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Disease Markers
Volume 2014, Article ID 485917, 8 pages
http://dx.doi.org/10.1155/2014/485917
Research Article

Levels of Human Erythrocyte Membrane-Bound and Cytosolic Glycohydrolases Are Associated with Oxidative Stress in Erectile Dysfunction Patients

1Department of Biomedical, Surgical and Dental Sciences, University of Milan, School of Medicine, Via Saldini 50, 20133 Milan, Italy
2Department of Health’s Sciences, University of Milan, Milan, Italy
3U.O. Andrology, San Paolo University Hospital, Milan, Italy
4IRCCS Policlinico San Donato, San Donato Milanese, Italy

Received 15 May 2014; Revised 13 July 2014; Accepted 14 July 2014; Published 5 August 2014

Academic Editor: Stamatios Theocharis

Copyright © 2014 L. Massaccesi 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. NIH Consensus Conference, “Impotence. NIH Consensus Development Panel on Impotence,” The Journal of the American Medical Association, vol. 270, no. 1, pp. 83–90, 1993. View at Google Scholar
  2. M. E. Sullivan, S. R. Keoghane, and M. A. W. Miller, “Vascular risk factors and erectile dysfunction,” BJU International, vol. 87, no. 9, pp. 838–845, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. K.-E. Andersson and G. Wagner, “Physiology of penile erection,” Physiological Reviews, vol. 75, pp. 191–236, 1995. View at Google Scholar · View at Scopus
  4. L. de Young, D. Yu, R. M. Bateman, and G. B. Brock, “Oxidative stress and antioxidant therapy: their impact in diabetes-associated erectile dysfunction,” Journal of Andrology, vol. 25, no. 5, pp. 830–836, 2004. View at Google Scholar · View at Scopus
  5. T. J. Bivalacqua, M. F. Usta, H. C. Champion, P. J. Kadowitz, and W. J. G. Hellstrom, “Endothelial dysfunction in erectile dysfunction: role of the endothelium in erectile physiology and disease,” Journal of Andrology, vol. 24, no. 6, pp. S17–S37, 2003. View at Google Scholar · View at Scopus
  6. G. Goi, R. Cazzola, C. Tringali et al., “Erythrocyte membrane alterations during ageing affect β-D-glucuronidase and neutral sialidase in elderly healthy subjects,” Experimental Gerontology, vol. 40, no. 3, pp. 219–225, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Lombardo, L. Caimi, S. Marchesini, G. C. Goi, and G. Tettamanti, “Enzymes of lysosomal origin in human plasma and serum: assay conditions and parameters influencing the assay,” Clinica Chimica Acta, vol. 108, no. 3, pp. 337–346, 1980. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Willemsen, R. Brunken, C. W. J. Sorber et al., “A quantitative immunoelectronmicroscopic study on soluble, membrane-associated and membrane-bound lysosomal enzymes in human intestinal epithelial cells,” Histochemical Journal, vol. 23, no. 10, pp. 467–473, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Goi, C. Bairati, L. Massaccesi, A. Lovagnini, A. Lombardo, and G. Tettamanti, “Membrane anchoring and surface distribution of glycohydrolases of human erythrocyte membranes,” FEBS Letters, vol. 473, no. 1, pp. 89–94, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Massaccesi, A. Lombardo, B. Venerando, G. Tettamanti, and G. Goi, “Isoenzyme pattern and partial characterization of hexosaminidases in the membrane and cytosol of human erythrocytes,” Clinical Biochemistry, vol. 40, no. 7, pp. 467–477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Goi, C. Bairati, G. Segalini et al., “Alterations in the activity of several glycohydrolases in red blood cell membrane from type 2 diabetes mellitus patients,” Metabolism: Clinical and Experimental, vol. 48, no. 7, pp. 817–821, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. G. J. C. G. M. Bosman, F. E. Visser, A. J. M. De man, I. G. P. Bartholomeus, and W. J. Grip, “Erythrocyte membrane changes of individuals with Down's syndrome in various stages of Alzheimer-type dementia,” Neurobiology of Aging, vol. 14, no. 3, pp. 223–228, 1993. