Skeletal muscle desmin alterations following revascularization in peripheral artery disease claudicants.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
01 Jun 2024
Historique:
received: 11 01 2024
accepted: 30 05 2024
medline: 2 6 2024
pubmed: 2 6 2024
entrez: 1 6 2024
Statut: epublish

Résumé

Peripheral artery disease (PAD) is characterized by varying severity of arterial stenosis, exercise induced claudication, malperfused tissue precluding normal healing and skeletal muscle dysfunction. Revascularization interventions improve circulation, but post-reperfusion changes within the skeletal muscle are not well characterized. This study investigates if revascularization enhanced hemodynamics increases walking performance with concurrent improvement of mitochondrial function and reverses abnormal skeletal muscle morphological features that develop with PAD. Fifty-eight patients completed walking performance testing and muscle biopsy before and 6 months after revascularization procedures. Muscle fiber morphology, desmin structure, and mitochondria respiration assessments before and after the revascularization were evaluated. Revascularization improved limb hemodynamics, walking function, and muscle morphology. Qualitatively not all participants recovered normal structural architecture of desmin in the myopathic myofibers after revascularization. Heterogenous responses in the recovery of desmin structure following revascularization may be caused by other underlying factors not reversed with hemodynamic improvements. Revascularization interventions clinically improve patient walking ability and can reverse the multiple subcellular functional and structural abnormalities in muscle cells. Further study is needed to characterize desmin structural remodeling with improvements in skeletal muscle morphology and function.

Identifiants

pubmed: 38824194
doi: 10.1038/s41598-024-63626-3
pii: 10.1038/s41598-024-63626-3
doi:

Substances chimiques

Desmin 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

12609

Subventions

Organisme : NIA NIH HHS
ID : R01AG064420
Pays : United States

Informations de copyright

© 2024. The Author(s).

