Skip to main content

Advertisement

SpringerLink
Log in

Heart of Newt: A Recipe for Regeneration

  • Published:
Journal of Cardiovascular Translational Research Aims and scope Submit manuscript

Abstract

The field of regenerative medicine holds tremendous promise for the treatment of chronic diseases. While the adult mammalian heart has limited regenerative capacity, previous studies have focused on cellular therapeutic strategies in an attempt to modulate cardiac regeneration. An alternative strategy relies on the modulation of endogenous stem/progenitor cells or signaling pathways to promote cardiac regeneration. Several organisms, including the newt, have an incomparable capacity for the regeneration of differentiated tissues. An enhanced understanding of the signals, pathways, and factors that mediate the regenerative response in these organisms may be useful in modulating the regenerative response of mammalian organs including the injured adult heart.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Morgan, T. H. (1900). Regeneration in teleosts. Arch. Entwickelungsmech., 10, 120–134.

    Article  Google Scholar 

  2. Morgan, T. H. (1901). Regeneration. New York: Columbia University.

    Google Scholar 

  3. Slack, J. M. W. (2003). Regeneration research today. Dev. Dyn., 226, 162–166.

    Article  PubMed  CAS  Google Scholar 

  4. Bosch, T. C. G. (1998). In P. Ferreti & J. Geraudie (Eds.), Hydra, in cellular and molecular basis of regeneration: from invertebrates to humans (pp. 111–134). New York: Wiley.

    Google Scholar 

  5. Hata, S., Namae, M., & Nishina, H. (2007). Liver development and regeneration: from laboratory study to clinical therapy. Dev Growth Differ, 49, 163–170.

    PubMed  CAS  Google Scholar 

  6. Shi, X., & Garry, D. J. (2006). Muscle stem cells in development, regeneration, and disease. Genes Dev., 20, 1692–1708.

    Article  PubMed  CAS  Google Scholar 

  7. Sancho-Bru, P., Najimi, M., Caruso, M., Pauwelyn, K., Cantz, T., Forbes, S., et al. (2009). Stem and progenitor cells for liver repopulation: can we standardise the process from bench to bedside? Gut, 58, 594–603.

    Article  PubMed  CAS  Google Scholar 

  8. Masaki, H., & Ide, H. (2007). Regeneration potency of mouse limbs. Dev. Growth Differ., 49, 89–98.

    PubMed  Google Scholar 

  9. Brockes, J. P., & Kumar, A. (2002). Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev Mol Cell Biol, 3, 566–574.

    Article  PubMed  CAS  Google Scholar 

  10. Brockes, J. P. (1997). Amphibian limb regeneration: rebuilding a complex structure. Science, 276, 81–87.

    Article  PubMed  CAS  Google Scholar 

  11. Brockes, J. P., & Kumar, A. (2005). Appendage regeneration in adult vertebrates and implications for regenerative medicine. Science, 310, 1919–1923.

    Article  PubMed  CAS  Google Scholar 

  12. Muneoka, K., Holler-Dinsmore, G., & Bryant, S. V. (1986). Intrinsic control of regenerative loss in Xenopus laevis limbs. J Exp Zool, 240, 47–54.

    Article  PubMed  CAS  Google Scholar 

  13. Roget, J. (1963). Les Sciences de la Vie dans la Pensee Francaise du XVIIe Siecle la Generation des Animaux de Descartes a l’Encyclopedie. Paris: France.

    Google Scholar 

  14. Reai IRAF (1712) Sur les diverses reproductions que se font dans les Ecrevisse, les Omars, les Crabes, etc. et antr’autres sure celles de leurs Jambes et de leurs Ecailles. Mem Acad Roy Sci, pp 223–245

  15. Trembley A (1744) Memoires, Pour Servir a L’histoire d’un Genre de Polypes d’eau Douce, a Bras en Forme de Cornes. Leiden, Verbeek

  16. Lenhoff, S. G., & Lenhoff, H. M. (1986). Hydra and the birth of experimental biology, 1744: Abraham Trembley’s memoirs concerning the natural history of a type of freshwater polyp with arms shaped like horns. Pacific Grove, CA: Boxwoord Press.

