Inadequate reinforcement of transmedial disruptions at branch points subtends aortic aneurysm formation in apolipoprotein-E-deficient mice

Cardiovascular Pathology

Volumn 23, Issue 3, 2014, Pages 152-159

  Gavish, Lilach ^a   Beeri, Ronen ^b   Gilon, Dan ^b   Rubinstein, Chen ^b   Berlatzky, Yacov ^b   Gavish, Leah Y ^a   Bulut, Atilla ^b   Harlev, Mickey ^b   Reissman, Petachia ^c   Gertz, S David ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c SHAARE ZEDEK MEDICAL CENTER   (Israel)

Author keywords

Abdominal aortic aneurysm; Aneurysm; Angiotensin II; Apolipoprotein e deficient mice

Indexed keywords

ANGIOTENSIN II; APOLIPOPROTEIN E; COLLAGEN; PARAFFIN; SODIUM CHLORIDE;

ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELIAC ARTERY; CONTROLLED STUDY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PHOTOTHERAPY; PRIORITY JOURNAL; REINFORCEMENT; RENAL ARTERY; SUPERIOR MESENTERIC ARTERY; ABDOMINAL AORTA; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHI SQUARE DISTRIBUTION; DEFICIENCY; DISEASE COURSE; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TIME; TUNICA MEDIA;

ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; CHI-SQUARE DISTRIBUTION; COLLAGEN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; TIME FACTORS; TUNICA MEDIA;

EID: 84900314226     PISSN: 10548807     EISSN: 18791336     Source Type: Journal    
DOI: 10.1016/j.carpath.2013.12.005     Document Type: Article

References (66)

