Taurine synthesis in teleost-importance of cysteamine pathway
Keywords:
Taurine, Synthesis, TeleostsAbstract
Taurine plays various roles in animals such as growth promotion, osmoregulation, bile acid conjugation,
neurotransmission, cardiac muscle contraction, antioxidant activity, and reproduction. Taurine is one of the
essential nutrients for marine fish larvae and in fishes which lack endogenous taurine production. Taurine is
synthesized from methionine via cysteine. Cysteine is converted to cysteine sulfinic acid by activity of cysteine
dioxygenase (CDO) and cysteine sulfinic acid is converted into hypotaurine by cysteine sulfinic acid
decarboxylase (CSD) in CSD pathway which is considered to be a major taurine production pathway in fish.
Hypotaurine is finally converted into taurine by auto-oxidation. In addition to CSD pathway, there is two other
taurine synthetic pathways are know: cysteic acid pathway where cysteine is oxidized into cysteic acid, and it is
directly converted into taurine by cysteic acid decarboxylase (CAD) activity and cysteamine pathway where
cysteine is converted into cysteamine and it is converted into hypotaurine by cysteamine dioxygenase (ADO).
However, detail on taurine production by these two pathways is not understood.
Common carp is widely cultured in the world and world production of cypriniforms is highest among food fish
species. Rainbow trout is known to have sufficient CSD activity to produce taurine via methionine. In contrast,
it was reported that CSD activity in common carp is about half of that reported in rainbow trout. However,
common carp did not show growth retardation when it was fed taurine deficient diet. These observations led
265
Haga, Y. et al., 2017.Taurine synthesis in teleosts-importance of cysteamine pathway. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-López, M.G.,
Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola Universidad Autónoma de Nuevo
León, San Nicolás de los Garza, Nuevo León, México, pp. 264-283. ISBN 978-607-27-0822-8.
hypothesis that common carp is able to produce sufficient amount of taurine beside the CSD pathway. The
purpose of the present study is to investigate effect of dietary supplementation of cysteine, cysteamine,
methionine, and taurine on the growth, sulfur amino acid content, and gene expression of taurine synthesizing
enzymes.
Eight different diets supplemented with taurine, methionine, cysteine, and cysteamine were fed to the juvenile
common carps for 30 days. For control, a diet without supplying sulfur amino acid was fed. Feeding diets
supplemented sulfur amino acid resulted in better survival, growth, feed conversion ratio, and protein efficiency
ratio except treatments supplemented with cysteamine. It was observed that the supplementation of dietary
cysteamine caused growth retardation, myopathy, and body deformity in common carp. All sulfur amino acids
increased taurine deposition in the carcass and 1.5% cysteamine increased taurine deposition by 1.8 and 5.5
times higher than those of the methionine and cysteine treatments. CDO was tended to be down-regulated by
cysteine and low dose of taurine but up-regulated by a high dose of cysteamine. It was observed that CSD was
down-regulated by sulfur amino acids. ADO was down-regulated by methionine, cysteine and low dose of
taurine but up-regulated by cysteamine.
These results suggest that CSD pathway plays a role in taurine synthesis and cysteamine pathway is another
major taurine synthesizing pathway in common carp.
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References
Al-Feky SSA, El-Sayed A-FM, Ezzat AA. 2016. Dietary taurine improves reproductive performance of Nile
tilapia (Oreochromis niloticus) broodstock. Aquaculture Nutrition 22: 392-399.
Calduch-Giner JA, Davey G, Saera-Vila A, Houeix B, Talbot A, Prunet P, Cairns MT, Perez-Sanchez J. 2010.
Use of microarray technology to assess the time course of liver stress response after confinement
exposure in gilthead sea bream (Sparus aurata L.). BMC Genomics 11: 193-210.
Chang Y-C, Ding S-T, Lee Y-H, Wang Y-C, Huang M-F, Liu I-H. 2013. Taurine homeostasis requires de novo
synthesis via cysteine sulfinic acid decarboxylase during zebrafish early embryogenesis. Amino Acids
:615–629
FAO. The State of World Fisheries and Aquaculture. 2016. Rome, Italy.
Gaume V, Figard H, Mougin F, Guilland JC, Alberto JM, Gueant JL, Alber D, Demougeot C, Berthelot A. 2005.
