Transducing Bioelectric Signals into Epigenetic Pathways During Tadpole Tail Regeneration

Anatomical Record

Volumn 295, Issue 10, 2012, Pages 1541-1551

  Tseng, Ai Sun ^a   Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Bioelectricity; Epigenetic; Regeneration; Voltage; Xenopus

Indexed keywords

BUB1 RELATED PROTEIN; BUTYRIC ACID; HISTONE DEACETYLASE; IVERMECTIN; PROTEIN; SODIUM COUPLED MONOCARBOXYLATE TRANSPORTER; UNCLASSIFIED DRUG;

ACTION POTENTIAL; BLASTEMA; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CHROMOSOME INACTIVATION; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; ENZYME ACTIVITY; EPIGENETICS; GAP JUNCTION; HISTONE ACETYLATION; IN VIVO STUDY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TAIL; TISSUE REGENERATION; X CHROMOSOME;

ANIMALS; BIOELECTRIC ENERGY SOURCES; CATION TRANSPORT PROTEINS; EPIGENESIS, GENETIC; LARVA; LIGHT SIGNAL TRANSDUCTION; MEMBRANE POTENTIALS; REGENERATION; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 84866174537     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22495     Document Type: Review

References (96)

1. Adams DS, Masi A, Levin M. 2007. H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134: 1323-1335.
2. Adams DS, Robinson KR, Fukumoto T, Yuan S, Albertson RC, Yelick P, Kuo L, McSweeney M, Levin M. 2006. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133: 1657-1671.
3. Anderson RM, Bosch JA, Goll MG, Hesselson D, Dong PD, Shin D, Chi NC, Shin CH, Schlegel A, Halpern M, Stainier DY. 2009. Loss of Dnmt1 catalytic activity reveals multiple roles for DNA methylation during pancreas development and regeneration. Dev Biol 334: 213-223.
4. Arcangeli A. 2005. Expression and role of hERG channels in cancer cells. Novartis Found Symp 266: 225-232; discussion 232-224.
5. Arosio D, Ricci F, Marchetti L, Gualdani R, Albertazzi L, Beltram F. 2010. Simultaneous intracellular chloride and pH measurements using a GFP-based sensor. Nat Methods 7: 516-518.
6. Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K, Surani MA. 2009. Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 461: 1292-1295.
7. Barrero MJ, Izpisua Belmonte JC. 2011. Regenerating the epigenome. EMBO Rep 12: 208-215.
8. Beane WS, Morokuma J, Adams DS, Levin M. 2011. A chemical genetics approach reveals H, K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem Biol 18: 77-89.
9. Becchetti A. 2011. Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am J Physiol Cell Physiol 301: C255-C265.
10. Beck CW, Christen B, Barker D, Slack JM. 2006. Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech Dev 123: 674-688.
11. Beck CW, Christen B, Slack JM. 2003. Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell 5: 429-439.
12. Beck CW, Izpisua Belmonte JC, Christen B. 2009. Beyond early development: xenopus as an emerging model for the study of regenerative mechanisms. Dev Dyn 238: 1226-1248.
13. Beck CW, Slack JM. 1999. A developmental pathway controlling outgrowth of the Xenopus tail bud. Development 126: 1611-1620.
14. Beck CW, Slack JM. 2001. An amphibian with ambition: a new role for Xenopus in the 21st century. Genome Biol 2: REVIEWS1029.
15. Beck CW, Slack JM. 2002. Notch is required for outgrowth of the Xenopus tail bud. Int J Dev Biol 46: 255-258.
16. Beck CW, Whitman M, Slack JM. 2001. The role of BMP signaling in outgrowth and patterning of the Xenopus tail bud. Dev Biol 238: 303-314.
17. Blackiston D, Adams DS, Lemire JM, Lobikin M, Levin M. 2010. Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Dis Model Mech 4: 67-85.
18. Blackiston D, Adams DS, Lemire JM, Lobikin M, Levin M. 2011. Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Dis Models Mech 4: 67-85.
19. Blackiston DJ, McLaughlin KA, Levin M. 2009. Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8: 3519-3528.
