1932

Abstract

The majority of animal phyla have species that can regenerate. Comparing regeneration across animals can reconstruct the molecular and cellular evolutionary history of this process. Recent studies have revealed some similarity in regeneration mechanisms, but rigorous comparative methods are needed to assess whether these resemblances are ancestral pathways (homology) or are the result of convergent evolution (homoplasy). This review aims to provide a framework for comparing regeneration across animals, focusing on gene regulatory networks (GRNs), which are substrates for assessing process homology. The homology of the wound-induced activation of Wnt signaling and of adult stem cells provides examples of ongoing studies of regeneration that enable comparisons in a GRN framework. Expanding the study of regeneration GRNs in currently studied species and broadening taxonomic sampling for these approaches will identify processes that are unifying principles of regeneration biology across animals. These insights are important both for evolutionary studies of regeneration and for human regenerative medicine.

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2021-10-06
2024-04-27
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Literature Cited

  1. Abouheif E. 1997. Developmental genetics and homology: a hierarchical approach. Trends Ecol. Evol. 12:405–8
    [Google Scholar]
  2. Abouheif E 1999. Establishing homology criteria for regulatory gene networks: prospects and challenges. Novartis Foundation Symposium 222 - Homology GK Bock, G Cardew 207–25 Chichester, UK: John Wiley & Sons
  3. Adler CE, Seidel CW, McKinney SA, Sanchez Alvarado A 2014. Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. eLife 3:e02238
    [Google Scholar]
  4. Alie A, Hayashi T, Sugimura I, Manuel M, Sugano W et al. 2015. The ancestral gene repertoire of animal stem cells. PNAS 112:E7093–100
    [Google Scholar]
  5. Alie A, Leclere L, Jager M, Dayraud C, Chang P et al. 2011. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev. Biol. 350:183–97
    [Google Scholar]
  6. Almuedo-Castillo M, Crespo-Yanez X, Seebeck F, Bartscherer K, Salo E, Adell T 2014. JNK controls the onset of mitosis in planarian stem cells and triggers apoptotic cell death required for regeneration and remodeling. PLOS Genet 10:e1004400
    [Google Scholar]
  7. Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C et al. 2016. The origin and evolution of cell types. Nat. Rev. Genet. 17:744–57This article provides examples of how cell-type identity networks inform the evolution of cell types.
    [Google Scholar]
  8. Arnone MI, Davidson EH. 1997. The hardwiring of development: organization and function of genomic regulatory systems. Development 124:1851–64
    [Google Scholar]
  9. Arvizu F, Aguilera A, Salgado LM. 2006. Activities of the protein kinases STK, PI3K, MEK, and ERK are required for the development of the head organizer in Hydra magnipapillata. Differentiation 74:305–12
    [Google Scholar]
  10. Avaron F, Smith A, Akimenko MA 2006. Sonic hedgehog signalling in the developing and regenerating fins of zebrafish. Shh and Gli Signalling and Development CE Fisher, SEM Howie 93–106 New York: Springer
    [Google Scholar]
  11. Bely AE, Nyberg KG. 2010. Evolution of animal regeneration: re-emergence of a field. Trends Ecol. Evol. 25:161–70
    [Google Scholar]
  12. Benson KR 1991. Observation versus philosophical commitment in eighteenth-century ideas of regeneration and generation. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 91–100 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  13. Boehm AM, Khalturin K, Anton-Erxleben F, Hemmrich G, Klostermeier UC et al. 2012. FoxO is a critical regulator of stem cell maintenance in immortal Hydra. PNAS 109:19697–702
    [Google Scholar]
