Enhanced caspase activity contributes to aortic wall remodeling and early aneurysm development in a murine model of marfan syndrome

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 1, 2016, Pages 146-154

  Emrich, Fabian C ^a,c   Okamura, Homare ^a,d   Dalal, Alex R ^a   Penov, Kiril ^a,c   Merk, Denis R ^a,c   Raaz, Uwe ^b   Hennigs, Jan K ^b   Chin, Jocelyn T ^a   Miller, Miquell O ^a   Pedroza, Albert J ^a   Craig, Juliana K ^a   Koyano, Tiffany K ^a   Blankenberg, Francis G ^b   Connolly, Andrew J ^a   Mohr, Friedrich W ^c   Alvira, Cristina M ^b   Rabinovitch, Marlene ^b   Fischbein, Michael P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Aneurysm; apoptosis; caspases; extracellular matrix; Marfan syndrome

Indexed keywords

ANNEXIN; CASPASE; CASPASE 3; CASPASE 9; ELASTIN; PROTEIN BCL 2; PROTEIN MCL 1; STAUROSPORINE; TECHNETIUM 99M; ACTIN BINDING PROTEIN; CASPASE INHIBITOR; FIBRILLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; AORTA ANEURYSM; AORTA WALL; APOPTOSIS; ARTERIAL WALL THICKNESS; ARTICLE; ASCENDING AORTA; AUTORADIOGRAPHY; CELL ISOLATION; CELL SURFACE; CONTROLLED STUDY; CYTOSOLIC FRACTION; DESCENDING AORTA; ENZYME ACTIVITY; EX VIVO STUDY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MARFAN SYNDROME; MOUSE; NONHUMAN; PROTEIN DEGRADATION; SCANNING ELECTRON MICROSCOPY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SMOOTH MUSCLE FIBER; SMOOTH MUSCLE FIBER MEMBRANE; WESTERN BLOTTING; ANIMAL; AORTIC ANEURYSM; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; COMPLICATION; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; MALE; METABOLISM; MUTANT MOUSE STRAIN; MUTATION; SCINTISCANNING; TIME; ULTRASTRUCTURE; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA; AORTIC ANEURYSM; APOPTOSIS; AUTORADIOGRAPHY; CASPASE INHIBITORS; CASPASES; CELL MEMBRANE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ELASTIN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MALE; MARFAN SYNDROME; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; TIME FACTORS; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; VASCULAR REMODELING;

EID: 84920276864     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304364     Document Type: Article

References (26)

