N-Acetylglucosamine Assimilation in Escherichia coli
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1 JOURNAL OF BACTERIOLOGY, Feb. 1968, p American Society for Microbiology Vol. 95, No. 2 Prinzted in U.S.A. N-Acetylglucosamine Assimilation in Escherichia coli and Its Relation to Catabolite Repression' WALTER J. DOBROGOSZ Department of Microbiology, North Carolina State University, Raleigh, North Carolina 2767 Received for publication 25 November 1967 The ability of N-acetylglucosamine to enhance catabolite repression by glucose was studied by using cultures grown on a combination of these substrates. Under these conditions, it was shown that two-thirds of the N-acetylglucosamine utilized was routed into dissimilatory pathways, whereas the remaining one-third was channeled into biosynthesis. It was established that over 5% of the N-acetylglucosamine assimilated was incorporated directly into amino sugar polymers. It was also shown that this exogenous supply of N-acetylglucosamine was in fact used preferentially over glucose as the precursor for amino sugar polymer biosynthesis. These findings provided support for the prediction that catabolite repression in Escherichia coli may be interrelated with certain reactions involved in amino sugar biosynthesis. Glucose repression of,b-galactosidase formation in Escherichia coli was shown to be significantly enhanced when N-acetylglucosamine (AcGN) was added to the growth medium. It was found that the AcGN was utilized under these conditions and that a high percentage was assimilated into the cells. These findings, described in the accompanying report (4), indicated that catabolite repression may be interrelated with certain reactions involved in amino sugar metabolism. To further examine this possibility, it was necessary to obtain information concerning the general nature of AcGN metabolism under the conditions in which its specific effects on repression are manifested. This is the primary objective of the present study. Many of the enzymes and pathways involved in amino sugar metabolism by bacteria have been described and characterized. Much of this work has been done with the gram-positive bacteria, although E. coli has received some attention in this regard (13, 15). The information that is available, however, is largely derived from in vitro studies, whereas in vivo studies along these lines are scarce. This is a handicap when one needs to consider relationships between the concomitant metabolism of amino sugars and hexoses. As a secondary purpose, the present report sheds some light on this relationship. 1 Paper no. 254 of the Journal Series of the North Carolina State University Agricultural Experiment Station, Raleigh, N.C. MATERIALS AND METHODS Chemicals. Glucosamine hydrochloride and (AcGN) were purchased from Mann Research Laboratories, New York, N.Y. Glucosamine-1-14C and N-(J-'4C) acetylglucosamine and glucose-j-14c were obtained from New England Nuclear Corp., Boston, Mass. N-acetylglucosamine-1-'4C was prepared from the glucosamine-1-14c by acetylation according to the procedure of Roseman and Ludoweig (14) as indicated elsewhere (4). Dowex 5 ion exchange resin was purchased from Calbiochem (Los Angeles, Calif.) as the reagent Bio-Rad AG 5W-X8 (2-4 mesh [H+]). 2, 5-Diphenyloxazole (PPO) and 1,4-bis-2- (5-phenyloxazolyl)-benzene (POPOP) were products of Packard Instrument Co., Inc., Downers Grove, Ill. All other chemicals were of reagent grade and are readily available. Culture and cultural conditions. E. coli ML3 was used in all experiments. The organism was grown as described elsewhere (3, 8) in media containing, per liter: K2HPO4, 28 g; KH2PO4, 8. g; MgSO4.7H2,.1 g; (NH4)2 SO, 1. g; ph 7.2. Prior to inoculation,.25% vitamin-free, acid hydrolyzed casein was added to the medium. Unless otherwise indicated, substrates were added at.2 M concentration. All cultures were grown aerobically at 37 C. Cultures grown in radiorespirometer vessels were continuously flushed with oxygen during the 2-hr growth period. Determination of 14C2. Cultures in exponential growth were harvested, washed, and inoculated into fresh media contained in radiorespirometer vessels, as described elsewhere (8). N-acetyl-1-14C-glucosamine or N-acetylglucosamine-1-14C, stored in side arms on the vessels, was added at zero-time, when the cultures contained 5,ug (dry weight) of cells per ml. The cul- 585
