Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment

Cell Stem Cell

Volumn 15, Issue 3, 2014, Pages 326-339

  Van Wolfswinkel, Josien C ^a   Wagner, Daniel E ^a   Reddien, Peter W ^a  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EPIDERMIS CELL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HOMEOSTASIS; MITOSIS; NEOBLAST; NONHUMAN; PLATYHELMINTH; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL; TURBELLARIA; ANIMAL; CELL CYCLE; CYTOLOGY; EPIDERMIS; METABOLISM; PROCEDURES; REGENERATION; RNA INTERFERENCE; SINGLE CELL ANALYSIS;

PLANARIA; PLATYHELMINTHES; TURBELLARIA;

BIOLOGICAL MARKER;

ANIMALS; BIOMARKERS; CELL COMPARTMENTATION; CELL CYCLE; CELL LINEAGE; EPIDERMIS; GENE EXPRESSION PROFILING; PLANARIANS; PLURIPOTENT STEM CELLS; REGENERATION; RNA INTERFERENCE; SINGLE-CELL ANALYSIS; STEM CELLS;

EID: 84909590292     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.06.007     Document Type: Article

References (42)

1. Blythe, M.J., Kao, D., Malla, S., Rowsell, J.,Wilson, R., Evans, D.,Jowett, J.,Hall, A., Lemay, V., Lam, S., and Aboobaker, A.A. (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.
2. Cowles, M.W., Brown, D.D.R., Nisperos, S.V., Stanley, B.N., Pearson, B.J., and Zayas, R.M. (2013). Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 140, 4691-4702.
3. Currie, K.W., and Pearson, B.J. (2013). Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 140, 3577-3588.
4. Dalerba, P., Kalisky, T., Sahoo, D., Rajendran, P.S., Rothenberg, M.E., Leyrat, A.A., Sim, S., Okamoto, J., Johnston, D.M., Qian, D., et al. (2011). Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol. 29, 1120-1127.
5. Eisenhoffer, G.T., Kang, H., and 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.
6. Forsthoefel, D.J., James, N.P., Escobar, D.J., Stary, J.M., Vieira, A.P., Waters, F.A., and Newmark, P.A. (2012). An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev. Cell 23, 691-704.
7. Galloni, M. (2012). Global irradiation effects, stem cell genes and rare transcripts in the planarian transcriptome. Int. J. Dev. Biol. 56, 103-116.
8. Guedelhoefer, O.C., 4th, and Sánchez Alvarado, A. (2012). Amputation induces stem cell mobilization to sites of injury during planarian regeneration. Development 139, 3510-3520.
9. Guo, G., Huss, M., Tong, G.Q., Wang, C., Li Sun, L., Clarke, N.D., and Robson, P. (2010). Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 18, 675-685.
10. Guo, T., Peters, A.H.F.M., and Newmark, P.A. (2006). A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11, 159-169.
11. Hayashi, T., Asami, M., Higuchi, S., Shibata, N., and Agata, K. (2006). Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev. Growth Differ. 48, 371-380.
12. Hayashi, T., Shibata, N., Okumura, R., Kudome, T., Nishimura, O., Tarui, H., and Agata, K. (2010). Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its "index sorting" function for stem cell research. Dev. Growth Differ. 52, 131-144.
13. Junker, J.P., and van Oudenaarden, A. (2014). Every cell is special: genomewide studies add a new dimension to single-cell biology. Cell 157, 8-11.
14. Labbé, R.M., Irimia, M., Currie, K.W., Lin, A., Zhu, S.J., Brown, D.D.R., Ross, E.J., Voisin, V., Bader, G.D., Blencowe, B.J., and Pearson, B.J. (2012). A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30, 1734-1745.
15. Lapan, S.W., and Reddien, P.W. (2011). dlx and sp6-9 Control optic cup regeneration in a prototypic eye. PLoS Genet. 7, e1002226.
16. Livak, K.J., Wills, Q.F., Tipping, A.J., Datta, K., Mittal, R., Goldson, A.J., Sexton, D.W., and Holmes, C.C. (2013). Methods for qPCR gene expression profiling applied to 1440 lymphoblastoid single cells. Methods 59, 71-79.
17. Moritz, S., Stöckle, F., Ortmeier, C., Schmitz, H., Rodríguez-Esteban, G., Key, G., and Gentile, L. (2012). Heterogeneity of planarian stem cells in the S/G2/M phase. Int. J. Dev. Biol. 56, 117-125.
18. Newmark, P.A., and Sánchez Alvarado, A. (2000). Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220, 142-153.
19. Onal, P., Grün, D., Adamidi, C., Rybak, A., Solana, J., Mastrobuoni, G., Wang, Y., Rahn, H.-P., Chen, W., Kempa, S., et al. (2012). Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO J. 31, 2755-2769.
20. Palakodeti, D., Smielewska, M., Lu, Y.-C., Yeo, G.W., and Graveley, B.R. (2008). The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14, 1174-1186
21. Pearson, B.J., and Sánchez Alvarado, A. (2010). A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development 137, 213-221.
22. Pearson, B.J., Eisenhoffer, G.T., Gurley, K.A., Rink, J.C., Miller, D.E., and Sánchez Alvarado, A. (2009). Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn. 238, 443-450.
23. Raj, A., and van Oudenaarden, A. (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226.
24. Reddien, P.W., and Sánchez Alvarado, A. (2004). Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20, 725-757.
25. Reddien, P.W., Bermange, A.L., Murfitt, K.J., Jennings, J.R., and Sánchez Alvarado, A. (2005a). Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 8, 635-649.
26. Reddien, P.W., Oviedo, N.J., Jennings, J.R., Jenkin, J.C., and Sánchez Alvarado, A. (2005b). SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310, 1327-1330.
27. Resch, A.M., Palakodeti, D., Lu, Y.-C., Horowitz, M., and Graveley, B.R. (2012). Transcriptome analysis reveals strain-specific and conserved stemness genes in Schmidtea mediterranea. PLoS ONE 7, e34447.
28. Rossi, A., Ross, E.J., Jack, A., and Sánchez Alvarado, A. (2014). Molecular cloning and characterization of SL3: a stem cell-specific SL RNA from the planarian Schmidtea mediterranea. Gene 533, 156-167.
29. Salvetti, A., Rossi, L., Deri, P., and Batistoni, R. (2000). An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Dev. Dyn. 218, 603-614.
30. Salvetti, A., Rossi, L., Lena, A., Batistoni, R., Deri, P., Rainaldi, G., Locci, M.T., Evangelista, M., and Gremigni, V. (2005). DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132, 1863-1874.
31. Scimone, M.L., Meisel, J., and Reddien, P.W. (2010). The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 137, 1231-1241.
32. Scimone, M.L., Srivastava, M., Bell, G.W., and Reddien, P.W. (2011). A regulatory program for excretory system regeneration in planarians. Development 138, 4387-4398.
33. Shibata, N., Hayashi, T., Fukumura, R., Fujii, J., Kudome-Takamatsu, T., Nishimura, O., Sano, S., Son, F., Suzuki, N., Araki, R., et al. (2012). Comprehensive gene expression analyses in pluripotent stem cells of a planarian, Dugesia japonica. Int. J. Dev. Biol. 56, 93-102.
34. Solana, J., Lasko, P., and Romero, R. (2009). Spoltud-1 is a chromatoid body component required for planarian long-term stem cell self-renewal. Dev. Biol. 328, 410-421.
35. Solana, J., Kao, D., Mihaylova, Y., Jaber-Hijazi, F., Malla, S., Wilson, R., and Aboobaker, A. (2012). Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol. 13, R19.
36. Voronina, E., Seydoux, G., Sassone-Corsi, P., and Nagamori, I. (2011). RNA granules in germ cells. Cold Spring Harb. Perspect. Biol. 3, 12.
37. Wagner, D.E., Wang, I.E., and Reddien, P.W. (2011). Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332, 811-816.
38. Wagner, D.E., Ho, J.J., and Reddien, P.W. (2012). Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10, 299-311.
39. Wenemoser, D., and Reddien, P.W. (2010). Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 344, 979-991.
40. Wolff, E., and Dubois, F. (1948). Sur la migration des cellules de régénération chez les planaires [On the migration of regenerative cells in planarians]. Rev. Suisse Zool. 55, 218-227.
41. Zayas, R.M., Cebrià, F., Guo, T., Feng, J., and Newmark, P.A. (2010). The use of lectins as markers for differentiated secretory cells in planarians. Dev. Dyn. 239, 2888-2897.
42. Zhu, S.J., and Pearson, B.J. (2013). The Retinoblastoma pathway regulates stem cell proliferation in freshwater planarians. Dev. Biol. 373, 442-452.