Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome
- 28 December 2009
- journal article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 107 (2), 862-865
- https://doi.org/10.1073/pnas.0910312107
Abstract
An aneurysm of the aorta is a common pathology characterized by segmental weakening of the artery. Although it is generally accepted that the vessel-wall weakening is caused by an impaired collagen metabolism, a clear association has been demonstrated only for rare syndromes such as the vascular type Ehlers-Danlos syndrome. Here we show that vessel-wall failure in growing aneurysms of patients who have aortic abdominal aneurysm (AAA) or Marfan syndrome is not related to a collagen defect at the molecular level. On the contrary our findings indicate similar (Marfan) or even higher collagen concentrations (AAA) and increased collagen cross-linking in the aneurysms. Using 3D confocal imaging we show that the two conditions are associated with profound defects in collagen microarchitecture. Reconstructions of normal vessel wall show that adventitial collagen fibers are organized in a loose braiding of collagen ribbons. These ribbons encage the vessel, allowing the vessel to dilate easily but preventing overstretching. AAA and aneurysms in Marfan syndrome show dramatically altered collagen architectures with loss of the collagen knitting. Evaluations of the functional characteristics by atomic force microscopy showed that the wall has lost its ability to stretch easily and revealed a second defect: although vascular collagen in normal aortic wall behaves as a coherent network, in AAA and Marfan tissues it does not. As result, mechanical forces loaded on individual fibers are not distributed over the tissue. These studies demonstrate that the mechanical properties of tissue are strongly influenced by collagen microarchitecture and that perturbations in the collagen networks may lead to mechanical failure.Keywords
This publication has 27 references indexed in Scilit:
- Candidate Cell and Matrix Interaction Domains on the Collagen Fibril, the Predominant Protein of VertebratesJournal of Biological Chemistry, 2008
- Mechanical Stresses in Abdominal Aortic Aneurysms: Influence of Diameter, Asymmetry, and Material AnisotropyJournal of Biomechanical Engineering, 2008
- Variation in the histopathological features of patients with ascending aortic aneurysms: a study of 111 surgically excised casesJournal of Clinical Pathology, 2007
- Atomic force microscopy in biology: technology and techniquesBiotechnic & Histochemistry, 2006
- Biomechanical Determinants of Abdominal Aortic Aneurysm RuptureArteriosclerosis, Thrombosis, and Vascular Biology, 2005
- Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fractureNature Materials, 2005
- Lysyl oxidase: Properties, specificity, and biological roles inside and outside of the cellJournal of Cellular Biochemistry, 2002
- The Biology of Fetal Wound HealingPlastic and Reconstructive Surgery, 1991
- Collagen types and matrix protein content in human abdominal aortic aneurysmsJournal of Vascular Surgery, 1989
- Collagen in abdominal aortic aneurysm: Typing, content, and degradationJournal of Vascular Surgery, 1987