Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle

<p dir="ltr">Mice with ectopic expression of uncoupling protein-1 (UCP1) in skeletal muscle exhibit a healthy aging phenotype with increased longevity and resistance to impaired metabolic health. This may be achieved by decreasing protein glycation by the reactive metabolite, methylg...

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محفوظ في:
التفاصيل البيبلوغرافية
المؤلف الرئيسي: Jinit Masania (7164239) (author)
مؤلفون آخرون: Patrick Wijten (2029159) (author), Susanne Keipert (4797369) (author), Mario Ost (551406) (author), Susanne Klaus (551409) (author), Naila Rabbani (291722) (author), Paul J. Thornalley (291723) (author)
منشور في: 2023
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author Jinit Masania (7164239)
author2 Patrick Wijten (2029159)
Susanne Keipert (4797369)
Mario Ost (551406)
Susanne Klaus (551409)
Naila Rabbani (291722)
Paul J. Thornalley (291723)
author2_role author
author
author
author
author
author
author_facet Jinit Masania (7164239)
Patrick Wijten (2029159)
Susanne Keipert (4797369)
Mario Ost (551406)
Susanne Klaus (551409)
Naila Rabbani (291722)
Paul J. Thornalley (291723)
author_role author
dc.creator.none.fl_str_mv Jinit Masania (7164239)
Patrick Wijten (2029159)
Susanne Keipert (4797369)
Mario Ost (551406)
Susanne Klaus (551409)
Naila Rabbani (291722)
Paul J. Thornalley (291723)
dc.date.none.fl_str_mv 2023-02-01T00:00:00Z
dc.identifier.none.fl_str_mv 10.1016/j.redox.2022.102574
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Decreased_methylglyoxal-mediated_protein_glycation_in_the_healthy_aging_mouse_model_of_ectopic_expression_of_UCP1_in_skeletal_muscle/24501055
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Clinical sciences
Aging
Uncoupling protein 1
Skeletal muscle
Protein glycation
Methylglyoxal
Proteomics
dc.title.none.fl_str_mv Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">Mice with ectopic expression of uncoupling protein-1 (UCP1) in skeletal muscle exhibit a healthy aging phenotype with increased longevity and resistance to impaired metabolic health. This may be achieved by decreasing protein glycation by the reactive metabolite, methylglyoxal (MG). We investigated protein glycation and oxidative damage in skeletal muscle of mice with UCP1 expression under control of the human skeletal actin promoter (HSA-mUCP1) at age 12 weeks (young) and 70 weeks (aged). We found both young and aged HSA-mUCP1 mice had decreased advanced glycation endproducts (AGEs) formed from MG, lysine-derived Nε(1-carboxyethyl)lysine (CEL) and arginine-derived hydroimidazolone, MG-H1, whereas protein glycation by glucose forming Nε-fructosyl-lysine (FL) was increased ca. 2-fold, compared to wildtype controls. There were related increases in FL-linked AGEs, Nε-carboxymethyl-lysine (CML) and 3-deoxylglucosone-derived hydroimidazolone 3DG-H, and minor changes in protein oxidative and nitration adducts. In aged HSA-mUCP1 mice, urinary MG-derived AGEs/FL ratio was decreased ca. 60% whereas there was no change in CML/FL ratio – a marker of oxidative damage. This suggests that, normalized for glycemic status, aged HSA-mUCP1 mice had a lower flux of whole body MG-derived AGE exposure compared to wildtype controls. Proteomics analysis of skeletal muscle revealed a shift to increased heat shock proteins and mechanoprotection and repair in HSA-mUCP1 mice. Decreased MG-derived AGE protein content in skeletal muscle of aged HSA-mUCP1 mice is therefore likely produced by increased proteolysis of MG-modified proteins and increased proteostasis surveillance of the skeletal muscle proteome. From this and previous transcriptomic studies, signaling involved in enhanced removal of MG-modified protein is likely increased HSPB1-directed HUWE1 ubiquitination through eIF2α-mediated, ATF5-induced increased expression of HSPB1. Decreased whole body exposure to MG-derived AGEs may be linked to increased weight specific physical activity of HSA-mUCP1 mice. Decreased formation and increased clearance of MG-derived AGEs may be associated with healthy aging in the HSA-mUCP1 mouse.</p><h2>Other Information</h2><p dir="ltr">Published in: Redox Biology<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1016/j.redox.2022.102574" target="_blank">https://dx.doi.org/10.1016/j.redox.2022.102574</a></p>
