Types or States? Cellular Dynamics and Regenerative Potential

Trends in Cell Biology

Volumn 25, Issue 11, 2015, Pages 687-696

  Adler, Carolyn E ^a,c   Sánchez Alvarado, Alejandro ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Cornell University ^*  (United States)

Author keywords

Homeostasis; Planaria; Plasticity; Regeneration; Stem cells

Indexed keywords

CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CELL REGENERATION; HOMEOSTASIS; NONHUMAN; PHARYNX; PHOTORECEPTOR; PLASTICITY; PLATYHELMINTH; PRIORITY JOURNAL; REVIEW; SCHMIDTEA MEDITERRANEA; SIGNAL TRANSDUCTION; STEM CELL; TISSUE REGENERATION; TURBELLARIA; UPREGULATION; WOUND HEALING; ANIMAL; CELL DIFFERENTIATION; HUMAN; PHYSIOLOGY; REGENERATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; HOMEOSTASIS; HUMANS; REGENERATION; STEM CELLS;

EID: 84945579263     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2015.07.008     Document Type: Review

References (99)

1. Mikkers H., Frisén J. Deconstructing stemness. EMBO J. 2005, 24:2715-2719.
2. Blanpain C., Fuchs E. Plasticity of epithelial stem cells in tissue regeneration. Science 2014, 344:1242281.
3. Donati G., Watt F.M. Stem cell heterogeneity and plasticity in epithelia. Cell Stem Cell 2015, 16:465-476.
4. Lu C.P., et al. Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell 2012, 150:136-150.
5. Van Keymeulen A., et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011, 479:189-193.
6. Goldstein A.S., et al. Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20882-20887.
7. Xin L., et al. Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 2007, 25:2760-2769.
8. Stingl J., et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006, 439:993-997.
9. Shackleton M., et al. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
10. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013, 154:274-284.
11. Buczacki S.J.A., et al. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 2013, 495:65-69.
12. + secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 2012, 14:1099-1104.
13. + distal airway stem cells are essential for lung regeneration. Nature 2015, 517:616-620.
14. Vaughan A.E., et al. Lineage-negative progenitors mobilize to regenerate lung epithelium after major injury. Nature 2015, 517:621-625.
15. Chubb J.R., Liverpool T.B. Bursts and pulses: insights from single cell studies into transcriptional mechanisms. Curr. Opin. Genet. Dev. 2010, 20:478-484.
16. Levine J.H., et al. Functional roles of pulsing in genetic circuits. Science 2013, 342:1188-1193.
17. Bonev B., et al. MicroRNA-9 modulates Hes1 ultradian oscillations by forming a double-negative feedback loop. Cell Rep. 2012, 2:10-18.
18. Goodfellow M., et al. microRNA input into a neural ultradian oscillator controls emergence and timing of alternative cell states. Nat. Commun. 2014, 5:1-10.
19. Buettner F., et al. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat. Biotechnol. 2015, 33:155-160.
20. Newmark P., Sánchez Alvarado A. Not your father's planarian: a classic model enters the era of functional genomics. Nat. Rev. Genet. 2002, 3:210-219.
21. Cebrià F., et al. The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech. Dev. 2002, 116:199-204.
22. Okamoto K., et al. Neural projections in planarian brain revealed by fluorescent dye tracing. Zool. Sci. 2005, 22:535-546.
23. Lapan S.W., Reddien P.W. dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet. 2011, 7:e1002226.
24. Forsthoefel D.J., et al. Stem cell-based growth, regeneration, and remodeling of the planarian intestine. Dev. Biol. 2011, 356:445-459.
25. Scimone M.L., et al. A regulatory program for excretory system regeneration in planarians. Development 2011, 138:4387-4398.
26. Rink J.C., et al. The maintenance and regeneration of the planarian excretory system are regulated by EGFR signaling. Development 2011, 138:3769-3780.
27. Newmark P., Sánchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 2000, 220:142-153.
28. Cowles M.W., et al. Genome-wide analysis of the bHLH gene family in planarians identifies factors required for adult neurogenesis and neuronal regeneration. Development 2013, 140:4691-4702.
29. Wagner D.E., et al. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011, 332:811-816.
30. Solana J., et al. Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNA-seq, RNA interference and irradiation approach. Genome Biol. 2012, 13:R19.
31. Wagner D.E., et al. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 2012, 10:299-311.
