Abstract
Important progress in arginine metabolism includes the discovery of widespread expression of two isoforms of arginase, arginase I and II, not only in hepatic cells but also in non-hepatic cells, and the formation of nitric oxide, a widely distributed signal-transducing molecule, from arginine by nitric oxide synthase. Possible physiological roles of arginase may therefore include regulation of nitric oxide synthesis through arginine availability for nitric oxide synthase. In this paper, arginase was investigated in the submandibular, sublingual, and parotid glands of rat, mouse, guinea pig, and rabbit. From their arginase contents, the salivary glands of these species were divided into two groups. Variable levels of arginase activity were detected in the salivary glands of mouse and rat. However, salivary glands of rabbit and guinea pig had almost no arginase activity. The presence of nitric oxide synthase has been reported in all the salivary glands used in this study. Therefore, one of the important findings was the presence of species specificity in the co-localization of arginase and nitric oxide synthase in the salivary glands of the four species. The highest specific activity of arginase was found in mouse parotid gland. In rat, considerable arginase activity was detected in all three glands, at 3.6–7.3% of that in rat liver. In rat submandibular gland, arginase was detected in both cytosolic and particulate fractions. In addition, arginase was detected in isolated acinar cells, but not in duct cells. Experiments on the intracellular distribution and the effects of the arginase inhibitors ornithine and Nω-hydroxy-L-arginine (NOHA), suggested the presence of both arginase I and arginase II in rat submandibular gland.
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Abbreviations
- cGMP :
-
cyclic guanosine 3′,5′-monophosphate
- NO :
-
nitric oxide
- NOHA :
-
Nω-hydroxy-L-arginine
- NOS :
-
nitric oxide synthase
References
Akiba T, Kuroiwa N, Yabe AS, Iwase K, Hiwasa T, Yokoe H, Kubosawa H, Kageyama R, Dahrington GJ, Mori M, Tanzawa H, Takiguchi M (2002) Expression and regulation of the gene for arginase I in mouse salivary glands: requirement of CCAAT/enhancer-binding protein αfor the expression in the parotid gland. J Biochem 132:621–627
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt Biochem 72:248–254
Bredt DS, Snyder SH (1994) Nitric oxide: a physiological messenger molecule. Ann Rev Biochem 63:175–195
Chinkers M, Garbers DL (1991) Signal transduction by guanylyl cyclases. Annu Rev Biochem 60:553–575
Colleluori DM, Morris SM Jr, Ash DE (2001) Expression, purification, and characterization of human type II arginase. Arch Biochem Biophys 389:135–143
Custot J, Moali C, Brollo M, Boucher JL, Delaforge M, Mansuy D, Tenu JP, Zimmermann JL (1997) The new α-amino acid Nωhydroxy-nor- arginine: a high affinity inhibitor of arginase well adapted to bind to its manganese cluster. J Am Chem Soc 119:4086–4087
Daghigh F, Fukuto JM, Ash DE (1994) Inhibition of rat- liver arginase by an intermediate in NO biosynthesis, N-G-hydroxy-L-arginine—implications for the regulation of nitric-oxide biosynthesis by arginase. Biochem Bioph Res Commun 202:174–180
Furchgott RF (1988) Vasodilations. In: Vanhoutte PM (ed) Vascular smooth muscle, peptides, autonomic nerves and endothelium. Raven, New York, pp 401–411
Herzfeld A, Raper SM (1976) The heterogeneity of arginase in rat tissues. Biochem J 153:469–478
Ignarro L, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265–9269
Jenkinson CP, Grody WW, Cederbaum SD (1996) Comparative properties of arginases. Comp Biochem Physiol B 114:107–132
Koesling D, Bohme E, Schultz G (1991) Guanylyl cyclases, a growing family of signal-transducing enzymes. FASEB J 5:2785–2791
Michikawa H, Mitsui Y, Yoshigaki JF, Yokoyama MH, Furuyama S, Sugiya H (1998) cGMP production is coupled to Ca2+-dependent nitric oxide generation in rabbit parotid acinar cells. Cell Calcium 23:405–412
Mitsui Y, Yasuda N, Furuyama S, Sugiya H (1997) Nitric oxide synthase activities in mammalian parotid and submandibular salivary glands. Archs Oral Biol 42:621–624
Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142
Mori M, Gotoh T (2000) Regulation of nitric oxide production by arginine metabolic enzymes. Biochem Biophys Res Commun 275:715–719
Morris MM Jr (2002) Regulation of enzymes of the urea cycle and arginine metabolism. Annu Rev Nutr 22:87–105
Nathan C (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J 6:3051–3064
Palmer RMJ, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature (Lond) 327:524–526
Reczkowski RS, Ash DE (1994) Rat-Liver arginase-kinetic mechanism, alternate substrates, and inhibitors. Arch Biochem Biophys 312:31–37
Rüegg UT, Russell AS (1980) A rapid and sensitive assay for arginase. Analyt Biochem 102:206–212
Wu G, Morris SM (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336:1–17
Zamecka E, Porembska Z (1988) Five forms of arginase in human tissue. Biochem Med Metab Biol 39:258–266
Acknowledgements
This work was supported in part by a grant from the Ministry of Education, Culture, Sports, Science and Technology to promote 2003-Multidisciplinary Research Projects (in 2003–2007). The protocols were approved by the Animal Care and Ethics Committee of the Nihon University School of Dentistry at Matsudo.
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Communicated by I.D. Hume
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Yasuda, N., Moriwaki, K. & Furuyama, S. Distribution and properties of arginase in the salivary glands of four species of laboratory mammals. J Comp Physiol B 174, 237–242 (2004). https://doi.org/10.1007/s00360-003-0407-z
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DOI: https://doi.org/10.1007/s00360-003-0407-z