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The rRNA epitranscriptome and myonuclear SNORD landscape in skeletal muscle fibers contributes to ribosome heterogeneity and is altered by a hypertrophic stimulus.
Cui, Minying; Jannig, Paulo; Halladjian, Maral; Figueiredo, Vandré C; Wen, Yuan; Vechetti, Ivan J; Krogh, Nicolai; Jude, Baptiste; Edman, Sebastian; Lanner, Johanna; McCarthy, John; Murach, Kevin A; Sejersen, Thomas; Nielsen, Henrik; von Walden, Ferdinand.
Affiliation
  • Cui M; Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
  • Jannig P; Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
  • Halladjian M; Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.
  • Figueiredo VC; Department of Biological Sciences, Oakland University, Rochester, Michigan, United States.
  • Wen Y; Department of Physiology, College of Medicine, University of Kentucky, Lexington, Kentucky, United States.
  • Vechetti IJ; Center for Muscle Biology, University of Kentucky, Lexington, Kentucky, United States.
  • Krogh N; Division of Biomedical Informatics, Department of Internal Medicine, College of Medicine, University of Kentucky, Lexington, Kentucky, United States.
  • Jude B; Department of Nutrition and Health Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, United States.
  • Edman S; Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.
  • Lanner J; Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
  • McCarthy J; Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
  • Murach KA; Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden.
  • Sejersen T; Department of Physiology, College of Medicine, University of Kentucky, Lexington, Kentucky, United States.
  • Nielsen H; Center for Muscle Biology, University of Kentucky, Lexington, Kentucky, United States.
  • von Walden F; Department of Health, Human Performance, and Recreation, Exercise Science Research Center, University of Arkansas, Fayetteville, Arkansas, United States.
Am J Physiol Cell Physiol ; 327(3): C516-C524, 2024 Sep 01.
Article in En | MEDLINE | ID: mdl-38912733
ABSTRACT
In cell biology, ribosomal RNA (rRNA) 2'O-methyl (2'-O-Me) is the most prevalent posttranscriptional chemical modification contributing to ribosome heterogeneity. The modification involves a family of small nucleolar RNAs (snoRNAs) and is specified by box C/D snoRNAs (SNORDs). Given the importance of ribosome biogenesis for skeletal muscle growth, we asked if rRNA 2'-O-Me in nascent ribosomes synthesized in response to a growth stimulus is an unrecognized mode of ribosome heterogeneity in muscle. To determine the pattern and dynamics of 2'-O-Me rRNA, we used a sequencing-based profiling method called RiboMeth-seq (RMS). We applied this method to tissue-derived rRNA of skeletal muscle and rRNA specifically from the muscle fiber using an inducible myofiber-specific RiboTag mouse in sedentary and mechanically overloaded conditions. These analyses were complemented by myonuclear-specific small RNA sequencing to profile SNORDs and link the rRNA epitranscriptome to known regulatory elements generated within the muscle fiber. We demonstrate for the first time that mechanical overload of skeletal muscle 1) induces decreased 2'-O-Me at a subset of skeletal muscle rRNA and 2) alters the SNORD profile in isolated myonuclei. These findings point to a transient diversification of the ribosome pool via 2'-O-Me during growth and adaptation in skeletal muscle. These findings suggest changes in ribosome heterogeneity at the 2'-O-Me level during muscle hypertrophy and lay the foundation for studies investigating the functional implications of these newly identified "growth-induced" ribosomes.NEW & NOTEWORTHY Ribosomal RNAs (rRNAs) are posttranscriptionally modified by 2'O-methyl (2'-O-Me). This study applied RiboMeth-seq (RMS) to detect changes in 2'-O-Me levels during skeletal muscle hypertrophy, uncovering transient diversification of the ribosome pool in skeletal muscle fibers. This work implies a role for ribosome heterogeneity in skeletal muscle growth and adaptation.
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Full text: 1 Collection: 01-internacional Database: MEDLINE Main subject: Ribosomes / RNA, Ribosomal / Muscle Fibers, Skeletal / RNA, Small Nucleolar / Transcriptome Limits: Animals Language: En Journal: Am J Physiol Cell Physiol Journal subject: FISIOLOGIA Year: 2024 Document type: Article Affiliation country: Suecia

Full text: 1 Collection: 01-internacional Database: MEDLINE Main subject: Ribosomes / RNA, Ribosomal / Muscle Fibers, Skeletal / RNA, Small Nucleolar / Transcriptome Limits: Animals Language: En Journal: Am J Physiol Cell Physiol Journal subject: FISIOLOGIA Year: 2024 Document type: Article Affiliation country: Suecia