Flatworm stem cells and the germ line: Developmental and evolutionary implications of macvasa expression in Macrostomum lignano

Developmental Biology

Volumn 319, Issue 1, 2008, Pages 146-159

  Pfister, Daniela ^a   De Mulder, Katrien ^a,b   Hartenstein, Volker ^c   Kuales, Georg ^a   Borgonie, Gaetan ^b   Marx, Florentine ^d   Morris, Joshua ^e   Ladurner, Peter ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e AZUSA PACIFIC UNIVERSITY   (United States)

Author keywords

Evolution; Germline; Neoblasts; Planaria; Totipotent; Vasa

Indexed keywords

MESSENGER RNA; PROTEIN;

AMINO ACID SEQUENCE; AMPUTATION; ARTICLE; CELL PROLIFERATION; CORRELATION ANALYSIS; DOWN REGULATION; EGG; EMBRYO DEVELOPMENT; EVOLUTION; FEEDING; GENE EXPRESSION; GENE FUNCTION; GENETIC EPIGENESIS; GERM LINE; GONAD DEVELOPMENT; IN SITU HYBRIDIZATION; ISOLATION PROCEDURE; MACROSTOMUM LIGNANO; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PLATYHELMINTH; PRIORITY JOURNAL; REGENERATION; RNA INTERFERENCE; SOMATIC CELL; STARVATION; STEM CELL; TESTIS;

MACROSTOMUM; MACROSTOMUM LIGNANO; PLANARIA; PLATYHELMINTHES;

EID: 44749091488     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.02.045     Document Type: Article

References (112)

