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Planarian Stem Cell Heterogeneity

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Stem Cells Heterogeneity - Novel Concepts

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1123))

Abstract

Planarian (Platyhelminthes, Triclads) are free-living flatworms endowed with extraordinary regenerative capabilities, i.e., the ability to rebuild any missing body parts also from small fragments. Planarian regenerative capabilities fascinated scientific community since early 1800, including high-standing scientists such as J.T. Morgan and C. M. Child. Today, it is known that planarian regeneration is due to the presence of a wide population of stem cells, the so-called neoblasts. However, the understanding of the nature of cells orchestrating planarian regeneration was a long journey, and several questions still remain unanswered. In this chapter, beginning from the definition of the classical concept of neoblast, we review progressive discoveries that have brought to the modern view of these cells as a highly heterogeneous population of stem cells including pluripotent stem cells and undifferentiated populations of committed progenies.

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References

  1. Randolph H (1897) Observations and experiments on regeneration in planarians. Arch Entwickl Mech Org 5:352–372

    Article  Google Scholar 

  2. Hyman LH (1951) The invertebrates: Platyhelminthes and Rhynchocoela the acoelomatebilateria. McGraw-Hill, New York

    Google Scholar 

  3. Hori I (1992) Cytological approach to morphogenesis in the planarian blastema. I. Cell behavior during blastema formation. J Submicrosc Cytol Pathol 24:75–84

    Google Scholar 

  4. Morita M (1967) Observations on the fine structure of the neoblast and its cell division in the regenerating planaria. Sci Rep Tohoku Univ 33:399–406

    Google Scholar 

  5. Pedersen KJ (1959) Cytological studies on the planarian neoblast. Z Zellforsch Mikrosk Anat 50:799–817

    Article  CAS  Google Scholar 

  6. Coward SJ (1974) Chromatoid bodies in somatic cells of the planarian: observations on their behavior during mitosis. Anat Rec 180:533–545

    Article  CAS  Google Scholar 

  7. Hay ED, Coward SJ (1975) Fine structure studies on the planarian, Dugesia. I. Nature of the "neoblast" and other cell types in noninjured worms. J Ultrastruct Res 50:1–21

    Article  CAS  Google Scholar 

  8. Hori I (1982) An ultrastructural study of the chromatoid body in planarian regenerative cells. J Electron Microsc (Tokyo) 31:63–72

    Google Scholar 

  9. Morita M, Best JB, Noel J (1969) Electron microscopic studies of planarian regeneration. I. Fine structure of neoblasts in Dugesia dorotocephala. J Ultrastruct Res 27:7–23

    Article  Google Scholar 

  10. Strome S, Updike D (2015) Specifying and protecting germ cell fate. Nat Rev Mol Cell Biol 16:406–416

    Article  CAS  Google Scholar 

  11. Fernandéz-Taboada E, Moritz S, Zeuschner D et al (2010) Smed-SmB, a member of the LSm protein superfamily, is essential for chromatoid body organization and planarian stem cell proliferation. Development 137:1055–1065

    Article  Google Scholar 

  12. Solana J, Lasko P, Romero R (2009) Spoltud-1 is a chromatoid body component required for planarian long-term stem cell self-renewal. Dev Biol 328:410–421

    Article  CAS  Google Scholar 

  13. Yoshida-Kashikawa M, Shibata N, Takechi K et al (2007) DjCBC-1, a conserved DEAD box RNA helicase of the RCK/p54/Me31B family, is a component of RNA-protein complexes in planarian stem cells and neurons. Dev Dyn 236:3436–3450

    Article  CAS  Google Scholar 

  14. Kashima M, Kumagai N, Agata K et al (2016) Heterogeneity of chromatoid bodies in adult pluripotent stem cells of planarian Dugesia japonica. Dev Growth Differ 58:225–237

    Article  CAS  Google Scholar 

  15. Juliano CE, Swartz SZ, Wessel GM (2010) A conserved germline multipotency program. Development 137:4113–4126

    Article  CAS  Google Scholar 

  16. Rouhana L, Vieira AP, Roberts-Galbraith RH et al (2012) PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development 139:1083–1094

