{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T06:53:31Z","timestamp":1791010411032,"version":"4.1.0"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,4,15]],"date-time":"2016-04-15T00:00:00Z","timestamp":1460678400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,4,15]],"date-time":"2016-04-15T00:00:00Z","timestamp":1460678400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>We have succeeded in creating see-through frogs from natural color mutants of the Japanese brown frog <jats:italic>Rana japonica<\/jats:italic>, which usually possesses an ochre or brown back; this coloration enables the organs, blood vessels and eggs to be observed through the skin without performing dissection. We crossed two kinds of recessive color mutant (black-eyed and gray-eyed) frogs through artificial insemination and F2 offspring produced frogs whose skin is translucent throughout the life cycle. Three kinds of dermal chromatophores\u2014xanthophores, iridophores and melanophores\u2014are observed in a layered arrangement in the skin of wild-type frogs, but few chromatophores were present in the skin of the see-through frogs. The translucent skin enables observation of organ growth and cancer formation and progression in the animal, which can be monitored over its entire life without the need for dissection. See-through frogs thus provide a useful animal model for environmental, medical and biological research.<\/jats:p>","DOI":"10.1038\/srep24431","type":"journal-article","created":{"date-parts":[[2016,4,15]],"date-time":"2016-04-15T09:27:37Z","timestamp":1460712457000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["The first see-through frog created by breeding: description, inheritance patterns and dermal chromatophore structure"],"prefix":"10.1038","volume":"6","author":[{"given":"Masayuki","family":"Sumida","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammed Mafizul","family":"Islam","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takeshi","family":"Igawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Atsushi","family":"Kurabayashi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yukari","family":"Furukawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Naomi","family":"Sano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamotsu","family":"Fujii","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Norio","family":"Yoshizaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,4,15]]},"reference":[{"key":"BFsrep24431_CR1","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1083\/jcb.38.1.67","volume":"38","author":"JT Bagnara","year":"1968","unstructured":"Bagnara, J. T., Taylor, J. D. & Hadley, M. E. The dermal chromatophore unit. J. Cell Biol. 38, 67\u201379 (1968).","journal-title":"J. Cell Biol."},{"key":"BFsrep24431_CR2","doi-asserted-by":"publisher","first-page":"10046","DOI":"10.1073\/pnas.181204298","volume":"98","author":"Y Wakamatsu","year":"2001","unstructured":"Wakamatsu, Y., Pristyazhnyuk, S., Kinoshita, M., Tanaka, M. & Ozato, K. The see-through medaka: A fish model that is see-through throughout life. Proc. Natl. Acad. Sci. USA 98, 10046\u201310050 (2001).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFsrep24431_CR3","first-page":"19","volume":"2010","author":"S-I Akiyama","year":"2010","unstructured":"Akiyama, S.-I. & Tamaru, Y. Development of transgenic technology using transparent goldfish. Abst. Ann. Meet. Soc. Biosci. Bioengineer. Japan 2010, 19 (2010).","journal-title":"Abst. Ann. Meet. Soc. Biosci. Bioengineer. Japan"},{"key":"BFsrep24431_CR4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.11646\/zootaxa.3851.1.1","volume":"3851","author":"E Twomey","year":"2014","unstructured":"Twomey, E., Delia, J. & Castroviejo-Fisher, S. A review of Northern Peruvian glassfrogs (Centrolenidae), with the description of four new remarkable species. Zootaxa 3851, 1\u201387 (2014).","journal-title":"Zootaxa"},{"key":"BFsrep24431_CR5","doi-asserted-by":"publisher","first-page":"69","DOI":"10.11646\/zootaxa.3920.1.4","volume":"3920","author":"B