Transcriptome analysis reveals strain-specific and conserved stemness genes in schmidtea mediterranea

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Resch, Alissa M ^a   Palakodeti, Dasaradhi ^b   Lu, Yi Chien ^c   Horowitz, Michael ^a   Graveley, Brenton R ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; BIOLOGICAL MARKER; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; REGENERATION; RNA ANALYSIS; RNA SEQUENCE; SCHMIDTEA MEDITERRANEA; STEM CELL; STRAIN DIFFERENCE; TURBELLARIA; ANIMAL; CELL CULTURE; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PHYSIOLOGY; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALIA; METAZOA; PLANARIA; SCHMIDTEA MEDITERRANEA;

ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; GENE EXPRESSION PROFILING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANARIANS; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS;

EID: 84859355786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034447     Document Type: Article

References (77)

1. Newmark P, Sanchez Alvarado A, (2002) Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3: 210-219.
2. Sánchez Alvarado A, (2004) Regeneration and the need for simpler model organisms. Philos Trans R Soc Lond, B, Biol Sci 359: 759-763.
3. Robb S, Ross E, Alvarado A, (2007) SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res 36: D599-D606.
4. Zayas RM, Hernández A, Habermann B, Wang Y, Stary JM, et al. (2005) The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 102: 18491-18496.
5. Sánchez Alvarado A, Newmark PA, Robb SM, Juste R, (2002) The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129: 5659-5665.
6. Blythe MJ, Kao D, Malla S, Rowsell J, Wilson R, et al. (2010) A dual platform approach to transcript discovery for the planarian Schmidtea mediterranea to establish RNAseq for stem cell and regeneration biology. PLoS One 5: e15617.
7. Abril JF, Cebria F, Rodriguez-Esteban G, Horn T, Fraguas S, et al. (2011) Smed454 dataset: unravelling the transcriptome of Schmidtea mediterranea. BMC Genomics 11: 731.
8. 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.
9. Lu YC, Smielewska M, Palakodeti D, Lovci MT, Aigner S, et al. (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. RNA 15: 1483-1491.
10. Friedländer MR, Chen W, Adamidi C, Maaskola J, Einspanier R, et al. (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26: 407-415.
11. Wolff E, Dubois F, (1948) Sur la migration des cellules de regeneration chez les planaires. Rev Suisse Zool 55: 218-227.
12. Lange CS, (1968) Studies on the cellular basis of radiation lethality II. Survival-curve parameters for standardized planarian populations. Int J Radiat Biol 14: 119-132.
13. Reddien P, Bermange A, Murfitt K, Jennings J, Sanchez 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.
14. Eisenhoffer G, Kang H, 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.
15. Fernandez-Taboada E, Rodriguez-Esteban G, Salo E, Abril JF, (2011) A proteomics approach to decipher the molecular nature of planarian stem cells. BMC Genomics 12: 133.
16. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
17. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
18. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
19. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460: 352-358.
20. Consortium TSjGSaFA (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345-351.
21. Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, et al. (2010) The dynamic genome of Hydra. Nature 464: 592-596.
22. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775-1787.
23. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479.
24. IHGS Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431: 931-945.
25. Alvarez-Presas M, Baguna J, Riutort M, (2008) Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back. Mol Phylogenet Evol 47: 555-568.
26. Lazaro EM, Harrath AH, Stocchino GA, Pala M, Baguna J, et al. (2011) Schmidtea mediterranea phylogeography: an old species surviving on a few Mediterranean islands? BMC Evol Biol 11: 274.
27. Zerbino DR, Birney E, (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
28. Consortium CeS, (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282: 2012-2018.
29. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056-1060.
30. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
31. Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, et al. (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 30: 281-283.
32. Frieden C, (1989) The regulation of protein polymerization. Trends Biochem Sci 14: 283-286.
33. Eads BD, Colbourne JK, Bohuski E, Andrews J, (2007) Profiling sex-biased gene expression during parthenogenetic reproduction in Daphnia pulex. BMC Genomics 8: 464.
34. Harris JE, Govindan JA, Yamamoto I, Schwartz J, Kaverina I, et al. (2006) Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev Biol 299: 105-121.
35. Kawamura K, Sugino YM, (1999) Cell adhesion in the process of asexual reproduction of tunicates. Microsc Res Tech 44: 269-278.
36. Lechler T, Fuchs E, (2005) Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437: 275-280.
37. Marthiens V, Kazanis I, Moss L, Long K, Ffrench-Constant C, (2010) Adhesion molecules in the stem cell niche-more than just staying in shape? J Cell Sci 123: 1613-1622.
38. Nilsen TW, Graveley BR, (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
39. Resch A, Xing Y, Alekseyenko A, Modrek B, Lee C, (2004) Evidence for a subpopulation of conserved alternative splicing events under selection pressure for protein reading frame preservation. Nucleic Acids Res 32: 1261-1269.