1. H Abdul-Hussien, R Hanemaaijer, R Kleemann, BF Verhaaren, JH van Bockel, and JH Lindeman The pathophysiology of abdominal aortic aneurysm growth: corresponding and discordant inflammatory and proteolytic processes in abdominal aortic and popliteal artery aneurysms J Vasc Surg 51 2010 1479 1487
2. MM Dua, and RL Dalman Hemodynamic influences on abdominal aortic aneurysm disease: application of biomechanics to aneurysm pathophysiology Vascul Pharmacol 53 2010 11 21
3. J Golledge, J Muller, A Daugherty, and P Norman Abdominal aortic aneurysm: pathogenesis and implications for management Arterioscler Thromb Vasc Biol 26 2006 2605 2613
4. EL Henderson, YJ Geng, GK Sukhova, AD Whittemore, J Knox, and P Libby Death of smooth muscle cells and expression of mediators of apoptosis by T lymphocytes in human abdominal aortic aneurysms Circulation 99 1999 96 104
5. JD Humphrey, and CA Taylor Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models Annu Rev Biomed Eng 10 2008 221 246
6. VL Rowe, SL Stevens, TT Reddick, MB Freeman, R Donnell, and RC Carroll et al. Vascular smooth muscle cell apoptosis in aneurysmal, occlusive, and normal human aortas J Vasc Surg 31 2000 567 576
7. RW Thompson, and WC Parks Role of matrix metalloproteinases in abdominal aortic aneurysms Ann N Y Acad Sci 800 1996 157 174
8. CK Zarins, C Xu, and S Glagov Atherosclerotic enlargement of the human abdominal aorta Atherosclerosis 155 2001 157 164
9. RW Thompson, PJ Geraghty, and JK Lee Abdominal aortic aneurysms: basic mechanisms and clinical implications Curr Probl Surg 39 2002 110 230
10. A Daugherty, MW Manning, and LA Cassis Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice J Clin Invest 105 2000 1605 1612
11. MW Manning, LA Cassi, J Huang, SJ Szilvassy, and A Daugherty Abdominal aortic aneurysms: fresh insights from a novel animal model of the disease Vasc Med 7 2002 45 54
12. K Saraff, F Babamusta, LA Cassis, and A Daugherty Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice Arterioscler Thromb Vasc Biol 23 2003 1621 1626
13. L Gavish, C Rubinstein, A Bulut, Y Berlatzky, R Beeri, and D Gilon et al. Low-level laser irradiation inhibits abdominal aortic aneurysm progression in apolipoprotein E-deficient mice Cardiovasc Res 83 2009 785 792
14. L Gavish, C Rubinstein, Y Berlatzky, LY Gavish, R Beeri, and D Gilon et al. Low level laser arrests abdominal aortic aneurysm by collagen matrix reinforcement in apolipoprotein e-deficient mice Lasers Surg Med 44 2012 664 674
15. C Barisione, R Charnigo, DA Howatt, JJ Moorleghen, DL Rateri, and A Daugherty Rapid dilation of the abdominal aorta during infusion of angiotensin II detected by noninvasive high-frequency ultrasonography J Vasc Surg 44 2006 372 376
16. D Bruemmer, A Daugherty, H Lu, and DL Rateri Relevance of angiotensin II-induced aortic pathologies in mice to human aortic aneurysms Ann N Y Acad Sci 1245 2011 7 10
17. C Fatini, G Pratesi, F Sofi, F Gensini, E Sticchi, and B Lari et al. ACE DD genotype: a predisposing factor for abdominal aortic aneurysm Eur J Vasc Endovasc Surg 29 2005 227 232
18. DG Hackam, D Thiruchelvam, and DA Redelmeier Angiotensin-converting enzyme inhibitors and aortic rupture: a population-based case-control study Lancet 368 2006 659 665
19. MJ Sweeting, SG Thompson, LC Brown, RM Greenhalgh, and JT Powell Use of angiotensin converting enzyme inhibitors is associated with increased growth rate of abdominal aortic aneurysms J Vasc Surg 52 2010 1 4
20. J Golledge, and PE Norman Current status of medical management for abdominal aortic aneurysm Atherosclerosis 217 2011 57 63
21. A Thompson, JA Cooper, M Fabricius, SE Humphries, HA Ashton, and H Hafez An analysis of drug modulation of abdominal aortic aneurysm growth through 25 years of surveillance J Vasc Surg 52 2010 55 61 [e2]
22. CM He, and MR Roach The composition and mechanical properties of abdominal aortic aneurysms J Vasc Surg 20 1994 6 13
23. AJ Schriefl, MJ Collins, DM Pierce, GA Holzapfel, LE Niklason, and JD Humphrey Remodeling of intramural thrombus and collagen in an Ang-II infusion ApoE-/- model of dissecting aortic aneurysms Thromb Res 130 2012 e139 e146
