Long-term effects of losartan on structure and function of the thoracic aorta in a mouse model of Marfan syndrome

British Journal of Pharmacology

Volumn 158, Issue 6, 2009, Pages 1503-1512

  Yang, H H Clarice ^a   Kim, Jong Moo ^a   Chum, Elliott ^a   Van Breemen, Cornelis ^a   Chung, Ada W Y ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Aortic contractile function; Endothelial dependent relaxation; Long term treatment; Losartan; Marfan syndrome; Thoracic aortic aneurysm

Indexed keywords

ACETYLCHOLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GELATINASE A; GELATINASE B; LOSARTAN; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENZYME INHIBITION; HISTOPATHOLOGY; MARFAN SYNDROME; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE; THORACIC AORTA ANEURYSM; VASOMOTOR REFLEX;

AGE FACTORS; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; AORTA, THORACIC; AORTIC ANEURYSM, THORACIC; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; LOSARTAN; MARFAN SYNDROME; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE; TIME FACTORS;

EID: 70350538712     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2009.00443.x     Document Type: Article

References (46)

1. Baumgartner D, Baumgartner C, Schermer E, Engl G, Schweigmann U, Matyas G et al. (2006). Different patterns of aortic wall elasticity in patients with Marfan syndrome: a noninvasive follow-up study. J Thorac Cardiovasc Surg 132 : 811 819.
2. Brooke BS, Habashi JP, Judge DP, Patel N, Loeys B, Dietz HC, 3rd. (2008). Angiotensin II blockade and aortic-root dilation in Marfan's syndrome. N Engl J Med 358 : 2787 2795.
3. Chew DK, Conte MS, Khalil RA (2004). Matrix metalloproteinase-specific inhibition of Ca2+ entry mechanisms of vascular contraction. J Vasc Surg 40 : 1001 1010.
4. Chung AW, Au Yeung K, Cortes SF, Sandor GG, Judge DP, Dietz HC et al. (2007a). Endothelial dysfunction and compromised eNOS/Akt signaling in the thoracic aorta during the progression of Marfan syndrome. Br J Pharmacol 150 : 1075 1083.
5. Chung AW, Au Yeung K, Sandor GG, Judge DP, Dietz HC, van Breemen C (2007b). Loss of elastic fiber integrity and reduction of vascular smooth muscle contraction resulting from the upregulated activities of matrix metalloproteinase-2 and -9 in the thoracic aortic aneurysm in Marfan syndrome. Circ Res 101 : 512 522.
6. Chung AW, Yang HH, van Breemen C (2007c). Imbalanced synthesis of cyclooxygenase-derived thromboxane A(2) and prostacyclin compromises vasomotor function of the thoracic aorta in Marfan syndrome. Br J Pharmacol 152 : 305 312.
7. Chung AW, Yang HHC, Au Yeung K, van Breemen C (2008a). Mechanical and pharmacological approaches to investigate the pathogenesis of Marfan syndrome in the abdominal aorta. J Vasc Res 45 : 314 322.
8. Chung AW, Yang HHC, Radomski MW, van Breemen C (2008b). Long-term doxycycline is more effective than atenolol to prevent thoracic aortic aneurysm in Marfan syndrome through the inhibition of matrix metalloproteinase-2 and -9. Circ Res 102 : e73 e85.
9. Clark-Greuel JN, Connolly JM, Sorichillo E, Narula NR, Rapoport HS, Mohler ER, 3rd. et al. (2007). Transforming growth factor-beta1 mechanisms in aortic valve calcification: increased alkaline phosphatase and related events. Ann Thorac Surg 83 : 946 953.
10. Cohn RD, van Erp C, Habashi JP, Soleimani AA, Klein EC, Lisi MT et al. (2007). Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med 13 : 204 210.
11. D'Arrigo C, Burl S, Withers AP, Dobson H, Black C, Boxer M (1998). TGF-beta1 binding protein-like modules of fibrillin-1 and -2 mediate integrin-dependent cell adhesion. Connect Tissue Res 37 : 29 51.
12. Davis EC (1993). Smooth muscle cell to elastic lamina connections in developing mouse aorta. Role in aortic medial organization. Lab Invest 68 : 89 99.
13. Davis EC (1994). Immunolocalization of microfibril and microfibril-associated proteins in the subendothelial matrix of the developing mouse aorta. J Cell Sci 107 : 727 736.
14. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM et al. (1991). Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 352 : 337 339.
15. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999). Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399 : 601 605.
16. Han YP, Tuan TL, Hughes M, Wu H, Garner WL (2001). Transforming growth factor-beta- and tumor necrosis factor-alpha-mediated induction and proteolytic activation of MMP-9 in human skin. J Biol Chem 276 : 22341 22350.
17. Gersony DR, McClaughlin MA, Jin Z, Gersony WM (2007). The effect of beta-blocker therapy on clinical outcome in patients with Marfan's syndrome: a meta-analysis. Int J Cardiol 114 : 303 308.
18. Grainger DJ, Kemp PR, Metcalfe JC, Liu AC, Lawn RM, Williams NR et al. (1995). The serum concentration of active transforming growth factor-beta is severely depressed in advanced atherosclerosis. Nat Med 1 : 74 79.
19. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK et al. (2006). Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. sci 312 : 117 121.
