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J Biol Chem, Vol. 275, Issue 13, 9447-9451, March 31, 2000

Thioredoxin Activation of Phosphoribulokinase in a Bi-enzyme Complex from Chlamydomonas reinhardtii Chloroplasts^*

Luisana Avilan, Sandrine Lebreton^§, and Brigitte Gontero^§¶

From the ^§ Institut Jacques MONOD (UMR 7592), CNRS-Universités Paris VIVII, 2 Place Jussieu, 75251 Paris Cedex 05, France

	ABSTRACT

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

The activation of oxidized phosphoribulokinase either "free" or as part of a bi-enzyme complex by reduced thioredoxins during the enzyme reaction was studied. In the presence of reduced thioredoxin, the product of the reaction catalyzed by phosphoribulokinase within the bi-enzyme complex does not appear in a linear fashion. It follows a mono-exponential pattern that suggests a slow dissociation process of the bi-enzyme complex in the assay cuvette. A plot of the steady state of product appearance against thioredoxin concentration gave a sigmoid curve. On the basis of our experimental results, we propose a minimum model of the activation of phosphoribulokinase by reduced thioredoxin. Reduced thioredoxin may act on the phosphoribulokinase, either within the complex or in the dissociated metastable form. However, the time required to activate the enzyme as part of the complex is shorter (about 20 s) than that required to activate the dissociated form (about 10 min). This might be of physiological relevance, and we discuss the role of the interactions between phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase in the regulation of the Calvin cycle.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

Phosphoribulokinase (EC 2.7.1.19) catalyzes the ATP-dependent phosphorylation of ribulose 5-phosphate to form ribulose 1,5-bisphosphate and belongs to the Calvin cycle. This chloroplast enzyme is regulated by light through several mechanisms (1-8). Thioredoxins are small (about 12 kDa) regulatory proteins that mediate disulfide bridge reduction in specific target proteins (9-11). Once reduced by the electron flux from the photosystem I, thioredoxin activates various target enzymes. Reduction of these enzymes entails the oxidation of thioredoxin. Recently, the molecular description of the thiol-disulfide exchange pathway between spinach phosphoribulokinase and thioredoxin has provided evidence that Cys-46 of thioredoxin and Cys-55 of spinach phosphoribulokinase participate in the intermolecular mixed disulfide (12-14). The identities of the pairing residues are thus well established.

There is now considerable evidence that phosphoribulokinase interacts with other Calvin cycle enzymes leading to the formation of a multienzyme complex (15-30). We have shown that chloroplast phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase (EC 1.2.1.13) in Chlamydomonas reinhardtii cells exist as a bi-enzyme complex made up of two molecules of dimeric phosphoribulokinase and two molecules of tetrameric glyceraldehyde-3-phosphate dehydrogenase (24). A similar bi-enzyme complex has recently been found to contain a so-called CP12, besides the two enzymes (29).

Unlike the free stable enzyme, oxidized phosphoribulokinase may have a quite significant activity when associated with glyceraldehyde-3-phosphate dehydrogenase (25). On dilution, the complex may dissociate, and the released metastable phosphoribulokinase is also active and slowly relapses into the free stable form (25). Therefore, the association of phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase gives rise to conformation changes resulting in the appearance of active oxidized phosphoribulokinase.

We have therefore studied the activation by thioredoxin of algal phosphoribulokinase within a bi-enzyme complex made up of this enzyme and glyceraldehyde-3-phosphate dehydrogenase.

	EXPERIMENTAL PROCEDURES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

Strains and Culture Conditions-- The wild type WM3 strain of C. reinhardtii was heterotrophically grown in the dark at 25 °C on Tris acetate/phosphate medium (31).

Materials-- Ribulose 5-phosphate was obtained from Sigma. ATP, NAD(H), phosphoenolpyruvate, pyruvate kinase, and lactate dehydrogenase were supplied by Roche Molecular Biochemicals.

