Angiotensin-converting enzyme-induced activation of local angiotensin signaling is required for ascending aortic aneurysms in fibulin-4-deficient mice

Science Translational Medicine

Volumn 5, Issue 183, 2013, Pages

  Huang, Jianbin ^a   Yamashiro, Yoshito ^a   Papke, Christina L ^a   Ikeda, Yuichi ^a,b   Lin, Yanling ^a   Patel, Miteshkumar ^a   Inagami, Tadashi ^c   Le, Victoria P ^d   Wagenseil, Jessica E ^d   Yanagisawa, Hiromi ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Saint Louis University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1A RECEPTOR; ANGIOTENSIN 1B RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE; FIBULIN; FIBULIN 4; LOSARTAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ANEURYSM; ARTICLE; BLOOD VESSEL WALL; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION;

ANGIOTENSIN II; ANIMALS; AORTA; AORTIC ANEURYSM; BIOLOGICAL MARKERS; BIOMECHANICAL PHENOMENA; BLOOD PRESSURE; CAPTOPRIL; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE DELETION; LOSARTAN; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PEPTIDYL-DIPEPTIDASE A; PHENOTYPE; PHOSPHORYLATION; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; SIGNAL TRANSDUCTION; TIME FACTORS; UP-REGULATION;

EID: 84878267172     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005025     Document Type: Article

References (49)

