The head-regeneration transcriptome of the planarian Schmidtea mediterranea

Genome Biology

Volumn 12, Issue 8, 2011, Pages

  Sandmann, Thomas ^a,b   Vogg, Matthias C ^c   Owlarn, Suthira ^c   Boutros, Michael ^a,b   Bartscherer, Kerstin ^c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONTIG; EARLY GROWTH RESPONSE FACTOR 1; SMED RUNT LIKE 1 PROTEIN; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTOME; UNCLASSIFIED DRUG; HELMINTH PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPRESSED SEQUENCE TAG; EYE; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; HEAD; HEAD REGENERATION; IMMUNOFLUORESCENCE TEST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; REGENERATION; RNA INTERFERENCE; SCHMIDTEA MEDITERRANEA; TRANSCRIPTION REGULATION; TURBELLARIA; ANIMAL; BRAIN; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALIA; PLANARIA; PLATYHELMINTHES; SCHMIDTEA MEDITERRANEA; TURBELLARIA;

ANIMALS; BODY PATTERNING; BRAIN; CORE BINDING FACTOR ALPHA SUBUNITS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME, HELMINTH; HEAD; HELMINTH PROTEINS; IN SITU HYBRIDIZATION; PLANARIANS; REGENERATION; RNA INTERFERENCE; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 80051634344     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-8-r76     Document Type: Article

References (63)

