zic-1 Expression in Planarian Neoblasts after Injury Controls Anterior Pole Regeneration

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Vásquez Doorman, Constanza ^a   Petersen, Christian P ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WNT PROTEIN; HELMINTH PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; FOXD GENE; GENE; GENE EXPRESSION PROFILING; HEAD; NEOBLAST; NONHUMAN; NOTUM GENE; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; RNA INTERFERENCE; SCHMIDTEA MEDITERRANEA; SIGNAL TRANSDUCTION; TAIL; TISSUE REGENERATION; TURBELLARIA; ZIC 1 GENE; ANIMAL; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; REGENERATION;

ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAD; HELMINTH PROTEINS; PLANARIANS; PLURIPOTENT STEM CELLS; REGENERATION; SIGNAL TRANSDUCTION; TAIL; TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84905449736     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004452     Document Type: Article

References (77)

1. Tanaka EM, Reddien PW, (2011) The cellular basis for animal regeneration. Dev Cell 21: 172-185.
2. Rink JC, (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223: 67-84.
3. Wagner DE, Wang IE, Reddien PW, (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332: 811-816.
4. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sánchez Alvarado A, (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.
5. Newmark PA, Sánchez Alvarado A, (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220: 142-153.
6. Hayashi T, Asami M, Higuchi S, Shibata N, Agata K, (2006) Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48: 371-380.
7. Wenemoser D, Reddien PW, (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344: 979-991.
8. Guedelhoefer OCt, Sánchez Alvarado A, (2012) Amputation induces stem cell mobilization to sites of injury during planarian regeneration. Development 139: 3510-3520.
9. Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW, (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26: 988-1002.
10. Gurley KA, Rink JC, Sánchez Alvarado A, (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319: 323-327.
11. Petersen CP, Reddien PW, (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319: 327-330.
12. Adell T, Saló E, Boutros M, Bartscherer K, (2009) Smed-Evi/Wntless is required for beta-catenin-dependent and-independent processes during planarian regeneration. Development 136: 905-910.
13. Petersen CP, Reddien PW, (2009) A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci U S A 106: 17061-17066.
14. Petersen CP, Reddien PW, (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332: 852-855.
15. Rink JC, Gurley KA, Elliott SA, Sánchez Alvarado A, (2009) Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 326: 1406-1410.
16. Liu SY, Selck C, Friedrich B, Lutz R, Vila-Farre M, et al. (2013) Reactivating head regrowth in a regeneration-deficient planarian species. Nature 500: 81-84.
17. Sikes JM, Newmark PA, (2013) Restoration of anterior regeneration in a planarian with limited regenerative ability. Nature 500: 77-80.
18. Umesono Y, Tasaki J, Nishimura Y, Hrouda M, Kawaguchi E, et al. (2013) The molecular logic for planarian regeneration along the anterior-posterior axis. Nature 500: 73-76.
19. Gavino MA, Reddien PW, (2011) A Bmp/Admp regulatory circuit controls maintenance and regeneration of dorsal-ventral polarity in planarians. Curr Biol 21: 294-299.
20. Reddien PW, Bermange AL, Kicza AM, Sánchez Alvarado A, (2007) BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134: 4043-4051.
21. Gonzalez-Sastre A, Molina MD, Saló E, (2012) Inhibitory Smads and bone morphogenetic protein (BMP) modulate anterior photoreceptor cell number during planarian eye regeneration. Int J Dev Biol 56: 155-163.
22. Molina MD, Neto A, Maeso I, Gomez-Skarmeta JL, Saló E, et al. (2011) Noggin and noggin-like genes control dorsoventral axis regeneration in planarians. Curr Biol 21: 300-305.
23. Molina MD, Saló E, Cebria F, (2007) The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Dev Biol 311: 79-94.
24. Roberts-Galbraith RH, Newmark PA, (2013) Follistatin antagonizes activin signaling and acts with notum to direct planarian head regeneration. Proc Natl Acad Sci U S A 110: 1363-1368.
25. Gavino MA, Wenemoser D, Wang IE, Reddien PW, (2013) Tissue absence initiates regeneration through Follistatin-mediated inhibition of Activin signaling. Elife 2: e00247.
26. Yazawa S, Umesono Y, Hayashi T, Tarui H, Agata K, (2009) Planarian Hedgehog/Patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc Natl Acad Sci U S A 106: 22329-22334.
27. Zhang D, Chan JD, Nogi T, Marchant JS, (2011) Opposing roles of voltage-gated Ca2+ channels in neuronal control of regenerative patterning. J Neurosci 31: 15983-15995.
28. Oviedo NJ, Morokuma J, Walentek P, Kema IP, Gu MB, et al. (2010) Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev Biol 339: 188-199.
29. Oviedo NJ, Levin M, (2007) smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 134: 3121-3131.
30. Beane WS, Morokuma J, Lemire JM, Levin M, (2013) Bioelectric signaling regulates head and organ size during planarian regeneration. Development 140: 313-322.
31. Beane WS, Morokuma J, Adams DS, Levin M, (2011) A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem Biol 18: 77-89.
32. Gurley KA, Elliott SA, Simakov O, Schmidt HA, Holstein TW, et al. (2010) Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol 347: 24-39.
33. Witchley JN, Mayer M, Wagner DE, Owen JH, Reddien PW, (2013) Muscle cells provide instructions for planarian regeneration. Cell Rep 4: 633-641.
34. Giraldez AJ, Copley RR, Cohen SM, (2002) HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2: 667-676.
35. Gerlitz O, Basler K, (2002) Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev 16: 1055-1059.
