Getting to the heart of cardiac remodeling; how collagen subtypes may contribute to phenotype

P Collier, C J Watson, M H van Es, D Phelan, C McGorrian, M Tolan, M T Ledwidge, K M McDonald, J A Baugh

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Abstract

The objective of this study was to investigate the nature and biomechanical properties of collagen fibers within the human myocardium. Targeting cardiac interstitial abnormalities will likely become a major focus of future preventative strategies with regard to the management of cardiac dysfunction. Current knowledge regarding the component structures of myocardial collagen networks is limited, further delineation of which will require application of more innovative technologies. We applied a novel methodology involving combined confocal laser scanning and atomic force microscopy to investigate myocardial collagen within ex-vivo right atrial tissue from 10 patients undergoing elective coronary bypass surgery. Immuno-fluorescent co-staining revealed discrete collagen I and III fibers. During single fiber deformation, overall median values of stiffness recorded in collagen III were 37±16% lower than in collagen I [p<0.001]. On fiber retraction, collagen I exhibited greater degrees of elastic recoil [p<0.001; relative percentage increase in elastic recoil 7±3%] and less energy dissipation than collagen III [p<0.001; relative percentage increase in work recovered 7±2%]. In atrial biopsies taken from patients in permanent atrial fibrillation (n=5) versus sinus rhythm (n=5), stiffness of both collagen fiber subtypes was augmented (p<0.008). Myocardial fibrillar collagen fibers organize in a discrete manner and possess distinct biomechanical differences; specifically, collagen I fibers exhibit relatively higher stiffness, contrasting with higher susceptibility to plastic deformation and less energy efficiency on deformation with collagen III fibers. Augmented stiffness of both collagen fiber subtypes in tissue samples from patients with atrial fibrillation compared to those in sinus rhythm are consistent with recent published findings of increased collagen cross-linking in this setting.

Original languageEnglish
Pages (from-to)148-53
Number of pages6
JournalJournal of Molecular and Cellular Cardiology
Volume52
Issue number1
DOIs
Publication statusPublished - Jan 2012

Keywords

  • Aged
  • Atrial Fibrillation
  • Collagen Type I
  • Collagen Type III
  • Female
  • Humans
  • Male
  • Microscopy, Atomic Force
  • Middle Aged
  • Phenotype
  • Ventricular Remodeling

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    Collier, P., Watson, C. J., van Es, M. H., Phelan, D., McGorrian, C., Tolan, M., Ledwidge, M. T., McDonald, K. M., & Baugh, J. A. (2012). Getting to the heart of cardiac remodeling; how collagen subtypes may contribute to phenotype. Journal of Molecular and Cellular Cardiology, 52(1), 148-53. https://doi.org/10.1016/j.yjmcc.2011.10.002