Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway

DMM Disease Models and Mechanisms

Volumn 4, Issue 1, 2011, Pages 67-85

  Blackiston, Douglas ^a,b   Adams, Dany S ^a   Lemire, Joan M ^a   Lobikin, Maria ^a   Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

^b FORSYTH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE RECEPTOR; METALLOPROTEINASE; SEROTONIN; SEROTONIN TRANSPORTER;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL POPULATION; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; EMBRYONIC STEM CELL; FACE; HEART; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOCYTE; MOLECULAR GENETICS; MORPHOGENESIS; NEURAL CREST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL; XENOPUS LAEVIS;

ANIMALS; CELL COUNT; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELL TRANSFORMATION, NEOPLASTIC; CHLORIDES; CHORISTOMA; EPIDERMIS; GENE EXPRESSION REGULATION; HUMANS; HYPERPIGMENTATION; ION CHANNEL GATING; IVERMECTIN; MELANOCYTES; MELANOMA; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; RECEPTORS, GLYCINE; RNA, MESSENGER; SEROTONIN; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 78650908705     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.005561     Document Type: Article

References (194)

1. Aberg, P., Geladi, P., Nicander, I., Hansson, J., Holmgren, U. and Ollmar, S. (2005). Non-invasive and microinvasive electrical impedance spectra of skin cancer-a comparison between two techniques. Skin Res. Technol. 11, 281-286. (Pubitemid 41614686)
2. Adams, D. S. (2008). A new tool for tissue engineers: ions as regulators of morphogenesis during development and regeneration. Tissue Eng. Part A 14, 1461-1468.
3. Adams, D. S. and Levin, M. (2006a). Inverse drug screens: a rapid and inexpensive method for implicating molecular targets. Genesis 44, 530-540.
4. Adams, D. S. and Levin, M. (2006b). Strategies and techniques for investigation of biophysical signals in patterning. In Analysis of Growth Factor Signaling in Embryos (ed. M. Whitman and A. K. Sater), pp. 177-262. Taylor and Francis Books.
5. +-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133, 1657-1671.
6. Adams, D. S., Masi, A. and 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. (Pubitemid 46706039)
7. Adams, S. V. and DeFelice, L. J. (2002). Flux coupling in the human serotonin transporter. Biophys. J. 83, 3268-3282.
8. Al-Hajj, M., Becker, M. W., Wicha, M., Weissman, I. and Clarke, M. F. (2004). Therapeutic implications of cancer stem cells. Curr. Opin. Genet. Dev. 14, 43-47.
9. Anderson, K. L. and Woodruff, R. I. (2001). A gap junctionally transmitted epithelial cell signal regulates endocytic yolk uptake in Oncopeltus fasciatus. Dev. Biol. 239, 68-78.
10. Arcangeli, A. (2005). Expression and role of hERG channels in cancer cells. Novartis Found. Symp. 266, 225-232; discussion 232-234.
11. Arcangeli, A., Crociani, O., Lastraioli, E., Masi, A., Pillozzi, S. and Becchetti, A. (2009). Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr. Med. Chem. 16, 66-93.
12. Asai, R., Taguchi, E., Kume, Y., Saito, M. and Kondo, S. (1999). Zebrafish leopard gene as a component of the putative reaction-diffusion system. Mech. Dev. 89, 87-92. (Pubitemid 29528277)
13. Aw, S., Adams, D. S., Qiu, D. and Levin, M. (2008). H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech. Dev. 125, 353-372.
14. Barlow, A. J., Wallace, A. S., Thapar, N. and Burns, A. J. (2008). Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135, 1681-1691. (Pubitemid 351895497)
15. Baylin, S. B. and Ohm, J. E. (2006). Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 6, 107-116.
16. Beckstead, M. J., Phelan, R., Trudell, J. R., Bianchini, M. J. and Mihic, S. J. (2002). Anesthetic and ethanol effects on spontaneously opening glycine receptor channels. J. Neurochem. 82, 1343-1351.
17. + channels confer invasive properties on human prostate cancer cells. Pflugers Arch. 447, 908-914.
18. Bergstrom, C. S., Saunders, R. A., Hutchinson, A. K. and Lambert, S. R. (2005). Iris hypoplasia and aorticopulmonary septal defect: a neurocristopathy. J. AAPOS 9, 264-267.
19. Biagiotti, T., D'Amico, M., Marzi, I., Di Gennaro, P., Arcangeli, A., Wanke, E. and Olivotto, M. (2006). Cell renewing in neuroblastoma: electrophysiological and immunocytochemical characterization of stem cells and derivatives. Stem Cells 24, 443-453.
20. Binggeli, R. and Weinstein, R. (1986). Membrane potentials and sodium channels: hypotheses for growth regulation and cancer formation based on changes in sodium channels and gap junctions. J. Theor. Biol. 123, 377-401.
