Long Range Interactions Regulate Igf2 Gene Transcription during Skeletal Muscle Differentiation
Open accessAbstract
The differentiation, maintenance, and repair of skeletal muscle is controlled by interactions between genetically determined transcriptional programs regulated by myogenic transcription factors and environmental cues activated by growth factors and hormones. Signaling through the insulin-like growth factor 1 (IGF1) receptor by locally produced IGF2 defines one such pathway that is critical for normal muscle growth and for regeneration after injury. IGF2 gene and protein expression are induced as early events in muscle differentiation, but the responsible molecular mechanisms are unknown. Here we characterize a distal DNA element within the imprinted mouse Igf2-H19 locus with properties of a muscle transcriptional enhancer. We find that this region undergoes a transition to open chromatin during differentiation, whereas adjacent chromatin remains closed, and that it interacts in differentiating muscle nuclei but not in mesenchymal precursor cells with the Igf2 gene found more than 100 kb away, suggesting that chromatin looping or sliding to bring the enhancer in proximity to Igf2 promoters is also an early event in muscle differentiation. Because this element directly stimulates the transcriptional activity of an Igf2 promoter-reporter gene in differentiating myoblasts, our results indicate that we have identified a bona fide distal transcriptional enhancer that supports Igf2 gene activation in skeletal muscle cells. Because this DNA element is conserved in the human IGF2-H19 locus, our results further suggest that its muscle enhancer function also is conserved among different mammalian species.
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IGF-2 expression during skeletal muscle differentiation is regulated at the transcriptional level, and signaling through the IGF-1 receptor by locally produced IGF-2 defines a pathway critical for normal muscle growth and regeneration.
“IGF-2 expression during skeletal muscle differentiation is regulated at the transcriptional level 33, and signaling through the IGF-1 receptor by locally produced IGF-2 defines a pathway that is critical for normal muscle growth and regeneration 34.”
From Akt-dependent anabolic activity of natural and synthetic brassinosteroids in rat skeletal muscle cells (2011) · cites this paper as [34]
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“Yet until recently little was known about mechanisms of regulation of IGF2 in muscle cells (1, 14).”
BackgroundMethodInfluentialSelf-citationZhang, J., Han, B., Li, X., Bies, J., Jiang, P., Koller, R. P., & Wolff, L. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.267 · Cited by 6 · see citing works
“A distal DNA element within the imprinted mouse Igf2-H19 locus interacts with the Igf2 gene 4100 kb away via chromatin looping or sliding during skeletal muscle differentiation.(35) In the INK4b-ARF-INK4a locus, EZH2-dependent chromatin looping controls INK4a and INK4b but not ARF during human progenitor cell differen…”
SH2B1 modulates chromatin state and MyoD occupancy to enhance expressions of myogenic genes
Chen, K., Chang, Y., Yeh, C., Lian, Y.-L., Chan, M. W. Y., Kao, C.-F., & Chen, L. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.12.007 · Cited by 5 · see citing works
“4C), which is consistent with published result [31].”
BackgroundMethodResultInfluentialMasterPATH: network analysis of functional genomics screening data
Rubanova, N., Pinna, G., Kropp, J., Campalans, A., Radicella, J. P., Polesskaya, A., Harel‐Bellan, A., & Morozova, N. (2020) · BMC Genomics · doi:10.1186/s12864-020-07047-2 · Cited by 4 · see citing works
Thorvaldsen, J. L., Juan, A. M., Lan, Y., Krapp, C. J., & Bartolomei, M. S. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011834 · Cited by 3 · see citing works
eQTL Analysis and Association of MYF6 mRNA Expression with Meat Quality Traits in Pigs
Çınar, M. U., Fan, H., Neuhoff, C., et al. (2012) · Kafkas Universitesi Veteriner Fakultesi Dergisi · Cited by 3 · see citing works
Dermawan, J. K., Vanoli, F., de Wardin, H. D. T., Levi, J. N., Sanchez, G. D. I., Siddiquee, A. H., Brosius, S., You, D., Tirode, F., