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00019616-200603000-00002Miscellaneous-ArticleThe EndocrinologistThe Endocrinologist© 2006 Lippincott Williams & Wilkins, Inc.16March 2006 p 57-60The Effect of Thyroid Hormones on Erythrocyte 2,3-DiphosphoglyceratePreliminary StudyTokay, Alper PhD*; Raymondjean, Michel PhD†; Alicigüzel, Yakup PhD*From the *Department of Biochemistry, Faculty of Medicine Akdeniz University, Antalya, Turkey; and the †University Pierre et Marie Curie, Paris, France.Reprints: Yakup Alıcıgüzel, PhD, Akdeniz University, School of Medicine, Department of Biochemistry, 07070 Antalya, Turkey. E-mail: [email protected] 2,3-diphosphoglycerate (2,3-DPG) levels increase in hyperthyroidism. The objective of this study was to investigate the effect of thyroid hormones on red blood cell (RBC) 2,3-DPG levels. Erythrocyte suspensions, prepared from whole blood samples of healthy volunteers, were incubated with 4 ng/mL 3,5,3′-triiodothyronine (T3) and 0,15 μg/mL 3,3′,5,5′-tetraiodothyronine (T4) at 37°C for 1 hour. These incubations were also done in the presence of inhibitors that exert effect on the enzymes of the Rapoport-Luebering cycle (RLC) in which 2,3-DPG is formed. Diphosphoglycerate mutase (DPGM) and phosphoglycerate kinase (PGK) were inhibited by N-ethylmaleimide (NEM; 750 mg/L) and suramin (SUR; 3 mmol/L), respectively. Triiodothyronine, T3 + NEM, and T3 + SUR incubations all caused an increase in erythrocyte 2,3-DPG levels compared with controls. When erythrocytes were incubated with T3 in the presence of both inhibitors, however, no increase in 2,3-DPG levels was observed. These data suggest that thyroid hormones may control 2,3-DPG accumulation in RBCs.Thyroid hormone receptors have been found on the cell membrane in mitochondria, cytosol, and the nucleus.1–3 Interestingly, erythrocytes have been shown to possess these receptors in the cellular membrane.1,2 Thus, thyroid hormones may play a role in erythrocyte metabolism.Thyroid hormones increase the basal metabolic rate and oxidative metabolism by inducing specific enzymes.4–7 Reactive oxygen species (ROS), which trigger cellular and subcellular membrane damage, are formed in the process of mitochondrial respiration, which is modulated by thyroid hormones.4,8As a result of increased cellular oxygen consumption observed in hyperthyroidism, erythrocytes that function in oxygen delivery could become more susceptible to oxidative damage.7,9 Previous studies demonstrate increased erythrocyte antioxidant enzyme activity in hyperthyroid patients. With effective antithyroid hormone therapy, the reported increase in erythrocyte antioxidant enzyme activity returned to normal levels.8In hyperthyroidism, increased delivery of oxygen into tissues requires a parallel increase in formation of 2,3-diphosphoglycerate10,11 in red cells. This in turn causes increased ROS formation in erythrocytes.9Previous studies show that thyroid hormones10,11 decrease erythrocyte ATP and lactate levels. This observation has led researchers to conclude that thyroid hormones may directly stimulate diphosphoglycerate mutase (DPGM) enzyme activity and thus increase 2,3-diphosphoglycerate (DPG) levels.12 The aim of this study was to understand the role of thyroid hormones in 2,3-DPG formation. The effect of T3 and T4 on DPGM activity catalyzing the reaction between 1,3-BPG and 2,3-DPG was also investigated.MATERIALS AND METHODSBlood samples were obtained from 23 normal healthy volunteers (age range, 36 ± 9.7 years; 12 females, 11 males). Blood samples were drawn from the cubital vein into heparinized test tubes. All samples were placed on ice and plasma fractions were separated by centrifugation (1500 × g) for 15 minutes at +4°C. After discarding the plasma fractions, samples were washed three times with an isotonic solution at +4°C to obtain erythrocyte suspensions. Hemoglobin (Hb) content in all samples was measured from hemolysate dilutions (1:100).13 Erythrocyte suspensions were initially incubated with thyroid hormones and then with thyroid hormones