Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: Ancient association of "germline genes" with stemness

Developmental Biology

Volumn 350, Issue 1, 2011, Pages 183-197

  Alié, Alexandre ^a   Leclère, Lucas ^a,b   Jager, Muriel ^a   Dayraud, Cyrielle ^a   Chang, Patrick ^a   Le Guyader, Hervé ^a   Quéinnec, Eric ^a   Manuel, Michaël ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b Sars International Centre for Marine Molecular Biology   (Norway)

Author keywords

Ctenophore; Evolution; Germline; Piwi; Stem cell; Vasa

Indexed keywords

ARTICLE; CELL RENEWAL; CONTROLLED STUDY; CTENOPHORA; CYTOLOGY; CYTOPLASM; EXPRESSED SEQUENCE TAG; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; NONHUMAN; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PIWI GENE; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN DOMAIN; SOMATIC CELL; STEM CELL; TRANSPOSON; VASA GENE;

ANIMALIA; BILATERIA; CNIDARIA; HYDRIDAE; PLATYHELMINTHES; PLEUROBRACHIA PILEUS; VERTEBRATA;

EID: 78651250489     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.10.019     Document Type: Article

References (94)

1. Abdelhaleem M. RNA helicases: regulators of differentiation. Clin. Biochem. 2005, 38:499-503.
2. Agata K., Nakajima E., Funayama N., Shibata N., Saito Y., Umesono Y. Two different evolutionary origins of stem cell systems and their molecular basis. Semin. Cell Dev. Biol. 2006, 17:503-509.
3. Alunni A., Hermel J.M., Heuzé A., Bourrat F., Jamen F., Joly J.-S. Evidence for neural stem cells in the medaka optic tectum proliferation zones. Dev. Neurobiol. 2010, 70(10):693-713.
4. Arai, F. and Suda, T., 2008. Quiescent stem cells in the niche (July 11, 2008), StemBook, ed. The Stem Cell Research Community, StemBook, doi/10.3824/stembook.1.6.1, http://www.stembook.org.
5. Aravin A.A., Hannon G.J., Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318:761-764.
6. Arendt D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 2008, 9:868-882.
7. Arendt D., Tessmar-Raible K., Snyman H., Dorresteijn A.W., Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004, 306:869-871.
8. Benwitz G. Elektronenmikroskopische Untersuchung der Colloblasten-Entwicklung bei der Ctenophore Pleurobrachia pileus (Tentaculifera, Cydippea). Zoomorphologie 1978, 89:257-278.
9. Bidaut G., Stoeckert J.R. Characterization of unknown adult stem cell samples by large scale data integration and artificial neural networks. Pac. Symp. Biocomput. 2008, 14:356-367.
10. Bosch T.C. Hydra and the evolution of stem cells. Bioessays 2009, 31(4):478-486.
11. Bosch T.C.G., Anton-Erxleben F., Hemmrich G., Khalturin K. The Hydra polyp: nothing but an active stem cell community. Dev. Growth Differ. 2010, 52:15-25.
12. Brown F.D., Keeling E.L., Le A.D., Swalla B.J. Whole body regeneration in a colonial ascidian, Botrylloides violaceus. J. Exp. Zool. B Mol. Dev. Evol. 2009, 312(8):885-900.
13. Brusca R.C., Brusca G.J. Invertebrates 2003, Sinauer, Sunderland, MA. second ed.
14. Castrillon D.H., Quade B.J., Wang T.Y., Quigley C., Crum C.P. The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl Acad. Sci. USA 2000, 97:9585-9590.
15. Chehrehasa F., Meedeniya A.C., Dwyer P., Abrahamsen G., Mackay-Sim A. EdU, a new thymidine analogue for labelling proliferating cells in the nervous system. J. Neurosci. Methods 2009, 177:122-130.
16. Chun C. Die Ctenophoren des Golfes von Neapel und der angrenzenden Meeres-Abschnitte: eine Monographie 1880, Verlag von W, Engelmann, Leipzig.
17. Chun C. Die Dissogonie, eine neue Form der geschlechtlichen Zeugung, Festsch. Zum siehenzigsten Geburtstage Rudorf Leuckarts, Leipzig 1892, 77-108.
18. Cox D., Chao A., Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 2000, 127:503-514.
19. De Mulder K., Kuales G., Pfister D., Willems M., Egger B., Salvenmoser W., Thaler M., Gorny A.K., Hrouda M., Borgonie G., Ladurner P. Characterization of the stem cell system of the acoel Isodiametra pulchra. BMC Dev. Biol. 2009, 9:69.