1. D. M. Milewicz, D. C. Guo, V. Tran-Fadulu, A. L. Lafont, C. L. Papke, S. Inamoto, C. S. Kwartler, H. Pannu, Genetic basis of thoracic aortic aneurysms and dissections: Focus on smooth muscle cell contractile dysfunction. Annu. Rev. Genomics Hum. Genet. 9, 283-302 (2008).
2. D. Jain, H. C. Dietz, G. L. Oswald, J. J. Maleszewski, M. K. Halushka, Causes and histopathology of ascending aortic disease in children and young adults. Cardiovasc. Pathol. 20, 15-25 (2011).
3. E. R. Neptune, P. A. Frischmeyer, D. E. Arking, L. Myers, T. E. Bunton, B. Gayraud, F. Ramirez, L. Y. Sakai, H. C. Dietz, Dysregulation of TGF-β activation contributes to pathogenesis in Marfan syndrome. Nat. Genet. 33, 407-411 (2003).
4. I. M. van de Laar, R. A. Oldenburg, G. Pals, J. W. Roos-Hesselink, B. M. de Graaf, J. M. Verhagen, Y. M. Hoedemaekers, R. Willemsen, L. A. Severijnen, H. Venselaar, G. Vriend, P. M. Pattynama, M. Collée, D. Majoor-Krakauer, D. Poldermans, I. M. Frohn-Mulder, D. Micha, J. Timmermans, Y. Hilhorst-Hofstee, S. M. Bierma-Zeinstra, P. J. Willems, J. M. Kros, E. H. Oei, B. A. Oostra, M. W. Wessels, A. M. Bertoli-Avella, Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nat. Genet. 43, 121-126 (2011).
5. B. L. Loeys, J. Chen, E. R. Neptune, D. P. Judge, M. Podowski, T. Holm, J. Meyers, C. C. Leitch, N. Katsanis, N. Sharifi, F. L. Xu, L. A. Myers, P. J. Spevak, D. E. Cameron, J. De Backer, J. Hellemans, Y. Chen, E. C. Davis, C. L. Webb, W. Kress, P. Coucke, D. B. Rifkin, A. M. De Paepe, H. C. Dietz, A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat. Genet. 37, 275-281 (2005).
6. T. M. Holm, J. P. Habashi, J. J. Doyle, D. Bedja, Y. Chen, C. van Erp, M. E. Lindsay, D. Kim, F. Schoenhoff, R. D. Cohn, B. L. Loeys, C. J. Thomas, S. Patnaik, J. J. Marugan, D. P. Judge, H. C. Dietz, Noncanonical TGFb signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 332, 358-361 (2011).
7. K. Hanada, M. Vermeij, G. A. Garinis, M. C. de Waard, M. G. Kunen, L. Myers, A. Maas, D. J. Duncker, C. Meijers, H. C. Dietz, R. Kanaar, J. Essers, Perturbations of vascular homeostasis and aortic valve abnormalities in fibulin-4 deficient mice. Circ. Res. 100, 738-746 (2007).
8. J. P. Habashi, D. P. Judge, T. M. Holm, R. D. Cohn, B. L. Loeys, T. K. Cooper, L. Myers, E. C. Klein, G. Liu, C. Calvi, M. Podowski, E. R. Neptune, M. K. Halushka, D. Bedja, K. Gabrielson, D. B. Rifkin, L. Carta, F. Ramirez, D. L. Huso, H. C. Dietz, Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312, 117-121 (2006).
9. 1) receptor blockade. PLoS One 6, e23411 (2011).
10. P. J. McLaughlin, Q. Chen, M. Horiguchi, B. C. Starcher, J. B. Stanton, T. J. Broekelmann, A. D. Marmorstein, B. McKay, R. Mecham, T. Nakamura, L. Y. Marmorstein, Targeted disruption of fibulin-4 abolishes elastogenesis and causes perinatal lethality in mice. Mol. Cell. Biol. 26, 1700-1709 (2006).
11. N. Kobayashi, G. Kostka, J. H. Garbe, D. R. Keene, H. P. Bächinger, F. G. Hanisch, D. Markova, T. Tsuda, R. Timpl, M. L. Chu, T. Sasaki, A comparative analysis of the fibulin protein family. Biochemical characterization, binding interactions, and tissue localization. J. Biol. Chem. 282, 11805-11816 (2007).
12. M. Horiguchi, T. Inoue, T. Ohbayashi, M. Hirai, K. Noda, L. Y. Marmorstein, D. Yabe, K. Takagi, T. O. Akama, T. Kita, T. Kimura, T. Nakamura, Fibulin-4 conducts proper elastogenesis via interaction with cross-linking enzyme lysyl oxidase. Proc. Natl. Acad. Sci. U.S.A. 106, 19029-19034 (2009).
13. J. Huang, E. C. Davis, S. L. Chapman, M. Budatha, L. Y. Marmorstein, R. A. Word, H. Yanagisawa, Fibulin-4 deficiency results in ascending aortic aneurysms: A potential link between abnormal smooth muscle cell phenotype and aneurysm progression. Circ. Res. 106, 583-592 (2010).
14. V. Hucthagowder, N. Sausgruber, K. H. Kim, B. Angle, L. Y. Marmorstein, Z. Urban, Fibulin-4: A novel gene for an autosomal recessive cutis laxa syndrome. Am. J. Hum. Genet. 78, 1075-1080 (2006).
15. M. Dasouki, D. Markova, R. Garola, T. Sasaki, N. L. Charbonneau, L. Y. Sakai, M. L. Chu, Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodactyly, and mild cutis laxa. Am. J. Med. Genet. A 143A, 2635-2641 (2007).
16. L. K. Erickson, J. Opitz, H. H. Zhou, Lethal osteogenesis imperfecta-like condition with cutis laxa and arterial tortuosity in MZ twins due to a homozygous fibulin-4 mutation. Pediatr. Dev. Pathol. 15, 137-141 (2012).