2 586 DOBROGOSZ J. BACTERIOL. tures were continuously flushed with 2, and the i4c2 produced during the subsequent 2 hr of growth was collected by passing the carrier 2 and metabolic C2 into an ethanolamine trap. Samples of the ethanolamine solutions were counted in a liquid scintillation counter (Packard Instrument Co.). Determination of assimilated 14C. Cells were placed in an equal volume of 1% trichloroacetic acid, allowed to stand for 3 min in an ice bath, and then filtered onto membrane filters as described in the previous report (8). The dried filters were counted in the scintillation counter after addition of 15 ml of scintillation fluid (.4% PPO and.1% POPOP in tcluene). Determination of nongaseous end products. After 2 hr of growth in the presence of the appropriate 14C label, 5 ml of the culture medium was added to 5 ml of a cold carrier-acid mixture; it was then centrifuged, and the supernatant fluid was analyzed for 14C end products by silicic acid chromatography. This procedure was identical to that described elsewhere (3). Determination of amino sugars. Glucosamine, galactosamine, and AcGN were determined colorimetrically according to the procedure of Levvy and Mc- Allan (7), with the potassium tetraborate reagent (.7 M) prepared as described by Reissig et al. (11). The acetylation step was omitted when analyzing the AcGN. Cell fraction studies. Cell constituents were chemically fractionated by the trichloroacetic acid procedure described by Roberts et al. (12). The protein fraction, i.e., the hot trichloroacetic acid-insoluble fraction was divided into two fractions by a trypsin treatment according to the procedure of Park and Hancock (1). The hot trichloroacetic acid-insoluble residue was suspended in 1.9 ml of.5 M (NH4)2CO3 containing.5 M NH4OH (ph, 8.2). A.1-ml amount of trypsin solution (1 mg/ml) was added, and the mixture was incubated at 37 C for 5 hr. The material was centrifuged, and the supernatant fluid was designated the trypsin-soluble fraction; the remaining pellet was termed the residue fraction rich in cell wall constituents. Hydrolysis procedure. Cell fractions were dried in vacuo at 5 C. A 5-ml amount of 4 N HCl was added, and the material was transferred to tight-sealing tubes; it was flushed with nitrogen for 5 min, sealed, and placed in a boiling-water bath for 6 hr. At the end of this time, the HCl was evaporated in vacuo at 5 C, 1 ml of water was added to the residue, and the evaporation step was repeated. The dried hydrolysates were dissolved in 1.5 ml of.33 N HCI; they were then filtered through Whatman no. 1 paper and used for direct 4-C counting and application to Dowex 5 [H+] columns for amino sugar analyses. Amino sugar chromatography. The 14C-labeled hydrolysates dissolved in.33 N HCl were applied to Dowex 5 [H+] (5) columns (1 X 37 cm) along with 5.5 mg of glucosamine and 8 mg of galactosamine as cold carriers and column-reference indicators. Elution was conducted with.33 N HCl applied to the column at a constant rate by use of a peristaltic pump. Fractions (5.5 ml) were collected at a flow rate of approximately 17 ml/hr. After elution with approximately 275 ml of.33 N HCl, the column elution was completed by elution with approximately 8 ml of 4 N HCI. Portions (.5 ml) of each fraction were placed in scintillation vials; 15 ml of the tt21 scintillation fluid prepared according to the procedure of Patterson and Greene (9) was added, mixed, and the samples were counted under previously standardized counting conditions. RESULTS The data presented in Fig. 1 show the incorporation of glucosamine and AcGN into E. coli cells grown in media containing glucose and labeled amino sugar. Glucosamine was barely incorporated into the cells under these conditions; whereas, AcGN was rapidly assimilated, as demonstrated by the incorporation of 14C from AcGN-1-"4C. When the 14(C was located in the acetyl portion of the molecule, only a low rate of label incorporation was detected, and this occurred only after a substantial lag period. These data clearly show that exogenous AcGN was readily incorporated into cells growing on glucose, but that