Regeneration and maintenance of the planarian midline is regulated by a slit orthologue

Developmental Biology

Volumn 307, Issue 2, 2007, Pages 394-406

  Cebrià, Francesc ^a,b   Guo, Tingxia ^a   Jopek, Jessica ^a   Newmark, Phillip A ^a,b  

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

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

Author keywords

Axon guidance; Midline; Neural differentiation; Planarian; Regeneration; Schmidtea mediterranea; Slit

Indexed keywords

PROTEIN; SLIT PROTEIN; SMED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL REGENERATION; DIGESTIVE SYSTEM; MORPHOLOGY; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; RNA INTERFERENCE; TURBELLARIA; VENTRAL ROOT;

ANIMALIA; PLANARIA; SCHMIDTEA MEDITERRANEA; TURBELLARIA;

EID: 34347272302     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.05.006     Document Type: Article

References (61)

1. Agata K. Regeneration and gene regulation in planarians. Curr. Opin. Genet. Dev. 13 (2003) 492-496
2. Agata K., Soejima Y., Kato K., Kobayashi C., Umesono Y., and Watanabe K. Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool. Sci. 15 (1998) 433-440
3. Bagri A., Marin O., Plump A.S., Mak J., Pleasure S.J., Rubenstein J.L., and Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33 (2002) 233-248
4. Baguñà J., Saló E., and Auladell C. Regeneration and pattern formation in planarians. III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107 (1989) 77-86
5. Barresi M.J., Hutson L.D., Chien C.B., and Karlstrom R.O. Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132 (2005) 3643-3656
6. Benazzi M., Ballester R., Baguñà J., and Puccinelli I. The fissiparous race of the planarian Dugesia lugubris S.L. found in Barcelona (Spain) belongs to the biotype G: comparative analysis of the karyotypes. Caryologia 25 (1972) 59-68
7. Brose K., and Tessier-Lavigne M. Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10 (2000) 95-102
8. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., and Kidd T. Slit proteins bind Robo receptors and have an evolutionary conserved role in repulsive axon guidance. Cell 96 (1999) 795-806
9. Cebrià F., and 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 132 (2005) 3691-3703
10. Cebrià F., and Newmark P.A. Morphogenesis defects are associated with abnormal nervous system regeneration after roboA RNAi in planarians. Development 134 (2007) 833-837
11. Cebrià F., Nakazawa M., Mineta K., Ikeo K., Gojobori T., and Agata K. Dissecting planarian CNS regeneration by the expression of neural-specific genes. Dev. Growth Differ. 44 (2002) 135-146
12. Cebrià F., Kobayashi C., Umesono Y., Nakazawa M., Mineta K., Ikeo K., Gojobori T., Itoh M., Taira M., Sánchez Alvarado A., and Agata K. FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419 (2002) 620-624
13. Dickson B.J., and Gilestro G.F. Regulation of commissural pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 22 (2006) 651-675
14. Fusaoka E., Inoue T., Minetas K., Agata K., and Takeuchi K. Structure and function of primitive immunoglobulin superfamily neural cell adhesion molecules: a lesson from studies on planarian. Genes Cells 11 (2006) 541-555
15. Guo T., Peters A.H.F.M., and Newmark P.A. A bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11 (2006) 159-169
16. Hao J.C., Yu T.W., Fujisawa K., Culotti J.G., Gengyo-Ando K., Mitani S., Moulder G., Barstead R., Tessier-Lavigne M., and Bargmann C.I. C. elegans slit acts in midline, dorso-ventral, and antero-posterior guidance via the sax-3/robo receptor. Neuron 32 (2001) 25-38
17. Hu H. Chemorepulsion of neuronal migration by slit2 in the developing mammalian forebrain. Neuron 23 (1999) 703-711