17. U. Schmitz, B. C. Berk, Angiotensin II signal transduction: Stimulation of multiple mitogen-activated protein kinase pathways. Trends Endocrinol. Metab. 8, 261-266 (1997).
18. V. P. Le, R. H. Knutsen, R. P. Mecham, J. E. Wagenseil, Decreased aortic diameter and compliance precedes blood pressure increases in postnatal development of elastin-insufficient mice. Am. J. Physiol. Heart Circ. Physiol. 301, H221-H229 (2011).
19. H. Yanagisawa, E. C. Davis, B. C. Starcher, T. Ouchi, M. Yanagisawa, J. A. Richardson, E. N. Olson, Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415, 168-171 (2002).
20. J. E. Wagenseil, C. H. Ciliberto, R. H. Knutsen, M. A. Levy, A. Kovacs, R. P. Mecham, Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circ. Res. 104, 1217-1224 (2009). Downloaded from stm.sciencemag.org on May 23, 2013
21. J. M. Burson, G. Aguilera, K. W. Gross, C. D. Sigmund, Differential expression of angiotensin receptor 1A and 1B in mouse. Am. J. Physiol. 267, E260-E267 (1994).
22. J. Stegbauer, T. M. Coffman, New insights into angiotensin receptor actions: From blood pressure to aging. Curr. Opin. Nephrol. Hypertens. 20, 84-88 (2011).
23. J. P. Habashi, J. J. Doyle, T. M. Holm, H. Aziz, F. Schoenhoff, D. Bedja, Y. Chen, A. N. Modiri, D. P. Judge, H. C. Dietz, Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332, 361-365 (2011).
24. R. Morishita, G. H. Gibbons, K. E. Ellison, W. Lee, L. Zhang, H. Yu, Y. Kaneda, T. Ogihara, V. J. Dzau, Evidence for direct local effect of angiotensin in vascular hypertrophy. In vivo gene transfer of angiotensin converting enzyme. J. Clin. Invest. 94, 978-984 (1994).
25. V. J. Dzau, K. Bernstein, D. Celermajer, J. Cohen, B. Dahlof, J. Deanfield, J. Diez, H. Drexler, R. Ferrari, W. van Gilst, L. Hansson, B. Hornig, A. Husain, C. Johnston, H. Lazar, E. Lonn, T. Luscher, J. Mancini, A. Mimran, C. Pepine, T. Rabelink, W. Remme, L. Ruilope, M. Ruzicka, H. Schunkert, K. Swedberg, T. Unger, D. Vaughan, M. Weber; Working Group on Tissue Angiotensin-converting enzyme, International Society of Cardiovascular Pharmacotherapy, The relevance of tissue angiotensin-converting enzyme: Manifestations in mechanistic and endpoint data. Am. J. Cardiol. 88, 1L-20L (2001).
26. G. Bakris, Are there effects of renin-angiotensin system antagonists beyond blood pressure control? Am. J. Cardiol. 105, 21A-29A (2010).
27. H. Rakugi, D. K. Kim, J. E. Krieger, D. S. Wang, V. J. Dzau, R. E. Pratt, Induction of angiotensin converting enzyme in the neointima after vascular injury. Possible role in restenosis. J. Clin. Invest. 93, 339-346 (1994).
28. M. Ohishi, M. Ueda, H. Rakugi, A. Okamura, T. Naruko, A. E. Becker, K. Hiwada, A. Kamitani, K. Kamide, J. Higaki, T. Ogihara, Upregulation of angiotensin-converting enzyme during the healing process after injury at the site of percutaneous transluminal coronary angioplasty in humans. Circulation 96, 3328-3337 (1997).
29. F. S. de Man, L. Tu, M. L. Handoko, S. Rain, G. Ruiter, C. Francois, I. Schalij, P. Dorfmuller, G. Simonneau, E. Fadel, F. Perros, A. Boonstra, P. E. Postmus, J. van der Velden, A. Vonk-Noordegraaf, M. Humbert, S. Eddahibi, C. Guignabert, Dysregulated renin-angiotensin - aldosterone system contributes to pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 186, 780-789 (2012).
30. H. Pannu, V. Tran-Fadulu, C. L. Papke, S. Scherer, Y. Liu, C. Presley, D. Guo, A. L. Estrera, H. J. Safi, A. R. Brasier, G. W. Vick, A. J. Marian, C. S. Raman, L. M. Buja, D. M. Milewicz, MYH11 mutations result in a distinct vascular pathology driven by insulin-like growth factor 1 and angiotensin II. Hum. Mol. Genet. 16, 2453-2462 (2007).
31. R. S. Fishel, V. Thourani, S. J. Eisenberg, S. Y. Shai, M. A. Corson, E. G. Nabel, K. E. Bernstein, B. C. Berk, Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. Possible mediator of the response to vascular injury. J. Clin. Invest. 95, 377-387 (1995).
32. M. Moroi, M. Fukazawa, M. Ishikawa, J. Aikawa, A. Namiki, T. Yamaguchi, Effect of endothelin on angiotensin converting enzyme activity in cultured vascular smooth muscle cells. Gen. Pharmacol. 27, 463-465 (1996).
33. W. Gosgnach, M. Challah, F. Coulet, J. B. Michel, T. Battle, Shear stress induces angiotensin converting enzyme expression in cultured smooth muscle cells: Possible involvement of bFGF. Cardiovasc. Res. 45, 486-492 (2000).
