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Trehalose-6-Phosphate, a New Regulator of Yeast Glycolysis That Inhibits Hexokinases

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Trehalose-6-Phosphate, a New Regulator of Yeast Glycolysis That Inhibits Hexokinases View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Volume 329, number 1,2, 51-54 FEBS 12858 August 1993 0 1993 Federation of European Ei~h~ical Societies ~145793/93/$6.~ Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases Miguel A. Blizquez, Rosario Lagunas, Carlos Gancedo and Juana M. Gancedo Institute de Investigaciones Biom&dicas de1 CSIC, Madrid, Spain Received 2 July 1993 Tre~lo~6-phosphate (P) ~mpetitively inhibited the hexokinases from ~~cc~omyee~ cerevisiae. The strongest inhibition was observed upon hexokinase II, with a K, of 40 FM, while in the case of hexoklnase I the K, was 200 NM. Glucokinase was not inhibited by trehalose-6-P up to 5 mM. This inhibition appears to have physiological significance, since the intracellular levels of trehalose-6-P were about 0.2 mM. Hexokinases from other organisms were also inhibited, while glucokinases were unaffected. The hexokinase from the yeast, Yarrowia iipolytica, was particularly sensitive to the inhibition by trehalose-6-P: when assayed with 2 mM fructose an apparent K, of 5 PM was calculated. Two 5. cerevisiae mutants with abnormal levels of trehalose-6-P exhibited defects in glucose metabolism. It is concluded that trehalose-6-P plays an important role in the regulation of the first steps of yeast glycolysis, mainly through the inhibition of hexokinase II. Trehalose-6-phosphate; Hexokinase; Glycolysis; Yeast 1. PRODUCTION turned out to be allelic [9], and strains bearing them become depleted of ATP upon addition of glucose and Control of the glycolytic flux in Succhurowryces cere- accumulate fructose-l ,6-bisphosphate up to 20 mM visicze has been considered to occur mainly at the level [6,7,10], suggesting that the rate of the first glycolytic of phosphofructokinase and pyruvate kinase. steps exceeds the capacity of the glycolytic pathway. Phosphofructokinase is regulated through activation by The sequence of the CIFZ gene [lo] encodes the small fructose-2,6-bisphosphate, phosphate (P) and AMP, subunit of the trehalose-6-P synthase/trehalose-6-P and inhibition by ATP, while pyruvate kinase activity phosphatase complex [ 11,123. A plausible explanation is modulated by its activation by fructose-l,(i-bis- for the growth behaviour and the metabolic defects of phosphate (for a review see [l]). However, since cifl strains could be that either trehalose or trehalose-6- phosphof~~tokinase does not catalyze the first irrevers- P play a role in the regulation of the yeast glycolytic ible step in the utilization of glucose, its regulation is not flux. We show in this article that trehalose-6-P inhibits sufficient to control the rate of glucose utilization, and sugar phospho~lation. The stron~st inhibition is ob- thus some mechanism should exist to regulate the rate served upon hexokinase II, which is the most abundant of glucose transport, phosphorylation, or both. Regula- isoenzyme of hexokinase during growth of S. cerevisiae tion of glucose transport by glucose-6-P was suggested on glucose [13]. by Sols [2], but experimental results obtained using mu- tants affected in phosphoglucose isomerase activity did 2. MATERIALS AND METHODS not support this idea [3,4]. Besides, none of the yeast kinases that phosphorylate glucose are sensitive to glu- 2.1. Yeast strains and growth conditions cose-6-P, in contrast with the mammalian hexokinase The following strains were used: W303-IA, MATa ade2-1 his3-1 I, 15 ura3-I leu2-l trpl-I [14]; WDC3A, MATa ade2-l his3-II,15 ura3-I PI- feu2-1 trpl-i c1fl::HiS3 (constructed for this work); S2072D, h4ATa The need for a regulation of the first steps of yeast arg4 leul trpl rhr4 gal2 [15]; tsl265, MATa arg4 Ieul trpl thr4 gal2 glycolysis is illustrated by the pattern of ambulation trel [16]; CJM 018, MATa Hxlyl hxk2 glkl; CJM 019, MATa hxkl of metabolites in certain yeast mutants upon addition HXK? glkl; CJMl18, MATa hxkl hxk2 GLKI; Yarrowia ~i~olyti~a INAG 35667, MATa 1~~11-23ura3-302 leu2-270; Kluyveromyces factis of glucose [6-81. Yeast strains carrying the mutations Yll40 (NRL) and Zygosaccharomyces bailii. They were grown at fdpl [6] or cifl [7] do not grow on glucose, although the 30°C in 2% peptone, 1% yeast extract and 2% glucose, except WDC- glycolytic enzymes are operative. These mutations 3A which was grown with 2% galactose, and ts1265 which was grown at 24°C. Correspondence aaiiress: J.M. Gancedo, Instituto de Investigaciones Biomedicas de1 CSIC, Arturo Duperier 4, E-28029 Madrid, Spain. 