Advertisement

Cellular and Molecular Mechanisms of Hydra Regeneration

  • Puli Chandramouli Reddy
  • Akhila Gungi
  • Manu Unni
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 68)

Abstract

Regeneration of lost body parts is essential to regain the fitness of the organism for successful living. In the animal kingdom, organisms from different clades exhibit varied regeneration abilities. Hydra is one of the few organisms that possess tremendous regeneration potential, capable of regenerating complete organism from small tissue fragments or even from dissociated cells. This peculiar property has made this genus one of the most invaluable model organisms for understanding the process of regeneration. Multiple studies in Hydra led to the current understanding of gross morphological changes, basic cellular dynamics, and the role of molecular signalling such as the Wnt signalling pathway. However, cell-to-cell communication by cell adhesion, role of extracellular components such as extracellular matrix (ECM), and nature of cell types that contribute to the regeneration process need to be explored in depth. Additionally, roles of developmental signalling pathways need to be elucidated to enable more comprehensive understanding of regeneration in Hydra. Further research on cross communication among extracellular, cellular, and molecular signalling in Hydra will advance the field of regeneration biology. Here, we present a review of the existing literature on Hydra regeneration biology and outline the future perspectives.

Notes

Acknowledgements

The authors would like to thank Prof. Sanjeev Galande for the discussions and suggestions and Dr. Apurva Barve for reviewing this chapter. PCR is supported by Early Career Fellowship of the Wellcome Trust-DBT India Alliance (IA/E/16/1/503057). AG is supported by a fellowship from the Council of Scientific and Industrial Research, India. MU is supported by fellowship from the University Grants Commission (UGC), India.

References

  1. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2(10):e1031.  https://doi.org/10.1371/journal.pone.0001031 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12(5):494–518.  https://doi.org/10.1111/j.1525-142X.2010.00435.x CrossRefPubMedGoogle Scholar
  3. Alexandre C, Baena-Lopez A, Vincent JP (2014) Patterning and growth control by membrane-tethered Wingless. Nature 505(7482):180–185.  https://doi.org/10.1038/nature12879 CrossRefPubMedGoogle Scholar
  4. Alvarado AS (2006) Planarian regeneration: its end is its beginning. Cell 124(2):241–245CrossRefGoogle Scholar
  5. Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138(17):3593.  https://doi.org/10.1242/dev.063610 CrossRefPubMedGoogle Scholar
  6. 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(6):305–312PubMedCrossRefGoogle Scholar
  7. Auger H, Sasakura Y, Joly JS, Jeffery WR (2010) Regeneration of oral siphon pigment organs in the ascidian Ciona intestinalis. Dev Biol 339(2):374–389.  https://doi.org/10.1016/j.ydbio.2009.12.040 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ayling AL (1983) Growth and regeneration rates in thinly encrusting Demospongiae from temperate waters. Biol Bull 165(2):343–352.  https://doi.org/10.2307/1541200 CrossRefPubMedGoogle Scholar
  9. Bai S, Thummel R, Godwin AR, Nagase H, Itoh Y, Li L, Evans R, McDermott J, Seiki M, Sarras MP Jr (2005) Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1-MMP, MMP2 and TIMP2. Matrix Biol 24(4):247–260PubMedCrossRefGoogle Scholar
  10. Bannister R, McGonnell IM, Graham A, Thorndyke MC, Beesley PW (2005) Afuni, a novel transforming growth factor-beta gene is involved in arm regeneration by the brittle star Amphiura filiformis. Dev Genes Evol 215(8):393–401.  https://doi.org/10.1007/s00427-005-0487-8 CrossRefPubMedGoogle Scholar
  11. Barberán S, Fraguas S, Cebrià F (2016) The EGFR signaling pathway controls gut progenitor differentiation during planarian regeneration and homeostasis. Development 143(12):2089.  https://doi.org/10.1242/dev.131995 CrossRefPubMedGoogle Scholar
  12. Barolo S, Posakony JW (2002) Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16(10):1167–1181.  https://doi.org/10.1101/gad.976502 CrossRefPubMedGoogle Scholar
  13. Beck CW, Christen B, Slack JM (2003) Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell 5(3):429–439PubMedCrossRefGoogle Scholar
  14. Bellairs AA, Bryant S (1985) Autotomy and regeneration in reptiles. Biol Reptil 15(5):301–410Google Scholar
  15. Bely AE (2006) Distribution of segment regeneration ability in the Annelida. Integr Comp Biol 46(4):508–518.  https://doi.org/10.1093/icb/icj051 CrossRefPubMedGoogle Scholar
  16. Bely AE, Nyberg KG (2010) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25(3):161–170.  https://doi.org/10.1016/j.tree.2009.08.005 CrossRefPubMedGoogle Scholar
  17. Berrill NJ (1951) Regeneration and budding in tunicates. Biol Rev 26(4):456–475.  https://doi.org/10.1111/j.1469-185X.1951.tb01207.x CrossRefGoogle Scholar
  18. Bode HR (2003) Head regeneration in Hydra. Dev Dyn 226(2):225–236.  https://doi.org/10.1002/dvdy.10225 CrossRefPubMedGoogle Scholar
