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Journal of Ophthalmology
Volume 2015 (2015), Article ID 405234, 6 pages
http://dx.doi.org/10.1155/2015/405234
Review Article

The Role of the Endothelin System in the Vascular Dysregulation Involved in Retinitis Pigmentosa

1Department of Surgical Sciences, Unit of Ophthalmology, Ospedale Maggiore, Bologna, Italy
2Department of Biomedical and Surgical Sciences, Section of Human Physiology, University of Ferrara, 44100 Ferrara, Italy
3Department of Biomedical and Surgical Sciences, Division of Ophthalmology, University of Ferrara, 44100 Ferrara, Italy

Received 23 August 2015; Accepted 18 October 2015

Academic Editor: Suphi Taneri

Copyright © 2015 Francesco Saverio Sorrentino 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. K. Konieczka, A. J. Flammer, M. Todorova, P. Meyer, and J. Flammer, “Retinitis pigmentosa and ocular blood flow,” EPMA Journal, vol. 3, no. 1, article 17, 2012. View at Publisher · View at Google Scholar
  2. J. E. Grunwald, A. M. Maguire, and J. Dupont, “Retinal hemodynamics in retinitis pigmentosa,” American Journal of Ophthalmology, vol. 122, no. 4, pp. 502–508, 1996. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Cellini, E. Strobbe, C. Gizzi, and E. C. Campos, “ET-1 plasma levels and ocular blood flow in retinitis pigmentosa,” Canadian Journal of Physiology and Pharmacology, vol. 88, no. 6, pp. 630–635, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Falsini, G. M. Anselmi, D. Marangoni et al., “Subfoveal choroidal blood flow and central retinal function in retinitis pigmentosa,” Investigative Ophthalmology & Visual Science, vol. 52, no. 2, pp. 1064–1069, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Wolf, H. Pöstgens, B. Bertram, K. Schulte, C. Teping, and M. Reim, “Hemodynamic findings of patients with retinitis pigmentosa,” Klinische Monatsblätter für Augenheilkunde, vol. 199, no. 5, pp. 325–329, 1991. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Cellini, L. Santiago, P. Versura, and R. Caramazza, “Plasma levels of endothelin-1 in retinitis pigmentosa,” Ophthalmologica, vol. 216, no. 4, pp. 265–268, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. E. M. Vingolo, S. Lupo, P. L. Grenga et al., “Endothelin-1 plasma concentrations in patients with retinitis pigmentosa,” Regulatory Peptides, vol. 160, no. 1–3, pp. 64–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Ohguro, Y. Mashima, and M. Nakazawa, “Low levels of plasma endothelin-1 in patients with retinitis pigmentosa,” Clinical Ophthalmology, vol. 4, no. 1, pp. 569–573, 2010. View at Google Scholar · View at Scopus
  9. H. Saner, H. Würbel, F. Mahler, J. Flammer, and P. Gasser, “Microvasculatory evaluation of vasospastic syndromes,” in Continuous Transcutaneous Monitoring, vol. 7 of Advances in Experimental Medicine and Biology, pp. 215–218, Springer, New York, NY, USA, 1987. View at Publisher · View at Google Scholar
  10. U. Guthauser, J. Flammer, and F. Mahler, “The relationship between digital and ocular vasospasm,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 226, no. 3, pp. 224–226, 1988. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Mahler, H. Saner, H. Würbel, and J. Flammer, “Local cooling test for clinical capillaroscopy in Raynaud's phenomenon, unstable angina, and vasospastic visual disorders,” Vasa, vol. 18, no. 3, pp. 201–204, 1989. View at Google Scholar · View at Scopus
  12. J. Flammer and M. Mozaffarieh, “Autoregulation, a balancing act between supply and demand,” Canadian Journal of Ophthalmology, vol. 43, no. 3, pp. 317–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Kavroulaki, K. Gugleta, A. Kochkorov, R. Katamay, J. Flammer, and S. Orgül, “Relation of body mass index and blood pressure to subjective and objective acral temperature,” Klinische Monatsblatter fur Augenheilkunde, vol. 226, no. 4, pp. 328–331, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Emre, S. Orgül, K. Gugleta, and J. Flammer, “Ocular blood flow alteration in glaucoma is related to systemic vascular dysregulation,” British Journal of Ophthalmology, vol. 88, no. 5, pp. 662–666, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Gugleta, C. Zawinka, I. Rickenbacher et al., “Analysis of retinal vasodilation after flicker light stimulation in relation to vasospastic propensity,” Investigative Ophthalmology and Visual Science, vol. 47, no. 9, pp. 4034–4041, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. C. P. Hamel, “Retinitis pigmentosa,” Orphanet Journal of Rare Diseases, vol. 1, article 40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. A. T. Fahim, S. P. Daiger, and R. G. Weleber, “Retinitis pigmentosa overview,” in GeneReviews, R. A. Pagon, M. P. Adam, H. H. Ardinger et al., Eds., University of Washington, Seattle, Wash, USA, 1993–2015. View at Google Scholar