Kubicki","year":"2015","unstructured":"Kubicki, B., Salazar, S. & Puschendorf, R. A new species of glassfrog, genus Hyalinobatrachium (Anura: Centrolenidae), from the Caribbean foothills of Costa Rica. Zootaxa 3920, 69\u201384 (2015).","journal-title":"Zootaxa"},{"key":"BFsrep24431_CR6","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1002\/jez.1402210116","volume":"221","author":"KF Sally","year":"1982","unstructured":"Sally, K. F., Ellinger, M. S. & Murphy, J. F. The pale mutation in Bombina orientaris: Effects on melanophores and xanthophores. J. Exp. Zool. 221, 125\u2013129 (1982).","journal-title":"J. Exp. Zool."},{"key":"BFsrep24431_CR7","unstructured":"Bagnara, J. T. Comparative anatomy and phylogeny of pigment cells in no mammalian tissues in The pigmentary system: Physiology and pathophysiology (eds Nordlung, J. J. et al.) 9\u201340 (Oxford Univ. Press, 1998)."},{"key":"BFsrep24431_CR8","first-page":"1","volume":"7","author":"M Nishioka","year":"1985","unstructured":"Nishioka, M. & Ueda, H. Genetics and morphology of 13 albino stocks in the Rana nigromaculata group. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 7, 1\u2013121 (1985).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ."},{"key":"BFsrep24431_CR9","first-page":"123","volume":"7","author":"M Nishioka","year":"1985","unstructured":"Nishioka, M. & Ueda, H. Electron-microscopic observation on the dermal chromatophores of normal frogs and three kinds of color variants in Rhacophorus schlegelii. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 7, 123\u2013155 (1985).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR10","first-page":"157","volume":"7","author":"M Nishioka","year":"1985","unstructured":"Nishioka, M. & Ueda, H. Two kinds of black-eyed variants in Hyla arborea japonica. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 7, 157\u2013179 (1985).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR11","first-page":"199","volume":"7","author":"M Nishioka","year":"1985","unstructured":"Nishioka, M. & Ueda, H. Non-inheritable color variants in Rana brevipoda porosa. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 7, 199\u2013217 (1985).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/jhered\/91.1.1","volume":"91","author":"M Sumida","year":"2000","unstructured":"Sumida, M. & Nishioka, M. Genetic linkage groups in the Japanese brown frog (Rana japonica). J. Hered. 91, 1\u20137 (2000).","journal-title":"J. Hered."},{"key":"BFsrep24431_CR13","first-page":"207","volume":"38","author":"Y Ichikawa","year":"2003","unstructured":"Ichikawa, Y., Ohtani, H. & Miura, I. Pigment cells of amphibians. Electronmicroscope 38, 207\u2013212 (2003). (in Japanese)","journal-title":"Electronmicroscope"},{"key":"BFsrep24431_CR14","first-page":"173","volume":"13","author":"M Sumida","year":"1994","unstructured":"Sumida, M. & Nishioka, M. Geographic variability of sex-linked loci in the Japanese brown frog Rana japonica. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 13, 173\u2013195 (1994).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR15","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1007\/BF00554413","volume":"34","author":"M Sumida","year":"1996","unstructured":"Sumida, M. Inheritance and linkage analysis of ten enzyme and blood protein loci in the Japanese brown frog Rana japonica. Biochem. Genet. 34, 375\u2013388 (1996).","journal-title":"Biochem. Genet"},{"key":"BFsrep24431_CR16","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/S0305-0491(00)00204-2","volume":"126","author":"M Sumida","year":"2000","unstructured":"Sumida, M. & Nishioka, M. Sex-linked genes and linkage maps in amphibians. Comp. Biochem. Physiol. 