  19. Bohn H (1970) Interkalare Regeneration und segmentale Gradienten bei den Extremitäten von Leucophaea-Larven (Blattaria): II. Coxa und Tarsus. Dev Biol 23(3):355–379PubMedCrossRefGoogle Scholar
  20. Bolognesi R, Farzana L, Fischer TD, Brown SJ (2008) Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 18(20):1624–1629.  https://doi.org/10.1016/j.cub.2008.09.057 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Borisenko IE, Adamska M, Tokina DB, Ereskovsky AV (2015) Transdifferentiation is a driving force of regeneration in Halisarca dujardini (Demospongiae, Porifera). PeerJ 3:e1211.  https://doi.org/10.7717/peerj.1211 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Bossert PE, Dunn MP, Thomsen GH (2013) A staging system for the regeneration of a polyp from the aboral physa of the anthozoan Cnidarian Nematostella vectensis. Dev Dyn 242(11):1320–1331.  https://doi.org/10.1002/dvdy.24021 CrossRefPubMedGoogle Scholar
  23. Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in Hydra involves the canonical Wnt pathway. Development 132(12):2907–2916.  https://doi.org/10.1242/dev.01848 CrossRefPubMedGoogle Scholar
  24. Broussonet M (1786) Observations sur la régénérations de quelques parties du corps des poissons. Hist d l’Acad Roy des SciencesGoogle Scholar
  25. Brown FD, Keeling EL, Le AD, Swalla BJ (2009) Whole body regeneration in a colonial ascidian, Botrylloides violaceus. J Exp Zool B Mol Dev Evol 312(8):885–900.  https://doi.org/10.1002/jez.b.21303 CrossRefPubMedGoogle Scholar
  26. Bryant SV, Bellairs AA (1967) Tail regeneration in the lizards Anguis fragilis and Lacerta dugesii. J Linn Soc London Zool 46(310):297–305CrossRefGoogle Scholar
  27. Bryant DM, Sousounis K, Payzin-Dogru D, Bryant S, Sandoval AGW, Martinez Fernandez J, Mariano R, Oshiro R, Wong AY, Leigh ND, Johnson K, Whited JL (2017) Identification of regenerative roadblocks via repeat deployment of limb regeneration in axolotls. NPJ Regen Med 2(1):30.  https://doi.org/10.1038/s41536-017-0034-z CrossRefPubMedPubMedCentralGoogle Scholar
  28. Campbell RD (1967) Tissue dynamics of steady state growth in Hydra littoralis. II Patterns of tissue movement. J Morphol 121(1):19–28PubMedCrossRefGoogle Scholar
  29. Campbell RD (1987) A new species of Hydra (Cnidaria: Hydrozoa) from North America with comments on species clusters within the genus. Zool J Linnean Soc 91(3):253–263CrossRefGoogle Scholar
  30. Campbell R, David CN (1974) Cell cycle kinetics and development of Hydra attenuata: II. Interstitial cells. J Cell Sci 16(2):349–358PubMedGoogle Scholar
  31. Carnevali MC (2006) Regeneration in Echinoderms: repair, regrowth, cloning. Invertebr Surviv J 3(1):64–76Google Scholar
  32. Casari A, Schiavone M, Facchinello N, Vettori A, Meyer D, Tiso N, Moro E, Argenton F (2014) A Smad3 transgenic reporter reveals TGF-beta control of zebrafish spinal cord development. Dev Biol 396(1):81–93.  https://doi.org/10.1016/j.ydbio.2014.09.025 CrossRefPubMedGoogle Scholar
  33. Caubit X, Nicolas S, Le Parco Y (1997) Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev Dyn 210(1):1–10.  https://doi.org/10.1002/(SICI)1097-0177(199709)210:1<1::AID-AJA1>3.0.CO;2-L CrossRefPubMedGoogle Scholar
  34. Chablais F, Jaźwińska A (2012) The regenerative capacity of the zebrafish heart is dependent on TGFβ signaling. Development 139(11):1921.  https://doi.org/10.1242/dev.078543 CrossRefPubMedGoogle Scholar
  35. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F (2004) Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 101(20):7641–7645.  https://doi.org/10.1073/pnas.0401654101 CrossRefPubMedGoogle Scholar
  36. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W, Martinou J-C, Galliot B (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive Hydra head regeneration. Dev Cell 17(2):279–289PubMedCrossRefGoogle Scholar
  37. Choi W-Y, Gemberling M, Wang J, Holdway JE, Shen M-C, Karlstrom RO, Poss KD (2013) In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development 140(3):660.  https://doi.org/10.1242/dev.088526 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Chourrout D, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, De Jong P, Steele RE (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. Nature 442(7103):684PubMedCrossRefGoogle Scholar
  39. Contreras EG, Gaete M, Sánchez N, Carrasco H, Larraín J (2009) Early requirement of hyaluronan for tail regeneration in Xenopus tadpoles. Development 136(17):2987–2996PubMedCrossRefGoogle Scholar
  40. Cotanche DA (1987) Regeneration of the tectorial membrane in the chick cochlea following severe acoustic trauma. Hear Res 30(2–3):197–206PubMedCrossRefGoogle Scholar
  41. Crest J, Diz-Muñoz A, Chen D-Y, Fletcher DA, Bilder D (2017) Organ sculpting by patterned extracellular matrix stiffness. Elife 6:e24958PubMedPubMedCentralCrossRefGoogle Scholar
  42. Cuénot L (1948) Anatomie, éthologie et systématique des échinodermes. Traité de zoologie 11:1–363Google Scholar
  43. Dahlberg C, Auger H, Dupont S, Sasakura Y, Thorndyke M, Joly JS (2009) Refining the Ciona intestinalis model of central nervous system regeneration. PLoS One 4(2):e4458.  https://doi.org/10.1371/journal.pone.0004458 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Dalyell J (1814) Observations on some interesting phenomena in animal physiology. Exhibited by several species of Planariae illustrated by coloured figures of living animals. Edinburgh, Archibald ConstableGoogle Scholar
