Cited by 17Planarian Biology and ElectrostimulationDevelopmental Biology and Gene RegulationPluripotent Stem Cells Research

Regulation of genomic output and (pluri)potency in regeneration

Open access
Duncan, Elizabeth M., Sánchez Alvarado, Alejandro·2019·Annual Review of Genetics

Abstract

Regeneration is a remarkable phenomenon that has been the subject of awe and bafflement for hundreds of years. Although regeneration competence is found in highly divergent organisms throughout the animal kingdom, recent advances in tools used for molecular and genomic characterization have uncovered common genes, molecular mechanisms, and genomic features in regenerating animals. In this review we focus on what is known about how genome regulation modulates cellular potency during regeneration. We discuss this regulation in the context of complex tissue regeneration in animals, from Hydra to humans, with reference to ex vivo–cultured cell models of pluripotency when appropriate. We emphasize the importance of a detailed molecular understanding of both the mechanisms that regulate genomic output and the functional assays that assess the biological relevance of such molecular characterizations.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1146/annurev-genet-112618-043733

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Genes controlling embryonic development are often reused for adult tissue repair.

    “Genes controlling embryonic development are often reused for adult tissue repair, 16,24”

    From Kupffer-cell-derived IL-6 is repurposed for hepatocyte dedifferentiation via activating progenitor genes from injury-specific enhancers (2023) · cites this paper as [24]

    The review’s “Pioneers of Regeneration” section gives a relevant example: ascl1a is required for retinal regeneration in zebrafish, while its mammalian homolog Ascl1 has a developmental role. It does not establish the broader claim that genes controlling embryonic development are often reused for adult tissue repair; it also notes that Ascl1 is not upregulated after retinal damage in mice. No page number is available in our copy. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 120

