EGFR signaling regulates cell proliferation, differentiation and morphogenesis during planarian regeneration and homeostasis

Developmental Biology

Volumn 354, Issue 1, 2011, Pages 87-101

  Fraguas, Susanna ^a   Barberán, Sara ^a   Cebrià, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cell differentiation; Epidermal growth factor; Planarian; Regeneration; Signaling pathway

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 1; EPIDERMAL GROWTH FACTOR RECEPTOR 3; PROTEIN SMED; REGULATOR PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTEMA; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; GENE SILENCING; HOMEOSTASIS; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARYNX; PIGMENT CELL; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TURBELLARIA;

ANIMALIA; PLANARIA; SCHMIDTEA MEDITERRANEA; TURBELLARIA;

EID: 79955524004     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.03.023     Document Type: Article

References (84)

1. Agata K., Tanaka C., Kobayashi C., Kato K., Saitoh Y. Intercalary regeneration in planarians. Dev. Dyn. 2003, 226:308-316.
2. Aguirre A., Dupree J.L., Mangin J.M., Gallo V. A functional role for EGFR signaling in myelination and remyelination. Nat. Neurosci. 2007, 10:990-1002.
3. Aroian R.V., Koga M., Mendel J.E., Ohshima Y., Sternberg P.W. The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature 1990, 348:693-699.
4. Baguñà J., Saló E., Auladell C. Regeneration and pattern formation in planarians III. Evidence that neoblasts. Are totipotent stem cells and the source of blastema cells. Development 1989, 107:77-86.
5. Baguñà J., Saló E., Romero R. Effects of activators and antagonists of the neuropeptides substance P and substance K on cell proliferation in planarians. Int. J. Dev. Biol. 1989, 33:261-264.
6. Bardeen C.R., Baetjer F.H. The inhibitive action of the Roentgen rays on regeneration in planarians. J. Exp. Zool. 1904, 1:191-195.
7. Bergmann A., Steller H. Apoptosis, stem cells, and regeneration. Sci. Signal. 2010, 3(145):re8.
8. Bianco R., Gelardi T., Damiano V., Ciardiello F., Tortora G. Rational bases for the development of EGFR inhibitors for cancer treatment. Int. J. Biochem. Cell Biol. 2007, 39:1416-1431.
9. Birchmeier C. ErbB receptors and the development of the nervous system. Exp. Cell Res. 2009, 315:611-618.
10. Brown K.E., Baonza A., Freeman M. Epithelial cell adhesion in the developing Drosophila retina is regulated by Atonal and the EGF receptor pathway. Dev. Biol. 2006, 300:710-721.
11. Bueno D., Baguñà J., Romero R. A central body region defined by a position-specific molecule in the planarian Dugesia (Girardia) tigrina: spatial and temporal variations during regeneration. Dev. Biol. 1996, 178:446-458.
12. Bueno D., Espinosa L., Baguñà J., Romero R. Planarian pharynx regeneration in regenerating tail fragments monitored with cell-specific monoclonal antibodies. Dev. Genes Evol. 1997, 206:425-434.
13. Burgess A.W. EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 2008, 26:263-274.
14. Cebrià F. Organization of the nervous system in the model planarian Schmidtea mediterranea: an immunocytochemical study. Neurosci. Res. 2008, 61:375-384.
15. 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.
16. Cebrià F., Vispo M., Newmark P.A., Bueno D., Romero R. Myocyte differentiation and body wall musculatura in the planarian Girardia tigrina. Dev. Genes Evol. 1997, 207:306-316.
17. Cebrià F., Kobayashi C., Umesono Y., Nakazawa M., Mineta K., Ikeo K., Gojobori T., Itoh M., Taira M., Sánchez-Alvarado A., Agata K. FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 2002, 419:620-624.
18. Cebrià F., Nakazawa M., Mineta K., Ikeo K., Gojobori T., Agata K. Dissecting planarian central nervous system regeneration by the expression of neural-specific genes. Dev. Growth Differ. 2002, 44:135-146.
19. 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.
20. Chai G., Ma C., Bao K., Zheng L., Wang X., Sun Z., Saló E., Adell T., Wu W. Complete functional segregation of planarian beta-catenin-1 and -2 in mediating WNT signaling and cell adhesion. J. Biol. Chem. 2010, 285:24120-24130.
21. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36:1021-1034.
22. Dumstrei K., Wang F., Shy D., Tepass U., Hartenstein V. Interaction between EGFR signaling and DE-cadherin during nervous system morphogenesis. Development 2002, 129:3983-3994.
