Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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The Functional Relevance of Prepro-melanin Concentrating Hormone (pMCH) to Skin Color Change, Blind-side Malpigmentation and Feeding of Oliver Flounder Paralichthys olivaceus

  • Kang, Duk-Young (West Sea Fisheries Research Institute, National Fisheries Research and Development Institute) ;
  • Kim, Hyo-Chan (West Sea Fisheries Research Institute, National Fisheries Research and Development Institute) ;
  • Kang, Han-Seung (West Sea Fisheries Research Institute, National Fisheries Research and Development Institute)
  • Received : 2014.08.04
  • Accepted : 2014.09.15
  • Published : 2014.09.30
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Abstract

To assess the functional structure of prepro-melanin-concentrating hormone (pMCH), we isolated and cloned pMCH (of-pMCH) mRNA from the brain of the olive flounder, Paralichthys olivaceus, and compared its amino acid sequence with those from other animals. In addition, to examine whether activation of the brain of-pMCH gene is influenced by background color, density, and feeding, we compared pMCH mRNA activities against different background colors (bright and dark) and at different densities (100% PCA and 200% PCA). To examine whether the pMCH gene is related with malpigmentation of blind-side skin and appetite, we compared pMCH gene expression between ordinary and hypermelanic flounders, and between feeding and fasting flounders. The of-pMCH cDNA was 405 bp in the open reading frame [ORF] and encoded a protein of 135 amino acids; MCH was 51 bp in length and encoded a protein of 17 amino acids. An obvious single band of the expected size was obtained from the brain and pituitary by RT-PCR. In addition, of-pMCH gene activity was significantly higher in the bright background only at low density (< 100% PCA) making the ocular skin of fish whitening, and in ordinary fish. However, the gene activity was significantly decreased in dark background, at high density (>200% PCA), and in hypermelano fish. These results suggest that skin whitening camouflage of the flounder is induced by high MCH gene activity, and the density disturbs the function of background color in the physiological color change. Moreover, our data suggest that a low level of MCH gene activity may be related to malpigmentation of the blind-side skin. In feeding, although pMCH gene activity was significantly increased by feeding in the white background, the pMCH gene activity in the dark background was not influenced by feeding, indicating that the MCH gene activity increased by feeding can be offset by dark background color, or is unaffected by appetite. In conclusion, this study showed that MCH gene expression is related to ocular-skin whitening camouflage and blind-skin hypermelanosis, and is influenced by background color and density.

Keywords

References

  1. Abbott CR, Kennedy AR, Wren AM, Rossi M, Murphy KG, Seal LJ, Todd JF, Ghatei MA, Small CJ and Bloom SR. 2003. Identification of hypothalamic nuclei involved in the orexigenic effect of melanin-concentrating hormone. Endocrinology 144, 3943-3949. https://doi.org/10.1210/en.2003-0149
  2. Amano M and Takahashi A. 2009. Melanin-concentrating hormone: A neuropeptide hormone affecting the relationship between photic environment and fish with special reference to background color and food intake regulation. Peptides 30, 1979-1984. https://doi.org/10.1016/j.peptides.2009.05.022
  3. Amano M, Takahashi A, Oka Y, Yamanome T, Kawauchi H and Yamamori K. 2003. Immunocytochemical localization and ontogenic development of melanin-concentrating hormone in the brain of a pleuronectiform fish, the barfin flounder. Cell Tiss Res 311, 71-77. https://doi.org/10.1007/s00441-002-0660-6