  1. [1]Adler CE, Sánchez Alvarado A. 2017. PHRED-1 is a divergent neurexin-1 homolog that organizes muscle fibers and patterns organs during regeneration. Dev. Biol 427: 165– 75 28461239 PMC5497596
  2. [2]Adler CE, Seidel CW, McKinney SA, Sánchez Alvarado A. 2014. Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. eLife 3: e02238 24737865 PMC3985184
  3. [3]Alibardi L 2010. Morphological and cellular aspects of tail and limb regeneration in lizards. A model system with implications for tissue regeneration in mammals. Adv. Anat. Embryol. Cell Biol 207: 1– 109 20334040
  4. [4]Allis CD, Caparros M-L, Jenuwein T, Reinberg D. 2015. Epigenetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 2nd ed.
  5. [5]Ardehali MB, Mei A, Zobeck KL, Caron M, Lis JT, Kusch T. 2011. Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. EMBO J. 30: 2817– 28 21694722 PMC3160253
  6. [7]Azimzadeh J, Wong ML, Downhour DM, Sánchez Alvarado A, Marshall WF. 2012. Centrosome loss in the evolution of planarians. Science 335: 461– 63 22223737 PMC3347778
  7. [8]Azuara V, Perry P, Sauer S, Spivakov M, Jørgensen HF, 2006. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol 8: 532– 38 16570078
  8. [9]Baguñà J 2012. The planarian neoblast: the rambling history of its origin and some current black boxes. Int. J. Dev. Biol 56: 19– 37 22252540
  9. [10]Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823– 37 17512414
  10. [13]Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. PNAS 99: 8695– 700 12060701 PMC124361
  11. [14]Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315– 26 16630819
  12. [16]Birnbaum KD, Sánchez Alvarado A. 2008. Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697– 710 18295584 PMC2692308
  13. [18]Bosch TCG. 2009. Hydra and the evolution of stem cells. Bioessays 31: 478– 86 19274660
  14. [20]Bresnick EH, Katsumura KR, Lee HY, Johnson KD, Perkins AS. 2012. Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies. Nucleic Acids Res. 40: 5819– 31 22492510 PMC3401466
  15. [21]Brockes JP, Kumar A. 2008. Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol 24: 525– 49 18598212
  16. [22]Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML, 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523: 486– 90 26083756 PMC4685948
  17. [23]Buganim Y, Markoulaki S, van Wietmarschen N, Hoke H, Wu T, 2014. The developmental potential of iPSCs is greatly influenced by reprogramming factor selection. Cell Stem Cell 15: 295– 309 25192464 PMC4170792
  18. [24]Castro DS, Martynoga B, Parras C, Ramesh V, Pacary E, 2011. A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev. 25: 930– 45 21536733 PMC3084027
  19. [25]Chen CH, Poss KD. 2017. Regeneration genetics. Annu. Rev. Genet 51: 63– 82 28853919 PMC5705327
  20. [27]Choi J, Huebner AJ, Clement K, Walsh RM, Savol A, 2017. Prolonged Mek1/2 suppression impairs the developmental potential of embryonic stem cells. Nature 548: 219– 23 28746311 PMC5905676
  21. [28]Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu. Rev. Biochem 78: 273– 304 19355820
  22. [29]Dattani A, Kao D, Mihaylova Y, Abnave P, Hughes S, 2018. Epigenetic analyses of planarian stem cells demonstrate conservation of bivalent histone modifications in animal stem cells. Genome Res. 28: 1543– 54 30143598 PMC6169894
  23. [30]Davies EL, Lei K, Seidel CW, Kroesen AE, McKinney SA, 2017. Embryonic origin of adult stem cells required for tissue homeostasis and regeneration. eLife 6: e21052 28072387 PMC5293490
  24. [31]Davis RL, Weintraub H, Lassar AB. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987– 1000 3690668
  25. [32]Denissov S, Hofemeister H, Marks H, Kranz A, Ciotta G, 2014. Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development 141: 526– 37 24423662
  26. [33]Dolan CP, Dawson LA, Muneoka K. 2018. Digit tip regeneration: merging regeneration biology with regenerative medicine. Stem Cells Transl. Med 7: 262– 70 29405625 PMC5827737