along with inhibitors in the presence of Krebs buffer at 37°C for 1 hour.14 Thyroid hormones prepared for incubations were dissolved in a weak base solution (0.001 N NaOH). Incubation of each sample was performed in three experimental groups. The first group (n = 8) was incubated with thyroid hormones alone as described in Table 1. The second group (n = 15) was incubated with thyroid hormones along with enzyme inhibitors as described in Table 2. The third group was erythrocyte hemolysates incubated in the presence of thyroid hormones (Table 3). After incubations were completed, 1:100 hemolysate dilutions were prepared and 2,3-DPG levels in all experiment media were calculated against controls by a spectrophotometric assay.15,16 All experimental reagents were purchased from Merck (Whitehouse Station, NJ) and Sigma (St. Louis, MO). Statistical significance was assessed by “correlation regression analysis” and the differences between nonparametric groups were determined by Wilcoxon analysis.JOURNAL/endst/04.03/00019616-200603000-00002/table1-2/v/2021-02-17T201807Z/r/image-tiff Procedure for Incubations Done With Thyroid Hormones and Erythrocyte SuspensionsJOURNAL/endst/04.03/00019616-200603000-00002/table2-2/v/2021-02-17T201807Z/r/image-tiff Procedure for Incubations Done With Thyroid Hormones Erythrocyte Suspensions and Inhibitors of RLC EnzymesJOURNAL/endst/04.03/00019616-200603000-00002/table3-2/v/2021-02-17T201807Z/r/image-tiff Procedure for Incubations Done With Thyroid Hormones and Erythrocyte HemolysatesRESULTSGroup I ResultsSamples that were incubated with both T3 (4 ng/mL) and T4 (0.15 μg/mL) had significantly (P < 0.05) greater levels of 2,3-DPG compared with controls (Table 4 and Fig. 1).JOURNAL/endst/04.03/00019616-200603000-00002/table4-2/v/2021-02-17T201807Z/r/image-tiff Results of Group I (Incubations Done With Thyroid Hormones)JOURNAL/endst/04.03/00019616-200603000-00002/figure1-2/v/2021-02-17T201807Z/r/image-png Results of incubations done with thyroid hormones and erythrocyte suspensions.Group II ResultsSamples were incubated with T3 (4 ng/mL) along with inhibitors. Diphosphoglycerate mutase and phosphoglycerate kinase (PGK) were inhibited with N-ethylmaleimide (NEM; 750 mg/L) and suramin (SUR; 3 mmol/L), respectively. Triiodothyronine, T3 + NEM, and T3+ SUR incubations all caused an increase in erythrocyte 2,3-DPG levels compared with controls (P < 0.05). When both inhibitors were applied concurrently in the presence of T3, the calculated 2,3-DPG levels were similar to those of controls (Fig. 2). Results for group 3 are given in Table 5. The calculated levels of 2,3-DPG in T3, T3 + NEM, and T3 + SUR groups were significantly increased (P < 0.05) when compared with those of controls. No significant difference was observed between T3 and T3 + NEM, whereas a statistical increase (P < 0.05) was present between the groups T3 and T3 + SUR. No significant difference was observed between T3 and T3 + NEM + SUR.JOURNAL/endst/04.03/00019616-200603000-00002/figure2-2/v/2021-02-17T201807Z/r/image-png Results of incubations done with thyroid hormones, erythrocyte suspensions, and inhibitors of the Rapoport-Luebering cycle.JOURNAL/endst/04.03/00019616-200603000-00002/table5-2/v/2021-02-17T201807Z/r/image-tiff Results of Group II (Incubations Done With Inhibitors).Group III ResultsHemolysates and T3 (4 ng/mL) were incubated for 1 hour at 37°C. No significant change in 2,3-DPG levels was observed between T3 incubated groups compared with those of controls (data not shown).DISCUSSIONHyperthyroidism causes an increase in the basal metabolic rate. Therefore, the need for oxygen is increased.7,9 The ability of erythrocytes to bind and deliver oxygen to tissues is dependent on factors like pO2, pH, temperature and 2,3-DPG concentrations.21–25 Among these factors, 2,3-DPG, which is specific to erythrocytes, seems to be most important. The affinity of 2,3-DPG for Hb is greater than that of oxygen. Thus, an increase in erythrocyte 2,3-DPG levels will lead to the release of oxygen into tissues.In an