Effect of a swim training on homocysteine and cysteine levels in rats. Amino Acids 28: 337-342.
Goto T, Ui T, Une M, Kuramoto T, Kihira K, Hoshita T. 1996. Bile salt composition and distribution of the
D-cysteinolic acid conjugated bile salts in fish. Fish Sci 62: 606–609.
Goto T, Matsumoto T, Murakami S, Takagi S, Hasumi F. 2003. Conversion of cysteate into taurine in liver of
fish. Fish. Sci. 69: 216-218.
Haga Y, Kumagai A, Kondo H, Hirono I, Satoh S. 2015. Isolation, molecular characterization of cysteine
sulfinic acid decarboxylase (CSD) of red sea bream Pagrus major and yellowtail Seriola
quinquieradiata and expression analysis of CSD from several marine fish species. Aquaculture 449,
-17. DOI: 10.1016/j.aquaculture.2015.04.004
Hagey LR, Møller PR, Hofmann AF, Krasowski MD: Diversity of bile salts in fish and amphibians: evolution of
a complex biochemical pathway. Physiol Biochem Zool 2010, 83:308-321.
Han X, Patters AB, Jones DP, Zelikovic I, Chesney RW.2006. The taurine transporter: mechanisms of
regulation. Acta Physiol 187:61-73.
Hiraoka Y, Sasaki Y, Sonoda K. 2011. Investigation of contents of nitrogenous constituents in the extracts of
seafood caught in Ehime (Part1). Research Report of Ehime Institute of Industrial Technology 49:
-22. (in Japanese).
Impellizzeri G, Mangiafico S, Oriente G, Piattelli M, Sciuto S, Fattorusso E, Magno S, Santacroce C, Sica D.
Constituents of red algae. I. Amino acids and lowmolecular-weight carbohydrates of some
marine red algae. Phytochemistry 14, 1549-1557.
Ito K. 1965. Occurrence of D-glyceryltaurine and amino acid pattern in the extractives of a red algae,
Gymnogongrus flabelliformis. Nippon Suisan Gakkaishi 31, 307-311.
Ishihara Y, Nakata C, Morimoto M, Mori N, Watanabe F. 2013. Free amino acid and mineral contents in viscera
of bluefin tuna Thunnus orientalis unloaded in Sakai fishing port, Tottori Prefecture. Nippon Suisan
Gakkaishi 79, 433-435.
Iwatani H, Inoue K, Takei Y, Abe H. 2012. Changes in the free amino acid content in the skeletal muscle of
fourspine sculpin Cottus kazika reared in different environmental salinities. Aquac. Sci. 60, 495-501.
Jacobsen JG, Smith LH. 1968. Biochemistry and physiology of taurine and taurine derivatives. Physiol. Rev.
: 424-511.
Jusadi D, Ruchani S, Mokoginta I, Ekasari J. 2011. Improvement of survival and development of Pacific white
shrimp Litopenaeus vannamei by feeding taurine enriched rotifers. J. Aquac. Indonesia 10: 131-136
(in Indonesian with English abstract).
Kataoka H, Ohishi K, Imai J, Omori M, Mukai M, Makita M. 1986. Distribution of cysteine sulfonate
decarboxylase and cysteamine dioxygenase activity in various animal tissues. Sulfar Amino Acids 9:
-298. (in Japanese with English abstract)
Kato K, Yamamoto M, Hung NP, Fukada H, Biswas A, Yamamoto S, Takii K, Murata O, Miyashita S. 2012.
Effect of taurine supplementation on skin thickness and scale detachability in red sea bream Pagrus
major. Aquaculture Science, 60, 59-64.
Kato K, Yamamoto M, Peerapon K, Fukada H, Biswas A, Yamamoto S, Takii K, Miyashita S. 2014. Effects of
dietary taurine levels on epidermal thickness and scale loss in red sea bream, Pagrus major.
Aquaculture Research 45: 1818-1824.
Khaoian P, Ogita H, Watanabe H, Nishioka M, Kanosue F, Ngyuen HP, Fukuda H, Masumoto T. 2014. Effects
of taurine supplementation to low fishmeal practical diet on growth, tissue taurine content and taste of
year yellowtail Seriola quinqueradiata. Aquaculture Science 62: 415-423.