1. Agata K. Regeneration and gene regulation in planarians. Curr. Opin. Genet. Dev. 13 (2003) 492-496
2. Agata K., Nakajima E., Funayama N., Shibata N., Saito Y., and Umesono Y. Two different evolutionary origins of stem cell systems and their molecular basis. Semin. Cell Dev. Biol. 17 4 (2006) 503-509
3. Anderson R.A., Berges R.A., Harrison P.J., and Watanabe M.M. Appendix A - Recipes for Freshwater and Seawater Media; Enriched Natural Seawater Media. In: Anderson R.A. (Ed). Algal Culturing Techniques (2005), Elsevier Academic Press, Burlington, USA 507
4. Baguñá J. Mitosis in the intact and regenerating planarian Dugesia mediterranea n. sp. I. Mitotic studies during growth, feeding and starvation. J. Exp. Biol. 195 (1976) 53-64
5. Baguñá J., and Romero R. Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina. Hydrobiologia 84 (1981) 181-194
6. Baguñá J., Saló E., and Auladell C. Regeneration and pattern formation in planarians. III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107 (1989) 77-86
7. Bartfai R., and Orban L. The vasa locus in zebrafish: multible RGG boxes from duplications. DNA Cell Biol. 22 1 (2003) 47-54
8. Batalova F., and Parfenov V. Immunomorphological localization of Vasa protein and pre-mRNA splicing factors in Panorpa communis trophocytes and oocytes. Cell Biol. Int. 27 (2003) 795-807
9. Bermange A.L., Reddien P., and Sánchez Alvarado A. An RNAi screen for regeneration genes in the planarian S. mediterranea. Dev. Biol. 259 (2003) 536
10. Bilinski S.M., Jaglarz M.K., Szymanska B., Etkin L.D., and Kloc M. Sm proteins, the constituents of the spliceosome, are components of nuage and mitochondrial cement in Xenopus oocytes. Exp. Cell Res. 299 (2004) 171-178
11. Bode A., Salvenmoser W., Nimeth K., Mahlknecht M., Adamski Z., Rieger R.M., Peter R., and Ladurner P. Immunogold labeled S-phase neoblasts, total neoblast number, their distribution and evidence for arrested neoblasts in Macrostomum lignano (Platyhelminthes, Rhabditophora). Cell Tissue Res. 325 3 (2006) 577-587
12. Braat A.K., van de Water S., Goos H., Bogerd J., and Zivkovic D. Vasa protein expression and localization in the zebrafish. Mech. Dev. 95 (2000) 271-274
13. Braat A.K., van de Water S., Korving J., and Zivkovic D. A zebrafish vasa morphant abolishes vasa protein but does not affect the establishment of the germline. Genesis 30 (2001) 183-185
14. Campos-Ortega J.A., and Hartenstein V. The Embryonic Development of Drosophila melanogaster. Second Edition (1997), Springer, Heidelberg
15. Carre D., Djediat C., and Sardet C. Formation of a large Vasa-positive germ granule and its inheritance by germ cells in the enigmatic Chaetognaths. Development 129 (2002) 661-670
16. 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. U. S. A. 97 (2000) 9585-9590
17. Cebria F., and Newmark P.A. Morphogenesis defects are associated with abnormal nervous system regeneration following roboA RNAi in planarians. Development 134 5 (2007) 833-837
18. Cebria F., Kobayashi C., Umesono Y., Nakazawa M., Mineta K., Ikeo K., Gojobori T., Itoh M., Taira M., Alvarado A.S., and Agata K. FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419 (2002) 620-624
19. Cebria F., Guo T., Jopek J., and Newmark P.A. Regeneration and maintenance of the planarian midline is regulated by a slit orthologue. Dev. Biol. 307 2 (2007) 394-406
20. Coward S.J. Chromatoid bodies in somatic cells of the planarian: observation on their behavior during mitosis. Anat. Rec. 180 (1974) 533-546
21. Dubois F. Contribution à l'étude de la régénération chez planaires dulcicoles. Bull. Biol. 83 (1949) 213-283
22. Egger B., Ladurner P., Nimeth K., Gschwentner R., and Rieger R. The regeneration capacity of the flatworm Macrostomum lignano - on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Dev. Genes Evol. 216 (2006) 565-577
23. Egger B., Gschwentner R., and Rieger R. Free-living flatworms under the knife: past and present. Dev. Genes Evol. 217 2 (2007) 89-104
24. Extavour C.G. The fate of isolated blastomeres with respect to germ cell formation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol. 277 (2005) 387-402
25. Extavour C.G.M. Gray Anatomy: phylogenetic patterns of somatic gonad structures and reproductive strategies across the Bilateria. Integr. Comp. Biol. (2007) 1-7 10.1093/icb/icm052
26. Extavour C.G.M. Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr. Comp. Biol. (2007) 1-16 10.1093/icb/icm027
27. Extavour C.G., and Akam M. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130 (2003) 5869-5884