    Google Scholar 

  17. Bonnet C (1783) Oeuvres D’histoire Naturelle et de Philosophie. Tome 3. Memoires d’histoire naturalle. Neuchatel

  18. Spallanzani L (1769) Prodromo di un opera da imprimersi sopra la riproduzioni animali. Modena (1786). English translation by Matthieu Mary (1718–1776). An essay on animal reproductions. London, UK

  19. Todd, T. J. (1823). On the process of reproduction of the members of the aquatic salamander. Q J Sci Lit Arts, 16, 84–96.

    Google Scholar 

  20. Samuels, S. (1860). Die trophischen Nerven. Leipzig: Wigand.

    Google Scholar 

  21. Frasse, P. (1885). Die Regeneration von Geweben und Organen bei den Wirbelthierer, besonders Amphibien und Reptilien. Berlin: Cassel T Fischer.

    Google Scholar 

  22. Higginbottom. (1853). Triton laevis. Ann Mag Nat Hist Ser, 12, 370.

    Google Scholar 

  23. Philippeaux, J. M. (1866). Note sur la regeneration de la rate. Comp Rend de 1' Acad de. Sciences, 576, 1058.

    Google Scholar 

  24. Barfurth Arch, F. (1895). Entwickelungsmechanik der Organismen, 1, 1–283.

    Google Scholar 

  25. Wiedersheim, R. (1875). Versuch einer Vergleichenden Anatomie der Salamandrinen mit Besonderer Berücksichtigung der Skelet-Verhaeltnisse. Genoa: Druck des Instituts der Sordo-Muti.

    Google Scholar 

  26. Eberth (1876) Epithelregeneration. Virch Arch, p 67

  27. Goette, A. (1879). Ueber Entwicklung und Regeneration des Gliedmassenskelets der Molche. Leipzig: L Voss.

    Google Scholar 

  28. Colucci, V. (1884). Intorno all rigenerazione degli art arti es della coda nei Tritoni. Studio sperimentale. Mem Ric Accad Sci Bologna Ser, 5, 501–566.

    Google Scholar 

  29. Muller, E. (1896). Uber die Regeneration der Augenlinse nach Exstirpation derselben bei Triton. Archiv für Mikroskopische Anatomie, 47, 23–33.

    Article  Google Scholar 

  30. Liversage RA (1991) Origin of blastema cells in epimorphic regeneration of urodele appendages: a history of ideas. In: C.E. Dinsmore (Ed.), A history of regeneration research. Cambridge University Press, pp. 191–199

  31. Hellmich, W. (1930). Untersuchungen uber Herkunft und Determination des regnerrativen Materiels bei Amphibien. Arch F EntwMech, 121, 135–202.

    Article  Google Scholar 

  32. Weiss, P. (1925). Abhangigkeit der Regeneration entiwickelter Amphibienextremitaten vom Nervensystem. Arch F Mik Anat, 104, 317–358.

    Google Scholar 

  33. Cameron, J. A., Hilger, A. R., & Hinterberger, T. J. (1986). Evidence that reserve cells are a source of regenerated adult newt muscle in vitro. Nature, 321, 607–610.

    Article  Google Scholar 

  34. Godlewski, E. (1928). Untersuchungen uber Auslosung und Hemmung der Regeneration beim Axolotl. Arch f EntwMech, 114, 108–143.

    Article  Google Scholar 

  35. Rose, S. M. (1948). Epidermal dedifferentiation during blastema formation in regenerating limbs of Triturus vididescens. J Exp Zool, 108, 337–361.

    Article  PubMed  CAS  Google Scholar 

  36. Singer M, Saltpeter M (1961) Regeneration in vertebrates: The role of the wound epithelium. In: Growth in living systems ed. Basic Books, New York, pp. 277-311.

  37. Campbell, L. J., & Crews, C. M. (2007). Wound epidermis formation and function in urodele amphibian limb regeneration. Cell Mol Life Sci, 65, 73–79.

    Article  CAS  Google Scholar 

  38. Butler, E. G. (1935). Studies on limb regeneration in x-rayed Amblystoma larvae. Anat Rec, 62, 95–307.

    Article  Google Scholar 

  39. Chalkley, D. T. (1954). A quantitative histological analysis of forelimb regeneration in Triturus viridescens. J Morphol, 94, 21–70.