  45. Darras S, Fritzenwanker JH, Uhlinger KR, Farrelly E, Pani AM, Hurley IA, Norris RP, Osovitz M, Terasaki M, Wu M, Aronowicz J, Kirschner M, Gerhart JC, Lowe CJ (2018) Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development. PLoS Biol 16(1):e2003698.  https://doi.org/10.1371/journal.pbio.2003698 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Davis LE, Haynes JF (1968) An ultrastructural examination of the mesoglea of Hydra. Z Zellforsch Mikrosk Anat 92(2):149–158PubMedCrossRefGoogle Scholar
  47. De Robertis EM, Kuroda H (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285–308.  https://doi.org/10.1146/annurev.cellbio.20.011403.154124 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Dogra D, Ahuja S, Kim H-T, Rasouli SJ, Stainier DYR, Reischauer S (2017) Opposite effects of Activin type 2 receptor ligands on cardiomyocyte proliferation during development and repair. Nat Commun 8(1):1902.  https://doi.org/10.1038/s41467-017-01950-1 CrossRefPubMedPubMedCentralGoogle Scholar
  49. DuBuc TQ, Stephenson TB, Rock AQ, Martindale MQ (2018) Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation. Nat Commun 9(1):2007.  https://doi.org/10.1038/s41467-018-04184-x CrossRefPubMedPubMedCentralGoogle Scholar
  50. Egger B, Gschwentner R, Rieger R (2007) Free-living flatworms under the knife: past and present. Dev Genes Evol 217(2):89PubMedCrossRefGoogle Scholar
  51. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689.  https://doi.org/10.1016/j.cell.2006.06.044 CrossRefPubMedGoogle Scholar
  52. Etheridge R (1967) Lizard caudal vertebrae. Copeia:699–721Google Scholar
  53. Feng XH, Derynck R (2005) Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21:659–693.  https://doi.org/10.1146/annurev.cellbio.21.022404.142018 CrossRefPubMedGoogle Scholar
  54. Fraguas S, Barberan S, Cebria F (2011) EGFR signaling regulates cell proliferation, differentiation and morphogenesis during planarian regeneration and homeostasis. Dev Biol 354(1):87–101.  https://doi.org/10.1016/j.ydbio.2011.03.023 CrossRefPubMedGoogle Scholar
  55. Galliot B, Chera S (2010) The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration. Trends Cell Biol 20(9):514–523PubMedCrossRefGoogle Scholar
  56. Gauchat D, Mazet F, Berney C, Schummer M, Kreger S, Pawlowski J, Galliot B (2000) Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc Natl Acad Sci USA 97(9):4493–4498PubMedCrossRefGoogle Scholar
  57. Gerhart J (1999) 1998 Warkany lecture: signaling pathways in development. Teratology 60(4):226–239PubMedCrossRefGoogle Scholar
  58. Gierer A, Berking S, Bode H, David CN, Flick K, Hansmann G, Schaller H, Trenkner E (1972) Regeneration of Hydra from reaggregated cells. Nat New Biol 239(91):98–101PubMedCrossRefGoogle Scholar
  59. Goss RJ (1963) Adaptive growth. Lagos, LondonGoogle Scholar
  60. Goss RJ (1969) Principles of regeneration. Elsevier, AmsterdamGoogle Scholar
  61. Goss RJ (1983) Deer antlers: regeneration, function and evolution. Academic Press, New YorkGoogle Scholar
  62. Goss RJ (1992) The evolution of regeneration: adaptive or inherent? J Theor Biol 159(2):241–260PubMedCrossRefGoogle Scholar
  63. Graff L (1882) VON. 1882. Monographie der Turbellarien. I Rhabdocoelida Ak der Wiss zu Berlin 442Google Scholar
  64. Grau-Bove X, Torruella G, Donachie S, Suga H, Leonard G, Richards TA, Ruiz-Trillo I (2017) Dynamics of genomic innovation in the unicellular ancestry of animals. Elife 6:e26036.  https://doi.org/10.7554/eLife.26036 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Grotek B, Wehner D, Weidinger G (2013) Notch signaling coordinates cellular proliferation with differentiation during zebrafish fin regeneration. Development 140(7):1412–1423.  https://doi.org/10.1242/dev.087452 CrossRefPubMedGoogle Scholar
  66. Gulati AK, Reddi A, Zalewski A (1983) Changes in the basement membrane zone components during skeletal muscle fiber degeneration and regeneration. J Cell Biol 97(4):957–962PubMedCrossRefGoogle Scholar
  67. Hess A, Cohen A, Robson EA (1957) Observations on the structure of Hydra as seen with the electron and light microscopes. J Cell Sci 3(43):315–326Google Scholar
  68. Ho DM, Whitman M (2008) TGF-beta signaling is required for multiple processes during Xenopus tail regeneration. Dev Biol 315(1):203–216.  https://doi.org/10.1016/j.ydbio.2007.12.031 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbacher U, Holstein TW (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407(6801):186–189.  https://doi.org/10.1038/35025063 CrossRefPubMedGoogle Scholar
  70. Hoffmeister S, Schaller HC (1985) A new biochemical marker for foot-specific cell differentiation in Hydra. Wilhelm Roux Arch Dev Biol 194(8):453–461CrossRefGoogle Scholar