  14. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947–56
    [Google Scholar]
  15. Brockes JP, Kumar A. 2008. Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol. 24:525–49
    [Google Scholar]
  16. Broun M, Gee L, Reinhardt B, Bode HR. 2005. Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907–16
    [Google Scholar]
  17. Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML et al. 2015. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523:486–90
    [Google Scholar]
  18. Cannon JT, Vellutini BC, Smith J, Ronquist F, Jondelius U, Hejnol A. 2016. Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93
    [Google Scholar]
  19. Cao J, Poss KD. 2018. The epicardium as a hub for heart regeneration. Nat. Rev. Cardiol. 15:631–47
    [Google Scholar]
  20. Carnevali MDC, Burighel P. 2010. Regeneration in echinoderms and ascidians. Encyclopedia of Life Sciences Chichester, UK: John Wiley & Sons
    [Google Scholar]
  21. Cary GA, McCauley BS, Zueva O, Pattinato J, Longabaugh W, Hinman VF. 2020. Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development. Nat. Commun. 11:6235
    [Google Scholar]
  22. Cary GA, Wolff A, Zueva O, Pattinato J, Hinman VF. 2019. Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa. BMC Biol 17:16
    [Google Scholar]
  23. Cazet J, Juliano CE. 2020. Oral regeneration is the default pathway triggered by injury in Hydra. BioRxiv 189811. https://doi.org/10.1101/2020.07.06.189811
    [Crossref]
  24. Chen C-Y, Yueh W-T, J-H C 2020. Canonical Wnt signaling is involved in anterior regeneration of the annelid Aeolosoma viride. BioRxiv 972448. https://doi.org/10.1101/2020.03.01.972448
    [Crossref]
  25. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C et al. 2009. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive Hydra head regeneration. Dev. Cell 17:279–89
    [Google Scholar]
  26. Chera S, Ghila L, Wenger Y, Galliot B. 2011. Injury-induced activation of the MAPK/CREB pathway triggers apoptosis-induced compensatory proliferation in hydra head regeneration. Dev. Growth Differ. 53:186–201
    [Google Scholar]
  27. Church SH, Extavour CG. 2020. Null hypotheses for developmental evolution. Development 147:dev178004
    [Google Scholar]
  28. Daley GQ. 2015. Stem cells and the evolving notion of cellular identity. Philos. Trans. R. Soc. B 370:20140376
    [Google Scholar]
  29. Davidson EH, Erwin DH. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311:796–800
    [Google Scholar]
  30. De Mulder K, Kuales G, Pfister D, Willems M, Egger B et al. 2009a. Characterization of the stem cell system of the acoel Isodiametra pulchra. BMC Dev. Biol. 9:69
    [Google Scholar]
  31. De Mulder K, Pfister D, Kuales G, Egger B, Salvenmoser W et al. 2009b. Stem cells are differentially regulated during development, regeneration and homeostasis in flatworms. Dev. Biol. 334:198–212
    [Google Scholar]
  32. Denker E, Manuel M, Leclere L, Le Guyader H, Rabet N 2008. Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev. Biol. 315:99–113
    [Google Scholar]
  33. Dinsmore CE 1991. Lazzaro Spallanzani: concepts of generation and regeneration. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 67–90 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  34. DuBuc TQ, Schnitzler CE, Chrysostomou E, McMahon ET, Febrimarsa, et al. 2020. Transcription factor AP2 controls cnidarian germ cell induction. Science 367:757–62
    [Google Scholar]
  35. DuBuc TQ, Traylor-Knowles N, Martindale MQ. 2014. Initiating a regenerative response; cellular and molecular features of wound healing in the cnidarian Nematostella vectensis. BMC Biol 12:24
    [Google Scholar]
  36. Erkenbrack EM, Davidson EH, Peter IS. 2018. Conserved regulatory state expression controlled by divergent developmental gene regulatory networks in echinoids. Development 145:dev167288
