Stem cell-based growth, regeneration, and remodeling of the planarian intestine

Developmental Biology

Volumn 356, Issue 2, 2011, Pages 445-459

  Forsthoefel, David J ^a   Park, Amanda E ^a   Newmark, Phillip A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Intestine; Neoblast; Organogenesis; Planarian; Regeneration; Remodeling

Indexed keywords

ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; BLASTEMA; CELL DIFFERENTIATION; CONTROLLED STUDY; IN VIVO STUDY; INTESTINE; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE GROWTH; INTESTINE REGENERATION; MORPHOGENESIS; NEOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STEM CELL; TISSUE REGENERATION; TURBELLARIA;

ANIMALIA; PLANARIA; TURBELLARIA;

EID: 79960561671     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.05.669     Document Type: Article

References (100)

1. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004, 11:36-42.
2. Adell T., Saló E., Boutros M., Bartscherer K. Smed-Evi/Wntless is required for β-catenin-dependent and -independent processes during planarian regeneration. Development 2009, 136:905-910.
3. Affolter M., Zeller R., Caussinus E. Tissue remodelling through branching morphogenesis. Nat. Rev. Mol. Cell Biol. 2009, 10:831-842.
4. Agata K., Saito Y., Nakajima E. Unifying principles of regeneration I: epimorphosis versus morphallaxis. Dev. Growth Differ. 2007, 49:73-78.
5. Amcheslavsky A., Jiang J., Ip Y.T. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 2009, 4:49-61.
6. Andrew D.J., Ewald A.J. Morphogenesis of epithelial tubes: insights into tube formation, elongation, and elaboration. Dev. Biol. 2010, 341:34-55.
7. Baguñà J. Dramatic mitotic response in planarians after feeding, and a hypothesis for the control mechanism. J. Exp. Zool. 1974, 190:117-122.
8. Baguñà J. Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. I. Mitotic studies during growth, feeding and starvation. J. Exp. Zool. 1976, 195:53-64.
9. Baguñà J. Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. II. Mitotic studies during regeneration, and a possible mechanism of blastema formation. J. Exp. Zool. 1976, 195:65-80.
10. Baguñá J., Romero R. Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina. Hydrobiologia 1981, 84:181-194.
11. Bergmann A., Steller H. Apoptosis, stem cells, and tissue regeneration. Sci. Signal. 2010, 3:re8.
12. Bowen I.D. Phagocytosis in Polycelis tenuis. Nutrition in the Lower Metazoa 1980, 1-14. Pergamon Press, Oxford. D.C. Smith, Y. Tiffon (Eds.).
13. Bowen I.D., Ryder T.A., Thompson J.A. The fine structure of the planarian Polycelis tenuis Iijima. II. The intestine and gastrodermal phagocytosis. Protoplasma 1974, 79:1-17.
14. Brockes J.P., Kumar A. Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol. 2008, 24:525-549.
15. Brøndsted H.V. Planarian Regeneration 1969, Pergamon Press, Oxford.
16. Bueno D., Baguñà J., Romero R. Cell-, tissue-, and position-specific monoclonal antibodies against the planarian Dugesia (Girardia) tigrina. Histochem. Cell Biol. 1997, 107:139-149.
17. Casali A., Batlle E. Intestinal stem cells in mammals and Drosophila. Cell Stem Cell 2009, 4:124-127.
18. Cebrià F. Regenerating the central nervous system: how easy for planarians!. Dev. Genes Evol. 2007, 217:733-748.
19. Cebrià F., Newmark P.A. Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 2005, 132:3691-3703.
20. Cebrià F., Guo T., Jopek J., Newmark P.A. Regeneration and maintenance of the planarian midline is regulated by a slit orthologue. Dev. Biol. 2007, 307:394-406.
21. Chatterjee M., Ip Y.T. Pathogenic stimulation of intestinal stem cell response in Drosophila. J. Cell. Physiol. 2009, 220:664-671.
22. Crosnier C., Stamataki D., Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet. 2006, 7:349-359.
