Origin of adult‐type pigment cells forming the asymmetric pigment pattern, in Japanese flounder (Paralichthys olivaceus)

The flatfish‐specific asymmetric pigment pattern depends on the asymmetric appearance of adult‐type pigment cells after the late metamorphic stages. To understand the mechanism enabling the formation of this asymmetric pattern, we investigated the behavior of pigment cell latent precursors in postembryonic Japanese flounder, Paralichthys olivaceus, by analysis of the expression patterns of pigment lineage markers (colony stimulating factor 1 receptor, dopachrome tautomerase, kit) and the DiI (DiO) labeling test for latent precursors. We found that, throughout the larval stages, pigment cell latent precursors were predominantly localized along the dorsal and ventral margins of the flank symmetrically and migrated continuously from these regions to the lateral sides symmetrically, and after late metamorphic stages these precursors differentiated into adult‐type pigment cells on the lateral side asymmetrically. We conclude that adult‐type pigment cells that form the asymmetric pigment pattern are continuously derived from the dorsal and ventral margins of the flank during larval development. Developmental Dynamics 239:3147–3162, 2010. © 2010 Wiley‐Liss, Inc.

[1]  Kevin B. Walters,et al.  Muscle degeneration and leukocyte infiltration caused by mutation of zebrafish fad24 , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[2]  Tohru Suzuki,et al.  Adult‐type pigment cells, which color the ocular sides of flounders at metamorphosis, localize as precursor cells at the proximal parts of the dorsal and anal fins in early larvae , 2008, Development, growth & differentiation.

[3]  D. Parichy,et al.  Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation , 2008, Development.

[4]  C. Tohyama,et al.  Dickkopf 1 (DKK1) regulates skin pigmentation and thickness by affecting Wnt/ β‐catenin signaling in keratinocytes , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[5]  T. Kurth,et al.  Bone morphogenetic protein-4 and Noggin signaling regulates pigment cell distribution in the axolotl trunk. , 2008, Differentiation; research in biological diversity.

[6]  J. Matsumoto,et al.  Comparative Anatomy and Physiology of Pigment Cells in Nonmammalian Tissues , 2007 .

[7]  D. Parichy,et al.  Regulation of Melanoblast Migration and Differentiation , 2007 .

[8]  K. Hamre,et al.  Pigmentation and eye migration in Atlantic halibut (Hippoglossus hippoglossus L.) larvae: new findings and hypotheses , 2007 .

[9]  C. Tickle,et al.  Molecular interactions between Tbx3 and Bmp4 and a model for dorsoventral positioning of mammary gland development , 2006, Proceedings of the National Academy of Sciences.

[10]  A. Kudo,et al.  Medaka unextended-fin mutants suggest a role for Hoxb8a in cell migration and osteoblast differentiation during appendage formation. , 2006, Developmental biology.

[11]  J. W. Ragland,et al.  Reiterated Wnt and BMP signals in neural crest development. , 2005, Seminars in Cell and Developmental Biology.

[12]  Ian K Quigley,et al.  Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus , 2004, Development.

[13]  穣 芳賀,et al.  ヒラメ Paralichthys olivaceus 仔稚魚の真の両面有色型黒化の発現過程における無眼側皮膚の超微細構造 , 2005 .

[14]  J. M. Turner,et al.  Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes , 2004, Development.

[15]  J. W. Ragland,et al.  Reiterated Wnt signaling during zebrafish neural crest development , 2004, Development.

[16]  Andreas Russ,et al.  Dorsoventral Patterning of the Mouse Coat by Tbx15 , 2004, PLoS biology.

[17]  J. M. Turner,et al.  Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. , 2003, Developmental biology.

[18]  J. M. Turner,et al.  Essential role for puma in development of postembryonic neural crest-derived cell lineages in zebrafish. , 2003, Developmental biology.

[19]  J. M. Turner,et al.  Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development , 2003, Development.