the incorporation was preceded by deacetylation of the AcGN to glucosamine. To determine the overall fate of the AcGN metabolized under these conditions, an inventory was conducted on the distribution of 14C after 12 min of growth in media containing either N-acetyl-1-14C-glucosamine or N-acetylglucos- 1o a- c 4 2 a. N-Acetyl- Glucosamine _4C 1Ī- C -// N -Acetyl [- I -1'4C Glucosomine -~ --Glucosomine -1C /LGroms Dry Weight / Ml FIG. 1. Incorporation of exogenous glucosamine and N-acetylglucosamine into Escherichia coli growing on glucose. When aerobic cultures growing exponentially on glucose reached a cell concentration of 65 ig (dry weight) per ml, 4.5 X 1-3 M levels of 14C-labeled glucosamine or N-acetylglucosamine were added. Samples were removed at intervals thereafter, and the cells were filtered and counted after washing with cold 5% trichloroacetic acid. The basal medium in each case contained.25% casein hydrolysate. (-).2M glucose plus 4.5 X 1-3 M glucosamine-1-14c [3.8 X 14 counts per min (cpm) per,umole]; ().2 m glucose plus 4.5 X 1-3 M N-acetyl-1-14C-glucosamine (3.8 X 14 cpm/,umole); (A).2 M glucose plus 4.5 X 1-3 M N-acetylglucosamine-1-14C (3.6 X 14 counts per min per,umole).
3 VOL. 95, 1968 N-ACETYLGLUCOSAMINE ASSIMILATION 587 amine-1-14c. The results of this carbon balance study are shown in Table 1. Total 14C recoveries were good with all 14C accounted for as incorporation into cells, 14CO2 formation, or "4CO2 present in the supernatant fraction. Analysis of this latter fraction by silicic acid chromatography and determination of unused AcGN also showed good 14C recoveries. Essentially all of the label was recovered as unused substrate or as 14C labeled acetate. Table 2 shows that essentially all of the 14C in N-acetyl-1-14C-glucosamine dissimilated was recovered as acetate in the medium. With N-acetylglucosamine-1-'4C, however, only two-thirds of the 14C was found as acetate in the medium; the remaining one-third of the label was found assimilated into the cells. The cells obtained from experiments similar to those described above were fractionated with the trichloroacetic acid method and 14C distributions were determined (12). More than onehalf of the label assimilated during growth in the presence of N-acetyl-1-'4C-glucosamine appeared in the alcohol-soluble fraction, with the remainder TABLE 1. Distribution and recovery of 14C after growth ofescherichia coli in medium containing l4c-labeled N-acetylglucosamine Distribution of 14C In culture fraction Total radioactivity determined during growth with" N-acetyl N-acetyl [1-14CJ glucosaglucosamine mine 1-4C (14 counts/ (14 counts/ min) min) Total added Cell fraction CO2 fraction Supernatant fraction Recovery (%) In supernatant fraction Supernatant total Calculated as unused N- acetylglucosamine Determined as 14C-acetateb Recovery (%) a Cultures grown for 12 min in radiorespirometer vessels flushed continuously with oxygen. The medium in one vessel contained.2 M glucose and 4 X 13 M N-acetyl [J-54C]-glucosamine (3.34 X 14 counts per min per,umole). The medium in the other vessel contained.2 M glucose and 6.2 X 1-3 M N-acetylglucosamine-1-'4C (2.38 X 14 counts per min per /Amole). b Determined after silicic acid chromatography of the culture supernatant fraction as described in Materials and Methods. TABLE 2. Distribution ofradioisotope during growth of Escherichia coli on "4C-N-acetylglucosamine Growth substrates Metabolic fraction 14C distributiona Glucose + N-acetyl-[1-_4C] CO2 2 glucosamine Acetate 93 Cells 5 Glucose + N-acetylglucosa- CO2 8 mine-1_14c Acetate 6 Cells 32 a Percentage of 14C distribution calculated on the basis of the amount of N-acetylglucosamine utilized as determined in the 14C recovery experiments described in Table 1. distributed in the cold trichloroacetic acidsoluble fraction and the hot trichloroacetic acidinsoluble residue (Table 3.) This pattern is essentially identical to that obtained when E. coli is grown on "4C-labeled acetate (12), again indicating that AcGN is deacetylated prior to its assimilation into cell material. The 14C assimilated from N-acetylglucosamine-1-14C was found to be widely distributed among the cell fractions, with the hot trichloroacetic acid-soluble fraction containing the