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Effect of non-enzymatic glycation on esterase activities of hemoglobin and myoglobin

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Abstract

Heme proteins––hemoglobin and myoglobin possess esterase activities. Studies with purified hemoglobin from normal individuals and diabetic patients revealed that the esterase activity as measured from hydrolysis of p-nitrophenyl acetate (p-NPA) was higher in diabetic condition and increased progressively with extent of the disease. HbA1c, the major glycated hemoglobin, which increases proportionately with blood glucose level in diabetes mellitus, exhibited more esterase activity than the non-glycated hemoglobin fraction, HbA0, as demonstrated spectrophotometrically as well as by activity staining. Glycation influenced esterase activity of hemoglobin by increasing the affinity for the substrate and the rate of the reaction. Both HbA0 and HbA1c-mediated catalysis of p-NPA hydrolysis was pH-dependent. Esterase activity of in vitro-glycated myoglobin (GMb) was also higher than that of its non-glycated analog (Mb). The amplified esterase activities of hemoglobin and myoglobin might be associated with glycation-induced structural modifications of the proteins.

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References

  1. Schleicher ED, Olgemoller B, Weidenman E, Gerbitz KD (1993) Specific glycation of albumin depends on its half-life. Clin Chem 39:625–628

    PubMed  CAS  Google Scholar 

  2. Biemel KM, Friedl DA, Lederer MO (2002) Identification and quantification of major Maillard-crosslinks in human serum albumin and lens protein: evidence for glucosepane as the dominant compound. J Biol Chem 277:24907–24915

    Article  PubMed  CAS  Google Scholar 

  3. Turk Z, Misur I, Turk N, Benko B (1999) Rat tissue collagen modified by advanced glycation: correlation with duration of diabetes and glycemic control. Clin Chem Lab Med 37:813–820

    Article  PubMed  CAS  Google Scholar 

  4. Stewart JM, Kilpatric ES, Cathcart S, Small M, Dominiczac MH (1994) Low-density lipoprotein particle size in type 2 diabetic patients and age matched controls. Ann Clin Biochem 31:153–159

    PubMed  Google Scholar 

  5. De Rosa MC, Sanna MT, Messana I, Castagnola M, Galtieri A, Tellone E, Scatena R, Bolta M, Giardina B (1998) Glycated human hemoglobin (HbA1c): functional characteristics and molecular modeling studies. Biophys Chem 72:323–335

    Article  PubMed  Google Scholar 

  6. Cohen MP, Wu V (1994) Purification of glycated hemoglobin. Meth Enzymol 231:65–75

    PubMed  CAS  Google Scholar 

  7. Wolffenbuttel BH, Giordino D, Founds HW, Bucala R (1996) Long-term assessment of glucose control by hemoglobin-AGE management. Lancet 347:513–515

    Article  PubMed  CAS  Google Scholar 

  8. Svacina S, Hovorka R, Skrha J (1990) Computer models of albumin and hemoglobin glycation. Comput Meth Programs Biomed 32:259–263

    Article  CAS  Google Scholar 

  9. Watala C, Gwozdzinski K, Malek M (1992) Direct evidence for the alterations in protein structure and conformation upon in vitro non-enzymatic glycosylation. Int J Biochem 24:1295–1302

    Article  PubMed  CAS  Google Scholar 

  10. Peterson KP, Pavlovich JG, Goldstein D, Little R, England J, Peterson CM (1998) What is hemoglobin A1c ? An analysis of glycated hemoglobin by electrospray ionization mass spectrometry. Clin Chem 44:1951–1958

    PubMed  CAS  Google Scholar 

  11. Inouye M, Mio T, Sumino K (1999) Glycated hemoglobin and lipid peroxidation in erythrocytes of diabetic patients. Metabolism 48:205–209

    Article  PubMed  CAS  Google Scholar 

  12. Khoo UY, Newman DJ, Miller WK, Price CP (1994) The influence of glycation on the peroxidase activity of hemoglobin. Eu J Clin Chem Clin Biochem 32:435–440

