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International Journal of Hypertension
Volume 2014, Article ID 859793, 12 pages
http://dx.doi.org/10.1155/2014/859793
Research Article

Time-Related Alteration in Flow- (Shear Stress-) Mediated Remodeling in Resistance Arteries from Spontaneously Hypertensive Rats

1CNRS UMR 6214, INSERM U1083, Université d’Angers, UFR de Médecine, rue Haute de Reculée, 49045 Angers, France
2University Hospital Center (CHU) of Angers, rue Larrey, 49000 Angers, France

Received 12 December 2013; Revised 31 March 2014; Accepted 31 March 2014; Published 8 May 2014

Academic Editor: Tomohiro Katsuya

Copyright © 2014 Odile Dumont 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. M. J. Mulvany, “Small artery remodeling in hypertension,” Current Hypertension Reports, vol. 4, no. 1, pp. 49–55, 2002. View at Google Scholar · View at Scopus
  2. E. L. Schiffrin, “Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment,” The American Journal of Hypertension, vol. 17, no. 12, pp. 1192–1200, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. R. L. Prewitt, D. C. Rice, and A. D. Dobrian, “Adaptation of resistance arteries to increases in pressure,” Microcirculation, vol. 9, no. 4, pp. 295–304, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Rizzoni, E. Porteri, G. E. M. Boari et al., “Prognostic significance of small-artery structure in hypertension,” Circulation, vol. 108, no. 18, pp. 2230–2235, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. H. L. Matlung, E. N. T. P. Bakker, and E. VanBavel, “Shear stress, reactive oxygen species, and arterial structure and function,” Antioxidants and Redox Signaling, vol. 11, no. 7, pp. 1699–1709, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Vessières, M. L. Freidja, L. Loufrani, C. Fassot, and D. Henrion, “Flow (shear stress)-mediated remodeling of resistance arteries in diabetes,” Vascular Pharmacology, vol. 57, no. 5-6, pp. 173–178, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Kojda and R. Hambrecht, “Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy?” Cardiovascular Research, vol. 67, no. 2, pp. 187–197, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. N. I. Gokina, M. Mandalà, and G. Osol, “Induction of localized differences in rat uterine radial artery behavior and structure during gestation,” The American Journal of Obstetrics and Gynecology, vol. 189, no. 5, pp. 1489–1493, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Gorny, L. Loufrani, N. Kubis, B. I. Lévy, and D. Henrion, “Chronic hydralazine improves flow (shear stress)-induced endothelium-dependent dilation in mouse mesenteric resistance arteries in vitro,” Microvascular Research, vol. 64, no. 1, pp. 127–134, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Carmeliet, “Mechanisms of angiogenesis and arteriogenesis,” Nature Medicine, vol. 6, no. 4, pp. 389–395, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. O. Dumont, F. Pinaud, A.-L. Guihot, C. Baufreton, L. Loufrani, and D. Henrion, “Alteration in flow (shear stress)-induced remodelling in rat resistance arteries with aging: improvement by a treatment with hydralazine,” Cardiovascular Research, vol. 77, no. 3, pp. 600–608, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Pourageaud and J. G. R. De Mey, “Structural properties of rat mesenteric small arteries after 4-wk exposure to elevated or reduced blood flow,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 273, no. 4, pp. H1699–H1706, 1997. View at Google Scholar · View at Scopus
  13. O. Dumont, L. Loufrani, and D. Henrion, “Key role of the NO-pathway and matrix metalloprotease-9 in high blood flow-induced remodeling of rat resistance arteries,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 2, pp. 317–324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Tarhouni, A. L. Guihot, M. L. Freidja et al., “Key role of estrogens and endothelial estrogen receptor alpha in blood flow-mediated remodeling of resistance arteries,” Arterioscler Thromb Vasc Biol, vol. 33, no. 3, pp. 605–611, 2013. View at Google Scholar
  15. X. Zhou, H. G. Bohlen, S. J. Miller, and J. L. Unthank, “NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 295, no. 3, pp. H1008–H1016, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Y. Qiu, D. Henrion, J. Benessiano, C. Heymes, B. Tournier, and B. I. Levy, “Decreased flow-induced dilation and increased production of cGMP in spontaneously hypertensive rats,” Hypertension, vol. 32, no. 6, pp. 1098–1103, 1998. View at Google Scholar · View at Scopus
  17. M. Kelm, “The L-arginine-nitric oxide pathway in hypertension,” Current Hypertension Reports, vol. 5, no. 1, pp. 80–86, 2003. View at Google Scholar · View at Scopus
  18. K. Matrougui, Y. E. G. Eskildsen-Helmond, A. Fiebeler et al., “Angiotensin II stimulates extracellular signal-regulated kinase activity in intact pressurized rat mesenteric resistance arteries,” Hypertension, vol. 36, no. 4, pp. 617–621, 2000. View at Google Scholar · View at Scopus
  19. M. Iglarz, K. Matrougui, B. I. Lévy, and D. Henrion, “Chronic blockade of endothelin ET(A) receptors improves flow dependent dilation in resistance arteries of hypertensive rats,” Cardiovascular Research, vol. 39, no. 3, pp. 657–664, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Matrougui, B. I. Levy, and D. Henrion, “Tissue angiotensin II and endothelin-1 modulate differently the response to flow in mesenteric resistance arteries of normotensive and spontaneously hypertensive rats,” British Journal of Pharmacology, vol. 130, no. 3, pp. 521–526, 2000. View at Google Scholar · View at Scopus
  21. J. L. Tuttle, B. M. Sanders, H. M. Burkhart et al., “Impaired collateral artery development in spontaneously hypertensive rats,” Microcirculation, vol. 9, no. 5, pp. 343–351, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. L. Freidja, E. Vessieres, N. Clere et al., “Heme oxygenase-1 induction restores high-blood-flow-dependent remodeling and endothelial function in mesenteric arteries of old rats,” Journal of Hypertension, vol. 29, no. 1, pp. 102–112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Castier, R. P. Brandes, G. Leseche, A. Tedgui, and S. Lehoux, “p47phox-dependent NADPH oxidase regulates flow-induced vascular remodeling,” Circulation Research, vol. 97, no. 6, pp. 533–540, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Belin De Chantemèle, E. Vessiéres, O. Dumont et al., “Reactive oxygen species are necessary for high flow (shear Stress)-induced diameter enlargement of rat resistance arteries,” Microcirculation, vol. 16, no. 5, pp. 391–402, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. A. Payne, J. F. Reckelhoff, and R. A. Khalil, “Role of oxidative stress in age-related reduction of NO-cGMP-mediated vascular relaxation in SHR,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 285, no. 3, pp. R542–R551, 2003. View at Google Scholar · View at Scopus
  26. C. A. Hamilton, M. J. Brosnan, M. McIntyre, D. Graham, and A. F. Dominiczak, “Superoxide excess in hypertension and aging a common cause of endothelial dysfunction,” Hypertension, vol. 37, no. 2, pp. 529–534, 2001. View at Google Scholar · View at Scopus
  27. M. Cousin, M.-A. Custaud, C. Baron-Menguy et al., “Role of angiotensin II in the remodeling induced by a chronic increase in flow in rat mesenteric resistance arteries,” Hypertension, vol. 55, no. 1, pp. 109–115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. D. A. Tulis, J. L. Unthank, and R. L. Prewitt, “Flow-induced arterial remodeling in rat mesenteric vasculature,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 274, no. 3, pp. H874–H882, 1998. View at Google Scholar · View at Scopus
  29. A. B. Driss, C. Devaux, D. Henrion et al., “Hemodynamic stresses induce endothelial dysfunction and remodeling of pulmonary artery in experimental compensated heart failure,” Circulation, vol. 101, no. 23, pp. 2764–2770, 2000. View at Google Scholar · View at Scopus
  30. M. Bolla, K. Matrougui, L. Loufrani et al., “p38 mitogen-activated protein kinase activation is required for thromboxane-induced contraction in perfused and pressurized rat mesenteric resistance arteries,” Journal of Vascular Research, vol. 39, no. 4, pp. 353–360, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Bouvet, E. B. De Chantemèle, A.-L. Guihot et al., “Flow-induced remodeling in resistance arteries from obese Zucker rats is associated with endothelial dysfunction,” Hypertension, vol. 50, no. 1, pp. 248–254, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Vessieres, E. J. Belin de Chantemele, B. Toutain et al., “Cyclooxygenase-2 inhibition restored endothelium-mediated relaxation in old obese zucker rat mesenteric arteries,” Frontiers in Physiology, vol. 1, article 145, 2010. View at Google Scholar
  33. D. Henrion, I. Laher, and J. A. Bevan, “Intraluminal flow increases vascular tone and 45Ca2+ influx in the rabbit facial vein,” Circulation Research, vol. 71, no. 2, pp. 339–345, 1992. View at Google Scholar · View at Scopus
  34. L. Loufrani, C. Dubroca, D. You et al., “Absence of dystrophin in mice reduces no-dependent vascular function and vascular density: total recovery after a treatment with the aminoglycoside gentamicin,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 4, pp. 671–676, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Seiler, M. Stoller, B. Pitt, and P. Meier, “The human coronary collateral circulation: development and clinical importance,” European Heart Journal, vol. 34, no. 34, pp. 2674–2682, 2013. View at Google Scholar
  36. I. Nakae, M. Fujita, K. Miwa et al., “Age-dependent impairment of coronary collateral development in humans,” Heart and Vessels, vol. 15, no. 4, pp. 176–180, 2000. View at Google Scholar · View at Scopus