21. Bissell, M. J. and Labarge, M. A. (2005). Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7, 17-23.
22. Bjerkvig, R., Tysnes, B. B., Aboody, K. S., Najbauer, J. and Terzis, A. J. (2005). Opinion: the origin of the cancer stem cell: current controversies and new insights. Nat. Rev. Cancer 5, 899-904.
23. Blackiston, D. J., McLaughlin, K. A. and Levin, M. (2009). Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8, 3519-3528.
24. Bolande, R. P. (1997). Neurocristopathy: its growth and development in 20 years. Pediatr. Pathol. Lab. Med. 17, 1-25.
25. Borgens, R. and Metcalf, M. (1994). Weak applied voltages interfere with amphibian morphogenesis and pattern. J. Exp. Zool. 268, 323-338.
26. Borgens, R., Robinson, K., Vanable, J. and McGinnis, M. (1989). Electric Fields in Vertebrate Repair. New York: Alan R. Liss.
27. Brooks, R. A. and Woodruff, R. I. (2004). Calmodulin transmitted through gap junctions stimulates endocytic incorporation of yolk precursors in insect oocytes. Dev. Biol. 271, 339-349.
28. Bulic-Jakus, F., Ulamec, M., Vlahovic, M., Sincic, N., Katusic, A., Juric-Lekc, G., Serman, L., Kruslin, B. and Belicza, M. (2006). Of mice and men: teratomas and teratocarcinomas. Coll. Antropol. 30, 921-924.
29. Cai, J., Cheng, A., Luo, Y., Lu, C., Mattson, M. P., Rao, M. S. and Furukawa, K. (2004). Membrane properties of rat embryonic multipotent neural stem cells. J. Neurochem. 88, 212-226. (Pubitemid 38030224)
30. Cardone, R. A., Casavola, V. and Reshkin, S. J. (2005). The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat. Rev. Cancer 5, 786-795.
31. Carr, J. A., Saland, L. C., Samora, A., Benavidez, S. and Krobert, K. (1991). In vivo effects of serotonergic agents on alpha-melanocyte-stimulating hormone secretion. Neuroendocrinology 54, 616-622.
32. Chakraborty, C., Nandi, S. S., Sinha, S. and Gera, V. K. (2006). Zebrafish caspase-3: molecular cloning, characterization, crystallization and phylogenetic analysis. Protein Pept. Lett. 13, 633-640.
33. Cho, T., Bae, J. H., Choi, H. B., Kim, S. S., McLarnon, J. G., Suh-Kim, H., Kim, S. U. and Min, C. K. (2002). Human neural stem cells: electrophysiological properties of voltage-gated ion channels. NeuroReport 13, 1447-1452.
34. Collazo, A., Bronner-Fraser, M. and Fraser, S. E. (1993). Vital dye labelling of Xenopus laevis trunk neural crest reveals multipotency and novel pathways of migration. Development 118, 363-376.
35. Cone, C. D. and Cone, C. M. (1976). Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192, 155-158.
36. Cone, C. D. and Tongier, M. (1971). Control of somatic cell mitosis by simulated changes in the transmembrane potential level. Oncology 25, 168-182.
37. Cooper, C. D. and Raible, D. W. (2009). Mechanisms for reaching the differentiated state: Insights from neural crest-derived melanocytes. Semin. Cell Dev. Biol. 20, 105-110.
38. Crane, J. F. and Trainor, P. A. (2006). Neural crest stem and progenitor cells. Annu. Rev. Cell Dev. Biol. 22, 267-286.
39. Cruse, G., Duffy, S. M., Brightling, C. E. and Bradding, P. (2006). Functional KCa3.1 K+ channels are required for human lung mast cell migration. Thorax 61, 880-885.
40. Davies, D. L., Trudell, J. R., Mihic, S. J., Crawford, D. K. and Alkana, R. L. (2003). Ethanol potentiation of glycine receptors expressed in Xenopus oocytes antagonized by increased atmospheric pressure. Alcohol. Clin. Exp. Res. 27, 743-755.
41. De Schepper, S., Boucneau, J., Lambert, J., Messiaen, L. and Naeyaert, J. M. (2005). Pigment cell-related manifestations in neurofibromatosis type 1, an overview. Pigment Cell Res. 18, 13-24.
42. Diss, J. K., Stewart, D., Pani, F., Foster, C. S., Walker, M. M., Patel, A. and Djamgoz, M. B. (2005). A potential novel marker for human prostate cancer: voltage-gated sodium channel expression in vivo. Prostate Cancer Prostatic Dis. 8, 266-273.
43. Domen, J. and Weissman, I. L. (2000). Hematopoietic stem cells need two signals to prevent apoptosis; BCL-2 can provide one of these, Kitl/c-Kit signaling the other. J. Exp. Med. 192, 1707-1718.
44. Domen, J., Gandy, K. L. and Weissman, I. L. (1998). Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 91, 2272-2282.
45. Ducasse, M. and Brown, M. A. (2006). Epigenetic aberrations and cancer. Mol. Cancer 5, 60.
46. Dumas, D. and Stoltz, J. F. (2005). New tool to monitor membrane potential by FRET Voltage Sensitive Dye (FRET-VSD) using Spectral and Fluorescence Lifetime Imaging Microscopy (FLIM). Interest in cell engineering. Clin. Hemorheol. Microcirc. 33, 293-302.
