AccScience Publishing / GTM / Volume 2 / Issue 2 / DOI: 10.36922/gtm.0897
Submit to GTM
Cite this article
91
Download
1199
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
ORIGINAL RESEARCH ARTICLE

Ultraviolet-induced mechanical augmentation of the degraded porcine aortic adventitia: Its significance for preventing aneurysmal rupture

Traian V. Chirila1,2,3,4,5* ,  Shuko Suzuki1
Show Less
1 Queensland Eye Institute, South Brisbane, Queensland, Australia
2 School of Chemistry and Physics, Queensland University of Technology, Brisbane, Queensland, Australia
3 Australian Institute of Bioengineering and Nanotechnology, University of Queensland, St Lucia, Queensland, Australia
4 School of Molecular Sciences, University of Western Australia, Crawley, Western Australia, Australia
5 Faculty of Medicine, George E. Palade University of Medicine, Pharmacy, Sciences and Technology, Târgu Mureş, Romania
Global Translational Medicine 2023, 2(2), 0897 https://doi.org/10.36922/gtm.0897
Submitted: 4 May 2023 | Accepted: 25 June 2023 | Published: 5 July 2023
© 2023 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

In the previous studies, we have shown that the tunica adventitia of porcine abdominal aorta could be mechanically reinforced by irradiating it with ultraviolet A (UV-A) rays to promote the photocrosslinking of constitutive collagen, and we have proposed the method as a procedure to prevent or delay abdominal aortic aneurysm (AAA) ruptures. We have also demonstrated that UV irradiation-induced mechanical augmentation despite the degradation of the adventitia through collagenolysis in vitro. Considering that elastolysis is equally a relevant event in the pathogenesis of AAA, the degradation of elastin was also investigated in the present study. A total of 50 porcine aortas were used in the study. All processed samples were evaluated in a mechanical tester before and after degradation and/or irradiation. The adventitial layer was isolated and subjected to elastase for either 1 – 48 h. We found that both elastin and collagen were digested by elastase, with the former being completely digested after 48 h. The samples degraded for 1 h were subsequently irradiated with UV-A (365 nm) in the presence of riboflavin as a photoinitiator, a process that induced an enhancement of the strength and stiffness of the tissue. This is an indication that a partly degenerated aortic wall, like that in an aneurysmal region, can be reinforced mechanically by UV irradiation, possibly to the extent of delaying, or preventing altogether, the wall’s rupture. It appears important to irradiate the wall as early as possible.

Keywords
Aortic aneurysms
Tunica adventitia
Photocrosslinking
Elastolysis
Vascular biomechanics
Funding
None.
Conflict of interest
The authors declare that they have no competing interests that are relevant to the content, authorship, or publication of this article.
References
  1. Thompson RW, Geraghty PJ, Lee JK, 2002, Abdominal aortic aneurysms: Basic mechanisms and clinical implications. Curr Probl Surg, 39: 110–230. https://doi.org/10.1067/msg.2002.121421

 

  1. Choke E, Cockerill G, Wilson WRW, et al., 2005, A review of biological factors implicated in abdominal aortic aneurysm rupture. Eur J Vasc Endovasc Surg, 30: 227–244. https://doi.org/10.1016/j.ejvs.2005.03.009

 

  1. Lu H, Rateri DL, Bruemmer D, et al., 2012, Novel mechanisms of abdominal aortic aneurysms. Curr Atheroscler Rep, 14: 402–412. https://doi.org/10.1007/s11883-012-0271-y

 

  1. Kuivaniemi H, Ryer EJ, Elmore JR, et al., 2015, Understanding the pathogenesis of abdominal aortic aneurysms. Expert Rev Cardiovasc Ther, 13: 975–987. https://doi.org/10.1586/14779072.2015.1074861

 

  1. Nordon IM, (Thompson M, ed) 2016, Abdominal aortic aneurysms: Fundamental concepts, in Oxford Textbook of Vascular Surgery, Oxford University Press, Oxford, 469–484.

 

  1. Jana S, Hu M, Shen M, et al., 2019, Extracellular matrix, regional heterogeneity of the aorta, and aortic aneurysm. Exp Mol Med, 51: 160. https://doi.org/10.1038/s12276-019-0286-3

 

  1. Golledge J, 2019, Abdominal aortic aneurysm: Update on pathogenesis and medical treatments. Nat Rev Cardiol, 16: 225–242. https://doi.org/10.1038/s41569-018-0114-9

 

  1. Liu B, Granville DJ, Golledge J, et al., 2020, Pathogenic mechanisms and the potential of drug therapies for aortic aneurysm. Am J Physiol Heart Circ Physiol, 318: H652–H670. https://doi.org/10.1152/ajpheart.00621.2019

 

