Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response

Developmental Biology

Volumn 347, Issue 1, 2010, Pages 24-39

  Gurley, Kyle A ^a,f   Elliott, Sarah A ^a   Simakov, Oleg ^b   Schmidt, Heiko A ^c,d   Holstein, Thomas W ^e   Alvarado, Alejandro Sánchez ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MAX F PERUTZ LABORATORIES   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Planarians; Regeneration; Stem cells; Tissue remodeling; Wnt signaling pathway

Indexed keywords

UNCLASSIFIED DRUG; WNT PROTEIN; WNT11 PROTEIN; WNT2 PROTEIN; WNT5 PROTEIN;

ANTERIOR POSTERIOR AXIS; ARTICLE; CONTROLLED STUDY; GENE; GENE SEQUENCE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RNA INTERFERENCE; SCHMIDTEA MEDITERRANEA; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SMED GENE; STEM CELL; TISSUE DIFFERENTIATION; TISSUE REGENERATION; TURBELLARIA; WNT GENE;

ANIMALIA; PLANARIA; SCHMIDTEA MEDITERRANEA; TURBELLARIA;

EID: 77957316159     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.08.007     Document Type: Article

References (76)

1. Adell T., Saló E., Boutros M., Bartscherer K. Smed-Evi/Wntless is required for beta-catenin-dependent and -independent processes during planarian regeneration. Development 2009, 136:905-910.
2. Agata K., Soejima Y., Kato K., Kobayashi C., Umesono Y., Watanabe K. Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool. Sci. 1998, 15:433-440.
3. Augustin R., Franke A., Khalturin K., Kiko R., Siebert S., Hemmrich G., Bosch T.C. Dickkopf related genes are components of the positional value gradient in Hydra. Dev. Biol. 2006, 296:62-70.
4. 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.
5. Bardeen C.R., Baetjer F.H. The inhibitive action of the Roentgen rays on regeneration in planarians. J. Exp. Zool. 1904, 1:191-195.
6. Brockes J.P., Kumar A. Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol. 2008, 24:525-549.
7. Broun M., Gee L., Reinhardt B., Bode H.R. Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 2005, 132:2907-2916.
8. 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.
9. 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.
10. Chera S., Ghila L., Dobretz K., Wenger Y., Bauer C., Buzgariu W., Martinou J.C., Galliot B. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev. Cell 2009, 17:279-289.
11. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
12. Dubois F. Contribution á l' étude de la migration des cellules de regeneration chez les Planaires dulcicoles. C.R. Hebd. Seances Acad. Sci. 1949, 229:747-749.
13. 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.
14. Felix D.A., Aboobaker A.A. The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genet. 2010, 6:e1000915.
15. Fradkin L.G., van Schie M., Wouda R.R., de Jong A., Kamphorst J.T., Radjkoemar-Bansraj M., Noordermeer J.N. The Drosophila Wnt5 protein mediates selective axon fasciculation in the embryonic central nervous system. Dev. Biol. 2004, 272:362-375.
16. Galliot B., Ghila L. Cell plasticity in homeostasis and regeneration. Mol. Reprod. Dev. 2010 Jul 2. [Electronic publication ahead of print] PMID: 20602493 2010.
17. Guder C., Pinho S., Nacak T.G., Schmidt H.A., Hobmayer B., Niehrs C., Holstein T.W. An ancient Wnt-Dickkopf antagonism in Hydra. Development 2006, 133:901-911.
18. Gurley, K. A., Sánchez Alvarado, A., 2008. Stem cells in animal models of regeneration. StemBook, ed. The Stem Cell Research Community, StemBook, doi/10.3824/stembook.1.32.1.
19. 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.
20. Hobmayer B., Rentzsch F., Kuhn K., Happel C.M., von Laue C.C., Snyder P., Rothbacher U., Holstein T.W. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 2000, 407:186-189.
21. Holstein T.W. Wnt signaling in cnidarians. Methods Mol. Biol. 2008, 469:47-54.