20. Ikonomidis JS, Jones JA, Barbour JR, Stroud RE, Clark LL, Kaplan BS et al. (2006). Expression of matrix metalloproteinases and endogenous inhibitors within ascending aortic aneurysms of patients with Marfan syndrome. Circulation 114 : I365 I370.
21. Inoue N, Venema RC, Sayegh HS, Ohara Y, Murphy TJ, Harrison DG (1995). Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler Thromb Vasc Biol 15 : 1255 1261.
22. Jones KB, Myers L, Judge DP, Kirby PA, Dietz HC, Sponseller PD (2005). Toward an understanding of dural ectasia: a light microscopy study in a murine model of Marfan syndrome. Spine 30 : 291 293.
23. Judge DP, Biery NJ, Keene DR, Geubtner J, Myers L, Huso DL et al. (2004). Evidence for a critical contribution of haploinsufficiency in the complex pathogenesis of Marfan syndrome. J Clin Invest 114 : 172 181.
24. Judge DP, Dietz HC (2005). Marfan's syndrome. Lancet 366 : 1965 1976.
25. Karasawa A, Guo JP, Ma XL, Lefer AM (1991). Beneficial effects of transforming growth factor-beta and tissue plasminogen activator in splanchnic artery occlusion and reperfusion in cats. J Cardiovasc Pharmacol 18 : 95 105.
26. Karnik SK, Brooke BS, Bayes-Genis A, Sorensen L, Wythe JD, Schwartz RS et al. (2003). A critical role for elastin signaling in vascular morphogenesis and disease. Development 130 : 411 423.
27. Kenny D, Coughlan MG, Pagel PS, Kampine JP, Warltier DC (1994). Transforming growth factor beta 1 preserves endothelial function after multiple brief coronary artery occlusions and reperfusion. Am Heart J 127 : 1456 1461.
28. Lacro RV, Dietz HC, Wruck LM, Bradley TJ, Colan SD, Devereux RB et al. Pediatric Heart Network Investigators (2007). Rationale and design of a randomized clinical trial of beta-blocker therapy (atenolol) versus angiotensin II receptor blocker therapy (losartan) in individuals with Marfan syndrome. Am Heart J 154 : 624 631.
29. Matt P, Habashi J, Carrel T, Cameron DE, Van Eyk JE, Dietz HC (2008). Recent advances in understanding Marfan syndrome: should we now treat surgical patients with losartan? J Thorac Cardiovasc Surg 135 : 389 394.
30. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M et al. (2003). Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation 108 : II329 II334.
31. Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B et al. (2003). Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet 33 : 407 411.
32. Ng CM, Cheng A, Myers LA, Martinez-Murillo F, Jie C, Bedja D et al. (2004). TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J Clin Invest 114 : 1586 1592.
33. Pfaff M, Reinhardt DP, Sakai LY, Timpl R (1996). Cell adhesion and integrin binding to recombinant human fibrillin-1. FEBS Lett 384 : 247 250.
34. Rios AS, Silber EN, Bavishi N, Varga P, Burton BK, Clark WA et al. (1999). Effect of long-term beta-blockade on aortic root compliance in patients with Marfan syndrome. Am Heart J 137 : 1057 1061.
35. Sakamoto H, Broekelmann T, Cheresh DA, Ramirez F, Rosenbloom J, Mecham RP (1996). Cell-type specific recognition of RGD- and non-RGD-containing cell binding domains in fibrillin-1. J Biol Chem 271 : 4916 4922.
36. Saura M, Zaragoza C, Cao W, Bao C, Rodríguez-Puyol M, Rodríguez-Puyol D et al. (2002). Smad2 mediates transforming growth factor-beta induction of endothelial nitric oxide synthase expression. Circ Res 91 : 806 813.
37. Schleicher M, Sessa WC (2008). Are the mechanisms for NO-dependent vascular remodeling different from vasorelaxation in vivo? Arterioscler Thromb Vasc Biol 28 : 1207 1208.
38. Sharma K, Deelman L, Madesh M, Kurz B, Ciccone E, Siva S et al. (2003). Involvement of transforming growth factor-beta in regulation of calcium transients in diabetic vascular smooth muscle cells. Am J Physiol Renal Physiol 285 : F1258 F1270.
39. Shores J, Berger KR, Murphy EA, Pyeritz RE (1994). Progression of aortic dilatation and the benefit of long-term beta-adrenergic blockade in Marfan's syndrome. N Engl J Med 330 : 1335 1341.
40. Simpson CF, Kling JM, Palmer RF (1968). The use of propranolol for the protection of turkeys from the development of beta-aminopropionitrile-induced aortic ruptures. Angiology 19 : 414 418.
41. Tong XK, Hamel E (2007). Transforming growth factor-beta 1 impairs endothelin-1-mediated contraction of brain vessels by inducing mitogen-activated protein (MAP) kinase phosphatase-1 and inhibiting p38 MAP kinase. Mol Pharmacol 72 : 1476 1483.
42. Viñals F, Pouysségur J (2001). Transforming growth factor beta1 (TGF-beta1) promotes endothelial cell survival during in vitro angiogenesis via an autocrine mechanism implicating TGF-alpha signaling. Mol Cell Biol 21 : 7218 7230.
43. Wang W, Viappiani S, Sawicka J, Schulz R (2005). Inhibition of endogenous nitric oxide in the heart enhances matrix metalloproteinase-2 release. Br J Pharmacol 145 : 43 49.
44. Wang M, Zhao D, Spinetti G, Zhang J, Jiang LQ, Pintus G et al. (2006). Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol 26 : 1503 1509.
45. Wolinsky H, Glagov S (1967). A lamellar unit of aortic medial structure and function in mammals. Circ Res 20 : 99 111.
46. Yin FC, Brin KP, Ting CT, Pyeritz RE (1989). Arterial hemodynamic indexes in Marfan's syndrome. Circulation 79 : 854 862.