  4. Amiya N, Amano M, Takahashi A, Yamanome T, Kawauchi H and Yamamori K. 2005. Effects of tank color on melanin-concentrating hormone levels in the brain, pituitary gland, and plasma of the barfin flounder as revealed by a newly developed time-resolved fluoroimmunoassay. Gen Comp Endocrinol 143, 251-256. https://doi.org/10.1016/j.ygcen.2005.04.012
  5. Baker B, Levy A, Hall L and Lightman S. 1995. Cloning and expression of melanin-concentrating hormone genes in the rainbow trout brain. Neuroendocrinology 61, 67-76. https://doi.org/10.1159/000126814
  6. Baker BI. 1993. The role of melanin-concentrating hormone in color change. Annals New York Acad Sci 680, 279-289. https://doi.org/10.1111/j.1749-6632.1993.tb19690.x
  7. Berman JR, Skariah G, Maro GS, Mignot E and Mourrain P. 2009. Characterization of two melanin-concentrating hormone genes in zebrafish reveals evolutionary and physiological links with the mammalian MCH system. J Comp Neurol 517, 695-710. https://doi.org/10.1002/cne.22171
  8. Della-Zuana O, Presse F, Ortola C, Duhault J, Nahon JL and Levens N. 2002. Acute and chronic administration of melanin-concentrating hormone enhances food intake and body weight in Wistar and Sprague-Dawley rats. Internat J Obesity 26, 1289-1295. https://doi.org/10.1038/sj.ijo.0802079
  9. Doolan BJ, Allan GL, Booth MA and Jones PL. 2008. Effects of cage netting colour and density on the skin pigmentation and stress response of Australian snapper, Pagrus auratus (Bloch & Schneider, 1801). Aquacult Res 39, 1360-1368. https://doi.org/10.1111/j.1365-2109.2008.02003.x
  10. Gomori A, Ishihara A, Ito M, Mashiko S, Matsushita H, Yumoto M, Ito M, Tanaka T, Tokita S, Moriya M, Iwaasa H and Kanatani A. 2003. Chronic intracerebroventricular infusion of MCH causes obesity in mice. Am J Physiol-Endocrinol Metabol 284, E583-E588. https://doi.org/10.1152/ajpendo.00350.2002
  11. Groneveld D, Eckhardt ERM, Coenen AJM, Martens GJM, Balm PHM and Wendelaar Bonga SE. 1995. Expression of tilapia prepro-melanin-concentrating hormone mRNA in hypothalamic and neurohypophysial cells. J Molec Endocrinol 14, 199-207. https://doi.org/10.1677/jme.0.0140199
  12. Hoglund E, Balm PHM and Winberg S. 2002. Behavioural and neuroendocrine effects of environmental background colour and social interaction in Arctic charr (Salvelinus alpinus). J Exper Biol 205, 2535-2543.
  13. Han D, Xie S, Lei W, Zhu X and Yang Y. 2005. Effect of light intensity on growth, survival and skin color of juvenile Chinese longsnout catfish (Leiocassis longirostris Gunther). Aquaculture 248, 299-306. https://doi.org/10.1016/j.aquaculture.2005.03.016
  14. Iwata N and Kikuchi K. 1998. Effects of sandy substrate and light on hypermelanosis of the blind side in cultured Japanese flounder Paralichthys olivaceus. Environ Biol Fish 52, 291-297.
  15. Jeong DS and Jeon CY. 2008. Genetic variability and population structure of olive flounder Paralichthys olivaceus from stocked areas using microsatellite DNA markers. Kor J Ichthyol 20, 156-162.
  16. Kalinowski CT, Robaina LE, Fernandez-Palacios H, Schuchardt D and Izquierdo MS. 2005. Effect of different carotenoid sources and their dietary levels on red porgy (Pagrus pagrus) growth and skin colour. Aquaculture 244, 223-231. https://doi.org/10.1016/j.aquaculture.2004.11.001
  17. Kang DY and Kim HC. 2012. Relevance of environmental factors and physiological pigment hormones to blind-side hypermelanosis in the cultured flounder, Paralichthys olivaceus. Aquaculture 356-357, 14-21. https://doi.org/10.1016/j.aquaculture.2012.05.041
  18. Kang DY and Kim HC. 2013. Functional characterization of two melanin-concentrating hormone genes in the color camouflage, hypermelanosis, and appetite of starry flounder. Gen Comp Endocrinol 189, 74-83. https://doi.org/10.1016/j.ygcen.2013.04.025
  19. Kang DY, Kim HC and Chang YJ. 2011. Effects of stocking density on the blind-side hypermelanosis of cultured olive flounder Paralichthys olivaceus. Fish Aquat Sci 14, 123-129.