  37. M. S. Ruiter, J. M. Van Golde, N. C. Schaper, C. D. Stehouwer, and M. S. Huijberts, “Diabetes impairs arteriogenesis in the peripheral circulation: review of molecular mechanisms,” Clinical Science, vol. 119, no. 6, pp. 225–238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. J. Miller, L. E. Norton, M. P. Murphy, M. C. Dalsing, and J. L. Unthank, “The role of the renin-angiotensin system and oxidative stress in spontaneously hypertensive rat mesenteric collateral growth impairment,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 292, no. 5, pp. H2523–H2531, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. M. L. Freidja, B. Toutain, A. Caillon et al., “Heme oxygenase 1 is differentially involved in blood flow-dependent arterial remodeling: role of inflammation, oxidative stress, and nitric oxide,” Hypertension, vol. 58, no. 2, pp. 225–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. R. D. Rudic, E. G. Shesely, N. Maeda, O. Smithies, S. S. Segal, and W. C. Sessa, “Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling,” Journal of Clinical Investigation, vol. 101, no. 4, pp. 731–736, 1998. View at Google Scholar · View at Scopus
  41. M. J. Mulvany and W. Halpern, “Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats,” Circulation Research, vol. 41, no. 1, pp. 19–26, 1977. View at Google Scholar · View at Scopus
  42. A. B. García-Redondo, A. M. Briones, M. S. Avendaño, R. Hernanz, M. J. Alonso, and M. Salaices, “Losartan and tempol treatments normalize the increased response to hydrogen peroxide in resistance arteries from hypertensive rats,” Journal of Hypertension, vol. 27, no. 9, pp. 1814–1822, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. M. A. Rodríguez-Martínez, E. C. García-Cohen, A. B. Baena, R. González, M. Salaíces, and J. Marín, “Contractile responses elicited by hydrogen peroxide in aorta from normotensive and hypertensive rats. Endothelial modulation and mechanism involved,” British Journal of Pharmacology, vol. 125, no. 6, pp. 1329–1335, 1998. View at Google Scholar · View at Scopus
  44. Y. Liu, H. Zhao, H. Li, B. Kalyanaraman, A. C. Nicolosi, and D. D. Gutterman, “Mitochondrial sources of H2O2 generation play a key role in flow-mediated dilation in human coronary resistance arteries,” Circulation Research, vol. 93, no. 6, pp. 573–580, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Altin, M. Kilickap, E. Tutar et al., “The relationship of chronic angiotensin converting enzyme inhibitor use and coronary collateral vessel development,” International Heart Journal, vol. 48, no. 4, pp. 435–442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Turhan, A. S. Yasar, A. R. Erbay, E. Yetkin, H. Sasmaz, and I. Sabah, “Impaired coronary collateral vessel development in patients with metabolic syndrome,” Coronary Artery Disease, vol. 16, no. 5, pp. 281–285, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Mouquet, F. Cuilleret, S. Susen et al., “Metabolic syndrome and collateral vessel formation in patients with documented occluded coronary arteries: association with hyperglycaemia, insulin-resistance, adiponectin and plasminogen activator inhibitor-1,” European Heart Journal, vol. 30, no. 7, pp. 840–849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. G. Kilian, A. Keech, M. R. Adams et al., “Coronary collateralization: determinants of adequate distal vessel filling after arterial occlusion,” Coronary Artery Disease, vol. 13, no. 3, pp. 155–159, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Abaci, A. Oguzhan, S. Kahraman et al., “Effect of diabetes mellitus on formation of coronary collateral vessels,” Circulation, vol. 99, no. 17, pp. 2239–2242, 1999. View at Google Scholar · View at Scopus
  50. E. Vessieres, E. J. Belin de Chantemele, B. Toutain et al., “COX-2-derived prostanoids and oxidative stress additionally reduce endothelium-mediated relaxation in old type 2 diabetic rats,” PLoS ONE, vol. 8, no. 7, Article ID e68217, 2013. View at Google Scholar
  51. E. N. T. P. Bakker, C. L. Buus, J. A. E. Spaan et al., “Small artery remodeling depends on tissue-type transglutaminase,” Circulation Research, vol. 96, no. 1, pp. 119–126, 2005. View at Google Scholar
  52. E. N. T. P. Bakker, H. L. Matlung, P. Bonta, C. J. De Vries, N. Van Rooijen, and E. Vanbavel, “Blood flow-dependent arterial remodelling is facilitated by inflammation but directed by vascular tone,” Cardiovascular Research, vol. 78, no. 2, pp. 341–348, 2008. View at Google Scholar
  53. J. Van Den Akker, M. J. C. Schoorl, E. N. T. P. Bakker, and E. Vanbavel, “Small artery remodeling: current concepts and questions,” Journal of Vascular Research, vol. 47, no. 3, pp. 183–202, 2010. View at Publisher · View at Google Scholar · View at Scopus