Planarian Epidermal Stem Cells Respond to Positional Cues to Promote Cell-Type Diversity

Developmental Cell

Volumn 40, Issue 5, 2017, Pages 491-504.e5

  Wurtzel, Omri ^a,b,c   Oderberg, Isaac M ^a,b,c   Reddien, Peter W ^a,b,c  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

BMP signaling; epidermis; neoblast; patterning; planaria; progenitors; regeneration; single cell sequencing; stem cells

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; TRANSCRIPTION FACTOR; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; EPIDERMAL STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA INTERFERENCE; RNA SEQUENCE; SIGNAL TRANSDUCTION; TURBELLARIA; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; EPIDERMIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOSIS; MORPHOGENESIS; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; STEM CELL;

ANIMALS; BIOMARKERS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; EPIDERMIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MITOSIS; MODELS, BIOLOGICAL; PLANARIANS; RNA INTERFERENCE; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 85015036061     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2017.02.008     Document Type: Article

References (59)

1. Adell, T., Salo, E., Boutros, M., Bartscherer, K., Smed-Evi/Wntless is required for beta-catenin-dependent and -independent processes during planarian regeneration. Development 136 (2009), 905–910.
2. Adler, C.E., Sánchez Alvarado, A., Types or States? Cellular dynamics and regenerative potential. Trends Cell Biol. 25 (2015), 687–696.
3. Adler, C.E., Seidel, C.W., McKinney, S.A., Sánchez Alvarado, A., Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. Elife, 3, 2014, e02238.
4. Azimzadeh, J., Wong, M.L., Downhour, D.M., Sánchez Alvarado, A., Marshall, W.F., Centrosome loss in the evolution of planarians. Science 335 (2012), 461–463.
5. Baxendale, S., Davison, C., Muxworthy, C., Wolff, C., Ingham, P.W., Roy, S., The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signaling. Nat. Genet. 36 (2004), 88–93.
6. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L., BLAST+: architecture and applications. BMC Bioinformatics, 10, 2009, 421.
7. Cibois, M., Luxardi, G., Chevalier, B., Thome, V., Mercey, O., Zaragosi, L.E., Barbry, P., Pasini, A., Marcet, B., Kodjabachian, L., BMP signalling controls the construction of vertebrate mucociliary epithelia. Development 142 (2015), 2352–2363.
8. 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 140 (2013), 4691–4702.
9. Dubaissi, E., Papalopulu, N., Embryonic frog epidermis: a model for the study of cell-cell interactions in the development of mucociliary disease. Dis. Model. Mech. 4 (2011), 179–192.
10. Duncan, E.M., Chitsazan, A.D., Seidel, C.W., Sánchez Alvarado, A., Set1 and MLL1/2 target distinct sets of functionally different genomic loci in vivo. Cell Rep. 13 (2015), 2741–2755.
11. 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 3 (2008), 327–339.
12. 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 23 (2012), 691–704.
13. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
14. Geer, L.Y., Domrachev, M., Lipman, D.J., Bryant, S.H., CDART: protein homology by domain architecture. Genome Res. 12 (2002), 1619–1623.
15. 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. 337 (2010), 148–156.
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. 347 (2010), 24–39.
17. 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. 48 (2006), 371–380.
18. Hopman, A.H., Ramaekers, F.C., Speel, E.J., Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for in situ hybridization using CARD amplification. J. Histochem. Cytochem. 46 (1998), 771–777.
19. Jones, P., Binns, D., Chang, H.Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30 (2014), 1236–1240.
20. Katoh, K., Asimenos, G., Toh, H., Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537 (2009), 39–64.
21. King, R.S., Newmark, P.A., In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev. Biol., 13, 2013, 8.
22. Lapan, S.W., Reddien, P.W., Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration. Cell Rep. 2 (2012), 294–307.
23. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
24. Liu, S.Y., Selck, C., Friedrich, B., Lutz, R., Vila-Farre, M., Dahl, A., Brandl, H., Lakshmanaperumal, N., Henry, I., Rink, J.C., Reactivating head regrowth in a regeneration-deficient planarian species. Nature 500 (2013), 81–84.
25. Mi, H., Poudel, S., Muruganujan, A., Casagrande, J.T., Thomas, P.D., PANTHER version 10: expanded protein families and functions, and analysis tools. Nucleic Acids Res. 44 (2016), D336–D342.
26. Molina, M.D., Salo, E., Cebria, F., The BMP pathway is essential for re-specification and maintenance of the dorsoventral axis in regenerating and intact planarians. Dev. Biol. 311 (2007), 79–94.
