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Erythrocyte membrane in type 2 diabetes mellitus

DISCOVERIES (ISSN 2359-7232), 2016, April-June issue

CITATION: 

Gabreanu GR, Angelescu S. Erythrocyte membrane in type 2 diabetes mellitus. Discoveries 2016, April-June; 4(2): e60. DOI: 10.15190/d.2016.7

Submitted: June 17, 2016; Revised: June 30, 2016; Accepted: June 30, 2016; Published: June 30, 2016;

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Erythrocyte membrane in type 2 diabetes mellitus

Georgiana Roxana Gabreanu, Silvana Angelescu*

Hematology Department, Coltea Clinical Hospital, Bucharest, Romania

*Correspondence to: Silvana Angelescu, MD, Hematology Department, Coltea Clinical Hospital, Bucharest, Romania; Email: sangelescu21@gmail.com 

Abstract

Type 2 diabetes mellitus represents a major public health challenge, due to the continuously growing prevalence and the complexity of the diabetic complications. Hyperglycemia seems to be the main mechanism for the disease progression. During erythrocyte’s long life span, erythrocyte membranes are affected by the chronic exposure to glucose, which triggers several biochemical modifications that lead to both structural and functional disruption, which are further involved in the physiopathology of diabetes and its complications. Non-enzymatic protein glycation of red blood cell membrane proteins occur in two phases: early glycation, characterized by Schiff bases and Amadouri compounds formation, and advanced glycation, characterized by advanced glycation end products (AGEs). These products could be valuable tools for early diagnosis or biomarkers for disease progression, depending on how advanced they are in the glycation process. Advanced glycated end products were linked with diabetic complications. Also, lipid peroxidation and decreased activity of the enzyme pumps occur in the erythrocyte membrane of the diabetic patients. The investigation of lipid rafts and erythrocyte membrane fatty acids are a valuable tool for long-term monitoring of metabolic status. Further investigation of the erythrocyte membrane could provide novel biomarkers for monitoring of diabetes and its complications. 

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References

1. International Diabetes Federation. IDF Diabetes Atlas, 1st ed. Brussels, Belgium: International Diabetes Federation, 2000.

2. International Diabetes Federation. IDF Diabetes Atlas, 7th ed. Brussels, Belgium: International Diabetes Federation, 2015.

3. Viskupicova J, Blaskovic D, Galiniak S, Soszyński M, Bartosz G, Horakova L, Sadowska-Bartosz I. Effect of high glucose concentrations on human erythrocytes in vitro. Redox Biol. 2015. 5:381-7.

4. Maillard LC. Action des acides aminés sur les sucres: formation des mélanoidines par voie méthodique. C.R. Acad. Sci. 1912. 154: 66–68.

5. Finot PA. Historical perspective of the Maillard reaction in food science. Ann N Y Acad Sci. 2005. 1043:1-8.

6. Holmquist WR, Schroeder WA. A new N-terminal blocking group involving a Schiff base in hemoglobin AIc. Biochemistry. 1966. 5(8):2489-503.

7. Bookchin RM, Gallop PM. Structure of hemoglobin AIc: nature of the N-terminal beta chain blocking group. Biochem Biophys Res Commun. 1968. 32(1):86-93.

8. Rahbar S. The discovery of glycated hemoglobin: a major event in the study of nonenzymatic chemistry in biological systems. Ann N Y Acad Sci. 2005. 1043:9-19.

9. Gillery P. A history of HbA1c through Clinical Chemistry and Laboratory Medicine. Clin Chem Lab Med. 2013. 51(1):65-74. 

10. Dagogo-Jack S. Piftalls in the use of HbA1(c) as a diagnostic test: the ethnic conundrum, Nat Rev Endocrinol. 2010. 6(10):589-93.

11. Shepard JG, Airee A, Dake AW, McFarland MS, Vora A. Limitations of A1c Interpretation. South Med J. 2015. 108(12):724-9. 