    [Google Scholar]
  37. Erwin DH, Davidson EH. 2009. The evolution of hierarchical gene regulatory networks. Nat. Rev. Genet. 10:141–48
    [Google Scholar]
  38. Fabila Y, Navarro L, Fujisawa T, Bode HR, Salgado LM. 2002. Selective inhibition of protein kinases blocks the formation of a new axis, the beginning of budding. Hydra. Mech. Dev 119:157–64
    [Google Scholar]
  39. Fagnocchi L, Zippo A. 2017. Multiple roles of MYC in integrating regulatory networks of pluripotent stem cells. Front. Cell Dev. Biol. 5:7
    [Google Scholar]
  40. Farkas JE, Freitas PD, Bryant DM, Whited JL, Monaghan JR. 2016. Neuregulin-1 signaling is essential for nerve-dependent axolotl limb regeneration. Development 143:2724–31
    [Google Scholar]
  41. Fei J-F, Schuez M, Knapp D, Taniguchi Y, Drechsel DN, Tanaka EM 2017. Efficient gene knockin in axolotl and its use to test the role of satellite cells in limb regeneration. PNAS 114:12501–6
    [Google Scholar]
  42. Fincher CT, Wurtzel O, de Hoog T, Kravarik KM, Reddien PW. 2018. Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360:eaaq1736
    [Google Scholar]
  43. Fowler T, Sen R, Roy AL. 2011. Regulation of primary response genes. Mol. Cell 44:348–60
    [Google Scholar]
  44. Fraguas S, Barberan S, Iglesias M, Rodriguez-Esteban G, Cebria F. 2014. egr-4, a target of EGFR signaling, is required for the formation of the brain primordia and head regeneration in planarians. Development 141:1835–47
    [Google Scholar]
  45. Funayama N. 2010. The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev. Growth Differ. 52:1–14
    [Google Scholar]
  46. Funayama N. 2018. The cellular and molecular bases of the sponge stem cell systems underlying reproduction, homeostasis and regeneration. Int. J. Dev. Biol. 62:513–25
    [Google Scholar]
  47. Funayama N, Nakatsukasa M, Mohri K, Masuda Y, Agata K 2010. Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol. Dev. 12:275–87
    [Google Scholar]
  48. Gahan JM, Bradshaw B, Flici H, Frank U. 2016. The interstitial stem cells in Hydractinia and their role in regeneration. Curr. Opin. Genet. Dev. 40:65–73
    [Google Scholar]
  49. Gavino MA, Wenemoser D, Wang IE, Reddien PW. 2013. Tissue absence initiates regeneration through follistatin-mediated inhibition of activin signaling. eLife 2:e00247
    [Google Scholar]
  50. Gehrke AR, Neverett E, Luo Y-J, Brandt A, Ricci L et al. 2019. Acoel genome reveals the regulatory landscape of whole-body regeneration. Science 363:eaau6173
    [Google Scholar]
  51. Gehrke AR, Srivastava M. 2016. Neoblasts and the evolution of whole-body regeneration. Curr. Opin. Genet. Dev. 40:131–37
    [Google Scholar]
  52. Gemberling M, Karra R, Dickson AL, Poss KD 2015. Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. eLife 4:e05871
    [Google Scholar]
  53. Gilbert SF, Bolker JA. 2001. Homologies of process and modular elements of embryonic construction. J. Exp. Zool. 291:1–12
    [Google Scholar]
  54. Gilbert SF, Opitz JM, Raff RA. 1996. Resynthesizing evolutionary and developmental biology. Dev. Biol. 173:357–72
    [Google Scholar]
  55. Goldman JA, Poss KD. 2020. Gene regulatory programmes of tissue regeneration. Nat. Rev. Genet. 21:511–25
    [Google Scholar]
  56. Goss RJ 1991. The natural history (and mystery) of regeneration. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 7–24 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  57. Grose R, Harris BS, Cooper L, Topilko P, Martin P. 2002. Immediate early genes krox-24 and krox-20 are rapidly up-regulated after wounding in the embryonic and adult mouse. Dev. Dyn. 223:371–78
    [Google Scholar]
  58. Gurley KA, Elliott SA, Simakov O, Schmidt HA, Holstein TW, Sanchez Alvarado A 2010. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev. Biol. 347:24–39
    [Google Scholar]