27. Molina, M.D., Neto, A., Maeso, I., Gomez-Skarmeta, J.L., Saló, E., Cebrià, F., Noggin and noggin-like genes control dorsoventral axis regeneration in planarians. Curr. Biol. 21 (2011), 300–305.
28. Orii, H., Watanabe, K., Bone morphogenetic protein is required for dorso-ventral patterning in the planarian Dugesia japonica. Dev. Growth Differ. 49 (2007), 345–349.
29. 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. 238 (2009), 443–450.
30. Petersen, C.P., Reddien, P.W., A wound-induced Wnt expression program controls planarian regeneration polarity. Proc. Natl. Acad. Sci. USA 106 (2009), 17061–17066.
31. Picelli, S., Bjorklund, A.K., Faridani, O.R., Sagasser, S., Winberg, G., Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 10 (2013), 1096–1098.
32. Picelli, S., Faridani, O.R., Bjorklund, A.K., Winberg, G., Sagasser, S., Sandberg, R., Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9 (2014), 171–181.
33. Quigley, I.K., Stubbs, J.L., Kintner, C., Specification of ion transport cells in the Xenopus larval skin. Development 138 (2011), 705–714.
34. Quinlan, A.R., Hall, I.M., BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 (2010), 841–842.
35. Reddien, P.W., Constitutive gene expression and the specification of tissue identity in adult planarian biology. Trends Genet. 27 (2011), 277–285.
36. Reddien, P.W., Specialized progenitors and regeneration. Development 140 (2013), 951–957.
37. Reddien, P.W., Sánchez Alvarado, A., Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20 (2004), 725–757.
38. 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 310 (2005), 1327–1330.
39. Reddien, P.W., Bermange, A.L., Kicza, A.M., Sánchez Alvarado, A., BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134 (2007), 4043–4051.
40. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
41. Rouhana, L., Weiss, J.A., Forsthoefel, D.J., Lee, H., King, R.S., Inoue, T., Shibata, N., Agata, K., Newmark, P.A., RNA interference by feeding in vitro-synthesized double-stranded RNA to planarians: methodology and dynamics. Dev. Dyn. 242 (2013), 718–730.
42. Sánchez Alvarado, A., Yamanaka, S., Rethinking differentiation: stem cells, regeneration, and plasticity. Cell 157 (2014), 110–119.
43. Satija, R., Farrell, J.A., Gennert, D., Schier, A.F., Regev, A., Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33 (2015), 495–502.
44. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
45. Scimone, M.L., Srivastava, M., Bell, G.W., Reddien, P.W., A regulatory program for excretory system regeneration in planarians. Development 138 (2011), 4387–4398.
46. Scimone, M.L., Kravarik, K.M., Lapan, S.W., Reddien, P.W., Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Rep. 3 (2014), 339–352.
47. Scimone, M.L., Lapan, S.W., Reddien, P.W., A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet., 10, 2014, e1003999.
48. Stamatakis, A., RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006), 2688–2690.
49. Tazaki, A., Kato, K., Orii, H., Agata, K., Watanabe, K., The body margin of the planarian Dugesia japonica: characterization by the expression of an intermediate filament gene. Dev. Genes Evol. 212 (2002), 365–373.
50. Trost, A., Bauer, J.W., Lanschutzer, C., Laimer, M., Emberger, M., Hintner, H., Onder, K., Rapid, high-quality and epidermal-specific isolation of RNA from human skin. Exp. Dermatol. 16 (2007), 185–190.
51. Tu, K.C., Cheng, L.C., T.K.Vu, H., Lange, J.J., McKinney, S.A., Seidel, C.W., Sánchez Alvarado, A., Egr-5 is a post-mitotic regulator of planarian epidermal differentiation. Elife, 4, 2015, e10501.
52. van der Maaten, L., Hinton, G., Visualizing data using t-SNE. J. Mach. Learn. Res., 9, 2008, 85.
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 15 (2014), 326–339.
54. Vij, S., Rink, J.C., Ho, H.K., Babu, D., Eitel, M., Narasimhan, V., Tiku, V., Westbrook, J., Schierwater, B., Roy, S., Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS Genet., 8, 2012, e1003019.
55. Wagner, D.E., Wang, I.E., Reddien, P.W., Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332 (2011), 811–816.
56. Wenemoser, D., Reddien, P.W., Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 344 (2010), 979–991.
57. Witchley, J.N., Mayer, M., Wagner, D.E., Owen, J.H., Reddien, P.W., Muscle cells provide instructions for planarian regeneration. Cell Rep. 4 (2013), 633–641.
58. Wurtzel, O., Cote, L.E., Poirier, A., Satija, R., Regev, A., Reddien, P.W., A generic and cell-type-specific wound response precedes regeneration in planarians. Dev. Cell 35 (2015), 632–645.
59. Zhu, S.J., Hallows, S.E., Currie, K.W., Xu, C., Pearson, B.J., A mex3 homolog is required for differentiation during planarian stem cell lineage development. Elife, 4, 2015, e07025.