    Article  Google Scholar 

  40. Hay, E. D., & Fischman, D. A. (1961). Origin of the blastema in regeneration limbs of the newt Triturus viridescens: an autoradiographic study using tritiated thymidine to follow cell proliferation and migration. Dev Biol, 3, 26–59.

    Article  PubMed  CAS  Google Scholar 

  41. Oberpriller, J. O., & Oberpriller, J. C. (1974). Response of the adult newt ventricle to injury. J Exp Zool, 187, 249–253.

    Article  PubMed  CAS  Google Scholar 

  42. Oberpriller, J. O., Oberpriller, J. C., Bader, D. M., & McDonnell, T. M. (1981). Cardiac muscle and its potential for regeneration in the adult newt heart. In R. O. Becker (Ed.), Mechanisms of growth control (pp. 343–372). Springfield: Charles C. Thomas.

    Google Scholar 

  43. Bader, D., & Oberpriller, J. (1979). Autoradiographic and electron microscopic studies of minced cardiac muscle regeneration in the ault newt, Notophthalamus viridescens. J Exp Zool, 208, 177–193.

    Article  PubMed  CAS  Google Scholar 

  44. Oberpriller, J. O., & Oberpriller, J. C. (1991). Cell division in adult newt cardiac myocytes. In J. O. Oberpriller, J. C. Oberpriller, & A. Mauro (Eds.), The development and regenerative potential of cardiac muscle (pp. 293–312). New York, London, Paris: Harwood Academic Press.

    Google Scholar 

  45. Oberpriller, J. O., Oberpriller, J. C., Matz, D. G., & Soonpaa, M. H. (1995). Stimulation of proliferative events in the adult amphibian cardiac myocyte. Ann New York Acad Sci, 752, 30–46.

    Article  CAS  Google Scholar 

  46. Bettencourt-Dias, M., Mittnacht, S., & Brockes, J. P. (2003). Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J Cell Sci, 116, 4001–4009.

    Article  PubMed  CAS  Google Scholar 

  47. Laube, F., Heister, M., Scholz, C., Borchardt, T., & Braun, T. (2006). Re-programming of newt cardiomyocytes is induced by tissue regeneration. J Cell Sci, 119, 4719–4729.

    Article  PubMed  CAS  Google Scholar 

  48. Brockes, J., & Kumar, A. (2005). Newts. Current Biology, 15, R42–44.

    Article  PubMed  CAS  Google Scholar 

  49. Iovine, M. K., & Johnson, S. L. (2000). Genetic analysis of isometric growth control mechanisms in the zebrafish caudal fin. Genetics, 155, 1321–1329.

    PubMed  CAS  Google Scholar 

  50. Poss, K. D., Keating, M. T., & Nechiporuk, A. (2003). Tales of regeneration in zebrafish. Dev Dyn, 226, 202–210.

    Article  PubMed  Google Scholar 

  51. Iovine, M. K. (2007). Conserved mechanisms regulate outgrowth in zebrafish fins. Nat Chem Biol, 3, 613–618.

    Article  PubMed  CAS  Google Scholar 

  52. Poleo, G., Brown, C. W., Laforest, L., & Akimenko, M. A. (2001). Cell proliferation and movement during early fin regeneration in zebrafish. Dev Dyn, 221, 380–390.

    Article  PubMed  CAS  Google Scholar 

  53. Poss, K. D., Shen, J., & Keating, M. T. (2000). Induction of lef1 during zebrafish fin regeneration. Dev Dyn, 219, 282–286.

    Article  PubMed  CAS  Google Scholar 

  54. Nechiporuk, A., & Keating, M. T. (2002). A proliferation gradient between proximal and msxb expressing distal blastema directs zebrafish fin regeneration. Development, 129, 2607–2617.

    PubMed  CAS  Google Scholar 

  55. Akimenko, M. A., Johnson, S. L., Westerfield, M., & Ekker, M. (1995). Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development, 121, 347–357.

    PubMed  CAS  Google Scholar 

  56. Geraudie, J., & Borday Birraux, V. (2003). Posterior hoxa genes expression during zebrafish bony fin ray development and regeneration suggests their involvement in scleroblast differentiation. Dev Genes Evol, 213, 182–186.

