全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

The Origin And Migration Of Primordial Germ Cells In Sturgeons

DOI: 10.1371/journal.pone.0086861

Full-Text   Cite this paper   Add to My Lib

Abstract:

Primordial germ cells (PGCs) arise elsewhere in the embryo and migrate into developing gonadal ridges during embryonic development. In several model animals, formation and migration patterns of PGCs have been studied, and it is known that these patterns vary. Sturgeons (genus Acipenser) have great potential for comparative and evolutionary studies of development. Sturgeons belong to the super class Actinoptergii, and their developmental pattern is similar to that of amphibians, although their phylogenetic position is an out-group to teleost fishes. Here, we reveal an injection technique for sturgeon eggs allowing visualization of germplasm and PGCs. Using this technique, we demonstrate that the PGCs are generated at the vegetal pole of the egg and they migrate on the yolky cell mass toward the gonadal ridge. We also provide evidence showing that PGCs are specified by inheritance of maternally supplied germplasm. Furthermore, we demonstrate that the migratory mechanism is well-conserved between sturgeon and other remotely related teleosts, such as goldfish, by a single PGCs transplantation (SPT) assay. The mode of PGCs specification in sturgeon is similar to that of anurans, but the migration pattern resembles that of teleosts.

References

[1]  Grande L, Bemis WE (1991) Osteology and Phylogenetic Relationships of Fossil and Recent Paddlefishes (Polyodontidae) with Comments on the Interrelationships of Acipenseriformes. Journal of Vertebrate Paleontology 11: 1–121 doi:10.1080/02724634.1991.10011424.
[2]  Inoue JG, Miya M, Venkatesh B, Nishida M (2005) The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349: 227–235 doi:10.1016/j.gene.2005.01.008.
[3]  Bolker JA (2004) Embryology. In: LeBreton G, Beamish F, McKinley RS, editors. Sturgeons and paddlefish of North America. Kluwer Academic Publishers. 134–146.
[4]  Elinson RP (2009) Nutritional endoderm: a way to breach the holoblastic-meroblastic barrier in tetrapods. J Exp Zool 312B: 526–532 doi:10.1002/jez.b.21218.
[5]  Ballard WW, Ginsburg AS (1980) Morphogenetic movements in acipenserid embryos. J Exp Zool 213: 69–103. doi: 10.1002/jez.1402130110
[6]  Bolker JA (1993) Gastrulation and mesoderm morphogenesis in the white sturgeon. J Exp Zool 266: 116–131 doi:10.1002/jez.1402660206.
[7]  Ginsburg AS, Dettlaff TA (1991) The russian sturgeon Acipenser guldensadti. Part1. Gametes and early development up to time of hatching. In: Dettlaff TA, Vassetzky SG, editors. Animal species for developmental studies, Volume2, Vertebrates. Springer. 16–65.
[8]  Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253–310 doi:10.1002/aja.1002030302.
[9]  Cooper MS, Virta VC (2007) Evolution of gastrulation in the ray-finned (actinopterygian) fishes. J Exp Zool B Mol Dev Evol 308: 591–608 doi:10.1002/jez.b.21142.
[10]  Bolker JA (1993) The mechanism of gastrulation in the white sturgeon. J Exp Zool 266: 132–145 doi:10.1002/jez.1402660207.
[11]  Takeuchi M, Okabe M, Aizawa S (2009) The Genus Polypterus (Bichirs): A Fish Group Diverged at the Stem of Ray-Finned Fishes (Actinopterygii). Cold Spring Harbor Protocols 2009: pdb.emo117–pdb.emo117 doi:10.1101/pdb.emo117.
[12]  Takeuchi M, Takahashi M, Okabe M, Aizawa S (2009) Germ layer patterning in bichir and lamprey; an insight into its evolution in vertebrates. Developmental Biology 332: 90–102 doi:10.1016/j.ydbio.2009.05.543.
[13]  Long WL, Ballard WW (2001) Normal embryonic stages of the longnose gar, Lepisosteus osseus. BMC Dev Biol 1: 6.
