Abstract
Taurine is an abundant amino acid essential to various physiological functions in many organisms; however, invertebrate taurine biosynthesis pathways are largely unknown. Here, we investigated the activities of taurine biosynthesis enzymes, cysteinesulfinic acid decarboxylase (CSD), cysteic acid decarboxylase (CAD), and cysteamine dioxygenase (CAO) in the livers of spear squid Heterololigo bleekeri and swordtip squid Uroteuthis edulis. When the enzyme reactions were performed at 35 °C for 60 min, CSD and CAD activities of spear squid were 1.49 ± 0.25 and 0.79 ± 0.11 nmol/(min mg protein), respectively; no CAO activity was observed. The CSD and CAD activities of swordtip squid were lower than those of spear squid, but CAO activity was also observed. These results suggest that taurine biosynthesis pathways in squids vary between species, as in fish. Under the conditions of our experiment, kinetic analysis revealed that in spear squid, the Michaelis–Menten constant and maximum reaction rate were 0.20 ± 0.02 mM and 1.78 ± 0.22 nmol/(min mg protein), respectively, for CSD, and for CAD 0.57 ± 0.02 mM and 1.29 ± 0.17 nmol/(min mg protein), respectively. Cysteic acid competitively inhibited spear squid CSD activity, indicating that a single enzyme catalyzes the decarboxylation of cysteinesulfinic and cysteic acids in this squid.
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References
Allen K, Awapara J (1960) Metabolism of sulfur amino acids in Mytilus edulis and Rangia cuneata. Biol Bull 118:173–182
Allen JA, Garrett MR (1971) Taurine in marine invertebrates. Adv Mar Biol 9:205–253
Asano K, Suzuki T, Saito A, Wei F-Y, Ikeuchi Y, Numata T, Tanaka R, Yamane Y, Yamamoto T, Goto T, Kishita Y, Murayama K, Ohtake A, Okazaki Y, Tomizawa K, Sakaguchi Y, Suzuki T (2018) Metabolic and chemical regulation of tRNA modification associated with taurine deficiency and human disease. Nucleic Acids Res 46:1565–1583
Cárdenas-López JL, Haard NF (2009) Identification of a cysteine proteinase from Jumbo squid (Dosidicus gigas) hepatopancreas as cathepsin L. Food Chem 112:442–447
Cashman JR, Zhang J (2006) Human Flavin-containing monooxygenases. Annu Rev Pharmacol Toxicol 46:65–100
Ciaula AD, Garruti G, Baccetto RL, Molina-Molina E, Bonfrate L, Wang DQ, Portincasa P (2017) Bile acid physiology. Ann Hepatol 16:s4–s14
Dixon M (1953) The determination of enzyme inhibitor constants. Biochem J 55:170–171
Eilertsen KE, Larsen R, Mæhre HK, Jensen I-J, Elvevoll EO (2012) Anticholesterolemic and antiatherogenic effects of taurine supplementation is model dependent. In: Frank S, Kostner G (eds) Lipoproteins-role in health and diseases. IntechOpen, London, pp 269–288
Foos TM, Wu JY (2002) The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem Res 27:21–26
Goto T, Tiba K, Sakurada Y, Takagi S (2001a) Determination of hepatic cysteinesulfinate decarboxylase activity in fish by means of OPA-prelabeling and reverse-phase high-performance liquid chromatographic separation. Fish Sci 67:553–555
Goto T, Matsumoto T, Takagi S (2001b) Distribution of the hepatic cysteamine dioxygenase activities in fish. Fish Sci 67:1187–1189
Goto T, Mochizuki A, Hasumi F (2002) Distribution and activities of enzymes involved in taurine biosynthesis in the liver of fish. Suisanzoshoku 50:443–449 (in Japanese with English abstract)
Goto T, Matsumoto T, Murakami S, Takagi S, Hasumi F (2003) Conversion of cysteate into taurine in liver fish. Fish Sci 69:216–218