    PubMed  CAS  Google Scholar 

  57. White, J. A., Boffa, M. B., Jones, B., & Petkovich, M. (1994). A zebrafish retinoic acid receptor expressed in the regenerating caudal fin. Development, 120, 1861–1872.

    PubMed  CAS  Google Scholar 

  58. Nakatani, Y., Kawakami, A., & Kudo, A. (2007). Cellular and molecular processes of regeneration, with special emphasis on fish fins. Dev Growth Differ, 49, 145–154.

    PubMed  Google Scholar 

  59. Padhi, B. K., Joly, L., Tellis, P., Smith, A., Nanjappa, P., Chevrette, M., et al. (2004). Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev Dyn, 231, 527–541.

    Article  PubMed  CAS  Google Scholar 

  60. Schebesta, M., Lien, C. L., Engel, F. B., & Keating, M. T. (2006). Transcriptional profiling of caudal fin regeneration in zebrafish. ScientificWorldJournal, 6, 38–54.

    Article  PubMed  Google Scholar 

  61. Thatcher, E. J., Paydar, I., Anderson, K. K., & Patton, J. G. (2008). Regulation of zebrafish fin regeneration by microRNAs. Proc Natl Acad Sci, 105, 18384–18389.

    Article  PubMed  Google Scholar 

  62. Yin, V. P., Thomson, J. M., Thummel, R., Hyde, D. R., Hammond, S. M., & Poss, K. D. (2008). Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev, 22, 728–733.

    Article  PubMed  CAS  Google Scholar 

  63. Deuchar, E. M. (1975). Regeneration of the tail bud in Xenopus embryos. J Exp Zool, 192, 381–390.

    Article  PubMed  CAS  Google Scholar 

  64. Tseng, A. S., & Levin, M. (2008). Tail regeneration in Xenopus laevis as a model for understanding tissue repair. J Dent Res, 87, 806–816.

    Article  PubMed  CAS  Google Scholar 

  65. Pueyo, J. I., & Couso, J. P. (2005). Parallels between the proximal–distal development of vertebrate and arthropod appendages: homology without an ancestor? Curr Opin Genet Dev, 15, 439–446.

    Article  PubMed  CAS  Google Scholar 

  66. Shubin, N., Tabin, C., & Carroll, S. (1997). Fossils, genes and the evolution of animal limbs. Nature, 388, 639–648.

    Article  PubMed  CAS  Google Scholar 

  67. Broughton, G., II, Janis, J. E., & Attinger, C. E. (2006). The basic science of wound healing. Plast Reconstr Surg, 117, 12S–34S.

    Article  PubMed  CAS  Google Scholar 

  68. Yokoyama, H. (2008). Initiation of limb regeneration: the critical steps for regenerative capacity. Dev Growth Differ, 50, 13–22.

    Article  PubMed  CAS  Google Scholar 

  69. Kragl, M., Knapp, D., Nacu, E., Khattak, S., Maden, M., Epperlein, H. H., et al. (2009). Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature., 460, 60–65.

    Article  PubMed  CAS  Google Scholar 

  70. Sugiura, T., Taniguchi, Y., Tazaki, A., Ueno, N., Watanabe, K., & Mochii, M. (2004). Differential gene expression between the embryonic tail bud and regenerating larval tail in Xenopus laevis. Dev Growth Differ, 46, 97–105.

    Article  PubMed  CAS  Google Scholar 

  71. Tazaki, A., Kitayama, A., Terasaka, C., Watanabe, K., Ueno, N., & Mochii, M. (2005). Macroarray-based analysis of tail regeneration in Xenopus laevis larvae. Dev Dyn, 233, 1394–1404.

    Article  PubMed  CAS  Google Scholar 

  72. Laflamme, M. A., & Murry, C. E. (2005). Regenerating the heart. Nat Biotechnol, 23, 845–856.

    Article  PubMed  CAS  Google Scholar 

  73. Rubart, M., & Field, L. J. (2006). Cardiac regeneration: repopulating the heart. Annu Rev Physiol, 68, 29–49.

    Article  PubMed  CAS  Google Scholar 

  74. Srivastava, D., & Ivey, K. N. (2006). Potential of stem-cell-based therapies for heart disease. Nature, 441, 1097–1099.