    Article  CAS  Google Scholar 

  17. Rossi L, Salvetti A, Batistoni R et al (2008) Planarians, a tale of stem cells. Cell Mol Life Sci 65:16–23

    Article  CAS  Google Scholar 

  18. Hayashi T, Asami M, Higuchi S et al (2006) Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48:371–380

    Article  Google Scholar 

  19. Baguñà J (1976) Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. I. Mitotic studies during growth feeding and starvation. J Exp Zool 195:53–64

    Article  Google Scholar 

  20. Newmark PA, Sanchez Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142–153

    Article  CAS  Google Scholar 

  21. Orii H, Sakurai T, Watanabe K (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev Genes Evol 215:143–157

    Article  CAS  Google Scholar 

  22. Salvetti A, Rossi L, Deri P et al (2000) An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Dev Dyn 218:603–614

    Article  CAS  Google Scholar 

  23. Solana J, Kao D, Mihaylova Y et al (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol 13:R19

    Article  CAS  Google Scholar 

  24. Rossi L, Bonuccelli L, Iacopetti P et al (2014) Prohibitin 2 regulates cell proliferation and mitochondrial cristae morphogenesis in planarian stem cells. Stem Cell Rev 10:871–887

    Article  CAS  Google Scholar 

  25. Guo T, Peters AH, Newmark PA (2006) A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11:159–169

    Article  CAS  Google Scholar 

  26. Reddien PW, Oviedo NJ, Jennings JR et al (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–1330

    Article  CAS  Google Scholar 

  27. Salvetti A, Rossi L, Lena A et al (2005) DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132:1863–1874

    Article  CAS  Google Scholar 

  28. Shibata N, Umesono Y, Orii H et al (1999) Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev Biol 206:73–87

    Article  CAS  Google Scholar 

  29. Chandebois R (1980) The dynamics of wound closure and its role in the programming of planarian regeneration. II—distalization. Dev Growth Differ 22:693–704

    Article  Google Scholar 

  30. Hori I (1989) Observations on planarian epithelization after wounding. J Submicrosc Cytol Pathol 21:307–315

    CAS  PubMed  Google Scholar 

  31. Pellettieri J, Fitzgerald P, Watanabe S et al (2010) Cell death and tissue remodeling in planarian regeneration. Dev Biol 338:76–85

    Article  CAS  Google Scholar 

  32. Wenemoser D, Reddien PW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344:979–991

    Article  CAS  Google Scholar 

  33. Baguñà J (2018) Planarian regeneration between 1960s and 1990s: From skilful baffled ancestors to bold integrative descendants. A personal account. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2018.04.011

    Article  Google Scholar 

  34. Higuchi S, Hayashi T, Hori I et al (2007) Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis. Dev Growth Differ 49:571–581

    Article  Google Scholar 

  35. Rossi L, Salvetti A, Lena A et al (2006) DjPiwi-1, a member of the PAZ-Piwi gene family, defines a subpopulation of planarian stem cells. Dev Genes Evol 216:335–346

    Article  CAS  Google Scholar 

  36. Rossi L, Salvetti A, Marincola FM et al (2007) Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol 8:R62

    Article  Google Scholar 

  37. Sato K, Shibata N, Orii H et al (2006) Identification and origin of the germline stem cells as revealed by the expression of nanos related gene in planarians. Dev Growth Differ 48:615–628

    Article  CAS  Google Scholar 

  38. Handberg-Thorsager M, Salo E (2007) The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev Genes Evol 217:403–411

    Article  CAS  Google Scholar 

  39. Salvetti A, Rossi L, Bonuccelli L et al (2009) Adult stem cell plasticity: neoblast repopulation in non-lethally irradiated planarians. Dev Biol 328:305–314