Enzymes-- The phosphoribulokinase-glyceraldehyde-3-phosphate dehydrogenase complex was purified from C. reinhardtii cells, essentially as described previously, but in the absence of cysteine (24). Thioredoxin from a cyanobacterium, Spirulina sp. (Sigma), was used because our efforts to purify thioredoxin from Chlamydomonas have failed, probably because of the instability of this protein in the alga (32). Free metastable enzyme was obtained after dilution of the bi-enzyme complex (about 500-fold) in the assay cuvette at pH 7.7 and 30 °C in the absence of substrates. Under these conditions, the complex dissociates, and the free metastable form of phosphoribulokinase appears. In most experiments, the phosphoribulokinase activity of the bi-enzyme complex or of the dissociated metastable form was followed, in the presence of both substrates and thioredoxin, using the principle of Tian and Tsou (33).

Reaction Assay and Activity Measurements-- Phosphoribulokinase was measured spectrophotometrically using a coupled assay with pyruvate kinase and lactate dehydrogenase at 30 °C (7). Thioredoxins were reduced by incubation with 20 mM dithiothreitol for 15 min. For thioredoxin activation experiments, thioredoxin was always present in a large excess relative to the bi-enzyme complex and kept permanently reduced in the assay cuvette using 0.5 or 1 mM dithiothreitol. Protein concentrations were determined according to Ref. 34.

Data Analysis-- The experimental data were fitted to the equations generated by the model using Simplex (35) or Marquardt (36) algorithms and a VAX computer.

	RESULTS

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

Oxidized phosphoribulokinase can be reduced and activated by reducing agents. Therefore, the activity of the bi-enzyme complex can be followed while undergoing reduction by thioredoxin. Different thioredoxin concentrations were used with a fixed concentration of dithiothreitol, and the activity of the phosphoribulokinase was measured at saturating concentrations of both substrates (1 mM ribulose 5-phosphate and ATP). There was a latency period, whatever the thioredoxin concentration used, and all progress curves were monophasic (Fig. 1). Indeed in the presence of 1 µM reduced thioredoxin, the progress curve was not a straight line or an exponential but could be fit using a combination of these two functions. The lag phase was associated with the slow depolymerization of the complex on dilution in the reaction mixture at 30 °C. Exactly as in the case of oxidized form, a best fit was obtained by assuming that the complex and the dissociated forms were active (25). The lag therefore resulted from the conversion of a less active form (phosphoribulokinase in the complex) into a more active one (phosphoribulokinase released from the complex).

View larger version (20K): [in this window] [in a new window]   Fig. 1.   Progress curves of the reaction catalyzed by reduced phosphoribulokinase within the bi-enzyme complex using different thioredoxin concentrations. The product q of the phosphoribulokinase activity is continuously measured in the presence of 0 (), 0.08 µM (*), 0.16 µM (), 0.5 µM (), 0.8 µM (), 4 µM () thioredoxin, and 0.5 mM dithiothreitol. The final concentration of the bi-enzyme complex in the assay cuvette is 2.3 nM. The data are fitted to Equation 4 in the main text.

If the bi-enzyme complex was allowed to dissociate (25) in the assay cuvette for 10 min at 30 °C before the substrates and 1 µM reduced thioredoxins were added, no lag was detected (curve 2, Fig. 2), contrary to the curve obtained with the complex (curve 1, Fig. 2). Therefore the metastable phosphoribulokinase released from the complex on dilution did not exhibit a lag phase even upon reduction by thioredoxin. These results indicate that the binding of reduced thioredoxin was fast relative to the dissociation process. The dissociation process was therefore the limiting step and was responsible for the lag.