  71. Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C, Heldin CH (2009) Emergence, development and diversification of the TGF-beta signalling pathway within the animal kingdom. BMC Evol Biol 9:28.  https://doi.org/10.1186/1471-2148-9-28 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Hutchins ED, Markov GJ, Eckalbar WL, George RM, King JM, Tokuyama MA, Geiger LA, Emmert N, Ammar MJ, Allen AN, Siniard AL, Corneveaux JJ, Fisher RE, Wade J, DeNardo DF, Rawls JA, Huentelman MJ, Wilson-Rawls J, Kusumi K (2014) Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. PLoS One 9(8):e105004.  https://doi.org/10.1371/journal.pone.0105004 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Hyman LH (1940) Aspects of regeneration in annelids. Am Nat 74(755):513–527CrossRefGoogle Scholar
  74. Hyman LH (1955) The invertebrates: Echinodermata, the coelomate bilateria, vol 4. McGraw-Hill, New YorkGoogle Scholar
  75. Iismaa SE, Kaidonis X, Nicks AM, Bogush N, Kikuchi K, Naqvi N, Harvey RP, Husain A, Graham RM (2018) Comparative regenerative mechanisms across different mammalian tissues. NPJ Regen Med 3:6.  https://doi.org/10.1038/s41536-018-0044-5 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Johnson SL, Weston JA (1995) Temperature-sensitive mutations that cause stage-specific defects in Zebrafish fin regeneration. Genetics 141(4):1583–1595PubMedPubMedCentralGoogle Scholar
  77. Jopling C, Boue S, Belmonte JCI (2011) Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat Rev Mol Cell Biol 12(2):79PubMedCrossRefGoogle Scholar
  78. Kaliszewicz A (2018) Sex ratio patterns and trade-off between sexual and asexual reproduction in the brown Hydra. Freshw Sci 37(3):551–561CrossRefGoogle Scholar
  79. Kasbauer T, Towb P, Alexandrova O, David CN, Dall’armi E, Staudigl A, Stiening B, Bottger A (2007) The Notch signaling pathway in the cnidarian Hydra. Dev Biol 303(1):376–390.  https://doi.org/10.1016/j.ydbio.2006.11.022 CrossRefPubMedGoogle Scholar
  80. Kawabata M, Miyazono K (1999) Signal transduction of the TGF-beta superfamily by Smad proteins. J Biochem 125(1):9–16PubMedCrossRefGoogle Scholar
  81. Kawakami Y, Rodriguez Esteban C, Raya M, Kawakami H, Marti M, Dubova I, Izpisua Belmonte JC (2006) Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev 20(23):3232–3237.  https://doi.org/10.1101/gad.1475106 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Kitisin K, Saha T, Blake T, Golestaneh N, Deng M, Kim C, Tang Y, Shetty K, Mishra B, Mishra L (2007) Tgf-Beta signaling in development. Sci STKE 2007(399):cm1.  https://doi.org/10.1126/stke.3992007cm1 CrossRefPubMedGoogle Scholar
  83. Kopan R (2012) Notch signaling. Cold Spring Harb Perspect Biol 4(10):a011213.  https://doi.org/10.1101/cshperspect.a011213 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Kragl M, Knapp D, Nacu E, Khattak S, Maden M, Epperlein HH, Tanaka EM (2009) Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460(7251):60PubMedCrossRefGoogle Scholar
  85. Krishnapati LS, Ghaskadbi S (2013) Identification and characterization of VEGF and FGF from Hydra. Int J Dev Biol 57(11–12):897–906.  https://doi.org/10.1387/ijdb.130077sg CrossRefPubMedGoogle Scholar
  86. Lane MC, Koehl M, Wilt F, Keller R (1993) A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 117(3):1049–1060PubMedGoogle Scholar
  87. Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS, Degnan BM (2007) The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol 17(8):706–710.  https://doi.org/10.1016/j.cub.2007.03.008 CrossRefPubMedGoogle Scholar
  88. Le Grand F, Rudnicki MA (2007) Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19(6):628–633PubMedPubMedCentralCrossRefGoogle Scholar
  89. Leclere L, Bause M, Sinigaglia C, Steger J, Rentzsch F (2016) Development of the aboral domain in Nematostella requires beta-catenin and the opposing activities of Six3/6 and Frizzled5/8. Development 143(10):1766–1777.  https://doi.org/10.1242/dev.120931 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Lei K, Thi-Kim Vu H, Mohan RD, McKinney SA, Seidel CW, Alexander R, Gotting K, Workman JL, Sanchez Alvarado A (2016) Egf signaling directs neoblast repopulation by regulating asymmetric cell division in planarians. Dev Cell 38(4):413–429.  https://doi.org/10.1016/j.devcel.2016.07.012 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330(1):186–199.  https://doi.org/10.1016/j.ydbio.2009.02.004 CrossRefPubMedGoogle Scholar
  92. Lenhoff SG, Lenhoff HM, Trembley A (1986) Hydra and the birth of experimental biology, 1744: Abraham Trembley’s Mémoires concerning the polyps. Boxwood Press, GroveGoogle Scholar
  93. Levesque M, Gatien S, Finnson K, Desmeules S, Villiard E, Pilote M, Philip A, Roy S (2007) Transforming growth factor: beta signaling is essential for limb regeneration in axolotls. PLoS One 2(11):e1227.  https://doi.org/10.1371/journal.pone.0001227 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Liao BK, Jorg DJ, Oates AC (2016) Faster embryonic segmentation through elevated Delta-Notch signalling. Nat Commun 7:11861.  https://doi.org/10.1038/ncomms11861 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Loh KM, van Amerongen R, Nusse R (2016) Generating cellular diversity and spatial form: Wnt signaling and the evolution of multicellular animals. Dev Cell 38(6):643–655.  https://doi.org/10.1016/j.devcel.2016.08.011 CrossRefPubMedGoogle Scholar
  96. Lozito TP, Tuan RS (2017) Lizard tail regeneration as an instructive model of enhanced healing capabilities in an adult amniote. Connect Tissue Res 58(2):145–154.  https://doi.org/10.1080/03008207.2016.1215444 CrossRefPubMedGoogle Scholar