  27. [35]Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, 2006. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol 13: 713– 19 16878130
  28. [36]Duncan EM, Chitsazan AD, Seidel CW, Sánchez Alvarado A. 2015. Set1 and MLL1/2 target distinct sets of functionally different genomic loci in vivo. Cell Rep. 13: 2741– 55 26711341 PMC4707048
  29. [37]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– 39 18786419 PMC2614339
  30. [38]Elliott SA, Sánchez Alvarado A. 2013. The history and enduring contributions of planarians to the study of animal regeneration. Wiley Interdiscip. Rev. Dev. Biol 2: 301– 26 23799578 PMC3694279
  31. [39]Fausett BV, Goldman D. 2006. A role for α1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. J. Neurosci 26: 6303– 13 16763038 PMC6675181
  32. [40]Fausett BV, Gumerson JD, Goldman D. 2008. The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J. Neurosci 28: 1109– 17 18234889 PMC2800945
  33. [41]Fei JF, Schuez M, Tazaki A, Taniguchi Y, Roensch K, Tanaka EM. 2014. CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem. Cell Rep 3: 444– 59 PMC4266004 25241743
  34. [42]Fimbel SM, Montgomery JE, Burket CT, Hyde DR. 2007. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J. Neurosci 27: 1712– 24 17301179 PMC6673754
  35. [44]Fujisawa T 2003. Hydra regeneration and epitheliopeptides. Dev. Dyn 226: 182– 89 12557197
  36. [45]Gawriluk TR, Simkin J, Thompson KL, Biswas SK, Clare-Salzler Z, 2016. Comparative analysis of ear-hole closure identifies epimorphic regeneration as a discrete trait in mammals. Nat. Commun 7: 11164 27109826 PMC4848467
  37. [46]Gemberling M, Bailey TJ, Hyde DR, Poss KD. 2013. The zebrafish as a model for complex tissue regeneration. Trends Genet. 29: 611– 20 23927865 PMC3812420
  38. [47]Goldman D 2014. Müller glial cell reprogramming and retina regeneration. Nat. Rev. Neurosci 15: 431– 42 24894585 PMC4249724
  39. [48]Goss RJ, Powel RS. 1985. Induction of deer antlers by transplanted periosteum. I. Graft size and shape. J. Exp. Zool 235: 359– 73 4056697
  40. [49]Guo T, Peters AHFM, Newmark PA. 2006. A bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11: 159– 69 16890156
  41. [50]Hemmrich G, Khalturin K, Boehm AM, Puchert M, Anton-Erxleben F, 2012. Molecular signatures of the three stem cell lineages in Hydra and the emergence of stem cell function at the base of multicellularity. Mol. Biol. Evol 29: 3267– 80 22595987
  42. [52]Howe FS, Fischl H, Murray SC, Mellor J. 2017. Is H3K4me3 instructive for transcription activation? Bioessays 39: 1– 12 28004446
  43. [53]Hubert A, Henderson JM, Ross KG, Cowles MW, Torres J, Zayas RM. 2013. Epigenetic regulation of planarian stem cells by the SET1/MLL family of histone methyltransferases. Epigenetics 8: 79– 91 23235145 PMC3549883
  44. [54]Jorstad NL, Wilken MS, Grimes WN, Wohl SG, VandenBosch LS, 2017. Stimulation of functional neuronal regeneration from Müller glia in adult mice. Nature 548: 103– 7 28746305 PMC5991837
  45. [55]Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA. 2008. Stimulation of neural regeneration in the mouse retina. PNAS 105: 19508– 13 19033471 PMC2614791
  46. [56]Kim K, Doi A, Wen B, Ng K, Zhao R, 2010. Epigenetic memory in induced pluripotent stem cells. Nature 467: 285– 90 20644535 PMC3150836
  47. [57]Kirmizis A, Bartley SM, Kuzmichev A, Margueron R, Reinberg D, 2004. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev. 18: 1592– 605 15231737 PMC443521
  48. [58]Knaupp AS, Buckberry S, Pflueger J, Lim SM, Ford E, 2017. Transient and permanent reconfiguration of chromatin and transcription factor occupancy drive reprogramming. Cell Stem Cell 21: 834– 45.e6 29220667
  49. [59]Knopf F, Hammond C, Chekuru A, Kurth T, Hans S, 2011. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev. Cell 20: 713– 24 21571227
  50. [60]Kragl M, Knapp D, Nacu E, Khattak S, Maden M, 2009. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460: 60– 65 19571878
  51. [61]Kurdistani SK, Tavazoie S, Grunstein M. 2004. Mapping global histone acetylation patterns to gene expression. Cell 117: 721– 33 15186774