40. Yeo GW, Van Nostrand E, Holste D, Poggio T, Burge CB, (2005) Identification and analysis of alternative splicing events conserved in human and mouse. Proc Natl Acad Sci U S A 102: 2850-2855.
41. Magen A, Ast G, (2005) The importance of being divisible by three in alternative splicing. Nucleic Acids Res 33: 5574-5582.
42. Hartmann B, Castelo R, Minana B, Peden E, Blanchette M, et al. (2011) Distinct regulatory programs establish widespread sex-specific alternative splicing in Drosophila melanogaster. RNA 17: 453-468.
43. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y, (2010) Sex-specific and lineage-specific alternative splicing in primates. Genome Res 20: 180-189.
44. Ho TH, Charlet BN, Poulos MG, Singh G, Swanson MS, et al. (2004) Muscleblind proteins regulate alternative splicing. EMBO J 23: 3103-3112.
45. Vicente M, Monferrer L, Poulos MG, Houseley J, Monckton DG, et al. (2007) Muscleblind isoforms are functionally distinct and regulate alpha-actinin splicing. Differentiation 75: 427-440.
46. Kalsotra A, Xiao X, Ward AJ, Castle JC, Johnson JM, et al. (2008) A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci USA 105: 20333-20338.
47. Sundaram P, Echalier B, Han W, Hull D, Timmons L, (2006) ATP-binding cassette transporters are required for efficient RNA interference in Caenorhabditis elegans. Mol Biol Cell 17: 3678-3688.
48. Reddien P, Oviedo N, Jennings J, Jenkin J, Sanchez Alvarado A, (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.
49. Palakodeti D, Smielewska M, Lu Y-C, Yeo G, Graveley B, (2008) The PIWI Proteins SMEDWI-2 and SMEDWI-3 are Required for Stem Cell Function and piRNA Expression in Planarians. RNA 14: 1174-1186.
50. 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.
51. Meier-Stiegen F, Schwanbeck R, Bernoth K, Martini S, Hieronymus T, et al. (2010) Activated Notch1 target genes during embryonic cell differentiation depend on the cellular context and include lineage determinants and inhibitors. PLoS One 5: e11481.
52. Sestan N, Artavanis-Tsakonas S, Rakic P, (1999) Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286: 741-746.
53. Besset V, Rhee K, Wolgemuth DJ, (1999) The cellular distribution and kinase activity of the Cdk family member Pctaire1 in the adult mouse brain and testis suggest functions in differentiation. Cell Growth Differ 10: 173-181.
54. Fu WY, Cheng K, Fu AK, Ip NY, (2011) Cyclin-dependent kinase 5-dependent phosphorylation of Pctaire1 regulates dendrite development. Neuroscience 180: 353-359.
55. Huggins CE, Domenighetti AA, Ritchie ME, Khalil N, Favaloro JM, et al. (2008) Functional and metabolic remodelling in GLUT4-deficient hearts confers hyper-responsiveness to substrate intervention. J Mol Cell Cardiol 44: 270-280.
56. Kondoh E, Konno A, Inaba K, Oishi T, Murata M, et al. (2008) Valosin-containing protein/p97 interacts with sperm-activating and sperm-attracting factor (SAAF) in the ascidian egg and modulates sperm-attracting activity. Dev Growth Differ 50: 665-673.
57. Wang Y, Stary JM, Wilhelm JE, Newmark PA, (2010) A functional genomic screen in planarians identifies novel regulators of germ cell development. Genes Dev 24: 2081-2092.
58. Orkin SH, Hochedlinger K, (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell 145: 835-850.
59. Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, et al. (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447: 725-729.
60. Hollenbach JP, Resch AM, Palakodeti D, Graveley BR, Heinen CD, (2011) Loss of DNA mismatch repair imparts a selective advantage in planarian adult stem cells. PLoS One 6: e21808.
61. Koledova Z, Kramer A, Kafkova LR, Divoky V, (2010) Cell-cycle regulation in embryonic stem cells: centrosomal decisions on self-renewal. Stem Cells Dev 19: 1663-1678.
62. Ng HH, Surani MA, (2011) The transcriptional and signalling networks of pluripotency. Nat Cell Biol 13: 490-496.
63. Saiki Y, Yamazaki Y, Yoshida M, Katoh O, Nakamura T, (2000) Human EVI9, a homologue of the mouse myeloid leukemia gene, is expressed in the hematopoietic progenitors and down-regulated during myeloid differentiation of HL60 cells. Genomics 70: 387-391.
64. Calvanese V, Lara E, Suarez-Alvarez B, Abu Dawud R, Vazquez-Chantada M, et al. (2010) Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci U S A 107: 13736-13741.
65. Holubcova Z, Matula P, Sedlackova M, Vinarsky V, Dolezalova D, et al. (2010) Human embryonic stem cells suffer from centrosomal amplification. Stem Cells 29: 46-56.
66. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
67. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
68. Antin PB, Pier M, Sesepasara T, Yatskievych TA, Darnell DK, (2010) Embryonic expression of the chicken Kruppel-like (KLF) transcription factor gene family. Dev Dyn 239: 1879-1887.
69. Phillips K, Luisi B, (2000) The virtuoso of versatility: POU proteins that flex to fit. J Mol Biol 302: 1023-1039.
70. Archer TC, Jin J, Casey ES, (2010) Interaction of Sox1, Sox2, Sox3 and Oct4 during primary neurogenesis. Dev Biol 350: 429-440.
71. Laronda MM, Jameson JL, (2011) Sox3 functions in a cell-autonomous manner to regulate spermatogonial differentiation in mice. Endocrinology 152: 1606-1615.
72. Ritter AR, Beckstead RB, (2010) Sox14 is required for transcriptional and developmental responses to 20-hydroxyecdysone at the onset of drosophila metamorphosis. Dev Dyn 239: 2685-2694.
73. Guth SI, Wegner M, (2008) Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 65: 3000-3018.
74. Cebria F, Newmark P, (2005) 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: 3691-3703.
75. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
76. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
77. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.