    CAS  Google Scholar 

  13. Kar M, Chakraborti AS (1999) Release of iron from hemoglobin––a possible source of free radicals in diabetes mellitus. Ind J Exptl Biol 37:190–192

    CAS  Google Scholar 

  14. Kar M, Chakraborti AS (2001) Effect of glycosylation on iron-mediated free radical reactions of hemoglobin. Curr Sci 80:770–773

    CAS  Google Scholar 

  15. Sen S, Kar M, Roy A, Chakraborti AS (2005) Effect of non-enzymatic glycation on functional and structural properties of hemoglobin. Biophys Chem 113:289–298

    Article  PubMed  CAS  Google Scholar 

  16. Roy A, Sen S, Chakraborti AS (2004) In vitro non-enzymatic glycation enhances the role of myoglobin as a source of oxidative stress. Free Radic Res 38:139–146

    Article  PubMed  CAS  Google Scholar 

  17. Kar M, Roy A, Bose T, Chakraborti AS (2006) Effect of glycation of hemoglobin on its interaction with trifluoperazine. The Protein J 25:202–211

    Article  CAS  Google Scholar 

  18. Everse J, Johnson MC, Marini MA (1994) Peroxidase activities of hemoglobin and hemoglobin derivatives. Meth Enzymol 231:547–561

    PubMed  CAS  Google Scholar 

  19. Elbaum D, Nagel RL (1981) Esterase activity of hemoglobin: differences between HbA and HbS. J Biol Chem 256:2280–2283

    PubMed  CAS  Google Scholar 

  20. Elbaum D, Weidenmann B, Nagel RL (1982) Some properties of the reaction site for the esterase activity of hemoglobin. J Biol Chem 257:8454–8458

    PubMed  CAS  Google Scholar 

  21. Breslow E, Guard FRN (1962) Reactivity of sperm whale metmyoglobin towards hydrogen ions and p-nitrophenyl acetate. J Biol Chem 237:371–381

    PubMed  CAS  Google Scholar 

  22. Trinder P (1969) Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J Clin Pathol 22:158–161

    PubMed  CAS  Google Scholar 

  23. Bhattacharyya J, Bhattacharyya M, Chakraborti AS, Chaudhuri U, Poddar RK (1998) Structural organizations of hemoglobin and myoglobin influence their binding behaviour with phenothiazines. Int J Biol Macromol 23:11–18

    Article  PubMed  CAS  Google Scholar 

  24. Flukiger R, Winterhalter KH (1976) In vitro synthesis of hemoglobin A1c. FEBS Lett 71:356–366

    Article  Google Scholar 

  25. Bhattacharyya J, Bhattacharyya M, Chakraborti AS, Chaudhuri U, Poddar RK (1994) Interaction of chlorpromazine with myoglobin and hemoglobin––a comparative study. Biochem Pharmacol 47:2049–2053

    Article  PubMed  CAS  Google Scholar 

  26. Wittenberg JB, Wittenberg BA (1981) Preparation of myoglobin. Meth Enzymol 76:29–42

    Article  PubMed  CAS  Google Scholar 

  27. Riedel K, Talker-Huiber D, Givskov M, Schwab H, Eberl L (2003) Identification and characterization of a GDSL esterase gene located proxima to the swr Quorum-sensing system of Serratia liquifaciens MG1. Appl Environ Microbiol 69:3901–3910

    Article  PubMed  CAS  Google Scholar 

  28. Stryer L (1995) Biochemistry. 4th edn. W. H. Freeman and Co., New York, pp147–178

    Google Scholar 

  29. Watanabe H, Tanase S, Nakajou K, Maruyama T, Kragh-Hansen U, Otagiri M (2000) Role of Arg-410 and Tyr-411 in human serum albumin for ligand binding and esterase-like activity. Biochem J 349:813–819

    PubMed  CAS  Google Scholar 

  30. Bourdon E, Loreau N, Blache D (1999) Glucose and free radicals impair the antioxidant properties of serum albumin. FASEB J 13:233–244