47. Fanburg, B. and Lee, S. (1997). A new role for an old molecule: serotonin as a mitogen. Am. J. Physiol. 272, L795-L806.
48. Fang, D., Nguyen, T. K., Leishear, K., Finko, R., Kulp, A. N., Hotz, S., Van Belle, P. A., Xu, X., Elder, D. E. and Herlyn, M. (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65, 9328-9337. (Pubitemid 41508000)
49. Finbow, M. E., Harrison, M. and Jones, P. (1995). Ductin-a proton pump component, a gap junction channel and a neurotransmitter release channel. BioEssays 17, 247-255.
50. Frankfurt, O. S. (1990). Decreased stability of DNA in cells treated with alkylating agents. Exp. Cell Res. 191, 181-185.
51. Fraser, S. P., Grimes, J. A. and Djamgoz, M. B. (2000). Effects of voltage-gated ion channel modulators on rat prostatic cancer cell proliferation: comparison of strongly and weakly metastatic cell lines. Prostate 44, 61-76.
52. Fraser, S. P., Diss, J. K., Chioni, A. M., Mycielska, M. E., Pan, H., Yamaci, R. F., Pani, F., Siwy, Z., Krasowska, M., Grzywna, Z. et al. (2005). Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin. Cancer Res. 11, 5381-5389. (Pubitemid 41060811)
53. Fuchs, S. and Sommer, L. (2007). The neural crest: understanding stem cell function in development and disease. Neurodegen. Dis. 4, 6-12.
54. Fukumoto, T., Blakely, R. and Levin, M. (2005a). Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev. Neurosci. 27, 349-363. (Pubitemid 41567384)
55. Fukumoto, T., Kema, I. P. and Levin, M. (2005b). Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr. Biol. 15, 794-803. (Pubitemid 40689397)
56. Fukuzawa, T. and Ide, H. (1983). Proliferation in vitro of melanophores from Xenopus laevis. J. Exp. Zool. 226, 239-244.
57. Gersdorff Korsgaard, M. P., Christophersen, P., Ahring, P. K. and Olesen, S. P. (2001). Identification of a novel voltage-gated Na+ channel rNa(v)1.5a in the rat hippocampal progenitor stem cell line HiB5. Pflugers Arch. 443, 18-30.
58. Gillespie, J. I. (1983). The distribution of small ions during the early development of Xenopus laevis and Ambystoma mexicanum embryos. J. Physiol. 344, 359-377.
59. Gonzalez, C. (2007). Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat. Rev. Genet. 8, 462-472.
60. Grahn, J. C., Reilly, D. A., Nuccitelli, R. L. and Isseroff, R. R. (2003). Melanocytes do not migrate directionally in physiological DC electric fields. Wound Repair Regen. 11, 64-70.
61. Gupta, D., Lis, C. G., Dahlk, S. L., Vashi, P. G., Grutsch, J. F. and Lammersfeld, C. A. (2004). Bioelectrical impedance phase angle as a prognostic indicator in advanced pancreatic cancer. Br. J. Nutr. 92, 957-962.
62. Haass, N. K. and Herlyn, M. (2005). Normal human melanocyte homeostasis as a paradigm for understanding melanoma. J. Investig. Dermatol. Symp. Proc. 10, 153-163.
63. Haass, N. K., Smalley, K. S., Li, L. and Herlyn, M. (2005). Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res. 18, 150-159.
64. Harland, R. (1991). In situ hybridization: an improved whole mount method for Xenopus embryos. In Xenopus laevis: Practical Uses in Cell and Molecular Biology, Vol. 36 (ed. B. Kay and H. Peng), pp. 685-695. San Diego: Academic Press.
65. Heath, E. I. and Grochow, L. B. (2000). Clinical potential of matrix metalloprotease inhibitors in cancer therapy. Drugs 59, 1043-1055.
66. Hendrix, M. J., Seftor, E. A., Seftor, R. E., Kasemeier-Kulesa, J., Kulesa, P. M. and Postovit, L. M. (2007). Reprogramming metastatic tumour cells with embryonic microenvironments. Nat. Rev. Cancer 7, 246-255.
67. Hess, A. R., Margaryan, N. V., Seftor, E. A. and Hendrix, M. J. (2007). Deciphering the signaling events that promote melanoma tumor cell vasculogenic mimicry and their link to embryonic vasculogenesis: role of the Eph receptors. Dev. Dyn. 236, 3283-3296.
68. Heubach, J. F., Graf, E. M., Leutheuser, J., Bock, M., Balana, B., Zahanich, I., Christ, T., Boxberger, S., Wettwer, E. and Ravens, U. (2004). Electrophysiological properties of human mesenchymal stem cells. J. Physiol. 554, 659-672. (Pubitemid 38219882)
69. Heukelbach, J., Winter, B., Wilcke, T., Muehlen, M., Albrecht, S., de Oliveira, F. A., Kerr-Pontes, L. R., Liesenfeld, O. and Feldmeier, H. (2004). Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull. World Health Organ. 82, 563-571.