  20. Kawauchi H. 1989. Structure and biosynthesis of melanin-concentrating hormone. Life Sci 45, 1133-1140. https://doi.org/10.1016/0024-3205(89)90500-6
  21. Kawauchi H. 2006. Functions of melanin-concentrating hormone in fish. J Exper Zool-part A: Comp Exper Biol 305, 751-760.
  22. Kawauchi H and Baker BI. 2004. Melanin-concentrating hormone signaling systems in fish. Peptides 25, 1577-1584. https://doi.org/10.1016/j.peptides.2004.03.025
  23. Kawauchi H, Kawazoe I and Tsubokawa M. 1983. Characterization of melanin- concentrating hormone in chum salmon pituitaries. Nature 305, 321-323. https://doi.org/10.1038/305321a0
  24. Kishida M, Baker BI and Eberle AN. 1989. The measurement of melanin-concentrating hormone in trout blood. Gen Comp Endocrinol 74, 221-229. https://doi.org/10.1016/0016-6480(89)90216-5
  25. Kobayashi Y, Chiba H, Amiya N, Yamanome T, Mizusawa K, Amano M and Takahashi A. 2008. Transcription elements and functional expression of proopiomelanocortin genes in the pituitary gland of the barfin flounder. Gen Comp Endocrinol 158, 259-267. https://doi.org/10.1016/j.ygcen.2008.07.015
  26. Lin X, Volkoff H, Narnaware Y, Bernier NJ, Peyon P and Peter RE. 2000. Brain regulation of feeding behavior and food intake in fish. Comp Biochem Physiol- part A. Molec Integr Physiol 126, 415-434. https://doi.org/10.1016/S1095-6433(00)00230-0
  27. Livak KJ and Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-\Delta\Delta{CT}}$ method. Methods 25, 402-408. https://doi.org/10.1006/meth.2001.1262
  28. Ludwig DS, Mountjoy KG, Tatro JB, Gillette JA, Frederich RC, Flier JS and Maratos-Flier E. 1998. Melanin-concentrating hormone: A functional melanocortin antagonist in the hypothalamus. Am J Physiol- Endocrinol Metabol 274, E627-E633. https://doi.org/10.1152/ajpendo.1998.274.4.E627
  29. Matsuda K and Maruyama K. 2007. Regulation of feeding behavior by pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal polypeptide (VIP) in vertebrates. Peptides 28, 1761-1766. https://doi.org/10.1016/j.peptides.2007.03.007
  30. Matsuda K, Kojima K, Shimakura SI and Takahashi A. 2009. Regulation of food intake by melanin-concentrating hormone in goldfish. Peptides 30, 2060-2065. https://doi.org/10.1016/j.peptides.2009.02.015
  31. Matsuda K, Shimakura SI, Maruyama K, Miura T, Uchiyama M, Kawauchi H, Shioda S and Takahashi A. 2006. Central administration of melanin-concentrating hormone (MCH) suppresses food intake, but not locomotor activity, in the goldfish, Carassius auratus. Neurosci Lett 399, 259-263. https://doi.org/10.1016/j.neulet.2006.02.005
  32. Matsuda K, Shimakura SI, Miura T, Maruyama K, Uchiyama M, Kawauchi H, Shioda S and Takahashi A. 2007. Feeding-induced changes of melanin-concentrating hormone (MCH)-like immunoreactivity in goldfish brain. Cell Tiss Res 328, 375-382. https://doi.org/10.1007/s00441-006-0347-5
  33. Minth CD, Qiu H, Akil H, Watson SJ and Dixon JE. 1989. Two precursors of melanin-concentrating hormone: DNA sequence analysis and in situ and immunochemical localization. Proc Nat' Acad Sci US Am 86, 4292-4296. https://doi.org/10.1073/pnas.86.11.4292
  34. Mizusawa K, Saito Y, Wang Z, Kobayashi Y, Matsuda K and Takahashi A. 2009. Molecular cloning and expression of two melanin-concentrating hormone receptors in goldfish. Peptides 30, 1990-1996. https://doi.org/10.1016/j.peptides.2009.04.010
  35. Nahon JL, Presse F, Schoepfer R and Vale W. 1991. Identification of a single melanin-concentrating hormone messenger ribonucleic acid in coho salmon: Structural relatedness with 7SL ribonucleic acid. J Neuroendocrinol 3, 173-183. https://doi.org/10.1111/j.1365-2826.1991.tb00260.x
  36. Naito N, Nakai Y, Kawauchi H and Hayashi Y. 1985. Immunocytochemical identification of melanin-concentrating hormone in the brain and pituitary gland of the teleost fishes Oncorhynchus keta and Salmo gairdneri. Cell Tiss Res 242, 41-48.