  1. Lederle FA, Kyriakides TC, Stroupe KT, et al., 2019, Open versus endovascular repair of abdominal aortic aneurysm. N Engl J Med, 380: 2126–2135. https://doi.org/10.1056/NEJMoa1715955

 

  1. Swerdlow NJ, Wu WW, Schermerhorn ML, 2019, Open and endovascular management of aortic aneurysms. Circ Res, 124: 647–661. https://doi.org/10.1161/CIRCRESAHA.118.313186

 

  1. Wanhainen A, Verzini F, Van Herzeele I, et al., 2019, European Society for Vascular Surgery (ESVS) 2019 Clinical practice guidelines on the management of abdominal aorto-iliac artery aneurysms. Eur J Vasc Endovasc Surg, 57: 8–93. https://doi.org/10.1016/j.ejvs.2018.09.020

 

  1. Gaar J, Naffa R, Brimble M, 2020, Enzymatic and non-enzymatic crosslinks found in collagen and elastin and their chemical synthesis. Org Chem Front, 7: 2789–2814. https://doi.org/10.1039/D0QO00624F

 

  1. Fuentes-Lemus E, Hägglund P, López-Alarcón C, et al., 2022, Oxidative crosslinking of peptides and proteins: Mechanisms of formation, detection, characterization and quantification. Molecules, 27: 15. https://doi.org/10.3390/molecules27010015

 

  1. Khor E, 1996, Methods for the treatment of collagenous tissues for bioprostheses. Biomaterials, 18: 95–105. https://doi.org/10.1016/s0142-9612(96)00106-8

 

  1. Paul RG, Bailey AJ, 2003, Chemical stabilization of collagen as a biomimetic. Sci World J, 3: 138–155. https://doi.org/10.1100/tsw.2003.13

 

  1. Lamp A, Kaltschmitt M, Dethloff J, 2022, Options to improve the mechanical properties of protein-based materials. Molecules, 27: 446. https://doi.org/10.3390/molecules27020446

 

  1. Sorkin N, Varssano D, 2014, Corneal collagen crosslinking: A systematic review. Ophthalmologica, 332: 10–27. https://doi.org/10.1159/000357979

 

  1. Randleman JB, Khandelwal SS, Hafezi F, 2015, Corneal cross-linking. Surv Ophthalmol, 60: 509–523. https://doi.org/10.1016/j.survophthal.2015.04.002

 

  1. Smith TM, Suzuki S, Cronin BG, et al., 2018, Photochemically induced crosslinking of tarsal collagen as a treatment for eyelid laxity: Assessing potentiality in animal tissue. Ophthal Plast Reconstr Surg, 34: 477–482. https://doi.org/10.1097/IOP.0000000000001063

 

  1. Smith TM, Suzuki S, Sabat N, et al., 2019, Further investigations on the crosslinking of tarsal collagen as a treatment for eyelid laxity: Optimizing the procedure in animal tissue. Ophthal Plast Reconstr Surg, 35: 600–603. https://doi.org/10.1097/IOP.0000000000001413

 

  1. Chirila TV, Suzuki S, 2022, Photocrosslinking of adventitial collagen in the porcine abdominal aorta: A preliminary approach to a strategy for prevention of aneurysmal rupture. Designs, 6: 5. https://doi.org/10.3390/designs6010005

 

  1. Chirila TV, Suzuki S, 2023, Effects of ultraviolet-A radiation on enzymatically degraded tunica adventitia of the porcine abdominal aorta. Biomed Mater Dev. https://doi.org/10.1007/s44174-023-00080-1

 

  1. Dobrin PB, 1999, Animal models of aneurysms. Ann Vasc Surg, 13: 641–648. https://doi.org/10.1007/s100169900315

 

  1. Daugherty A, Cassis LA, 2004, Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol, 24: 429–434. https://doi.org/10.1161/01.ATV.0000118013.72016.ea

 

  1. Trollope A, Moxon JV, Moran CS, et al., 2011, Animal models of abdominal aortic aneurysm and their role in furthering management of human disease. Cardiovasc Pathol, 20: 114–123. https://doi.org/10.1016/j.carpath.2010.01.001

 

  1. Dobrin PB, Canfield TR, 1984, Elastase, collagenase, and the biaxial elastic properties of dog carotid artery. Am J Physiol Heart Circ Physiol, 247: H124–H131. https://doi.org/10.1152/ajpheart.1984.247.1.H124

 

  1. Dobrin PB, Baker WH, Gley WC, 1984, Elastolytic and collagenolytic studies of arteries. Arch Surg, 119: 405–409. https://doi.org/10.1001/archsurg.1984.01390160041009

 

  1. Wills A, Thompson MM, Crowther M, et al., 1996, Elastase-induced matrix degradation in arterial organ cultures: An in vitro model of aneurysmal disease. J Vasc Surg, 24: 667–679. https://doi.org/10.1016/s0741-5214(96)70083-6

 

  1. Dadgar L, Marois Y, Deng X, et al., 1997, Arterial wall mechanical characteristics after treatment in collagenase: An aneurysmal model. Clin Invest Med, 20: 25–34.