Guion-Rain MC, Portemer C, Chatagner F (1975) Rat liver cysteine sulfinate decarboxylase: purification, new appraisal of the molecular weight and determination of catalytic properties. Biochim Biophys Acta 384:265–276
Heinämäki AA, Piha RS (1980) Partial purification of cysteinesulfinic acid decarboxylase from calf brain. Acta Chem Scand B 34:363–267
Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163
Jacobsen JG, Smith LH (1968) Biochemistry and physiology of taurine and taurine derivatives. Physiol Rev 48:424–511
Jacobsen JG, Thomas LL, Smith LH Jr (1964) Properties and distribution of mammalian L-cysteine sulfinate carboxy-lyases. Biochim Biophys Acta 85:103–116
Kataoka H, Ohnishi N (1986) Occurrence of taurine in plants. Agric Biol Chem 50:1887–1888
Kataoka H, Ohishi K, Inoue N, Makita M (1986a) Determination of cysteic acid in animal tissues by gas chromatography. Bunseki Kagaku 35:389–393 (in Japanese with English abstract)
Kataoka H, Ohishi K, Imai J, Makita M (1986b) Determination of cysteine sulfinic acid in animal tissues by gas chromatography. Bunseki Kagaku 35:508–512 (in Japanese with English abstract)
Kataoka H, Ohishi K, Imai J, Ohmori M, Mukai M, Makita M (1986c) Distribution of cysteine sulfinate decarboxylase and cysteamine dioxygenase activity in various animal tissues. Sulfur Amino Acids 9:293–298 (in Japanese with English abstract)
Kawasaki A, Ono A, Mizuta S, Kamiya M, Takenaga T, Murakami S (2017) The taurine content of Japanese seaweed. In: Lee DH, Schaffer SW, Park E, Kim HW (eds) Taurine 10. Advances in experimental medicine and biology 975. Springer, Geneva, pp 1105–1112
Lorsch JR (2014) Practical steady-state enzyme kinetics. Methods Enzymol 536:3–15
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193:165–275
Matsumiya M, Mochizuki A (1997) Purification and characterization of chitinase from the liver of Japanese common squid Todarodes pacificus. Fish Sci 63:409–413
Meng J, Zhu Q, Zhang L, Li C, Li L, She Z, Huang B, Zhang G (2013) Genome and transcriptome analyses provide insight into the euryhaline adaptation mechanism of Crassostrea gigas. PLoS ONE 8:e58563
Mushiroda T, Douya R, Takahara E, Nagata O (2000) The involvement of flavin-containing monooxygenase but not CYP3A4 in metabolism of itopride hydrochloride, a gastroprokinetic agent: comparison with cisapride and mosapride citrate. Drug Metab Dispos 28:1231–1237
Nagasaki T, Hongo Y, Koito T, Koito T, Nakamura-Kusakabe I, Shimamura S, Takaki Y, Yoshida T, Maruyama T, Inoue K (2015) Cysteine dioxygenase and cysteine sulfinate decarboxylase genes of the deep-sea mussel Bathymodiolus septemdierum: possible involvement in hypotaurine synthesis and adaptation to hydrogen sulfide. Amino Acids 47:571–578
Overby LH, Buckpitt AR, Lawton MP, Atta-Asafo-Adjei E, Schulze J, Philpot RM (1995) Characterization of flavin-containing monooxygenase 5 (FMO5) cloned from human and guinea pig: evidence that the unique catalytic properties of FMO5 are not confined to the rabbit ortholog. Arch Biochem Biophys 317:275–284
Peters LD, Livingstone DR, Shenin-Johnson S, Hines RN, Schlenk D (1995) Characterization of hepatic flavin monooxygenase from the marine teleost turbot (Scophthalmus maximus L.). Xenobiotica 25:121–131
Rane A, Wilkinson GR, Shand DG (1977) Prediction of hepatic extraction ratio from in vitro measurement of intrinsic clearance. J Pharmacol Exp Ther 200:420–424