  18. S. Ferrari, E. Di Iorio, V. Barbaro, D. Ponzin, F. S. Sorrentino, and F. Parmeggiani, “Retinitis pigmentosa: genes and disease mechanisms,” Current Genomics, vol. 12, no. 4, pp. 238–249, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Parmeggiani, “Clinics, epidemiology and genetics of retinitis pigmentosa,” Current Genomics, vol. 12, no. 4, pp. 236–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. S. P. Daiger, L. S. Sullivan, and S. J. Bowne, “Genes and mutations causing retinitis pigmentosa,” Clinical Genetics, vol. 84, no. 2, pp. 132–141, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Flammer, M. Pache, and T. Resink, “Vasospasm, its role in the pathogenesis of diseases with particular reference to the eye,” Progress in Retinal and Eye Research, vol. 20, no. 3, pp. 319–349, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Flammer, K. Konieczka, and A. J. Flammer, “The primary vascular dysregulation syndrome: implications for eye diseases,” EPMA Journal, vol. 4, no. 1, article 14, 2013. View at Publisher · View at Google Scholar
  23. V. A. Convertino, “Neurohumoral mechanisms associated with orthostasis: reaffirmation of the significant contribution of the heart rate response,” Frontiers in Physiology, vol. 5, article 236, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. I. O. Haefliger, P. Meyer, J. Flammer, and T. F. Lüscher, “The vascular endothelium as a regulator of the ocular circulation: a new concept in ophthalmology?” Survey of Ophthalmology, vol. 39, no. 2, pp. 123–132, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. I. O. Haefliger, J. Flammer, J.-L. Bény, and T. F. Lüscher, “Endothelium-dependent vasoactive modulation in the ophthalmic circulation,” Progress in Retinal and Eye Research, vol. 20, no. 2, pp. 209–225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Flammer and M. Mozaffarieh, “Autoregulation, a balancing act between supply and demand,” Canadian Journal of Ophthalmology, vol. 43, no. 3, pp. 317–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Neuhuber and F. Schrödl, “Autonomic control of the eye and the iris,” Autonomic Neuroscience: Basic and Clinical, vol. 165, no. 1, pp. 67–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. R. M. Kedzierski and M. Yanagisawa, “Endothelin system: the double-edged sword in health and disease,” Annual Review of Pharmacology and Toxicology, vol. 41, pp. 851–876, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. D. E. Clouthier, K. Hosoda, J. A. Richardson et al., “Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice,” Development, vol. 125, no. 5, pp. 813–824, 1998. View at Google Scholar · View at Scopus
  30. A. G. Baynash, K. Hosoda, A. Giaid et al., “Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons,” Cell, vol. 79, no. 7, pp. 1277–1285, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Hosoda, R. E. Hammer, J. A. Richardson et al., “Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice,” Cell, vol. 79, no. 7, pp. 1267–1276, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Bianchi, J. Adur, S. Takizawa, K. Saida, and V. H. Casco, “Endothelin system in intestinal villi: a possible role of endothelin-2/vasoactive intestinal contractor in the maintenance of intestinal architecture,” Biochemical and Biophysical Research Communications, vol. 417, no. 4, pp. 1113–1118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. A. N. Bramall, M. J. Szego, L. R. Pacione et al., “Endothelin-2-mediated protection of mutant photoreceptors in inherited photoreceptor degeneration,” PLoS ONE, vol. 8, no. 2, Article ID e58023, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Yanagisawa, H. Kurihara, S. Kimura et al., “A novel potent vasoconstrictor peptide produced by vascular endothelial cells,” Nature, vol. 332, no. 6163, pp. 411–415, 1988. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Masaki, S. Kimura, M. Yanagisawa, and K. Goto, “Molecular and cellular mechanism of endothelin regulation: implications for vascular function,” Circulation, vol. 84, no. 4, pp. 1457–1468, 1991. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Vane, R. Botting, and T. Masaki, “Endothelin,” Journal of Cardiovascular Pharmacology, vol. 13, supplement 5, pp. S1–S23, 1989. View at Google Scholar