Kim H-Y, Shin J-W, Park H-O, Choi S-H, Jang Y-M, Lee S-O. 2000. Comparison of taste compounds of red sea
bream, rockfish and flounders differing in the location and growing conditions. Kr. J. Food Sci.
Technol. 32: 550-563 (in Korean with English abstract).
Kim S-K, Takeuchi T, Yokoyama M, Murata Y, Kaneniwa M, Sakakura Y. 2005. Effect of dietary taurine levels
on growth and feeding behavior of juvenile Japanese flounder Paralichthys olivaceus. Aquaculture
: 765-774.
Kurihara A. 2008. Studies on exploring effective nutrients for octopus paralarva in Artemia. Ph D thesis,
Graduate School of Marine Science and Technology, Tokyo University of Marine Science and
Technology, Tokyo, Japan, 150p. (in Japanese)
Lindberg B. 1955. Methyrated taurines and choline sulfate in red algae. Acta Chem Scand 9, 1323.
Liu QR, López-Corcuera B, Mandiyan S, Nelson H, Nelson N. 1993. Molecular characterization of four
pharmacologically distinct gamma-aminobutyric acid transporters in mouse brain. J. Biol Chem. 268:
-2112.
Liu P, Ge X, Ding H, Jiang H, Christensen BM, Li J. 2012. Role of glutamate decarboxylase-like protein 1
(GADL1) in taurine biosynthesis. J. Biol. Chem. 287:40898-40906.
Matsunari H, Takeuchi T, Murata Y, Takahashi M, Ishibashi N, Chuda H, Arakawa T. 2003. Changes in the
taurine content during the early growth stages of artificially produced yellowtail compared with wild
fish. Nippon Suisan Gakkaishi 69: 757–762.
Matsunari H, Furuita H, Yamamoto T, Kim S-K, Sakakura Y, Takeuchi T. 2008. Effect of dietary taurine and
cystine on growth performance of juvenile red sea bream Pagrus major. Aquaculture 274: 142-147.
Morishita T, Uno K, Arai T, Takahashi T. 1989. Comparison of the amounts of extractive constituents in the
meats of cultured mathods, and those of wild. Nippon Suisan Gakkaishi 55: 1565-1573.
Morita T, Sakiyama K, Fujimoto H, Yamada T, Tominaga O. 2011. Improvement of survival of hatchery-raise
fry of Japanese flounder soon after release into wild by feeding taurine enriched feed and sandy
substrate. Gihou 13: 41-47. (in Japanese)
Murakoshi Y, Hatanaka S. 1977. Sulfer-containing amino acid in nature. Journal of Synthetic Organic
Chemistry, Japan 35: 343-353.
Nakamura S, Miyamoto A, Tsuchihashi Y. 2014. Influence of low-fishmeal diet used the fish powder
alternative material on growth performance and epidermal thickness of red sea bream Pagrus major.
Bull. Mie Pref. Fish. Res. Inst., 23: 11-17 (in Japanese).
Ohyama H, Kubo M, Enomoto T. 1991. Determination of taurine in foods using an absorption-distribution
HPLC. J. Jpn. Soc. Nutr. Food Sci. 44: 305-308 (in Japanese with English abstract).
Ozawa A, Aoki S, Suzuki K, Sugimoto M, Fujita T, Tsuji K. 1984. Taurine content in fish and shells. Journal
of Japan Society of Nutrition and Food Science 37: 561-567. (in Japanese).
Paneflorida VD. 2004. Amino acid profiles in the midgut, ovary, developing eggs and zoea of the mud crab,
Scylla serrata. Israeli J. Aquac. 56: 111-123.
Rise MT, Gordon WN, Hall JR, Booman M, Hori TS, Trippel EA, Gamperl AK. 2014. Variation in embryonic
mortality and maternal transcript expression among atlantic cod (Gadus morhua) broodstock: A
functional genomic study. Mar Genomics 18: 3-20.
Ronnestad I, Tonheim SK, Fyhn HJ, Rojas-Garci CR, Kamisaka Y, Koven W, Finn RN, Terjesen BF, Barr Y,
Conceicao LEC. 2003. The supply of amino acids during early feeding stages of marine fish larvae: a
review of recent findings. Aquaculture 227, 147-164.