[14]  Ballard WW (1986) Morphogenetic movements and a provisional fate map of development in the holostean fish Amia calva. J Exp Zool 238: 355–372 doi:10.1002/jez.1402380309.
[15]  Ballard WW (1986) Stages and rates of normal development in the holostean fish Amia calva. J Exp Zool 238: 337–354 doi:10.1002/jez.1402380308.
[16]  Whitington PM, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33: 57–74.
[17]  Houston DW, Zhang J, Maines JZ, Wasserman SA, King ML (1998) A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development 125: 171–180.
[18]  Knaut H, Pelegri F, Bohmann K, Schwarz H, Nüsslein-Volhard C (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. The Journal of Cell Biology 149: 875–888. doi: 10.1083/jcb.149.4.875
[19]  Miyake A, Saito T, Kashiwagi T, Ando D, Yamamoto A, et al. (2006) Cloning and pattern of expression of the shiro-uo vasa gene during embryogenesis and its roles in PGC development. Int J Dev Biol 50: 619–625 doi:10.1387/ijdb.062172am.
[20]  Herpin A, Rohr S, Riedel D, Kluever N, Raz E, et al. (2007) Specification of primordial germ cells in medaka (Oryzias latipes). BMC Dev Biol 7: 3 doi:10.1186/1471-213X-7-3.
[21]  Kitauchi T, Saito T, Motomura T, Arai K, Yamaha E (2012) Distribution and function of germ plasm in cytoplasmic fragments from centrifuged eggs of the goldfish, Carassius auratus. Journal of Applied Ichthyology 28: 998–1005 doi:10.1111/jai.12068.
[22]  Ressom RE, Dixon KE (1988) Relocation and reorganization of germ plasm in Xenopus embryos after fertilization. Development 103: 507–518.
[23]  Savage RM, Danilchik MV (1993) Dynamics of Germ Plasm Localization and Its Inhibition by Ultraviolet Irradiation in Early Cleavage Xenopus Embryos. Developmental Biology 157: 371–382 doi:10.1006/dbio.1993.1142.
[24]  Taguchi A, Takii M, Motoishi M, Orii H, Mochii M, et al. (2012) Analysis of localization and reorganization of germ plasm in Xenopus transgenic line with fluorescence-labeled mitochondria. Dev Growth Differ 54: 767–776 doi:10.1111/dgd.12005.
[25]  Robb DL, Heasman J, Raats J, Wylie C (1996) A kinesin-like protein is required for germ plasm aggregation in Xenopus. Cell 87: 823–831. doi: 10.1016/s0092-8674(00)81990-x
[26]  Pelegri F, Knaut H, Maischein HM, Schulte-Merker S, Nüsslein-Volhard C (1999) A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr Biol 9: 1431–1440. doi: 10.1016/s0960-9822(00)80112-8
[27]  Theusch E, Brown K, Pelegri F (2006) Separate pathways of RNA recruitment lead to the compartmentalization of the zebrafish germ plasm. Developmental Biology 292: 129–141 doi:10.1016/j.ydbio.2005.12.045.
[28]  Sutasurja LA, Nieuwkoop PD (1974) The induction of the primordial germ cells in the urodeles. Development Genes and Evolution 175: 199–220 doi:10.1007/BF00582092.
[29]  Takeuchi T, Tanigawa Y, Minamide R, Ikenishi K, Komiya T (2010) Analysis of SDF-1/CXCR4 signaling in primordial germ cell migration and survival or differentiation in Xenopus laevis. Mechanisms of Development 127: 146–158 doi:10.1016/j.mod.2009.09.005.
[30]  Heasman J, Hynes RO, Swan AP, Thomas V, Wylie CC (1981) Primordial germ cells of Xenopus embryos: the role of fibronectin in their adhesion during migration. Cell 27: 437–447. doi: 10.1016/0092-8674(81)90385-8
[31]  Yoon C, Kawakami K, Hopkins N (1997) 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: 3157–3165.
[32]  Braat AK, Zandbergen T, van de Water S, Goos HJ, Zivkovic D (1999) Characterization of zebrafish primordial germ cells: Morphology and early distribution of vasa RNA. Dev Dyn 216: 153–167. doi: 10.1002/(sici)1097-0177(199910)216:2<153::aid-dvdy6>3.0.co;2-1
