Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T04:34:01.089Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of Aortic Collagen Fiber Angle Distribution in Mouse Models of Atherosclerosis Using Second-Harmonic Generation (SHG) Microscopy

Published online by Cambridge University Press:  07 January 2016

Shana R. Watson ,
Piaomu Liu ,
Edsel A. Peña ,
Michael A. Sutton ,
John F. Eberth  and
Susan M. Lessner
Shana R. Watson
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Piaomu Liu
Affiliation:
Department of Statistics, University of South Carolina, Columbia, SC 29208, USA
Edsel A. Peña
Affiliation:
Department of Statistics, University of South Carolina, Columbia, SC 29208, USA
Michael A. Sutton
Affiliation:
Department of Mechanical Engineering, University of South Carolina, Columbia, SC 29208, USA
John F. Eberth
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Susan M. Lessner*
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC 29209, USA
*
*Corresponding author. Susan.Lessner@uscmed.sc.edu
Get access

Abstract

Characterization of collagen fiber angle distribution throughout the blood vessel wall provides insight into the mechanical behavior of healthy and diseased arteries and their capacity to remodel. Atherosclerotic plaque contributes to the overall mechanical behavior, yet little is known experimentally about how collagen fiber orientation is influenced by atherogenesis. We hypothesized that atherosclerotic lesion development, and the factors contributing to lesion development, leads to a shift in collagen fiber angles within the aorta. Second-harmonic generation microscopy was used to visualize the three-dimensional organization of collagen throughout the aortic wall and to examine structural differences in mice maintained on high-fat Western diet versus age-matched chow diet mice in a model of atherosclerosis. Image analysis was performed on thoracic and abdominal sections of the aorta from each mouse to determine fiber orientation, with the circumferential (0°) and blood flow directions (axial ±90°) as the two reference points. All measurements were used in a multiple regression analysis to determine the factors having a significant influence on mean collagen fiber angle. We found that mean absolute angle of collagen fibers is 43° lower in Western diet mice compared with chow diet mice. Mice on a chow diet have a mean collagen fiber angle of ±63°, whereas mice on a Western diet have a more circumferential fiber orientation (~20°). This apparent shift in absolute angle coincides with the development of extensive aortic atherosclerosis, suggesting that atherosclerotic factors contribute to collagen fiber angle orientation.

