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Regulation of Pyrimidine Biosynthesis by Purine and Pyrimidine Nucleosides in Slices of Rat Tissues’

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Regulation of Pyrimidine Biosynthesis by Purine and Pyrimidine Nucleosides in Slices of Rat Tissues’ ARCHIVES OF BIOCHEMISTRY AND BIOPHYSKS Vol. 188, No. 1, May, pp. 194-205, 1978 Regulation of Pyrimidine Biosynthesis by Purine and Pyrimidine Nucleosides in Slices of Rat Tissues’ DAVID E. CRANDALL, CAROL J. LOVATT, AND GEORGE C. TREMBLAY Department of Biochemistry and Biophysics, University of Rhode Island, Kingston, Rhode Island 02881 Received November 4, 1977; revised January 27, 1978 Evidence of the primary sites for the regulation of de novo pyrimidine biosynthesis by purine and pyrimidine nucleosides has been obtained in tissue slices through measurements of the incorporation of radiolabeled precursors into an intermediate and end product of the pathway. Both purine and pyrimidine nucleosides inhibited the incorporation of [‘“Cl- NaHCO:< into erotic acid and uridine nucleotides, and the inhibition was found to be reversible upon transferring the tissue slices to a medium lacking nucleoside. The ammonia- stimulated incorporation of [‘4C]NaHCOa into erotic acid, which is unique to liver slices, was sensitive to inhibition by pyrimidine nucleosides at physiological levels of ammonia, but this regulatory mechanism was lost at toxic levels of ammonia. Adenosine, hut not uridine, was found to have the additional effects of inhibiting the conversion of [%]orotic acid to UMP and depleting the tissue slices of PKPP. Since PKPP is required as an activator of the first enzyme of the de novo pathway, CPSase II, and a substrate of the fifth enzyme, OPRTase, these results indicate that adenosine inhibits the incorporation of [‘%]NaHC03 into erotic acid and the incorporation of [‘%]orotic acid into UMP by depriving CPSase II and ‘OPRTase, respectively, of PRPP. Uridine or its metabolites, on the other hand, appear to control the de nouo biosynthesis of pyrimidines through end product inhibition of an early enzyme, most likely CPSase II. We found no evidence of end product inhibition of the conversion of erotic acid lo UMP in tissue slices. Studies employing cell-free extracts of genase are inhibited by erotic acid (3-5); mammalian tissues have demonstrated that and orotidine-5’-phosphate decarboxylase several of the enzymes of the orotate path- (ODCase) is inhibited by UMP and CMP way for the de nouo biosynthesis of pyrim- (6,7). Attempts to determine which of these idines are subject to regulation by end prod- enzymes has physiological importance as a ucts or intermediates of the pathway. The regulatory site include several recent stud- glutamine-dependent carbamoylphosphate ies employing intact cells. Work performed synthetase (CPSase II)” is inhibited by in our laboratory has shown that uridine UTP (1) and activated by &phosphoribo- inhibits the incorporation of [‘4C]NaHC03, syl-I-pyrophosphate (PRPP) (2); dihy- but not [‘4C]carbamoylphosphate (CP) or droorotase and dihydroorotate dehydro- [‘4C]carbamoylaspartate, into erotic acid in ’ This investigation was supported by Public Health slices of several rat tissues (8, 9), and Ito Service Research Grant No. CA17131 from the Na- and Uchino have found that uridine inhibits tional Cancer Institute. the incorporation of [‘4C]NaHC03 into car- ’ Abbreviations used: CPSase I, ATP:carbamate bamoylaspartate in human lymphocytes phosphotransferase (dephosphorylating; EC 2.7.2.5); (10). In addition, the incorporation of CPSase II, ATP:carbamate phosphotransferase (de- [14C]NaHC03, but not [14C]CP, into uridine phosphorylating, amido transferring; EC 2.7.2.9); nucleotides was stimulated in perfused liver PRPP, 5phosphoribosyl-I-pyrophosphate; CP, car- after UTP levels had been depleted by bamoylphosphate; OPRTase, orotidine-5’.phosphate: treatment with galactosamine (11). These pyrophosphate phosphoribosyltransferase (EC 2.4.2.10); ODCase, orotidine-5’-phosphate decarboxyl- results are consistent with the interpreta- ase (EC 4.1.1.23); ACTase, aspartate carbamoyltrans- tion that the regulation of pyrimidine bio- ferase (EC 2.1.3.2); uv, ultraviolet. synthesis observed in the intact cells of 194 ooO3-9861/78/1881-0194$02.00/O Copyright Q 1978 by Academic Press, Inc. All rights of reproduction in any form reserved REGULATION OF PYRIMIDINE BIOSYNTHESIS 195 mammalian tissues occurs at CPSase II. purine nucleosides on the de novo pathway We have recently demonstrated that CP for pyrimidine biosynthesis. Work in our produced from ammonia by CPSase I laboratory has demonstrated that purine within liver mitochondria constituted at nucleosides inhibit the incorporation of least 80% of the CP incorporated into erotic [‘4C]NaHC03 into erotic acid in the chick acid when liver slices were incubated with oviduct and in the rat brain and mammary ammonia and ornithine