  37. M. S. Simonson and M. J. Dunn, “Cellular signaling by peptides of the endothelin gene family,” The FASEB Journal, vol. 4, no. 12, pp. 2989–3000, 1990. View at Google Scholar · View at Scopus
  38. T. Miyauchi, M. Yanagisawa, T. Tomizawa et al., “Increased plasma concentrations of endothelin-1 and big endothelin-1 in acute myocardial infarction,” The Lancet, vol. 334, no. 8653, pp. 53–54, 1989. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Takahashi, M. A. Ghatei, H.-C. Lam, D. J. O'Halloran, and S. R. Bloom, “Elevated plasma endothelin in patients with diabetes mellitus,” Diabetologia, vol. 33, no. 5, pp. 306–310, 1990. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Kohno, K. Yasunari, K.-I. Murakawa et al., “Plasma immunoreactive endothelin in essential hypertension,” The American Journal of Medicine, vol. 88, no. 6, pp. 614–618, 1990. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Lerman, B. S. Edwards, J. W. Hallett, D. M. Heublein, S. M. Sandberg, and J. C. Burnett Jr., “Circulating and tissue endothelin immunoreactivity in advanced atherosclerosis,” The New England Journal of Medicine, vol. 325, no. 14, pp. 997–1001, 1991. View at Publisher · View at Google Scholar · View at Scopus
  42. M. W. MacCumber, H. D. Jampel, and S. H. Snyder, “Ocular effects of the endothelins: abundant peptides in the eye,” Archives of Ophthalmology, vol. 109, no. 5, pp. 705–709, 1991. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Granstam, L. Wang, and A. Bill, “Ocular effects of endothelin-1 in the cat,” Current Eye Research, vol. 11, no. 4, pp. 325–332, 1992. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Chollet, F. Malecaze, L. Gouzi, J. L. Arne, and J. Plouet, “Endothelin 1 is a growth factor for corneal endothelium,” Experimental Eye Research, vol. 57, no. 5, pp. 595–600, 1993. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Ripodas, J. A. de Juan, M. Roldán-Pallarés et al., “Localisation of endothelin-1 mRNA expression and immunoreactivity in the retina and optic nerve from human and porcine eye. Evidence for endothelin-1 expression in astrocytes,” Brain Research, vol. 912, no. 2, pp. 137–143, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Narayan, A. M. Brun, and T. Yorio, “Endothelin-1 distribution and basolateral secretion in the retinal pigment epithelium,” Experimental Eye Research, vol. 79, no. 1, pp. 11–19, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. H. J. Kaiser, J. Flammer, M. Wenk, and T. Luscher, “Endothelin-1 plasma levels in normal-tension glaucoma. Abnormal response to postural changes,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 233, no. 8, pp. 484–488, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Oku, T. Kida, T. Sugiyama, J. Hamada, B. Sato, and T. Ikeda, “Possible involvement of endothelin-1 and nitric oxide in the pathogenesis of proliferative diabetic retinopathy,” Retina, vol. 21, no. 6, pp. 647–651, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Roldán-Pallarés, R. Rollín, A. Mediero et al., “Immunoreactive ET-1 in the vitreous humor and epiretinal membranes of patients with proliferative vitreoretinopathy,” Molecular Vision, vol. 11, pp. 461–471, 2005. View at Google Scholar · View at Scopus
  50. I. Ohguro, H. Ohguro, H. Ohkuro, and M. Nakazawa, “Study of contribution of low level of plasma endothelin-1 concentration to pathogenesis of glaucomatous optic neuropathy,” Hirosaki Medical Journal, vol. 57, no. 2–4, pp. 59–64, 2006. View at Google Scholar · View at Scopus
  51. A. Finzi, M. Cellini, E. Strobbe, and E. C. Campos, “ET-1 plasma levels, choroidal thickness and multifocal electroretinogram in retinitis pigmentosa,” Life Sciences, vol. 118, no. 2, pp. 386–390, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. M. J. Grimshaw, J. L. Wilson, and F. R. Balkwill, “Endothelin-2 is a macrophage chemoattractant: implications for macrophage distribution in tumors,” European Journal of Immunology, vol. 32, no. 9, pp. 2393–2400, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Rattner and J. Nathans, “The genomic response to retinal disease and injury: evidence for endothelin signaling from photoreceptors to glia,” Journal of Neuroscience, vol. 25, no. 18, pp. 4540–4549, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. L. R. Pacione, M. J. Szego, S. Ikeda, P. M. Nishina, and R. R. McInnes, “Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations,” Annual Review of Neuroscience, vol. 26, pp. 657–700, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Bringmann and A. Reichenbach, “Role of Muller cells in retinal degenerations,” Frontiers in Bioscience, vol. 6, pp. e72–92, 2001. View at Google Scholar · View at Scopus