  97. Lukjanenko L, Jung MJ, Hegde N, Perruisseau-Carrier C, Migliavacca E, Rozo M, Karaz S, Jacot G, Schmidt M, Li L (2016) Loss of fibronectin from the aged stem cell niche affects the regenerative capacity of skeletal muscle in mice. Nat Med 22(8):897PubMedPubMedCentralCrossRefGoogle Scholar
  98. Maden M, Brant JO, Rubiano A, Sandoval AGW, Simmons C, Mitchell R, Collin-Hooper H, Jacobson J, Omairi S, Patel K (2018) Perfect chronic skeletal muscle regeneration in adult spiny mice, Acomys cahirinus. Sci Rep 8(1):8920PubMedPubMedCentralCrossRefGoogle Scholar
  99. Mailman ML, Dresden MH (1976) Collagen metabolism in the regenerating forelimb of Notophthalmus viridescens: synthesis, accumulation, and maturation. Dev Biol 50(2):378–394PubMedCrossRefGoogle Scholar
  100. Mao Y, Baum B (2015) Tug of war—the influence of opposing physical forces on epithelial cell morphology. Dev Biol 401(1):92–102PubMedCrossRefGoogle Scholar
  101. Marlow H, Roettinger E, Boekhout M, Martindale MQ (2012) Functional roles of Notch signaling in the cnidarian Nematostella vectensis. Dev Biol 362(2):295–308.  https://doi.org/10.1016/j.ydbio.2011.11.012 CrossRefPubMedGoogle Scholar
  102. Marques AC, Collins AG (2004) Cladistic analysis of Medusozoa and cnidarian evolution. Invertebr Biol 123(1):23–42CrossRefGoogle Scholar
  103. Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6(12):917–927.  https://doi.org/10.1038/nrg1725 CrossRefPubMedGoogle Scholar
  104. Martínez DE, Bridge D (2012) Hydra, the everlasting embryo, confronts aging. Int J Dev Biol 56(6–7–8):479–487PubMedCrossRefGoogle Scholar
  105. McGregor AP, Pechmann M, Schwager EE, Feitosa NM, Kruck S, Aranda M, Damen WG (2008) Wnt8 is required for growth-zone establishment and development of opisthosomal segments in a spider. Curr Biol 18(20):1619–1623PubMedCrossRefGoogle Scholar
  106. Meyer JJ, Byers JE (2005) As good as dead? Sublethal predation facilitates lethal predation on an intertidal clam. Ecol Lett 8(2):160–166CrossRefGoogle Scholar
  107. Michalopoulos GK, DeFrances MC (1997) Liver regeneration. Science 276(5309):60–66PubMedCrossRefGoogle Scholar
  108. Miller JR (2002) The Wnts. Genome Biol 3(1):REVIEWS3001PubMedGoogle Scholar
  109. Minelli A, Boxshall G, Fusco G (2013) Arthropod biology and evolution: molecules, development, morphology. Springer Science and Business Media, HeidelbergCrossRefGoogle Scholar
  110. Miyawaki K, Mito T, Sarashina I, Zhang H, Shinmyo Y, Ohuchi H, Noji S (2004) Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech Dev 121(2):119–130.  https://doi.org/10.1016/j.mod.2004.01.002 CrossRefPubMedGoogle Scholar
  111. Monti R (1900) La rigenerazione nelle planarie marine. Milan R. Istituto Lombardo, MilanGoogle Scholar
  112. Münch J, González-Rajal A, de la Pompa JL (2013) Notch regulates blastema proliferation and prevents differentiation during adult zebrafish fin regeneration. Development 140(7):1402.  https://doi.org/10.1242/dev.087346 CrossRefPubMedGoogle Scholar
  113. Munder S, Kasbauer T, Prexl A, Aufschnaiter R, Zhang X, Towb P, Bottger A (2010) Notch signalling defines critical boundary during budding in Hydra. Dev Biol 344(1):331–345.  https://doi.org/10.1016/j.ydbio.2010.05.517 CrossRefPubMedGoogle Scholar
  114. Munder S, Tischer S, Grundhuber M, Buchels N, Bruckmeier N, Eckert S, Seefeldt CA, Prexl A, Kasbauer T, Bottger A (2013) Notch-signalling is required for head regeneration and tentacle patterning in Hydra. Dev Biol 383(1):146–157.  https://doi.org/10.1016/j.ydbio.2013.08.022 CrossRefPubMedGoogle Scholar
  115. Naito M, Ishiguro H, Fujisawa T, Kurosawa Y (1993) Presence of eight distinct homeobox-containing genes in cnidarians. FEBS Lett 333(3):271–274PubMedCrossRefGoogle Scholar
  116. Nakamura Y, Tsiairis CD, Ozbek S, Holstein TW (2011) Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer. Proc Natl Acad Sci USA 108(22):9137–9142.  https://doi.org/10.1073/pnas.1018109108 CrossRefPubMedGoogle Scholar
  117. Newmark PA, Sanchez Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220(2):142–153.  https://doi.org/10.1006/dbio.2000.9645 CrossRefPubMedGoogle Scholar
  118. Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103(33):12451–12456.  https://doi.org/10.1073/pnas.0604065103 CrossRefPubMedGoogle Scholar
  119. Nistala H, Lee-Arteaga S, Smaldone S, Siciliano G, Carta L, Ono RN, Sengle G, Arteaga-Solis E, Levasseur R, Ducy P (2010) Fibrillin-1 and -2 differentially modulate endogenous TGF-β and BMP bioavailability during bone formation. J Cell Biol 190(6):1107–1121PubMedPubMedCentralCrossRefGoogle Scholar
  120. Notari M, Ventura-Rubio A, Bedford-Guaus SJ, Jorba I, Mulero L, Navajas D, Martí M, Raya Á (2018) The local microenvironment limits the regenerative potential of the mouse neonatal heart. Sci Adv 4(5):eaao5553PubMedPubMedCentralCrossRefGoogle Scholar
  121. Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287(5785):795–801PubMedCrossRefGoogle Scholar
  122. O’Connor MB, Umulis D, Othmer HG, Blair SS (2006) Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133(2):183–193.  https://doi.org/10.1242/dev.02214 CrossRefPubMedPubMedCentralGoogle Scholar