20. Borgens RB, Vanable JW, Jr, Jaffe L. 1979. Small artificial currents enhance Xenopus limb regeneration. J Exp Zool 207: 217-226.
21. Brower V. 2011. Epigenetics: unravelling the cancer code. Nature 471: S12-13.
22. Bubenik AB, Pavlansky R. 1965. Trophic responses to trauma in growing antlers. J Exp Zool 159: 289-302.
23. Burr HS, Hovland CI. 1937. Bio-electric correlates of development in amblystoma. The Yale J Biol Med 9: 540-549.
24. Burr HS, Sinnott EW. 1944. Electrical correlates of form in cucurbit fruits. Am J Botany 31: 249-253.
25. Carneiro K, Donnet C, Rejtar T, Karger BL, Barisone GA, Diaz E, Kortagere S, Lemire JM, Levin M. 2011. Histone deacetylase activity is necessary for left-right patterning during vertebrate development. BMC Dev Biol 11: 29.
26. Contreras EG, Gaete M, Sanchez N, Carrasco H, Larrain J. 2009. Early requirement of Hyaluronan for tail regeneration in Xenopus tadpoles. Development 136: 2987-2996.
27. Costa RM, Mason J, Lee M, Amaya E, Zorn AM. 2003. Novel gene expression domains reveal early patterning of the Xenopus endoderm. Gene Exp Patterns 3: 509-519.
28. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. 2004. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42: 535-552.
29. DeSimone DW, Davidson LA, Marsden M, Alfandari D. 2005. The Xenopus embryo as a model system for studies of cell migration. In: Guan JL, editor. Cell migration. Totowa, NJ: Humana Press.
30. Dvash T, Fan G. 2009. Epigenetic regulation of X-inactivation in human embryonic stem cells. Epigenetics: Off J DNA Methyl Soc 4: 19-22.
31. Epps D, Wolfe M, Groppi V. 1994. Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1, 3-dibutylbarbituric acid)trimethine oxonol (Dibac4(3)) in model systems and cells. Chem Phys Lipids 69: 137-150.
32. Fagot D, Buquet-Fagot C, Lallemand F, Mester J. 1994. Antiproliferative effects of sodium butyrate in adriamycin-sensitive and -resistant human cancer cell lines. Anticancer Drugs 5: 548-556.
33. Franchini A, Bertolotti E. 2011. Tail regenerative capacity and iNOS immunolocalization in Xenopus laevis tadpoles. Cell Tissue Res 344: 261-269.
34. Fraser SP, Diss JK, Chioni AM, Mycielska ME, Pan H, Yamaci RF, Pani F, Siwy Z, Krasowska M, Grzywna Z, Brackenbury WJ, Theodorou D, Koyuturk M, Kaya H, Battaloglu E, De Bella MT, Slade MJ, Tolhurst R, Palmieri C, Jiang J, Latchman DS, Coombes RC, Djamgoz MB. 2005. Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin Cancer Res 11: 5381-5389.
35. Fukazawa T, Naora Y, Kunieda T, Kubo T. 2009. Suppression of the immune response potentiates tadpole tail regeneration during the refractory period. Development 136: 2323-2327.
36. Fukumoto T, Blakely R, Levin M. 2005. Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev Neurosci 27: 349-363.
37. Gargioli C, Slack JM. 2004. Cell lineage tracing during Xenopus tail regeneration. Development 131: 2669-2679.
38. Goss RJ. 1990. Interactions between asymmetric brow tines in caribou and reindeer antlers. Can J Zool 68: 1115-1119.
39. Hague A, Manning AM, Hanlon KA, Huschtscha LI, Hart D, Paraskeva C. 1993. Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer. Int J Cancer 55: 498-505.
40. Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, Cesari F, Lee C, Almouzni G, Schneider R, Surani MA. 2008. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452: 877-881.
41. Harland RM. 1991. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36: 685-695.
42. Hechavarria D, Dewilde A, Braunhut S, Levin M, Kaplan DL. 2010. BioDome regenerative sleeve for biochemical and biophysical stimulation of tissue regeneration. Med Eng Phys 32: 1065-1073.
43. Ho DM, Whitman M. 2008. TGF-beta signaling is required for multiple processes during Xenopus tail regeneration. Dev Biol 315: 203-216.