[20]  Stephen L. Johnson,et al.  How the zebrafish gets its stripes. , 2001, Developmental biology.

[21]  S. Takada,et al.  Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. , 2001, Developmental biology.

[22]  Stephen L. Johnson,et al.  Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. , 2000, Developmental biology.

[23]  R. Kelsh,et al.  Genetic analysis of melanophore development in zebrafish embryos. , 2000, Developmental biology.

[24]  Stephen L. Johnson,et al.  An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. , 2000, Development.

[25]  J. Bolker,et al.  Pigmentation development in hatchery‐reared flatfishes , 2000 .

[26]  D. Raible,et al.  Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. , 2000, Genes & development.

[27]  Stephen L. Johnson,et al.  Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. , 1999, Development.

[28]  A. Venizelos,et al.  Pigment abnormalities in flatfish , 1999 .

[29]  S. Miwa,et al.  Retinoic acid stimulates development of adult-type chromatophores in the flounder. , 1998, The Journal of experimental zoology.

[30]  D. Kimelman,et al.  Conservation of intracellular Wnt signaling components in dorsal-ventral axis formation in zebrafish , 1999, Development Genes and Evolution.

[31]  Randall T. Moon,et al.  Control of neural crest cell fate by the Wnt signalling pathway , 1998, Nature.

[32]  S. Sokol.  Analysis of Dishevelled signalling pathways during Xenopus development , 1996, Current Biology.

[33]  H. Steinbeisser,et al.  β-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos , 1996, Mechanisms of Development.

[34]  D. Parichy.  When neural crest and placodes collide: interactions between melanophores and the lateral lines that generate stripes in the salamander Ambystoma tigrinum tigrinum (Ambystomatidae). , 1996, Developmental biology.

[35]  D. Parichy.  Pigment patterns of larval salamanders (Ambystomatidae, Salamandridae): the role of the lateral line sensory system and the evolution of pattern-forming mechanisms. , 1996, Developmental biology.

[36]  Harold E. Varmus,et al.  Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos , 1995, Nature.

[37]  P. McCrea,et al.  Embryonic axis induction by the armadillo repeat domain of beta- catenin: evidence for intracellular signaling , 1995, The Journal of cell biology.

[38]  J. H. Law,et al.  Evidence that MIF plays a role in the development of pigmentation patterns in the frog. , 1995, Developmental biology.

[39]  N. Ueno,et al.  A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[40]  N. Ueno,et al.  A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: roles of animal pole tissue in the development of ventral mesoderm. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Graff,et al.  Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo , 1994, Cell.

[42]  J. Matsumoto,et al.  Mechanism of Pseudoalbinism in Flatfish: An Association Between Pigment Cell and Skin Differentiation , 1994 .

[43]  E. Hirose,et al.  Dual appearances of pigment cells from in vitro cultured embryonic cells of Japanese flounder: an implication for a differentiation-associated clock. , 1993, Pigment cell research.

[44]  R. Harland,et al.  Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm , 1993, Nature.

[45]  J. Matsumoto,et al.  Asymmetric pigmentation and pigment disorders in pleuronectiformes (flounders). , 2008, Pigment cell research.

[46]  T. Seikai.  Process of pigment cell differentiation in skin on the left and right sides of the Japanese flounder,Paralichthys olivaceus, during metamorphosis , 1992 .

[47]  H. Epperlein,et al.  The development of the larval pigment patterns in Triturus alpestris and Ambystoma mexicanum. , 1990, Advances in anatomy, embryology, and cell biology.

[48]  J. Matsumoto,et al.  An association of melanophores appearing at metamorphosis as vehicles of asymmetric skin color formation with pigment anomalies developed under hatchery conditions in the Japanese flounder, Paralichthys olivaceus. , 1987, Pigment cell research.

[49]  H. Ide,et al.  Melanophore differentiation in Xenopus laevis, with special reference to dorsoventral pigment pattern formation. , 1983, Journal of embryology and experimental morphology.