A Generic and Cell-Type-Specific Wound Response Precedes Regeneration in Planarians

Developmental Cell

Volumn 35, Issue 5, 2015, Pages 632-645

  Wurtzel, Omri ^a,b   Cote, Lauren E ^a,b   Poirier, Amber ^a,b   Satija, Rahul ^c,d,e   Regev, Aviv ^b,c   Reddien, Peter W ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d NEW YORK GENOME CENTER   (United States)

^e NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; DOUBLE STRANDED RNA; ESTERASE; WNT PROTEIN;

ARTICLE; CELL SPECIFICITY; EPIDERMIS; GENE; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; MUSCLE CELL; NONHUMAN; NOTUM GENE; PLATYHELMINTH; PRIORITY JOURNAL; RNA SEQUENCE; STEM CELL; TISSUE SPECIFICITY; TURBELLARIA; WOUND HEALING; ANIMAL; CELL SEPARATION; CLUSTER ANALYSIS; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; METABOLISM; MOLECULAR CLONING; MORPHOGENESIS; PHYSIOLOGY; REGENERATION;

ANIMALS; BODY PATTERNING; CELL SEPARATION; CLONING, MOLECULAR; CLUSTER ANALYSIS; ESTERASES; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; PLANARIANS; REGENERATION; RNA, DOUBLE-STRANDED; STEM CELLS; TRANSCRIPTION, GENETIC; WNT PROTEINS; WOUND HEALING;

EID: 84961620215     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.11.004     Document Type: Article

References (58)

1. Adell T., Salò 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. Chechik G., Koller D. Timing of gene expression responses to environmental changes. J. Comput. Biol. 2009, 16:279-290.
3. Chechik G., Oh E., Rando O., Weissman J., Regev A., Koller D. Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nat. Biotechnol. 2008, 26:1251-1259.
4. Cowles M.W., Brown D.D., Nisperos S.V., Stanley B.N., Pearson B.J., Zayas R.M. Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 2013, 140:4691-4702.
5. DuBuc T.Q., Traylor-Knowles N., Martindale M.Q. Initiating a regenerative response; cellular and molecular features of wound healing in the cnidarian Nematostella vectensis. BMC Biol. 2014, 12:24.
6. 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.
7. Engreitz J.M., Sirokman K., McDonel P., Shishkin A.A., Surka C., Russell P., Grossman S.R., Chow A.Y., Guttman M., Lander E.S. RNA-RNA interactions enable specific targeting of noncoding RNAs to nascent Pre-mRNAs and chromatin sites. Cell 2014, 159:188-199.
8. Ester, M., Kriegel, H.-P., Sander, J., and Xu, X. (1996). A density-based algorithm for discovering clusters in large spatial databases with noise. Proceedings of 2nd International Conference on Knowledge Discovery and Data Mining (KDD-96), . http://www.dbs.ifi.lmu.de/Publikationen/Papers/KDD-96.final.frame.pdf.
9. Flickinger R.A., Coward S.J. The induction of cephalic differentiation in regenerating Dugesia dorotocephala in the presence of the normal head and in unwounded tails. Dev. Biol. 1962, 5:179-204.
10. Forsthoefel D.J., Park A.E., Newmark P.A. Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev. Biol. 2011, 356:445-459.
11. Forsthoefel D.J., James N.P., Escobar D.J., Stary J.M., Vieira A.P., Waters F.A., Newmark P.A. An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev. Cell 2012, 23:691-704.
12. Gaviño M.A., Wenemoser D., Wang I.E., Reddien P.W. Tissue absence initiates regeneration through follistatin-mediated inhibition of activin signaling. eLife 2013, 2:e00247.
13. Gerlitz O., Basler K. Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev. 2002, 16:1055-1059.
14. Glazer A.M., Wilkinson A.W., Backer C.B., Lapan S.W., Gutzman J.H., Cheeseman I.M., Reddien P.W. The Zn finger protein Iguana impacts Hedgehog signaling by promoting ciliogenesis. Dev. Biol. 2010, 337:148-156.
15. Guo T., Peters A.H., Newmark P.A. A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 2006, 11:159-169.
16. Gurley K.A., Elliott S.A., Simakov O., Schmidt H.A., Holstein T.W., Sánchez Alvarado A. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev. Biol. 2010, 347:24-39.
17. Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature 2008, 453:314-321.
18. Hayashi T., Asami M., Higuchi S., Shibata N., Agata K. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev. Growth Differ. 2006, 48:371-380.
19. Jaitin D.A., Kenigsberg E., Keren-Shaul H., Elefant N., Paul F., Zaretsky I., Mildner A., Cohen N., Jung S., Tanay A., Amit I. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 2014, 343:776-779.
20. Kao D., Felix D., Aboobaker A. The planarian regeneration transcriptome reveals a shared but temporally shifted regulatory program between opposing head and tail scenarios. BMC Genomics 2013, 14:797.
21. Knapp D., Schulz H., Rascon C.A., Volkmer M., Scholz J., Nacu E., Le M., Novozhilov S., Tazaki A., Protze S., et al. Comparative transcriptional profiling of the axolotl limb identifies a tripartite regeneration-specific gene program. PLoS ONE 2013, 8:e61352.
22. Lapan S.W., Reddien P.W. Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration. Cell Rep. 2012, 2:294-307.
23. 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.
24. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
25. Liu S.Y., Selck C., Friedrich B., Lutz R., Vila-Farré M., Dahl A., Brandl H., Lakshmanaperumal N., Henry I., Rink J.C. Reactivating head regrowth in a regeneration-deficient planarian species. Nature 2013, 500:81-84.
26. Louvi A., Grove E.A. Cilia in the CNS: the quiet organelle claims center stage. Neuron 2011, 69:1046-1060.
27. Macosko E.Z., Basu A., Satija R., Nemesh J., Shekhar K., Goldman M., Tirosh I., Bialas A.R., Kamitaki N., Martersteck E.M., et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 2015, 161:1202-1214.
28. McDavid A., Finak G., Chattopadyay P.K., Dominguez M., Lamoreaux L., Ma S.S., Roederer M., Gottardo R. Data exploration, quality control and testing in single-cell qPCR-based gene expression experiments. Bioinformatics 2013, 29:461-467.
29. Pearson B.J., Sánchez Alvarado A. A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development 2010, 137:213-221.
30. 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.
31. 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.
32. Petersen C.P., Reddien P.W. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
33. Petersen C.P., Reddien P.W. A wound-induced Wnt expression program controls planarian regeneration polarity. Proc. Natl. Acad. Sci. U S A 2009, 106:17061-17066.
34. Petersen C.P., Reddien P.W. Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 2011, 332:852-855.
35. Picelli S., Björklund A.K., Faridani O.R., Sagasser S., Winberg G., Sandberg R. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 2013, 10:1096-1098.
36. Picelli S., Faridani O.R., Björklund A.K., Winberg G., Sagasser S., Sandberg R. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 2014, 9:171-181.
37. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
38. Reddien P.W. Constitutive gene expression and the specification of tissue identity in adult planarian biology. Trends Genet. 2011, 27:277-285.
39. Reddien P.W., Sánchez Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 2004, 20:725-757.
40. 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.
41. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
42. 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.
43. Sandmann T., Vogg M.C., Owlarn S., Boutros M., Bartscherer K. The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol. 2011, 12:R76.
44. Satija R., Farrell J.A., Gennert D., Schier A.F., Regev A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 2015, 33:495-502.
45. Schwartz S., Bernstein D.A., Mumbach M.R., Jovanovic M., Herbst R.H., León-Ricardo B.X., Engreitz J.M., Guttman M., Satija R., Lander E.S., et al. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 2014, 159:148-162.
46. Scimone M.L., Srivastava M., Bell G.W., Reddien P.W. A regulatory program for excretory system regeneration in planarians. Development 2011, 138:4387-4398.
47. Scimone M.L., Kravarik K.M., Lapan S.W., Reddien P.W. Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Reports 2014, 3:339-352.
48. Shalek A.K., Satija R., Adiconis X., Gertner R.S., Gaublomme J.T., Raychowdhury R., Schwartz S., Yosef N., Malboeuf C., Lu D., et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498:236-240.
49. Shalek A.K., Satija R., Shuga J., Trombetta J.J., Gennert D., Lu D., Chen P., Gertner R.S., Gaublomme J.T., Yosef N., et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 2014, 510:363-369.
50. Shibata N., Umesono Y., Orii H., Sakurai T., Watanabe K., Agata K. Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev. Biol. 1999, 206:73-87.
51. Sing T., Sander O., Beerenwinkel N., Lengauer T. ROCR: visualizing classifier performance in R. Bioinformatics 2005, 21:3940-3941.
52. Sivriver J., Habib N., Friedman N. An integrative clustering and modeling algorithm for dynamical gene expression data. Bioinformatics 2011, 27:i392-i400.
53. van Wolfswinkel J.C., Wagner D.E., Reddien P.W. Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment. Cell Stem Cell 2014, 15:326-339.
54. Vogg M.C., Owlarn S., Pérez Rico Y.A., Xie J., Suzuki Y., Gentile L., Wu W., Bartscherer K. Stem cell-dependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Dev. Biol. 2014, 390:136-148.
55. Wagner D.E., Wang I.E., Reddien P.W. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011, 332:811-816.
56. Wenemoser D., Reddien P.W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 2010, 344:979-991.
57. Wenemoser D., Lapan S.W., Wilkinson A.W., Bell G.W., Reddien P.W. A molecular wound response program associated with regeneration initiation in planarians. Genes Dev. 2012, 26:988-1002.
58. Witchley J.N., Mayer M., Wagner D.E., Owen J.H., Reddien P.W. Muscle cells provide instructions for planarian regeneration. Cell Rep. 2013, 4:633-641.