  59. Gurley KA, Rink JC, Sanchez Alvarado A 2008. Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319:323–27
    [Google Scholar]
  60. Halfon MS. 2017. Perspectives on gene regulatory network evolution. Trends Genet 33:436–47
    [Google Scholar]
  61. Han M, Yang X, Farrington JE, Muneoka K. 2003. Digit regeneration is regulated by Msx1 and BMP4 in fetal mice. Development 130:5123–32
    [Google Scholar]
  62. Harris RE, Setiawan L, Saul J, Hariharan IK 2016. Localized epigenetic silencing of a damage-activated WNT enhancer limits regeneration in mature Drosophila imaginal discs. eLife 5:e11588
    [Google Scholar]
  63. Hemmrich G, Khalturin K, Boehm AM, Puchert M, Anton-Erxleben F et al. 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
    [Google Scholar]
  64. Hinman VF, Davidson EH 2007. Evolutionary plasticity of developmental gene regulatory network architecture. PNAS 104:19404–9
    [Google Scholar]
  65. Hinman VF, Nguyen AT, Cameron RA, Davidson EH 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. PNAS 100:13356–61
    [Google Scholar]
  66. Hobmayer B, Rentzsch F, Kuhn K, Happel CM, Cramer von Laue C et al. 2000. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186–89
    [Google Scholar]
  67. Imokawa Y, Yoshizato K 1997. Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. PNAS 94:9159–64
    [Google Scholar]
  68. Jeffery WR. 2015. Distal regeneration involves the age dependent activity of branchial sac stem cells in the ascidian Ciona intestinalis. Regeneration 2:1–18
    [Google Scholar]
  69. Juliano CE, Reich A, Liu N, Götzfried J, Zhong M et al. 2014. PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells. PNAS 111:337–42
    [Google Scholar]
  70. Juliano CE, Swartz SZ, Wessel GM. 2010. A conserved germline multipotency program. Development 137:4113–26
    [Google Scholar]
  71. Kaloulis K, Chera S, Hassel M, Gauchat D, Galliot B 2004. Reactivation of developmental programs: the cAMP-response element-binding protein pathway is involved in hydra head regeneration. PNAS 101:2363–68
    [Google Scholar]
  72. Kang J, Hu J, Karra R, Dickson AL, Tornini VA et al. 2016. Modulation of tissue repair by regeneration enhancer elements. Nature 532:201–6
    [Google Scholar]
  73. Kapli P, Telford MJ. 2020. Topology-dependent asymmetry in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Sci. Adv. 6:eabc5162
    [Google Scholar]
  74. Kassmer SH, Langenbacher AD, De Tomaso AW. 2020. Integrin-alpha-6+ Candidate stem cells are responsible for whole body regeneration in the invertebrate chordate Botrylloides diegensis. Nat. Commun. 11:4435
    [Google Scholar]
  75. Kassmer SH, Nourizadeh S, De Tomaso AW. 2019. Cellular and molecular mechanisms of regeneration in colonial and solitary Ascidians. Dev. Biol. 448:271–78
    [Google Scholar]
  76. Kawakami Y, Rodriguez Esteban C, Raya M, Kawakami H, Martí M et al. 2006. Wnt/β-catenin signaling regulates vertebrate limb regeneration. Genes Dev 20:3232–37
    [Google Scholar]
  77. Khan SJ, Schuster KJ, Smith-Bolton RK. 2016. Regeneration in crustaceans and insects. Encyclopedia of Life Sciences Chichester, UK: John Wiley & Sons
    [Google Scholar]
  78. Konstantinides N, Averof M. 2014. A common cellular basis for muscle regeneration in arthropods and vertebrates. Science 343:788–91
    [Google Scholar]
  79. Koonin EV. 2005. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39:309–38
    [Google Scholar]
  80. Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ et al. 2012. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 30:1734–45
    [Google Scholar]
  81. Lai AG, Aboobaker AA. 2018. EvoRegen in animals: time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes. Dev. Biol. 433:118–31This article provides a comprehensive review of Piwi+ cells and their potency across animals.