1. Judge DP, Dietz HC. Marfan's syndrome. Lancet. 2005;366:1965-1976.
2. Dietz HC, Loeys B, Carta L, Ramirez F. Recent progress towards a molecular understanding of Marfan syndrome. Am J Med Genet. 2005;139C:4-9.
3. Habashi JP, Judge DP, Holm TM, et al. Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science. 2006;312:117-121.
4. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, Tsao PS, Iosef C, Berry GJ, Mohr FW, Spin JM, Alvira CM, Robbins RC, Fischbein MP. miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res. 2012;110:312-324.
5. Mohamed SA, Misfeld M, Hanke T, Charitos EI, Bullerdiek J, Belge G, Kuehnel W, Sievers HH. Inhibition of caspase-3 differentially affects vascular smooth muscle cell apoptosis in the concave versus convex aortic sites in ascending aneurysms with a bicuspid aortic valve. Ann Anat. 2010;192:145-150.
6. Nagashima H, Sakomura Y, Aoka Y, Uto K, Kameyama K, Ogawa M, Aomi S, Koyanagi H, Ishizuka N, Naruse M, Kawana M, Kasanuki H. Angiotensin II type 2 receptor mediates vascular smooth muscle cell apop-tosis in cystic medial degeneration associated with Marfan's syndrome. Circulation. 2001;104(12 suppl 1):I282-I287.
7. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, Dietz HC. Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science. 2011;332:361-365.
8. Okamura H, Pisani LJ, Dalal AR, et al. Assessment of elastin defcit in a Marfan mouse aneurysm model using an elastin-specifc magnetic resonance imaging contrast agent. Circ Cardiovasc Imaging. 2014;7.
9. Cowan KN, Leung WCY, Mar C, Bhattacharjee R, Zhu Y, Rabinovitch M. Caspases from apoptotic myocytes degrade extracellular matrix: a novel remodeling paradigm. FASEB J. 2005;19:1848-1850.
10. Umeda H, Aikawa M, Libby P. Liberation of desmosine and isodesmosine as amino acids from insoluble elastin by elastolytic proteases. Biochem Biophys Res Commun. 2011;411:281-286.
11. Bunton TE, Biery NJ, Myers L, Gayraud B, Ramirez F, Dietz HC. Phenotypic alteration of vascular smooth muscle cells precedes elastolysis in a mouse model of Marfan syndrome. Circ Res. 2001;88:37-43.
12. Schmid FX, Bielenberg K, Schneider A, Haussler A, Keyser A, Birnbaum D. Ascending aortic aneurysm associated with bicuspid and tricuspid aortic valve: involvement and clinical relevance of smooth muscle cell apop-tosis and expression of cell death-initiating proteins. Eur J Cardiothorac Surg. 2003;23:537-543.
13. Henderson EL, Geng YJ, Sukhova GK, Whittemore AD, Knox J, Libby P. Death of smooth muscle cells and expression of mediators of apoptosis by T lymphocytes in human abdominal aortic aneurysms. Circulation. 1999;99:96-104.
14. Lesauskaite V, Tanganelli P, Sassi C, Neri E, Diciolla F, Ivanoviene L, Epistolato MC, Lalinga AV, Alessandrini C, Spina D. Smooth muscle cells of the media in the dilatative pathology of ascending thoracic aorta: morphology, immunoreactivity for osteopontin, matrix metalloprotein-ases, and their inhibitors. Hum Pathol. 2001;32:1003-1011.
15. Leeper NJ, Raiesdana A, Kojima Y, et al. Loss of CDKN2B Promotes p53-Dependent Smooth Muscle Cell Apoptosis and Aneurysm Formation. Arterioscler Thromb Vasc Biol. 2013;33:e1-e10.
16. Miyake T, Aoki M, Masaki H, Kawasaki T, Oishi M, Kataoka K, Ogihara T, Kaneda Y, Morishita R. Regression of abdominal aortic aneurysms by simultaneous inhibition of nuclear factor kappaB and ets in a rabbit model. Circ Res. 2007;101:1175-1184.
17. Kovacevic M, Jonjic N, Stalekar H, Zaputovic L, Stifter S, Vitezic D. Apoptotic cell death and rupture of abdominal aortic aneurysm. Med Hypotheses. 2010;74:908-910.
18. Daugherty A, Rateri DL, Charo IF, Owens AP, Howatt DA, Cassis LA. Angiotensin II infusion promotes ascending aortic aneurysms: attenuation by CCR2 defciency in apoE-/-mice. Clin Sci (Lond). 2010;118:681-689.
19. Rateri DL, Moorleghen JJ, Balakrishnan A, Owens AP, Howatt DA, Subramanian V, Poduri A, Charnigo R, Cassis LA, Daugherty A. Endothelial cell-specifc defciency of Ang II type 1a receptors attenuates Ang II-induced ascending aortic aneurysms in LDL receptor-/-mice. Circ Res. 2011;108:574-581.
20. Balasubramanian K, Mirnikjoo B, Schroit AJ. Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J Biol Chem. 2007;282:18357-18364.
21. Gomez D, Kessler K, Borges LF, Richard B, Touat Z, Ollivier V, Mansilla S, Bouton MC, Alkoder S, Nataf P, Jandrot-Perrus M, Jondeau G, Vranckx R, Michel JB. Smad2-dependent protease nexin-1 overexpression differentiates chronic aneurysms from acute dissections of human ascending aorta. Arterioscler Thromb Vasc Biol. 2013;33:2222-2232.
22. Berger AB, Sexton KB, Bogyo M. Commonly used caspase inhibitors designed based on substrate specifcity profles lack selectivity. Cell Res. 2006;16:961-963.
23. Kenagy RD, Min SK, Mulvihill E, Clowes AW. A link between smooth muscle cell death and extracellular matrix degradation during vascular atrophy. J Vasc Surg. 2011;54:182-191.
24. Yu H, Clarke MC, Figg N, Littlewood TD, Bennett MR. Smooth muscle cell apoptosis promotes vessel remodeling and repair via activation of cell migration, proliferation, and collagen synthesis. Arterioscler Thromb Vasc Biol. 2011;31:2402-2409.
25. Skjøt-Arkil H, Barascuk N, Register T, Karsdal MA. Macrophage-mediated proteolytic remodeling of the extracellular matrix in atherosclerosis results in neoepitopes: a potential new class of biochemical markers. Assay Drug Dev Technol. 2010;8:542-552.
26. Guo G, Gehle P, Doelken S, Martin-Ventura JL, von Kodolitsch Y, Hetzer R, Robinson PN. Induction of macrophage chemotaxis by aortic extracts from patients with Marfan syndrome is related to elastin binding protein. PLoS One. 2011;6:e20138.