  52. [62]Lee DY, Hayes JJ, Pruss D, Wolffe AP. 1993. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72: 73– 84 8422685
  53. [63]Lenhoff SG, Lenhoff HM, Trembley A. 1986. Hydra and the Birth of Experimental Biology—1744. Abraham Trembley’s Mémoires Concerning the Polyps. Pacific Grove, CA: Boxwood Press
  54. [64]Lim DA, Huang Y-C, Swigut T, Mirick AL, Garcia-Verdugo JM, 2009. Chromatin remodeling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458: 529– 33 19212323 PMC3800116
  55. [65]Lin R, Leone JW, Cook RG, Allis CD. 1989. Antibodies specific to acetylated histones document the existence of deposition- and transcription-related histone acetylation in Tetrahymena. J. Cell Biol 108: 1577– 88 2654136 PMC2115542
  56. [67]Marks H, Kalkan T, Menafra R, Denissov S, Jones K, 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149: 590– 604 22541430 PMC3398752
  57. [68]Martello G, Smith A. 2014. The nature of embryonic stem cells. Annu. Rev. Cell Dev. Biol 30: 647– 75 25288119
  58. [69]Martínez DE. 1998. Mortality patterns suggest lack of senescence in Hydra. Exp. Gerontol 33: 217– 25 9615920
  59. [70]McCusker CD, Athippozhy A, Diaz-Castillo C, Fowlkes C, Gardiner DM, Voss SR. 2015. Positional plasticity in regenerating Ambystoma mexicanum limbs is associated with cell proliferation and pathways of cellular differentiation. BMC Dev. Biol 15: 45 26597593 PMC4657325
  60. [71]Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10: 1107– 17 12453418
  61. [72]Morris AC, Scholz TL, Brockerhoff SE, Fadool JM. 2008. Genetic dissection reveals two separate pathways for rod and cone regeneration in the teleost retina. Dev. Neurobiol 68: 605– 19 18265406 PMC2801137
  62. [73]Morrison SJ, Uchida N, Weissman IL. 1995. The biology of hematopoietic stem cells. Annu. Rev. Cell Dev. Biol 11: 35– 71 8689561
  63. [74]Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197– 208 12408864
  64. [75]Murawala P, Tanaka EM, Currie JD. 2012. Regeneration: the ultimate example of wound healing. Semin. Cell Dev. Biol 23: 954– 62 23059793
  65. [76]Nacu E, Tanaka EM. 2011. Limb regeneration: a new development? Annu.Rev.Cell Dev.Biol 27: 409– 40 21801016
  66. [77]Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, 2008. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol 26: 101– 6 18059259
  67. [78]Newmark PA, Reddien PW, Cebrià F, Sánchez Alvarado A. 2003. Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. PNAS 100(Suppl. 1): 11861– 65 12917490 PMC304099
  68. [79]Newmark PA, Sánchez Alvarado A. 2000. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol 220: 142– 53 10753506
  69. [80]Newmark PA, Sánchez Alvarado A. 2002. Not your father’s planarian: a classic model enters the era of functional genomics. Nat. Rev. Genet 3: 210– 19 11972158
  70. [82]Papayannopoulou T, Scadden DT. 2008. Stem-cell ecology and stem cells in motion. Blood 111: 3923– 30 18398055 PMC2288715
  71. [83]Pearson BJ, Sánchez Alvarado A. 2010. A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development 137: 213– 21 20040488 PMC2799157
  72. [84]Plass M, Solana J, Wolf FA, Ayoub S, Misios A, 2018. Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360: eaaq1723 29674432
  73. [85]Pogo BG, Pogo AO, Allfrey VG, Mirsky AE. 1968. Changing patterns of histone acetylation and RNA synthesis in regeneration of the liver. PNAS 59: 1337– 44 5240033 PMC224872
  74. [86]Pollak J, Wilken MS, Ueki Y, Cox KE, Sullivan JM, 2013. ASCL1 reprograms mouse Müller glia into neurogenic retinal progenitors. Development 140: 2619– 31 23637330 PMC3666387
  75. [87]Ramalho-Santos M, Willenbring H. 2007. On the origin of the term “stem cell.” Cell Stem Cell 1: 35– 38 18371332
  76. [88]Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. 2006. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev. Biol 6: 36 16872490 PMC1564002
  77. [89]Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sánchez Alvarado A. 2005. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 8: 635– 49 15866156 PMC2267917