34. K. Iizuka, T. Machida, H. Kawaguchi, M. Hirafuji, Pulsatile mechanical pressure promotes angiotensin-converting enzyme expression in aortic smooth muscle cells. Cardiovasc. Drugs Ther. 22, 383-390 (2008).
35. S. D. Crowley, M. P. Vasievich, P. Ruiz, S. K. Gould, K. K. Parsons, A. K. Pazmino, C. Facemire, B. J. Chen, H. S. Kim, T. T. Tran, D. S. Pisetsky, L. Barisoni, M. C. Prieto-Carrasquero, M. Jeansson, M. H. Foster, T. M. Coffman, Glomerular type 1 angiotensin receptors augment kidney injury and inflammation in murine autoimmune nephritis. J. Clin. Invest. 119, 943-953 (2009).
36. U. M. Steckelings, M. Larhed, A. Hallberg, R. E. Widdop, E. S. Jones, C. Wallinder, P. Namsolleck, B. Dahlöf, T. Unger, Non-peptide AT2-receptor agonists. Curr. Opin. Pharmacol. 11, 187-192 (2011).
37. L. Paulis, S. T. Becker, K. Lucht, K. Schwengel, S. Slavic, E. Kaschina, C. Thöne-Reineke, B. Dahlöf, J. Baulmann, T. Unger, U. M. Steckelings, Direct angiotensin II type 2 receptor stimulation in Nw-nitro-L-arginine-methyl ester-induced hypertension: The effect on pulse wave velocity and aortic remodeling. Hypertension 59, 485-492 (2012).
38. E. Kaschina, A. Grzesiak, J. Li, A. Foryst-Ludwig, M. Timm, F. Rompe, M. Sommerfeld, U. R. Kemnitz, C. Curato, P. Namsolleck, C. Tschöpe, A. Hallberg, M. Alterman, T. Hucko, I. Paetsch, T. Dietrich, B. Schnackenburg, K. Graf, B. Dahlöf, U. Kintscher, T. Unger, U. M. Steckelings, Angiotensin II type 2 receptor stimulation: A novel option of therapeutic interference with the renin-angiotensin system in myocardial infarction? Circulation 118, 2523-2532 (2008).
39. A. Rehman, A. Leibowitz, N. Yamamoto, Y. Rautureau, P. Paradis, E. L. Schiffrin, Angiotensin type 2 receptor agonist compound 21 reduces vascular injury and myocardial fibrosis in stroke-prone spontaneously hypertensive rats. Hypertension 59, 291-299 (2012).
40. A. B. Jehle, Y. Xu, J. M. Dimaria, B. A. French, F. H. Epstein, S. S. Berr, R. J. Roy, B. A. Kemp, R. M. Carey, C. M. Kramer, A nonpeptide angiotensin II type 2 receptor agonist does not attenuate postmyocardial infarction left ventricular remodeling in mice. J. Cardiovasc. Pharmacol. 59, 363-368 (2012).
41. D. G. Hackam, D. Thiruchelvam, D. A. Redelmeier, Angiotensin-converting enzyme inhibitors and aortic rupture: A population-based case-control study. Lancet 368, 659-665 (2006).
42. A. A. Ahimastos, A. Aggarwal, K. M. D'Orsa, M. F. Formosa, A. J. White, R. Savarirayan, A. M. Dart, B. A. Kingwell, Effect of perindopril on large artery stiffness and aortic root diameter in patients with Marfan syndrome: A randomized controlled trial. JAMA 298, 1539-1547 (2007).
43. A. T. Yetman, R. A. Bornemeier, B. W. McCrindle, Usefulness of enalapril versus propranolol or atenolol for prevention of aortic dilation in patients with the Marfan syndrome. Am. J. Cardiol. 95, 1125-1127 (2005).
44. K. Möberg, S. De Nobele, D. Devos, E. Goetghebeur, P. Segers, B. Trachet, C. Vervaet, M. Renard, P. Coucke, B. Loeys, A. De Paepe, J. De Backer, The Ghent Marfan Trial - A randomized, double-blind placebo controlled trial with losartan in Marfan patients treated with b-blockers. Int. J. Cardiol. 157, 354-358 (2012).
45. T. Radonic, P. de Witte, M. J. Baars, A. H. Zwinderman, B. J. Mulder, M. Groenink; COMPARE study group, Losartan therapy in adults with Marfan syndrome: Study protocol of the multi-center randomized controlled COMPARE trial. Trials 11, 3 (2010).
46. X. Jiang, D. H. Rowitch, P. Soriano, A. P. McMahon, H. M. Sucov, Fate of the mammalian cardiac neural crest. Development 127, 1607-1616 (2000).
47. C. Pouget, R. Gautier, M. A. Teillet, T. Jaffredo, Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 133, 1013-1022 (2006).
48. S. Topouzis, J. D. Catravas, J. W. Ryan, T. H. Rosenquist, Influence of vascular smooth muscle heterogeneity on angiotensin converting enzyme activity in chicken embryonic aorta and in endothelial cells in culture. Circ. Res. 71, 923-931 (1992).
49. T. Ichiki, P. A. Labosky, C. Shiota, S. Okuyama, Y. Imagawa, A. Fogo, F. Niimura, I. Ichikawa, B. L. Hogan, T. Inagami, Effects on blood pressure and exploratory behaviour of mice lacking angiotensin II type-2 receptor. Nature 377, 748-750 (1995).