36. Flowers GP, Topczewska JM, Topczewski J, (2012) A zebrafish Notum homolog specifically blocks the Wnt/beta-catenin signaling pathway. Development 139: 2416-2425.
37. Chen CC, Wang IE, Reddien PW, (2013) pbx is required for pole and eye regeneration in planarians. Development 140: 719-729.
38. Blassberg RA, Felix DA, Tejada-Romero B, Aboobaker AA, (2013) PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration. Development 140: 730-739.
39. Marz M, Seebeck F, Bartscherer K, (2013) A Pitx transcription factor controls the establishment and maintenance of the serotonergic lineage in planarians. Development 140: 4499-4509.
40. Currie KW, Pearson BJ, (2013) Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 140: 3577-3588.
41. Scimone ML, Lapan SW, Reddien PW, (2014) A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet 10: e1003999.
42. Fujimi TJ, Hatayama M, Aruga J, (2012) Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/beta-catenin signaling pathway. Dev Biol 361: 220-231.
43. Warr N, Powles-Glover N, Chappell A, Robson J, Norris D, et al. (2008) Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17: 2986-2996.
44. Lee H, Stultz BG, Hursh DA, (2007) The Zic family member, odd-paired, regulates the Drosophila BMP, decapentaplegic, during adult head development. Development 134: 1301-1310.
45. Aruga J, Kamiya A, Takahashi H, Fujimi TJ, Shimizu Y, et al. (2006) A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87: 783-792.
46. Kuo JS, Patel M, Gamse J, Merzdorf C, Liu X, et al. (1998) Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125: 2867-2882.
47. Nakata K, Nagai T, Aruga J, Mikoshiba K, (1997) Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci U S A 94: 11980-11985.
48. Mizuseki K, Kishi M, Matsui M, Nakanishi S, Sasai Y, (1998) Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125: 579-587.
49. DiNardo S, O'Farrell PH, (1987) Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes. Genes Dev 1: 1212-1225.
50. Houtmeyers R, Souopgui J, Tejpar S, Arkell R, (2013) The ZIC gene family encodes multi-functional proteins essential for patterning and morphogenesis. Cell Mol Life Sci 70: 3791-3811.
51. Lapan SW, Reddien PW, (2012) Transcriptome Analysis of the Planarian Eye Identifies ovo as a Specific Regulator of Eye Regeneration. Cell Rep 2: 294-307.
52. Lapan SW, Reddien PW, (2011) dlx and sp6-9 Control optic cup regeneration in a prototypic eye. PLoS Genet 7: e1002226.
53. Reddien PW, Newmark PA, Sánchez Alvarado A, (2008) Gene nomenclature guidelines for the planarian Schmidtea mediterranea. Dev Dyn 237: 3099-3101.
54. Guo T, Peters AH, Newmark PA, (2006) A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11: 159-169.
55. Eisenhoffer GT, Kang H, Sánchez Alvarado A, (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3: 327-339.
56. Felix DA, Aboobaker AA, (2010) The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genet 6: e1000915.
57. Cebria F, Guo T, Jopek J, Newmark PA, (2007) Regeneration and maintenance of the planarian midline is regulated by a slit orthologue. Dev Biol 307: 394-406.
58. Adell T, Cebria F, Saló E, (2010) Gradients in planarian regeneration and homeostasis. Cold Spring Harb Perspect Biol 2: a000505.
59. Iglesias M, Gomez-Skarmeta JL, Saló E, Adell T, (2008) Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 135: 1215-1221.
60. Scimone ML, Srivastava M, Bell GW, Reddien PW, (2011) A regulatory program for excretory system regeneration in planarians. Development 138: 4387-4398.
61. Forsthoefel DJ, Park AE, Newmark PA, (2011) Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev Biol 356: 445-459.
62. Cowles MW, Brown DD, Nisperos SV, Stanley BN, Pearson BJ, et al. (2013) Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 140: 4691-4702.
63. Wagner DE, Ho JJ, Reddien PW, (2012) Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10: 299-311.
64. Scimone ML, Meisel J, Reddien PW, (2010) The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 137: 1231-1241.
65. Pearson BJ, Sánchez Alvarado A, (2008) Regeneration, stem cells, and the evolution of tumor suppression. Cold Spring Harb Symp Quant Biol 73: 565-572.
66. Sandmann T, Vogg MC, Owlarn S, Boutros M, Bartscherer K, (2011) The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol 12: R76.
67. Hayashi T, Motoishi M, Yazawa S, Itomi K, Tanegashima C, et al. (2011) A LIM-homeobox gene is required for differentiation of Wnt-expressing cells at the posterior end of the planarian body. Development 138: 3679-3688.
68. Maurus D, Harris WA, (2009) Zic-associated holoprosencephaly: zebrafish Zic1 controls midline formation and forebrain patterning by regulating Nodal, Hedgehog, and retinoic acid signaling. Genes Dev 23: 1461-1473.
69. Pourebrahim R, Houtmeyers R, Ghogomu S, Janssens S, Thelie A, et al. (2011) Transcription factor Zic2 inhibits Wnt/beta-catenin protein signaling. J Biol Chem 286: 37732-37740.
70. Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, et al. (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20: 180-183.
71. Adamidi C, Wang Y, Gruen D, Mastrobuoni G, You X, et al. (2011) De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics. Genome Res 21: 1193-1200.
72. Resch AM, Palakodeti D, Lu YC, Horowitz M, Graveley BR, (2012) Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS One 7: e34447.
73. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
74. Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ, et al. (2012) A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30: 1734-1745.
75. Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sánchez Alvarado A, (2005) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8: 635-649.
76. Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, et al. (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238: 443-450.
77. King RS, Newmark PA, (2013) In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev Biol 13: 8.