70. Higashimori, H. and Sontheimer, H. (2007). Role of Kir4.1 channels in growth control of glia. GLIA 55, 1668-1679.
71. Hilber, B., Scholze, P., Dorostkar, M. M., Sandtner, W., Holy, M., Boehm, S., Singer, E. A. and Sitte, H. H. (2005). Serotonin-transporter mediated efflux: a pharmacological analysis of amphetamines and non-amphetamines. Neuropharmacology 49, 811-819.
72. Hong, D., Gupta, R., Ancliff, P., Atzberger, A., Brown, J., Soneji, S., Green, J., Colman, S., Piacibello, W., Buckle, V. et al. (2008). Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 319, 336-339.
73. + channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res. 70, 6957-6967.
74. Ingber, D. E. (2008). Can cancer be reversed by engineering the tumor microenvironment? Semin. Cancer Biol. 18, 356-364.
75. Ingber, D. E. and Levin, M. (2007). What lies at the interface of regenerative medicine and developmental biology? Development 134, 2541-2547.
76. Inoue, K., Ohyama, T., Sakuragi, Y., Yamamoto, R., Inoue, N. A., Li-Hua, Y., Goto, Y. I., Wegner, M. and Lupski, J. R. (2007). Translation of SOX10 3′ untranslated region causes a complex severe neurocristopathy by generation of a deleterious functional domain. Hum. Mol. Genet. 16, 3037-3046.
77. Isseroff, R., Grahn, J., Reilly, D. and Nuccitelli, R. (2001). Melanocytes do not exhibit directional migration in a DC electric field. J. Investig. Dermatol. 117, 556.
78. Iwashita, M., Watanabe, M., Ishii, M., Chen, T., Johnson, S. L., Kurachi, Y., Okada, N. and Kondo, S. (2006). Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: implications for the regulation of melanosome movement. PLoS Genet. 2, e197.
79. Iyengar, B. (1998). Photomodulation of the melanocyte cell cycle by indoleamines. Biol. Signals Recept. 7, 345-350.
80. Jaffe, L. (1982). Developmental currents, voltages, and gradients. In Developmental Order: its Origin and Regulation (ed. S. Subtelny), pp. 183-215. New York: Alan R Liss.
81. Jaffe, L. F. (2003). Epigenetic theories of cancer initiation. Adv. Cancer Res. 90, 209-230.
82. Jeon, S., Kim, N. H., Koo, B. S., Lee, H. J. and Lee, A. Y. (2007). Bee venom stimulates human melanocyte proliferation, melanogenesis, dendricity and migration. Exp. Mol. Med. 39, 603-613.
83. +-activated membrane K+ current and migration of MDCK II cells. J. Membr. Biol. 191, 77-86.
84. Kasemeier-Kulesa, J. C., Teddy, J. M., Postovit, L. M., Seftor, E. A., Seftor, R. E., Hendrix, M. J. and Kulesa, P. M. (2008). Reprogramming multipotent tumor cells with the embryonic neural crest microenvironment. Dev. Dyn. 237, 2657-2666.
85. Kelsh, R. N., Schmid, B. and Eisen, J. S. (2000). Genetic analysis of melanophore development in zebrafish embryos. Dev. Biol. 225, 277-293.
86. Kim, C. F. and Dirks, P. B. (2008). Cancer and stem cell biology: how tightly intertwined? Cell Stem Cell 3, 147-150.
87. Konig, S., Hinard, V., Arnaudeau, S., Holzer, N., Potter, G., Bader, C. R. and Bernheim, L. (2004). Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation. J. Biol. Chem. 279, 28187-28196. (Pubitemid 38900094)
88. Kraft, R., Krause, P., Jung, S., Basrai, D., Liebmann, L., Bolz, J. and Patt, S. (2003). BK channel openers inhibit migration of human glioma cells. Pflugers Arch. 446, 248-255.
89. Kucheryavykh, Y. V., Kucheryavykh, L. Y., Nichols, C. G., Maldonado, H. M., Baksi, K., Reichenbach, A., Skatchkov, S. N. and Eaton, M. J. (2007). Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55, 274-281.
90. Kulesa, P. M., Kasemeier-Kulesa, J. C., Teddy, J. M., Margaryan, N. V., Seftor, E. A., Seftor, R. E. and Hendrix, M. J. (2006). Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment. Proc. Natl. Acad. Sci. USA 103, 3752-3757.
91. Kumasaka, M., Sato, S., Yajima, I. and Yamamoto, H. (2003). Isolation and developmental expression of tyrosinase family genes in Xenopus laevis. Pigment Cell Res. 16, 455-462.
92. Kumasaka, M., Sato, H., Sato, S., Yajima, I. and Yamamoto, H. (2004). Isolation and developmental expression of Mitf in Xenopus laevis. Dev. Dyn. 230, 107-113.