[33]  Weidinger G, Wolke U, K?prunner M, Klinger M, Raz E (1999) Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126: 5295–5307.
[34]  Doitsidou M, Reichman-Fried M, Stebler J, K?prunner M, Dorries J, et al. (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111: 647–659. doi: 10.1016/s0092-8674(02)01135-2
[35]  Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, et al. (2008) Control of Chemokine-Guided Cell Migration by Ligand Sequestration. Cell 132: 463–473 doi:10.1016/j.cell.2007.12.034.
[36]  Nieuwkoop PD, Sutasurya LA (1979) Primordial Germ Cells in the Chordates: Embryogenesis and Phylogenesis. Cambridge University Press.
[37]  Grandi G, Giovannini S, Chicca M (2007) Gonadogenesis in early developmental stages of Acipenser naccarii and influence of estrogen immersion on feminization. Journal of Applied Ichthyology 23: 3–8 doi:10.1111/j.1439-0426.2006.00819.x.
[38]  Grandi G, Chicca M (2008) Histological and ultrastructural investigation of early gonad development and sex differentiation in Adriatic sturgeon (Acipenser naccarii, Acipenseriformes, Chondrostei). J Morphol 269: 1238–1262 doi:10.1002/jmor.10657.
[39]  Bolker JA (1994) Comparison of Gastrulation in Frogs and Fish. Integrative and Comparative Biology 34: 313–322 doi:10.1093/icb/34.3.313.
[40]  K?prunner M, Thisse C, Thisse B, Raz E (2001) A zebrafish nanos-related gene is essential for the development of primordial germ cells. Gene Dev 15: 2877–2885.
[41]  Saito T, Fujimoto T, Maegawa S, Inoue K, Tanaka M, et al. (2006) Visualization of primordial germ cells in vivo using GFP-nos1 3’UTR mRNA. Int J Dev Biol 50: 691–699 doi:10.1387/ijdb.062143ts.
[42]  Bontems F, Stein A, Marlow F, Lyautey J, Gupta T, et al. (2009) Bucky Ball Organizes Germ Plasm Assembly in Zebrafish. Current Biology 19: 414–422 doi:10.1016/j.cub.2009.01.038.
[43]  Saito T, Goto R, Arai K, Yamaha E (2008) Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biology of Reproduction 78: 159–166 doi:10.1095/biolreprod.107.060038.
[44]  Saito T, Goto R, Fujimoto T, Kawakami Y, Arai K, et al. (2010) Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int J Dev Biol 54: 1479–1484 doi:10.1387/ijdb.103111ts.
[45]  Saito T, Goto R, Kawakami Y, Nomura K, Tanaka H, et al.. (2011) The mechanism for primordial germ-cell migration is conserved between Japanese eel and zebrafish. PLoS ONE 6: e24460–. doi:10.1371/journal.pone.0024460.
[46]  Goto R, Saito T, Takeda T, Fujimoto T, Takagi M, et al. (2012) Germ cells are not the primary factor for sexual fate determination in goldfish. Developmental Biology 370: 98–109. doi: 10.1016/j.ydbio.2012.07.010
[47]  Extavour CGM (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130: 5869–5884 doi:10.1242/dev.00804.
[48]  Ewen-Campen B, Schwager EE, Extavour CGM (2009) The molecular machinery of germ line specification. Mol Reprod Dev 77: 3–18 doi:10.1002/mrd.21091.
[49]  Mishima Y, Giraldez AJ, Takeda Y, Fujiwara T, Sakamoto H, et al. (2006) Differential Regulation of Germline mRNAs in Soma and Germ Cells by Zebrafish miR-430. Current Biology 16: 2135–2142 doi:10.1016/j.cub.2006.08.086.
[50]  Giraldez AJ (2006) Zebrafish MiR-430 Promotes Deadenylation and Clearance of Maternal mRNAs. Science 312: 75–79 doi:10.1126/science.1122689.
[51]  Mishima Y (2011) Widespread roles of microRNAs during zebrafish development and beyond. Development.
[52]  Ikenishi K, Kotani M, Tanabe K (1974) Ultrastructural changes associated with UV irradiation in the “germinal plasm” of Xenopus laevis. Developmental Biology 36: 155–168. doi: 10.1016/0012-1606(74)90198-5