  37. Nery LEM and Castrucci AMDL. 1997. Pigment cell signalling for physiological color change. Comp Biochem Physiol-part A. Physiol 118, 1135-1144. https://doi.org/10.1016/S0300-9629(97)00045-5
  38. Nilsson Skold H, Aspengren S and Wallin M. 2013. Rapid color change in fish and amphibians-function, regulation, and emerging applications. Pigment Cell Melano Res 26, 29-38. https://doi.org/10.1111/pcmr.12040
  39. Oshima N. 2001. Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Res 14, 312-319. https://doi.org/10.1034/j.1600-0749.2001.140502.x
  40. Ottesen OH and Strand HK. 1996. Growth, development, and skin abnormalities of halibut (Hippoglossus hippoglossus L.) juveniles kept on different bottom substrates. Aquaculture 146, 17-25. https://doi.org/10.1016/S0044-8486(96)01359-2
  41. Perez Sirkin DI, Canepa MM, Fossati M, Fernandino JI, Delgadin T, Canosa LF, Somoza GM and Vissio PG. 2012. Melanin concentrating hormone (MCH) is involved in the regulation of growth hormone in Cichlasoma dimerus (Cichlidae, Teleostei). Gen Comp Endocrinol 176, 102-111. https://doi.org/10.1016/j.ygcen.2012.01.002
  42. Pandolfi M, Canepa MM, Ravaglia MA, Maggese MC, Paz DA and Vissio PG. 2003. Melanin-concentrating hormone system in the brain and skin of the cichlid fish Cichlasoma dimerus: Anatomical localization ontogeny and distribution in comparison to $\alpha$-melanocyte-stimulating hormone-expressing cells. Cell Tiss Res 311, 61-69. https://doi.org/10.1007/s00441-002-0654-4
  43. Pissios P, Bradley RL and Maratos-Flier E. 2006. Expanding the scales: The multiple roles of MCH in regulating energy balance and other biological functions. Endoc Rev 27, 606-620. https://doi.org/10.1210/er.2006-0021
  44. Presse F, Sorokovsky I, Max JP, Nicolaidis S and Nahon JL. 1996. Melanin-concentrating hormone is a potent anorectic peptide regulated by food-deprivation and glucopenia in the rat. Neuroscience 71, 735-745. https://doi.org/10.1016/0306-4522(95)00481-5
  45. Pritchard LE, Turnbull AV and White A. 2002. Pro-opiomelanocortin processing in the hypothalamus: Impact on melanocortin signalling and obesity. J Endocrinol 172, 411-421. https://doi.org/10.1677/joe.0.1720411
  46. Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek J, Kanarek R and Maratos-Flier E. 1996. A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380, 243-247. https://doi.org/10.1038/380243a0
  47. Ramachandran VS, Tyler CW, Gregory RL, Rogers-Ramachandran D, Duensing S, Pillsbury C and Ramachandran C. 1996. Rapid adaptive camouflage in tropical flounders. Nature 379, 815-818. https://doi.org/10.1038/379815a0
  48. Rossi M, Choi SJ, O'Shea D, Miyoshi T, Ghatei MA and Bloom SR. 1997. Melanin-concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight. Endocrinology 138, 351-355. https://doi.org/10.1210/endo.138.1.4887
  49. Seikai T. 1992. Process of pigment cell differentiation in skin on the left and right side of the Japanese flounder, Paralichthys olivaceus, during metamorphosis. Jap J Ichthyol 29, 85-92.