28. Extavour C.G., Pang K., Matus D.Q., and Martindale M.Q. vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms. Evolut. Develop. 7 (2005) 201-215
29. Fedecka-Brunner B. Régénération des testicules des Planaries après destruction par les rayons X. In: Kiortsis V., and Trampusch H.A.L. (Eds). Regeneration in Animals and Related Problems (1965), North-Holland Publ. Co., Amsterdam 185-192
30. Fedecka-Brunner B. Etudes sur la régénération des organes genitaux chez la planaire Dugesia lugubris. I. Régénération des testicules après destruction. Bull. Biol. Fr. Belg. 101 (1967) 255-319
31. Findley S.D., Tamanaha M., Clegg N.J., and Ruohola-Baker H. Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130 (2003) 859-871
32. Fire A., et al. Potent and specific interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998) 806-811
33. Fujiwara Y., Komiya T., Kawabata H., Sato M., Fujimoto H., Furusawa M., and Noce T. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12258-12262
34. Fuller M.T., and Spradling A.C. Male and female Drosophila germline stem cells: two versions of immortality. Science 316 5823 (2007) 402-404
35. Ghirardelli E. Differentiation of the germ cells and regeneration of the gonads in Planarians. In: Kiortsis V., and Trampusch H.A.L. (Eds). Regeneration in Animals and Related Problems (1965), North-Holland Publ. Co., Amsterdam 177-184
36. Gremigni V. The origin and cytodifferentiation of germ cells in the planarians. Boll. Zool. 41 (1974) 359-377 (Atti del XLII Convegno dell'U.Z.I)
37. Gremigni V. In: Adiyodi K.G., and Adiyodi R.G. (Eds). Reproductive Biology of Invertebrates. Volume 1: Oogenesis, Oviposition, and Oosorption (1983), John Wiley & Sons, Ltd. 67-107
38. Grens A., Mason E., Marsh J.L., and Bode H. Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. Development 121 (1995) 4027-4035
39. Grens A., Gee L., Fisher D.A., and Bode H. CnNK-2, an NK-2 homeobox gene, has a role in patterning the basa end of the axis in Hydra. Dev. Biol. 180 (1996) 473-488
40. Gruidl M.E., Smith P.A., Kuznicki K.A., McCrone J.S., Kirchner J., Roussell D.L., Strome S., and Bennett K.L. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 13837-13842
41. Guo T., Peters A.H., and Newmark P.A. A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11 2 (2006) 159-169
42. Handberg-Thorsager M., and Saló E. The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev. Genes Evol. 217 5 (2007) 403-411
43. Hori I. An ultrastructural study of the chromatoid body in planarian regenerative cells. J. Electron Microsc. 31 (1982) 63-72
44. Hori I. Cytological approach to morphogenesis in the planarian blastema. II. The effect of neuropeptides. J. Submicrosc. Cytol. Pathol. 29 (1997) 91-97
45. Ikenishi K. Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev. Growth Differ. 40 (1998) 1-10
46. Ikenishi K., and Tanaka T.S. Spatio-temporal expression of Xenopus vasa homolog, XVLG1, in oocytes and embryos: the presence of XVLG1 RNA in somatic cells as well as germline cells. Dev. Growth Differ. 42 (2000) 95-103
47. Johnstone O., Deuring R., Bock R., Linder P., Fuller M.T., and Lasko P. Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Dev. Biol. 277 (2005) 92-101
48. Kimble J.E., and White J.G. On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81 2 (1981) 208-219
49. Knaut H., Pelegri F., Bohmann K., Schwarz H., and 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 (2000) 875-888
50. Kobayashi T., and Hoshi M. Switching from asexual to sexual reproduction in the planarian Dugesia ryukyuensis: change of the fissiparous capacity along with the sexualizing process. Zoolog. Sci. 19 6 (2002) 661-666
51. Kobayashi T., Kajiura-Kobayashi H., and Nagahama Y. Two isoforms of vasa homologs in a teleost fish: their differential expression during germ cell differentiation. Mech. Dev. 111 (2002) 161-171
52. Krovel A.V., and Olsen L.C. Expression of a vas{proportion}EGFP transgene in primordial germ cells of the zebrafish. Mech. Dev. 116 (2002) 141-150
53. Krovel A.V., and Olsen L.C. Sexual dimorphic expression pattern of a splice variant of zebrafish vasa during gonadal development. Dev. Biol. 271 (2004) 190-197
54. Kuznicki K.A., Smith P.A., Leung-Chiu W.M., Estevez A.O., Scott H.C., and Bennett K.L. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127 (2000) 2907-2916
55. Ladurner P., Rieger R., and Baguñá J. Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyuridine analysis. Dev. Biol. 226 (2000) 231-241
