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Oxidative Medicine and Cellular Longevity
Volume 2014, Article ID 203512, 9 pages
http://dx.doi.org/10.1155/2014/203512
Clinical Study

L-Arginine/NO Pathway Is Altered in Children with Haemolytic-Uraemic Syndrome (HUS)

1Department of Paediatric Kidney, Liver and Metabolic Diseases, Hannover Medical School, Carl-Neuberg-Straße 1, 30625 Hannover, Germany
2Institute of Clinical Pharmacology, Hannover Medical School, Carl-Neuberg-Straße 1, 30625 Hannover, Germany
3Department of Paediatrics, University of Mainz, Langenbeckstraße 1, 55131 Mainz, Germany
4Institute of Biometry, Hannover Medical School, Carl-Neuberg-Straße 1, 30625 Hannover, Germany
5Department of Medicine III, Klinikum Fulda, Pacelliallee 4, 36043 Fulda, Germany
6Department of Neuropaediatrics, University Children’s Hospital, Ruhr University Bochum, Gudrunstraße 56, 44791 Bochum, Germany

Received 6 January 2014; Accepted 11 February 2014; Published 17 March 2014

Academic Editor: Daniela Giustarini

Copyright © 2014 Nele Kirsten Kanzelmeyer et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. M. T. Loo, L. Monnens, T. van der Velden, M. Karmali, L. van de Heuvel, and V. van Hinsbergh, “Shiga toxin-1 affects nitric oxide production by human glomerular endothelial and mesangial cells,” Pediatric Nephrology, vol. 21, no. 12, pp. 1815–1823, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Razzaq, “Hemolytic uremic syndrome: an emerging health risk,” The American Family Physician, vol. 74, no. 6, pp. 991–996, 2006. View at Google Scholar · View at Scopus
  3. S. Loos, T. Ahlenstiel, B. Kranz et al., “An outbreak of Shiga toxin-producing Escherichia coli O104:H4 hemolytic uremic syndrome in Germany: presentation and short-term outcome in children,” Clinical Infectious Diseases, vol. 55, no. 6, pp. 753–759, 2012. View at Publisher · View at Google Scholar
  4. A. Gerber, H. Karch, F. Allerberger, H. M. Verweyen, and L. B. Zimmerhackl, “Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997–2000, in Germany and Austria: a prospective study,” Journal of Infectious Diseases, vol. 186, no. 4, pp. 493–500, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. S. E. Richardson, M. A. Karmali, L. E. Becker, and C. R. Smith, “The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing Escherichia coli infections,” Human Pathology, vol. 19, no. 9, pp. 1102–1108, 1988. View at Google Scholar · View at Scopus
  6. C. D. Inward, A. J. Howie, M. M. Fitzpatrick, F. Rafaat, D. V. Milford, and C. M. Taylor, “Renal histopathology in fatal cases of diarrhoea-associated haemolytic uraemic syndrome,” Pediatric Nephrology, vol. 11, no. 5, pp. 556–559, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Gordjani, A. H. Sutor, L. B. Zimmerhackl, and M. Brandis, “Hemolytic uremic syndromes in childhood,” Seminars in Thrombosis and Hemostasis, vol. 23, no. 3, pp. 281–293, 1997. View at Google Scholar · View at Scopus
  8. A. X. Garg, R. S. Suri, N. Barrowman et al., “Long-term renal prognosis of diarrhea-associated hemolytic uremic syndrome: a systematic review, meta-analysis, and meta-regression,” The Journal of the American Medical Association, vol. 290, no. 10, pp. 1360–1370, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Lingwood, “Shiga toxin receptor glycolipid binding. Pathology and utility,” Methods in Molecular Medicine, vol. 73, pp. 165–186, 2003. View at Google Scholar · View at Scopus
  10. D. D. Rees, R. M. J. Palmer, and S. Moncada, “Role of endothelium-derived nitric oxide in the regulation of blood pressure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 9, pp. 3375–3378, 1989. View at Google Scholar · View at Scopus