18. Hyman L.H. The Invertebrates: Platyhelminthes and Rhynchocoela (1951), McGraw-Hill Book Company, New York
19. Inoue T., Kumamoto H., Okamoto K., Umesono Y., Sakai M., Sánchez Alvarado A., and Agata K. Morphological and functional recovery of the planarian photosensing system during head regeneration. Zool. Sci. 21 (2004) 275-283
20. Kidd T., Bland K.S., and Goodman C.S. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96 (1999) 785-794
21. Klagsbrun M., and Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev. 16 (2005) 535-548
22. Kolesnikov T., and Beckendorf S.K. NETRIN and SLIT guide salivary gland migration. Dev. Biol. 282 (2005) 102-111
23. Kramer S.G., Kidd T., Simpson J.H., and Goodman C.S. Switching repulsion to attraction: changing response to Slit during transition in mesoderm migration. Science 292 (2001) 737-740
24. Long H., Sabatier C., Ma L., Plump A., Yuan W., Ornitz D.M., Tamada A., Murakami F., Goodman C.S., and Tessier-Lavigne M. Conserved roles for slit and robo proteins in midline commissural axon guidance. Neuron 42 (2004) 213-223
25. MacMullin A., and Jacobs J.R. Slit coordinates cardiac morphogenesis in Drosophila. Dev. Biol. 293 (2006) 154-164
26. Mannini L., Rossi L., Deri P., Gremigni V., Salvetti A., Saló E., and Batistoni R. Djeyes absent (Djeya) controls prototypic planarian eye regeneration by cooperating with the transcription factor Djsix-1. Dev. Biol. 269 (2004) 346-359
27. Morita M., and Best J.B. Electron microscopic studies of Planaria. 3. Some observations on the fine structure of planarian nervous tissue. J. Exp. Zool. 161 (1966) 391-411
28. Newmark P.A., and Sánchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220 (2000) 142-153
29. Newmark P.A., and Sánchez Alvarado A. Not your father's planarian: a classic model enters the era of functional genomics. Nat. Rev., Genet. 3 (2002) 210-219
30. Newmark P.A., Reddien P.W., Cebrià F., and Sánchez Alvarado A. Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc. Natl. Acad. Sci. U. S. A. 100 Suppl. 1 (2003) 11861-11865
31. Okamoto K., Takeuchi K., and Agata K. Neural projections in planarian brain revealed by fluorescent dye tracing. Zool. Sci. 22 (2005) 535-546
32. Orii H., Kato K., Agata K., and Watanabe K. Molecular cloning of bone morphogenetic protein (BMP) gene from the planarian Dugesia japonica. Zool. Sci. 15 (1998) 871-877
33. Oviedo N.J., Newmark P.A., and Sánchez Alvarado A. Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev. Dyn. 226 (2003) 326-333
34. Pineda D., González J., Callaerts P., Ikeo K., Ghering W.J., and Saló E. Searching for the prototypic eye genetic network: sine oculis is essential for eye regeneration in planarians. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4525-4529
35. Piper M., Georgas K., Yamada T., and Little M. Expression of the vertebrate Slit gene family and their putative receptors, the Robo genes, in the developing murine kidney. Mech. Dev. 94 (2000) 213-217
36. Plump A.S., Erskine L., Sabatier C., Brose K., Epstein C.J., Goodman C.S., Mason C.A., and Tessier-Lavigne M. Slit1 and slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33 (2002) 219-232
37. Qian L., Liu J., and Bodmer R. Slit and Robo control cardiac cell polarity and morphogenesis. Curr. Biol. 15 (2005) 2271-2278
38. Reddien P.W., and Sánchez Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20 (2004) 725-757
39. Reddien P.W., Bermange A.L., Murfitt K.J., Jennings J.R., and Sánchez Alvarado A. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 8 (2005) 635-649
40. Reddien P.W., Oviedo N.J., Jennings J.R., Jenkin J.C., and Sánchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310 (2005) 1327-1330