highest percentage. It was of interest, then, to determine to what extent AcGN-1-14C was directly incorporated into amino sugar-containing polymers as contrasted to randomized, nonspecific assimilation. For this purpose, fractions similar to those described in Table 3 were hydrolyzed with 4 N HCI, then concentrated and chromatographed on columns of Dowex 5 [H+] to determine the presence of amino sugars. Only glucosamine and galactosamine were identified in these experiments by use of colorimetric assay of added carrier material. Some of the results of this study are shown in Fig. 2 and Table 4. Cells were grown for 12 min in medium containing.2 M glucose and 1.8 x 1-3 M AcGN-I- 14C (1.95 X 14 counts per min per,umole). The cells were fractionated as described elsewhere, and each fraction was hydrolyzed and then chromatographed on Dowex 5 [H+], with cold glucosamine and galactosamine added as internal standards and reference points. The column fractions obtained after elution with.33 N HCI were counted and the resultant profiles graphed as shown in Fig. 2. High levels of '4C-glucosamine were observed in all fractions tested. Galactosamine was present primarily in the hot trichloroacetic acid-soluble and residue fractions. Peaks other than glucosamine and galactosamine were not identified. 14C recovery data from these chromatographic experiments
4 588 DOBROGOSZ J. BAmpERoL. TABLE 3. Distribution of radioactivity in cells grown with glucose and N-acetylglucosamine Cell fraction Incorporation during growth witha N-acetyl [l-14cj-lucosa- mine N-acetyl glucosamine 1-14C Whole cells Cold trichloroacetic acid soluble Alcohol soluble Alcohol-ether soluble.9 3. Hot trichloroacetic acid soluble Trypsin soluble lb Residue Recovery (%) a Cultures grown for 14 min in medium containing.2 M glucose and 1.2 X 1-3 M N-acetylglucosamine. N-acetyl [1-4C] -glucosamine, 33,4 counts per min per Amole; N-acetylglucosamine- 1_14C, 23,8 counts per min per,mole. b Per cent in trypsin-soluble and residue fractions combined. are listed in Table 4. Total radioactivity in each fraction is listed before and after acid hydrolysis. It was calculated that 48 to 82% of the counts were lost from the various fractions during hydrolysis. Of the 14C present in the hydrolysate, 16 to 68 % was accounted for in the various fractions as glucosamine and galactosamine after chromatographic analysis. From these data, it could be calculated that approximately 2% of the 14C assimilated into cells as AcGN-1-14C could be recovered as glucosamine-galactosamine. This value is an absolute minimum and does not take into account the material lost during hydrolysis. Approximately 5% of the '4C that survived hydrolysis was recovered as glucosamine-galactosamine. It was thus clear that a large percentage of the exogenous AcGN assimilated by cells growing on glucose and AcGN was incorporated into amino sugarcontaining polymers. This point was further established by the results shown in Fig. 3 and 4. In these experiments, cultures were grown with glucose and AcGN as before, but the AcGN was unlabeled and the glucose was labeled in the 1-14C position. A control culture in which AcGN was omitted was also analyzed. Both cultures were grown for 12 min; the cells were fractionated, the fractions hydrolyzed, and the hydrolysates chromatographed as previously described. The radioisotope profiles obtained from analysis of the GN 7Hot TCA Soluble ~~~~GaIN 2-3F Residue a.l ~ci,. L, 4 Cold TCA Soluble Ethanol Soluble Ether- Ethanol-TryVsin Soluble Fraction Number FIG. 2. Dowex 5 [H+] chromatography of amino sugars present in all cell fractions of Escherichia coli grown in medium containing glucose and N-acetylglucosamine-1-14C. Only the glucosamine (GN) and galactosamine (GalN) regions were identified in these chromatographic profiles. Cells grown for 2 hr in medium containing.25% casein hydrolysate,.2 M glucose, and 1.8 X 1-3 M N-acetylglucosamine-1-14C [1.95 X 14 counts per min (cpm) per,umole] were fractionated, hydrolyzed, and chromatographed as described in the text. The alcohol-ether-soluble fraction and the trypsin-soluble fractions (see Table 3) were pooled after hydrolysis and were chromatographed together. TCA = trichloroacetic acid. residue fraction of these cells