    [Google Scholar]
  82. Lehoczky JA, Tabin CJ. 2015. Lgr6 marks nail stem cells and is required for digit tip regeneration. PNAS 112:13249–54
    [Google Scholar]
  83. Lei K, Thi-Kim Vu H, Mohan RD, McKinney SA, Seidel CW et al. 2016. Egf signaling directs neoblast repopulation by regulating asymmetric cell division in planarians. Dev. Cell 38:413–29
    [Google Scholar]
  84. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L et al. 2009. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev. Biol. 330:186–99
    [Google Scholar]
  85. Lenhoff HM, Lenhoff SG 1991. Abraham Trembley and the origin of research on regeneration in animals. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 47–66 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  86. Levine M, Davidson EH 2005. Gene regulatory networks for development. PNAS 102:4936–42
    [Google Scholar]
  87. Lin G, Slack JM. 2008. Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Dev. Biol. 316:323–35
    [Google Scholar]
  88. Liu P, Zhong TP. 2017. MAPK/ERK signalling is required for zebrafish cardiac regeneration. Biotechnol. Lett. 39:1069–77
    [Google Scholar]
  89. Liu X, Huang J, Chen T, Wang Y, Xin S et al. 2008. Yamanaka factors critically regulate the developmental signaling network in mouse embryonic stem cells. Cell Res 18:1177–89
    [Google Scholar]
  90. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781–810
    [Google Scholar]
  91. Manuel GC, Reynoso R, Gee L, Salgado LM, Bode HR. 2006. PI3K and ERK 1–2 regulate early stages during head regeneration in hydra. Dev. Growth Differ. 48:129–38
    [Google Scholar]
  92. Marletaz F, Peijnenburg K, Goto T, Satoh N, Rokhsar DS. 2019. A new spiralian phylogeny places the enigmatic arrow worms among gnathiferans. Curr. Biol. 29:312–18.e3
    [Google Scholar]
  93. Martin P, Nobes CD. 1992. An early molecular component of the wound healing response in rat embryos—induction of c-fos protein in cells at the epidermal wound margin. Mech. Dev. 38:209–15
    [Google Scholar]
  94. Maruzzo D, Bortolin F 2013. Arthropod regeneration. Arthropod Biology and Evolution A Minelli, G Boxshall, G Fusco 149–69 Berlin: Springer
    [Google Scholar]
  95. Mashanov VS, Zueva OR, Garcia-Arraras JE. 2013. Radial glial cells play a key role in echinoderm neural regeneration. BMC Biol 11:49
    [Google Scholar]
  96. Mashanov VS, Zueva OR, Garcia-Arraras JE. 2015. Heterogeneous generation of new cells in the adult echinoderm nervous system. Front. Neuroanat. 9:123
    [Google Scholar]
  97. McCusker C, Bryant SV, Gardiner DM 2015. The axolotl limb blastema: cellular and molecular mechanisms driving blastema formation and limb regeneration in tetrapods. Regeneration 2:54–71
    [Google Scholar]
  98. Mevel R, Draper JE, Lie-a-Ling M, Kouskoff V, Lacaud G. 2019. RUNX transcription factors: orchestrators of development. Development 146:dev148296
    [Google Scholar]
  99. Miller BM, Johnson K, Whited JL 2019. Common themes in tetrapod appendage regeneration: a cellular perspective. Evodevo 10:11
    [Google Scholar]
  100. Mokalled MH, Poss KD. 2018. A regeneration toolkit. Dev. Cell 47:267–80
    [Google Scholar]
  101. Morgan TH. 1901. Regeneration New York: Macmillan
  102. Morris SA. 2019. The evolving concept of cell identity in the single cell era. Development 146:dev169748
    [Google Scholar]
  103. Muneoka K, Bryant SV. 1982. Evidence that patterning mechanisms in developing and regenerating limbs are the same. Nature 298:369–71
    [Google Scholar]
  104. Muneoka K, Bryant SV. 1984. Cellular contribution to supernumerary limbs in the axolotl, Ambystoma mexicanum. Dev. Biol. 105:166–78
    [Google Scholar]
  105. Nakamura T, Mito T, Tanaka Y, Bando T, Ohuchi H, Noji S. 2007. Involvement of canonical Wnt/Wingless signaling in the determination of the positional values within the leg segment of the cricket Gryllus bimaculatus. Dev. Growth Differ. 49:79–88
    [Google Scholar]
  106. Newmark PA, Sanchez Alvarado A 2000. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 220:142–53
    [Google Scholar]
  107. Nusse R, Varmus HE. 1992. Wnt genes. Cell 69:1073–87
    [Google Scholar]