at physiological gland (9, 18), but the mechanism of inhibi- concentrations (12). Since CPSase I was tion of pyrimidine biosynthesis by purines thus revealed to be an important source of has remained a matter for conjecture. In CP for hepatic pyrimidine biosynthesis, we the present paper, we report results which sought evidence for regulation of the show that adenosine inhibits both the in- CPSase I-catalyzed production of CP or of corporation of bicarbonate into erotic acid the export of CP from liver mitochondria, and the conversion of erotic acid to uridine or both, by end products of the de novo nucleotides. Since the metabolism of aden- pathway. osine consumes PRPP and since PRPP is An additional mechanism of control, at a involved in the de novo biosynthesis of site other than CPSase II, has been sug- pyrimidine nucleotides as an activator of gested by the observation of Hoogenraad CPSase II and as a substrate for OPRTase, and Lee (13) that incubation of rat hepa- we tested the possibility that inhibition of toma cells with uridine resulted in a rapid pyrimidine biosynthesis by adenosine loss of orotate phosphoribosyltransferase might be associated with a depletion of the (OPRTase), but not any of the other en- tissue levels of PRPP. Our findings, re- zymes of the orotate pathway; this result ported herein, show that adenosine, but not led the authors to conclude that OPRTase uridine, reduces the PRPP concentrations is also a principal site of control in the de in tissue slices; thus adenosine most likely novo biosynthesis of pyrimidines. Earlier inhibits the de novo biosynthesis of pyrim- measurements showing that OPRTase may idines by removing the PRPP needed for be the rate-limiting enzyme in the orotate the reactions catalyzed by CPSase II and pathway of Ehrlich ascites cells (14) and OPRTase. the observation that a mild erotic aciduria occurs during normal human pregnancy MATERIALS AND METHODS (15) also indicate that OPRTase may be a Chemicals. All radiolabeled chemicals and Aquasol site of regulation, or at least of interruption, (liquid scintillation cocktail) were purchased from of the de novo biosynthesis of pyrimidine New England Nuclear Corp., Boston, Massachusetts. nucleotides. In order to assess the relative The mixed enzymes orotidylate phosphoribosyltrans- physiological importance of regulation at a ferase and orotidylate decarboxylase (prepared from site early in the de novo pathway (CPSase yeast) were obtained from Sigma Chemical Co., St. II) or late in the pathway (OPRTase), we Louis, Missouri. Acids, bases, and salts were purchased tested the effect of uridine on the incorpo- from Fisher Scientific Co., Boston, Massachusetts, and all other chemicals were purchased from Sigma Chem- ration of [‘4C]NaHC03 and [6-‘4C]orotic ical Co., St. Louis, Missouri. acid into uridine nucleotides in slices of rat Preparation of tissues. Tissues from adult male liver and spleen. The results of these meas- rats weighing 200-250 g were employed in these stud- urements, reported below, support the in- ies; these animals were obtained from the Charles terpretation that feedback regulation of de River Colony, Boston, Massachusetts. The animals novo pyrimidine biosynthesis occurs pri- were killed by decapitation and the tissues of interest marily at an early point in the pathway, were quickly excised and placed in ice-cold saline. most likely at the reaction catalyzed by Tissue slices were prepared using a Stadie-Riggs tissue CPSase II. slicer (Arthur H. Thomas Co.), blotted on filter paper, The observation that the addition of the weighed, and transferred to flasks containing Krebs Improved Ringer II solution (19) to which various purine nucleoside adenosine to cultures of intermediates and inhibitors of pyrimidine biosyn- mammalian cells causes pyrimidine star- thesis had been added as indicated. vation with resulting cell death (16, 17) Measurement of the incorporation of “C-labeled prompted us to examine the influence of precursors into erotic acid. Studies on the incorpo- 196 CRANDALL, LOVATT, AND TREMBLAY ration of [‘4C]NaHC03 into erotic acid were performed tallized from 67% ethanol, as above, to constant spe- using 500 mg of tissue slices incubated at 37.5”C for 3 cific activity, which rarely required more than two h in 20 ml of Krebs Improved Ringer II solution (19) recrystallizations. The specific activity of the [‘“Cl- I which was supplemented with 6-azauridine (10 mM) to UMP obtained from the final recrystallization was inhibit the conversion of erotic acid to UMP (20). The used to calculate the incorporation of [‘4C]NaHC0:j [‘4C]orotic acid synthesized during the 3-h incubation into uridine nucleotides during the 3-h incubation was isolated from the reaction mixture by cocrystalli- period. This method, employing Krebs Improved zation with carrier monosodium orotate as described Ringer II solution made 30 mM in NaHCO:j, was
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