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network_acronym_str Manara2
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oai_identifier_str oai:figshare.com:article/24501055
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spelling Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscleJinit Masania (7164239)Patrick Wijten (2029159)Susanne Keipert (4797369)Mario Ost (551406)Susanne Klaus (551409)Naila Rabbani (291722)Paul J. Thornalley (291723)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesClinical sciencesAgingUncoupling protein 1Skeletal muscleProtein glycationMethylglyoxalProteomics<p dir="ltr">Mice with ectopic expression of uncoupling protein-1 (UCP1) in skeletal muscle exhibit a healthy aging phenotype with increased longevity and resistance to impaired metabolic health. This may be achieved by decreasing protein glycation by the reactive metabolite, methylglyoxal (MG). We investigated protein glycation and oxidative damage in skeletal muscle of mice with UCP1 expression under control of the human skeletal actin promoter (HSA-mUCP1) at age 12 weeks (young) and 70 weeks (aged). We found both young and aged HSA-mUCP1 mice had decreased advanced glycation endproducts (AGEs) formed from MG, lysine-derived Nε(1-carboxyethyl)lysine (CEL) and arginine-derived hydroimidazolone, MG-H1, whereas protein glycation by glucose forming Nε-fructosyl-lysine (FL) was increased ca. 2-fold, compared to wildtype controls. There were related increases in FL-linked AGEs, Nε-carboxymethyl-lysine (CML) and 3-deoxylglucosone-derived hydroimidazolone 3DG-H, and minor changes in protein oxidative and nitration adducts. In aged HSA-mUCP1 mice, urinary MG-derived AGEs/FL ratio was decreased ca. 60% whereas there was no change in CML/FL ratio – a marker of oxidative damage. This suggests that, normalized for glycemic status, aged HSA-mUCP1 mice had a lower flux of whole body MG-derived AGE exposure compared to wildtype controls. Proteomics analysis of skeletal muscle revealed a shift to increased heat shock proteins and mechanoprotection and repair in HSA-mUCP1 mice. Decreased MG-derived AGE protein content in skeletal muscle of aged HSA-mUCP1 mice is therefore likely produced by increased proteolysis of MG-modified proteins and increased proteostasis surveillance of the skeletal muscle proteome. From this and previous transcriptomic studies, signaling involved in enhanced removal of MG-modified protein is likely increased HSPB1-directed HUWE1 ubiquitination through eIF2α-mediated, ATF5-induced increased expression of HSPB1. Decreased whole body exposure to MG-derived AGEs may be linked to increased weight specific physical activity of HSA-mUCP1 mice. Decreased formation and increased clearance of MG-derived AGEs may be associated with healthy aging in the HSA-mUCP1 mouse.</p><h2>Other Information</h2><p dir="ltr">Published in: Redox Biology<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1016/j.redox.2022.102574" target="_blank">https://dx.doi.org/10.1016/j.redox.2022.102574</a></p>2023-02-01T00:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1016/j.redox.2022.102574https://figshare.com/articles/journal_contribution/Decreased_methylglyoxal-mediated_protein_glycation_in_the_healthy_aging_mouse_model_of_ectopic_expression_of_UCP1_in_skeletal_muscle/24501055CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/245010552023-02-01T00:00:00Z
spellingShingle Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
Jinit Masania (7164239)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Clinical sciences
Aging
Uncoupling protein 1
Skeletal muscle
Protein glycation
Methylglyoxal
Proteomics
status_str publishedVersion
title Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
title_full Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
title_fullStr Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
title_full_unstemmed Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
title_short Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
title_sort Decreased methylglyoxal-mediated protein glycation in the healthy aging mouse model of ectopic expression of UCP1 in skeletal muscle
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Clinical sciences
Aging
Uncoupling protein 1
Skeletal muscle
Protein glycation
Methylglyoxal
Proteomics