  56. M. García and E. Vecino, “Role of Müller glia in neuroprotection and regeneration in the retina,” Histology and Histopathology, vol. 18, no. 4, pp. 1205–1218, 2003. View at Google Scholar · View at Scopus
  57. G. P. Lewis and S. K. Fisher, “Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression,” International Review of Cytology, vol. 230, pp. 263–290, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Ulrich, W.-D. Ulrich, K. Vehlow, and S. Vehlow, “Hemodynamic aspects of retinitis pigmentosa,” Fortschritte der Ophthalmologie, vol. 88, no. 6, pp. 642–647, 1991. View at Google Scholar · View at Scopus
  59. M. Cellini, R. Lodi, G. L. Possati, M. Sbrocca, D. Pelle, and N. Giubilei, “Color Doppler ultrasonography in retinitis pigmentosa: preliminary study,” Journal Français d'Ophtalmologie, vol. 20, no. 9, pp. 659–663, 1997. View at Google Scholar
  60. E. Strobbe, M. Cellini, M. Fresina, and E. C. Campos, “ET-1 plasma levels, aqueous flare, and choroidal thickness in patients with retinitis pigmentosa,” Journal of Ophthalmology, vol. 2015, Article ID 292615, 6 pages, 2015. View at Publisher · View at Google Scholar
  61. K. Polak, V. Petternel, A. Luksch et al., “Effect of endothelin and BQ123 on ocular blood flow parameters in healthy subjects,” Investigative Ophthalmology & Visual Science, vol. 42, no. 12, pp. 2949–2956, 2001. View at Google Scholar · View at Scopus
  62. K. Polak, A. Luksch, B. Frank, K. Jandrasits, E. Polska, and L. Schmetterer, “Regulation of human retinal blood flow by endothelin-1,” Experimental Eye Research, vol. 76, no. 5, pp. 633–640, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. D. T. Hartong, E. L. Berson, and T. P. Dryja, “Retinitis pigmentosa,” The Lancet, vol. 368, no. 9549, pp. 1795–1809, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. J. L. Stone, W. E. Barlow, M. S. Humayun, E. De Juan Jr., and A. H. Milam, “Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa,” Archives of Ophthalmology, vol. 110, no. 11, pp. 1634–1639, 1992. View at Publisher · View at Google Scholar · View at Scopus
  65. C. J. Pournaras, C. E. Riva, M. Tsacopoulos, and K. Strommer, “Diffusion of O2 in the retina of anesthetized miniature pigs in normoxia and hyperoxia,” Experimental Eye Research, vol. 49, no. 3, pp. 347–360, 1989. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Dallinger, G. T. Dorner, R. Wenzel et al., “Endothelin-1 contributes to hyperoxia-induced vasoconstriction in the human retina,” Investigative Ophthalmology and Visual Science, vol. 41, no. 3, pp. 864–869, 2000. View at Google Scholar · View at Scopus
  67. M. Shihara, Y. Hirooka, N. Hori et al., “Endothelin-1 increases the neuronal activity and augments the responses to glutamate in the NTS,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 275, no. 2, pp. R658–R665, 1998. View at Google Scholar · View at Scopus
  68. T. Kobayashi, H. Oku, M. Fukuhara et al., “Endothelin-1 enhances glutamate-induced retinal cell death, possibly through ETA receptors,” Investigative Ophthalmology & Visual Science, vol. 46, no. 12, pp. 4684–4690, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. R. R. Krishnamoorthy, V. R. Rao, R. Dauphin, G. Prasanna, C. Johnson, and T. Yorio, “Role of the ETB receptor in retinal ganglion cell death in glaucoma,” Canadian Journal of Physiology and Pharmacology, vol. 86, no. 6, pp. 380–393, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. V. Marigo, “Programmed cell death in retinal degeneration: targeting apoptosis in photoreceptors as potential therapy for retinal degeneration,” Cell Cycle, vol. 6, no. 6, pp. 652–655, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. Z.-Y. Li, D. E. Possin, and A. H. Milam, “Histopathology of bone spicule pigmentation in retinitis pigmentosa,” Ophthalmology, vol. 102, no. 5, pp. 805–816, 1995. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Komeima, B. S. Rogers, and P. A. Campochiaro, “Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa,” Journal of Cellular Physiology, vol. 213, no. 3, pp. 809–815, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Martínez-Fernández de la Cámara, D. Salom, M. D. Sequedo et al., “Altered antioxidant-oxidant status in the aqueous humor and peripheral blood of patients with retinitis pigmentosa,” PLoS ONE, vol. 8, no. 9, Article ID e74223, 2013. View at Publisher · View at Google Scholar · View at Scopus