    Article  PubMed  CAS  Google Scholar 

  75. Engel, F. B., Hsieh, P. C., Lee, R. T., & Keating, M. T. (2006). FGF1/p38 MAP kinase inhibitor therapy induces cardiomyocyte mitosis, reduces scarring, and rescues function after myocardial infarction. Proc Natl Acad Sci USA, 103, 15546–15551.

    Article  PubMed  CAS  Google Scholar 

  76. Orlic, D., Kajstura, J., Chimenti, S., Jakoniuk, I., Anderson, S. M., Li, B., et al. (2001). Bone marrow cells regenerate infarcted myocardium. Nature, 410, 701–705.

    Article  PubMed  CAS  Google Scholar 

  77. Laflamme, M. A., Chen, K. Y., Naumova, A. V., Muskheli, V., Fugate, J. A., Dupras, S. K., et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol, 25, 1015–1024.

    Article  PubMed  CAS  Google Scholar 

  78. Rosenzweig, A. (2006). Cardiac cell therapy—mixed results from mixed cells. N Engl J Med., 355, 1274–1277.

    Article  PubMed  CAS  Google Scholar 

  79. Poss, K. D., Wilson, L. G., & Keating, M. T. (2002). Heart regeneration in zebrafish. Science, 298, 2188–2190.

    Article  PubMed  CAS  Google Scholar 

  80. Becker, R. O., Chapin, S., & Sherry, R. (1974). Regeneration of the ventricular myocardium in amphibians. Nature, 248, 145–147.

    Article  PubMed  CAS  Google Scholar 

  81. Peterkin, T., Gibson, A., & Patient, R. (2009). Common genetic control of haemangioblast and cardiac development in zebrafish. Development., 136, 1465–1474.

    Article  PubMed  CAS  Google Scholar 

  82. Raya, A., Consiglio, A., Kawakami, Y., Rodriguez-Esteban, C., & Izpisúa-Belmonte, J. C. (2004). The zebrafish as a model of heart regeneration. Cloning Stem Cells, 6, 345–351.

    Article  PubMed  CAS  Google Scholar 

  83. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G., et al. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell., 127, 607–619.

    Article  PubMed  CAS  Google Scholar 

  84. Lien, C. L., Schebesta, M., Makino, S., Weber, G. J., & Keating, M. T. (2006). Gene expression analysis of zebrafish heart regeneration. PLoS Biol, 4, e260.

    Article  PubMed  CAS  Google Scholar 

  85. Borchardt, T., & Braun, T. (2007). Cardiovascular regeneration in non-mammalian model systems: what are the differences between newts and man? Thromb Haemost, 98, 311–318.

    PubMed  CAS  Google Scholar 

  86. Lo, D. C., Allen, F., & Brockes, J. P. (1993). Reversal of muscle differentiation during urodele limb regeneration. Proc Natl Acad Sci, 90, 7230–7234.

    Article  PubMed  CAS  Google Scholar 

  87. Tanaka, E. M., Gann, A. A., Gates, P. B., & Brockes, J. P. (1997). Newt myotubes reenter the cell cycle by phosphorylation of the retinoblastoma protein. J Cell Biol, 136, 155–165.

    Article  PubMed  CAS  Google Scholar 

  88. Soonpaa, M. H., & Field, L. J. (1998). Survey of studies examining mammalian cardiomyocyte DNA synthesis. Circ Res, 83, 15–26.

    PubMed  CAS  Google Scholar 

  89. Raya, A., Koth, C. M., Büscher, D., Kawakami, Y., Itoh, T., Raya, R. M., et al. (2003). Activation of Notch signaling pathway precedes heart regeneration in zebrafish. Proc Natl Acad Sci, 100(S1), 11889–11895.

    Article  PubMed  CAS  Google Scholar 

  90. Ferretti, P., & Géraudie, J. (1995). Retinoic acid-induced cell death in the wound epidermis of regenerating zebrafish fins. Dev Dyn, 202, 271–283.

    PubMed  CAS  Google Scholar 

  91. Wolberg, A. S., & Campbell, R. A. (2008). Thrombin generation, fibrin clot formation and hemostasis. Transfus Apher Sci, 38, 15–23.