  78. [90]Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sánchez Alvarado A. 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327– 30 16311336
  79. [91]Rickels R, Herz HM, Sze CC, Cao K, Morgan MA, 2017. Histone H3K4 monomethylation catalyzed by Trr and mammalian COMPASS-like proteins at enhancers is dispensable for development and viability. Nat. Genet 49: 1647– 53 28967912 PMC5663216
  80. [92]Rossant J 2018. Genetic control of early cell lineages in the mammalian embryo. Annu. Rev. Genet 52: 185– 201 30183407
  81. [94]Sánchez Alvarado A, Yamanaka S. 2014. Rethinking differentiation: stem cells, regeneration, and plasticity. Cell 157: 110– 19 24679530 PMC4074550
  82. [95]Schlesinger S, Meshorer E. 2019. Open chromatin, epigenetic plasticity, and nuclear organization in pluripotency. Dev. Cell 48: 135– 50 30695696
  83. [96]Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol 6: 73– 77 14661024
  84. [97]Seifert AW, Kiama SG, Seifert MG, Goheen JR, Palmer TM, Maden M. 2012. Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489: 561– 65 23018966 PMC3480082
  85. [98]Seifert AW, Muneoka K. 2018. The blastema and epimorphic regeneration in mammals. Dev. Biol 433: 190– 99 29291973 PMC5753424
  86. [99]Shi X, Hong T, Walter KL, Ewalt M, Michishita E, 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96– 99 16728974 PMC3089773
  87. [100]Singh SP, Holdway JE, Poss KD. 2012. Regeneration of amputated zebrafish fin rays from de novo osteoblasts. Dev. Cell 22: 879– 86 22516203 PMC3341140
  88. [101]Smith JJ, Antonacci F, Eichler EE, Amemiya CT. 2009. Programmed loss of millions of base pairs from a vertebrate genome. PNAS 106: 11212– 17 19561299 PMC2708698
  89. [102]Soares LM, He PC, Chun Y, Suh H, Kim T, Buratowski S. 2017. Determinants of histone H3K4 methylation patterns. Mol. Cell 68: 773– 85.e6 29129639 PMC5706784
  90. [103]Soldner F, Jaenisch R. 2018. Stem cells, genome editing, and the path to translational medicine. Cell 175: 615– 32 30340033 PMC6461399
  91. [105]Stewart S, Stankunas K. 2012. Limited dedifferentiation provides replacement tissue during zebrafish fin regeneration. Dev. Biol 365: 339– 49 22426105 PMC3370987
  92. [106]Stewart S, Tsun Z-Y, Izpisua Belmonte JC. 2009. A histone demethylase is necessary for regeneration in zebrafish. PNAS 106: 19889– 94 19897725 PMC2785262
  93. [107]Strahl BD, Ohba R, Cook RG, Allis CD. 1999. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. PNAS 96: 14967– 72 10611321 PMC24756
  94. [108]Sugiyama T, Wanek N. 1993. Genetic analysis of developmental mechanisms in Hydra: XXI. Enhancement of regeneration in a regeneration-deficient mutant strain by the elimination of the interstitial cell lineage. Dev. Biol 160: 64– 72 8224549
  95. [109]Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663– 76 16904174
  96. [110]Underwood JM, Becker KA, Stein GS, Nickerson JA. 2017. The ultrastructural signature of human embryonic stem cells. J. Cell Biochem 118: 764– 74 27632380 PMC5558502
  97. [111]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– 39 25017721 PMC4171737
  98. [112]Wagner DE, Ho JJ, Reddien PW. 2012. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 10: 299– 311 22385657 PMC3338251
  99. [113]Wagner DE, Wang IE, Reddien PW. 2011. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332: 811– 16 21566185 PMC3338249
  100. [114]Walter M, Teissandier A, Pérez-Palacios R, Bourc’his D. 2016. An epigenetic switch ensures transposon repression upon dynamic loss of DNA methylation in embryonic stem cells. eLife 5: e11418 26814573 PMC4769179
  101. [115]Wan J, Goldman D. 2016. Retina regeneration in zebrafish. Curr. Opin. Genet. Dev 40: 41– 47 27281280 PMC5135611
  102. [116]Watanabe H, Hoang VT, Mattner R, Holstein TW. 2009. Immortality and the base of multicellular life: lessons from cnidarian stem cells. Semin. Cell Dev. Biol 20: 1114– 25 19761866