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Massaccesi, M. M. Corsi, C. J. Baquero-Herrera et al., “Erythrocyte glycohydrolases in subjects with trisomy 21: could Down's syndrome be a model of accelerated ageing?” Mechanisms of Ageing and Development, vol. 127, no. 4, pp. 324–331, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. M. M. Corsi, L. Massaccesi, G. Dogliotti et al., “O-β-N-acetyl-D-glucosaminidase in erythrocytes of Italian air force acrobatic pilots,” Clinical Chemistry and Laboratory Medicine, vol. 48, no. 2, pp. 213–216, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. D. L. Dong and G. W. Hart, “Purification and characterization of an O-GlcNAc selective N-acetyl-β-D- glucosaminidase from rat spleen cytosol,” The Journal of Biological Chemistry, vol. 269, no. 30, pp. 19321–19330, 1994. View at Google Scholar · View at Scopus
  16. Y. Gao, L. Wells, F. I. Comer, G. J. Parker, and G. W. Hart, “Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic β-N-acetylglucosaminidase from human brain,” The Journal of Biological Chemistry, vol. 276, no. 13, pp. 9838–9845, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. F. I. Comer and G. W. Hart, “O-glycosylation of nuclear and cytosolic proteins. Dynamic interplay between O-GlcNAc and O-phosphate,” Journal of Biological Chemistry, vol. 275, no. 38, pp. 29179–29182, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. A. L. Burnett, C. J. Lowenstein, D. S. Bredt, T. S. K. Chang, and S. H. Snyder, “Nitric oxide: a physiologic mediator of penile erection,” Science, vol. 257, no. 5068, pp. 401–403, 1992. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Kleinbongard, R. Schulz, T. Rassaf et al., “Red blood cells express a functional endothelial nitric oxide synthase,” Blood, vol. 107, no. 7, pp. 2943–2951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Misiti, C. Carelli-Alinovi, B. Sampaolese, and B. Giardina, “β-amyloid decreases detectable endothelial nitric oxide synthase in human erythrocytes: a role for membrane acetylcholinesterase,” Cell Biochemistry and Function, vol. 30, no. 6, pp. 474–479, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Özüyaman, M. Grau, M. Kelm, M. W. Merx, and P. Kleinbongard, “RBC NOS: regulatory mechanisms and therapeutic aspects,” Trends in Molecular Medicine, vol. 14, no. 7, pp. 314–322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Ulker, N. Yaras, O. Yalcin et al., “Shear stress activation of nitric oxide synthase and increased nitric oxide levels in human red blood cells,” Nitric Oxide, vol. 24, no. 4, pp. 184–191, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. Cortese-Krott, A. Rodriguez-Mateos, R. Sansone et al., “Human red blood cells at work: identification and visualization of erythrocytic eNOS activity in health and disease,” Blood, vol. 120, no. 20, pp. 4229–4237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Eligini, B. Porro, A. Lualdi et al., “Nitric oxide synthetic pathway in red blood cells is impaired in coronary artery disease,” PLoS ONE, vol. 8, no. 8, Article ID e66945, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Erba, M. C. Casiraghi, C. Martinez-Conesa, G. Goi, and L. Massaccesi, “Isoflavone supplementation reduces DNA oxidative damage and increases O-β-N-acetyl-d-glucosaminidase activity in healthy women,” Nutrition Research, vol. 32, no. 4, pp. 233–240, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Barassi, G. M. Colpi, G. Piediferro, G. Dogliotti, G. V. Melzi D'Eril, and M. M. Corsi, “Oxidative stress and antioxidant status in patients with erectile dysfunction,” Journal of Sexual Medicine, vol. 6, no. 10, pp. 2820–2825, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. R. C. Rosen, J. C. Cappelleri, M. D. Smith, J. Lipsky, and B. M. Peñ, “Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction,” International Journal of Impotence Research, vol. 11, no. 6, pp. 319–326, 1999. View at Google Scholar · View at Scopus