Reichert P, Urban PF (1986) Purification and properties of rat brain cysteine sulfinate decarboxylase (EC 4.1.1.29). Neurochem Int 9:315–321
Schaffer SW, Jong CJ, Ramila KC, Azuma J (2010) Physiological roles of taurine in heart and muscle. J Biomed Sci 17:S2. https://doi.org/10.1186/1423-0127-17-S1-S2
Schlenk D, Buhler DR (1990) Flavin-containing monooxygenase activity in the gumboot chiton Cryptochiton stelleri. Mar Biol 104:47–50
Schlenk D, Buhler DR (1991) Flavin-containing monooxygenase activity in liver microsomes from the rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 20:13–24
Schlenk D, Li-Schlenk R (1994) Characterization of liver flavin-containing monooxygenase of the dogfish shark (Squalus acanthias) and partial purification of liver flavin-containing monooxygenase of the silky shark (Carcharhinus falciformis). Comp Biochem Physiol B Biochem Mol Biol 109:655–664
Sumizu K (1962) Oxidation of hypotaurine in rat liver. Biochim Biophys Acta 63:210–212
Suyama M, Kobayashi H (1980) Free amino acids and quaternary ammonium Bases in mantle muscle of squids. Nippon Suisan Gakkaishi 46:1261–1264 (in Japanese with English abstract)
Taniguchi-Takizawa T, Shimizu M, Kume T, Yamazaki H (2015) Benzydamine N-oxygenation as an index for flavin-containing monooxygenase activity and benzydamine N-demethylation by cytochrome P450 enzymes in liver microsomes from rats, dogs, monkeys, and humans. Drug Metab Pharmacokinet 30:64–69
Veeravalli S, Phillips IR, Freire RT, Varshavi D, Everett JR, Shephard EA (2020) Flavin-containing monooxygenase 1 catalyzes the production of taurine from hypotaurine. Drug Metab Dispos 48:378–385
Welborn J, Manahan D (1995) Taurine metabolism in larvae of marine invertebrate molluscs (Bilvalvia, Gastropoda). J Exp Biol 198:1791–1799
Wu JY (1982) Purification and characterization of cysteic acid and cysteinesulfinic acid decarboxylase and L-glutamate decarboxylase from bovine brain. Proc Natl Acad Sci USA 79:4270–4274
Wu JY, Prentice H (2010) Role of taurine in the central nervous system. J Biomed Sci 17:S1. https://doi.org/10.1186/1423-0127-17-S1-S1
Wu JY, Moss LG, Chen MS (1979) Tissue and regional distribution of cysteic acid decarboxylase. A new assay method. Neurochem Res 4:201–212
Yamanaka H, Kawashima Y, Hideki U, Ohsima T (1998) Comparative biochemical studies on extractive components and antibacterial activities of squid and octopus Ink. Nihon Chourikagaku Kaishi 31:206–213 (in Japanese with English abstract)
Yamaoka K, Tanigawara Y, Nakagawa T, Uno T (1981) A pharmacokinetic analysis program (MULTI) for microcomputer. J Pham Dyn 4:879–885
Yokoyama M, Takeuchi T, Park GS, Nakazoe J (2001) Hepatic cysteinesulphinate decarboxylase activity in fish. Aquac Res 32:216–220
Zhao X, Li Q, Meng Q, Xu C (2017) Identification and expression of cysteine sulfinate decarboxylase, possible regulation of taurine biosynthesis in Crassostrea gigas in response to low salinity. Sci Rep 7:5505
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This work was partly supported by an academic grant from the Toyo Suisan Foundation.
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Matsumoto, T., Akita, M., Ogawa, M. et al. Evaluation of taurine biosynthesis in the livers of the spear squid Heterololigo bleekeri and the swordtip squid Uroteuthis edulis. Fish Sci 87, 717–725 (2021). https://doi.org/10.1007/s12562-021-01544-3
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DOI: https://doi.org/10.1007/s12562-021-01544-3