  103. [117]Weintraub H, Dwarki VJ, Verma I, Davis R, Hollenberg S, 1991. Muscle-specific transcriptional activation by MyoD. Genes Dev. 5: 1377– 86 1651276
  104. [118]Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, 1989. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. PNAS 86: 5434– 38 2748593 PMC297637
  105. [120]Wen D, Saiz N, Rosenwaks Z, Hadjantonakis AK, Rafii S. 2014. Completely ES cell-derived mice produced by tetraploid complementation using inner cell mass (ICM) deficient blastocysts. PLOS ONE 9: e94730 24733255 PMC3986396
  106. [121]Wenemoser D, Reddien PW. 2010. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol 344: 979– 91 20599901 PMC2950745
  107. [122]Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, 2007. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318– 24 17554336
  108. [123]Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F, Bosch TCG. 2006. Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. PNAS 103: 6208– 11 16556723 PMC1458856
  109. [124]Wu T, Liu Y, Wen D, Tseng Z, Tahmasian M, 2014. Histone variant H2A.X deposition pattern serves as a functional epigenetic mark for distinguishing the developmental potentials of iPSCs. Cell Stem Cell 15: 281– 94 25192463
  110. [125]Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121: 859– 72 15960974
  111. [126]Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, 2006. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86– 90 16728976
  112. [127]Xu CR, Cole PA, Meyers DJ, Kormish J, Dent S, Zaret KS. 2011. Chromatin “prepattern” and histone modifiers in a fate choice for liver and pancreas. Science 332: 963– 66 21596989 PMC3128430
  113. [128]Xue Z, Huang K, Cai C, Cai L, Jiang CY, 2013. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500: 593– 97 23892778 PMC4950944
  114. [129]Yagi M, Kishigami S, Tanaka A, Semi K, Mizutani E, 2017. Derivation of ground-state female ES cells maintaining gamete-derived DNA methylation. Nature 548: 224– 27 28746308
  115. [130]Yokoyama RW, Yao MC. 1982. Elimination of DNA sequences during macronuclear differentiation in Tetrahymena thermophila, as detected by in situ hybridization. Chromosoma 85: 11– 22 6284452
  116. [131]Yoshida-Kashikawa M, Shibata N, Takechi K, Agata K. 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– 50 17994545
  117. [132]Yu BD, Hanson RD, Hess JL, Horning SE, Korsmeyer SJ. 1998. MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. PNAS 95: 10632– 36 9724755 PMC27946
  118. [133]Yun MH, Gates PB, Brockes JP. 2013. Regulation of p53 is critical for vertebrate limb regeneration. PNAS 110: 17392– 97 24101460 PMC3808590
  119. [134]Zaret KS, Mango SE. 2016. Pioneer transcription factors, chromatin dynamics, and cell fate control. Curr. Opin. Genet. Dev 37: 76– 81 26826681 PMC4914445
  120. [135]Zeng A, Li H, Guo L, Gao X, McKinney S, 2018. Prospectively isolated tetraspanin+ neoblasts are adult pluripotent stem cells underlying planaria regeneration. Cell 173: 1593– 608.e20 29906446 PMC9359418

Cited by

Sorted by citations

Authors
Duncan, E. M., & Sánchez Alvarado, A.
Affiliations
  • University of Kentucky (US)
  • Howard Hughes Medical Institute, Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA;
Venue
Annual Review of Genetics
Published
2019-12-03
Volume
53
Issue
1
Pages
327-346
ISSN
  • 0066-4197 (ISSN-L)
  • 1545-2948
OpenAlex
W2972854533
Cited by
17
References
7
Citations by year
2025: 2 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 3
FWCI
0.26
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Genetics (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of General Medical Sciences (R37GM057260)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Keywords
regeneration, genome regulation, cellular potency, pluripotency, tissue regeneration, Hydra, molecular mechanisms of regeneration
MeSH terms
Animals, Chromatin, Histones, Humans, Hydra, Regeneration, Stem Cells, Genome, Feedback, Physiological, Pluripotent Stem Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review