Whole body regeneration in a colonial ascidian, Botrylloides violaceus

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 312, Issue 8, 2009, Pages 885-900

  Brown, Federico D ^a,c   Keeling, Elena L ^a,b,d   Le, Anna D ^a,b   Swalla, Billie J ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^d CALIFORNIA POLYTECHNIC STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE;

ANIMAL; ARTICLE; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REGENERATION; UROCHORDATA; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; IMMUNOHISTOCHEMISTRY; PROLIFERATING CELL NUCLEAR ANTIGEN; REGENERATION; UROCHORDATA;

ASCIDIA; ASCIDIACEA; BOTRYLLOIDES VIOLACEUS; CHORDATA;

EID: 70449093932     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.21303     Document Type: Article

References (67)

1. Ambros V, Chen X. 2007. The regulation of genes and genomes by small RNAs. Development (Cambridge, England) 134:1635-1641.
2. Bancroft F. 1903. Variation and fusion of colonies in compound ascidians. Proc Calif Acad Sci 3:137-186.
3. Berrill NJ. 1941a. Size and morphogenesis in the bud of Botryllus. Biol Bull 80:185-193.
4. Berrill NJ. 1941b. The development of the bud in Botryllus. Biol Bull 80:169-184.
5. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089-1103.
6. Brown FD, Swalla BJ. 2007. Vasa expression in a colonial ascidian, Botrylloides violaceus. Evol Dev 9:165-177.
7. Burighel P, Cloney RA. 1997. Urochordata: Ascidiacea. Microscopic Anatomy of Invertebrates Hemichordata, Chaetognatha, and the Invertebrate Chordates. p 221-347.
8. Candia Carnevali MD. 2006. Regeneration in echinoderms: repair, regrowth, cloning. ISJ 3:64-76.
9. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ. 2007. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12:503-514.
10. Cima F, Perin A, Burighel P, Ballarin L. 2001. Morphofunctional characterization of haemocytes of the compound ascidian Botrylloides leachi (Tunicata, Ascidiacea). Acta Zool 82:261-274.
11. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. 1998. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 12:3715-3727.
12. Cox DN, Chao A, Lin H. 2000. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development (Cambridge, England) 127:503-514.
13. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KEM, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science (New York, NY) 298:2157-2167.
14. De Leo G. 1992. Ascidian hemocytes and their involvement in defense reaction. Boll Zoll 59:195-213.
15. Deng W, Lin H. 2002. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2:819-830.
16. Extavour CG, Akam M. 2003. Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development (Cambridge, England) 130:5869-5884.
17. Freeman G. 1964. The role of blood cells in the process of asexual reproduction in the tunicate Perophora viridis. J Exp Zool 156:157-184.
18. Fujiwara S, Kawamura K. 1992. Ascidian budding as a transdifferentiation-like system-multipotent epithelium is not undifferentiated. Dev Growth Differ 34:463-472.
19. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455:1193-1197.
20. Grivna ST, Pyhtila B, Lin H. 2006. MIWI associates with translational machinery and PIWI-interacting RNAs (piR-NAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 103:13415-13420.
21. Hiruta J, Mazet F, Ogasawara M. 2006. Restricted expression of NADPH oxidase/peroxidase gene (Duox) in zone VII of the ascidian endostyle. Cell Tissue Res 326:835-841.
22. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, Draper BW, Ketting RF. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129:69-82.
23. Hyslop LA, Armstrong L, Stojkovic M, Lako M. 2005. Human embryonic stem cells: biology and clinical implications. Expert Rev Mol Med 7:1-21.
24. Kawamura K, Fujiwara S, Sugino YM. 1991. Budding-specific lectin induced in epithelial cells is an extracellular matrix component for stem cell aggregation in tunicates. Development (Cambridge, England) 113:995-1005.
25. Laird DJ, Weissman IL. 2004. Telomerase maintained in selfrenewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol 273:185-194.
26. Laird DJ, De Tomaso AW, Weissman IL. 2005. Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351-1360.
27. Laird DJ, von Andrian UH, Wagers AJ. 2008. Stem cell trafficking in tissue development, growth, and disease. Cell 132:612-630.
28. Lin H. 2007. piRNAs in the germ line. Science (New York, NY) 316:397.
29. Manni L, Zaniolo G, Cima F, Burighel P, Ballarin L. 2007. Botryllus schlosseri: a model ascidian for the study of asexual reproduction. Dev Dyn 236:335-352.
30. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. 2002. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110:689-699.
31. Morgan TH. 1901. Regeneration. New York: Macmillan Co.
32. Murphy D, Dancis B, Brown JR. 2008. The evolution of core proteins involved in microRNA biogenesis. BMC Evol Biol 8:92.
33. Nakauchi M. 1982. Asexual development of ascidians: its biological significance, diversity, and morphogenesis. Am Zool 22:753-763.