12. Takahashi S Uchino H, Shimizu T, Kanazawa A, Tamura Y, Sakai K, Watada H, Hirose T, Kawamori R, Tanaka Y. Comparison of glycated albumin (GA) and glycated hemoglobin (HbA1c) in type 2 diabetic patients: usefulness of GA for evaluation of short-term changes in glycemic control. Endocr J. 2007. 54(1):139-44. 

13. Raghav A, Ahmad J. Glycated serum albumin: a potential disease marker and an intermediate index of diabetes control. Diabetes Metab Syndr. 2014. 8(4):245-51. 

14. Zhang Q, Tang N, Schepmoes AA, Phillips LS, Smith RD, Metz TO. Proteomic profiling of nonenzymatically glycated proteins in human plasma and erythrocyte membranes. J Proteome Res. 2008. 7(5):2025-32

15. Cho SJ, Roman G, Yeboah F, Konishi Y. The road to advanced glycation end products: a mechanistic perspective. Curr Med Chem. 2007. 14(15):1653-71.

16. Goh SY, Cooper ME. Clinical review: The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab. 2008. 93(4):1143-52. 

17. De Oliveira S, Saldanha C. An overview about erythrocyte membrane. Clin Hemorheol Microcirc. 2010. 44(1):63-74. 

18. Zhang Q, Monroe ME, Schepmoes AA, Clauss TR, Gritsenko MA, Meng D, Petyuk VA, Smith RD, Metz TO. Comprehensive identification of glycated peptides and their glycation motifs in plasma and erythrocytes of control and diabetic subjects. J Proteome Res. 2011. 10(7):3076-88. 

19. Niwa T, Katsuzaki T, Miyazaki S, Miyazaki T, Ishizaki Y, Hayase F, Tatemichi N, Takei Y. Immunohistochemical detection of imidazolone, a novel advanced glycation end product, in kidneys and aortas of diabetic patients. J Clin Invest. 1997. 99(6):1272-80.

20. Yamaguchi M, Nakamura N, Nakano K, Kitagawa Y, Shigeta H, Hasegawa G, Ienaga K, Nakamura K, Nakazawa Y, Fukui I, Obayashi H, Kondo M. Immunochemical quantification of crossline as a fluorescent advanced glycation endproduct in erythrocyte membrane proteins from diabetic patients with or without retinopathy. Diabet Med. 1998. 15(6):458-62.

21. Portero-Otín M, Pamplona R, Bellmunt MJ, Bergua M, Prat J. Glycaemic control and in vivo non-oxidative Maillard reaction: urinary excretion of pyrraline in diabetes patients. Eur J Clin Invest. 1997. 27(9):767-73.

22. Nε-(carboxymethyl)-lysine, White Matter, and Cognitive Function in Diabetes Patients. Zhang JH, Xu HZ, Shen QF, Lin YZ, Sun CK, Sha L, Ge YS, Liu Y, Wang C. Can J Neurol Sci. 2016. 4:1-5. 

23. Morales S, García-Salcedo JA, Muñoz-Torres M. Pentosidine: a new biomarker in diabetes mellitus complications. Med Clin (Barc). 2011. 136(7):298-302. 

24. Kerkeni M, Saïdi A, Bouzidi H, Letaief A, Ben Yahia S, Hammami M. Pentosidine as a biomarker for microvascular complications in type 2 diabetic patients. Diab Vasc Dis Res. 2013. 10(3):239-45. 

25. Kuwajima S. Immunochemical determination of advanced glycation end products in erythrocyte peripheral-membrane proteins from diabetic patients. Hokkaido Igaku Zasshi. 1993. 68(5):695-704.

26. Wautier JL, Wautier MP, Schmidt AM, Anderson GM, Hori O, Zoukourian C, Capron L, Chappey O, Yan SD, Brett J, et al. Advanced glycation end products (AGEs) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: a link between surface-associated AGEs and diabetic complications. Proc Natl Acad Sci U S A. 1994. 91(16):7742-6.