Keywords

atherosclerosissecond-harmonic generation microscopycollagen fibersarterial tissue
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 1 , February 2016 , pp. 55 - 62
Copyright
© Microscopy Society of America 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, J.J. (2004). The pathobiology of aortic aneurysms. J Surg Res 117, 163–175.CrossRefGoogle ScholarPubMed
Anderson, G.F. & Chu, E. (2007). Expanding priorities—Confronting chronic disease in countries with low income. N Eng J Med 356, 209–211.CrossRefGoogle ScholarPubMed
Arifler, D., Pavlova, I., Gillenwater, A. & Richards-Kortum, R. (2007). Light scattering from collagen fiber networks: Micro-optical properties of normal and neoplastic stroma. Biophys J 92, 3260–3274.CrossRefGoogle ScholarPubMed
Avril, S., Badel, P., Gabr, M., Sutton, M.A., & Lessner, S.M. (2013). Biomechanics of porcine renal arteries and role of axial stretch. J Biomech Eng 135, 081007-1-10.CrossRefGoogle ScholarPubMed
Badel, P., Avril, S., Lessner, S. & Sutton, M. (2012). Mechanical identification of layer-specific properties of mouse carotid arteries using 3D-DIC and a hyperelastic anisotropic constitutive model. Comput Met Biomech Biomed Engin 15, 37–48.CrossRefGoogle Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015). Fitting linear mixed-effects models using lme4. J Stat Softw 67, 1–51.CrossRefGoogle Scholar
Canham, P.B., Finlay, H. & Tong, S.Y. ( 1996). Stereological analysis of the layered collagen of human intracranial aneurysms. J Microsc 183, 170–180.CrossRefGoogle Scholar
Collins, M.J., Bersi, M., Wilson, E. & Humphrey, J.D. (2011). Mechanical properties of suprarenal and infrarenal abdominal aorta: Implications for mouse models of aneurysms. Med Engin Phys 33, 1262–1269.CrossRefGoogle ScholarPubMed
Collins, M.J., Eberth, J., Wilson, E. & Humphrey, J.D. (2012). Acute mechanical effects of elastase on the intrarenal mouse aorta: Implications for models of aneurysms. J Biomech 45, 660–665.CrossRefGoogle Scholar
Doras, C., Taupier, G., Barsella, A., Mager, L., Boeglin, A., Bulou, H., Bousquet, P. & Dorkenoo, K.D. (2011). Polarization state studies in second harmonic generation signals to trace atherosclerosis lesions. Opt Exp 19, 15062–15068.CrossRefGoogle ScholarPubMed
Driessen, N.J.B., Cox, M.A.J., Bouten, C.V.C. & Baaijens, F.P.T. (2008). Remodelling of the angular collagen fiber distribution in cardiovascular tissues. Biomech Model Mechanobiol 7, 93–103.CrossRefGoogle ScholarPubMed
Finlay, H.M., McCullough, L. & Canham, P.B. (1995). Three-dimensional collagen organization of human brain arteries at different transmural pressures. J Vasc Res 32, 301–312.CrossRefGoogle ScholarPubMed
Galis, Z.S. & Khatri, J.J. (2002). Matrix metalloproteinases in vascular remodeling and atherogenesis: The good, the bad, and the ugly. Circ Res 90, 251–262.CrossRefGoogle ScholarPubMed
Gasser, T.C., Ogden, R.W. & Holzapfel, G.A. (2006). Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface 3, 15–35.CrossRefGoogle ScholarPubMed
Guo, X. & Kassab, G.S. (2003). Variation of mechanical properties along the length of the aorta in C57Bl/6 mice. Am J Physiol Heart Circ Physiol 285, H2614–H2622.CrossRefGoogle ScholarPubMed
Hellenthal, F.A.M.V.I., Geenen, I.L.A., Teijink, J.A.W., Heeneman, S. & Schurink, G.W.H. (2009). Histological features of human abdominal aortic aneurysm are not related to clinical characteristics. Cardiovasc Pathol 18, 286–293.CrossRefGoogle Scholar
Hill, M.R., Duan, X., Gibson, G.A., Watkins, S. & Robertson, A.M. (2012). A theoretical and non-destructive experimental approach for direct inclusion of measured collagen orientation and recruitment into mechanical models of the artery wall. J Biomech 45, 762–771.CrossRefGoogle ScholarPubMed
Holzapfel, G.A. (2001). Biomechanics of Soft Tissue. In The Handbook of Materials Behavior Models, Vol III, Multiphysics Behaviors, Chapter 10, Composite Media, Biomaterials, Lemaitre, J. (Ed.), pp. 1049--1063. Boston, MA: Academic Press.Google Scholar
Holzapfel, G.A. (2008). Collagen in arterial walls: Biomechanical aspects. In Collagen: Structure and Mechanics, Fratzl, P. (Ed.), pp. 285–324. Boston, MA: Springer US. Biomechanics.Google Scholar
Holzapfel, G.A., Gasser, T.C. & Stadler, M. (2002). A structural model for the viscoelastic behavior of arterial walls: Continuum formulation and finite element analysis. Eur J Mech A 21, 441–463.CrossRefGoogle Scholar
Holzapfel, G.A., Niestrawska, J.A., Ogden, R.W., Reinisch, A.J. & Schriefl, A.J. (2015). Modelling non-symmetric collagen fibre dispersion in arterial walls. J R Soc Interf 12, 20150188.CrossRefGoogle ScholarPubMed
