The Parhyale germline project
For certain animals such as sponges, cnidarians, flatworms, and colonial sea squirts, replacing a lost germline (the population of diploid cells that ultimately produces haploid gametes) is a simple corollary of total body plan regeneration (Bely and Nyberg 2009). Many types of animals, however, lack such powers of regeneration and cannot replace a lost germline; examples include humans and the familiar research models Caenorhabditis, Drosophila, Xenopus, Danio, and Mus (e.g., Barnes et al. 2006; Klein et al. 2010; Nieuwkoop and Sutasurya 1979; Sulston et al. 1983; Weidinger et al. 2003).
Research from our lab demonstrates the extraordinary ability of Parhyale hawaiensis, a marine amphipod crustacean, to replace its germline despite being incapable of total body plan regeneration. Experimental elimination of Parhyale’s germline progenitor cell (which is specified embryonically by the 8-cell stage) results in an absence of primordial germ cells, as assayed by several criteria, including loss of expression of Vasa, a highly conserved germline RNA helicase. Remarkably, a return of Vasa expression is observed in the gonads of these animals approximately one month after hatching (halfway to adulthood), and when maturation is finally reached, these animals are fully fertile. Thus, Parhyale exhibits two mechanisms of germline formation: during normal development, the germline forms cell-autonomously in the early embryo due to topographic restriction of maternally provided determinants (including vasa transcripts) (Extavour 2005; Gerberding et al. 2002; Özhan-Kizil et al. 2009), and during contingency-based development, a lost germline is replaced postembryonically via induction. In no other bilaterian has this flexibility been demonstrated.
Due to the absence of a normally specified germline, this replacement process necessarily involves an endogenous mechanism effecting soma-to-de novo germline stem cell transdifferentiation. To gain deeper insight into this unprecedented process, we are investigating 1) the source of the somatically derived replacement cells, and 2) the signaling events between gonadal cells that regulate replacement. In addition to its implications for evo-devo biology, our research is biomedically relevant in that it seeks to elucidate a seemingly clear-cut example of endogenously acquired developmental plasticity, and it promotes the Parhyale gonad as a highly tractable model for studying the interactions between stem cells and their supporting cellular niche.
Barnes AI, Boone JM, Jacobson J, Partridge L, Chapman T (2006) No extension of lifespan by ablation of germ line in Drosophila. Proc R Soc B 273:939-947
Bely AE, Nyberg KG (2009) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25:161-170
Extavour CG (2005) The fate of isolated blastomeres with respect to germ cell formation in the amphipod crustacean Parhyale hawaiensis. Dev Biol 277:387-402
Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789-5801
Klein AM, Nakagawa T, Ichikawa R, Yoshida S, Simons BD (2010) Mouse germ line stem cell undergo rapid and stochastic turnover. Cell Stem Cell 7:214-224
Nieuwkoop PD, Sutasurya LA (1979) Primordial germ cells in the chordates: embryogenesis and phylogenesis. Cambridge University Press, Cambridge, England
Özhan-Kizil G, Havemann J, Gerberding M (2009) Germ cells in the crustacean Parhyale hawaiensis depend on Vasa protein for their maintenance but not for their formation. Dev Biol 327:230-239
Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64-119
Weidinger G, Stebler J, Slanchev K, Durnstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E (2003) dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429-1434