Sakaguchi M, Murata M. 1987. Taurine content in fish and shellfish. Bulletin of the Research Institute for
Food Science, Kyoto University 50: 23-26. (in Japanese)
Satake M, Chiba Y, Makuta M, Fujita T, Kohama Y, Mimura T. 1987. Studies on pharmacological activities of
D-cysteinoic acid. Yakugaku Zasshi 107: 917-919.
Seikai T, Takeuchi T, Park GS. 1997. Comparison of growth, feed efficiency, and chemical composition of
juvenile flounder fed live mysids and formula feed under laboratory conditions. Fish. Sci. 63:
-526.
Shiraita T, Kado Y, Matubara H. 2012. Maintenance of freshness of bluefin tuna (Thunnus tynnus). Bulletin of
Food Research Institute of Aomori Prefectural Industral Technology Center, 3, 21-24 (in Japanese).
Suyama M, Hirano T, Sato K, Fukuda H. 1979. Nitrogenous consituents of meat extract of freshwater softshell
turtle. Nippon Suisan Gakkaishi 45; 595-599. (in Japanese with English abstract)
Takagi S, Murata H, Goto T, Hatate H, Endo M, Yamashita H, Miyatake H, Ukawa M. 2011. Role of taurine
deficiency in inducing green liver syndrome and effect of dietary taurine supplementation in
improving growth in juvenile red sea bream Pagrus major fed non-fishmeal diets based on soy protein
concentrate. Fish. Sci. 77, 235-244.
Takahashi T, Amano T, Takeuchi T. 2005. Establishment of direct enrichment method of taurine to rotifer.
Aquaculture Science 53: 121–126.
Takeuchi T. 2014. Progress on larval and juvenile nutrition to improve the quality and health of seawater fish: a
review. Fisheries Science 80: 389–403.
Takeuchi T, Park G-S, Seikai T, Yokoyama M. 2001. Taurine content in Japanese founder Paralichthys
olivaceus T. & S. and red sea bream Pagrus major T. & S. during the period of seed production.
Aquaculture Research 32 (S1), 244-248.
Ueki I, Roman HB, Valli A, Fieselmann K, Lam J, Peters R, Hirschberger LL, Stipanuk ML. 2011. Knockout of
the murine cysteine dioxygenase gene results in severe impairment in ability to synthesize taurine and
an increased catabolism of cysteine to hydrogen sulfide. Am J Physiol Endocrinol Metab 301:
E668–E684.
Warskulat U, Heller-Stilb B, Oermann E, Zilles K, Haas H, Lang F, Häussinger D.2007. Phenotype of the
taurine transporter knockout mouse. Methods Enzymol. 428:439-58.
Wang Q, Gen H, Wang X, Mai K, Xu W, Zhou H. 2014. Dietary sulfur amino acid modulations of taurine
biosynthesis in juvenile turbot (Psetta maxima). Aquaculture 422–423: 141–145.
Wang X, He G, Mai K, Xu W, Zhou H. 2016. Differential regulation of taurine biosynthesis in rainbow trout and
Japanese flounder. Scientific Reports 6, 21231.
Winge I, Teigen K, Fossbakk A, Mahootchi E, Kleppe R, Sköldberg F, Kämpe O, Haavik J. 2015. Mammalian
CSAD and GADL1 have distinct biochemical properties and patterns of brain expression. Neurochem.
Int. 90: 173-184.
Xu Y, Xie Y, Shao X, Ni Z, Mou S. 2015. L-FABP: A novel biomarker of kidney disease. Clin Chim Acta. 2015
May 20;445:85-90
Yamamoto T, Unuma T, Akiyama T. 2000. The influence of dietary protein and lipid levels on tissue free amino
acid levels of fingerling rainbow trout (Oncorhynchus mykiss). Aquaculture 182: 353-372.
Yeh YH, Hwang DF .2001. High-performance liquid chromatographic determination for bile components in
fish, chicken and duck. J Chromatogr B Biomed Sci Appl 751: 1–8.
Yoneda T, Yoshimura K. 1965. Isolatin of D-cysteinolic acid from a starfish Asteria Pectinifera. Nippon Suisan
Gakkaishi 31: 1045.