  28. T. L. Steck and J. A. Kant, “Preparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes,” Methods in Enzymology, vol. 31, pp. 172–180, 1974. View at Publisher · View at Google Scholar · View at Scopus
  29. N. E. Zachara, K. Vosseller, and G. W. Hart, “Detection and analysis of proteins modified by O-linked N-acetylglucosamine,” in Current Protocols in Molecular Biology, chapter 17, unit 17.6, John Wiley & Sons, 2011. View at Google Scholar
  30. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the Folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  31. R. Cazzola, S. Russo-Volpe, G. Cervato, and B. Cestaro, “Biochemical assessments of oxidative stress, erythrocyte membrane fluidity and antioxidant status in professional soccer players and sedentary controls,” European Journal of Clinical Investigation, vol. 33, no. 10, pp. 924–930, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Trotti, M. Carratelli, M. Barbieri et al., “Oxidative stress and a thrombophilic condition alcoholics without severe liver disease,” Haematologica, vol. 86, no. 1, pp. 85–91, 2001. View at Google Scholar · View at Scopus
  33. G. Cervato, P. Viani, R. Cazzola, and B. Cestaro, “A fluorescence method for the determination of plasma susceptibility to lipid peroxidation,” Clinical Biochemistry, vol. 32, no. 3, pp. 171–177, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. K. M. Azadzoi, T. Golabek, Z. M. Radisavljevic, S. V. Yalla, and M. B. Siroky, “Oxidative stress and neurodegeneration in penile ischaemia,” BJU International, vol. 105, no. 3, pp. 404–410, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. R. B. Moreland, G. Hsieh, M. Nakane, and J. D. Brioni, “The biochemical and neurologic basis for the treatment of male erectile dysfunction,” Journal of Pharmacology and Experimental Therapeutics, vol. 296, no. 2, pp. 225–234, 2001. View at Google Scholar · View at Scopus
  36. R. W. A. Jones, R. W. Rees, S. Minhas, D. Ralph, R. A. Persad, and J. Y. Jeremy, “Oxygen free radicals and the penis,” Expert Opinion on Pharmacotherapy, vol. 3, no. 7, pp. 889–897, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. K. J. Hurt, B. Musicki, M. A. Palese et al., “Akt-dependent phosphorylation of endothelial nitric-oxide synthase mediates penile erection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 4061–4066, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Musicki, M. F. Kramer, R. E. Becker, and A. L. Burnett, “Inactivation of phosphorylated endothelial nitric oxide synthase (Ser-1177) by O-GlcNAc in diabetes-associated erectile dysfunction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 33, pp. 11870–11875, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. B. Laczy, B. G. Hill, K. Wang et al., “Protein O-GlcNAcylation: a new signaling paradigm for the cardiovascular system,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 296, no. 1, pp. H13–H28, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Goi, L. Massaccesi, C. J. B. Herrera et al., “Oxidative stress in elderly chronic renal failure patients: effects of renal replacement therapies on cell membrane fluidity,” Journal of Nephrology, vol. 22, no. 5, pp. 630–636, 2009. View at Google Scholar · View at Scopus
  41. N. E. Zachara and G. W. Hart, “O-GlcNAc a sensor of cellular state: the role of nucleocytoplasmic glycosylation in modulating cellular function in response to nutrition and stress,” Biochimica et Biophysica Acta, vol. 1673, no. 1-2, pp. 13–28, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. Q. Zhang, Z. M. Radisavljevic, M. B. Siroky, and K. M. Azadzoi, “Dietary antioxidants improve arteriogenic erectile dysfunction,” International Journal of Andrology, vol. 34, no. 3, pp. 225–235, 2011. View at Publisher · View at Google Scholar · View at Scopus