27. Aoki S, Hasegawa G, Shigeta H, Obayashi H, Fujii M, Kimura F, Moriwaki A, Nakamura N, Ienaga K, Nakamura K, Kondo M. Crossline levels in serum and erythrocyte membrane proteins from patients with diabetic nephropathy. Diabetes Res Clin Pract. 2000. 48(2):119-25.

28. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G Jr, Thornalley PJ, Schleicher E, Wieder T, Lang F. Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem. 2006. 18(4-5):223-32.

29. Lang KS, Duranton C, Poehlmann H, Myssina S, Bauer C, Lang F, Wieder T, Huber SM. Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ. 2003. 10(2):249-56.

30. Calderón-Salinas JV, Muñoz-Reyes EG, Guerrero-Romero JF, Rodríguez-Morán M, Bracho-Riquelme RL, Carrera-Gracia MA, Quintanar-Escorza MA. Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease.  Mol Cell Biochem. 2011. 357(1-2):171-9. 

31. Inouye M, Hashimoto H, Mio T, Sumino K. Levels of lipid peroxidation product and glycated hemoglobin A1c in the erythrocytes of diabetic patients. Clin Chim Acta. 1998. 276(2):163-72.

32. Inouye M, Mio T, Sumino K. Glycated hemoglobin and lipid peroxidation in erythrocytes of diabetic patients. Metabolism. 1999. 48(2):205-9.

33. Inouye M, Mio T, Sumino K. Link between glycation and lipoxidation in red blood cells in diabetes. Clin Chim Acta. 1999. 285(1-2):35-44.

34. Jiang M, Jia L, Jiang W, Hu X, Zhou H, Gao X, Lu Z, Zhang Z. Protein disregulation in red blood cell membranes of type 2 diabetic patients. Biochem Biophys Res Commun. 2003. 309(1):196-200.

35. Jiang M, Ding Y, Su Y, Hu X, Li J, Zhang Z. Arginase-flotillin interaction brings arginase to red blood cell membrane. FEBS Lett. 2006. 580(28-29):6561-4. 

36. Wall R, Ross RP, Fitzgerald GF, Stanton C. Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev. 2010. 68(5):280-9. 

37. S. Imamura, T. Morioka, Y. Yamazaki, R. Numaguchi, H. Urata, K. Motoyama, et al. Plasma polyunsaturated fatty acid profile and delta-5 desaturase activity are altered in patients with type 2 diabetes. Metabolism. 2014. 63 (11):1432–1438

38. Navarro-González JF, Mora-Fernández C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol. 2008. 19(3):433-42.

39. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011. 11(2):98-107. 

40. Gupta S, Gambhir JK, Kalra O, Gautam A, Shukla K, Mehndiratta M, Agarwal S, Shukla R. Association of biomarkers of inflammation and oxidative stress with the risk of chronic kidney disease in Type 2 diabetes mellitus in North Indian population. J Diabetes Complications. 2013. 27(6):548-52.

41. Domingueti CP, Dusse LM, Carvalho Md, de Sousa LP, Gomes KB, Fernandes AP. Diabetes mellitus: The linkage between oxidative stress, inflammation, hypercoagulability and vascular complications. J Diabetes Complications. 2016. 30(4):738-45

42. Sertoglu E, Uyanik M, Kayadibi H, Tapan. Erythrocyte membrane fatty acids may be superior to plasma fatty acids in patients with type 2 diabetes. Metabolism. 2015. 64(4):e1-2. 

43. Takkunen M, Agren J, Kuusisto J, Laakso M, Uusitupa M, Schwab U. Dietary fat in relation to erythrocyte fatty acid composition in men. Lipids. 2013. 48(11):1093-102. 

44. Sertoglu E, Kurt I, Tapan S, Uyanik M, Serdar MA, Kayadibi H, El-Fawaeir S. Comparison of plasma and erythrocyte membrane fatty acid compositions in patients with end-stage renal disease and type 2 diabetes mellitus. Chem Phys Lipids. 2014. 178:11-7. 