32. Baguñà J. The planarian neoblast: the rambling history of its origin and some current black boxes. Int. J. Dev. Biol. 2012, 52:19-37.
33. Rink J.C. Stem cell systems and regeneration in planaria. Dev. Genes Evol. 2012, 223:67-84.
34. Hayashi T., et al. 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. 2010, 52:131-144.
35. Shibata N., et al. Comprehensive gene expression analyses in pluripotent stem cells of a planarian, Dugesia japonica. Int. J. Dev. Biol. 2012, 56:93-102.
36. van Wolfswinkel J.C., et al. Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment. Cell Stem Cell 2014, 15:326-339.
37. 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.
38. 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.
39. Forsthoefel D.J., et al. An RNAi screen reveals intestinal regulators of branching morphogenesis, differentiation, and stem cell proliferation in planarians. Dev. Cell 2012, 23:691-704.
40. Adler C.E., et al. Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. Elife 2014, 3:e02238.
41. Scimone M.L., et al. Neoblast specialization in regeneration of the planarian Schmidtea mediterranea. Stem Cell Rep. 2014, 3:339-352.
42. Reddien P.W. Specialized progenitors and regeneration. Development 2013, 140:951-957.
43. Reddien P., Sánchez Alvarado A. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 2004, 20:725-757.
44. Baguñà J., et al. Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. Experimental Embryology in Aquatic Plants and Animals 1990, 129-162. Springer. H.-J. Marthy (Ed.).
45. Kang H., Alvarado A. Flow cytometry methods for the study of cell-cycle parameters of planarian stem cells. Dev. Dyn. 2009, 238:1111-1117.
46. Pellettieri J., et al. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2010, 338:76-85.
47. Oviedo N., et al. Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev. Dyn. 2003, 226:326-333.
48. González-Estévez C., et al. Decreased neoblast progeny and increased cell death during starvation-induced planarian degrowth. Int. J. Dev. Biol. 2012, 56:83-91.
49. Takeda H., et al. Planarians maintain a constant ratio of different cell types during changes in body size by using the stem cell system. Zool. Sci. 2009, 26:805-813.
50. Abeloos M. Recherches expérimentales sur la croissance et la régénération chez les planaires. Bull. Biol. 1930, 1:1-140.
51. Lillie F. Some notes on regeneration and regulation in planarians. Am. Nat. 1900, 34:173-177.
52. Schultz E. Über Reduktionen. I. Über Hungerserscheinungen bei Planaria lactea. Arch. Entwm. 1904, 18:555-577.
53. Berninger J. Über die Einwirkung des Hungers auf Planarien. J. Zool. Jahrb. 1911, 30:181-216.
54. Baguñà J., Romero R. Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina. Hydrobiologia 1981, 84:181-194.
55. Cowles M.W., et al. COE loss-of-function analysis reveals a genetic program underlying maintenance and regeneration of the nervous system in planarians. PLoS Genet. 2014, 10:e1004746.
56. Mann R.S., Carroll S.B. Molecular mechanisms of selector gene function and evolution. Curr. Opin. Genet. Dev. 2002, 12:592-600.
57. Koinuma S., et al. Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells. Gene 2000, 259:171-176.
58. Morgan T. Regeneration 1901, The Macmillan Company.
59. Kobayashi C., et al. The process of pharynx regeneration in planarians. Dev. Biol. 1999, 211:27-38.
60. Bueno D., et al. Maintenance of A/P body regions in planarians by TCEN49, a putative cystine-knot neurotrophin. Belg. J. Zool. 2001, 131:89-95.
61. Bueno D., et al. Regeneration of gross molecular body regions in planarian: from molecules to organs. Int. J. Dev. Biol. 2001, 45:S121-S122.
62. Reddien P., et al. BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 2007, 134:4043-4051.
63. Gurley K.A., et al. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev. Biol. 2010, 347:24-39.
64. Wenemoser D., et al. A molecular wound response program associated with regeneration initiation in planarians. Genes Dev. 2012, 26:988-1002.
65. Sandmann T., et al. The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol. 2011, 12:R76.
66. Reddien P.W. Constitutive gene expression and the specification of tissue identity in adult planarian biology. Trends Genet. 2011, 27:277-285.
67. 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.
68. Petersen C.P., Reddien P.W. Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 2011, 332:852-855.