126, 257\u2013270 (2000).","journal-title":"Comp. Biochem. Physiol"},{"key":"BFsrep24431_CR17","doi-asserted-by":"crossref","unstructured":"Nature (News-in-Brief). See-through frogs created by breeding. Nature 449, 521 (2007).","DOI":"10.1038\/449521f"},{"key":"BFsrep24431_CR18","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1046\/j.1440-169x.2000.00530.x","volume":"42","author":"M Kinoshita","year":"2000","unstructured":"Kinoshita, M., Kani, S., Ozato, K. & Wakamatsu, Y. Activity of the medaka translation elongation factor 1\u03b1-A promoter examined using the GFP gene as a reporter. Dev. Growth Differ. 42, 469\u2013478 (2000).","journal-title":"Dev. Growth Differ."},{"key":"BFsrep24431_CR19","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1002\/jmor.1051320205","volume":"132","author":"MW Berns","year":"1970","unstructured":"Berns, M. W. & Narayan, K. S. A histological and ultrastructural analysis of the dermal chromatophores of the variant ranid blue frog. J. Morph. 132, 169\u2013179 (1970).","journal-title":"J. Morph"},{"key":"BFsrep24431_CR20","first-page":"25","volume":"2","author":"M Nishioka","year":"1977","unstructured":"Nishioka, M. Color variants induced by radiation and their inheritance in Rana nigromaculata. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 2, 25\u201389 (1977).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR21","first-page":"181","volume":"7","author":"M Nishioka","year":"1985","unstructured":"Nishioka, M. & Ueda, H. Blue variants in Hyla arborea japonica. Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ. 7, 181\u2013197 (1985).","journal-title":"Sci. Rep. Lab. Amphibian Biol. Hiroshima Univ"},{"key":"BFsrep24431_CR22","unstructured":"Nishioka, M. & Ueda, H. Study on the color mutants in anurans. Research report by 1988 fiscal Grant-in-Aid for Scientific Research (General Research A) 1\u201326 (1989). (in Japanese)"},{"key":"BFsrep24431_CR23","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1016\/j.cell.2014.10.034","volume":"159","author":"K Tainaka","year":"2014","unstructured":"Tainaka, K. et al. Whole-body imaging with single-cell resolution by tissue decolorization. Cell 159, 911\u2013924 (2014).","journal-title":"Cell"},{"key":"BFsrep24431_CR24","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1002\/jez.1401250203","volume":"125","author":"MC Niu","year":"1954","unstructured":"Niu, M. C. Further studies on the origin of amphibian pigment cells. J. Exp. Zool. 125, 199\u2013220 (1954).","journal-title":"J. Exp. Zool."},{"key":"BFsrep24431_CR25","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1083\/jcb.18.1.181","volume":"18","author":"AV Loud","year":"1963","unstructured":"Loud, A. V. & Mishima, Y. The induction of melanization in goldfish scales with ACTH in vivo. J. Cell Biol. 18, 181\u2013194 (1963).","journal-title":"J. Cell Biol."},{"key":"BFsrep24431_CR26","unstructured":"Bagnara, J. T. & Ferris, W. Interrelationships of vertebrate chromatophores in Biology of normal and abnormal melanocytes (eds Kawamura, T. et al.) 57\u201376 (Univ. Tokyo Press, 1971)."},{"key":"BFsrep24431_CR27","first-page":"319","volume":"30","author":"S-t Chen","year":"1974","unstructured":"Chen, S.-t., Wahn, H., Turner, W. A., Taylor, J. D. & Tchen, T. T. MSH, cyclic AMP and melanocyte differentiation. Recent Progress in Hormone Research 30, 319\u2013345 (1974).","journal-title":"Recent Progress in Hormone Research"},{"key":"BFsrep24431_CR28","doi-asserted-by":"publisher","first-page":"646","DOI":"10.1016\/0014-4827(68)90504-1","volume":"52","author":"M Obika","year":"1968","unstructured":"Obika, M. & Matsumoto, J. Morphological and biochemical studies on amphibian bright-colored pigment cells and their pterinosomes. Exp. Cell Res. 52, 646\u2013659 (1968).","journal-title":"Exp. Cell Res."},{"key":"BFsrep24431_CR29","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1016\/0304-4165(69)90356-0","volume":"192","author":"H Ide","year":"1969","unstructured":"Ide, H. & Hama, T. Tyrosinase activity of the melanin and pteridine granules in goldfish chromatophores. Biochim. Biophys. Acta 192, 200\u2013204 (1969).","journal-title":"Biochim. Biophys. Acta"},{"key":"BFsrep24431_CR30","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1111\/j.1440-169X.1971.00141.x","volume":"13","author":"M Yasutomi","year":"1971","unstructured":"Yasutomi, M. & Hama, T. Ultramicroscopic study of the developmental change of the xanthophore in the frog, Rana japonica with special reference to pterinosomes. Dev. Growth Differ. 