Références

Rutherford, R. B. et al. Recommended standards for reports dealing with lower extremity ischemia: Revised version. J. Vasc. Surg. 26(3), 517–538 (1997).
pubmed: 9308598 doi: 10.1016/S0741-5214(97)70045-4
Gornik, H. L. & Beckman, J. A. Cardiology patient page Peripheral arterial disease. Circulation 111(13), e169–e172 (2005).
pubmed: 15811861 doi: 10.1161/01.CIR.0000160581.58633.8B
Norgren, L. et al. Inter-society consensus for the management of peripheral arterial disease (TASC II). J. Vasc. Surg. 45(Suppl S), S5-67 (2007).
pubmed: 17223489 doi: 10.1016/j.jvs.2006.12.037
Pipinos, I. I. et al. The myopathy of peripheral arterial occlusive disease: Part 1. Functional and histomorphological changes and evidence for mitochondrial dysfunction. Vasc. Endovasc. Surg. 41(6), 481–489 (2008).
doi: 10.1177/1538574407311106
Pipinos, I. I. et al. The myopathy of peripheral arterial occlusive disease: Part 2. Oxidative stress, neuropathy, and shift in muscle fiber type. Vasc. Endovasc. Surg. 42(2), 101–112 (2008).
doi: 10.1177/1538574408315995
Steven, S., Daiber, A., Dopheide, J. F., Munzel, T. & Espinola-Klein, C. Peripheral artery disease, redox signaling, oxidative stress - Basic and clinical aspects. Redox Biol. 12, 787–797 (2017).
pubmed: 28437655 pmcid: 5403804 doi: 10.1016/j.redox.2017.04.017
McDermott, M. M. et al. Skeletal muscle pathology in peripheral artery disease: A brief review. Arterioscler. Thromb. Vasc. Biol. 40(11), 2577–2585 (2020).
pubmed: 32938218 pmcid: 9571495 doi: 10.1161/ATVBAHA.120.313831
Liang, Z. et al. Ischemia-reperfusion injury in peripheral artery disease and traditional Chinese medicine treatment. Evid. Based Complement Alternat. Med. 2021, 4954070 (2021).
pubmed: 34899949 pmcid: 8660193 doi: 10.1155/2021/4954070
Eltzschig, H. K. & Collard, C. D. Vascular ischaemia and reperfusion injury. Br. Med. Bull. 70, 71–86 (2004).
pubmed: 15494470 doi: 10.1093/bmb/ldh025
Makris, K. I. et al. Mitochondriopathy of peripheral arterial disease. Vascular 15(6), 336–343 (2007).
pubmed: 18053417 doi: 10.2310/6670.2007.00054
Koutakis, P. et al. Oxidative stress and antioxidant treatment in patients with peripheral artery disease. Physiol. Rep. 6(7), e13650 (2018).
pubmed: 29611350 pmcid: 5880878 doi: 10.14814/phy2.13650
Koutakis, P. et al. Abnormal accumulation of desmin in gastrocnemius myofibers of patients with peripheral artery disease: Associations with altered myofiber morphology and density, mitochondrial dysfunction and impaired limb function. J. Histochem. Cytochem. Off. J. Histochem. Soc. 63(4), 256–269 (2015).
doi: 10.1369/0022155415569348
Koutakis, P. et al. Oxidative damage in the gastrocnemius of patients with peripheral artery disease is myofiber type selective. Redox Biol. 2, 921–928 (2014).
pubmed: 25180168 pmcid: 4143812 doi: 10.1016/j.redox.2014.07.002
Pipinos, I. I. et al. Mitochondrial defects and oxidative damage in patients with peripheral arterial disease. Free Radic. Biol. Med. 41(2), 262–269 (2006).
pubmed: 16814106 doi: 10.1016/j.freeradbiomed.2006.04.003
Ismaeel, A. et al. Oxidative stress and arterial dysfunction in peripheral artery disease. Antioxidants 7(10), 145 (2018).
pubmed: 30347720 pmcid: 6210426 doi: 10.3390/antiox7100145
Ismaeel, A. et al. Effects of limb revascularization procedures on oxidative stress. J. Surg. Res. 232, 503–509 (2018).
pubmed: 30463765 doi: 10.1016/j.jss.2018.07.024
Thompson, J. R. et al. Protein concentration and mitochondrial content in the gastrocnemius predicts mortality rates in patients with peripheral arterial disease. Ann. Surg. 261(3), 605–610 (2015).
pubmed: 24670845 doi: 10.1097/SLA.0000000000000643
Lazarides, E. Intermediate filaments as mechanical integrators of cellular space. Nature 283(5744), 249–256 (1980).
pubmed: 7188712 doi: 10.1038/283249a0
Desmin cytoskeleton: A potential regulator of muscle mitochondrial behavior and function, (2002).
Capetanaki, Y., Bloch, R. J., Kouloumenta, A., Mavroidis, M. & Psarras, S. Muscle intermediate filaments and their links to membranes and membranous organelles. Exp. Cell Res. 313(10), 2063–2076 (2007).
pubmed: 17509566 doi: 10.1016/j.yexcr.2007.03.033
Capetanaki, Y., Milner, D. J. & Weitzer, G. Desmin in muscle formation and maintenance: Knockouts and consequences. Cell Struct. Funct. 22(1), 103–116 (1997).
pubmed: 9113396 doi: 10.1247/csf.22.103
Maloyan, A. et al. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in alpha-B-crystallin desmin-related cardiomyopathy. Circulation 112(22), 3451–3461 (2005).
pubmed: 16316967 pmcid: 1398051 doi: 10.1161/CIRCULATIONAHA.105.572552
Li, Z. L. et al. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J. Cell Biol. 139(1), 129–144 (1997).
pubmed: 9314534 pmcid: 2139820 doi: 10.1083/jcb.139.1.129
Koutakis, P. et al. Abnormal myofiber morphology and limb dysfunction in claudication. J. Surg. Res. 196(1), 172–179 (2015).
pubmed: 25791828 pmcid: 4512658 doi: 10.1016/j.jss.2015.02.011
McDermott, M. M. et al. Impairments of muscles and nerves associated with peripheral arterial disease and their relationship with lower extremity functioning: the InCHIANTI Study. J. Am. Geriatr. Soc. 52(3), 405–410 (2004).
pubmed: 14962156 doi: 10.1111/j.1532-5415.2004.52113.x
Farah, B. Q. et al. Sedentary behavior is associated with impaired biomarkers in claudicants. J. Vasc. Surg. 63(3), 657–663 (2016).
pubmed: 26518099 doi: 10.1016/j.jvs.2015.09.018
Weiss, D. J. et al. Oxidative damage and myofiber degeneration in the gastrocnemius of patients with peripheral arterial disease. J. Transl. Med. 11, 230 (2013).
pubmed: 24067235 pmcid: 3849592 doi: 10.1186/1479-5876-11-230
Huang, D. et al. Quantitative fluorescence imaging analysis for cancer biomarker discovery: Application to beta-catenin in archived prostate specimens. Cancer Epidemiol. Biomark. Prev. Publ. Am. Assoc. Cancer Res. Cosponsored Am. Soc. Prev. Oncol. 16(7), 1371–1381 (2007).
doi: 10.1158/1055-9965.EPI-06-0718
Cluff, K. et al. Morphometric analysis of gastrocnemius muscle biopsies from patients with peripheral arterial disease: objective grading of muscle degeneration. Am. J. Physiol. Regul. Integr. Comparat. Physiol. 305(3), R291–R299 (2013).
doi: 10.1152/ajpregu.00525.2012
Ismaeel, A. et al. Skeletal muscle MiR-210 expression is associated with mitochondrial function in peripheral artery disease patients. Transl. Res. 246, 66–77 (2022).
pubmed: 35288364 pmcid: 9197925 doi: 10.1016/j.trsl.2022.03.003
Janssen, R. C. & Boyle, K. E. Microplate assays for spectrophotometric measurement of mitochondrial enzyme activity. Methods Mol. Biol. 1978, 355–368 (2019).
pubmed: 31119674 doi: 10.1007/978-1-4939-9236-2_22
Watanabe, K. et al. Endovascular revascularization improves the central hemodynamics and augmentation index in patients with peripheral artery disease. Intern. Med. 59(1), 37–44 (2020).
pubmed: 31511483 doi: 10.2169/internalmedicine.3413-19
Giugliano, G. et al. Endovascular treatment of lower extremity arteries is associated with an improved outcome in diabetic patients affected by intermittent claudication. BMC Surg. 12(Suppl 1), S19 (2012).
pubmed: 23174008 pmcid: 3499211 doi: 10.1186/1471-2482-12-S1-S19
Miller, A. J. et al. Peripheral revascularization attenuates the exercise pressor reflex and increases coronary exercise hyperemia in peripheral arterial disease. J. Appl. Physiol. 125(1), 58–63 (2018).
pubmed: 29648515 pmcid: 6086975 doi: 10.1152/japplphysiol.01046.2017
Regensteiner, J. G., Hargarten, M. E., Rutherford, R. B. & Hiatt, W. R. Functional benefits of peripheral vascular bypass surgery for patients with intermittent claudication. Angiology 44(1), 1–10 (1993).
pubmed: 8424578 doi: 10.1177/000331979304400101
Hogan, S. E. et al. Improvement in walking impairment following surgical and endovascular revascularization: Insights from VOYAGER PAD. Vasc. Med. 27(4), 343–349 (2022).
pubmed: 35467452 doi: 10.1177/1358863X221085606
Gardner, A. W. & Killewich, L. A. Lack of functional benefits following infrainguinal bypass in peripheral arterial occlusive disease patients. Vasc. Med. 6(1), 9–14 (2001).
pubmed: 11358164 doi: 10.1177/1358836X0100600103
Hoover, H. E., Thuerauf, D. J., Martindale, J. J. & Glembotski, C. C. alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38 - A potential role for alpha B-crystallin as a target of the p38 branch of the cardiac stress response. J. Biol. Chem. 275(31), 23825–23833 (2000).
pubmed: 10816593 doi: 10.1074/jbc.M003864200
Nagaraj, R. H. et al. Therapeutic potential of alpha-crystallin. Biochim. Biophys. Acta 1860(1 Pt B), 252–257 (2016).
pubmed: 25840354 doi: 10.1016/j.bbagen.2015.03.012
Wang, X. et al. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ. Res. 89(1), 84–91 (2001).
pubmed: 11440982 doi: 10.1161/hh1301.092688
Biol, A. J., Odena, M. A., Oliveira, E., Olive, M. & Ferrer, I. Desmin is oxidized and nitrated in affected muscles in myotilinopathies and desminopathies. J. Neuropathol. Exp. Neur. 66(8), 711–723 (2007).
doi: 10.1097/nen.0b013e3181256b4c
Aweida, D., Rudesky, I., Volodin, A., Shimko, E. & Cohen, S. GSK3-beta promotes calpain-1-mediated desmin filament depolymerization and myofibril loss in atrophy. J. Cell Biol. 217(10), 3698–3714 (2018).
pubmed: 30061109 pmcid: 6168250 doi: 10.1083/jcb.201802018
Volodin, A., Kosti, I., Goldberg, A. L. & Cohen, S. Myofibril breakdown during atrophy is a delayed response requiring the transcription factor PAX4 and desmin depolymerization. Proc. Natl. Acad. Sci. USA 114(8), E1375–E1384 (2017).
pubmed: 28096335 pmcid: 5338431 doi: 10.1073/pnas.1612988114
Cohen, S., Zhai, B., Gygi, S. P. & Goldberg, A. L. Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J. Cell Biol. 198(4), 575–589 (2012).
pubmed: 22908310 pmcid: 3514026 doi: 10.1083/jcb.201110067
Baylor, S. M. & Hollingworth, S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J. Physiol. 551(Pt 1), 125–138 (2003).
pubmed: 12813151 pmcid: 2343150 doi: 10.1113/jphysiol.2003.041608
Armstrong, R. B., Warren, G. L. & Warren, J. A. Mechanisms of exercise-induced muscle fibre injury. Sports Med. 12(3), 184–207 (1991).
pubmed: 1784873 doi: 10.2165/00007256-199112030-00004
Raastad, T. et al. Changes in calpain activity, muscle structure, and function after eccentric exercise. Med. Sci. Sports Exerc. 42(1), 86–95 (2010).
pubmed: 20010126 doi: 10.1249/MSS.0b013e3181ac7afa
Yoshiko, A. et al. Muscle deoxygenation and neuromuscular activation in synergistic muscles during intermittent exercise under hypoxic conditions. Sci. Rep. 10(1), 295 (2020).
pubmed: 31941906 pmcid: 6962371 doi: 10.1038/s41598-019-57099-y
Williams, R. S. & Benjamin, I. J. Protective responses in the ischemic myocardium. J. Clin. Invest. 106(7), 813–818 (2000).
pubmed: 11018066 pmcid: 381426 doi: 10.1172/JCI11205
Jennings, R. B. & Ganote, C. E. Structural changes in myocardium during acute ischemia. Circ. Res. 35(Suppl 3), 156–172 (1974).
pubmed: 4607107

Auteurs

Dylan Wilburn (D)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Dimitrios Miserlis (D)

Department of Surgery and Perioperative Care, University of Texas, Austin, TX, USA.
Department of Surgery, University of Texas Health Science Center San Antonio, San Antonio, TX, USA.

Emma Fletcher (E)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Evlampia Papoutsi (E)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Ahmed Ismaeel (A)

Department of Physiology, University of Kentucky, Lexington, KY, USA.

Cassandra Bradley (C)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Andrew Ring (A)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Trevor Wilkinson (T)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA.

Robert S Smith (RS)

Department of Surgery, Baylor Scott & White Medical Center, Temple, TX, USA.

Lucas Ferrer (L)

Department of Surgery and Perioperative Care, University of Texas, Austin, TX, USA.

Gleb Haynatzki (G)

Department of Biostatistics, University of Nebraska Medical Center, Omaha, NE, USA.

Peter Monteleone (P)

Department of Internal Medicine, University of Texas, Austin, TX, USA.

Subhash Banerjee (S)

Department of Cardiology, Baylor Scott & White Medical Center, Dallas, TX, USA.

Elizabeth Brisbois (E)

School of Chemical, Materials and Biomedical Engineering, College of Engineering, University of Georgia, Athens, GA, USA.

William T Bohannon (WT)

Department of Surgery, Baylor Scott & White Medical Center, Temple, TX, USA.

Panagiotis Koutakis (P)

Department of Biology, Baylor University, B.207 Baylor Science Building, One Bear Place #97388, Waco, TX, 76798-7388, USA. panagiotis_koutakis@baylor.edu.

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