are shown in Fig. 3. As expected, glucosamine and galactosamine were highly labeled in the cells grown on the glucose-1_14c. Also, when cold AcGN was added to the medium, the diversion of glucose into the glucosamine pathway was totally inhibited. It was surprising to find that 14C was still present in the galactosamine peak under these conditions. Similar findings were made when the hot trichloroacetic acid cell fractions were analyzed. Cold exogenous AcGN in the medium totally repressed the conversion of glucose-j-'4c into the glucosamine-containing polymers. It is thus clearly indicated that at least one major function of the added AcGN is its preferential incorporation into the amino sugar polymers of these cells. In addition, it would appear that this occurs in a regulated manner, possibly owing to an end product inhibition or repression effect.
5 VOL. 95, 1968 N-ACETYLGLUCOSAMINE ASSIMILATION 589 TABLE 4. Distribution of N-acetylglucosamine-1-14C assimilated during growth of Escherichia colia Fraction Distribution of total radioactivity Radioactivity in (1' counts/min) hydrolysate' Radioactivity of nonhydrolyzed Before hydrolysis After hydrolysis5 Loss during hydrolysis 1' counts/ Percentage fhractions min Total cells 41. _ Cold trichloroacetic acid soluble Alcohol soluble Alcohol-ether soluble _ Hot trichloroacetic acid soluble Trypsin soluble e Residue Total recovery Recovery (%) f a Culture (2 ml) grown aerobically for 12 min in medium containing.2 M glucose and 1.77 A.moles/ ml of N-acetylglucosamine-1-14C (1.95 X 14 counts per min per,umole). Cells harvested and washed twice in cold basal medium prior to fractionation. Eluted in major amino sugar fraction from Dowex 5 [H+] column. Recovered in major amino sugar fraction. d Dried fractions hydrolyzed with S ml of 4 N HC1 for 6 hr at 1 C., Alcohol-ether soluble fraction combined with trypsin fraction prior to hydrolysis step. f Recovery based on total assimilated radioactivity prior to hydrolysis. DIscussIoN This study begins to clarify the role that exogenous AcGN plays in enhancing catabolite repression by glucose. It was found, for example, that the acetyl portion of the molecule is required, but only in the sense that AcGN is metabolized by E. coli in the presence of glucose; whereas, the nonacetylated form is essentially inert under these conditions. This may be owing to inhibition of glucosamine kinase activity, but not AcGN kinase activity by glucose or related metabolites, as shown in Bacillus subtilis by Bates and Pasternak (1). In any event, deacetylation occurs with all the acetate recovered in the growth medium (Tables 2 and 3) and the amino sugar existing in the cells presumably as the glucosamine-6-p derivative. At this metabolic juncture (Table 3), approximately two-thirds of the glucosamine-6-p is deaminated to fructose-6-p, and is thus directly fed into the glycolytic route resulting in acetate, CO2, and energy formation in a manner indistinguishable from the glucose metabolizing system (3). The remaining one-third of the glucosamine- 6-P is assimilated into the cells with the major portion recovered as glucosamine and galactosamine from the amino sugar polymer fractions. As an absolute minimum value, 2% of the AcGN-1-'4C assimilated by the cells was recovered in these compounds. This calculation disregards loss of label by known degradation that occurs during hydrolysis (16). On a relative basis, 49.3% of the 14C in all the hydrolysates examined (Table 4) was recovered primarily as glucosamine with some galactosamine also accounted for in this regard. Since other amino sugars are known to exist in the gram-negative bacteria and were undoubtedly eluted but not identified from these columns, it is reasonable to conclude that at least 5% or more of the exogenous AcGN assimilated under the conditions described (i.e., concomitant with growth on glucose) was channeled into the biosynthesis of amino sugar polymers. It was also established that during growth on the combination of glucose and AcGN all of the glucosamine was formed from the exogenous supply of AcGN. Glucosamine formation from glucose was completely turned off, whereas galactosamine synthesis from glucose still occurred. This latter point indicates a need for re-examination in E. coli of the belief that glucosamine [as uridine diphosphate (UDP)-N- AcGN] is a direct precursor for galactosamine (as UDP-N-acetylgalactosamine) synthesis (17). It is known in mammalian systems (6) that UDP-N-AcGN acts as a feedback inhibitor in controlling amino sugar synthesis. UDP-N- AcGN was found to inhibit activity of L-glutamine-D-fructose-6-P transaminase-the first enzyme specifically involved in amino sugar synthesis. Kornfeld et al. (6) were unable to find similar inhibition of the transaminase activity in Salmonella paratyphi or E. coli B. They
6 59 DOBROGOSZ J. BACTERIOL. A 2a- B GN GaIN Glucose-I-14C 1 l S J 1- Is IV %f S Glucose-I- 14C+ 4 N-Acetylglucosamine 31 GN GaIN o , Fraction Number FIG. 3. Chromatography of'4c-labeled amino sugars in the residue fraction of cells grown on glucose-1-14c with and without exogenous N-acetylglucosamine. Onily the residue fractions were analyzed in these experiments. The procedures were identical to those described for Fig. 2. In this experiment, however, two cell systems were analyzed. The cells used for obtaining the data shown in (A) were grown in 2 ml ofmedium containing.2 M glucose-1_14c (1.25,ucuries/ml). The cells used for obtaining the data shown in (B) were grown in 2 ml of medium containing.2 M glucose-1-14c (1.25 iacuries/ml) plus 4.5 X 1-3 jf cold N-acetylglucosamine. GN = glucosamine; GalN = galactosamine. acknowledged the possibility that bacteria may regulate amino sugar nucleotide synthesis by end product repression or by feedback control focused on an enzyme other than the transaminase. Both possibilities remain to be explored in E. coli. In Bacillus subtilis, end product repression has been demonstrated for a number of the enzymes leading to amino sugar formation (1, 2). A predicted relationship between catabolite repression and amino sugar biosynthesis described in the accompanying study (4) was in large measure based on the studies described in this report; namely, that the ability of an exogenous supply of AcGN to augment an already severe repression by glucose was concomitant with the preferential incorporation of AcGN rather than glucose into the amino sugar polymers of the cells. AcGN dissimilation, however, also occurred under these conditions, so that one cannot directly rule out the possibility that enhancement of repression by AcGN was caused by some dissimilatory function. If one assumes, however, that catabolite repression occurring during growth on glucose (or gluconate) alone is in some way linked with amino sugar metabolism, one would have to reason that this association must be with amino sugar biosynthesis, since little if any amino sugar dissimilation would 4 A: a- N 51 B Glucose -I -14C GN GaIN 11 GN GaIN ( Fraction Number FIG. 4. Chromatography of '4C-labeled aminio sugars in the hot trichloroacetic acid fraction of cells grown on glucose-1_'4c with and without exogenous N-acetylglucosamine. All procedures were identical to those described in Fig. 3. In this case, however, the hot trichloroacetic acid-soluble cell fraction was analyzed. The cells used for obtaining the data shown in (A) were grown in 2 ml of medium containing.2 M glucose-1-14c (1.25 A.curies/ml). The cells used for obtaining the data shown in (B) were grown in 2 ml of medium containing.2 m glucose-1-_4c (1.25 Ascuries/ ml) plus 4.5 X 1-3 M cold N-acetylglucosamine. GN = glucosamine; GalN = galactosamine. be expected to occur under these conditions. It is, of course, evident that a more direct approach is needed for evaluating this hypothesis. In this connection, it would be of value to examine mutant cultures exhibiting various alterations in catabolite repression as well as alterations in repressor source and amino sugar metabolism. Mutants of this nature are currently being collected and studied. ACKNOWLEDGMENTS This investigation was supported by National Science Foundation grant GB-4952, by Public Health Service grant AI-672 from the National Institute of Allergy and Infectious Diseases, and by Public Health Service Research Career Development Award K3- Al-11,139, to the author, from the National Institute of Allergy and Infectious Diseases. The author gratefully acknowledges the excellent technical assistance of Janet Haire.