93. Kumasaka, M., Sato, S., Yajima, I., Goding, C. R. and Yamamoto, H. (2005). Regulation of melanoblast and retinal pigment epithelium development by Xenopus laevis Mitf. Dev. Dyn. 234, 523-534.
94. Kunzelmann, K. (2005). Ion channels and cancer. J. Membr. Biol. 205, 159-173.
95. Kuriyama, S. and Mayor, R. (2008). Molecular analysis of neural crest migration. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363, 1349-1362.
96. Kyrgidis, A., Tzellos, T. G. and Triaridis, S. (2010). Melanoma: Stem cells, sun exposure and hallmarks for carcinogenesis, molecular concepts and future clinical implications. J. Carcinog. 9, 3.
97. Lastraioli, E., Guasti, L., Crociani, O., Polvani, S., Hofmann, G., Witchel, H., Bencini, L., Calistri, M., Messerini, L., Scatizzi, M. et al. (2004). herg1 gene and HERG1 protein are overexpressed in colorectal cancers and regulate cell invasion of tumor cells. Cancer Res. 64, 606-611.
98. Lee, L. M., Seftor, E. A., Bonde, G., Cornell, R. A. and Hendrix, M. J. (2005). The fate of human malignant melanoma cells transplanted into zebrafish embryos: assessment of migration and cell division in the absence of tumor formation. Dev. Dyn. 233, 1560-1570. (Pubitemid 40995154)
99. Lee, M. and Vasioukhin, V. (2008). Cell polarity and cancer-cell and tissue polarity as a non-canonical tumor suppressor. J. Cell Sci. 121, 1141-1150.
100. Lerchner, W., Xiao, C., Nashmi, R., Slimko, E. M., van Trigt, L., Lester, H. A. and Anderson, D. J. (2007). Reversible silencing of neuronal excitability in behaving mice by a genetically targeted, ivermectin-gated Cl- channel. Neuron 54, 35-49.
101. Levens, D. (1990). Development and cancer: common themes? Lab. Invest. 63, 429-431.
102. Levin, M. (2004). A novel immunohistochemical method for evaluation of antibody specificity and detection of labile targets in biological tissue. J. Biochem. Biophys. Methods 58, 85-96.
103. Levin, M. (2007). Large-scale biophysics: ion flows and regeneration. Trends Cell Biol. 17, 262-271.
104. Levin, M. (2009a). Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin. Cell Dev. Biol. 20, 543-556.
105. Levin, M. (2009b). Errors of geometry: regeneration in a broader perspective. Semin. Cell Dev. Biol. 20, 643-645.
106. Levin, M. and Mercola, M. (1998). Gap junctions are involved in the early generation of left-right asymmetry. Dev. Biol. 203, 90-105.
107. Levin, M., Buznikov, G. A. and Lauder, J. M. (2006). Of minds and embryos: left-right asymmetry and the serotonergic controls of pre-neural morphogenesis. Dev. Neurosci. 28, 171-185.
108. Li, C., Zhong, H., Wang, Y., Wang, H., Yang, Z., Zheng, Y., Liu, K. and Liu, Y. (2006). Voltage and ionic regulation of human serotonin transporter in Xenopus oocytes. Clin. Exp. Pharmacol. Physiol. 33, 1088-1092.
109. Lindvall, C., Bu, W., Williams, B. O. and Li, Y. (2007). Wnt signaling, stem cells, and the cellular origin of breast cancer. Stem Cell Rev. 3, 157-168.
110. Liu, L. Y., Hu, C. L., Ma, L. J., Zhang, Z. H. and Mei, Y. A. (2004). ET-1 inhibits B-16 murine melanoma cell migration by decreasing K(+) currents. Cell Motil. Cytoskeleton 58, 127-136.
111. Liu, L. Y., Hoffman, G. E., Fei, X. W., Li, Z., Zhang, Z. H. and Mei, Y. A. (2007). Delayed rectifier outward K+ current mediates the migration of rat cerebellar granule cells stimulated by melatonin. J. Neurochem. 102, 333-344.
112. Lotti, T., Gori, A., Zanieri, F., Colucci, R. and Moretti, S. (2008). Vitiligo: new and emerging treatments. Dermatol. Ther. 21, 110-117.
113. Lund, E. (1947). Bioelectric fields and growth. Austin: Univ. of Texas Press.
114. Lynch, J. W. (2009). Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56, 303-309.
115. Macmillan, G. J. (1976). Melanoblast-tissue interactions and the development of pigment pattern in Xenopus larvae. J. Embryol. Exp. Morphol. 35, 463-484.
116. Makino, S., Whitehead, G. G., Lien, C. L., Kim, S., Jhawar, P., Kono, A., Kawata, Y. and Keating, M. T. (2005). Heat-shock protein 60 is required for blastema formation and maintenance during regeneration. Proc. Natl. Acad. Sci. USA 102, 14599-14604.