View larger version (11K): [in this window] [in a new window]   Fig. 2.   Progress curves of the reaction catalyzed by phosphoribulokinase either in the bi-enzyme complex or in the metastable form. The activity of the bi-enzyme complex is measured in the presence of 1 µM reduced thioredoxin plus 0.5 mM dithiothreitol, at 1 mM ribulose 5-phosphate and 1 mM ATP (curve 1). The bi-enzyme complex is allowed to dissociate as described in the text, and the activity of the released metastable form of phosphoribulokinase is measured in the same experimental conditions described above for the bi-enzyme complex (curve 2). In both cases, the concentration of the bi-enzyme complex is 2.35 nM in the assay cuvette. The product q of the phosphoribulokinase activity is continuously measured. The experimental results are fitted to Equation 6 in the main text describing a monoexponential law (curve 1) or to a straight line (curve 2). The steady-state values are 416 s1 when the target enzyme of the thioredoxin is the complex (curve 1) and 333 s1 when the target enzyme is the metastable form of phosphoribulokinase (curve 2).

The apparent steady state (quasi-linear part of the curve) after the lag, as observed with the bi-enzyme complex, was related to the dissociated metastable form. When the steady-state rates pertaining to the metastable phosphoribulokinase released from the complex were plotted as a function of reduced thioredoxin, a sigmoid curve was observed (Fig. 3). The simplest model that can accommodate these results is shown in Fig. 4.

View larger version (11K): [in this window] [in a new window]   Fig. 3.   Variation of the steady-state rates of the activation process of the bi-enzyme complex as a function of thioredoxin concentration. By fitting the progress curves of Fig. 2 to Equation 4 in the main text, the values of the steady-state are obtained. These results are fitted to Equation 6 that, indeed, can be reduced to Equation 9 which is of the form v/[E]0 = (a[T]2 + b)/(c[T]2 + d) with a = 517, b = 10, c = 1, and d = 0.2.

View larger version (17K): [in this window] [in a new window]   Fig. 4.   Theoretical model of oxidized phosphoribulokinase activation induced by reduced thioredoxin. C and D indicate phosphoribulokinase in the bi-enzyme complex and the released metastable phosphoribulokinase, respectively. The reduced and the oxidized states are labeled r and o whatever the phosphoribulokinase forms (free or in the complex). The constants Ki correspond to apparent binding constants of thioredoxin (T) to the different phosphoribulokinase forms. The constants ki correspond to the apparent dissociation constants of the complex forms into the dissociated (metastable (D)) forms. The constants ci and ci correspond to the binding and desorption constants of the substrates S (both ATP and ribulose 5-phosphate). The constants µi correspond to the catalytic constants.

As mentioned above, reduced thioredoxins were rapidly bound to phosphoribulokinase, and the corresponding steps can be considered to be in rapid equilibrium. The rate of conversion of the enzyme-substrate forms into enzyme-product forms was slower and was therefore in a steady state. One can therefore contract the kinetic scheme of Fig. 4 to the model of Fig. 5 by using Cha's factors (37).

View larger version (8K): [in this window] [in a new window]   Fig. 5.   Simplified model of the activation of phosphoribulokinase by thioredoxin. The reduced (normalized) steady-state concentrations of the various enzyme forms are (C, CS, D, and DS). The forms C, CS, D, and DS correspond to rapid equilibrium between oxidized and reduced states of phosphoribulokinase either in the complex (C and CS) or in the metastable form (D and DS). The fi coefficients correspond to Cha's factors.

The dissociation of the bi-enzyme complex, whether oxidized or reduced, was the slowest process and occurred in one step. The simplified kinetic Model 1 may thus be proposed,

where X and Y correspond to oxidoreduction states of the phosphoribulokinase included in the bi-enzyme complex (C_o, C_oS, C_r, and C_rS) and of the recently metastable dissociated phosphoribulokinase (D_o, D_oS, D_r, and D_rS), respectively. * corresponds to the grouping of apparent dissociation constants of the complex forms into the dissociated metastable phosphoribulokinase forms and is equal to Equation 1,

(Eq. 1)

where the  parameters represent the normalized steady-state concentrations of the various enzyme forms.