  123. Onai T, Aramaki T, Inomata H, Hirai T, Kuratani S (2015) On the origin of vertebrate somites. Zoological Lett 1:33.  https://doi.org/10.1186/s40851-015-0033-0 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Ozhan G, Weidinger G (2015) Wnt/beta-catenin signaling in heart regeneration. Cell Regen (Lond) 4(1):3.  https://doi.org/10.1186/s13619-015-0017-8 CrossRefGoogle Scholar
  125. Pang K, Ryan JF, Mullikin JC, Baxevanis AD, Martindale MQ, Program NCS (2010) Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. EvoDevo 1(1):10.  https://doi.org/10.1186/2041-9139-1-10 CrossRefPubMedPubMedCentralGoogle Scholar
  126. Pang K, Ryan JF, Baxevanis AD, Martindale MQ (2011) Evolution of the TGF-beta signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS One 6(9):e24152.  https://doi.org/10.1371/journal.pone.0024152 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Passano L, McCullough C (1964) Co-ordinating systems and behaviour in Hydra: I. Pacemaker system of the periodic contractions. J Exp Biol 41(3):643–664Google Scholar
  128. Patruno M, Smertenko A, Carnevali MC, Bonasoro F, Beesley P, Thorndyke M (2002) Expression of transforming growth factor β-like molecules in normal and regenerating arms of the crinoid Antedon mediterranea: immunocytochemical and biochemical evidence. Proc R Soc Lond B Biol Sci 269(1502):1741–1747CrossRefGoogle Scholar
  129. Patruno M, McGonnell I, Graham A, Beesley P, Carnevali MC, Thorndyke M (2003) Anbmp2/4 is a new member of the transforming growth factor-β superfamily isolated from a crinoid and involved in regeneration. Proc R Soc Lond B Biol Sci 270(1522):1341–1347CrossRefGoogle Scholar
  130. Petersen CP, Reddien PW (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319(5861):327–330.  https://doi.org/10.1126/science.1149943 CrossRefPubMedGoogle Scholar
  131. Petersen CP, Reddien PW (2009) A wound-induced Wnt expression program controls planarian regeneration polarity. Proc Natl Acad Sci USA 106(40):17061–17066.  https://doi.org/10.1073/pnas.0906823106 CrossRefPubMedGoogle Scholar
  132. Petersen HO, Hoger SK, Looso M, Lengfeld T, Kuhn A, Warnken U, Nishimiya-Fujisawa C, Schnolzer M, Kruger M, Ozbek S, Simakov O, Holstein TW (2015) A comprehensive transcriptomic and proteomic analysis of Hydra head regeneration. Mol Biol Evol 32(8):1928–1947.  https://doi.org/10.1093/molbev/msv079 CrossRefPubMedPubMedCentralGoogle Scholar
  133. Raya Á, Koth CM, Büscher D, Kawakami Y, Itoh T, Raya RM, Sternik G, Tsai H-J, Rodríguez-Esteban C, Izpisúa-Belmonte JC (2003) Activation of Notch signaling pathway precedes heart regeneration in zebrafish. Proc Natl Acad Sci USA 100(suppl 1):11889.  https://doi.org/10.1073/pnas.1834204100 CrossRefPubMedGoogle Scholar
  134. Reddy PC, Bidaye SS, Ghaskadbi S (2011) Genome-wide screening reveals the emergence and divergence of RTK homologues in basal Metazoan Hydra magnipapillata. J Biosci 36(2):289–296PubMedCrossRefGoogle Scholar
  135. Reddy PC, Unni MK, Gungi A, Agarwal P, Galande S (2015) Evolution of Hox-like genes in Cnidaria: study of Hydra Hox repertoire reveals tailor-made Hox-code for cnidarians. Mech Dev 138(Pt 2):87–96.  https://doi.org/10.1016/j.mod.2015.08.005 CrossRefPubMedGoogle Scholar
  136. Reddy PC, Ubhe S, Sirwani N, Lohokare R, Galande S (2017) Rapid divergence of histones in Hydrozoa (Cnidaria) and evolution of a novel histone involved in DNA damage response in Hydra. Zoology (Jena) 123:53–63.  https://doi.org/10.1016/j.zool.2017.06.005 CrossRefGoogle Scholar
  137. Reinhardt B, Broun M, Blitz IL, Bode HR (2004) HyBMP5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in Hydra. Dev Biol 267(1):43–59.  https://doi.org/10.1016/j.ydbio.2003.10.031 CrossRefPubMedGoogle Scholar
  138. Rentzsch F, Guder C, Vocke D, Hobmayer B, Holstein TW (2007) An ancient chordin-like gene in organizer formation of Hydra. Proc Natl Acad Sci USA 104(9):3249–3254.  https://doi.org/10.1073/pnas.0604501104 CrossRefPubMedGoogle Scholar
  139. Richards GS, Degnan BM (2012) The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development. EvoDevo 3(1):15.  https://doi.org/10.1186/2041-9139-3-15 CrossRefPubMedPubMedCentralGoogle Scholar
  140. Richards GS, Simionato E, Perron M, Adamska M, Vervoort M, Degnan BM (2008) Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol 18(15):1156–1161.  https://doi.org/10.1016/j.cub.2008.06.074 CrossRefPubMedGoogle Scholar
  141. Rigo-Watermeier T, Kraft B, Ritthaler M, Wallkamm V, Holstein T, Wedlich D (2012) Functional conservation of Nematostella Wnts in canonical and noncanonical Wnt-signaling. Biol Open 1(1):43–51.  https://doi.org/10.1242/bio.2011021 CrossRefPubMedGoogle Scholar
  142. Ritter WE, Congdon EM (1900) On the inhibition by artificial section of the normal fission plane in Stenostoma, vol 2, 6. Academy, San FranciscoGoogle Scholar
  143. Ruhl L (1927) Regenerationserscheinungen an Rhabdocoelen. Zool Anz 72:160–175Google Scholar
  144. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC, Finnerty JR (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7(7):R64.  https://doi.org/10.1186/gb-2006-7-7-R64 CrossRefPubMedPubMedCentralGoogle Scholar