23. Eisenhoffer G.T., Kang H., Sánchez-Alvarado A. Molecular analysis of stem cells and their descendents during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 2008, 3:327-339.
24. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunesekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucl. Acids Res. 38 (suppl 1), 2010, D211-D222.
25. Freeman M. Cell determination strategies in the Drosophila eye. Development 1997, 124:261-270.
26. Gonzalez-Perez O., Romero-Rodriguez R., Soriano-Navarro M., Garica-Verdugo J.M., Alvarez-Buylla A. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 2009, 27:2032-2043.
27. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
28. Gurley K.A., Rink J.C., Sánchez-Alvarado A. Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 2008, 319:323-327.
29. Hazan R.B., Norton L. The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 1998, 273:9078-9084.
30. Hoschuetzky H., Aberle H., Kemler R. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 1994, 127:1375-1380.
31. Hyman L.H. The Invertebrates: Platyhelminthes and Rhynchocoela 1951, McGraw-Hill, New York.
32. Iglesias M., Gómez-Skarmeta J.L., Saló E., Adell T. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 2008, 135:1215-1221.
33. Ishii S. Electron microscopic observations on the planarian tissues. I. A survey of the pharynx. Fukushima J. Med. Sci. 1962/1963, 9/10:51-73.
34. Ishii S. The ultrastructure of the outer epithelium of the planarian pharynx. Fukushima J. Med. Sci. 1964, 11:109-125.
35. Jiang H., Edgar B.A. EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development 2009, 136:483-493.
36. Kobayashi C., Watanabe K., Agata K. The process of pharynx regeneration in planarians. Dev. Biol. 1999, 211:27-38.
37. Kumar A., Godwin J.W., Gates P.B., Garza-Garcia A.A., Brockes J.P. Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 2007, 318:772-777.
38. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. ClustalW and ClustalX version 2. Bioinformatics 2007, 23:2947-2948.
39. Livneh E., Glazer L., Segal D., Schlessinger J., Shilo B.Z. The Drosophila EGF receptor gene homolog: conservation of both binding and kinase domains. Cell 1985, 40:599-607.
40. Miljkovic-Licina M., Chera S., Ghila L., Galliot B. Head regeneration in wild-type hydra requires de novo neurogenesis. Development 2007, 134:1191-1201.
41. Molina M.D., Saló E., Cebrià F. The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Dev. Biol. 2007, 311:79-94.
42. Nagaraj R., Banerjee U. Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 2007, 134:825-831.
43. Nakamura T., Mito T., Miyawaki K., Ohuchi H., Noji S. EGFR signaling is required for re-establishing the proximodistal axis during distal leg regeneration in the cricket Gryllus bimaculatus nymph. Dev. Biol. 2008, 319:46-55.
44. Natarajan A., Wagner B., Sibilia M. The EGF receptor is required for efficient liver regeneration. Proc. Natl. Acad. Sci. U S A 2007, 104:17081-17086.
45. Newmark P.A., Sánchez-Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 2000, 220:142-153.
46. 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.
47. Nishimura K., Kitamura Y., Inoue T., Umesono Y., Yoshimoto K., Takeuchi K., Taniguchi T., Agata K. Identification and distribution of tryptophan hydroxylase (TPH)-positive neurons in the planarian Dugesia japonica. Neurosci. Res. 2007, 59:101-106.
48. Nishimura K., Kitamura Y., Inoue T., Umesono Y., Sano S., Yoshimoto K., Inden M., Takata K., Taniguchi T., Shimohama S., Agata K. Reconstruction of dopaminergic neural network and locomotion function in planarian regenerates. Dev. Neurobiol. 2007, 67:1059-1078.
49. Normanno N., De Luca A., Bianco C., Strizzi L., Mancino M., Maiello M.R., Carotenuto A., De Feo G., Caponigro F., Salomon D.S. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006, 366:2-16.
50. O'Keeffe G.C., Tyers P., Aarsland D., Dalley J.W., Barker R.A., Caldwell M.A. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proc. Natl. Acad. Sci. USA 2009, 106:8754-8759.
51. Okamoto K., Takeuchi K., Agata K. Neural projections in planarian brain revealed by fluorescent dye tracing. Zool. Sci. 2005, 22:535-546.
52. Orii H., Watanabe K. Bone morphogenetic protein is required for dorso-ventral patterning in the planarian Dugesia japonica. Dev. Growth Differ. 2007, 49:345-349.
53. 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.