  50. Seikai T, Matsumoto J, Shimozaki M, Oikawa A and Akiyama T. 1987. 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. Pigment cell research 1, 143-151. https://doi.org/10.1111/j.1600-0749.1987.tb00405.x
  51. Shi Y. 2004. Beyond skin color: Emerging roles of melanin-concentrating hormone in energy homeostasis and other physiological functions. Peptides 25, 1605-1611. https://doi.org/10.1016/j.peptides.2004.02.023
  52. Stricker-Krongrad A, Dimitrov T and Beck B. 2001. Central and peripheral dysregulation of melanin-concentrating hormone in obese Zucker rats. Mol Brain Res 92, 43-48. https://doi.org/10.1016/S0169-328X(01)00130-9
  53. Sugimoto M. 2002. Morphological color changes in fish: Regulation of pigment cell density and morphology. Microscopy Res Tech 58, 496-503. https://doi.org/10.1002/jemt.10168
  54. Suzuki M, Narnaware YK, Baker BI and Levy A. 1995. Influence of environmental colour and diurnal phase on MCH gene expression in the trout. J Neuroendocrinol 7, 319-328. https://doi.org/10.1111/j.1365-2826.1995.tb00764.x
  55. Tagawa M, Kaji T, Kinoshita M and Tanaka M. 2004. Effect of stocking density and addition of proteins on larval survival in Japanese flounder, Paralichthys olivaceus. Aquaculture 230, 517-525. https://doi.org/10.1016/S0044-8486(03)00409-5
  56. Takahashi A, Kosugi T, Kobayashi Y, Yamanome T, Schioth HB and Kawauchi H. 2007. The melanin-concentrating hormone receptor 2 (MCH-R2) mediates the effect of MCH to control body color for background adaptation in the barfin flounder. Gen Comp Endocrinol 151, 210-219. https://doi.org/10.1016/j.ygcen.2007.01.011
  57. Takahashi A, Tsuchiya K, Yamanome T, Amano M, Yasuda A, Yamamori K and Kawauchi H. 2004. Possible involvement of melanin-concentrating hormone in food intake in a teleost fish, barfin flounder. Peptides 25, 1613-1622. https://doi.org/10.1016/j.peptides.2004.02.022
  58. Takahashi Y. 1994. Influence of stocking density and food at late phase of larval period on hypermelanosis on the blind body side in juvenile Japanese flounder. Nippon Suisan Gakkaishi 60, 593-598. https://doi.org/10.2331/suisan.60.593
  59. Takayama Y, Wada C, Kawauchi H and Ono M. 1989. Structures of two genes coding for melanin-concentrating hormone of chum salmon. Gene 80, 65-73. https://doi.org/10.1016/0378-1119(89)90251-5
  60. Tamura K, Dudley J, Nei M and Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596-1599. https://doi.org/10.1093/molbev/msm092
  61. Tuziak SM and Volkoff H. 2012. A preliminary investigation of the role of melanin-concentrating hormone (MCH) and its receptors in appetite regulation of winter flounder (Pseudopleuronectes americanus). Molec Cell Endocrinol 348, 281-296. https://doi.org/10.1016/j.mce.2011.09.015
  62. Yamanome T, Amano M and Takahashi A. 2005. White background reduces the occurrence of staining, activates melanin-concentrating hormone and promotes somatic growth in barfin flounder. Aquaculture 244, 323-329. https://doi.org/10.1016/j.aquaculture.2004.11.020
  63. Yamanome T, Chiba H and Takahashi A. 2007a. Melanocyte-stimulating hormone facilitates hypermelanosis on the non-eyed side of the barfin flounder, a pleuronectiform fish. Aquaculture 270, 505-511. https://doi.org/10.1016/j.aquaculture.2007.05.037
  64. Yamanome T, Amano M, Amiya N and Takahashi A. 2007b. Hypermelanosis on the blind side of Japanese flounder Paralichthys olivaceus is diminished by rearing in a white tank: Short paper. Fish Sci 73, 466-468. https://doi.org/10.1111/j.1444-2906.2007.01356.x