34. O'Donnell KA, Boeke JD. 2007. Mighty Piwis defend the germline against genome intruders. Cell 129:37-44.
35. Ogasawara M, Satoh N. 1998. Isolation and characterization of endostyle-specific genes in the ascidian Ciona intestinalis. Biol Bull 195:60-69.
36. Oka H, Watanabe H. 1957. Vascular Budding, a new type of budding in Botryllus. Biol Bull 112:225-240.
37. Oka H, Watanabe H. 1959. Vascular budding in Botrylloides. Biol Bull 117:340-346.
38. Overton J. 1966. The fine structure of blood cells in the ascidian Perophora viridis. J Morphol 119:305-326.
39. Parker JS, Roe SM, Barford D. 2005. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434:663-666.
40. Pestarino M. 1992. The distribution of neuropeptide Y-like immunoreactivity in the ascidian Styela plicata. Cell Mol Biol 38:255-262.
41. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science (New York, NY) 310:1327-1330.
42. Rinkevich B, Shlemberg Z, Fishelson L. 1995. Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695-7699.
43. Rinkevich Y, Paz G, Rinkevich B, Reshef R. 2007. Systemic bud induction and retinoic acid signaling underlie whole body regeneration in the urochordate Botrylloides leachi. PLoS Biol 5:e71.
44. Rosner A, Paz G, Rinkevich B. 2006. 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 235:1508-1521.
45. Rossi L, Salvetti A, Lena A, Batistoni R, Deri P, Pugliesi C, Loreti E, Gremigni V. 2006. DjPiwi-1, a member of the PAZPiwi gene family, defines a subpopulation of planarian stem cells. Dev Genes Evol 216:335-346.
46. Rychel AL, Swalla BJ. 2008. Anterior regeneration in the hemichordate Ptychodera flava. Dev Dyn 237:3222-3232.
47. Sabbadin A, Zaniolo G, Majone F. 1975. Determination of polarity and bilateral asymmetry in palleal and vascular buds of the ascidian Botryllus schlosseri. Dev Biol 46:79-87.
48. Sanchez Alvarado A. 2000. Regeneration in the metazoans: why does it happen? Bioessays 22:578-590.
49. Satou Y, Takatori N, Yamada L, Mochizuki Y, Hamaguchi M, Ishikawa H, Chiba S, Imai K, Kano S, Murakami SD, Nakayama A, Nishino A, Sasakura Y, Satoh G, Shimotori T, Shin IT, Shoguchi E, Suzuki MM, Takada N, Utsumi N, Yoshida N, Saiga H, Kohara Y, Satoh N. 2001. Gene expression profiles in Ciona intestinalis tailbud embryos. Development (Cambridge, England) 128:2893-2904.
50. Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A, Hamaguchi M, Awazu S, Yagi K, Sasakura Y, Nakayama A, Ishikawa H, Inaba K, Satoh N. 2002. A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153-154.
51. Seipel K, Yanze N, Schmid V. 2004. The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. Int J Dev Biol 48:1-7.
52. Seto AG, Kingston RE, Lau NC. 2007. The coming of age for Piwi proteins. Mol Cell 26:603-609.
53. Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Weller KP, Hoffman R. 2001. Human CD34(1) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 97:426-434.
54. Sunanaga T, Saito Y, Kawamura K. 2006. Postembryonic epigenesis of Vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian, Botryllus primigenus. Dev Growth Differ 48:87-100.
55. Sunanaga T, Satoh M, Kawamura K. 2008. The role of Nanos homologue in gametogenesis and blastogenesis with special reference to male germ cell formation in the colonial ascidian, Botryllus primigenus. Dev Biol 324:31-40.
56. Swalla BJ, Solursh M. 1984. Epithelial enhancement of connective tissue differentiation in explanted somites. J Embryol Exp Morphol 79:243-255.
57. Taneda Y, Watanabe H. 1982. Studies on colony specificity in the compound ascidian, Botryllus primigenus Oka. II. In vivo bioassay for analyzing the mechanism of ''nonfusion'' reaction. Dev Comp Immunol 6:243-252.
58. Thorndyke MC, Chen WC, Beesley PW, Patruno M. 2001. Molecular approach to echinoderm regeneration. Microsc Res Tech 55:474-485.
59. Tiozzo S, Brown FD, De Tomaso AW. 2008. Regeneration and stem cells in ascidians. In: Bosch TCG, editor. Stem cells from hydra to man. Dordrecht, Netherlands: Springer. p 95-112.
60. Voskoboynik A, Simon-Blecher N, Soen Y, Rinkevich B, De Tomaso AW, Ishizuka KJ, Weissman IL. 2007. Striving for normality: whole body regeneration through a series of abnormal generations. Faseb J 21:1335-1344.
61. Voskoboynik A, Soen Y, Rinkevich Y, Rosner A, Ueno H, Reshef R, Ishizuka KJ, Palmeri KJ, Moiseeva E, Rinkevich B, Weissman IL. 2008. Identification of the endostyle as a stem cell niche in a colonial chordate. Cell Stem Cell 3:456-464.
62. Weissman IL. 2000. Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157-168.
63. Wong MD, Jin Z, Xie T. 2005. Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 39:173-195.
64. Wright RK. 1981. Urochordates. In: Ratcliffe NA, Rowley AF, editors. Invertebrate blood cells. London: Academic Press. p 565-626.
65. Wylie C. 2000. Germ cells. Curr Opin Genet Dev 10:410-413.
66. Zeng L, Jacobs MW, Swalla BJ. 2006. Coloniality and sociality has evolved once in stolidobranch ascidians. Integr Comp Biol 46:255-268.
67. Zhang X. 2006. On the function of the Dictyostelium Argonaute A protein (AGnA) in epigenetic gene regulation. Kassel: Universität Kassel. 150p.