117. Maniotis, A. J., Folberg, R., Hess, A., Seftor, E. A., Gardner, L. M., Pe'er, J., Trent, J. M., Meltzer, P. S. and Hendrix, M. J. (1999). Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 155, 739-752.
118. McCaig, C. D., Rajnicek, A. M., Song, B. and Zhao, M. (2005). Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 85, 943-978.
119. McCaig, C. D., Song, B. and Rajnicek, A. M. (2009). Electrical dimensions in cell science. J. Cell Sci. 122, 4267-4276.
120. 2+ channels participate in regulating neural crest migration and differentiation. Am. J. Anat. 192, 14-22.
121. Morokuma, J., Blackiston, D., Adams, D. S., Seebohm, G., Trimmer, B. and Levin, M. (2008). Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc. Natl. Acad. Sci. USA 105, 16608-16613.
122. Mu, D., Chen, L., Zhang, X., See, L. H., Koch, C. M., Yen, C., Tong, J. J., Spiegel, L., Nguyen, K. C., Servoss, A. et al. (2003). Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene. Cancer Cell 3, 297-302.
123. 2+ entry: a way to control cell proliferation. Curr. Med. Chem. 11, 1533-1543.
124. Munaron, L., Antoniotti, S. and Lovisolo, D. (2004b). Intracellular calcium signals and control of cell proliferation: how many mechanisms? J. Cell Mol. Med. 8, 161-168. (Pubitemid 44145505)
125. Nebigil, C. G., Launay, J. M., Hickel, P., Tournois, C. and Maroteaux, L. (2000). 5-hydroxytryptamine 2B receptor regulates cell-cycle progression: cross-talk with tyrosine kinase pathways. Proc. Natl. Acad. Sci. USA 97, 2591-2596.
126. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company.
127. Nishiyama, M., von Schimmelmann, M. J., Togashi, K., Findley, W. M. and Hong, K. (2008). Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat. Neurosci. 11, 762-771.
128. Nozue, A. T. and Ono, S. (1991). Effects of catecholamine and serotonin in central nervous system in newborn mice with special reference to neural crest cells; presumptive evidence of neural crest origin. Anatomischer. Anzeiger. 173, 147-153.
129. Nuccitelli, R., Robinson, K. and Jaffe, L. (1986). On electrical currents in development. BioEssays 5, 292-294.
130. Olivotto, M., Arcangeli, A., Carla, M. and Wanke, E. (1996). Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. BioEssays 18, 495-504.
131. Ottesen, E. A. and Campbell, W. C. (1994). Ivermectin in human medicine. J. Antimicrob. Chemother. 34, 195-203.
132. + channel expression in human breast cancer cells: involvement in cell cycle regulation and carcinogenesis. J. Membr. Biol. 221, 1-6.
133. Ouwerkerk, R., Jacobs, M. A., Macura, K. J., Wolff, A. C., Stearns, V., Mezban, S. D., Khouri, N. F., Bluemke, D. A. and Bottomley, P. A. (2007). Elevated tissue sodium concentration in malignant breast lesions detected with non-invasive 23Na MRI. Breast Cancer Res. Treat. 106, 151-160.
134. Oviedo, N. J. and Beane, W. S. (2009). Regeneration: the origin of cancer or a possible cure? Semin. Cell Dev. Biol. 20, 557-564.
135. Pardo, L. A., del Camino, D., Sanchez, A., Alves, F., Bruggemann, A., Beckh, S. and Stuhmer, W. (1999). Oncogenic potential of EAG K(+) channels. EMBO J. 18, 5540-5547.
136. Park, P. C., Selvarajah, S., Bayani, J., Zielenska, M. and Squire, J. A. (2007). Stem cell enrichment approaches. Semin. Cancer Biol. 17, 257-264.
137. Pfeifer, A. and Verma, I. M. (2001). Gene therapy: promises and problems. Annu. Rev. Genomics Hum. Genet. 2, 177-211.
138. Pogge v Strandmann, E., Senkel, S. and Ryffel, G. U. (2000). Ectopic pigmentation in Xenopus in response to DCoH/PCD, the cofactor of HNF1 transcription factor/pterin-4alpha-carbinolamine dehydratase. Mech. Dev. 91, 53-60.
139. Potier, M., Joulin, V., Roger, S., Besson, P., Jourdan, M. L., Leguennec, J. Y., Bougnoux, P. and Vandier, C. (2006). Identification of SK3 channel as a new mediator of breast cancer cell migration. Mol. Cancer Ther. 5, 2946-2953.
140. Prevarskaya, N., Zhang, L. and Barritt, G. (2007). TRP channels in cancer. Biochim. Biophys. Acta 1772, 937-946.
141. Pullar, C. E., Baier, B. S., Kariya, Y., Russell, A. J., Horst, B. A., Marinkovich, M. P. and Isseroff, R. R. (2006). beta4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1. Mol. Biol. Cell 17, 4925-4935.
142. Rajnicek, A. M., Foubister, L. E. and McCaig, C. D. (2006). Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry. J. Cell Sci. 119, 1736-1745.