69. Kato K., et al. Dorsal and ventral positional cues required for the onset of planarian regeneration may reside in differentiated cells. Dev. Biol. 2001, 233:109-121.
70. Saló E., Baguñà J. Cell movement in intact and regenerating planarians. Quantitation using chromosomal, nuclear and cytoplasmic markers. J. Embryol. Exp. Morphol. 1985, 89:57-70.
71. Witchley J.N., et al. Muscle cells provide instructions for planarian regeneration. Cell Rep. 2013, 4:633-641.
72. Reuter H., et al. β-Catenin-dependent control of positional information along the AP body axis in planarians involves a teashirt family member. Cell Rep. 2015, 10:253-265.
73. Wenemoser D., Reddien P.W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 2010, 344:979-991.
74. Baguñà J. Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. I. Mitotic studies during growth, feeding and starvation. J. Exp. Zool. 1976, 195:53-64.
75. Baguñà J. Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. II. Mitotic studies during regeneration, and a possible mechanism of blastema formation. J. Exp. Zool. 1976, 195:65-80.
76. Guedelhoefer O.C., Sánchez Alvarado A. Amputation induces stem cell mobilization to sites of injury during planarian regeneration. Development 2012, 139:3510-3520.
77. Scimone M.L., et al. A forkhead transcription factor is wound-induced at the planarian midline and required for anterior pole regeneration. PLoS Genet. 2014, 10:e1003999.
78. Vogg M.C., et al. Stem cell-dependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Dev. Biol. 2014, 390:136-148.
79. Vásquez-Doorman C., Petersen C.P. zic-1 expression in planarian neoblasts after injury controls anterior pole regeneration. PLoS Genet. 2014, 10:e1004452.
80. Roberts-Galbraith R.H., Newmark P.A. Follistatin antagonizes activin signaling and acts with notum to direct planarian head regeneration. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1363-1368.
81. Blassberg R.A., et al. PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration. Development 2013, 140:730-739.
82. Fraguas S., et al. EGFR signaling regulates cell proliferation, differentiation and morphogenesis during planarian regeneration and homeostasis. Dev. Biol. 2011, 354:87-101.
83. Sakurai T., et al. The planarian P2X homolog in the regulation of asexual reproduction. Int. J. Dev. Biol. 2012, 56:173-182.
84. Gaviño M.A., et al. Tissue absence initiates regeneration through Follistatin-mediated inhibition of Activin signaling. Elife 2013, 2:e00247.
85. Tu K.C., et al. TORC1 is required to balance cell proliferation and cell death in planarians. Dev. Biol. 2012, 365:458-469.
86. Almuedo-Castillo M., et al. JNK controls the onset of mitosis in planarian stem cells and triggers apoptotic cell death required for regeneration and remodeling. PLoS Genet. 2014, 10:e1004400.
87. Day S.J., Lawrence P.A. Measuring dimensions: the regulation of size and shape. Development 2000, 127:2977-2987.
88. Lander A.D., et al. Cell lineages and the logic of proliferative control. PLoS Biol. 2009, 7:e15.
89. Stanger B.Z. The biology of organ size determination. Diabetes Obes. Metab. 2008, 10:16-22.
90. Bullough W.S. Mitotic and functional homeostasis: a speculative review. Cancer Res. 1965, 25:1683-1727.
91. McPherron A.C., et al. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387:83-90.
92. McPherron A.C., Lee S.J. Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:12457-12461.
93. Ziller-Sengel C. Sur le facteur inhibiteur de la régénération du pharynx chez les planaires d'eau douce. Bull. Soc. Zool. France 1967, 92:295-302. (in French).
94. Ziller-Sengel C. [Investigation of the inhibition of the regeneration of the planarian pharynx. I. Evidence of an auto-inhibiting factor found in the regenerating pharynx]. J. Embryol. Exp. Morphol. 1967, 18:91-105.
95. Ziller-Sengel C. [Investigation of the inhibition of the regeneration of the planarian pharynx. II. Variations of the amount of the inhibitor dependent on the species and the phase of regeneration]. J. Embryol. Exp. Morphol. 1967, 18:107-119.
96. Jenny M., et al. Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J. 2002, 21:6338-6347.
97. Schonhoff S.E., et al. Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev. Biol. 2004, 270:443-454.
98. Thi-Kim Vu H., et al. Stem cells and fluid flow drive cyst formation in an invertebrate excretory organ. ELife 2015, 4:e07405.
99. Zhu S.J., et al. A mex3 homolog is required for differentiation during planarian stem cell lineage development. Elife 2015, 4:e07025.