23. Eisenhoffer G.T., Kang H., Sánchez Alvarado A. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 2008, 3:327-339.
24. Faro A., Boj S.F., Clevers H. Fishing for intestinal cancer models: unraveling gastrointestinal homeostasis and tumorigenesis in zebrafish. Zebrafish 2009, 6:361-376.
25. Forsthoefel D.J., Newmark P.A. Emerging patterns in planarian regeneration. Curr. Opin. Genet. Dev. 2009, 19:412-420.
26. Galliot B., Chera S. The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol. 2010, 20:514-523.
27. García-Arrarás J.E., Estrada-Rodgers L., Santiago R., Torres I.I., Díaz-Miranda L., Torres-Avillán I. Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea:Echinodermata). J. Exp. Zool. 1998, 281:288-304.
28. Garcia-Corrales P., Gamo J. The ultrastructure of the gastrodermal gland cells in the freshwater planarian Dugesia gonocephala s.l. Acta Zool. 1986, 67:43-51.
29. Garcia-Corrales P., Gamo J. Ultrastructural changes in the gastrodermal phagocytic cells of the planarian Dugesia gonocephala s.l. during food digestion (Plathelminthes). Zoomorphology 1988, 108:109-117.
30. Goodchild C.G. Reconstitution of the intestinal tract in the adult leopard frog, Rana pipiens Schreber. J. Exp. Zool. 1956, 131:301-327.
31. 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.
32. Gurley, K.A., Sánchez Alvarado, A., 2008. Stem cells in animal models of regeneration, StemBook, ed. The Stem Cell Research Community, StemBook, http://www.stembook.org.
33. Gurley K.A., Rink J.C., Sánchez Alvarado A. β-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 2008, 319:323-327.
34. Gurley K.A., Elliott S.A., Simakov O., Schmidt H.A., Holstein T.W., Sanchez Alvarado A. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev. Biol. 2010, 347:24-39.
35. Hayashi T., Asami M., Higuchi S., Shibata N., Agata K. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev. Growth Differ. 2006, 48:371-380.
36. Hayashi T., Shibata N., Okumura R., Kudome T., Nishimura O., Tarui H., Agata K. Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its "index sorting" function for stem cell research. Dev. Growth Differ. 2010, 52:131-144.
37. Hyman L.H. The reproductive system and other characters of Planaria dorotocephala Woodworth. Trans. Am. Microsc. Soc. 1925, 44:51-89.
38. Iglesias M., Gomez-Skarmeta J.L., Saló E., Adell T. Silencing of Smed-βcatenin1 generates radial-like hypercephalized planarians. Development 2008, 135:1215-1221.
39. Illa-Bochaca I., Montuenga L.M. The regenerative nidi of the locust midgut as a model to study epithelial cell differentiation from stem cells. J. Exp. Biol. 2006, 209:2215-2223.
40. Ishii S. Electron microscopic observations on the Planarian tissues II. The intestine. Fukushima J. Med. Sci. 1965, 12:67-87.
41. Ishizuya-Oka A. Regeneration of the amphibian intestinal epithelium under the control of stem cell niche. Dev. Growth Differ. 2007, 49:99-107.
42. Jiang H., Patel P.H., Kohlmaier A., Grenley M.O., McEwen D.G., Edgar B.A. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009, 137:1343-1355.
43. Kaneko N., Katsuyama Y., Kawamura K., Fujiwara S. Regeneration of the gut requires retinoic acid in the budding ascidian Polyandrocarpa misakiensis. Dev. Growth Differ. 2010, 52:457-468.
44. Kobayashi C., Kobayashi S., Orii H., Watanabe K., Agata K. Identification of two distinct muscles in the planarian Dugesia japonica by their expression of myosin heavy chain genes. Zoolog. Sci. 1998, 15:861-869.
45. Kobayashi C., Watanabe K., Agata K. The process of pharynx regeneration in planarians. Dev. Biol. 1999, 211:27-38.
46. Lin S.-W. A new technique for planaria. Bios 1931, 2:115-117.
47. Martin F.A., Perez-Garijo A., Morata G. Apoptosis in Drosophila: compensatory proliferation and undead cells. Int. J. Dev. Biol. 2009, 53:1341-1347.