1. Umesono Y, Agata K. Evolution and regeneration of the planarian central nervous system. Dev Growth Differ 2009, 51:185-195. 10.1111/j.1440-169X.2009.01099.x, 19379275.
2. Cebria F, Kudome T, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Agata K. The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech Dev 2002, 116:199-204. 10.1016/S0925-4773(02)00134-X, 12128224.
3. Collins JJ, Hou X, Romanova EV, Lambrus BG, Miller CM, Saberi A, Sweedler JV, Newmark PA. Genome-wide analyses reveal a role for peptide hormones in planarian germline development. PLoS Biol 2010, 8:e1000509. 10.1371/journal.pbio.1000509, 2953531, 20967238.
4. Umesono Y, Watanabe K, Agata K. Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 1999, 209:31-39. 10.1007/s004270050224, 9914416.
5. Mineta K, Nakazawa M, Cebria F, Ikeo K, Agata K, Gojobori T. Origin and evolutionary process of the CNS elucidated by comparative genomics analysis of planarian ESTs. Proc Natl Acad Sci USA 2003, 100:7666-7671. 10.1073/pnas.1332513100, 164645, 12802012.
6. Handberg-Thorsager M, Fernandez E, Salo E. Stem cells and regeneration in planarians. Front Biosci 2008, 13:6374-6394.
7. Wenemoser D, Reddien PW. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 2010, 344:979-991. 10.1016/j.ydbio.2010.06.017, 2950745, 20599901.
8. Cebria 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. 10.1046/j.1440-169x.2002.00629.x, 11940100.
9. Inoue T, Kumamoto H, Okamoto K, Umesono Y, Sakai M, Sanchez Alvarado A, Agata K. Morphological and functional recovery of the planarian photosensing system during head regeneration. Zool Sci 2004, 21:275-283. 10.2108/zsj.21.275, 15056922.
10. Aboobaker AA. Planarian stem cells: a simple paradigm for regeneration. Trends Cell Biol 2011, 21:304-311. 10.1016/j.tcb.2011.01.005, 21353778, 21353778.
11. Gentile L, Cebria F, Bartscherer K. The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis Model Mech 2010, 4:12-19. 3014342, 21135057.
12. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Sanchez Alvarado A, Yandell M. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 2008, 18:188-196. 2134774, 18025269.
13. Schmidtea mediterranea genome sequencing project. , http://genome.wustl.edu/genomes/view/schmidtea_mediterranea/
14. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
15. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829. 10.1101/gr.074492.107, 2336801, 18349386.
16. Oases: de novo transcriptome assembler for very short reads. , http://www.ebi.ac.uk/~zerbino/oases/
17. Abril JF, Cebria F, Rodriguez-Esteban G, Horn T, Fraguas S, Calvo B, Bartscherer K, Salo E. Smed454 dataset: unravelling the transcriptome of Schmidtea mediterranea. BMC Genomics 2010, 11:731. 10.1186/1471-2164-11-731, 3022928, 21194483.
18. Blythe MJ, Kao D, Malla S, Rowsell J, Wilson R, Evans D, Jowett J, Hall A, Lemay V, Lam S, Aboobaker AA. A dual platform approach to transcript discovery for the planarian Schmidtea mediterranea to establish RNAseq for stem cell and regeneration biology. PLoS One 2010, 5:e15617. 10.1371/journal.pone.0015617, 3001875, 21179477.
19. O'Neil ST, Dzurisin JD, Carmichael RD, Lobo NF, Emrich SJ, Hellmann JJ. Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics 2010, 11:310. 10.1186/1471-2164-11-310, 2887415, 20478048.
20. Kent WJ. BLAT--the BLAST-like alignment tool. Genome Res 2002, 12:656-664. 187518, 11932250.
21. Mortazavi A, Schwarz EM, Williams B, Schaeffer L, Antoshechkin I, Wold BJ, Sternberg PW. Scaffolding a Caenorhabditis nematode genome with RNA-seq. Genome Res 2010, 20:1740-1747. 10.1101/gr.111021.110, 2990000, 20980554.
22. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610, 16081474.
23. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
24. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. 10.1186/gb-2010-11-10-r106, 20979621.
25. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
26. Flores GV, Daga A, Kalhor HR, Banerjee U. Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 1998, 125:3681-3687.
27. Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW. Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 2000, 103:87-97. 10.1016/S0092-8674(00)00107-0, 11051550.
28. Zayas RM, Hernandez A, Habermann B, Wang Y, Stary JM, Newmark PA. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 2005, 102:18491-18496. 10.1073/pnas.0509507102, 1317986, 16344473.
29. Nakazawa M, Cebria F, Mineta K, Ikeo K, Agata K, Gojobori T. Search for the evolutionary origin of a brain: planarian brain characterized by microarray. Mol Biol Evol 2003, 20:784-791. 10.1093/molbev/msg086, 12679532.
30. Rossi L, Salvetti A, Marincola FM, 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. 10.1186/gb-2007-8-4-r62, 1896013, 17445279.
31. Friedlander MR, Adamidi C, Han T, Lebedeva S, Isenbarger TA, Hirst M, Marra M, Nusbaum C, Lee WL, Jenkin JC, Sanchez Alvarado A, Kim JK, Rajewsky N. High-resolution profiling and discovery of planarian small RNAs. Proc Natl Acad Sci USA 2009, 106:11546-11551. 10.1073/pnas.0905222106, 2703670, 19564616.
32. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005, 310:1327-1330. 10.1126/science.1116110, 16311336.
33. Gurley KA, Rink JC, Sanchez Alvarado A. Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 2008, 319:323-327. 10.1126/science.1150029, 2755502, 18063757.
34. Okamoto K, Takeuchi K, Agata K. Neural projections in planarian brain revealed by fluorescent dye tracing. Zool Sci 2005, 22:535-546. 10.2108/zsj.22.535, 15930826.
35. 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. 10.1016/j.neures.2007.05.014, 17624455.
36. 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. 10.1002/dneu.20377, 17565705.
37. Cebria F, Newmark PA. 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. 10.1242/dev.01941, 16033796.
38. Felix DA, Aboobaker AA. The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genet 2010, 6:e1000915. 10.1371/journal.pgen.1000915, 2858555, 20422023.
39. Iglesias M, Gomez-Skarmeta JL, Salo E, Adell T. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 2008, 135:1215-1221. 10.1242/dev.020289, 18287199.
40. Adell T, Salo 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. 10.1242/dev.033761, 19211673.
41. Petersen CP, Reddien PW. A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci USA 2009, 106:17061-17066. 10.1073/pnas.0906823106, 2743725, 19805089.
42. Ha H, Han D, Choi Y. TRAF-mediated TNFR-family signaling. Curr Protoc Immunol 2009, Chapter 11:Unit11 19D.
43. Xie P, Kraus ZJ, Stunz LL, Bishop GA. Roles of TRAF molecules in B lymphocyte function. Cytokine Growth Factor Rev 2008, 19:199-207. 10.1016/j.cytogfr.2008.04.002, 2495079, 18499506.
44. Satoh A, Gardiner DM, Bryant SV, Endo T. Nerve-induced ectopic limb blastemas in the Axolotl are equivalent to amputation-induced blastemas. Dev Biol 2007, 312:231-244. 10.1016/j.ydbio.2007.09.021, 17959163.
45. Gomez-Martin D, Diaz-Zamudio M, Galindo-Campos M, Alcocer-Varela J. Early growth response transcription factors and the modulation of immune response: implications towards autoimmunity. Autoimmun Rev 2010, 9:454-458. 10.1016/j.autrev.2009.12.006, 20035903.
46. Elbarghati L, Murdoch C, Lewis CE. Effects of hypoxia on transcription factor expression in human monocytes and macrophages. Immunobiology 2008, 213:899-908. 10.1016/j.imbio.2008.07.016, 18926304.
47. Lim CP, Jain N, Cao X. Stress-induced immediate-early gene, egr-1, involves activation of p38/JNK1. Oncogene 1998, 16:2915-2926. 10.1038/sj.onc.1201834, 9671412.
48. Christy BA, Lau LF, Nathans D. A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc Natl Acad Sci USA 1988, 85:7857-7861. 10.1073/pnas.85.21.7857, 282296, 3141919.
49. Thiel G, Mayer SI, Muller I, Stefano L, Rossler OG. Egr-1-A Ca(2+)-regulated transcription factor. Cell Calcium 2010, 47:397-403. 10.1016/j.ceca.2010.02.005, 20303171.
50. Aggeli IK, Beis I, Gaitanaki C. ERKs and JNKs mediate hydrogen peroxide-induced Egr-1 expression and nuclear accumulation in H9c2 cells. Physiol Res 2010, 59:443-454.
51. Chen SJ, Ning H, Ishida W, Sodin-Semrl S, Takagawa S, Mori Y, Varga J. The early-immediate gene EGR-1 is induced by transforming growth factor-beta and mediates stimulation of collagen gene expression. J Biol Chem 2006, 281:21183-21197. 10.1074/jbc.M603270200, 16702209.
52. Shin SY, Kim JH, Baker A, Lim Y, Lee YH. Transcription factor Egr-1 is essential for maximal matrix metalloproteinase-9 transcription by tumor necrosis factor alpha. Mol Cancer Res 2010, 8:507-519. 10.1158/1541-7786.MCR-09-0454, 20332214.
53. Oviedo NJ, Morokuma J, Walentek P, Kema IP, Gu MB, Ahn JM, Hwang JS, Gojobori T, Levin M. Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev Biol 2010, 339:188-199. 10.1016/j.ydbio.2009.12.012, 2823934, 20026026.
54. Endo T, Bryant SV, Gardiner DM. A stepwise model system for limb regeneration. Dev Biol 2004, 270:135-145. 10.1016/j.ydbio.2004.02.016, 15136146.
55. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358. 10.1038/nature08160, 2756445, 19606141.
56. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
57. HTSeq: analysing high-throughput sequencing data with Python. , http://www-huber.embl.de/users/anders/HTSeq/doc/overview.html
58. Stein LD, Mungall C, Shu S, Caudy M, Mangone M, Day A, Nickerson E, Stajich JE, Harris TW, Arva A, Lewis S. The generic genome browser: a building block for a model organism system database. Genome Res 2002, 12:1599-1610. 10.1101/gr.403602, 187535, 12368253.
59. Robinson MD, Smyth GK. Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 2008, 9:321-332.
60. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006, 411:134-193.
61. Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Paro R, Perrimon N. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 2004, 303:832-835. 10.1126/science.1091266, 14764878.
62. 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.
63. 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. 10.1016/j.ydbio.2005.09.002, 16243308.