45. Mahendran Y, Ågren J, Uusitupa M, Cederberg H, Vangipurapu J, Stančáková A, Schwab U, Kuusisto J, Laakso M. Association of erythrocyte membrane fatty acids with changes in glycemia and risk of type 2 diabetes. Am J Clin Nutr. 2014. 99(1):79-85 

46. Mazzanti L, Rabini RA, Testa I, Bertoli E. Modifications induced by diabetes on the physicochemical and functional properties of erythrocyte plasma membrane. Eur J Clin Invest. 1989. 19(1):84-9.

47. Zadhoush F, Sadeghi M, Pourfarzam M. Biochemical changes in blood of type 2 diabetes with and without metabolic syndrome and their association with metabolic syndrome components. J Res Med Sci. 2015. 20(8):763-70  

48. Kumar R. Biochemical changes in erythrocyte membrane in type 2 diabetes mellitus. Indian J Med Sci. 2012. 66(5-6):131-5. 

49. Shahid SM, Rafique R, Mahboob T. Electrolytes and sodium transport mechanism in diabetes mellitus. Pak J Pharm Sci. 2005. 18(2):6-10.

50. Fujita J, Tsuda K, Seno M, Obayashi H, Fukui I, Seino Y. Erythrocyte sodium-lithium countertransport activity as a marker of predisposition to hypertension and diabetic nephropathy in NIDDM. Diabetes Care. 1994. 17(9):977-82.

51. Fujita J, Tsuda K, Seno M, Obayashi H, Fukui I, Seino Y. Elevated erythrocyte sodium-lithium countertransport activity correlates with increased intracellular sodium and free calcium-ion concentration in type 2 diabetes. Diabet Med. 1996. 13(1):53-8.

52. Senior PA, Thomas TH, Marshall SM. Abnormal thiol group modulation of sodium-lithium countertransport and membrane fluidity is associated with a disturbed relationship between serum triacylglycerols and membrane function in type II diabetes. Clin Sci (Lond). 2000. 98(6):673-80.

53. Vareesangthip K, Panthongdee W, Shayakul C, Nitiyanant W, Ong-Aj-Yooth L. Abnormal kinetics of erythrocyte sodium lithium countertransport in patients with diabetic nephropathy in Thailand. J Med Assoc Thai. 2006. 89 Suppl 2:S48-53.

54. González Flecha FL, Castello PR, Caride AJ, Gagliardino JJ, Rossi JP. The erythrocyte calcium pump is inhibited by non-enzymic glycation: studies in situ and with the purified enzyme. Biochem J. 1993. 293(Pt 2):369-75.

55. González Flecha FL, Castello PR, Gagliardino JJ, Rossi JP. Molecular characterization of the glycated plasma membrane calcium pump. J Membr Biol. 1999. 171(1):25-34.

56. Raftos JE, Edgley A, Bookchin RM, Etzion Z, Lew VL, Tiffert T. Normal Ca2+ extrusion by the Ca2+ pump of intact red blood cells exposed to high glucose concentrations. Am J Physiol Cell Physiol. 2001. 280(6):C1449-54.

57. Lew VL, Daw N, Etzion Z, Tiffert T, Muoma A, Vanagas L, Bookchin RM. Effects of age-dependent membrane transport changes on the homeostasis of senescent human red blood cells. Blood. 2007. 110(4):1334-42. 

58. Bookchin RM, Etzion Z, Lew VL, Tiffert T. Preserved function of the plasma membrane calcium pump of red blood cells from diabetic subjects with high levels of glycated haemoglobin. Cell Calcium. 2009. 45(3):260-3. 

59. Balasubramanyam M, Balaji RA, Subashini B, Mohan V. Evidence for mechanistic alterations of Ca2+ homeostasis in Type 2 diabetes mellitus. Int J Exp Diabetes Res. 2001. 1(4):275-87.

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