48. Mashanov V.S., Dolmatov I.Y. Ultrastructural features of gut regeneration in five-month-old pentactulae of the holothurian Eupentacta fraudatrix. Russ. J. Mar. Biol. 2001, 27:376-382.
49. Mashanov V.S., Zueva O.R., Rojas-Catagena C., Garcia-Arraras J.E. Visceral regeneration in a sea cucumber involves extensive expression of survivin and mortalin homologs in the mesothelium. BMC Dev. Biol. 2010, 10:117.
50. Merritt A.J., Potten C.S., Kemp C.J., Hickman J.A., Balmain A., Lane D.P., Hall P.A. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res. 1994, 54:614-617.
51. Micchelli C.A., Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006, 439:475-479.
52. Morgan T.H. Experimental studies of the regeneration of Planaria maculata. Arch. Entw. Mech. Org. 1898, 7:364-397.
53. Morgan T.H. Regeneration in planarians. Arch. Entw. Mech. Org. 1900, 10:58-119.
54. Morgan T.H. Regeneration 1901, Macmillan Co., New York.
55. Morgan T.H. Growth and regeneration in Planaria lugubris. Arch. Entw. Mech. Org. 1902, 13:179-212.
56. Newmark P.A., Sánchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 2000, 220:142-153.
57. Newmark P.A., Sánchez Alvarado A. Not your father's planarian: a classic model enters the era of functional genomics. Nat. Rev. Genet. 2002, 3:210-219.
58. Nogi T., Levin M. Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. Dev. Biol. 2005, 287:314-335.
59. Ohlstein B., Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006, 439:470-474.
60. Orii H., Ito H., Watanabe K. Anatomy of the planarian Dugesia japonica I. The muscular system revealed by antisera against myosin heavy chains. Zoolog. Sci. 2002, 19:1123-1131.
61. Orii H., Sakurai T., Watanabe K. Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev. Genes Evol. 2005, 215:143-157.
62. Ortiz-Pineda P.A., Ramirez-Gomez F., Perez-Ortiz J., Gonzalez-Diaz S., Santiago-De Jesus F., Hernandez-Pasos J., Del Valle-Avila C., Rojas-Cartagena C., Suarez-Castillo E.C., Tossas K., Mendez-Merced A.T., Roig-Lopez J.L., Ortiz-Zuazaga H., Garcia-Arraras J.E. Gene expression profiling of intestinal regeneration in the sea cucumber. BMC Genomics 2009, 10:262.
63. O'Steen W.K. Regeneration of the intestine in adult urodeles. J. Morphol. 1958, 103:435-477.
64. O'Steen W.K. Regeneration and repair of the intestine in Rana clamitans larvae. J. Exp. Zool. 1959, 141:449-475.
65. O'Steen W.K., Walker B.E. Radioautographic studies of regeneration in the common newt III. Regeneration and repair of the intestine. Anat. Rec. 1962, 142:179-187.
66. Oviedo N.J., Newmark P.A., Sánchez Alvarado A. Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev. Dyn. 2003, 226:326-333.
67. Oviedo N.J., Morokuma J., Walentek P., Kema I.P., Gu M.B., Ahn J.M., Hwang J.S., Gojobori T., Levin M. Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev. Biol. 2010, 339:188-199.
68. Palakodeti D., Smielewska M., Lu Y.C., Yeo G.W., Graveley B.R. The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 2008, 14:1174-1186.
69. Pearson B.J., Eisenhoffer G.T., Gurley K.A., Rink J.C., Miller D.E., Sánchez Alvarado A. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn. 2009, 238:443-450.
70. Pellettieri J., Fitzgerald P., Watanabe S., Mancuso J., Green D.R., Sánchez Alvarado A. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2009, 338:76-85.
71. Petersen C.P., Reddien P.W. Smed-βcatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
72. Poss K.D. Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat. Rev. Genet. 2010, 11:710-722.
73. Potten C.S. The significance of spontaneous and induced apoptosis in the gastrointestinal tract of mice. Cancer Metastasis Rev. 1992, 11:179-195.
74. Potten C.S. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1998, 353:821-830.