Holzapfel, G.A. & Ogden, R.W. (2010). Modelling the layer-specific three-dimensional residual stresses in arteries, with an application to the human aorta. J R Soc Interf 7, 787–799.CrossRefGoogle Scholar
Kuzuya, M. & Iguchi, A. (2003). Role of matrix metalloproteinases in vascular remodeling. J Atheroscler Thromb 10, 275–282.CrossRefGoogle ScholarPubMed
Levene, C.I. & Poole, J.C. ( 1962). The collagen content of the normal and atherosclerotic human aortic intima. Br J Exp Pathol 43, 469–471.Google Scholar
Li, D. & Robertson, A.M. (2009). A structural multi-mechanism damage model for cerebral arterial tissue. J Biomech Engin 131, 101013.CrossRefGoogle ScholarPubMed
Liu, H., Shao, Y., Ma, Z., Ye, T., Borg, T. & Gao, B. (2011). Myofibrillogenesis in live neonatal cardiomyocytes observed with hybrid two-photon excitation fluorescence-second harmonic generation microscopy. J Biomed Opt 12, 126012.CrossRefGoogle Scholar
Liu, H., Shao, Y., Qin, W., Runyan, R.B., Xu, M., Ma, Z., Borg, T.K., Markwald, R. & Gao, B.Z. (2013). Myosin filament assembly onto myofibrils in live neonatal cardiomyocytes observed by TPEF-SHG microscopy. Cardiovasc Res 97, 262–270.CrossRefGoogle ScholarPubMed
Liu, S., Bae, Y., Klein, E., Hawthorne, E.A., Xu, T. & Assoian, R.K. ( 2012). Abstract 15589: Matrix metalloproteinase-12 controls arterial stiffness in vascular remodeling. Circulation 126, A15589.Google Scholar
Luttun, A., Lutgens, E., Manderveld, A., Maris, K., Collen, D., Carmeliet, P. & Moons, L. (2004). Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth. Circulation 109, 1408–1414.CrossRefGoogle ScholarPubMed
Nakashima, Y., Plump, A.S., Raines, E.W., Breslow, J.L. & Ross, R. (1994). ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb Vasc Biol 14, 133–140. Available at http://atvb.ahajournals.org/content/14/1/133.short (retrieved February 20, 2015).CrossRefGoogle ScholarPubMed
NIH and NHLBI (2012). Disease statistics. In NHLBI Fact Book, Fisc. Year 2012, chapter 4, pp. 33–52. Bethesda, MD: National Institues of Health. Available at www.nhlbi.nih.gov/about/factbook/chapter4.htm#gr36 (retrieved February 20, 2015).Google Scholar
Raffetto, J.D. & Khalil, R.A. (2008). Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 75, 346–359.CrossRefGoogle ScholarPubMed
Rhodin, J. (1980). Architecture of the vessel wall. In Handbook of Physiology, The Cardiovascular System, Vascular Smooth Muscle Vessel Wall, 2nd ed. Sparks HV Jr, Bohr DF, Somlyo AD, Geiger SR (Eds.), pp. 644–673. Bethesda, MD: American Physiological Society.Google Scholar
Schriefl, A.J. (2012). Quantification of collagen fiber morphologies in human arterial walls: Novel experimental methodologies yielding 2D and 3D structural data. Doctoral Dissertation, Graz University of Technology.Google Scholar
Schriefl, A.J., Reinisch, A.J., Sankaran, S., Pierce, D.M. & Holzapfel, G.A. (2012). Quantitative assessment of collagen fibre orientations from two-dimensional images of soft biological tissues. J R Soc Interf 9, 3081–3093.CrossRefGoogle ScholarPubMed
Schriefl, A.J., Zeindlinger, G., Pierce, D.M., Regitnig, P. & Holzapfel, G.A. (2011). Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries. J R Soc Interf 9, 1275–1286.CrossRefGoogle ScholarPubMed
Tang, J., Zhang, Y., Zhang, M.-B., Li, Y.-M., Fei, X. & Song, Z.-G. (2014). Tissue elasticity displayed by elastography and its correlation with the characteristics of collagen type I and type III in prostatic stroma. Asian J Androl 16, 305–308.CrossRefGoogle ScholarPubMed
Tunstall-Pedoe, H. ( 2006). Preventing chronic diseases. A vital investment: WHO global report. Geneva: World Health Organization, 2005, pp. 200. CHF 30.00. ISBN 92 4 1563001. Int J Epidemiol 35, 1107.CrossRefGoogle Scholar
Voorhees, A.P. & Han, H.C. (2014). A model to determine the effect of collagen fiber alignment on heart function post myocardial infarction. Theor Biol Med Model 11, 6.CrossRefGoogle Scholar
Wicker, B.K., Hutchens, H.P., Wu, Q., Yeh, A.T. & Humphrey, J.D. (2008). Normal basilar artery structure and biaxial mechanical behaviour. Comput Methods Biomech Biomed Engin 11, 539–551.CrossRefGoogle ScholarPubMed
Williams, R.M., Zipfel, W.R. & Webb, W.W. (2005). Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 88, 1377–1386.CrossRefGoogle ScholarPubMed
Wolinsky, H. & Glagov, S. (1969). Comparison of abdominal and thoracic aortic medial structure in mammals. Circ Res 25, 677–686.CrossRefGoogle ScholarPubMed
Xu, C., Zarins, C.K. & Glagov, S. (2001). Aneurysmal and occlusive atherosclerosis of the human abdominal aorta. J Vasc Surg 33, 91–96.CrossRefGoogle ScholarPubMed
Zipfel, W.R., Williams, R.M., Christie, R., Nikitin, A.Y., Hyman, B.T. & Webb, W.W. (2003). Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci U S A 100, 7075–7080.CrossRefGoogle ScholarPubMed