Increase in red blood cell-nitric oxide synthase dependent nitric oxide production during red blood cell aging in health and disease: A study on age dependent changes of rheologic and enzymatic properties in red blood cells

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Bizjak, Daniel Alexander ^a   Brinkmann, Christian ^a   Bloch, Wilhelm ^a   Grau, Marijke ^a  

^a GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; ARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE; ARGINASE; BIOLOGICAL MARKER; ENZYME INHIBITOR; N(G)-IMINOETHYLORNITHINE; ORNITHINE; PHOSPHATIDYLSERINE;

ADULT; ARTICLE; CASE REPORT; CELL AGING; CELL FUNCTION; CELL SUBPOPULATION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE LIFESPAN; ERYTHROCYTE SHAPE; ERYTHROCYTE STRUCTURE; ERYTHROCYTE VOLUME; FLOW KINETICS; HUMAN; HUMAN CELL; MIDDLE AGED; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BLOOD; BLOOD RHEOLOGY; DRUG EFFECTS; ENZYMOLOGY; ERYTHROCYTE; HEALTH; METABOLISM; METABOLOME; NON INSULIN DEPENDENT DIABETES MELLITUS; STATISTICAL MODEL;

ADULT; ARGINASE; BIOMARKERS; CENTRIFUGATION, DENSITY GRADIENT; DIABETES MELLITUS, TYPE 2; ENZYME INHIBITORS; ERYTHROCYTE AGING; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE VOLUME; ERYTHROCYTES; HEALTH; HEMORHEOLOGY; HUMANS; LINEAR MODELS; METABOLOME; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITES; ORNITHINE; PHOSPHATIDYLSERINES;

EID: 84930674463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125206     Document Type: Article

References (81)

1. Palis J. Primitive and definitive erythropoiesis in mammals. Front in Physio. 2014 Jan 28; 5:3.
2. Franco RS. The measurement and importance of red cell survival. Am J Hematol. 2009; 84(2): 109-14. doi: 10.1002/ajh.21298 PMID: 19025796
3. Rifkind JM, Nagababu E. Hemoglobin Redox Reactions and Red Blood Cell Aging. Antioxid Redox Signal. 2013; 18(17) 2274-83. doi: 10.1089/ars.2012.4867 PMID: 23025272
4. Chandramouli V, Carter JR Jr. Cell membrane changes in chronically diabetic rats. Diabetes 1975; 24(3): 257-62. PMID: 163776
5. Nash GB, Wyard SJ. Changes in surface area and volume measured by micropipette aspiration for erythrocytes ageing in vivo. Biorheology 1980; 17(5-6): 479-84. PMID: 7407351
6. Linderkamp O, Meiselman HJ. Geometric, osmotic, and membrane mechanical properties of density-separated human red cells. Blood 1982; 59(6): 1121-7. PMID: 7082818
7. Clark MR, Mohandas N, Shohet SB. Osmotic gradient ektacytometry: comprehensive characterisation of red cell volume and surface maintenance. Blood 1983: 61(5): 899-910. PMID: 6831052
8. Nash GB, Meiselman HJ. Red cell and ghost viscoelasticity. Effects of hemoglobin concentration and in vivo aging. Biophys J. 1983; 43(1): 63-73. PMID: 6882863
9. Bosman GJCGM, Lasonder E, Groenen-Döpp YAM, Willekens FLA, Werre JM, Novotný VM. Comparative proteomics of erythrocyte aging in vivo and in vitro. J Proteomics 2010 3; 73(3): 396-402. doi: 10.1016/j.jprot.2009.07.010 PMID: 19660581
10. Antonelou MH, Kriebardis AG, Papassideri IS. Aging and death signalling in mature red cells: from basic science to transfusion practice. Blood Transfus. 2010; 8(3): 39-47.
11. Connor J, Pak CC, Schroit AJ. Exposure of phsophatidylserine in the outher leaflet of human red blood cells. J Biol Chem. 1994 28; 269(4): 2399-404. PMID: 8300565
12. Kleinbongard P, Schulz R, Rassaf T, Lauer T, Dejam A, Jax T, et al. Red blood cells express a functional endothelial nitric oxide synthase. Blood 2006 1; 107(7): 2943-51. PMID: 16368881
13. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993 30; 329(27): 2002-12. PMID: 7504210
14. Kleinbongard P, Keymel S, Kelm M. New functional aspects of the L-arginine-nitric oxide metabolism within the circulating blood. Thromb Haemost. 2007; 98(5): 970-4. PMID: 18000600
15. Tessari P, Cecchet D, Cosma A, Vettore M, Coracina A, Millioni R, et al. Nitric oxide synthesis is reduced in subjects with type 2 diabetes and nephropathy. Diabetes 2010; 59(9): 2152-9. doi: 10.2337/db09-1772 PMID: 20484137
16. Kolluru GK, Bir SC, Kevil CG. Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med. 2012. doi: 10.1155/2012/918267
17. Hobbs AJ, Gladwin MT, Patel RP, Williams DL, Butler AR. Haemoglobin: NO transporter, NO inactivator or NOne of the above? Trends Pharmacol Sci. 2002; 23(9): 406-11. PMID: 12237152
18. Liu X, Miller MJ, Joshi MS, Sadowska-Krowicka H, Clark DA, Lancaster JR Jr. Diffusion-limited reaction of free nitric oxide with erythrocytes. J Biol Chem. 1998; 273(30): 18709-13. PMID: 9668042
19. Liu X, Samouilov A, Lancaster JR Jr, Zweier JL. Nitric oxide uptake by erythrocytes is primarily limited by extracellular diffusion not membrane resistance. J Biol Chem.; 277(29): 26194-9. PMID: 12006567
20. Joshi MS, Ferguson TB Jr, Han TH, Hyduke DR, Liao JC, Rassaf T, et al. Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions. Proc Natl Acad Sci USA 2002; 99(16): 10341-6. PMID: 12124398
21. Vaughn MW, Huang KT, Kuo L, Liao JC. Erythrocyte consumption of nitric oxide: competition experiment and model analysis. Nitric Oxide. 2001; 5(1): 18-31. PMID: 11178933
22. Sakai H, Sato A, Masuda K, Takeoka S, Tsuchida E. Encapsulation of concentrated hemoglobin solution in phospholipid vesicles retards the reaction with NO, but not CO, by intracellular diffusion barrier. J Biol Chem. 2008; 283(3): 1508-17. PMID: 18003613
23. Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol. 2006; 26(4): 697-705. PMID: 16424350
24. Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996; 380(6571): 221-6. PMID: 8637569
25. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, et al. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 1997; 276(5321): 2034-7. PMID: 9197264
26. Gow AJ, Stamler JS. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 1998 Jan 8; 391(6663): 169-73. PMID: 9428761
27. Sharma VS, Ranney HM. The dissociation of NO from nitrosylhemoglobin. J Biol Chem. 1978; 253(18): 6467-72. PMID: 681362
28. Moore EG, Gibson QH. Cooperativity in the dissociation of nitric oxide from hemoglobin. J Biol Chem. 1976; 251(9): 2788-94. PMID: 1262343
29. Ignarro LJ, Fukuto JM, Griscavage JM, Rogers NE, Byms RE. Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: comparison with enzymatically formed nitric oxide from L-arginine. Proc Natl Acad Sci USA 1993; 90(17): 8103-7. PMID: 7690141
30. Kelm M, Preik-Steinhoff H, Preik M, Stauer BE. Serum nitrite sensitively reflects endothelial NO formation in human forearm vasculature: evidence for biochemical assessment of the endothelial L-arginine-NO pathway. Cardiovasc Res. 1999; 41(3): 765-72. PMID: 10435049
31. Huang KT, Keszler A, Patel N, Patel RP, Gladwin MT, Kim-Shapiro DB, et al. The reaction between nitrite and deoxyhemoglobin. Reassessment of reaction kinetics and stoichiometry. J Biol Chem. 2005; 280(35): 31126-31. PMID: 15837788
32. Huang Z, Shiva S, Kim-Shapiro DB, Patel RP, Ringwood LA, Irby CE, et al. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. J Clin Invest. 2005; 115(8): 2099-107. PMID: 16041407
33. Rassaf T, Flögel U, Drexhage C, Hendgen-Cotta U, Kelm M, Schrader J. Nitrite reductase function of deoxyhemoglobin: oxygen sensor and regulator of cardiac energetics and function. Circ Res. 2007; 100(12): 1749-54. PMID: 17495223
34. Shiva S. Nitrite: A physiological store of nitric oxide and modulator of mitochondrial function. Redox Biol. 2013; 1(1): 40-4. PMID: 23710434
35. Totzeck M, Hendgen-Cotta UB, Luedike P, Berenbrink M, Klare JP, Steinhoff HJ, et al. Nitrite regulates hypoxic vasodilation via myoglobin-dependent nitric oxide generation. Circulation 2012; 126(3): 325-34. doi: 10.1161/CIRCULATIONAHA.111.087155 PMID: 22685116
36. Grau M, Pauly S, Ali J, Walpurgis K, Thevis M, Bloch W, et al. RBC-NOS dependent S-nitrosylation of cytoskeletal proteins improves RBC deformability. PLoS One 2013; 8(2): e56759. doi: 10.1371 PMID: 23424675
37. Suhr F, Brenig J, Müller R, Behrens H, Bloch W, Grau M. Moderate exercise promotes human RBC-NOS activity, NO production and deformability through Akt kinase pathway. PLoS One 2012; 7(9): e45982. doi: 10.1371 PMID: 23049912
38. Grau M, Mozar A, Charlot K, Lamarre Y, Weyel L, Suhr F, et al. High red blood cell nitric oxide synthase activation is not associated with improved vascular function and red blood cell deformability in sickle cell anaemia. Br J Haematol. 2015; 168(5): 728-36. doi: 10.1111/bjh.13185 PMID: 25316332
39. Bor-Kucukatay M, Wenby RB, Meiselman HJ, Baskurt OK. Effects of nitric oxide on red blood cell deformability. Am J Physiol Heart Circ Physiol. 2003; 284(5): 1577-84. PMID: 12521942
40. Simmonds MJ, Detterich JA, Connes P. Nitric oxide, vasodilation and the red blood cell. Biorheology 2014; 51(2-3): 121-34. doi: 10.3233/BIR-14012 PMID: 25480930
41. Schwartz RS, Madsen JW, Rybicki AC, Nagel RL. Oxidation of spectrin and deformability defects in diabetic erythrocytes. Diabetes 1991; 40(6): 701-8. PMID: 2040386
42. Le Devehat C, Khodabandehlou T, Vimeux M. Relationship between hemorheological and microcirculatory abnormalities in diabetes mellitus. Diabete Metab. 1994; 20(4): 401-4. PMID: 7843471
43. Zimny S, Dessel F, Ehren M, Pfohl M, Schatz H. Early detection of microcirculatory impairment in diabetic patients with foot at risk. Diabetes Care 2001; 24(10): 1810-4. PMID: 11574447
44. Yang J, Gonon AT, Sjöquist PO, Lundberg JO, Pernow J. Arginase regulates red blood cell nitric oxid synthase and export of cardioprotective nitric oxide bioactivity. Proc Natl Acad Sci USA 2013; 110(37): 15049-54. doi: 10.1073/pnas.1307058110 PMID: 23980179
45. Ikemoto M, Tabata M, Miyake T, Kono T, Mori M, Totani M, et al. Expression of human liver arginase in Escherichia coli. Purification and properties of the product. Biochem J. 1990 Sep 15; 270(3): 697-703. PMID: 2241902
46. Munder M. Arginase: an emerging key player in the mammalian immune system. British Journal of Pharmacology 2009; 158(3): 638-51. doi: 10.1111/j.1476-5381.2009.00291.x PMID: 19764983
47. Savu O, Iosif L, Bradescu OM, Serafinceanu C, Papacocea R, Stoian I. L-arginine catabolism is driven mainly towards nitric oxide synthesis in the erythrocytes of patients with type 2 diabetes at first clinical onset. Ann Clin Biochem. 2015; 52(Pt 1): 135-43.
48. Grönros J, Jung C, Lundberg JO, Cerrato R, Ostenson CG, Pernow J. Arginase inhibition restores in vivo coronary microvascular function in type 2 diabetic rats. Am J Physiol Heart Circ Physiol. 2011; 300(4): 1174-81. doi: 10.1152/ajpheart.00560.2010 PMID: 21297024
49. Romero MJ, Platt DH, Tawfik HE, Labazi M, El-Remessy AB, Bartoli M, et al. Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ Res. 2008; 102(1): 95-102. PMID: 17967788
50. Bivalacqua TJ, Hellstrom WJ, Kadowitz PJ, Champion HC. Increased expression of arginase II in human diabetic corpus cavernosum: in diabetic-associated erectile dysfunction. Biochem Biophys Res Commun. 2001; 283(4): 923-7. PMID: 11350073
51. Shemyakin A, Kövamees O, Rafnsson A, Böhm F, Svenarud P, Settergren M, et al. Arginase inhibition improves endothelial function in patients with coronary artery disease and type 2 diabetes mellitus. Circulation 2012; 126(25): 2943-50. doi: 10.1161/CIRCULATIONAHA.112.140335 PMID: 23183942
52. Bosch FH, Werre JM, Roerdinkholder-Stoelwinder B, Huls TH, Willekens FL, Halie MR. Characteristics of red blood cell populations fractionated with a combination of counterflow centrifugation and Percoll separation. Blood 1992; 79(1): 254-60. PMID: 1728314
53. Gerke V, Moss SE. Annexins: From Structure to Function. Physiol Rev. 2002; 82(2): 331-71. PMID: 11917092
54. Clark MR, Mohandas N, Shohet S. Osmotic gradient ektacytometry: comprehensive characterisation of red cell volume and surface maintenance. Blood 1983 May; 61(5): 899-910. PMID: 6831052
55. Hardeman MR, Goedhart PT, Dobbe JGG, Lettinga KP. Laser-assisted Optical Rotational Analyser (LORCA); A new measurement for measurement of various structural hemorheological parameters. Clin Hemorheol. 1994; 14(4): 605-18.
56. Hardeman MR, Dobbe JG, Ince C. The Laser-assisted Optical Rotational Cell Analyzer (LORCA) as red blood cell aggregometer. Clin Hemorheol Microcirc. 2001; 25(1): 1-11. PMID: 11790865
57. Green DJ, Maiorana A, O'Driscoll G, Taylor R. Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol. 2004 561(Pt 1): 1-25. PMID: 15375191
58. Hayashino Y, Jackson JL, Hirata T, Fukumori N, Nakamura F, Fukuhara S, et al. Effects of exercise on C-reactive protein, inflammatory cytokine and adipokine in patients with type 2 diabetes: A meta-analysis of randomized controlled trials. Metabolism 2014; 63(3): 431-40. doi: 10.1016/j.metabol.2013.08.018 PMID: 24355625
59. Grau M, Hendgen-Cotta UB, Brouzos P, Drexhage C, Rassaf, Lauer T, et al. Recent methodological advances in the analysis of nitrite in the human circulation: nitrite as a biochemical paramteter of the L-arginine /NO pathway. J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 851(1-2): 106-23. PMID: 17400039
60. Pelletier MM, Kleinbongard P, Ringwood L, Hito R, Hunter CJ, Schechter AN, et al. The measurement of blood and plasma nitrite by chemilumiscence: pitfalls and solutions. Free Radic Biol Med. 2006; 41(4): 541-8. PMID: 16863986
61. Hendgen-Cotta UB, Grau M, Rassaf T, Gharini P, Kelm M, Kleinbongard P. Reductive gas-phase chemiluminescence and flow injection analysis for measurement of the nitric oxide pool in biological matrices. Methods Enzymol. 2008; 441: 295-315. doi: 10.1016/S0076-6879(08)01216-0 PMID: 18554541
62. Corraliza IM, Campo ML, Soler G, Modolell M. Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 1994; 174(1-2): 231-5. PMID: 8083541
63. Gifford SC, Derganc J, Shevkoplyas S, Yoshida T, Bitensky MW. A detailed study of time-dependent changes in human red blood cells: from reticulocyte maturation to erythrocyte senescence. Br J Haematol. 2006; 135(3): 395-404. PMID: 16989660
64. Handelman GJ, Levin NW. Red cell survival: relevance and mechanism involved. J Ren Nutr. 2010; 20(5): 84-8.
65. Mazzanti L, Faloia E, Rabini RA, Staffolani R, Kantar A, Fiorini R, et al. Diabetes mellitus induces red blood cell plasma membrane alterations possibly affecting the aging process. Clin Biochem. 1992; 25(1): 41-6. PMID: 1312917
66. Bosman GJCGM, Were JM, Willekens FLA, Novotný MJ. Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med. 2008; 18(6): 335-47. doi: 10.1111/j.1365-3148.2008.00892.x PMID: 19140816
67. Smith JA, Martin DT, Telford RD, Ballas SK. Greater erythrocyte deformability in world-class endurance athletes. Am. J. Physiol. 1999; 276(6 Pt 2): 2188-93. PMID: 10362703
68. Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr. Opin. Clin. Nutr. Metab. Care 2002; 5(5): 561-8. PMID: 12172481
69. Virtue MA, Furne JK, Nuttall FQ, Levitt MD. Relationship between GHb concentration and erythrocyte survival determined from breath carbon monoxide concentration. Diabetes Care 2004; 27(4): 931-5. PMID: 15047651
70. Subashinghe W, Spence DM. Simultaneous determination of cell aging and ATP release from erythrocytes and its implications in type 2 diabetes. Anal chim Acta 2008; 618(2): 227-33. doi: 10.1016/j.aca.2008.04.061 PMID: 18513544
71. Quiñones MJ, Nicholas SB, Lyon CJ. Insulin resistance and the endothelium. Curr Diab Rep. 2005; 5(4): 246-53. PMID: 16033673
72. Owusu BY, Stapley R, Honavar J, Patel RP. Effects of Erythrocyte Aging on Nitric Oxide and Nitrite Metabolism. Antioxid Redox Signal. 2013 Oct 10; 19(11): 1198-1208. doi: 10.1089/ars.2012.4884 PMID: 23311696
73. Bruckdorfer R. The basics about nitric oxide. Mol Aspects Med. 2005; 26(1-2): 3-31. PMID: 16125764
74. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen M, Feelisch M, et al. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 2001; 98(22): 12814-9. PMID: 11606734
75. Ramírez-Zamora S, Méndez-Rodriguez ML, Olguín-Martinez M, Sánchez-Sevilla L, Quintana-Quintana M, García-García N, et al. Increased Erythroctes By-Products of Arginine Catabolism are associated with Hyperglycemia and could be involved in the Pathogenesis of Type 2 Diabetes Mellitus. PLoS One 2013; 8(6). e66823. doi: 10.1371 PMID: 23826148
76. Horn P, Cortese-Krott MM, Amabile N, Hundsdörfer C, Kröncke KD, Kelm M, et al. Circulating microparticles carry a functional endothelial nitric oxide synthase that is decreased in patients with endothelial dysfunction. J Am Heart Assoc. 2012; 2(1). e003764. doi: 10.1161 PMID: 23525410
77. Alaarg A, Schiffelers RM, van Solinge WW, van Wijk R. Red blood cell vesiculation in hereditary haemolytic anemia. Front Physiol. 2013; 4(365). doi: 10.3389/fphys.2013.00365 PMID: 24379786
78. Yang Z, Ming XF. Arginase: the emerging therapeutic target for vascular oxidative stress and inflammation. Front Immunol. 2013; 4(149). doi: 10.3389/fimmu.2013.00149 PMID: 23781221
79. Witte MB, Thornton FJ, Tantry U, Barbul A. L-Arginine supplementation enhance diabetic wound healing: involvement of the nitric oxide synthase and arginase pathways. Metabolism 2002; 51(10): 1269-73. PMID: 12370845
80. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol. 2007; 34(9): 906-11. PMID: 17645639
81. Gupta BL, Preet A, Baquer NZ. Protective effects of sodium orthovanadate in diabetic reticulocytes and ageing red blood cells of Wistar rats. J. Biosci. 2004; 29(1): 73-9. PMID: 15286406