143. Reid, B., Nuccitelli, R. and Zhao, M. (2007). Non-invasive measurement of bioelectric currents with a vibrating probe. Nat. Protoc. 2, 661-669.
144. Reya, T., Morrison, S. J., Clarke, M. F. and Weissman, I. L. (2001). Stem cells, cancer, and cancer stem cells. Nature 414, 105-111.
145. Robinson, K. R. and Messerli, M. A. (1996). Electric embryos: the embryonic epithelium as a generator of developmental information. In Nerve Growth and Guidance (ed. C. D. McCaig), pp. 131-150. London: Portland Press.
146. Rubin, H. (1985). Cancer as a dynamic developmental disorder. Cancer Res. 45, 2935-2942.
147. Rubin, H. (1990). The significance of biological heterogeneity. Cancer and Metastasis Rev. 9, 1-20.
148. Saka, Y. and Smith, J. C. (2001). Spatial and temporal patterns of cell division during early Xenopus embryogenesis. Dev. Biol. 229, 307-318.
149. Sanchez Alvarado, A. (2003). The freshwater planarian Schmidtea mediterranea: embryogenesis, stem cells and regeneration. Curr. Opin. Genet. Dev. 13, 438-444.
150. Sauka-Spengler, T. and Bronner-Fraser, M. (2008). A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568. (Pubitemid 351881841)
151. Schlosser, G., Awtry, T., Brugmann, S. A., Jensen, E. D., Neilson, K., Ruan, G., Stammler, A., Voelker, D., Yan, B., Zhang, C. et al. (2008). Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. Dev. Biol. 320, 199-214.
152. Schwab, A., Reinhardt, J., Schneider, S. W., Gassner, B. and Schuricht, B. (1999). K(+) channel-dependent migration of fibroblasts and human melanoma cells. Cell Physiol. Biochem. 9, 126-132.
153. + channel in primary neuronal cultures. J. Biol. Chem. 259, 1491-1495.
154. Shan, Q., Haddrill, J. L. and Lynch, J. W. (2001). Ivermectin, an unconventional agonist of the glycine receptor chloride channel. J. Biol. Chem. 276, 12556-12564.
155. Sive, H. L., Grainger, R. M. and Harland, R. M. (2000). Early Development of Xenopus Laevis. New York: Cold Spring Harbor Laboratory Press.
156. Slominski, A., Tobin, D. J., Shibahara, S. and Wortsman, J. (2004). Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 84, 1155-1228.
157. Slominski, A., Wortsman, J. and Tobin, D. J. (2005). The cutaneous serotoninergic/melatoninergic system: securing a place under the sun. FASEB J. 19, 176-194.
158. Song, B., Gu, Y., Pu, J., Reid, B., Zhao, Z. and Zhao, M. (2007). Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo. Nat. Protoc. 2, 1479-1489.
159. Soto, A. M. and Sonnenschein, C. (2004). The somatic mutation theory of cancer: growing problems with the paradigm? BioEssays 26, 1097-1107.
160. + channels support proliferation of colonic carcinoma cells. FASEB J. 21, 35-44.
161. Stahelin, B. J., Marti, U., Solioz, M., Zimmermann, H. and Reichen, J. (1998). False positive staining in the TUNEL assay to detect apoptosis in liver and intestine is caused by endogenous nucleases and inhibited by diethyl pyrocarbonate. Mol. Pathol. 51, 204-208.
162. Stulberg, D. L., Clark, N. and Tovey, D. (2003). Common hyperpigmentation disorders in adults: Part II. Melanoma, seborrheic keratoses, acanthosis nigricans, melasma, diabetic dermopathy, tinea versicolor, and postinflammatory hyperpigmentation. Am. Fam. Physician 68, 1963-1968.
163. Stump, R. F. and Robinson, K. R. (1983). Xenopus neural crest cell migration in an applied electrical field. J. Cell Biol. 97, 1226-1233.
164. Sun, W., Buzanska, L., Domanska-Janik, K., Salvi, R. J. and Stachowiak, M. K. (2005). Voltage-sensitive and ligand-gated channels in differentiating neural stem-like cells derived from the nonhematopoietic fraction of human umbilical cord blood. Stem Cells 23, 931-945.
165. Sundelacruz, S., Levin, M. and Kaplan, D. L. (2008). Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS ONE 3, e3737.
166. Sundelacruz, S., Levin, M. and Kaplan, D. L. (2009). Role of membrane potential in the regulation of cell proliferation and differentiation. Stem. Cell Rev. Rep. 5, 231-246.
167. Taipale, J. and Beachy, P. A. (2001). The Hedgehog and Wnt signalling pathways in cancer. Nature 411, 349-354.
168. Tan, B. T., Park, C. Y., Ailles, L. E. and Weissman, I. L. (2006). The cancer stem cell hypothesis: a work in progress. Lab. Invest. 86, 1203-1207.