[53]  Marlow FL, Mullins MC (2008) Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish. Developmental Biology 321: 40–50 doi:10.1016/j.ydbio.2008.05.557.
[54]  Zelazowska M, Kilarski W, Bilinski SM, Podder DD, Kloc M (2007) Balbiani cytoplasm in oocytes of a primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani body (mitochondrial cloud) of Xenopus laevis oocytes. Cell Tissue Res 329: 137–145 doi:10.1007/s00441-007-0403-9.
[55]  Extavour CGM (2007) Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integrative and Comparative Biology 47: 770–785 doi:10.1093/icb/icm027.
[56]  Johnson AD, Drum M, Bachvarova RF, Masi T, White ME, et al. (2003) Evolution of predetermined germ cells in vertebrate embryos: implications for macroevolution. Evolution & Development 5: 414–431. doi: 10.1046/j.1525-142x.2003.03048.x
[57]  Johnson AD, Richardson E, Bachvarova RF, Crother BI (2011) Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction 141: 291–300 doi:10.1530/REP-10-0474.
[58]  Bachvarova RF, Crother BI, Johnson AD (2009) Evolution of germ cell development in tetrapods: comparison of urodeles and amniotes. Evolution & Development 11: 603–609 doi:10.1111/j.1525-142X.2009.00366.x.
[59]  MacArthur H, Houston DW, Bubunenko M, Mosquera L, King ML (2000) DEADSouth is a germ plasm specific DEAD-box RNA helicase in Xenopus related to eIF4A. Mechanisms of Development 95: 291–295. doi: 10.1016/s0925-4773(00)00357-9
[60]  Hudson C, Woodland HR (1998) Xpat, a gene expressed specifically in germ plasm and primordial germ cells of Xenopus laevis. Mechanisms of Development 73: 159–168. doi: 10.1016/s0925-4773(98)00047-1
[61]  Sekizaki H, Takahashi S, Tanegashima K, Onuma Y, Haramoto Y, et al. (2004) Tracing of Xenopus tropicalis germ plasm and presumptive primordial germ cells with the Xenopus tropicalis DAZ-like gene. Dev Dyn 229: 367–372 doi:10.1002/dvdy.10448.
[62]  Berekelya LA, Ponomarev MB, Luchinskaya NN, Belyavsky AV (2003) Xenopus Germes encodes a novel germ plasm-associated transcript. Gene Expression Patterns 3: 521–524. doi: 10.1016/s1567-133x(03)00055-3
[63]  Horvay K, Clau?en M, Katzer M, Landgrebe J, Pieler T (2006) Xenopus Dead end mRNA is a localized maternal determinant that serves a conserved function in germ cell development. Developmental Biology 291: 1–11 doi:10.1016/j.ydbio.2005.06.013.
[64]  Venkatarama T, Lai F, Luo X, Zhou Y, Newman K, et al. (2010) Repression of zygotic gene expression in the Xenopus germline. Development 137: 651–660 doi:10.1242/dev.038554.
[65]  Strome S, Lehmann R (2007) Germ versus soma decisions: lessons from flies and worms. Science 316: 392–393 doi:10.1126/science.1140846.
[66]  Mizuno T, Yamaha E, Wakahara M, Kuroiwa A, Takeda H (1996) Mesoderm induction in zebrafish. Nature 383: 131–132. doi: 10.1038/383131a0
[67]  Yamaha E, Mizuno T, Hasebe Y, Takeda H, Yamazaki F (1998) Dorsal specification in blastoderm at the blastula stage in the goldfish, Carassius auratus. Dev Growth Differ 40: 267–275. doi: 10.1046/j.1440-169x.1998.t01-1-00002.x
[68]  Maegawa S, Yasuda K, Inoue K (1999) Maternal mRNA localization of zebrafish DAZ-like gene. Mechanisms of Development 81: 223–226. doi: 10.1016/s0925-4773(98)00242-1
[69]  Buchholz DR, Singamsetty S, Karadge U, Williamson S, Langer CE, et al. (2007) Nutritional endoderm in a direct developing frog: a potential parallel to the evolution of the amniote egg. Dev Dyn 236: 1259–1272 doi:10.1002/dvdy.21153.
[70]  Elinson RP, Sabo MC, Fisher C, Yamaguchi T, Orii H, et al. (2011) Germ plasm in Eleutherodactylus coqui, a direct developing frog with large eggs. EvoDevo 2: 20 doi:10.1186/2041-9139-2-20.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133