24. JD Humphrey, and GA Holzapfel Mechanics, mechanobiology, and modeling of human abdominal aorta and aneurysms J Biomech 45 2012 805 814
25. M Fillinger The long-term relationship of wall stress to the natural history of abdominal aortic aneurysms (finite element analysis and other methods) Ann N Y Acad Sci 1085 2006 22 28
26. M Truijers, JA Pol, LJ Schultzekool, SM van Sterkenburg, MF Fillinger, and JD Blankensteijn Wall stress analysis in small asymptomatic, symptomatic and ruptured abdominal aortic aneurysms Eur J Vasc Endovasc Surg 33 2007 401 407
27. JS Wilson, S Baek, and JD Humphrey Parametric study of effects of collagen turnover on the natural history of abdominal aortic aneurysms Proc Math Phys Eng Sci 469 2013 1 18
28. GM Longo, W Xiong, TC Greiner, Y Zhao, N Fiotti, and BT Baxter Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms J Clin Invest 110 2002 625 632
29. M Tao, P Yu, BT Nguyen, B Mizrahi, N Savion, and FD Kolodgie et al. Locally applied leptin induces regional aortic wall degeneration preceding aneurysm formation in apolipoprotein e-deficient mice Arterioscler Thromb Vasc Biol 33 2013 311 320
30. MW Manning, LA Cassis, and A Daugherty Differential effects of doxycycline, a broad-spectrum matrix metalloproteinase inhibitor, on angiotensin II-induced atherosclerosis and abdominal aortic aneurysms Arterioscler Thromb Vasc Biol 23 2003 483 488
31. R Pyo, JK Lee, JM Shipley, JA Curci, D Mao, and SJ Ziporin et al. Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms J Clin Invest 105 2000 1641 1649
32. A Yamawaki-Ogata, R Hashizume, M Satake, H Kaneko, S Mizutani, and T Moritan et al. A doxycycline loaded, controlled-release, biodegradable fiber for the treatment of aortic aneurysms Biomaterials 31 2010 9554 9564
33. BR Dodd, and RA Spence Doxycycline inhibition of abdominal aortic aneurysm growth: a systematic review of the literature Curr Vasc Pharmacol 9 2011 471 478
34. BT Baxter, MC Terrin, and RL Dalman Medical management of small abdominal aortic aneurysms Circulation 117 2008 1883 1889
35. Y Wang, S Krishna, PJ Walker, P Norman, and J Golledge Transforming growth factor-beta and abdominal aortic aneurysms Cardiovasc Pathol 22 2013 126 132
36. SD Gertz, LY Gavish, R Beeri, D Gilon, C Rubinstein, and Y Berlatzky et al. Abstract: arrest of progression of pre-induced abdominal aortic aneurysm in apolipoprotein E-deficient mice by low level laser phototherapy J Am Coll Cardiol 59 2012 E907
37. L Gavish, L Perez, and SD Gertz Low-level laser irradiation modulates matrix metalloproteinase activity and gene expression in porcine aortic smooth muscle cells Lasers Surg Med 38 2006 779 786
38. AP Medrado, AP Soares, ET Santos, SR Reis, and ZA Andrade Influence of laser photobiomodulation upon connective tissue remodeling during wound healing J Photochem Photobiol B 92 2008 144 152
39. V Prabhu, SB Rao, S Chandra, P Kumar, L Rao, and V Guddattu et al. Spectroscopic and histological evaluation of wound healing progression following low level laser therapy (LLLT) J Biophotonics 5 2012 168 184
40. L Gavish, LS Perez, P Reissman, and SD Gertz Irradiation with 780 nm diode laser attenuates inflammatory cytokines but upregulates nitric oxide in lipopolysaccharide-stimulated macrophages: implications for the prevention of aneurysm progression Lasers Surg Med 40 2008 371 378
41. RT Chow, MI Johnson, RA Lopes-Martins, and JM Bjordal Efficacy of low-level laser therapy in the management of neck pain: a systematic review and meta-analysis of randomised placebo or active-treatment controlled trials Lancet 374 2009 1897 1908
42. H Chung, T Dai, SK Sharma, YY Huang, JD Carroll, and MR Hamblin The nuts and bolts of low-level laser (light) therapy Ann Biomed Eng 40 2012 516 533
43. CS Enwemeka, JC Parker, DS Dowdy, EE Harkness, LE Sanford, and LD Woodruff The efficacy of low-power lasers in tissue repair and pain control: a meta-analysis study Photomed Laser Surg 22 2004 323 329
44. MC Leung, SC Lo, FK Siu, and KF So Treatment of experimentally induced transient cerebral ischemia with low energy laser inhibits nitric oxide synthase activity and up-regulates the expression of transforming growth factor-beta 1 Lasers Surg Med 31 2002 283 288