7 VOL. 95, 1968 N-ACETYLGLUCOSAMINE ASSIMILATION 591 LITERATURE CITED 1. BATES, C. J., AND C. A. PASTERNAK Further studies on the regulation of amino sugar metabolism in Bacillus subtilis. Biochem. J. 96: BATES, C. J., AND C. A. PASTERNAK The incorporation of labelled amino sugars by Bacillus subtilis. Biochem. J. 96: DOBROGOSZ, W. J Altered end-product patterns and catabolite repression in Escherichia coli. J. Bacteriol. 91: DOBROGOSZ, W. J Effect of amino sugars on catabolite repression in Escherichia coli. J. Bacteriol. 95: GARDELL, S Separation on Dowex 5 ion exchange resin of glucosamine and galactosamine and their quantitative determination. Acta Chem. Scand. 7: KORNFELD, S., R. KORNFELD, E. F. NEUFELD, AND P. J. O'BRIEN The feedback control of sugar nucleotide biosynthesis in liver. Proc. Natl. Acad. Sci. U.S. 52: LEVVY, G. A., AND A. McALLAN The N- acetylation and estimation of hexosamines. Biochem. J. 73: OKINAKA, R. T., AND W. J. DOBROGOSZ Catabolite repression and pyruvate metabolism in Escherichia coli. J. Bacteriol. 93: PATTERSON, M. S., AND R. C. GREENE Measurement of low beta-emitters in aqueous solution by liquid scintillation counting of emulsions. Anal. Chem. 37: PARK, J. T., AND R. HANCOCK A fractionation procedure for studies of the synthesis of cell-wall mucopeptide and of other polymers in cells of Staphylococcus aureus. J. Gen. Microbiol. 22: REISSIG, J. L., J. L. STOMINGER, AND L. F. LELOIR A modified colorimetric method for the estimation of N-acetylamino sugars. J. Biol. Chem. 217: ROBERTS, R. B., P. H. ABELSON, D. B. CowaE, E. T. BOLTON, AND R. J. BRITTEN Studies of biosynthesis in Escherichia coli. Carnegie Inst. Wash. Publ ROSEMAN, S Metabolism of connective tissues. Ann. Rev. Biochem. 28: ROSEMAN, S., AND J. LUDOWEIG N-acetylation of the hexosamines. J. Am. Chem. Soc. 76 : SALTON, M. R. J The bacterial cell wall. Elsevier Publishing Co., New York. 16. SPIRO, R. G Analysis of sugars found in glycoproteins, p In S. P. Colowick and N.. Kaplan [ed.], Methods in enzymology, vol. 8. Academic Press, Inc., New York. 17. STROMINGER, J. L Mononucleotide acid anhydrides and related compounds as intermediates in metabolic reactions. Physiol. Rev. 4: Downloaded from on September 24, 218 by guest
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