The time evolution of the overall process may be described through Equation 2.

(Eq. 2)

Owing to the following conservation Equation 3,

(Eq. 3)

where P_t is the total protein concentration, it can be demonstrated that the product q assumes the form shown in Equation 4,

(Eq. 4)

and indeed, all experimental progress curves (Fig. 1) were fitted to this equation. Moreover, * is a complex function of the form shown in Equation 5,

(Eq. 5)

and therefore * should decrease as a function of thioredoxin concentration. This is what was obtained experimentally (Fig. 6).

View larger version (11K): [in this window] [in a new window]   Fig. 6.   Variation of the apparent dissociation constants of the phosphoribulokinase in the bi-enzyme complex as a function of thioredoxin concentration. By fitting the progress curves of Fig. 2 to Equation 4 in the main text, the values of * are obtained. These data follow the Equation 5 in the main text.

By using Equation 4, values of the steady-state rates (A) were plotted as a function of thioredoxin concentration, and a sigmoid was obtained (Fig. 3).

To test if the theoretical model depicted in Fig. 4 could also account for this experimental result, the equations were written under steady-state conditions, and the rate is as follows:

(Eq. 6)

Equation 6 therefore accounts for the sigmoidicity observed. Moreover, if [T]= 0, Equation 6 reduces to Equation 7.

(Eq. 7)

If [T] is high, Equation 6 then reduces to Equation 8.

(Eq. 8)

Equations 7 and 8 follow the Michaelis-Menten law, and they describe the behavior of the oxidized complex and of the fully reduced dissociated metastable phosphoribulokinase, respectively, as described previously (25, 28).

Fitting our experimental results to Equation 6 makes it possible to simplify this to give Equation 9,

(Eq. 9)

in which the terms in [T], both in the numerator and the denominator are negligible, with (µ₄c₄K₃K₄[S]) close to 520, (µ₂c₂[S]) to 10, (c₄[S]c₄ + µ₄)K₃K₄ close to 1, and c₂[S] + (c₂ + µ₂) to 0.2 (Fig. 7, curve 1). By taking into account these values, one can estimate the values of µ₂ and µ₄ to be approximately equal to 520 and 50 s¹, respectively. These values are in good agreement with those previously reported (25, 28).

View larger version (11K): [in this window] [in a new window]   Fig. 7.   Effect of the kinetic parameters associated to the bi-enzyme complex and to the metastable form of phosphoribulokinase on the sigmoidicity of the curves v/[E]0 versus thioredoxin concentration. Curve 1 represents the theoretical curve that gives the best fit of experimental data to v/[E]0 = (a[T]2 + b)/(c[T]2 + d) with a = 517, b = 10, c = 1, and d = 0.2. Curve 2 is obtained if all parameters are conserved but with a = 200. Curve 3 is obtained if all parameters are conserved but with d = 10.

Different parameters were used to simulate Equation 9, and the results are shown in Fig. 7. An increase in the parameter c₂[S] + (c₂ + µ₂) associated with the bi-enzyme complex results in a marked sigmoidicity (Fig. 7, curve 3). A decrease in the parameter [S]µ₄c₄K₃K₄ associated with the metastable form of phosphoribulokinase results in a decrease of the maximal steady-state rate, and at [T] = 0, the steady-state rate is null (Fig. 7, curve 2). The steady-state rate is related to the metastable form of phosphoribulokinase and obviously depends on the kinetic parameters of this form. These results also demonstrate that this rate depends on the kinetic parameters of the bi-enzyme complex from which the metastable form originates.