41. Reuter M., and Gustafsson M.K. The flatworm nervous system: pattern and phylogeny. In: Breibach O., and Kutsch W. (Eds). The Nervous System of Invertebrates: An Evolutionary and Comparative Approach (1995), Birkäuser Verlag, Basel 25-59
42. Reuter M., Sheiman I.M., Gustafsson M.K., Halton D.W., Maule A.G., and Shaw C. Development of the nervous system in Dugesia tigrina during regeneration after fission and decapitation. Invert. Reprod. Dev. 29 (1996) 199-211
43. Robb S.M.C., and Sánchez Alvarado A. Identification of immunological reagents for use in the study of freshwater planarians by jeans of whole-mount immunofluorescence and confocal microscopy. Genesis 32 (2002) 293-298
44. Rossi L., Salvetti A., Lena A., Batistoni R., Deri P., Pugliesi C., Loreti E., and Gremigni V. DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev. Genes Evol. 216 (2006) 335-346
45. Rothberg J.M., Hartley D.A., Walther Z., and Artavanis-Tsakonas S. Slit: an EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system. Cell 55 (1988) 1047-1059
46. Rothberg J.M., Jacobs J.R., Goodman C.S., and Artavanis-Tsakonas S. Slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4 (1990) 2169-2187
47. Sakai F., Agata K., Orii H., and Watanabe K. Organization and regeneration ability of spontaneous supernumerary eyes in planarians-Eye regeneration field and pathway selection by optic nerves. Zool. Sci. 17 (2000) 375-381
48. Salvetti A., Rossi L., Lena A., Batistoni R., Deri P., Rainaldi G., Locci M.T., Evangelista M., and Gremigni V. DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132 (2005) 184-1863
49. Sánchez Alvarado A. Planarian regeneration: its end is its beginning. Cell 124 (2006) 241-245
50. Sánchez Alvarado A., and Newmark P.A. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5049-5054
51. Sánchez Alvarado A., Newmark P.A., Robb S.M.C., and Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129 (2002) 5659-5665
52. Santiago-Martínez E., Soplop N.H., and Kramer S.G. Lateral positioning at the dorsal midline: Slit and Roundabout receptors guide Drosophila heart cell migration. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 12441-12446
53. Strickland P., Shin G.C., Plump A., Tessier-Lavigne M., and Hinck L. Slit2 and netrin1 act synergistically as adhesive cues to generate tubular bi-layers during ductal morphogenesis. Development 133 (2006) 823-832
54. Tazaki A., Gaudieri S., Ikeo K., Gojobori T., Watanabe K., and Agata K. Neural network in planarian revealed by an antibody against planarian synaptotagmin homologue. Biochem. Biophys. Res. Commun. 260 (1999) 426-432
55. Umesono Y., Watanabe K., and Agata K. A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain. Dev. Growth Differ. 39 (1997) 723-727
56. Umesono Y., Watanabe K., and Agata K. Distinct structural domains in the planarian brain defined by the expression of evolutionary conserved homeobox genes. Dev. Genes Evol. 209 (1999) 31-39
57. Wang B., Xiao Y., Ding B.B., Zhang N., Yuan X., Gui L., Qian K.X., Duan S., Chen Z., Rao Y., and Geng J.G. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 4 (2003) 19-29
58. Wong K., Park H.T., Wu J.Y., and Rao Y. Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr. Opin. Gen. Dev. 12 (2002) 583-591
59. Wu W., Wong K., Chen J., Jiang Z., Dupuis S., Wu J.Y., and Rao Y. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400 (1999) 331-336
60. Wu J.Y., Feng L., Park H.T., Havlioglu N., Wen L., Tang H., Bacon K.B., Jiang Z.H., Zhang X.C., and Rao Y. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 410 (2001) 948-952
61. Zayas R.M., Hernández A., Habermann B., Wang Y., Stary J., and 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. 102 (2005) 18491-18496