Reassessment of the function of somatolactin alpha in lipid metabolism using medaka mutant and transgenic strains

BMC Genetics

Shoji Fukamachi¹  Asami Yoshimura¹  Yuko Sasano¹ 

[1] Laboratory of Evolutionary Genetics, Department of Chemical and Biological Sciences, Japan Women’s University, Mejirodai 2-8-1, Bunkyo-ku, Tokyo, 112-8681, Japan

关键词: Pigmentation;    Hepatic triglycerides;    Medaka;    Somatolactin alpha (SLa);   

Others  :  1122437
DOI  :  10.1186/1471-2156-13-64

 received in 2012-06-21, accepted in 2012-07-09,  发布年份 2012

【 摘 要 】

Background

Somatolactin alpha (SLa) is a fish-specific peptide hormone secreted from the pituitary. In medaka, SLa functions to darken the skin color and lack of SLa makes it pale. Transcription of SLa is enhanced or suppressed when fish are kept in dark or bright conditions, respectively, indicating SLa’s important role in background acclimation of the skin color. Bizarrely, however, the lack of SLa seems to cause the additional defect of increased triglycerides in organs, which could not be rescued (decreased) by its overexpression.

Results

To assess this enigmatic result, we investigated genetic (the SLa, Slc45a2, r, and Y genes) and nongenetic (age, fasting, water temperature, and background color) effects on hepatic triglycerides. These experiments found that percent hepatic triglycerides quickly change in response to external/internal environments. Effects of SLa seemed to be much less obvious, although it may increase the proportion of hepatic triglycerides at least during certain breeding conditions or under certain genetic backgrounds.

Conclusions

The present results do not exclude the possibility that SLa takes part in lipid metabolism or other physiological processes. However, we suggest that skin-color regulation is the only definite role of SLa so far demonstrated in this species.