44. House CD, Vaske CJ, Schwartz AM, Obias V, Frank B, Luu T, Sarvazyan N, Irby R, Strausberg RL, Hales TG, Stuart JM, Lee NH. 2010. Voltage-gated Na+ channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res 70: 6957-6967.
45. Illingworth CM. 1974. Trapped fingers and amputated finger tips in children. J Pediatr Surg 9: 853-858.
46. Janicke RU, Sprengart ML, Wati MR, Porter AG. 1998. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360.
47. Jenkins LS, Duerstock BS, Borgens RB. 1996. Reduction of the current of injury leaving the amputation inhibits limb regeneration in the red spotted newt. Dev Biol 178: 251-262.
48. Koide T, Hayata T, Cho KW. 2005. Xenopus as a model system to study transcriptional regulatory networks. Proc Natl Acad Sci USA 102: 4943-4948.
49. 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: 60-65.
50. Kurtz I, Schrank AR. 1955. Bioelectrical properties of intact and regenerating earthworms Eisenia foetida. Physiol Zool 28: 322-330.
51. Levin M. 2007. Large-scale biophysics: ion flows and regeneration. Trends Cell Biol 17: 262-271.
52. Levin M. 2009. Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20: 543-556.
53. Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M. 2002. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111: 77-89.
54. Li H, Myeroff L, Smiraglia D, Romero MF, Pretlow TP, Kasturi L, Lutterbaugh J, Rerko RM, Casey G, Issa JP, Willis J, Willson JK, Plass C, Markowitz SD. 2003. SLC5A8, a sodium transporter, is a tumor suppressor gene silenced by methylation in human colon aberrant crypt foci and cancers. Proc Natl Acad Sci USA 100: 8412-8417.
55. Lin G, Chen Y, Slack JM. 2007. Regeneration of neural crest derivatives in the Xenopus tadpole tail. BMC Dev Biol 7: 56.
56. Lund E. 1947. Bioelectric fields and growth. Austin: University of Texas Press.
57. Lynch JW. 2009. Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56: 303-309.
58. Mandal M, Wu X, Kumar R. 1997. Bcl-2 deregulation leads to inhibition of sodium butyrate-induced apoptosis in human colorectal carcinoma cells. Carcinogenesis 18: 229-232.
59. Marsh G, Beams H. 1957. Electrical Control of morphogenesis in regenerating Dugesia tigrina. J Cell Comp Physiol 39: 191-211.
60. Marsh G, Beams HW. 1949. Electrical control of axial polarity in a regenerating annelid. Anat Record 105: 513-514.
61. McCaig CD, Rajnicek AM, Song B, Zhao M. 2005. Controlling cell behavior electrically: current views and future potential. Physiol Rev 85: 943-978.
62. McCaig CD, Song B, Rajnicek AM. 2009. Electrical dimensions in cell science. J Cell Sci 122: 4267-4276.
63. Miyauchi S, Gopal E, Fei YJ, Ganapathy V. 2004. Functional identification of SLC5A8, a tumor suppressor down-regulated in colon cancer, as a Na(+)-coupled transporter for short-chain fatty acids. J Biol Chem 279: 13293-13296.
64. Mochii M, Taniguchi Y, Shikata I. 2007. Tail regeneration in the Xenopus tadpole. Dev Growth Differ 49: 155-161.
65. Mondia JP, Levin M, Omenetto FG, Orendorff RD, Branch MR, Adams DS. 2011. Long-distance signals are required for morphogenesis of the regenerating Xenopus tadpole tail, as shown by femtosecond-laser ablation. PloS One 6: e24953.
66. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435: 1239-1243.
67. Nieukoop PD, Faber J. 1967. Normal table of xenopus laevis. Amersterdam: North-Holland Publishing Company.
68. Nogi T, Levin M. 2005. Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. Dev Biol 287: 314-335.
69. Nuccitelli R. 2003. Endogenous electric fields in embryos during development, regeneration and wound healing. Radiat Prot Dosimetry 106: 375-383.
70. Nuccitelli R, Robinson K, Jaffe L. 1986. On electrical currents in development. Bioessays 5: 292-294.
71. Okamura Y, Dixon JE. 2011. Voltage-sensing phosphatase: its molecular relationship with PTEN. Physiology (Bethesda) 26: 6-13.
72. Olivotto M, Arcangeli A, Carla M, Wanke E. 1996. Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. Bioessays 18: 495-504.