  11. J. P. Cooke and V. J. Dzau, “Nitric oxide synthase: role in the genesis of vascular disease,” Annual Review of Medicine, vol. 48, pp. 489–509, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. L. J. Ignarro, “Biosynthesis and metabolism of endothelium-derived nitric oxide,” Annual Review of Pharmacology and Toxicology, vol. 30, pp. 535–560, 1990. View at Google Scholar · View at Scopus
  13. D. Tsikas, F. Gutzki, and D. O. Stichtenoth, “Circulating and excretory nitrite and nitrate as indicators of nitric oxide synthesis in humans: methods of analysis,” European Journal of Clinical Pharmacology, vol. 62, no. 13, pp. 51–59, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Marletta, “Nitric oxide synthase structure and mechanism,” The Journal of Biological Chemistry, vol. 268, no. 17, pp. 12231–12234, 1993. View at Google Scholar · View at Scopus
  15. V. Achan, M. Broadhead, M. Malaki et al., “Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 8, pp. 1455–1459, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. J. M. Leiper and P. Vallance, “The synthesis and metabolism of asymmetric dimethylarginine (ADMA),” European Journal of Clinical Pharmacology, vol. 62, no. 13, pp. 33–38, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. T. Kielstein, S. M. Bode-Böger, J. C. Frölich, H. Haller, and R. H. Böger, “Relationship of asymmetric dimethylarginine to dialysis treatment and atherosclerotic disease,” Kidney International Supplements, vol. 78, pp. S9–S13, 2001. View at Publisher · View at Google Scholar
  18. H. Herlitz, A. Petersson, L. Sigström, A. Wennmalm, and G. Westberg, “The arginine-nitric oxide pathway in thrombotic microangiopathy,” Scandinavian Journal of Urology and Nephrology, vol. 31, no. 5, pp. 477–479, 1997. View at Google Scholar · View at Scopus
  19. T. Lücke, N. Kanzelmeyer, M. J. Kemper, D. Tsikas, and A. M. Das, “Developmental changes in the L-arginine/nitric oxide pathway from infancy to adulthood: plasma asymmetric dimethylarginine levels decrease with age,” Clinical Chemistry and Laboratory Medicine, vol. 45, no. 11, pp. 1525–1530, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Lücke, N. Kanzelmeyer, K. Chobanyan et al., “Elevated asymmetric dimethylarginine (ADMA) and inverse correlation between circulating ADMA and glomerular filtration rate in children with sporadic focal segmental glomerulosclerosis (FSGS),” Nephrology Dialysis Transplantation, vol. 23, no. 2, pp. 734–740, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Facorro, F. Aguirre, L. Florentin et al., “Oxidative stress and membrane fluidity in erythrocytes from patients with hemolytic uremic syndrome,” Acta Physiologica, Pharmacologica et Therapeutica Latinoamericana, vol. 47, no. 3, pp. 137–146, 1997. View at Google Scholar · View at Scopus
  22. V. Ferraris, A. Acquier, J. R. Ferraris, G. Vallejo, C. Paz, and C. F. Mendez, “Oxidative stress status during the acute phase of haemolytic uraemic syndrome,” Nephrology Dialysis Transplantation, vol. 26, no. 3, pp. 858–864, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. S. A. Gomez, M. J. Abrey-Recalde, C. A. Panek et al., “The oxidative stress induced in vivo by Shiga toxin-2 contributes to the pathogenicity of haemolytic uraemic syndrome,” Clinical and Experimental Immunology, vol. 173, no. 3, pp. 463–472, 2013. View at Publisher · View at Google Scholar
  24. T. Kajiume, A. Nagita, S. Yoshimi, K. Kobayashi, and N. Kataoka, “A case of hemolytic uremic syndrome improved with nitric oxide,” Bone Marrow Transplantation, vol. 25, no. 1, pp. 109–110, 2000. View at Google Scholar · View at Scopus