  108. Oshima Y, Ouchi N, Sato K, Izumiya Y, Pimentel DR, Walsh K. 2008. Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation 117:3099–108
    [Google Scholar]
  109. Owlarn S, Klenner F, Schmidt D, Rabert F, Tomasso A et al. 2017. Generic wound signals initiate regeneration in missing-tissue contexts. Nat. Commun. 8:2282
    [Google Scholar]
  110. Ozpolat BD, Bely AE. 2016. Developmental and molecular biology of annelid regeneration: a comparative review of recent studies. Curr. Opin. Genet. Dev. 40:144–53
    [Google Scholar]
  111. Panchen AL 1999. Homology – history of a concept. Novartis Foundation Symposium 222 - Homology GK Bock, G Cardew 5–23 Chichester, UK: John Wiley & Sons
  112. Peter IS, Davidson EH. 2011. Evolution of gene regulatory networks controlling body plan development. Cell 144:970–85
    [Google Scholar]
  113. Petersen CP, Reddien PW. 2008. Smed-βcatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319:327–30
    [Google Scholar]
  114. Petersen CP, Reddien PW. 2009a. Wnt signaling and the polarity of the primary body axis. Cell 139:1056–68
    [Google Scholar]
  115. Petersen CP, Reddien PW 2009b. A wound-induced Wnt expression program controls planarian regeneration polarity. PNAS 106:17061–66
    [Google Scholar]
  116. Petersen CP, Reddien PW. 2011. Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332:852–55
    [Google Scholar]
  117. Philippe H, Poustka AJ, Chiodin M, Hoff KJ, Dessimoz C et al. 2019. Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Ambulacraria. Curr. Biol. 29:1818–26.e6
    [Google Scholar]
  118. Plass M, Solana J, Wolf FA, Ayoub S, Misios A et al. 2018. Cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360:eaaq1723
    [Google Scholar]
  119. Plickert G, Frank U, Muller WA. 2012. Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency. Int. J. Dev. Biol. 56:519–34
    [Google Scholar]
  120. Raff RA. 1996. The Shape of Life. Chicago: Chicago Univ. Press
  121. Ramirez AN, Loubet-Senear K, Srivastava M. 2020. A regulatory program for initiation of Wnt signaling during posterior regeneration in acoels. Cell Rep 32:108098
    [Google Scholar]
  122. Rebscher N, Volk C, Teo R, Plickert G. 2008. The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev. Dyn. 237:1736–45
    [Google Scholar]
  123. Reddien PW. 2013. Specialized progenitors and regeneration. Development 140:951–57
    [Google Scholar]
  124. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A 2005. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310:1327–30
    [Google Scholar]
  125. Reddien PW, Sanchez Alvarado A 2004. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol. 20:725–57
    [Google Scholar]
  126. Rinkevich Y, Rosner A, Rabinowitz C, Lapidot Z, Moiseeva E, Rinkevich B. 2010. Piwi positive cells that line the vasculature epithelium, underlie whole body regeneration in a basal chordate. Dev. Biol. 345:94–104
    [Google Scholar]
  127. Rinkevich Y, Voskoboynik A, Rosner A, Rabinowitz C, Paz G et al. 2013. Repeated, long-term cycling of putative stem cells between niches in a basal chordate. Dev. Cell 24:76–88
    [Google Scholar]
  128. Roberts-Galbraith RH, Newmark PA 2013. Follistatin antagonizes Activin signaling and acts with Notum to direct planarian head regeneration. PNAS 110:1363–68
    [Google Scholar]
  129. Rojas-Muñoz A, Rajadhyksha S, Gilmour D, van Bebber F, Antos C et al. 2009. ErbB2 and ErbB3 regulate amputation-induced proliferation and migration during vertebrate regeneration. Dev. Biol. 327:177–90
    [Google Scholar]
  130. Rychel AL, Swalla BJ 2009. Regeneration in hemichordates and echinoderms. Stem Cells in Marine Organisms B Rinkevich, V Matranga 245–65 Dordrecht, Neth: Springer
    [Google Scholar]
  131. Sabin KZ, Jiang P, Gearhart MD, Stewart R, Echeverri K. 2019. AP-1cFos/JunB/miR-200a regulate the pro-regenerative glial cell response during axolotl spinal cord regeneration. Commun. Biol. 2:91
    [Google Scholar]
  132. Salih DA, Brunet A. 2008. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol. 20:126–36
    [Google Scholar]
  133. Sanchez Alvarado A 2000. Regeneration in the metazoans: why does it happen?. Bioessays 22:578–90
    [Google Scholar]