169. Tang, Y. B., Liu, Y. J., Zhou, J. G., Wang, G. L., Qiu, Q. Y. and Guan, Y. Y. (2008). Silence of ClC-3 chloride channel inhibits cell proliferation and the cell cycle via G/S phase arrest in rat basilar arterial smooth muscle cells. Cell Prolif. 41, 775-785.
170. Tataria, M., Perryman, S. V. and Sylvester, K. G. (2006). Stem cells: tissue regeneration and cancer. Semin. Pediatr. Surg. 15, 284-292.
171. Thomas, C. E., Ehrhardt, A. and Kay, M. A. (2003). Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 4, 346-358.
172. Tomlinson, M. L., Garcia-Morales, C., Abu-Elmagd, M. and Wheeler, G. N. (2008). Three matrix metalloproteinases are required in vivo for macrophage migration during embryonic development. Mech. Dev. 125, 1059-1070.
173. Tomlinson, M. L., Guan, P., Morris, R. J., Fidock, M. D., Rejzek, M., Garcia-Morales, C., Field, R. A. and Wheeler, G. N. (2009a). A chemical genomic approach identifies matrix metalloproteinases as playing an essential and specific role in Xenopus melanophore migration. Chem. Biol. 16, 93-104.
174. Tomlinson, M. L., Rejzek, M., Fidock, M., Field, R. A. and Wheeler, G. N. (2009b). Chemical genomics identifies compounds affecting Xenopus laevis pigment cell development. Mol. Biosyst. 5, 376-384.
175. Tseng, A. S., Adams, D. S., Qiu, D., Koustubhan, P. and Levin, M. (2007). Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev. Biol. 301, 62-69.
176. Tucker, R. P. (2004). Neural crest cells: a model for invasive behavior. Int. J. Biochem. Cell Biol. 36, 173-177.
177. Tung, J. J., Hobert, O., Berryman, M. and Kitajewski, J. (2009). Chloride intracellular channel 4 is involved in endothelial proliferation and morphogenesis in vitro. Angiogenesis 12, 209-220.
178. Uzman, J. A., Patil, S., Uzgare, A. R. and Sater, A. K. (1998). The role of intracellular alkalinization in the establishment of anterior neural fate in Xenopus. Dev. Biol. 193, 10-20.
179. van de Veerdonk, F. C. G. (1960). Serotonin, a melanocyte-stimulating component in the dorsal skin secretion of Xenopus laevis. Nature 187, 948-949.
180. van Kempen, M., van Ginneken, A., de Grijs, I., Mutsaers, N., Opthof, T., Jongsma, H. and van der Heyden, M. (2003). Expression of the electrophysiological system during murine embryonic stem cell cardiac differentiation. Cell Physiol. Biochem. 13, 263-270.
181. Varnum-Finney, B., Xu, L., Brashem-Stein, C., Nourigat, C., Flowers, D., Bakkour, S., Pear, W. S. and Bernstein, I. D. (2000). Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 6, 1278-1281.
182. Waddington, C. H. (1935). Cancer and the theory of organisers. Nature 135, 606-608.
183. Watanabe, M., Iwashita, M., Ishii, M., Kurachi, Y., Kawakami, A., Kondo, S. and Okada, N. (2006). Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep. 7, 893-897.
184. Welsch, T., Kleeff, J. and Friess, H. (2007). Molecular pathogenesis of pancreatic cancer: advances and challenges. Curr. Mol. Med. 7, 504-521. (Pubitemid 47244895)
185. White, R. M. and Zon, L. I. (2008). Melanocytes in development, regeneration, and cancer. Cell Stem Cell 3, 242-252.
186. Whitton, M. E., Ashcroft, D. M. and Gonzalez, U. (2008). Therapeutic interventions for vitiligo. J. Am. Acad. Dermatol. 59, 713-717.
187. Wicha, M. S., Liu, S. and Dontu, G. (2006). Cancer stem cells: an old idea-a paradigm shift. Cancer Res 66, 1883-1890; discussion 1895-1896.
188. 2+ channel expression. Biochem. Biophys. Res. Commun. 322, 1359-1363.
189. + channels in gastric epithelial cell migration. Mol. Cell. Biochem. 308, 219-226.
190. Yamamura, H., Ugawa, S., Ueda, T., Morita, A. and Shimada, S. (2008a). TRPM8 activation suppresses cellular viability in human melanoma. Am. J. Physiol. Cell Physiol. 295, C296-C301.
191. + channel delta subunit in human melanoma G-361 cells. Biochem. Biophys. Res. Commun. 366, 489-492.
192. Yu, S. Y., Yoo, S. J., Yang, L., Zapata, C., Srinivasan, A., Hay, B. A. and Baker, N. E. (2002). A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129, 3269-3278.
193. Zhang, Y. and Levin, M. (2009). Particle tracking model of electrophoretic morphogen movement reveals stochastic dynamics of embryonic gradient. Dev. Dyn. 238, 1923-1935.
194. Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., Wang, F., Guo, A., Walczysko, P., Gu, Y. et al. (2006). Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442, 457-460.