  25. V. V. Pham, D. O. Stichtenoth, and D. Tsikas, “Nitrite correlates with 3-nitrotyrosine but not with the F2-isoprostane 15(S)-8-iso-PGF2α in urine of rheumatic patients,” Nitric Oxide—Biology and Chemistry, vol. 21, no. 3-4, pp. 210–215, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Tsikas, B. Schubert, F. Gutzki, J. Sandmann, and J. C. Frölich, “Quantitative determination of circulating and urinary asymmetric dimethylarginine (ADMA) in humans by gas chromatography-tandem mass spectrometry as methyl ester tri(N-pentafluoropropionyl) derivative,” Journal of Chromatography B, vol. 798, no. 1, pp. 87–99, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Tsikas, “Simultaneous derivatization and quantification of the nitric oxide metabolites nitrite and nitrate in biological fluids by gas chromatography/mass spectrometry,” Analytical Chemistry, vol. 72, no. 17, pp. 4064–4072, 2000. View at Google Scholar · View at Scopus
  28. D. Tsikas, A. Wolf, A. Mitschke, F. Gutzki, W. Will, and M. Bader, “GC-MS determination of creatinine in human biological fluids as pentafluorobenzyl derivative in clinical studies and biomonitoring: inter-laboratory comparison in urine with Jaffé, HPLC and enzymatic assays,” Journal of Chromatography B, vol. 878, no. 27, pp. 2582–2592, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Tsikas, T. Thum, T. Becker et al., “Accurate quantification of dimethylamine (DMA) in human urine by gas chromatography-mass spectrometry as pentafluorobenzamide derivative: evaluation of the relationship between DMA and its precursor asymmetric dimethylarginine (ADMA) in health and disease,” Journal of Chromatography B, vol. 851, no. 1-2, pp. 229–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Woywodt, A. D. Blann, T. Kirsch et al., “Isolation and enumeration of circulating endothelial cells by immunomagnetic isolation: proposal of a definition and a consensus protocol,” Journal of Thrombosis and Haemostasis, vol. 4, no. 3, pp. 671–677, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Jacobi and P. S. Tsao, “Asymmetrical dimethylarginine in renal disease: limits of variation or variation limits? A systematic review,” The American Journal of Nephrology, vol. 28, no. 2, pp. 224–237, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Bogdan, M. Röllinhoff, and A. Difenbach, “The role of nitric oxide in innate immunity,” Immunological Reviews, vol. 173, no. 1, pp. 17–26, 2000. View at Publisher · View at Google Scholar
  33. T. Lücke, D. Tsikas, N. K. Kanzelmeyer et al., “Vaso-occlusion in Schimke-immuno-osseous dysplasia: is the NO pathway involved?” Hormone and Metabolic Research, vol. 38, no. 10, pp. 678–682, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. G. I. Dran, G. C. Fernández, C. J. Rubel et al., “Protective role of nitric oxide in mice with Shiga toxin-induced hemolytic uremic syndrome,” Kidney International, vol. 62, no. 4, pp. 1338–1348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Shao, T. Miyata, K. Yamada et al., “Protective role of nitric oxide in a model of thrombotic microangiopathy in rats,” Journal of the American Society of Nephrology, vol. 12, no. 10, pp. 2088–2097, 2001. View at Google Scholar · View at Scopus
  36. S. Tsuji, A. Iharada, T. Kimata, T. Shimo, M. Hirabayashi, and K. Kaneko, “Production of nitric oxide is lower in Shiga toxin-stimulated neutrophils of infants compared to those of children or adults,” Tohoku Journal of Experimental Medicine, vol. 228, no. 3, pp. 247–252, 2012. View at Publisher · View at Google Scholar