From the model in Fig. 4, it can be seen that thioredoxin is able to bind both to phosphoribulokinase within the bi-enzyme complex and to metastable phosphoribulokinase. To measure the time required to activate these two forms, they were separately mixed with reduced thioredoxins. At different times of incubation, an aliquot was withdrawn, and its activity was measured. In both case, an increase in activity was observed. The rates increased exponentially with incubation time before reaching a plateau value (Fig. 8). The amplitudes of these activation processes were slightly different, whereas the time constant for the activation of the enzyme inserted in the complex was higher (2 min¹) than that of the free enzyme (0.07 min¹).

View larger version (13K): [in this window] [in a new window]   Fig. 8.   Activation kinetics of the phosphoribulokinase whether free or in the bi-enzyme complex in the presence of reduced thioredoxins. The bi-enzyme is dissociated first by dilution, and the released phosphoribulokinase is mixed with thioredoxin for different times (curve 1). The bi-enzyme complex is incubated with reduced thioredoxin (curve 2). After increasing time period, the substrates are added, and the activity was measured. The final enzyme concentration and thioredoxin and dithiothreitol concentrations in both cases are 1.57 nM, 3.3 µM, and 1 mM, respectively. The curves are fitted to the following equation v/[E]0 = (A(1  et) + A0), where v is the velocity of the reaction, A and  stand for the amplitude and the time constant of the activation process, respectively, [E]0 is the total enzyme concentration, and A0, the initial velocity of the reaction.

	DISCUSSION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

Modifications of the kinetic properties of multienzyme complexes have been described (8, 38-42). The results presented here show that activation of phosphoribulokinase by thioredoxins is altered when the enzyme is embedded in a complex. Phosphoribulokinase in the complex form is more easily activated by thioredoxin than is the dissociated enzyme. It is likely that glyceraldehyde-3-phosphate dehydrogenase dictates a conformation to phosphoribulokinase that is more amenable to thioredoxin activation. The time required to activate this enzyme within the complex is shorter (about 20 s) than that required to activate its dissociated form (about 10 min). This time is comparable to the induction time (about 30 s) of phosphoribulokinase activity in crude extracts of C. reinhardtii following dark-light transition (43).

It has been demonstrated that the reduction process of phosphoribulokinase operates with the greatest efficiency via hydrophobic interactions. This efficiency is the consequence of a change of conformation that can be induced by chaotropic agents, organic solvents, and high pressure (44-45). Protein-protein interactions are good candidates for these effects in vivo. However, most experiments on phosphoribulokinase activation by thioredoxins have been performed with the stable, isolated enzyme (1, 12-14).

A new feature of the form embedded within the complex is the sigmoid curve obtained for its steady-state rate as a function of thioredoxin concentration. This curve can be explained by our proposed model, which involves a slow dissociation of the complex in the reaction mixture, and the binding of thioredoxin to the different forms of phosphoribulokinase. Whether or not this sigmoidicity is of physiological relevance, it results in a fine regulation of phosphoribulokinase within the complex.

Although the organization of the Calvin cycle is widely accepted, the regulation of these structures has been little studied. This paper shows that heterologous interactions are responsible for kinetic changes and that a physiological advantage might arise from these interactions. It may be that the differences between in vivo and in vitro activities result from interactions in the cell. As shown by Goodsell (46), macromolecular crowding in vivo favors interactions. The model presented here takes these interactions into account but is probably a simplified scheme because it is likely that, in the cell, these interactions involve more than two enzymes of the Calvin cycle.

	ACKNOWLEDGEMENTS

We are greatly indebted to Prof. J. Ricard for helpful discussions and for advice in writing this manuscript. We thank Dr. Owen Parkes for editing the English text.

	FOOTNOTES

^* The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

This paper is dedicated to the memories of Prof. P. A. Srere and Prof. C. Costes.

Present address: Facultad de ciencis. Universidad de Los Andes, Merida 5101, Venezuela.

^¶ To whom correspondence should be addressed. Tel.: (33) 1 44 27 63 56; Fax: (33) 1 44 27 57 16; E-mail: meunier@ijm.jussieu.fr.

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