2.2. Enzymatic assays and metabolite determination Extracts were obtained by shaking in a vortex 100 mg of cells in 0.5 Dedicated affectionately to the memory of Nice Van Uden who loved ml of ice-cold 20 mM imidazol, pH 7, with 1 g glass beads of 0.5 mm yeasts. diameter, for 4 periods of 1 min, with 1 min intervals in ice after each ~ab~~hed by Elsevier Science ~abl~hers B. F! 51 Volume 329, number 1,2 FEBSLETTERS August 1993 period. The liquid was centrifuged for 10 min at 700 x g and the results obtained: trehalose-6-P inhibited the phospho- supematant was used for enzyme assays. Phosphorylating activity on rylation of glucose and fructose by hexokinase II. This glucose or fructose was assayed spectrophotometrically as in [13]. inhibition was competitive with either substrate, and a To measure intracellular glucose, 200 mg of yeast cells (wet weight) were collected by rapid filtration, washed twice with 15 ml ice-cold Ki of 40 ,uM was calculated. The inhibition of hexoki- water, and extracted according to Gamo et al. [17]. Glucose was nase I activity was much weaker than that observed for assayed spectrophotometrically with hexokinase [18]. hexokinase II (Ki of 200 PM). Glucokinase remained Trehalose-6-P was measured in extracts obtained as above, heated unaffected even when assayed at concentrations of tre- at 100°C for 10 min in the presence of 0.1 M NaOH, and neutralized halose-6-P as high as 5 mM. Trehalose itself had no with HCI. The concentration of trehalose-6-P was assessed by the inhibition produced in a partially purified preparation of hexokinase effect, either on the phosphorylation of the sugars or on from Y lipolytica. Trehalose-6-P inhibits this enzyme with an appar- the inhibition produced by trehalose-6-P. The inhibition ent K, of 5 PM when assayed with 2 mM fructose. The enzyme was caused by trehalose-6-phosphate was non- competitive purified free from glucokinase as described by Hirai et al. [19]. A with respect to ATP (data not shown). standard curve with pure trehalose-6-P (Sigma, St. Louis, MO) was run in parallel. Trehalose-6-P added to the extracts was recovered with yields superior to 90%, and the reproducibility of the procedure was 3.2. Effect of trehalose-6-P on glucose-phosphorylating good with a coefficient of variation of less than 10%. (A detailed activity from other organisms description of the method will be published elsewhere.) Extracts from different organisms were tested to ex- Dictyostelium discoideum was grown and extracted as in [ZO].Rat amine whether the glucose-phosphorylating activity brain homogenate was obtained as in [21]. was also inhibited by trehalose-6-P. The results are pre- 2.3. Other methods sented in Table I. In all the extracts tested where hexok- Transport was measured at 20°C with uniformly labelled glucose inase was present there was inhibition by trehalose-6-P. as described by Bisson and Fraenkel [22]. In those cases where glucokinase was the predominant Fermentation was measured. in a conventional Warburg respirome- ter at 30°C using 50 mM glucose. or the only phosphorylating activity, like Z hpolytica [19] or D. discoideum [23], the inhibition was weak or absent. Partially purified hexokinase from I: lipolytica 3. RESULTS AND DISCUSSION free of glucokinase was particularly sensitive to treha- lose-6-P and exhibited an apparent Ki of 5 ,uM when 3.1. Inhibition of glucose-phosphorylating enzymes from assayed with 2 mM fructose. Based on this property it S. cerevisiae by trehalose-6-P was possible to develop a sensitive method of assaying Yeast strains expressing only one of the three en- trehalose-6-P (see section 2). The glucokinase from E zymes able to phosphorylate glucose were used to test lipolytica was not inhibited by trehalose-6-P up to 1 the possible effect of trehalose-6-P. Fig. 1 shows the mM. Hexokinase II Hexokinase II I 1000 2000 3000 4000 5000 0 100 200 300 400 500 600 v/mMglucose v / mM fructose 600 HexokinaseI 500 0 1000 2000 3000 4000 5000 500 1000 1.500 2000 2500 3000 v/mMglucose v/mMglucase Fig. 1. Inhibition of hexokinases and glucokinase from S. cerevisiue by trehalose-6-P. Phosphorylating activities were assayed, as described in section 2, in extracts from strains CJM019, CJM018 or CJMll8 that express only hexokinase II, hexokinase I or glucokinase, respectively. The concentrations of added trehalose-6-P were as follows: o, none; l, 0.1 mM; q, 0.4 mM; w, 1 mM. v is expressed in nmol/min . mg protein. 52 Volume 329, number 1,2 FEBSLETTERS August 1993 3.3. Possible physiological value of the inhibition 2000 r Changes in the activity of an enzyme in response to a metabolite may have only a curiosity value. An impor- 1600 tant requisite for one effect to be of physiological signif- icance is that the concentration needed to produce it in vitro, is reached in vivo under some physiological cir- cumstances.
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