in vitro study done by Snyder and Reddy,14 various concentrations of thyroid hormones increased the level of 2,3-DPG. They also estimated the effective thyroid hormone concentration (T3; 3.75 × 10−8 M and for T4; 3.75 × l0−10 M) and incubation time (1 hour) for establishing hyperthyroidism in an in vitro environment. A study done in hyperthyroid patients showed that the average concentrations of T3 and T4 were 3.77 ng/mL and 0.15 mg/mL, respectively.26 With reference to the reported values of T3 and T4 in hyperthyroidism, the T3 and T4 concentrations used in that study, 4 ng/mL and 0.15 mg/mL, were in the appropriate range.A significant increase in 2,3-DPG levels was previously reported in samples that were incubated with thyroid hormones.14 Similarly, after 1 hour of incubation, there was a significant increase in 2,3-DPG (P < 0.05) levels when compared with controls (Table 4, Fig. 1). These results are in agreement with previous studies and point out that thyroid hormones can increase the level of 2,3-DPG in erythrocytes.These findings, however, do not suggest a mechanism for thyroid hormone action in erythrocytes. In other cell types, thyroid hormones exert their effect at transcriptional level. Erythrocytes, however, do not possess active transcriptional machinery.To further evaluate the mechanism of 2,3-DPG increase in erythrocytes, experiments with T3 and RLC inhibitors (group II) were performed. A significant increase (16%) in 2,3-DPG levels (P < 0.05) was observed even in the presence of NEM, a DPGM inhibitor. As indicated previously, DPGM catalyzes the formation of 2,3-DPG. When PGK was inhibited by SUR in a T3-incubated media, a significant increase (P < 0.05) in the level of 2,3-DPG was found when compared with both controls and samples incubated only with T3 (26% and 6%, respectively) (Table 5, Fig. 2). This was an expected result because inhibition of PGK with SUR increases 2,3-DPG levels by blocking the catalysis of 1,3-BPG.When both enzymes of the RLC were inhibited in the presence of T3 (T3 + NEM + SUR), however, no change was found in erythrocyte 2,3-DPG levels compared with controls. Parallel to these observations, a significant (P < 0.05) decrease (20%) observed between T3 and T3 + NEM + SUR showed that 2,3-DPG could not be synthesized by 1,3-BPG. The calculated levels of 2,3-DPG in groups incubated with T3, SUR, and NEM were similar to those of controls, suggesting that some reversible conversion may occur between 1,3-BPG and 2,3-DPG.When hemolysates were incubated with T3 (4 ng/mL) for 1 hour at 37°C, no change was found in 2,3-DPG levels (Table 6). These results suggest that thyroid hormones have no direct effect on the reported enzyme systems. Increased levels of 2,3-DPG observed in intact erythrocytes after incubation with thyroid hormones suggest that these hormones may mediate secondary signaling pathways after binding membrane receptors.Although T3 does not directly affect BPGM activity, it can affect both PGK and diphosphoglycerate phosphatase. The suggested mechanism of T3 action in erythrocytes is shown in Figure 3.JOURNAL/endst/04.03/00019616-200603000-00002/figure3-2/v/2021-02-17T201807Z/r/image-tiff Possible mechanism of how the Rapoport-Luebering cycle can be affected by thyroid hormones.ACKNOWLEDGMENTSThis work was supported in part by funding from the Akdeniz University Research Foundation (20.02.0122.04).REFERENCES1. Botta JA, de Mendoza D, Morero RD, et al. High affinity L-triiodothyronine binding sites on washed rat erythrocyte membranes. J Biol Chem. 1983;258:6690–6692.[Context Link][CrossRef][Medline Link]2. Davis FB, Moffett MJ, Davis PJ, et al. Inositol phosphates modulate binding of thyroid hormone to human red cell membranes in vitro. J Clin Endocrinol Metab. 1993;77:1427–1430.[Context Link][CrossRef][Medline Link]3. Chin WW. Nuclear thyroid hormone receptors. In: Packer MD, ed. Nuclear Hormone Receptor. New York: Academic Press; 1991:79–102.[Context Link]4. Asayama K, Dobashi K, Hayashibe H, et al. 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