    Article  CAS  Google Scholar 

  40. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332:811–816

    Article  CAS  Google Scholar 

  41. Reddien PW (2013) Specialized progenitors and regeneration. Development 140:951–957

    Article  CAS  Google Scholar 

  42. Scimone ML, Kravarik KM, Lapan SW et al (2014) Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Rep 3:339–352

    Article  CAS  Google Scholar 

  43. Lapan SW, Reddien PW (2012) Transcriptome analysis of the planarian eye identifies ovo as a specific regulator of eye regeneration. Cell Rep 2:294–307

    Article  CAS  Google Scholar 

  44. Scimone ML, Srivastava M, Bell GW et al (2011) A regulatory program for excretory system regeneration in planarians. Development 138:4387–4398

    Article  CAS  Google Scholar 

  45. Currie KW, Pearson BJ (2013) Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development 140:3577–3588

    Article  CAS  Google Scholar 

  46. Cowles MW, Brown DD, Nisperos SV et al (2013) Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 140:4691–4702

    Article  CAS  Google Scholar 

  47. Adler CE, Seidel CW, McKinney SA et al (2014) Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. Elife 3:e02238

    Article  Google Scholar 

  48. Scimone ML, Lapan SW, Reddien PW (2014) A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet 10:e1003999

    Article  Google Scholar 

  49. Vásquez-Doorman C, Petersen CP (2014) zic-1 expression in planarian neoblasts after injury controls anterior pole regeneration. PLoS Genet 10:e1004452

    Article  Google Scholar 

  50. Flores NM, Oviedo NJ, Sage J (2016) Essential role for the planarian intestinal GATA transcription factor in stem cells and regeneration. Dev Biol 418:179–188

    Article  CAS  Google Scholar 

  51. Zhu SJ, Pearson BJ (2016) (Neo)blast from the past: new insights into planarian stem cell lineages. Curr Opin Genet Dev 40:74–80

    Article  CAS  Google Scholar 

  52. van Wolfswinkel JC, Wagner DE, Reddien PW (2014) Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment. Cell Stem Cell 15:326–339

    Article  Google Scholar 

  53. Fincher CT, Wurtzel O, de Hoog T et al (2018) Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360:eaaq1736

    Article  Google Scholar 

  54. Zeng A, Li H, Guo L, Gao X et al (2018) Prospectively isolated tetraspanin(+) neoblasts are adult pluripotent stem cells underlying planaria regeneration. Cell 173:1593–1608.e20

    Article  CAS  Google Scholar 

  55. Forsthoefel DJ, James NP, Escobar DJ et al (2012) An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev Cell 23:691–704

    Article  CAS  Google Scholar 

  56. Eisenhoffer GT, Kang H, 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

    Article  CAS  Google Scholar 

  57. Lai AG, Kosaka N, Abnave P et al (2018) The abrogation of condensin function provides independent evidence for defining the self-renewing population of pluripotent stem cells. Dev Biol 433:218–226

    Article  CAS  Google Scholar 

  58. Sahu S, Dattani A, Aboobaker AA (2017) Secrets from immortal worms: What can we learn about biological ageing from the planarian model system? Semin Cell Dev Biol 70:108–121

    Article  Google Scholar 

  59. Rossi L, Salvetti A (2018) Planarian stem cell niche, the challenge for understanding tissue regeneration. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2018.03.005

    Article  CAS  Google Scholar 

  60. Dattani A, Sridhar D, Aziz Aboobaker A (2018) Planarian flatworms as a new model system for understanding the epigenetic regulation of stem cell pluripotency and differentiation. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2018.04.007

    Article  CAS  Google Scholar 

  61. Felix DA, Gutiérrez-Gutiérrez Ó, Espada L et al (2018) It is not all about regeneration: planarians striking power to stand starvation. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2018.04.010

    Article  Google Scholar 

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Correspondence to Leonardo Rossi .

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Alessandra, S., Rossi, L. (2019). Planarian Stem Cell Heterogeneity. In: Birbrair, A. (eds) Stem Cells Heterogeneity - Novel Concepts. Advances in Experimental Medicine and Biology, vol 1123. Springer, Cham. https://doi.org/10.1007/978-3-030-11096-3_4

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