45. SM Safavi, B Kazemi, M Esmaeili, A Fallah, A Modarresi, and M Mir Effects of low-level He-Ne laser irradiation on the gene expression of IL-1beta, TNF-alpha, IFN-gamma, TGF-beta, bFGF, and PDGF in rat's gingiva Lasers Med Sci 23 2008 331 335
46. DL Rateri, DA Howatt, JJ Moorleghen, R Charnigo, LA Cassis, and A Daugherty Prolonged infusion of angiotensin II in apoE(-/-) mice promotes macrophage recruitment with continued expansion of abdominal aortic aneurysm Am J Pathol 179 2011 1542 1548
47. GM Grimshaw, JM Thompson, and JD Hamer Prevalence of abdominal aortic aneurysm associated with hypertension in an urban population J Med Screen 1 1994 226 228
48. LA Cassis, M Gupte, S Thayer, X Zhang, R Charnigo, and DA Howatt et al. ANG II infusion promotes abdominal aortic aneurysms independent of increased blood pressure in hypercholesterolemic mice Am J Physiol Heart Circ Physiol 296 2009 H1660 H1665
49. MA Gimbrone, and G Garcia-Cardena Vascular endothelium, hemodynamics, and the pathobiology of atherosclerosis Cardiovasc Pathol 22 2013 9 15
50. AM Malek, SL Alper, and S Izumo Hemodynamic shear stress and its role in atherosclerosis JAMA 282 1999 2035 2042
51. RM Nerem Vascular fluid mechanics, the arterial wall, and atherosclerosis J Biomech Eng 114 1992 274 282
52. O Traub, and BC Berk Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force Arterioscler Thromb Vasc Biol 18 1998 677 685
53. H Zakaria, AM Robertson, and CW Kerber A parametric model for studies of flow in arterial bifurcations Ann Biomed Eng 36 2008 1515 1530
54. MA Gimbrone, MI Cybulsky, N Kume, T Collins, and N Resnick Vascular endothelium. An integrator of pathophysiological stimuli in atherogenesis Ann N Y Acad Sci 748 1995 122 131 [discussion 31-2]
55. KB Pomerantz, AC Nicholson, and DP Hajjar Signal transduction in atherosclerosis: second messengers and regulation of cellular cholesterol trafficking Adv Exp Med Biol 369 1995 49 64
56. PF Davies, and SC Tripathi Mechanical stress mechanisms and the cell. An endothelial paradigm Circ Res 72 1993 239 245
57. B Trachet, M Renard, G De Santis, S Staelens, J De Backer, and L Antiga et al. An integrated framework to quantitatively link mouse-specific hemodynamics to aneurysm formation in angiotensin II-infused ApoE-/- mice Ann Biomed Eng 39 2011 2430 2444
58. CJ Goergen, J Azuma, KN Barr, L Magdefessel, DY Kallop, and A Gogineni et al. Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms Arterioscler Thromb Vasc Biol 31 2011 270 279
59. CJ Goergen, KN Barr, DT Huynh, JR Eastham-Anderson, G Choi, and M Hedehus et al. In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth J Magn Reson Imaging 32 2010 847 858
60. S Amirbekian, RC Long, MA Consolini, J Suo, NJ Willett, and SW Fielden et al. In vivo assessment of blood flow patterns in abdominal aorta of mice with MRI: implications for AAA localization Am J Physiol Heart Circ Physiol 297 2009 H1290 H1295
61. JE Moore, SE Maier, DN Ku, and P Boesiger Hemodynamics in the abdominal aorta: a comparison of in vitro and in vivo measurements J Appl Physiol 76 1994 1520 1527
62. G Ailawadi, JL Eliason, and GR Upchurch Current concepts in the pathogenesis of abdominal aortic aneurysm J Vasc Surg 38 2003 584 588
63. G Ailawadi, BS Knipp, G Lu, KJ Roelofs, JW Ford, and KK Hannawa et al. A nonintrinsic regional basis for increased infrarenal aortic MMP-9 expression and activity J Vasc Surg 37 2003 1059 1066
64. SD Gertz, C Rubinstein, A Bulut, Y Berlatzky, R Beeri, and D Gilon et al. Hemodynamic forces in the pathogenesis of abdominal aortic aneurysm A Kimchi, Recent Advances in Cardiovascular Diseases: Proceedings of the 16th World Congress on Heart Disease (International Academy of Cardiology). Vancouver, CA. July 23-26, 2011 2012 Medimond 95 102
65. R Holenstein, and DN Ku Reverse flow in the major infrarenal vessels-a capacitive phenomenon Biorheology 25 1988 835 842
66. CJ Hartley, AK Reddy, S Madala, B Martin-McNulty, R Vergona, and ME Sullivan et al. Hemodynamic changes in apolipoprotein E-knockout mice Am J Physiol Heart Circ Physiol 279 2000 H2326 H2334