) 1069-1079
29. Koprunner 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
30. Kubota H., Avarbock M.R., and Brinster R.L. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol. Reprod. 71 (2004) 722-731
31. Labosky P., Barlow D., and Hogan B. Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120 (1994) 3197-3204
32. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., and Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13 (1999) 424-436
33. Lin Y., and Page D. Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev. Biol. 288 (2005) 309-316
34. Lin H., and Spradling A.C. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124 (1997) 2463-2476
35. Maegawa S., Yasuda K., and Inoue K. Maternal mRNA localization of zebrafish DAZ-like gene. Mech. Dev. 81 (1999) 223-226
36. McLean D.J., Friel P.J., Johnston D.S., and Griswold M.D. Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice. Biol. Reprod. 69 (2003) 2085-2091
37. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., and Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113 (2003) 631-642
38. Mochizuki K., Nishimiya-Fujisawa C., and Fujisawa T. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev. Genes Evol. 211 (2001) 299-308
39. Moore F.L., Jaruzelska J., Fox M.S., Urano J., Firpo M.T., Turek P.J., Dorfman D.M., and Reijo Pera R.A. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-Like proteins. Proc. Natl. Acad. Sci. 100 (2003) 538-543
40. Moore F.L., Jaruzelska J., Dorfmann D., and Reijo Pera R.A. Identification of a novel gene, DZIP (DAZ Interacting Protein), that encodes a protein that interacts with DAZ and DAZL (Deleted in AZoospermia and DAZ-Like) and is expressed in embryonic stem cells and germ cells. Genomics 83 (2004) 834-843
41. Nakahata S., Katsu Y., Mita K., Inoue K., Nagahama Y., and Yamashita M. Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J. Biol. Chem. 276 (2001) 20945-20953
42. Nayernia K., Nolte J., Michelmann H., Lee J., Rathsack K., Drusenheimer N., Dev A., Wulf G., Ehrmann I., Elliott D., Okpanyi V., Zechner U., Haaf T., Meinhardt A., and Engel W. In vitro-differentiated embryonic stem cell give rise to male gametes that can generate offspring mice. Dev. Cell 11 (2006) 125-132
43. Nichols J., Zevnick B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Scholer H., and Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct-4. Cell 95 (1998) 379-391
44. Ohinata Y., Payer B., O'Carroll D., Ancelin K., Ono Y., Sano M., Barton S., Obukhanych T., Nussenzweig M., Tarakhovsky A., Saitou M., and Surani M. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436 (2005) 207-213
45. Onyango P., Jiang S., Uejima H., Shamblott M.J., Gearhart J.D., Cui H., and Feinberg A.P. Monoallelic expression and methylation of imprinted genes in human and mouse embryonic germ cell lineages. Proc. Natl. Acad. Sci. 99 (2002) 10599-10604
46. Padmanabhan K., and Richter J. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev. 20 (2006) 199-209
47. Parisi M., and Lin H. The Drosophila Pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis, and embryogenesis. Genetics 153 (1999) 235-250
48. Reijo R., Lee T.Y., Salo P., Alagappan R., Brown L.G., Rosenberg M., Rozen S., Jaffe T., Straus D., Hovatta O., Chapelle A.d.l., Silber S., and Page D.C. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat. Genet. 10 (1995) 383-393
49. Reijo R., Alagappan R.K., Patrizio P., and Page D.C. Severe oligospermia resulting from deletions of the Azoospermia Factor gene on the Y chromosome. Lancet 347 (1996) 1290-1293