56. Ladurner P., Pfister D., Seifarth C., Schärer L., Mahlknecht M., Salvenmoser W., Gerth R., Marx F., and Rieger R. Production and characterization of cell- and tissue-specific monoclonal antibodies for the flatworm Macrostomum sp. Histochem. Cell Biol. 123 (2005) 89-104
57. Ladurner P., Schärer L., and Rieger R.M. Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha): a new model organism among the lower bilateria and the use of digital video microscopy in taxonomy of meiobenthic Platyhelminthes. J. Zoolog. Syst. Evol. Res. 43 (2005) 114-126
58. Lawson K.A., and Hage W.J. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. symp. 182 (1994) 84-91
59. Lender T. Factors in morphogenesis of regenerating freshwater planaria. In: Abercrombie M., and Brachet J. (Eds). Advances in Morphogenesis (1962), Academic Press, New York 305-331
60. Liang L., Diehl-Johnes W., and Lasko P. Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120 (1994) 1201-1211
61. Linder P. DEAD-box proteins. Curr. Biol. 10 24 (2000) R887
62. Linder P., Lasko P.F., Ashburner M., Leroy P., Nielsen P.J., Nishi K., Schnier J., and Slonimski P.P. Birth of the D-E-A-D box. Nature 337 (1989) 121-122
63. Luking A., Stahl U., and Schmidt U. The protein family of RNA helicases. Crit. Rev. Biochem. Mol. Biol. 33 (1998) 259-296
64. Mahowald A.P. Assembly of the Drosophila germ plasm. Int. Rev. Cyt. 203 (2001) 187-213
65. Mannini L., Rossi L., Deri P., Gremigni V., Salvetti A., Saló E., and Batistoni R. Djeyes absent (Djeya) controls prototypic planarian eye regeneration by cooperating with the transcription factor Djsix-1. Dev. Biol. 269 (2004) 346-359
66. Melander Y. Cytogenetics aspects of embryogenesis in Paludicola, Tricladida. Hereditas (Lund) 49 (1963) 119-166
67. 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
68. Morris J., Nallur R., Ladurner P., Egger B., Rieger R., and Hartenstein V. The embryonic development of the flatworm Macrostomum sp. Dev. Genes Evol. 214 (2004) 220-239
69. Newmark P.A., and Sánchez A.A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220 (2000) 142-153
70. Newmark P.A., and Sánchez A.A. Not your father's planarian: a classic model enters the era of functional genomics. Nat. Rev., Genet. 3 (2002) 210-219
71. Nieuwkoop P.D. Experimental observations on the origin and determination of the germ cells, and on the development of the lateral plates and germ ridges in the urodeles. Arch. Neerl. Zool. 8 (1947) 1-205
72. Nimeth K.T., Mahlknecht M., Mezzanato A., Peter R., Rieger R., and Ladurner P. Stem cell dynamics during growth, feeding and starvation in the basal flatworm Macrostomum sp. (Platyhelminthes). Dev. Dyn. 230 (2004) 91-99
73. Ogawa K., Wakayama A., Kunisada T., Orii H., Watanabe K., and Agata K. Identification of a receptor tyrosine kinase involved in germ cell differentiation in planarians. Biochem. Biophys. Res. Commun. 248 (1998) 204-209
74. Orii H., and Watanabe K. Bone morphogenetic protein is required for dorso-ventral patterning in the planarian Dugesia japonica. Dev. Growth Differ. 49 4 (2007) 345-349
75. Orii H., Mochii M., and Watanabe K. A simple "soaking method" for RNA interference in the planarian Dugesia japonica. Dev. Genes Evol. 213 (2003) 138-141
76. Orii H., Sakurai T., and Watanabe K. Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev. Genes Evol. 215 (2005) 143-157
77. Oviedo N.J., Newmark P.A., and Sánchez Alvarado A. Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev. Dyn. 226 (2003) 326-333
78. Parvinen M. The chromatoid body in spermatogenesis. Int. J. Androl. 28 (2005) 189-201
79. Pfister D., De Mulder K., Philipp I., Kuales G., Hrouda M., Eichberger P., Borgonie G., Hartenstein V., and Ladurner P. The exceptional stem cell system of Macrostomum lignano: screening for gene expression and studying cell proliferation by hydroxyurea treatment and irradiation. Front. Zool. 4 9 (2007)
80. Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1 (2000) 1017
81. Rebscher N., Zelada-González F., Banisch T.U., Raible F., and Arendt D. Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev. Biol. 306 2 (2007) 599-611
82. Reddien P.W., and Sanchez A.A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20 (2004) 725-757
83. Reddien P.W., Bermange A., and Sánchez Alvarado A. An RNAi screen for regeneration genes in the planarian S. mediterranea. Dev. Biol. 259 (2003) 536 (abstract)