20. De Mulder K., Pfister D., Kuales G., Egger B., Salvenmoser W., Willems M., Steger J., Fauster K., Micura R., Borgonie G., Ladurner P. Stem cells are differentially regulated during development, regeneration and homeostasis in flatworms. Dev. Biol. 2009, 334:198-212.
21. Denker E., Manuel M., Leclère L., Le Guyader H., Rabet N. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev. Biol. 2008, 315:99-113.
22. Derelle R., Manuel M. Ancient connection between NKL genes and the mesoderm? Insights from Tlx expression in a ctenophore. Dev. Genes Evol. 2007, 217:253-261.
23. Dunlap, H.L., 1966. Oogenesis in the Ctenophora. Ph.D. Thesis, University of Washington, Seattle, Washington.
24. Dunlap-Pianka H. Ctenophora. Acoelomate and Pseudocoelomate Metazoans 1974, 1:281-304. Academic Press, New-York. A.C. Giese, J.S. Pearse (Eds.).
25. Dunn C.V., Hejnol A., Matus D.Q., Pang K., Browne W.E., Smith S.A., Seaver E., Rouse G.W., Obst M., Edgecombe G.D., Sørensen M.V., Haddock S.H.D., Schmidt-Rhaesa A., Okusu A., Kristensen R.M., Wheeler W.C., Martindale M.Q., Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
26. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
27. Eisenman E.A., Alfert M. A new fixation procedure for preserving the ultrastructure of marine invertebrate tissues. J. Microsc. 1981, V125:117-120.
28. Fleming H.E., Janzen V., Lo Celso C., Guo J., Leahy K.M., Kronenberg H.M., Scadden D.T. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2008, 2:274-283.
29. Foresta C., Ferlin A., Moro E. Deletion and expression analysis of AZFa genes on the human Y chromosome revealed a major role for DBY in male infertility. Hum. Mol. Genet. 2000, 9(8):1161-1169.
30. Franc J.M. La mésoglée des cténaires: Approches ultrastructurale, biochimique et métabolique 1985, Université Claude Bernard - Lyon I, Lyon.
31. Funayama N. The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev. Growth Differ. 2010, 52:1-14.
32. Funayama N., Nakatsukasa M., Mohri K., Masuda Y., Agata K. Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol. Dev. 2010, 12:275-287.
33. Gilbert S.F. Developmental Biology 2010, Sinauer, Sunderland MA. ninth ed.
34. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
35. Guo T., Peters A.H.F.M., Newmark P.A. A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 2006, 11:159-169.
36. Gustafson E.A., Wessel G.M. Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 2010, 32:626-637.
37. Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G.W., Edgecombe G.D., Martinez P., Baguñà J., Bailly X., Jondelius U., Wiens M., Müller W.E.G., Seaver E., Wheeler W.C., Martindale M.Q., Giribet G., Dunn C.W. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. Lond. B Biol. Sci. 2009, 276:4261-4270.
38. Hemmrich G., Bosch T.C. Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem-cell differentiation. Bioessays 2008, 30:1010-1018.
39. Hernandez-Nicaise M.-L. Ctenophora. Volume II: Placozoa, Porifera, Cnidaria, and Ctenophora 1991, 359-418. John Wiley, New York. F.W. Harrison, J.A. Westfall (Eds.).
40. Hertwig R. Ueber den Bau der Ctenophoren. Jena. Z. Naturwiss. 1880, 14:313-457.
41. Houliston E., Momose T., Manuel M. Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends Genet. 2010, 26:159-167.
42. Houwing S., Kamminga L.M., Berezikov E., Cronembold D., Girard A., van den Elst H., Filippov D.V., Blaser H., Raz E., Moens C.B., Plasterk R.H., Hannon G.J., Draper B.W., Ketting R.F. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 2007, 129(1):69-82.
43. Ikenishi K., Tanaka T.S. Spatio-temporal expression of Xenopus Vasa homolog, SVLG1, in oocytes and embryos: the presence of XVLG1 RNA in somatic cells as well as germline cells. Dev. Growth Differ. 2000, 42(2):95-103.
44. Ivanova N.B., Dimos J.T., Schaniel C., Hackney J.A., Moore K.A., Lemischka I.R. A stem cell molecular signature. Science 2002, 298:601-604.
45. Ivanova N.B., Dimos J.T., Schaniel C., Hackney J.A., Moore K.A., Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., Melton D.A., Lemischka I.R. Response to comments on "Stemness: transcriptional profiling of embryonic and adult stem cells" and "A stem cell molecular signature". Science 2003, 302:393.