  145. Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, Program NCS, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342(6164):1242592.  https://doi.org/10.1126/science.1242592 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Sakai T, Larsen M, Yamada KM (2003) Fibronectin requirement in branching morphogenesis. Nature 423(6942):876PubMedCrossRefGoogle Scholar
  147. Sanz-Ezquerro JJ, Munsterberg AE, Stricker S (2017) Editorial: Signaling pathways in embryonic development. Front Cell Dev Biol 5:76.  https://doi.org/10.3389/fcell.2017.00076 CrossRefPubMedPubMedCentralGoogle Scholar
  148. Sarras MP Jr (2012) Components, structure, biogenesis and function of the Hydra extracellular matrix in regeneration, pattern formation and cell differentiation. Int J Dev Biol 56(6–7–8):567–576PubMedCrossRefGoogle Scholar
  149. Sarras MP Jr, Zhang X, Huff JK, Accavitti MA, John PS, Abrahamson DR (1993) Extracellular matrix (mesoglea) of Hydra vulgaris: III. Formation and function during morphogenesis of Hydra cell aggregates. Dev Biol 157(2):383–398PubMedCrossRefGoogle Scholar
  150. Sasidharan V, Marepally S, Elliott SA, Baid S, Lakshmanan V, Nayyar N, Bansal D, Sánchez Alvarado A, Vemula PK, Palakodeti D (2017) The miR-124 family of microRNAs is crucial for regeneration of the brain and visual system in the planarian Schmidtea mediterranea. Development 144(18):3211.  https://doi.org/10.1242/dev.144758 CrossRefPubMedPubMedCentralGoogle Scholar
  151. Sato M, Bode HR, Sawada Y (1990) Patterning processes in aggregates of Hydra cells visualized with the monoclonal antibody, Ts19. Dev Biol 141(2):412–420PubMedCrossRefGoogle Scholar
  152. Schmid V, Tardent P (1971) The reconstitutional performances of the Leptomedusa Campanularia jonstoni. Mar Biol 8(2):99–104CrossRefGoogle Scholar
  153. Schubert M, Holland LZ (2013) The Wnt gene family and the evolutionary conservation of Wnt expression. In: Madame Curie bioscience database [Internet]. Landes Bioscience, Austin, TXGoogle Scholar
  154. Schummer M, Scheurlen I, Schaller C, Galliot B (1992) HOM/HOX homeobox genes are present in Hydra (Chlorohydra viridissima) and are differentially expressed during regeneration. EMBO J 11(5):1815–1823PubMedPubMedCentralCrossRefGoogle Scholar
  155. Scimone ML, Cote LE, Rogers T, Reddien PW (2016) Two FGFRL-Wnt circuits organize the planarian anteroposterior axis. Elife 5:e12845.  https://doi.org/10.7554/eLife.12845 CrossRefPubMedPubMedCentralGoogle Scholar
  156. 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(7417):561PubMedPubMedCentralCrossRefGoogle Scholar
  157. Shenk MA, Bode HR, Steele RE (1993) Expression of Cnox-2, a HOM/HOX homeobox gene in Hydra, is correlated with axial pattern formation. Development 117(2):657–667PubMedGoogle Scholar
  158. Shi S, Stanley P (2006) Evolutionary origins of Notch signaling in early development. Cell Cycle 5(3):274–278.  https://doi.org/10.4161/cc.5.3.2396 CrossRefPubMedGoogle Scholar
  159. Shimizu H, Zhang X, Zhang J, Leontovich A, Fei K, Yan L, Sarras MP (2002) Epithelial morphogenesis in Hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development (Cambridge, England) 129:1521–1532Google Scholar
  160. Shimizu T, Bae YK, Muraoka O, Hibi M (2005) Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev Biol 279(1):125–141.  https://doi.org/10.1016/j.ydbio.2004.12.007 CrossRefPubMedGoogle Scholar
  161. Shimizu H, Aufschnaiter R, Li L, Sarras MP Jr, Borza D-B, Abrahamson DR, Sado Y, Zhang X (2008) The extracellular matrix of Hydra is a porous sheet and contains type IV collagen. Zoology 111(5):410–418PubMedCrossRefGoogle Scholar
  162. Simpson SB Jr (1964) Analysis of tail regeneration in the lizard Lygosoma laterale. I. Initiation of regeneration and cartilage differentiation: the role of ependyma. J Morphol 114:425–435.  https://doi.org/10.1002/jmor.1051140305 CrossRefPubMedGoogle Scholar
  163. Souilhol C, Perea-Gomez A, Camus A, Beck-Cormier S, Vandormael-Pournin S, Escande M, Collignon J, Cohen-Tannoudji M (2015) NOTCH activation interferes with cell fate specification in the gastrulating mouse embryo. Development 142(21):3649–3660.  https://doi.org/10.1242/dev.121145 CrossRefPubMedGoogle Scholar
  164. Spallanzani L (1769) An essay on animal reproductions. T. Becket and PA de Hondt, LondonGoogle Scholar
  165. Stevens N, Boring A (1905) Regeneration in polychœrus caudatus. Part I. Observations on living material. J Exp Zool 2(3):335–346CrossRefGoogle Scholar
  166. Stone JS, Rubel EW (2000) Cellular studies of auditory hair cell regeneration in birds. Proc Natl Acad Sci USA 97(22):11714–11721PubMedCrossRefGoogle Scholar
  167. Sudhop S, Coulier F, Bieller A, Vogt A, Hotz T, Hassel M (2004) Signalling by the FGFR-like tyrosine kinase, Kringelchen, is essential for bud detachment in Hydra vulgaris. Development 131(16):4001–4011.  https://doi.org/10.1242/dev.01267 CrossRefPubMedGoogle Scholar
  168. Suga H, Katoh K, Miyata T (2001) Sponge homologs of vertebrate protein tyrosine kinases and frequent domain shufflings in the early evolution of animals before the parazoan-eumetazoan split. Gene 280(1–2):195–201PubMedCrossRefGoogle Scholar