84. Reddien P.W., Oviedo N.J., Jennings J.R., Jenkin J.C., and Sanchez A.A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310 (2005) 1327-1330
85. Reddien P.W., Bermange A.L., Murfitt K.J., Jennings J.R., and Sánchez A.A. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 8 (2005) 635-649 (abstract)
86. Rieger R.M., Gehlen M., Haszprunar G., Holmlund M., Legniti A., Salvenmoser W., and Tyler S. Laboratory cultures of marine Macrostomida (Turbellaria). Fortschr. Zool. 36 (1988) 523-525
87. Rossi L., Salvetti A., Lena A., Batistoni R., Deri P., Pugliesi C., Loreti E., and Gremigni V. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev. Genes Evol. 216 (2006) 335-346
88. Saló E. The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 5 (2006) 546-559
89. Saló E., and Baguñá J. Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J. Exp. Zool. 292 (2002) 528-539
90. Salvetti A., Rossi L., Lena A., Batistoni R., Deri P., Rainaldi G., Locci M.T., Evangelista M., and Gremigni V. DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132 (2005) 1863-1874
91. Sánchez Alvarado A. The freshwater planarian Schmidtea mediterranea: embryogenesis, stem cells and regeneration. Curr. Opin. Genet. Dev. 13 4 (2003) 438-444
92. Sánchez Alvarado A., and Kang H. Multicellularity, stem cells, and the neoblasts of the planarian Schmidtea mediterranea. Exp. Cell Res. 306 (2005) 299-308
93. Sánchez Alvarado A., and Newmark P.A. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5049-5054
94. Sano H., Nakamura A., and Kobayashi S. Identification of a transcriptional regulatory region for germline-specific expression of vasa gene in Drosophila melanogaster. Mech. Dev. 112 (2002) 129-139
95. Sato K., Shibata N., Orii H., Amikura R., Sakurai T., Agata K., Kobayashi S., and Watanabe K. Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Dev. Growth Differ. 48 (2006) 615-628
96. Shibata N., Umesono Y., Orii H., Sakurai T., Watanabe K., and Agata K. Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev. Biol. 206 (1999) 73-87
97. Shigenobu S., Arita K., Kitadate Y., Noda C., and Kobayashi S. Isolation of germline cells from Drosophila embryos by flow cytometry. Dev. Growth Differ. 48 (2006) 49-57
98. Styhler S., Nakamura A., Swan A., Suter B., and Lasko P. vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125 (1998) 1569-1578
99. Sunanaga T., Watanabe A., and Kawamura K. Involvement of vasa homolog in germline recruitment from coelomic stem cells in budding tunicates. Dev. Genes Evol. 217 1 (2006) 1-11
100. Takano T., Pulvers J.N., Inoue T., Tarui H., Sakamoto H., Agata K., and Umesono Y. Regeneration-dependent conditional gene knockdown (Readyknock) in planarian: demonstration of requirement for Djsnap-25 expression in the brain for negative phototactic behavior. Dev. Growth Differ. 49 5 (2007) 383-394
101. Takeuchi Y., Yoshizaki G., Kobayashi T., and Takeuchi T. Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol. Reprod. 67 (2002) 1087-1092
102. Tam P.P., and Zhou S.X. The allocation of the epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulation mouse embryo. Dev. Biol. 178 (1996) 124-132
103. 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
104. Toyooka Y., Tsunekawa N., Takahashi Y., Matsui Y., Satoh M., and Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech. Dev. 93 (2000) 139-149
105. Wang Y., Zayas R.M., Guo T., and Newmark P.A. nanos function is essential for development and regeneration of planarian germ cells. Proc. Natl. Acad. Sci. U. S. A. 104 14 (2007) 5901-5906
106. Williamson A., and Lehmann R. Germ cell development in Drosophila. Annu. Rev. Cell Dev. Biol. 12 (1996) 365-391
107. Wolff E. Recent researches on the regeneration of planaria. In: Rudnick D. (Ed). 20th Growth Symposium (Regeneration) (1962), Ronald Press, New York 53-84
108. Wolke U., Weidinger G., Koprunner M., and Raz E. Multiple levels of posttranscriptional control lead to germ line-specific gene expression in the zebrafish. Curr. Biol. 12 (2002) 289-294
109. Xu H., Gui J., and Hong Y. Differential expression of vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Dev. Dyn. 233 (2005) 872-882
110. 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
111. Yoshizaki G., Tago Y., Takeuchi Y., Sawatari E., Kobayashi T., and Takeuchi T. Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in salmonidae. Biol. Reprod. 73 (2005) 88-93
112. Zayas R.M., Hernandez A., Habermann B., Wang Y., Stary J.M., and Newmark P.A. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 18491-18496