  134. Sandoval-Guzman T, Wang H, Khattak S, Schuez M, Roensch K et al. 2014. Fundamental differences in dedifferentiation and stem cell recruitment during skeletal muscle regeneration in two salamander species. Cell Stem Cell 14:174–87
    [Google Scholar]
  135. Schaffer AA, Bazarsky M, Levy K, Chalifa-Caspi V, Gat U. 2016. A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis. BMC Genomics 17:718
    [Google Scholar]
  136. Sheng M, Greenberg ME. 1990. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477–85
    [Google Scholar]
  137. Shubin N, Tabin C, Carroll S 1997. Fossils, genes and the evolution of animal limbs. Nature 388:639–48
    [Google Scholar]
  138. Shubin N, Tabin C, Carroll S 2009. Deep homology and the origins of evolutionary novelty. Nature 457:818–23
    [Google Scholar]
  139. Siebert S, Farrell JA, Cazet JF, Abeykoon Y, Primack AS et al. 2019. Stem cell differentiation trajectories in Hydra resolved at single-cell resolution. Science 365:eaav9314
    [Google Scholar]
  140. Skinner DM, Cook JS 1991. New limbs for old ones: some highlights in the history of regeneration in Crustacea. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 25–46 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  141. Slack JM. 2017. Animal regeneration: ancestral character or evolutionary novelty?. EMBO Rep 18:1497–508
    [Google Scholar]
  142. Smith-Bolton RK, Worley MI, Kanda H, Hariharan IK. 2009. Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev. Cell 16:797–809
    [Google Scholar]
  143. Sogabe S, Hatleberg WL, Kocot KM, Say TE, Stoupin D et al. 2019. Pluripotency and the origin of animal multicellularity. Nature 570:519–22
    [Google Scholar]
  144. Solana J. 2013. Closing the circle of germline and stem cells: the Primordial Stem Cell hypothesis. Evodevo 4:2
    [Google Scholar]
  145. Somorjai IM, Somorjai RL, Garcia-Fernandez J, Escriva H 2012. Vertebrate-like regeneration in the invertebrate chordate amphioxus. PNAS 109:517–22
    [Google Scholar]
  146. Soubigou A, Ross EG, Touhami Y, Chrismas N, Modepalli V. 2020. Regeneration in the sponge Sycon ciliatum partly mimics postlarval development. Development 147:dev193714
    [Google Scholar]
  147. Srivastava M, Mazza-Curll K, van Wolfswinkel J, Reddien PW. 2014. Whole-body acoel regeneration is controlled by Wnt and Bmp-Admp signaling. Curr. Biol. 24:1107–13
    [Google Scholar]
  148. Stewart S, Gomez AW, Armstrong BE, Henner A, Stankunas K. 2014. Sequential and opposing activities of Wnt and BMP coordinate zebrafish bone regeneration. Cell Rep 6:482–98
    [Google Scholar]
  149. Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB et al. 2007. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134:479–89
    [Google Scholar]
  150. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–76
    [Google Scholar]
  151. Takahashi K, Yamanaka S. 2016. A decade of transcription factor-mediated reprogramming to pluripotency. Nat. Rev. Mol. Cell Biol. 17:183–93
    [Google Scholar]
  152. Takeo M, Chou WC, Sun Q, Lee W, Rabbani P et al. 2013. Wnt activation in nail epithelium couples nail growth to digit regeneration. Nature 499:228–32
    [Google Scholar]
  153. Takeo M, Hale CS, Ito M. 2016. Epithelium-derived Wnt ligands are essential for maintenance of underlying digit bone. J. Invest. Dermatol. 136:1355–63
    [Google Scholar]
  154. Tanaka EM, Reddien PW. 2011. The cellular basis for animal regeneration. Dev. Cell 21:172–85
    [Google Scholar]
  155. Tejada-Romero B, Carter JM, Mihaylova Y, Neumann B, Aboobaker AA. 2015. JNK signalling is necessary for a Wnt- and stem cell-dependent regeneration programme. Development 142:2413–24
    [Google Scholar]
  156. Tewari AG, Stern SR, Oderberg IM, Reddien PW. 2018. Cellular and molecular responses unique to major injury are dispensable for planarian regeneration. Cell Rep 25:2577–90.e3
    [Google Scholar]
  157. Tickle C. 1981. Limb regeneration. Am. Sci. 69:639–46
    [Google Scholar]
  158. Tiozzo S, Copley RR. 2015. Reconsidering regeneration in metazoans: an evo-devo approach. Front. Ecol. Evol. 3:67This article presents comparative thinking about regeneration from an evo-devo perspective.
