Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta

Jungsil Kim, Marius Catalin Staiculescu, Austin J. Cocciolone, Hiromi Yanagisawa, Robert P. Mecham, Jessica E. Wagenseil

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

In the large arteries, it is believed that elastin provides the resistance to stretch at low pressure, while collagen provides the resistance to stretch at high pressure. It is also thought that elastin is responsible for the low energy loss observed with cyclic loading. These tenets are supported through experiments that alter component amounts through protease digestion, vessel remodeling, normal growth, or in different artery types. Genetic engineering provides the opportunity to revisit these tenets through the loss of expression of specific wall components. We used newborn mice lacking elastin (Eln−/−) or two key proteins (lysyl oxidase, Lox−/−, or fibulin-4, Fbln4−/−) that are necessary for the assembly of mechanically-functional elastic fibers to investigate the contributions of elastic fibers to large artery mechanics. We determined component content and organization and quantified the nonlinear and viscoelastic mechanical behavior of Eln−/−, Lox−/−, and Fbln4−/− ascending aorta and their respective controls. We confirmed that the lack of elastin, fibulin-4, or lysyl oxidase leads to absent or highly fragmented elastic fibers in the aortic wall and a 56–97% decrease in crosslinked elastin amounts. We found that the resistance to stretch at low pressure is decreased only in Eln−/− aorta, confirming the role of elastin in the nonlinear mechanical behavior of the aortic wall. Dissipated energy with cyclic loading and unloading is increased 53–387% in Eln−/−, Lox−/−, and Fbln4−/− aorta, indicating that not only elastin, but properly assembled and crosslinked elastic fibers, are necessary for low energy loss in the aorta.

Original languageEnglish (US)
Pages (from-to)199-207
Number of pages9
JournalJournal of Biomechanics
Volume61
DOIs
StatePublished - Aug 16 2017

Fingerprint

Elastin
Elastic Tissue
Aorta
Energy dissipation
Fibers
Protein-Lysine 6-Oxidase
Arteries
Pressure
Genetic engineering
Genetic Engineering
Mechanics
Unloading
Collagen
Digestion
Peptide Hydrolases
Proteins

Keywords

  • Aorta
  • Collagen
  • Elastin
  • Extracellular matrix
  • Fibulin-4
  • Lysyl oxidase
  • Vascular mechanics

ASJC Scopus subject areas

  • Biophysics
  • Orthopedics and Sports Medicine
  • Biomedical Engineering
  • Rehabilitation

Cite this

Kim, J., Staiculescu, M. C., Cocciolone, A. J., Yanagisawa, H., Mecham, R. P., & Wagenseil, J. E. (2017). Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta. Journal of Biomechanics, 61, 199-207. https://doi.org/10.1016/j.jbiomech.2017.07.011

Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta. / Kim, Jungsil; Staiculescu, Marius Catalin; Cocciolone, Austin J.; Yanagisawa, Hiromi; Mecham, Robert P.; Wagenseil, Jessica E.

In: Journal of Biomechanics, Vol. 61, 16.08.2017, p. 199-207.

Research output: Contribution to journalArticle

Kim, J, Staiculescu, MC, Cocciolone, AJ, Yanagisawa, H, Mecham, RP & Wagenseil, JE 2017, 'Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta', Journal of Biomechanics, vol. 61, pp. 199-207. https://doi.org/10.1016/j.jbiomech.2017.07.011
Kim J, Staiculescu MC, Cocciolone AJ, Yanagisawa H, Mecham RP, Wagenseil JE. Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta. Journal of Biomechanics. 2017 Aug 16;61:199-207. https://doi.org/10.1016/j.jbiomech.2017.07.011
Kim, Jungsil ; Staiculescu, Marius Catalin ; Cocciolone, Austin J. ; Yanagisawa, Hiromi ; Mecham, Robert P. ; Wagenseil, Jessica E. / Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta. In: Journal of Biomechanics. 2017 ; Vol. 61. pp. 199-207.
@article{1267b72225fe475aaeb48020df948e95,
title = "Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta",
abstract = "In the large arteries, it is believed that elastin provides the resistance to stretch at low pressure, while collagen provides the resistance to stretch at high pressure. It is also thought that elastin is responsible for the low energy loss observed with cyclic loading. These tenets are supported through experiments that alter component amounts through protease digestion, vessel remodeling, normal growth, or in different artery types. Genetic engineering provides the opportunity to revisit these tenets through the loss of expression of specific wall components. We used newborn mice lacking elastin (Eln−/−) or two key proteins (lysyl oxidase, Lox−/−, or fibulin-4, Fbln4−/−) that are necessary for the assembly of mechanically-functional elastic fibers to investigate the contributions of elastic fibers to large artery mechanics. We determined component content and organization and quantified the nonlinear and viscoelastic mechanical behavior of Eln−/−, Lox−/−, and Fbln4−/− ascending aorta and their respective controls. We confirmed that the lack of elastin, fibulin-4, or lysyl oxidase leads to absent or highly fragmented elastic fibers in the aortic wall and a 56–97{\%} decrease in crosslinked elastin amounts. We found that the resistance to stretch at low pressure is decreased only in Eln−/− aorta, confirming the role of elastin in the nonlinear mechanical behavior of the aortic wall. Dissipated energy with cyclic loading and unloading is increased 53–387{\%} in Eln−/−, Lox−/−, and Fbln4−/− aorta, indicating that not only elastin, but properly assembled and crosslinked elastic fibers, are necessary for low energy loss in the aorta.",
keywords = "Aorta, Collagen, Elastin, Extracellular matrix, Fibulin-4, Lysyl oxidase, Vascular mechanics",
author = "Jungsil Kim and Staiculescu, {Marius Catalin} and Cocciolone, {Austin J.} and Hiromi Yanagisawa and Mecham, {Robert P.} and Wagenseil, {Jessica E.}",
year = "2017",
month = "8",
day = "16",
doi = "10.1016/j.jbiomech.2017.07.011",
language = "English (US)",
volume = "61",
pages = "199--207",
journal = "Journal of Biomechanics",
issn = "0021-9290",
publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Crosslinked elastic fibers are necessary for low energy loss in the ascending aorta