54. Pearson B.J., Sánchez-Alvarado A. A planarian p53 homolog regulates proliferation and self-renewal in adult stem cells. Development 2010, 137:213-221.
55. 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.
56. Pellettieri J., Fitzgerald P., Watanabe S., Mancuso J., Green D.R., Sánchez-Alvarado A. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2010, 338:76-85.
57. Petersen C.P., Reddien P.W. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
58. Reddien P.W., Sánchez-Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 2004, 20:725-757.
59. 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.
60. Reddien P.W., Bermange A.L., Kicza A.M., Sánchez Alvarado A. BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 2007, 134:4043-4051.
61. Reddien P.W., Newmark P.A., Sánchez-Alvarado A. Gene nomenclature guidelines for the planarian Schmidtea mediterranea. Dev. Dyn. 2008, 237:3099-3101.
62. Rink J.C., Kyle A., Gurley K.A., Elliott S.A., Sánchez-Alvarado A. Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 2009, 326:1406-1410.
63. Rojas-Muñoz A., Rajadhyksha S., Gilmour D., van Bebber F., Antos C., Rodríguez Esteban C., Nüsslein-Volhard C., Izpisúa Belmonte J.C. ErbB2 and ErbB3 regulate amputation-induced proliferation and migration during vertebrate regeneration. Dev. Biol. 2009, 327:177-190.
64. Romero R., Baguñà J. Quantitative cellular analysis of growth and reproduction in freshwater planarians (Turbellaria; Tricladida). I. A cellular description of the intact organism. Invertebr. Reprod. Dev. 1991, 19:157-165.
65. Sakai F., Agata K., Orii H., Watanabe K. Organization and regeneration ability of spontaneous supernumerary eyes in planarians - eye regeneration field and pathway selection by optic nerves. Zool. Sci. 2000, 17:375-381.
66. Saló E. The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 2006, 28:546-559.
67. Saló 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.
68. Saló E., Abril J.F., Adell T., Cebrià F., Eckelt K., Fernández-Taboada E., Handberg-Thorsager M., Iglesias M., Molina M.D., Rodríguez-Esteban G. Planarian regeneration: achievements and future directions after 20years of research. Int. J. Dev. Biol. 2009, 53:1317-1327.
69. Sánchez-Alvarado A., Newmark P.A., Robb S.M., Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 2002, 129:5659-5665.
70. Sánchez-Alvarado A., Newmark P.A. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. U S A 1999, 96:5049-5054.
71. Sánchez-Alvarado A., Tsonis P.A. Bridging the regeneration gap: genetic insights from diverse animal models. Nat. Rev. Genet. 2006, 7:873-884.
72. Sato Y., Kobayashi K., Matsumoto M., Hoshi M., Negishi S. Comparative study of eye defective worm "menashi" and regenerating wild-type in planarian, Dugesia ryukyuensis. Pigment Cell Res. 2005, 18:86-91.
73. Scimone M.L., Meisel J., Reddien P.W. The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 2010, 137:1231-1241.
74. Shoemaker C.B., Ramachandran H., Landa A., dos Reis M.G., Stein L.D. Alternative splicing of the Schistosoma mansoni gene encoding a homologue of epidermal growth factor receptor. Mol. Biochem. Parasitol. 1992, 53:17-32.
75. Singer M. The influence of the nerve in regeneration of the amphibian extremity. Q. Rev. Biol. 1952, 27:169-200.
76. Spiliotis M., Kroner A., Brehm K. Identification, molecular characterization and expression of the gene encoding the epidermal growth factor receptor orthologue from the fox-tapeworm Echinococcus multilocularis. Gene 2003, 323:57-65.
77. 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. Zool. Sci. 2009, 26:805-813.
78. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
79. 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.
80. Wenemoser D., Reddien P.W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 2010, 344:979-991.
81. Wong R.W., Guillaud L. The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev. 2004, 15:147-156.
82. Xian C.J., Zhou X.F. EGF family of growth factors: essential roles and functional redundancy in the nerve system. Front. Biosci. 2004, 9:85-92.
83. Yazawa S., Umesono Y., Hayashi T., Tarui H., Agata K. Planarian hedgehog/patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc. Natl. Acad. Sci. U S A 2009, 106:22329-22334.
84. Zayas R.M., Cebrià F., Guo T., Feng J., Newmark P.A. The use of lectins as markers for differentiated secretory cells in planarians. Dev. Dyn. 2010, 239:2888-2897.