    Article  PubMed  Google Scholar 

  92. Straube, W. L., Brockes, J. P., Drechsel, D. N., & Tanaka, E. M. (2004). Plasticity and reprogramming of differentiated cells in amphibian regeneration: partial purification of a serum factor that triggers cell cycle re-entry in differentiated muscle cells. Cloning Stem Cells, 6, 333–344.

    Article  PubMed  CAS  Google Scholar 

  93. Zeller, R., Lopez-Rios, J., & Zuniga, A. (2009). Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet, 10, 845–858.

    Article  PubMed  CAS  Google Scholar 

  94. Han, M. J., An, J. Y., & Kim, W. S. (2001). Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev Dyn, 220, 40–48.

    Article  PubMed  CAS  Google Scholar 

  95. Lin, G., & Slack, J. M. (2008). Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Dev Biol, 316, 323–335.

    Article  PubMed  CAS  Google Scholar 

  96. Beck, C. W., Christen, B., & Slack, J. M. (2003). Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell, 5, 429–439.

    Article  PubMed  CAS  Google Scholar 

  97. Han, M., Yang, X., Farrington, J. E., & Muneoka, K. (2003). Digit regeneration is regulated by Msx1 and BMP4 in fetal mice. Development, 130, 5123–5132.

    Article  PubMed  CAS  Google Scholar 

  98. Kumar, A., Velloso, C. P., Imokawa, Y., & Brockes, J. P. (2004). The regenerative plasticity of isolated urodele myofibers and its dependence on MSX1. PLoS Biol, 2, E218.

    Article  PubMed  CAS  Google Scholar 

  99. Simon, H. G., Nelson, C., Goff, D., Laufer, E., Morgan, B. A., & Tabin, C. (1995). Differential expression of myogenic regulatory genes and Msx-1 during dedifferentiation and redifferentiation of regenerating amphibian limbs. Dev Dyn, 202, 1–12.

    PubMed  CAS  Google Scholar 

  100. Odelberg, S. J. (2005). Cellular plasticity in vertebrate regeneration. Anat Rec B New Anat, 287, 25–35.

    PubMed  Google Scholar 

  101. Odelberg, S. J. (2004). Unraveling the molecular basis for regenerative cellular plasticity. PLoS Biol, 2, E232.

    Article  PubMed  CAS  Google Scholar 

  102. Forbes, S. J., Vig, P., Poulsom, R., Wright, N. A., & Alison, M. R. (2002). Adult stem cell plasticity: new pathways of tissue regeneration become visible. Clin Sci (Lond), 103, 355–369.

    CAS  Google Scholar 

  103. McGann, C. J., Odelberg, S. J., & Keating, M. T. (2001). Mammalian myotube dedifferentiation induced by newt regeneration extract. Proc Natl Acad Sci, 98, 13699–13704.

    Article  PubMed  CAS  Google Scholar 

  104. Bergmann, O., Bhardwaj, R. D., Bernard, S., Zdunek, S., Barnabé-Heider, F., Walsh, S., et al. (2009). Evidence for cardiomyocyte renewal in humans. Science., 324, 98–102.

    Article  PubMed  CAS  Google Scholar 

  105. Zhou, Q., & Melton, D. A. (2008). Extreme makeover: converting one cell into another., 3, 382–388.

    CAS  Google Scholar 

Download references

Acknowledgement

We acknowledge Ms. Cynthia Dekay for technical assistance in the preparations of the illustrations. We also thank Dr. Daniel J. Garry for useful suggestions.

Author information

Authors and Affiliations

  1. Lillehei Heart Institute, University of Minnesota, Minneapolis, MN, 55455, USA

    Bhairab N. Singh, Naoko Koyano-Nakagawa, John P. Garry & Cyprian V. Weaver

Authors
  1. Bhairab N. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naoko Koyano-Nakagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John P. Garry
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cyprian V. Weaver
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cyprian V. Weaver.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Singh, B.N., Koyano-Nakagawa, N., Garry, J.P. et al. Heart of Newt: A Recipe for Regeneration. J. of Cardiovasc. Trans. Res. 3, 397–409 (2010). https://doi.org/10.1007/s12265-010-9191-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12265-010-9191-9

Keywords

Search

Navigation