13, 141\u2013149 (1971).","journal-title":"Dev. Growth Differ."},{"key":"BFsrep24431_CR31","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1111\/j.1440-169X.1976.00289.x","volume":"18","author":"M Yasutomi","year":"1976","unstructured":"Yasutomi, M. & Hama, T. Electron microscopic demonstration of tyrosinase in pterinosomes of the frog xanthophore and the origin of pterinosomes. Dev. Growth Differ. 18, 289\u2013299 (1976).","journal-title":"Dev. Growth Differ."},{"key":"BFsrep24431_CR32","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1002\/jez.1402030211","volume":"203","author":"H Ide","year":"1978","unstructured":"Ide, H. Transformation of amphibian xanthophores into melanophores in clonal culture. J. Exp. Zool. 203, 287\u2013293 (1978).","journal-title":"J. Exp. Zool."},{"key":"BFsrep24431_CR33","unstructured":"Bagnara, J. T. The neural crest as a source of stem cells in Developmental and evolutionary aspects of the neural crest (ed Maderson, P. ) 57\u201387 (New York Wiley, 1987)."},{"key":"BFsrep24431_CR34","unstructured":"Bagnara, J. T. & Hadley, M. E. Chromatophores and Color Change: The Comparative Physiology of Animal Pigmentation, 202 pp. (Prentice-Hall, Englewood Cliffs, N.J., 1973)."},{"key":"BFsrep24431_CR35","doi-asserted-by":"publisher","first-page":"410","DOI":"10.1126\/science.760198","volume":"203","author":"JT Bagnara","year":"1979","unstructured":"Bagnara, J. T. et al. Common origin of pigment cells. Science 203, 410\u2013415 (1979).","journal-title":"Science"},{"key":"BFsrep24431_CR36","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1111\/j.1600-0749.1999.tb00506.x","volume":"12","author":"JT Bagnara","year":"1999","unstructured":"Bagnara, J. T. The emergence of pigment cell biology: a personal view. Pigment Cell Res. 12, 48\u201365 (1999).","journal-title":"Pigment Cell Res."},{"key":"BFsrep24431_CR37","first-page":"465","volume":"23","author":"JT Bagnara","year":"1983","unstructured":"Bagnara, J. T. Developmental aspects of vertebrate chromatophores. Integ. Comp. Biol. 23, 465\u2013478 (1983).","journal-title":"Integ. Comp. Biol"},{"key":"BFsrep24431_CR38","doi-asserted-by":"publisher","first-page":"333","DOI":"10.2307\/1565170","volume":"30","author":"M Sumida","year":"1996","unstructured":"Sumida, M. Incipient intraspecific isolating mechanisms in the Japanese brown frog Rana japonica. J. Herpetol. 30, 333\u2013346 (1996).","journal-title":"J. Herpetol."},{"key":"BFsrep24431_CR39","doi-asserted-by":"publisher","first-page":"567","DOI":"10.2108\/zsj.20.567","volume":"20","author":"M Sumida","year":"2003","unstructured":"Sumida, M., Ueda, H. & Nishioka, M. Reproductive isolating mechanisms and molecular phylogenetic relationships among Palearctic and Oriental brown frogs. Zool. Sci. 20, 567\u2013580 (2003).","journal-title":"Zool. Sci."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep24431","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep24431.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep24431.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T18:22:51Z","timestamp":1672856571000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep24431"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,4,15]]},"references-count":39,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,7,26]]}},"alternative-id":["BFsrep24431"],"URL":"https:\/\/doi.org\/10.1038\/srep24431","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,4,15]]},"assertion":[{"value":"5 November 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 March 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 April 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"24431"}}