    PubMed  CAS  Google Scholar 

  31. Nakajou K, Watanabe H, Kragh-Hansen U, Maruyama T, Otagiri M (2003) The effect of glycation on the structure, function and biological fate of human serum albumin as revealed by recombinant mutants. Biochim et Biophys Acta 1623:88–97

    CAS  Google Scholar 

  32. Thornalley PJ (2005) Dicarbonyl intermediates in the Maillard reaction. Ann N Y Acad Sci 1043:111–117

    Article  PubMed  CAS  Google Scholar 

  33. Ahmed N, Dobler D, Dean M, Thornally PJ (2005) Peptide mapping identifies hotspot site of modification in human serum albumin by methylglyoxal involved in ligand binding and esterase activity. J Biol Chem 280:5724–5732

    Article  PubMed  CAS  Google Scholar 

  34. Yan H, Harding JJ (1997) Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem J 328:599–605

    PubMed  CAS  Google Scholar 

  35. Zhao W, Devamanoharan PS, Varma SD (2000) Fructose-induced deactivation of antioxidant enzymes: preventive effect of pyruvate. Free Radic Res 33:23–30

    Article  PubMed  CAS  Google Scholar 

  36. Bousova I, Vukasovic D, Juretic D, Palicka V, Drsata J (2005) Enzyme activity and AGE formation in a model of AST glycoxidation by d-fructose in vitro. Acta Pharm 55:107–114

    PubMed  CAS  Google Scholar 

  37. Seidler NW, Seibel I (2000) Glycation of aspartate aminotransferase and conformational flexibility. Biochem Biophys Res Commun 277:47–50

    Article  PubMed  CAS  Google Scholar 

  38. Tanabashi S, Okuno F, Terakura T, Tsuji T, Wakahara T, Yamada S (1982) A case of diabetic ketoacidosis with a markedly raised level of serum creatin phosphokinase (CPK) and myoglobin. Nippon Naika Gakki Zasshi 71:802–809

    CAS  Google Scholar 

  39. Nakano S, Mugikura M, Endoh M, Ogami Y, Isuki M (1996) Acute pancreatitis with diabetic ketoacidosis associated with hypermyoglobinemia, acute renal failure and DIC. J Gastroenterol 31:623–626

    Article  PubMed  CAS  Google Scholar 

  40. Rumpf KW, Kaiser H, Grone HJ, Trapp VE, Meinck HM, Goebel HH, Kunze E, Kreuzer H, Schler F (1981) Myoglobinuric renal failure in hyperosmolar diabetic coma. Disch Med Wochenschr 106:708–711

    Article  CAS  Google Scholar 

  41. Brownlee M, Cerami A (1981) The biochemistry of the complications of diabetes mellitus. Ann Rev Biochem 50:385–432

    Article  PubMed  CAS  Google Scholar 

  42. Symeonidis A, Althanassiou G, Psiroyannis A, Kyriazopoulou V, Kapatais-Zoumb A, Missirlis Y, Zoumbos N (2001) Impairment of erythrocyte viscoelasticity is correlated with levels of glycosylated hemoglobin in diabetic patients. Clin Lab Haematol 23:103–109

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

S.S and T.B received research fellowships from Indian Council of Medical Research, New Delhi and University Grants Commission, New Delhi, respectively. We are thankful to Prof. U. Chaudhuri for helpful discussions.

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  1. Department of Biophysics, Molecular Biology and Genetics, University College of Science, University of Calcutta, 92, Acharyya Prafulla Chandra Road, Kolkata, 700009, India

    Subhrojit Sen, Tania Bose, Anjana Roy & Abhay Sankar Chakraborti

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  1. Subhrojit Sen
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  2. Tania Bose
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  3. Anjana Roy
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  4. Abhay Sankar Chakraborti
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Correspondence to Abhay Sankar Chakraborti.

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Sen, S., Bose, T., Roy, A. et al. Effect of non-enzymatic glycation on esterase activities of hemoglobin and myoglobin. Mol Cell Biochem 301, 251–257 (2007). https://doi.org/10.1007/s11010-007-9418-5

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  • DOI: https://doi.org/10.1007/s11010-007-9418-5

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