22. Holstein T.W., Hobmayer E., Technau U. Cnidarians: an evolutionarily conserved model system for regeneration?. Dev. Dyn. 2003, 226:257-267.
23. Huelsenbeck J.P., Ronquist F., Nielsen R., Bollback J.P. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 2001, 294:2310-2314.
24. Hunter S., Apweiler R., Attwood T.K., Bairoch A., Bateman A., Binns D., Bork P., Das U., Daugherty L., Duquenne L., Finn R.D., Gough J., Haft D., Hulo N., Kahn D., Kelly E., Laugraud A., Letunic I., Lonsdale D., Lopez R., Madera M., Maslen J., McAnulla C., McDowall J., Mistry J., Mitchell A., Mulder N., Natale D., Orengo C., Quinn A.F., Selengut J.D., Sigrist C.J., Thimma M., Thomas P.D., Valentin F., Wilson D., Wu C.H., Yeats C. InterPro: the integrative protein signature database. Nucleic Acids Res. 2009, 37:D211-D215.
25. Iglesias M., Gomez-Skarmeta J.L., Saló E., Adell T. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 2008, 135:1215-1221.
26. Kobayashi C., Saito Y., Ogawa K., Agata K. Wnt signaling is required for antero-posterior patterning of the planarian brain. Dev. Biol. 2007, 306:714-724.
27. Kusserow A., Pang K., Sturm C., Hrouda M., Lentfer J., Schmidt H.A., Technau U., von Haeseler A., Hobmayer B., Martindale M.Q., Holstein T.W. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 2005, 433:156-160.
28. Lengfeld T., Watanabe H., Simakov O., Lindgens D., Gee L., Law L., Schmidt H.A., Ozbek S., Bode H., Holstein T.W. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev. Biol. 2009, 330:186-199.
29. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
30. Marsal M., Pineda D., Salo E. Gtwnt-5 a member of the wnt family expressed in a subpopulation of the nervous system of the planarian Girardia tigrina. Gene Expr. Patterns 2003, 3:489-495.
31. Matsui T., Raya A., Kawakami Y., Callol-Massot C., Capdevila J., Rodríguez-Esteban C., Izpisúa Belmonte J.C. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 2005, 19(1):164-175. PMID is 15630025.
32. Mii Y., Taira M. Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development. 2009, 136:4083-4088.
33. Minh B.Q., Vinh le S., von Haeseler A., Schmidt H.A. pIQPNNI: parallel reconstruction of large maximum likelihood phylogenies. Bioinformatics 2005, 21:3794-3796.
34. Momose T., Houliston E. Two oppositely localised frizzled RNAs as axis determinants in a Cnidarian embryo. PLoS Biol. 2007, 5:e70.
35. Momose T., Derelle R., Houliston E. A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica. Development 2008, 135:2105-2113.
36. Moon R.T., Kohn A.D., De Ferrari G.V., Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 2004, 5:691-701.
37. Morgan T.H. Experimental studies of the regeneration of Planaria maculata. Arch. Entw. Mech. Org. 1898, 7:364-397.
38. Morgan T.H. Regeneration in planarians. Arch. Entw. Mech. Org. 1900, 10:58-119.
39. Morgan T.H. Polarity and axial heteromorphosis. Am. Nat. 1904, 38:502-505.
40. Nelson W.J., Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004, 303:1483-1487.
41. Newmark P.A., Sánchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 2000, 220:142-153.
42. Nogi T., Zhang D., Chan J.D., Marchant J.S. A novel biological activity of praziquantel requiring voltage-operated ca channel Beta subunits: subversion of flatworm regenerative polarity. PLoS Negl. Trop. Dis. 2009, 3:e464.
43. Ogawa K., Ishihara S., Saito Y., Mineta K., Nakazawa M., Ikeo K., Gojobori T., Watanabe K., Agata K. Induction of a noggin-like gene by ectopic DV interaction during planarian regeneration. Dev. Biol. 2002, 250:59-70.
44. 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(1):188-199.
45. Pearson B.J., Eisenhoffer G.T., Gurley K.A., Rink J.C., Miller D.E., Sanchez Alvarado A. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn. 2009, 238:443-450.