46. Jager M., Quéinnec E., Chiori R., Le Guyader H., Manuel M. Insights into the early evolution of SOX genes from expression analyses in a ctenophore. J. Exp. Zool. B Mol. Dev. Evol. 2008, 310:650-667.
47. Jager, M., Chiori, R., Alié, A., Dayraud, C., Quéinnec, E., Manuel, M., in press. New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Müller, 1776). J. Exp. Zool. B Mol. Dev. Evol.
48. Johnstone O., Deuring R., Bock R., Linder P., Fuller M.T., Lasko P. Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Dev. Biol. 2005, 277:92-101.
49. Juliano C.E., Wessel G.M. An evolutionary transition of Vasa regulation in echinoderms. Evol. Dev. 2009, 11(5):560-573.
50. Juliano C.E., Voronina E., Stack C., Aldrich M., Cameron A.R., Wessel G.M. Germ line determinants are not localized early in sea urchin development, but do accumulate in the small micromere lineage. Dev. Biol. 2006, 300(1):406-415.
51. Khalturin K., Anton-Erxleben F., Milde S., Plötz C., Wittlieb J., Hemmrich G., Bosch T.C.G. Transgenic stem cells in Hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Dev. Biol. 2007, 309:32-44.
52. Krovel A.V., Olsen L.C. Expression of a vas:EGFP transgene in primordial germ cells of the zebrafish. Mech. Dev. 2002, 116(1-2):141-150.
53. Kuramochi-Miyagawa S., Kimura T., Yomogida K., Kuroiwa A., Tadokoro Y., Fujita Y., Sato M., Matsuda Y., Nakano T. Two mouse piwi-related genes: miwi and mili. Mech. Dev. 2001, 108(1-2):121-133.
54. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Takamatsu K., Chuma S., Kojima-Kita K., Shiromoto Y., Asada N., Toyoda A., Fujiyama A., Totoki Y., Shibata T., Kimura T., Nakatsuji N., Noce T., Sasaki H., Nakano T. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010, 24(9):887-892.
55. Lasko P.F., Ashburner M. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 1990, 4:905-921.
56. Lau N.C., Ohsumi T., Borowsky M., Kingston R.E., Blower M.D. Systematic and single cell analysis of Xenopus Piwi-interacting RNAs and Xiwi. EMBO J. 2009, 28(19):2945-2958.
57. Leclère, L. 2008. Evolution de la reproduction sexuée des hydrozoaires: aspects historiques, analyse phylogénétique et développementale. Thèse de l'Université Pierre Marie Curie, Paris.
58. Lin H., Spradling A. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997, 124:2463-2476.
59. Liu N., Han H., Lasko P. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3' UTR. Genes Dev. 2009, 23:2742-2752.
60. Martindale M.Q. Larval reproduction in the ctenophore, Mnemiopsis myccradyi (order Lobata). Mar. Biol. 1987, 94:409-414.
61. Martindale M.Q., Henry J. Ctenophorans, the Comb Jellies. Embryology: constructing the organism 1997, 87-111. Sinauer, Sunderland, MA. S.F. Gilbert, A.M. Raunio (Eds.).
62. Miller D.J., Ball E.E., Technau U. Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet. 2005, 21:536-539.
63. Mochizuki K., Nishimiya-Fujisawa C., Fujisawa T. Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev. Genes Evol. 2001, 211:299-308.
64. Müller W.E.G. The stem cell concept in sponges (Porifera): metazoan traits. Semin. Cell Dev. Biol. 2006, 17:481-491.
65. Pfister D., De Mulder K., Hartenstein V., Kuales G., Borgonie G., Marx F., Morris J., Ladurner P. Flatworm stem cells and the germ line: developmental and evolutionary implications of macvasa expression in Macrostomum lignano. Dev. Biol. 2008, 319:146-159.
66. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Quéinnec E., Da Silva C., Wincker P., Le Guyader H., Leys S., Jackson D.J., Schreiber F., Erpenbeck D., Morgenstern B., Wörheide G., Manuel M. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
67. Pick K.S., Philippe H., Schreiber F., Erpenbeck D., Jackson D.J., Wrede P., Wiens M., Alié A., Morgenstern B., Manuel M., Wörheide G. Improved phylogenomic taxon sampling noticeably affects non-bilaterian relationships. Mol. Biol. Evol. 2010, 27(9):1983-1987.
68. Putnam N.H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V.V., Jurka J., Genikhovich G., Grigoriev I.V., Lucas S.M., Steele R.E., Finnerty J.R., Technau U., Martindale M.Q., Rokhsar D.S. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94.
69. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002, 298:597-600.
70. Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 2000, 1(3).
71. Rebscher N., Zelada-González F., Banisch T., Raible F., 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. 2007, 306:599-611.
72. Rebscher N., Volk C., Teo R., Plickert G. The germ plasm component vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev. Dyn. 2008, 237:1736-1745.
73. Reddien P.W., Oviedo N.J., Jennings J.R., Jenkin J.C., Sanchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005, 310:1327-1330.
74. Rosner A., Paz G., Rinkevich B. Divergent roles of the DEAD-box protein BS-PL10, the urochordate homologue of human DDX3 and DDX3Y proteins, in colony astogeny and ontogeny. Dev. Dyn. 2006, 235:1508-1521.
75. Rosner A., Moiseeva E., Rinkevich Y., Lapidot Z., Rinkevich B. Vasa and the germ line lineage in a colonial urochordate. Dev. Biol. 2009, 331(2):113-128.
76. Seipel K., Yanze N., Schmid V. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int. J. Dev. Biol. 2004, 48:1-7.
77. Sharma A.K., Nelson M.C., Brandt J.E., Wessman M., Mahmud N., Weller K.P., Hoffman R. Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 2001, 97(2):426-434.
78. Shibata N., Umesono Y., Orii H., Sakurai T., Watanabe K., Agata K. Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev. Biol. 1999, 206:73-87.
79. Siomi M.C., Miyoshi T., Siomi H. piRNA-mediated silencing in Drosophila germlines. Semin. Cell Dev. Biol. 2010, 21(7):754-759.
80. Snee M., Benz D., Jen J., Macdonald P.M. Two distinct domains of Bruno bind specifically to the oskar mRNA. RNA Biol. 2008, 5(1):1-9.
81. Spike C., Meyer N., Racen E., Orsborn A., Kirchner J., Kuznicki K., Yee C., Bennett K., Strome S. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 2008, 178(4):1973-1987.
82. Srivastava M., Begovic E., Chapman J., Putnam N.H., Hellsten U., Kawashima T., Kuo A., Mitros T., Salamov A., Carpenter M.L., Signorovitch A.Y., Moreno M.A., Kamm K., Grimwood J., Schmutz J., Shapiro H., Grigoriev I.V., Buss L.W., Schierwater B., Dellaporta S.L., Rokhsar D.S. The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955-960.
83. Sun M.G., Williams J., Munoz-Pinedo C., Perkins G.A., Brown J.M., Ellisman M.H., Green D.R., Frey T.G. Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 2007, 9:1057-1065.
84. Sunanaga T., Saito Y., Kawamura K. Postembryonic epigenesist of Vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian, Botryllus primigenus. Dev. Growth Differ. 2006, 48:87-100.
85. Sunanaga T., Watanabe A., Kawamura K. Involvement of vasa homolog in germline recruitment from coelomic stem cells in budding tunicates. Dev. Genes Evol. 2007, 217:1-11.
86. Tang F. Small RNAs in mammalian germline: tiny for immortal. Differentiation 2010, 79:141-146.
87. Thomson T., Lin H. The biogenesis and function PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 2009, 25:355-376.
88. Vagin V.V., Klenov M.S., Kalmikova A.I., Stolyanrenko A.D., Kotelnikov R.N., Gvozdev V.A. The RNA interference proteins and Vasa locus are involved in the same silencing of retrotransposon in the female germline of Drosophila melanogaster. RNA Biol. 2004, 1:54-58.
89. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
90. Vong Q.P., Li Y., Lau Y.-F.C., Dym M., Rennert O.M., Chan W.-Y. Structural characterization and expression studies of Dby and its homologs in the mouse. J. Androl. 2006, 27(5):653-661.
91. Webster P.J., Liang L., Berg C.A., Lasko P., Macdonald P.M. Translational repressor bruno plays multiple roles in development and is widely conserved. Genes Dev. 1997, 11:2510-2521.
92. Weissman I., Anderson D., Gage F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu. Rev. Cell Dev. Biol. 2001, 17:387-403.
93. Wu Q., Ma Q., Shehadeh L.A., Wilson A., Xia L., Yu H., Webster K.A. Expression of the Argonaute protein PiwiL2 and piRNAs in adult mouse mesenchymal stem cells. Biochem. Biophys. Res. Commun. 2010, 396(4):915-920.
94. Yin H., Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007, 450. 304-U16.