75. Potten C.S. Radiation, the ideal cytotoxic agent for studying the cell biology of tissues such as the small intestine. Radiat. Res. 2004, 161:123-136.
76. Potten C.S., Booth C., Pritchard D.M. The intestinal epithelial stem cell: the mucosal governor. Int. J. Exp. Pathol. 1997, 78:219-243.
77. Radtke F., Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 2005, 307:1904-1909.
78. Reddien P.W., Sánchez Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 2004, 20:725-757.
79. Reddien P.W., Oviedo N.J., Jennings J.R., Jenkin J.C., Sánchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005, 310:1327-1330.
80. Robb S.M., Ross E., Sánchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 2008, 36:D599-D606.
81. Rossi L., Salvetti A., Lena A., Batistoni R., Deri P., Pugliesi C., Loreti E., Gremigni V. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev. Genes Evol. 2006, 216:335-346.
82. Rossi L., Salvetti A., Marincola F.M., Lena A., Deri P., Mannini L., Batistoni R., Wang E., Gremigni V. Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol. 2007, 8:R62.
83. Rouhana L., Shibata N., Nishimura O., Agata K. Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Dev. Biol. 2010, 341:429-443.
84. Sakai T., Kato K., Watanabe K., Orii H. Planarian pharynx regeneration revealed by the expression of myosin heavy chain-A. Int. J. Dev. Biol. 2002, 46:329-332.
85. Salò E., Baguñà J. Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J. Embryol. Exp. Morphol. 1984, 83:63-80.
86. Salò E., Baguñà J. Cell movement in intact and regenerating planarians. Quantitation using chromosomal, nuclear and cytoplasmic markers. J. Embryol. Exp. Morphol. 1985, 89:57-70.
87. Salò E., Baguñà J. Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J. Exp. Zool. 2002, 292:528-539.
88. Salvetti A., Rossi L., Deri P., Batistoni R. An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Dev. Dyn. 2000, 218:603-614.
89. Salvetti A., Rossi L., Lena A., Batistoni R., Deri P., Rainaldi G., Locci M.T., Evangelista M., Gremigni V. DjPum, a homologue of Drosophila pumilio, is essential to planarian stem cell maintenance. Development 2005, 132:1863-1874.
90. 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.
91. Shukalyuk A.I., Dolmatov I.Y. Regeneration of the digestive tube in the holothurian Apostichopus japonicus after evisceration. Russ. J. Mar. Biol. 2001, 27:168-173.
92. Solana J., Lasko P., Romero R. Spoltud-1 is a chromatoid body component required for planarian long-term stem cell self-renewal. Dev. Biol. 2009, 328:410-421.
93. Takeda H., Nishimura K., Agata K. Planarians maintain a constant ratio of different cell types during changes in body size by using the stem cell system. Zoolog. Sci. 2009, 26:805-813.
94. Takeo M., Yoshida-Noro C., Tochinai S. Morphallactic regeneration as revealed by region-specific gene expression in the digestive tract of Enchytraeus japonensis (Oligochaeta, Annelida). Dev. Dyn. 2008, 237:1284-1294.
95. Umesono Y., Watanabe K., Agata K. A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain. Dev. Growth Differ. 1997, 39:723-727.
96. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 2009, 71:241-260.
97. von Bertalanffy L. Untersuchungen über die gesetzlichkeit des wachstums. III. Teil. Quantitative beziehungen zwischen darmoberfläche und körpergröße bei Planaria maculata. Wilhelm Roux Arch. Entwickl. Mech. Org. 1940, 140:81-89.
98. Wenemoser D., Reddien P.W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 2010, 344:979-991.
99. Zattara E.E., Bely A.E. Evolution of a novel developmental trajectory: fission is distinct from regeneration in the annelid Pristina leidyi. Evol. Dev. 2011, 13:80-95.
100. Zayas R.M., Hernandez A., Habermann B., Wang Y., Stary J.M., 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. 2005, 102:18491-18496.