AU - Kim, Jungsil

AU - Staiculescu, Marius Catalin

AU - Cocciolone, Austin J.

AU - Yanagisawa, Hiromi

AU - Mecham, Robert P.

AU - Wagenseil, Jessica E.

PY - 2017/8/16

Y1 - 2017/8/16

N2 - In the large arteries, it is believed that elastin provides the resistance to stretch at low pressure, while collagen provides the resistance to stretch at high pressure. It is also thought that elastin is responsible for the low energy loss observed with cyclic loading. These tenets are supported through experiments that alter component amounts through protease digestion, vessel remodeling, normal growth, or in different artery types. Genetic engineering provides the opportunity to revisit these tenets through the loss of expression of specific wall components. We used newborn mice lacking elastin (Eln−/−) or two key proteins (lysyl oxidase, Lox−/−, or fibulin-4, Fbln4−/−) that are necessary for the assembly of mechanically-functional elastic fibers to investigate the contributions of elastic fibers to large artery mechanics. We determined component content and organization and quantified the nonlinear and viscoelastic mechanical behavior of Eln−/−, Lox−/−, and Fbln4−/− ascending aorta and their respective controls. We confirmed that the lack of elastin, fibulin-4, or lysyl oxidase leads to absent or highly fragmented elastic fibers in the aortic wall and a 56–97% decrease in crosslinked elastin amounts. We found that the resistance to stretch at low pressure is decreased only in Eln−/− aorta, confirming the role of elastin in the nonlinear mechanical behavior of the aortic wall. Dissipated energy with cyclic loading and unloading is increased 53–387% in Eln−/−, Lox−/−, and Fbln4−/− aorta, indicating that not only elastin, but properly assembled and crosslinked elastic fibers, are necessary for low energy loss in the aorta.

AB - In the large arteries, it is believed that elastin provides the resistance to stretch at low pressure, while collagen provides the resistance to stretch at high pressure. It is also thought that elastin is responsible for the low energy loss observed with cyclic loading. These tenets are supported through experiments that alter component amounts through protease digestion, vessel remodeling, normal growth, or in different artery types. Genetic engineering provides the opportunity to revisit these tenets through the loss of expression of specific wall components. We used newborn mice lacking elastin (Eln−/−) or two key proteins (lysyl oxidase, Lox−/−, or fibulin-4, Fbln4−/−) that are necessary for the assembly of mechanically-functional elastic fibers to investigate the contributions of elastic fibers to large artery mechanics. We determined component content and organization and quantified the nonlinear and viscoelastic mechanical behavior of Eln−/−, Lox−/−, and Fbln4−/− ascending aorta and their respective controls. We confirmed that the lack of elastin, fibulin-4, or lysyl oxidase leads to absent or highly fragmented elastic fibers in the aortic wall and a 56–97% decrease in crosslinked elastin amounts. We found that the resistance to stretch at low pressure is decreased only in Eln−/− aorta, confirming the role of elastin in the nonlinear mechanical behavior of the aortic wall. Dissipated energy with cyclic loading and unloading is increased 53–387% in Eln−/−, Lox−/−, and Fbln4−/− aorta, indicating that not only elastin, but properly assembled and crosslinked elastic fibers, are necessary for low energy loss in the aorta.

KW - Aorta

KW - Collagen

KW - Elastin

KW - Extracellular matrix

KW - Fibulin-4

KW - Lysyl oxidase

KW - Vascular mechanics

UR - http://www.scopus.com/inward/record.url?scp=85026526393&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85026526393&partnerID=8YFLogxK

U2 - 10.1016/j.jbiomech.2017.07.011

DO - 10.1016/j.jbiomech.2017.07.011

M3 - Article

VL - 61

SP - 199

EP - 207

JO - Journal of Biomechanics

JF - Journal of Biomechanics

SN - 0021-9290

ER -