  169. Sugiyama T, Fujisawa T (1978) Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. J Cell Sci 29(1):35–52PubMedGoogle Scholar
  170. Sureda-Gomez M, Martin-Duran JM, Adell T (2016) Localization of planarian beta-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis. Development 143(22):4149–4160.  https://doi.org/10.1242/dev.135152 CrossRefPubMedGoogle Scholar
  171. Takaku Y, Hariyama T, Fujisawa T (2005) Motility of endodermal epithelial cells plays a major role in reorganizing the two epithelial layers in Hydra. Mech Dev 122(1):109–122PubMedCrossRefGoogle Scholar
  172. Tassava RA, Nace JD, Wei Y (1996) Extracellular matrix protein turnover during salamander limb regeneration. Wound Repair Regen 4(1):75–81PubMedCrossRefGoogle Scholar
  173. Technau U, Holstein TW (1992) Cell sorting during the regeneration of Hydra from reaggregated cells. Dev Biol 151(1):117–127PubMedCrossRefGoogle Scholar
  174. Tischer S, Reineck M, Soding J, Munder S, Bottger A (2013) Eph receptors and ephrin class B ligands are expressed at tissue boundaries in Hydra vulgaris. Int J Dev Biol 57(9–10):759–765.  https://doi.org/10.1387/ijdb.130158ab CrossRefPubMedGoogle Scholar
  175. Török A, Schiffer PH, Schnitzler CE, Ford K, Mullikin JC, Baxevanis AD, Bacic A, Frank U, Gornik SG (2016) The cnidarian Hydractinia echinata employs canonical and highly adapted histones to pack its DNA. Epigenetics Chromatin 9(1):36PubMedPubMedCentralCrossRefGoogle Scholar
  176. Trembley A (1744) Mémoires pour servir à l’histoire d’un genre de polypes d’eau douce, à bras en forme de cornes. Par A. Trembley. Chez Jean & Herman Verbeek, LeideGoogle Scholar
  177. Tressler J, Maddox F, Goodwin E, Zhang Z, Tublitz NJ (2014) Arm regeneration in two species of cuttlefish Sepia officinalis and Sepia pharaonis. Invertebr Neurosci 14(1):37–49.  https://doi.org/10.1007/s10158-013-0159-8 CrossRefGoogle Scholar
  178. Tu S, Johnson SL (2011) Fate restriction in the growing and regenerating zebrafish fin. Dev Cell 20(5):725–732PubMedPubMedCentralCrossRefGoogle Scholar
  179. Unguez GA (2013) Electric fish: new insights into conserved processes of adult tissue regeneration. J Exp Biol 216(13):2478.  https://doi.org/10.1242/jeb.082396 CrossRefPubMedPubMedCentralGoogle Scholar
  180. Volinsky N, Kholodenko BN (2013) Complexity of receptor tyrosine kinase signal processing. Cold Spring Harb Perspect Biol 5(8):a009043.  https://doi.org/10.1101/cshperspect.a009043 CrossRefPubMedPubMedCentralGoogle Scholar
  181. Vracko R, Benditt EP (1972) Basal lamina: the scaffold for orderly cell replacement: observations on regeneration of injured skeletal muscle fibers and capillaries. J Cell Biol 55(2):406–419PubMedPubMedCentralCrossRefGoogle Scholar
  182. Wagner GP, Misof BY (1992) Evolutionary modification of regenerative capability in vertebrates: a comparative study on teleost pectoral fin regeneration. J Exp Zool 261(1):62–78.  https://doi.org/10.1002/jez.1402610108 CrossRefPubMedGoogle Scholar
  183. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332(6031):811–816PubMedPubMedCentralCrossRefGoogle Scholar
  184. Wang J, Karra R, Dickson AL, Poss KD (2013) Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol 382(2):427–435PubMedCrossRefGoogle Scholar
  185. Watanabe H, Schmidt HA, Kuhn A, Hoger SK, Kocagoz Y, Laumann-Lipp N, Ozbek S, Holstein TW (2014) Nodal signalling determines biradial asymmetry in Hydra. Nature 515(7525):112–115.  https://doi.org/10.1038/nature13666 CrossRefPubMedGoogle Scholar
  186. 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(9):988–1002.  https://doi.org/10.1101/gad.187377.112 CrossRefPubMedPubMedCentralGoogle Scholar
  187. Wills AA, Kidd AR, Lepilina A, Poss KD (2008) Fgfs control homeostatic regeneration in adult zebrafish fins. Development 135(18):3063.  https://doi.org/10.1242/dev.024588 CrossRefPubMedPubMedCentralGoogle Scholar
  188. Windsor Reid PJ, Matveev E, McClymont A, Posfai D, Hill AL, Leys SP (2018) Wnt signaling and polarity in freshwater sponges. BMC Evol Biol 18(1):12.  https://doi.org/10.1186/s12862-018-1118-0 CrossRefPubMedPubMedCentralGoogle Scholar
  189. Wu MY, Hill CS (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16(3):329–343.  https://doi.org/10.1016/j.devcel.2009.02.012 CrossRefPubMedGoogle Scholar
  190. Yokoyama H (2008) Initiation of limb regeneration: the critical steps for regenerative capacity. Develop Growth Differ 50(1):13–22.  https://doi.org/10.1111/j.1440-169X.2007.00973.x CrossRefGoogle Scholar
  191. Zhang R, Han P, Yang H, Ouyang K, Lee D, Lin Y-F, Ocorr K, Kang G, Chen J, Stainier DYR, Yelon D, Chi NC (2013) In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 498:497.  https://doi.org/10.1038/nature12322. https://www.nature.com/articles/nature12322#supplementary-information CrossRefPubMedPubMedCentralGoogle Scholar
  192. Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE (2014) Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci USA 111(4):1403.  https://doi.org/10.1073/pnas.1311705111 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Puli Chandramouli Reddy
    • 1
  • Akhila Gungi
    • 1
  • Manu Unni
    • 1
  1. 1.Department of BiologyIndian Institute of Science Education and ResearchPuneIndia

Personalised recommendations