46. Pellettieri J., Sánchez Alvarado A. Cell turnover and adult tissue homeostasis: from humans to planarians. Annu. Rev. Genet. 2007, 41:83-105.
47. Pellettieri J., Fitzgerald P., Watanabe S., Mancuso J., Green D.R., Sánchez Alvareado A. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2010, 338:76-85.
48. Petersen C.P., Reddien P.W. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
49. Petersen C.P., Reddien P.W. A wound-induced Wnt expression program controls planarian regeneration polarity. Proc. Natl Acad. Sci. USA 2009, 106:17061-17066.
50. Pires-daSilva A., Sommer R.J. The evolution of signalling pathways in animal development. Nat. Rev. Genet. 2003, 4:39-49.
51. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science 2002, 298:2188-2190.
52. Randolph H. Observations and experiments on regeneration in planarians. Arch. Entw. Mech. Org. 1897, 5:352-372.
53. Reddien P.W., Sánchez Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 2004, 20:725-757.
54. Reddien P.W., Bermange A.L., Murfitt K.J., Jennings J.R., Sánchez Alvarado A. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 2005, 8:635-649.
55. Rink J.C., 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.
56. Robb S.M., Sánchez Alvarado A. Identification of immunological reagents for use in the study of freshwater planarians by means of whole-mount immunofluorescence and confocal microscopy. Genesis 2002, 32:293-298.
57. Robb S.M., Ross E., Sánchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 2008, 36:D599-D606.
58. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
59. 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.
60. 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.
61. Schmidt, H. A., 2003. Phylogenetic trees from large datasets. PhD Thesis, Universität Düsseldorf, Germany.
62. Schmidt H.A., von Haeseler A. Maximum-likelihood analysis using TREE-PUZZLE. Curr. Protoc. Bioinform. 2007, 17, 6.6.1-6.6.23.
63. Singh A.P., VijayRaghavan K., Rodrigues V. Dendritic refinement of an identified neuron in the Drosophila CNS is regulated by neuronal activity and Wnt signaling. Development 2010, 137:1351-1360.
64. Sirbulescu R.F., Zupanc G.K. Dynamics of caspase-3-mediated apoptosis during spinal cord regeneration in the teleost fish, Apteronotus leptorhynchus. Brain Res. 2009, 1304:14-25.
65. Stoick-Cooper C.L., Moon R.T., Weidinger G. Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev. 2007, 21:1292-1315.
66. Stoick-Cooper C.L., Weidinger G., Riehle K.J., Hubbert C., Major M.B., Fausto N., Moon R.T. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134:479-489.
67. Strimmer K., Von Haeseler A. Quartet puzzling: a quartet maximum - likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 1996, 13:964-969.
68. Strimmer K., Goldman N., Von Haeseler A. Bayesian probabilities and quartet puzzling. Mol. Biol. Evol. 1997, 14:210-213.
69. Tseng A.S., Adams D.S., Qiu D., Koustubhan P., Levin M. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev. Biol. 2007, 301:62-69.
70. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 136:3205-3214.
71. Veeman M.T., Axelrod J.D., Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 2003, 5:367-377.
72. Vinh le S., Von Haeseler A. IQPNNI: moving fast through tree space and stopping in time. Mol. Biol. Evol. 2004, 21:1565-1571.
73. Wenemosser D., Reddien P.W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol. 2010, 344(2):979-991. Epub 2010 Jun 19.PMID: 20599901 [PubMed - in process].
74. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 2001, 18:691-699.
75. Yang Z. Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol. Biol. Evol. 1993, 10:1396-1401.
76. 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. USA. 2009, 106:22329-22334.