 

  1. Kratzberg JA, Walker PJ, Rikkers E, et al., 2009, The effect of proteolytic treatment on plastic deformation of porcine aortic tissue. J Mech Behav Biomed Mater, 2: 65–72. https://doi.org/10.1016/j.jmbbm.2008.04.001

 

  1. Beenakker JW, Ashcroft BA, Lindeman JH, et al., 2012, Mechanical properties of the extracellular matrix of the aorta studied by enzymatic treatments. Biophys J, 102: 1731–1737. https://doi.org/10.1016/j.bpj.2012.03.041

 

  1. Gundiah N, Babu AR, Pruitt LA, 2013, Effects of elastase and collagenase on the nonlinearity and anisotropy of porcine aorta. Physiol Meas, 34: 1657–1673. https://doi.org/10.1088/0967-3334/34/12/1657

 

  1. Chow MJ, Mondonedo JR, Johnson VM, et al., 2013, Progressive structural and mechanical changes in elastin degraded aorta. Biomech Model Mechanobiol, 12: 361–372. https://doi.org/10.1007/s10237-012-0404-9

 

  1. Chow MJ, Choi M, Yun SH, et al., 2013, The effect of static stretch on elastin degradation in arteries. PLoS One, 8: e81951. https://doi.org/10.1371/journal.pone.0081951

 

  1. Cheheltani R, McGoverin CM, Rao J, et al., 2014, Fourier transform infrared spectroscopy to quantify collagen and elastin in an in vitro model of extracellular matrix degradation in aorta. Analyst, 139: 3039–3047. https://doi.org/10.1039/c3an02371k

 

  1. Silver FH, Horvath I, Foran DJ, 2001, Viscoelasticity of the vessel wall: The role of collagen and elastic fibers. Crit Rev Biomed Eng, 29: 279–302. https://doi.org/10.1615/critrevbiomedeng.v29.i3.10

 

  1. Gosline J, Lillie M, Carrington E, et al., 2002, Elastic proteins: Biological and mechanical properties. Philos Trans R Soc Lond B Biol Sci, 357: 121–132. https://doi.org/10.1098/rstb.2001.1022

 

  1. Baló J, Banga I, 1950, The elastolytic activity of pancreatic extracts. Biochem J, 46: 384–387. http://doi.org/10.1042/bj0460384

 

  1. Banga I, 1953, Thermal contraction of collagen and its dissolution with elastase. Nature, 172: 1099. https://doi.org/10.1038/1721099a0

 

  1. Starkey PM, Barrett AJ, Burleigh MC, 1977, The degradation of articular collagen by neutrophil proteinases. Biochim Biophys Acta, 483: 386–397. https://doi.org/10.1016/0005-2744(77)90066-3

 

  1. Starkey PM, 1977, The effect of human neutrophil elastase and cathepsin G on the collagen of cartilage, tendon, and cornea. Acta Biol Med Ger, 36: 1549–1554.

 

  1. Gadek JE, Fells GA, Wright DG, et al., 1980, Human neutrophil elastase functions as a Type III collagen “collagenase”. Biochem Biophys Res Commun, 95: 1815–1822. https://doi.org/10.1016/s0006-291x(80)80110-0

 

  1. Mainardi CL, Hasty DL, Seyer JM, et al., 1980, Specific cleavage of human Type III collagen by human polymorphonuclear leukocyte elastase. J Biol Chem, 255: 12006–12010.

 

  1. Gadher SJ, Eyre DR, Duance VC, et al., 1988, Susceptibility of cartilage collagens type II, IX, X, and XI to human synovial collagenase and neutrophil elastase. Eur J Biochem, 175: 1–7. https://doi.org/10.1111/j.1432-1033.1988.tb14158.x

 

  1. Watanabe H, Hattori S, Katsuda S, et al., 1990, Human neutrophil elastase: Degradation of basement membrane componenets and immunolocalization in the tissue. J Biochem, 108: 753–759. https://doi.org/10.1093/oxfordjournals.jbchem.a123277

 

  1. Kafienah W, Buttle DJ, Burnett D, et al., 1998, Cleavage of native Type I collagen by human neutrophil elastase. Biochem J, 330: 897–902. https://doi.org/10.1042/bj3300897
Share
Back to top
Global Translational Medicine, Electronic ISSN: 2811-0021 Print ISSN: 3060-8600, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept