Moderate Exercise Promotes Human RBC-NOS Activity, NO Production and Deformability through Akt Kinase Pathway

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Suhr, Frank ^a   Brenig, Julian ^a   Müller, Rebecca ^a   Behrens, Hilke ^a   Bloch, Wilhelm ^a   Grau, Marijke ^a  

^a GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ADULT; ARTICLE; BLOOD GAS ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ERYTHROCYTE DEFORMABILITY; EXERCISE INTENSITY; FLUOROMETRY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; SHEAR STRESS; UPREGULATION; WESTERN BLOTTING;

ADULT; ANTHROPOMETRY; BLOOD GAS ANALYSIS; ERYTHROCYTES; EXERCISE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROCIRCULATION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RUNNING; SHEAR STRENGTH; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

EID: 84866716792     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045982     Document Type: Article

References (54)

1. Gladwin MT, Crawford JH, Patel RP, (2004) The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic Biol Med 36: 707-717.
2. Malan D, Ji GJ, Schmidt A, Addicks K, Hescheler J, et al. (2004) Nitric oxide, a key signaling molecule in the murine early embryonic heart. FASEB J 18: 1108-1110.
3. Kroncke KD, Fehsel K, Kolb-Bachofen V, (1997) Nitric oxide: cytotoxicity versus cytoprotection-how, why, when, and where? Nitric Oxide 1: 107-120.
4. Cho HJ, Xie QW, Calaycay J, Mumford RA, Swiderek KM, et al. (1992) Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176: 599-604.
5. Ghafourifar P, Schenk U, Klein SD, Richter C, (1999) Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J Biol Chem 274: 31185-31188.
6. Giulivi C, Poderoso JJ, Boveris A, (1998) Production of nitric oxide by mitochondria. J Biol Chem 273: 11038-11043.
7. Jubelin BC, Gierman JL, (1996) Erythrocytes may synthesize their own nitric oxide. Am J Hypertens 9: 1214-1219.
8. Kleinbongard P, Schulz R, Rassaf T, Lauer T, Dejam A, et al. (2006) Red blood cells express a functional endothelial nitric oxide synthase. Blood 107: 2943-2951.
9. Mihov D, Vogel J, Gassmann M, Bogdanova A, (2009) Erythropoietin activates nitric oxide synthase in murine erythrocytes. Am J Physiol Cell Physiol 297: C378-C388.
10. Ulker P, Yaras N, Yalcin O, Celik-Ozenci C, Johnson PC, et al. (2011) Shear stress activation of nitric oxide synthase and increased nitric oxide levels in human red blood cells. Nitric Oxide 24: 184-191.
11. Green DJ, Maiorana A, O'Driscoll G, Taylor R, (2004) Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol 561: 1-25.
12. Yalcin O, Bor-Kucukatay M, Senturk UK, Baskurt OK, (2000) Effects of swimming exercise on red blood cell rheology in trained and untrained rats. J Appl Physiol 88: 2074-2080.
13. Ozuyaman B, Grau M, Kelm M, Merx MW, Kleinbongard P, (2008) RBC NOS: regulatory mechanisms and therapeutic aspects. Trends Mol Med 14: 314-322.
14. Bor-Kucukatay M, Wenby RB, Meiselman HJ, Baskurt OK, (2003) Effects of nitric oxide on red blood cell deformability. Am J Physiol Heart Circ Physiol 284: H1577-H1584.
15. Suhr F, Porten S, Hertrich T, Brixius K, Schmidt A, et al. (2009) Intensive exercise induces changes of endothelial nitric oxide synthase pattern in human erythrocytes. Nitric Oxide 20: 95-103.
16. Senturk UK, Gunduz F, Kuru O, Aktekin MR, Kipmen D, et al. (2001) Exercise-induced oxidative stress affects erythrocytes in sedentary rats but not exercise-trained rats. J Appl Physiol 91: 1999-2004.
17. Szygula Z, (1990) Erythrocytic system under the influence of physical exercise and training. Sports Med 10: 181-197.
18. Michell BJ, Griffiths JE, Mitchelhill KI, Rodriguez-Crespo I, Tiganis T, et al. (1999) The Akt kinase signals directly to endothelial nitric oxide synthase. Curr Biol 9: 845-848.
19. Ulker P, Sati L, Celik-Ozenci C, Meiselman HJ, Baskurt OK, (2009) Mechanical stimulation of nitric oxide synthesizing mechanisms in erythrocytes. Biorheology 46: 121-132.
20. Ludolph B, Bloch W, Kelm M, Schulz R, Kleinbongard P, (2007) Short-term effect of the HMG-CoA reductase inhibitor rosuvastatin on erythrocyte nitric oxide synthase activity. Vasc Health Risk Manag 3: 1069-1073.
21. Kabanova S, Kleinbongard P, Volkmer J, Andree B, Kelm M, et al. (2009) Gene expression analysis of human red blood cells. Int J Med Sci 6: 156-159.
22. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, et al. (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem 70: 2446-2453.
23. Itoh Y, Ma FH, Hoshi H, Oka M, Noda K, et al. (2000) Determination and bioimaging method for nitric oxide in biological specimens by diaminofluorescein fluorometry. Anal Biochem 287: 203-209.
24. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, et al. (1998) Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett 427: 263-266.
25. Espey MG, Miranda KM, Thomas DD, Wink DA, (2001) Distinction between nitrosating mechanisms within human cells and aqueous solution. J Biol Chem 276: 30085-30091.
26. Hardeman MR, Dobbe JG, Ince C, (2001) The Laser-assisted Optical Rotational Cell Analyzer (LORCA) as red blood cell aggregometer. Clin Hemorheol Microcirc 25: 1-11.
27. Baskurt OK, Boynard M, Cokelet GC, Connes P, Cooke BM, et al. (2009) New guidelines for hemorheological laboratory techniques. Clin Hemorheol Microcirc 42: 75-97.
28. Lincoln TM, (1989) Cyclic GMP and mechanisms of vasodilation. Pharmacol Ther 41: 479-502.
29. Hofmann F, Ammendola A, Schlossmann J, (2000) Rising behind NO: cGMP-dependent protein kinases. J Cell Sci 113 (Pt 10): 1671-1676.
30. Petrov V, Amery A, Lijnen P, (1994) Role of cyclic GMP in atrial-natriuretic-peptide stimulation of erythrocyte Na+/H+ exchange. Eur J Biochem 221: 195-199.
31. Petrov V, Lijnen P, (1996) Regulation of human erythrocyte Na+/H+ exchange by soluble and particulate guanylate cyclase. Am J Physiol 271: C1556-C1564.
32. Bateman RM, Sharpe MD, Ellis CG, (2003) Bench-to-bedside review: microvascular dysfunction in sepsis-hemodynamics, oxygen transport, and nitric oxide. Crit Care 7: 359-373.
33. Pries AR, Secomb TW, (2003) Rheology of the microcirculation. Clin Hemorheol Microcirc 29: 143-148.
34. Forstermann U, Munzel T, (2006) Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714.
35. Forstermann U, Nakane M, Tracey WR, Pollock JS, (1993) Isoforms of nitric oxide synthase: functions in the cardiovascular system. Eur Heart J 14Suppl I: 10-15.
36. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R, (2001) Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 88: E68-E75.
37. Fleming I, Busse R, (2003) Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 284: R1-12.
38. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, et al. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605.
39. Zhang QJ, McMillin SL, Tanner JM, Palionyte M, Abel ED, et al. (2009) Endothelial nitric oxide synthase phosphorylation in treadmill-running mice: role of vascular signalling kinases. J Physiol 587: 3911-3920.
40. Chmiel B, Cierpka L, (2003) Organ preservation solutions impair deformability of erythrocytes in vitro. Transplant Proc 35: 2163-2164.
41. de Oliveira S, Silva-Herdade AS, Saldanha C, (2008) Modulation of erythrocyte deformability by PKC activity. Clin Hemorheol Microcirc 39: 363-373.
42. Huang Q, Yuan Y, (1997) Interaction of PKC and NOS in signal transduction of microvascular hyperpermeability. Am J Physiol 273: H2442-H2451.
43. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ, (1996) ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol 271: H2717-H2722.
44. Busse R, Ogilvie A, Pohl U, (1988) Vasomotor activity of diadenosine triphosphate and diadenosine tetraphosphate in isolated arteries. Am J Physiol 254: H828-H832.
45. Bogle RG, Coade SB, Moncada S, Pearson JD, Mann GE, (1991) Bradykinin and ATP stimulate L-arginine uptake and nitric oxide release in vascular endothelial cells. Biochem Biophys Res Commun 180: 926-932.
46. Furchgott RF, Zawadzki JV, (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376.
47. Wan J, Ristenpart WD, Stone HA, (2008) Dynamics of shear-induced ATP release from red blood cells. Proc Natl Acad Sci U S A 105: 16432-16437.
48. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ, (1998) Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol 275: H1726-H1732.
49. Sprague RS, Stephenson AH, Ellsworth ML, Keller C, Lonigro AJ, (2001) Impaired release of ATP from red blood cells of humans with primary pulmonary hypertension. Exp Biol Med (Maywood) 226: 434-439.
50. Sprague RS, Stephenson AH, Bowles EA, Stumpf MS, Lonigro AJ, (2006) Reduced expression of G(i) in erythrocytes of humans with type 2 diabetes is associated with impairment of both cAMP generation and ATP release. Diabetes 55: 3588-3593.
51. Kaneko FT, Arroliga AC, Dweik RA, Comhair SA, Laskowski D, et al. (1998) Biochemical reaction products of nitric oxide as quantitative markers of primary pulmonary hypertension. Am J Respir Crit Care Med 158: 917-923.
52. Lin KY, Ito A, Asagami T, Tsao PS, Adimoolam S, et al. (2002) Impaired nitric oxide synthase pathway in diabetes mellitus: role of asymmetric dimethylarginine and dimethylarginine dimethylaminohydrolase. Circulation 106: 987-992.
53. Robertson BE, Schubert R, Hescheler J, Nelson MT, (1993) cGMP-dependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am J Physiol 265: C299-C303.
54. Armstead WM, (1996) Role of ATP-sensitive K+ channels in cGMP-mediated pial artery vasodilation. Am J Physiol 270: H423-H426.