    [Google Scholar]
  159. True JR, Haag ES. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evol. Dev. 3:109–19
    [Google Scholar]
  160. Tsonis PA. 2000. Regeneration in vertebrates. Dev. Biol. 221:273–84
    [Google Scholar]
  161. Tu KC, Cheng L-C, Vu HTK, Lange JJ, McKinney SA et al. 2015. Egr-5 is a post-mitotic regulator of planarian epidermal differentiation. eLife 4:e10501
    [Google Scholar]
  162. Tursch A, Bartsch N, Holstein TW. 2020. MAPK signaling links the injury response to Wnt-regulated patterning in Hydra regeneration. BioRxiv 189795. https://doi.org/10.1101/2020.07.06.189795
    [Crossref]
  163. Umansky KB, Gruenbaum-Cohen Y, Tsoory M, Feldmesser E, Goldenberg D et al. 2015. Runx1 transcription factor is required for myoblasts proliferation during muscle regeneration. PLOS Genet 11:e1005457
    [Google Scholar]
  164. van Wolfswinkel JC. 2014. Piwi and potency: PIWI proteins in animal stem cells and regeneration. Integr. Comp. Biol. 54:700–13
    [Google Scholar]
  165. 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
    [Google Scholar]
  166. Verrier B, Müller D, Bravo R, Müller R. 1986. Wounding a fibroblast monolayer results in the rapid induction of the c-fos proto-oncogene. EMBO J 5:913–17
    [Google Scholar]
  167. Vogg MC, Beccari L, Iglesias Olle L, Rampon C, Vriz S et al. 2019. An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra. Nat. Commun. 10:312
    [Google Scholar]
  168. Wagner GP. 2007. The developmental genetics of homology. Nat. Rev. Genet. 8:473–79
    [Google Scholar]
  169. Wagner GP. 2014. Homology, Genes, and Evolutionary Innovation Princeton, NJ: Princeton Univ. PressThis book provides a framework for assessing homology using core regulatory networks.
  170. Warner JF, Amiel AR, Johnston H, Röttinger E. 2019. Regeneration is a partial redeployment of the embryonic gene network. BioRxiv 658930. https://doi.org/10.1101/658930
    [Crossref]
  171. Wehner D, Cizelsky W, Vasudevaro MD, Ozhan G, Haase C et al. 2014. Wnt/β-catenin signaling defines organizing centers that orchestrate growth and differentiation of the regenerating zebrafish caudal fin. Cell Rep 6:467–81
    [Google Scholar]
  172. Wei K, Serpooshan V, Hurtado C, Diez-Cuñado M, Zhao M et al. 2015. Epicardial FSTL1 reconstitution regenerates the adult mammalian heart. Nature 525:479–85
    [Google Scholar]
  173. Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW. 2012. A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26:988–1002
    [Google Scholar]
  174. Wolpert L 1991. Morgan's ambivalence: a history of gradients and regeneration. A History of Regeneration Research: Milestones in the Evolution of a Science CE Dinsmore 201–18 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  175. Wurtzel O, Cote LE, Poirier A, Satija R, Regev A, Reddien PW. 2015. A generic and cell-type-specific wound response precedes regeneration in planarians. Dev. Cell 35:632–45
    [Google Scholar]
  176. Yasumuro H, Sakurai K, Toyama F, Maruo F, Chiba C. 2017. Implications of a multi-step trigger of retinal regeneration in the adult newt. Biomedicines 5:25
    [Google Scholar]
  177. Yokoyama H, Ogino H, Stoick-Cooper CL, Grainger RM, Moon RT. 2007. Wnt/β-catenin signaling has an essential role in the initiation of limb regeneration. Dev. Biol. 306:170–78
    [Google Scholar]
  178. Young RA. 2011. Control of the embryonic stem cell state. Cell 144:940–54
    [Google Scholar]
  179. Zeng A, Li H, Guo L, Gao X, McKinney S et al. 2018. Prospectively isolated tetraspanin+ neoblasts are adult pluripotent stem cells underlying planaria regeneration. Cell 173:1593–608.e20
    [Google Scholar]
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