50. Reynolds N., Collier B., Maratou K., Bingham V., Speed R., Taggart M., Semple C., NK N.G., and Cooke H. Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum. Mol. Genet. 14 (2005) 3899-3909
51. Ruggiu M., and Cooke H. In vivo and in vitro analysis of homodimerisation activity of the mouse Dazl protein. Gene 252 (2000) 119-126
52. Ruggiu M., Speed R., Taggart M., McKay S.J., Kilanowski F., Saunders P., Dorin J., and Cooke H. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389 (1997) 73-77
53. Saffman E.E., and Lasko P. Germline development in vertebrates and invertebrates. Cell. Mol. Life Sci. 55 (1999) 1141-1163
54. Saitou M., Barton S.C., and Surani M.A. A molecular programme for the specification of germ cell fate in mice. Nature 418 (2002) 293-300
55. Santos A., and Lehmann R. Germ cell specification and migration in Drosophila and beyond. Curr. Biol. 14 (2004) R578-R589
56. Scholer H., Dressler G., Balling R., Rohdewohld H., and Gruss P. Oct-4: a germ line specific transcription factor mapping to the mouse t-complex. EMBO J. 9 (1990) 2185-2195
57. Scholer H., Ruppert S., Suzuki N., Chowdhury K., and Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 344 (1990) 435-439
58. Subramaniam K., and Seydoux G. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126 (1999) 4861-4871
59. Tam P., and Zhou S. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by position of the cells in the gastrulating mouse embryo. Dev. Biol. 178 (1996) 124-132
60. Tanaka S.S., Toyooka Y., Akasu R., Katoh-Fukui Y., Nakahara Y., Suzuki R., Yokoyama M., and Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14 (2000) 841-853
61. Toyooka Y., Tsunekawa N., Akasu R., and Noce T. Embryonic stem cells can form germ cells in vitro. Proc. Natl. Acad. Sci. 100 (2003) 11457-11462
62. Tsuda M., Sasaoka Y., Kiso M., Abe K., Haraguchi S., Kobayashi S., and Saga Y. Conserved role of nanos proteins in germ cell development. Science 301 (2003) 1239-1241
63. Tsui S., Dai T., Roettger S., Schempp W., Salido E.C., and Yen P.H. Identification of two novel proteins that interact with germ-cell specific RNA-binding proteins DAZ and DAZL1. Genomics 65 (2000) 266-273
64. Tsui S., Dai T., Warren S.T., Salido E.C., and Yen P.H. Association of the mouse infertility factor DAZL1 with actively translating polyribosomes. Biol. Reprod. 62 (2000) 1655-1660
65. Tung J.Y., Rosen M.P., Nelson L.M., Turek P.J., Witte J.S., Cramer D.W., Cedars M.I., and Reijo Pera R.A. Variants in Deleted in AZoospermia-Like (DAZL) are correlated with reproductive parameters in men and women. Hum. Genet. 118 (2006) 730-740
66. Urano J., Fox M., and Reijo Pera R.A. Interaction of the conserved meiotic regulators, BOULE (BOL) and PUMILIO-2 (PUM2). Mol. Reprod. Dev. 71 (2005) 290-298
67. Venables J.P., Ruggiu M., and Cooke H.J. The RNA binding specificity of the mouse Dazl protein. Nucleic Acids Res. 29 (2001) 2479-2483
68. Weatherman R., Chang C., Clegg N., Carroll D., Day R., Baxter J., McDonnell D., Scanlan T., and Schaufele F. Ligand-selective interactions of ER detected in living cells by fluorescence resonance energy transfer. Mol. Endocrinol. 16 (2002) 487-496
69. Wylie C. Germ cells. Curr. Opin. Genet. Dev. 10 (2000) 410-413
70. Xu E.Y., Moore F.L., and Reijo Pera R.A. A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in all metazoans. Proc. Natl. Acad. Sci. 98 (2001) 7414-7419
71. Ying Y., Qi X., and Zhao G.-Q. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc. Natl. Acad. Sci. 98 (2001) 7858-7862
72. Zhou Y., and King M. Sending RNAs into the future: RNA localization and germ cell fate. IUBMB Life 56 (2004) 19-27
73. Zwaka T., and Thomson J. A germ cell origin of embryonic stem cells?. Development 132 (2005) 227-233