73. Oviedo NJ, Morokuma J, Walentek P, Kema IP, Gu MB, Ahn JM, Hwang JS, Gojobori T, Levin M. 2010. Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev Biol 339: 188-199.
74. Oviedo NJ, Nicolas CL, Adams DS, Levin M. 2008. Live imaging of planarian membrane potential using DiBAC4(3). Cold Spring Harb Protoc 2008:pdb.prot5055.
75. Ozkucur N, Epperlein HH, Funk RH. 2010. Ion imaging during axolotl tail regeneration in vivo. Dev Dyn 239: 2048-2057.
76. Pai VP, Aw S, Shomrat T, Lemire JM, Levin M. 2012. Transmembrane voltage potential conrols embryonic eye patterning in Xenopus laevis. Development.
77. Reid B, Song B, Zhao M. 2009. Electric currents in Xenopus tadpole tail regeneration. Dev Biol 335: 198-207.
78. Rinkevich Y, Lindau P, Ueno H, Longaker MT, Weissman IL. 2011. Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature 476: 409-413.
79. Roepke TK, Purtell K, King EC, La Perle KM, Lerner DJ, Abbott GW. 2010. Targeted deletion of Kcne2 causes gastritis cystica profunda and gastric neoplasia. PLoS One 5: e11451.
80. Sasaki M, Gonzalez-Zulueta M, Huang H, Herring WJ, Ahn S, Ginty DD, Dawson VL, Dawson TM. 2000. Dynamic regulation of neuronal NO synthase transcription by calcium influx through a CREB family transcription factor-dependent mechanism. Proc Natl Acad Sci USA 97: 8617-8622.
81. Shan Q, Haddrill JL, Lynch JW. 2001. Ivermectin, an unconventional agonist of the glycine receptor chloride channel. J Biol Chem 276: 12556-12564.
82. Shi R, Borgens RB. 1995. Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern. Dev Dyn 202: 101-114.
83. Siu D. 2004. Activity-dependent hepatocyte growth factor expression and its role in organogenesis and cancer growth suppression. Med Hypotheses 63: 62-70.
84. Sive HL GR, Harland RM. 2000. Early development of Xenopus Laevis: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
85. Stewart S, Tsun ZY, Izpisua Belmonte JC. 2009. A histone demethylase is necessary for regeneration in zebrafish. Proc Natl Acad Sci USA 106: 19889-19894.
86. Straka H, Simmers J. 2011. Xenopus laevis: an ideal experimental model for studying the developmental dynamics of neural network assembly and sensory-motor computations. Dev Neurobiol.
87. Sundelacruz S, Levin M, Kaplan DL. 2009. Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev Reports 5: 231-246.
88. Taylor SM, Jones PA. 1982. Changes in phenotypic expression in embryonic and adult cells treated with 5-azacytidine. J Cell Physiol 111: 187-194.
89. Tseng AS, Adams DS, Qiu D, Koustubhan P, Levin M. 2007. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev Biol 301: 62-69.
90. Tseng AS, Beane WS, Lemire JM, Masi A, Levin M. 2010. Induction of vertebrate regeneration by a transient sodium current. J Neurosci 30: 13192-13200.
91. Tseng AS, Carneiro K, Lemire JM, Levin M. 2011. HDAC activity is required during xenopus tail regeneration. PLoS One 6: e26382. doi:26310.21371/journal.pone.0026382.
92. Tseng AS, Levin M. 2008. Tail regeneration in Xenopus laevis as a model for understanding tissue repair. J Dent Res 87: 806-816.
93. Vandenberg LN, Morrie RD, Adams DS. 2011. V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev Dyn 240: 1889-1904.
94. Vergara MN, Del Rio-Tsonis K. 2009. Retinal regeneration in the Xenopus laevis tadpole: a new model system. Mol Vis 15: 1000-1013.
95. Waseem T, Mukhtarov M, Buldakova S, Medina I, Bregestovski P. 2010. Genetically encoded Cl-Sensor as a tool for monitoring of Cl-dependent processes in small neuronal compartments. J Neurosci Methods.
96. Yakushiji N, Suzuki M, Satoh A, Sagai T, Shiroishi T, Kobayashi H, Sasaki H, Ide H, Tamura K. 2007. Correlation between Shh expression and DNA methylation status of the limb-specific Shh enhancer region during limb regeneration in amphibians. Dev Biol 312: 171-182.