  37. A. Wennmalm, G. Benthin, and A. Peterssen, “Dependence of the metabolism of nitric oxide (NO) in healthy human whole blood on the oxygenation of its red cell haemoglobin,” The British Journal of Pharmacology, vol. 106, no. 3, pp. 507–508, 1992. View at Google Scholar · View at Scopus
  38. C. D. Reiter, X. Wang, J. E. Tanus-Santos et al., “Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease,” Nature Medicine, vol. 8, no. 12, pp. 1383–1389, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Cosby, K. S. Partovi, J. H. Crawford et al., “Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation,” Nature Medicine, vol. 9, no. 12, pp. 1498–1505, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. R. Pawloski, D. T. Hess, and J. S. Stamler, “Impaired vasodilation by red blood cells in sickle cell disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 7, pp. 2531–2536, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Akinsheye and E. S. Klings, “Sickle cell anemia and vascular dysfunction: the nitric oxide connection,” Journal of Cellular Physiology, vol. 224, no. 3, pp. 620–625, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. H. Maley, G. F. Lasker, and P. J. Kadowitz, “Nitric oxide and disorders of the erythrocyte: emerging roles and therapeutic targets,” Cardiovascular and Hematological Disorders—Drug Targets, vol. 10, no. 4, pp. 284–291, 2010. View at Google Scholar · View at Scopus
  43. U. Dreißigacker, M. Suchy, N. Maassen, and D. Tsikas, “Human plasma concentrations of malondialdehyde (MDA) and the F2-isoprostane 15(S)-8-iso-PGF2α may be markedly compromised by hemolysis: evidence by GC-MS/MS and potential analytical and biological ramifications,” Clinical Biochemistry, vol. 43, no. 1-2, pp. 159–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. N. J. Parks, K. J. Krohn, C. A. Mathis et al., “Nitrogen-13-labeled nitrite and nitrate: distribution and metabolism after intratracheal administration,” Science, vol. 212, no. 4490, pp. 58–60, 1981. View at Google Scholar · View at Scopus
  45. D. Tsikas, K. Sutmöller, M. Maassen et al., “Even and carbon dioxide independent distribution of nitrite between plasma and erythrocytes of healthy humans at rest,” Nitric Oxide, vol. 31, pp. 31–37, 2013. View at Publisher · View at Google Scholar
  46. R. Keimer, F. K. Stutzer, D. Tsikas, R. Troost, F. Gutzki, and J. C. Frölich, “Lack of oxidative stress during sustained therapy with isosorbide dinitrate and pentaerythrityl tetranitrate in healthy humans: a randomized, double-blind crossover study,” Journal of Cardiovascular Pharmacology, vol. 41, no. 2, pp. 284–292, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Tsikas and M. W. Duncan, “Mass spectrometry and 3-nitrotyrosine: strategies, controversies, and our current perspective,” Mass Spectrometry Reviews, 2013. View at Publisher · View at Google Scholar
  48. D. Tsikas, A. Böhmer, H. Großkopf et al., “Clinical-chemistry laboratory relevant hemolysis is unlikely to compromise human plasma concentration of free asymmetric dimethylarginine (ADMA),” Clinical Biochemistry, vol. 45, no. 16-17, pp. 1536–1538, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Wolf, J. M. Lorenzen, S. Stein et al., “Urinary asymmetric dimethylarginine (ADMA) is a predictor of mortality risk in patients with coronary artery disease,” International Journal of Cardiology, vol. 156, no. 3, pp. 289–294, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Giustarini, A. Milzani, I. Dalle-Donne, D. Tsikas, and R. Rossi, “N-Acetylcysteine ethyl ester (NACET): a novel lipophilic cell-permeable cysteine derivative with an unusual pharmacokinetic feature and remarkable antioxidant potential,” Biochemical Pharmacology, vol. 84, no. 11, pp. 1522–1533, 2012. View at Publisher · View at Google Scholar