【 授权许可】

   
2012 Sasano et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1 .

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【 参考文献 】

• [1]Fukamachi S, Meyer A: Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol 2007, 65(4):359-372.
• [2]Fukamachi S, Yada T, Meyer A, Kinoshita M: Effects of constitutive expression of somatolactin alpha on skin pigmentation in medaka. Gene 2009, 442(1–2):81-87.
• [3]Takeda H, Shimada A: The art of medaka genetics and genomics: what makes them so unique? Annu Rev Genet 2010, 44:217-241.
• [4]Fukamachi S: Medaka spontaneous mutants for body coloration. In Medaka: Model for organogenesis, human disease and evolution. Edited by Tanaka M, Naruse K, Takeda H. Springer, Japan; 2011:173-184.
• [5]Fukamachi S, Sugimoto M, Mitani H, Shima A: Somatolactin selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. Proc Natl Acad Sci USA 2004, 101(29):10661-10666.
• [6]Sugimoto M: Morphological color changes in fish: regulation of pigment cell density and morphology. Microsc Res Tech 2002, 58(6):496-503.
• [7]Canepa MM, Pandolfi M, Maggese MC, Vissio PG: Involvement of somatolactin in background adaptation of the cichlid fish Cichlasoma dimerus. J Exp Zool A Comp Exp Biol 2006, 305(5):410-419.
• [8]Zhu Y, Thomas P: Elevations of somatolactin in plasma and pituitaries and increased alpha-MSH cell activity in red drum exposed to black background and decreased illumination. Gen Comp Endocrinol 1996, 101(1):21-31.
• [9]Canepa MM, Zhu Y, Fossati M, Stiller JW, Vissio PG: Cloning, phylogenetic analysis and expression of somatolactin and its receptor in Cichlasoma dimerus: Their role in long-term background color acclimation. Gen Comp Endocrinol 2012, 176(1):52-61.
• [10]Fukamachi S, Kinoshita M, Aizawa K, Oda S, Meyer A, Mitani H: Dual control by a single gene of secondary sexual characters and mating preferences in medaka. BMC Biol 2009, 7:64. BioMed Central Full Text
• [11]Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Swanson P, Dickhoff WW: Identification of the salmon somatolactin receptor, a new member of the cytokine receptor family. Endocrinology 2005, 146(5):2354-2361.
• [12]Chen M, Huang X, Yuen DS, Cheng CH: A study on the functional interaction between the GH/PRL family of polypeptides with their receptors in zebrafish: Evidence against GHR1 being the receptor for somatolactin. Mol Cell Endocrinol 2011, 337(1–2):114-121.
• [13]Fukamachi S, Yada T, Mitani H: Medaka receptors for somatolactin and growth hormone: phylogenetic paradox among fish growth hormone receptors. Genetics 2005, 171(4):1875-1883.
• [14]Yada T, Moriyama S, Suzuki Y, Azuma T, Takahashi A, Hirose S, Naito N: Relationships between obesity and metabolic hormones in the "cobalt" variant of rainbow trout. Gen Comp Endocrinol 2002, 128(1):36-43.
• [15]Vega-Rubin De Celis S, Gomez P, Calduch-Giner JA, Medale F, Perez-Sanchez J: Expression and characterization of European sea bass (Dicentrarchus labrax) somatolactin: assessment of in vivo metabolic effects. Mar Biotechnol (NY) 2003, 5(1):92-101.
• [16]Mingarro M, Vega-Rubin De Celis S, Astola A, Pendon C, Valdivia MM, Perez-Sanchez J: Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 2002, 128(2):102-111.
• [17]Company R, Astola A, Pendon C, Valdivia MM, Perez-Sanchez J: Somatotropic regulation of fish growth and adiposity: growth hormone (GH) and somatolactin (SL) relationship. Comparative biochemistry and physiology Toxicology & pharmacology : CBP 2001, 130(4):435-445.
• [18]Matsumoto T, Terai S, Oishi T, Kuwashiro S, Fujisawa K, Yamamoto N, Fujita Y, Hamamoto Y, Furutani-Seiki M, Nishina H, et al.: Medaka as a model for human nonalcoholic steatohepatitis. Dis Model Mech 2010, 3(7–8):431-440.
• [19]Hirayama M, Mukai T, Miya M, Murata Y, Sekiya Y, Yamashita T, Nishida M, Watabe S, Oda S, Mitani H: Intraspecific variation in the mitochondrial genome among local populations of Medaka Oryziaslatipes. Gene 2010, 457(1–2):13-24.
• [20]Laiz-Carrion R, Fuentes J, Redruello B, Guzman JM: Martin del Rio MP, Power D, Mancera JM: Expression of pituitary prolactin, growth hormone and somatolactin is modified in response to different stressors (salinity, crowding and food-deprivation) in gilthead sea bream Sparus auratus. Gen Comp Endocrinol 2009, 162(3):293-300.
• [21]Uchida K, Moriyama S, Breves JP, Fox BK, Pierce AL, Borski RJ, Hirano T, Grau EG: cDNA cloning and isolation of somatolactin in Mozambique tilapia and effects of seawater acclimation, confinement stress, and fasting on its pituitary expression. Gen Comp Endocrinol 2009, 161(2):162-170.
• [22]Kakizawa S, Kaneko T, Hasegawa S, Hirano T: Effects of feeding, fasting, background adaptation, acute stress, and exhaustive exercise on the plasma somatolactin concentrations in rainbow trout. Gen Comp Endocrinol 1995, 98(2):137-146.
• [23]Pottinger TG, Rand-Weaver M, Sumpter JP: Overwinter fasting and re-feeding in rainbow trout: plasma growth hormone and cortisol levels in relation to energy mobilisation. Comp Biochem Physiol B Biochem Mol Biol 2003, 136(3):403-417.
• [24]Ayson FG, de Jesus-Ayson EG, Takemura A: mRNA expression patterns for GH, PRL, SL, IGF-I and IGF-II during altered feeding status in rabbitfish, Siganus guttatus. Gen Comp Endocrinol 2007, 150(2):196-204.
• [25]Amano M, Takahashi A: 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 2009, 30(11):1979-1984.
• [26]Tanaka M, Azuma M, Nejigaki Y, Saito Y, Mizusawa K, Uchiyama M, Takahashi A, Shioda S, Matsuda K: Melanin-concentrating hormone reduces somatolactin release from cultured goldfish pituitary cells. J Endocrinol 2009, 203(3):389-398.
• [27]Canepa M, Pozzi A, Astola A, Maggese MC, Vissio P: Effect of salmon melanin-concentrating hormone and mammalian gonadotrophin-releasing hormone on somatolactin release in pituitary culture of Cichlasoma dimerus. Cell Tissue Res 2008, 333(1):49-59.
• [28]Wan G, Chan KM: A study of somatolactin actions by ectopic expression in transgenic zebrafish larvae. J Mol Endocrinol 2010, 45(5):301-315.
• [29]Rand-Weaver M, Swanson P, Kawauchi H, Dickhoff WW: Somatolactin, a novel pituitary protein: purification and plasma levels during reproductive maturation of coho salmon. J Endocrinol 1992, 133(3):393-403.
• [30]Johnson LL, Norberg B, Willis ML, Zebroski H, Swanson P: Isolation, characterization, and radioimmunoassay of Atlantic halibut somatolactin and plasma levels during stress and reproduction in flatfish. Gen Comp Endocrinol 1997, 105(2):194-209.
• [31]Mousa MA, Mousa SA: Implication of somatolactin in the regulation of sexual maturation and spawning of Mugil cephalus. J Exp Zool 2000, 287(1):62-73.
• [32]Vissio PG, Andreone L, Paz DA, Maggese MC, Somoza GM, Strussmann CA: Relation between the reproductive status and somatolactin cell activity in the pituitary of pejerrey, Odontesthes bonariensis (Atheriniformes). J Exp Zool 2002, 293(5):492-499.
• [33]Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HD, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, et al.: Speciation through sensory drive in cichlid fish. Nature 2008, 455(7213):620-626.
• [34]Ishikawa T, Kamei Y, Otozai S, Kim J, Sato A, Kuwahara Y, Tanaka M, Deguchi T, Inohara H, Tsujimura T, et al.: High-resolution melting curve analysis for rapid detection of mutations in a Medaka TILLING library. BMC Mol Biol 2010, 11:70. BioMed Central Full Text
• [35]Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, et al.: DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417(6888):559-563.
• [36]Fukamachi S, Shimada A, Shima A: Mutations in the gene encoding B, a novel transporter protein, reduce melanin content in medaka. Nat Genet 2001, 28(4):381-385.
• [37]Aida T: On the inheritance of color in a fresh-water fish, APLOCHEILUS LATIPES Temmick and schlegel, with special reference to sex-linked inheritance. Genetics 1921, 6(6):554-573.
• [38]Kinoshita M, Murata K, Naruse K, Tanaka M: Medaka: biology, management, and experimental protocols. Wiley-Blackwell, USA; 2009.
• [39]Bligh EG, Dyer WJ: A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959, 37(8):911-917.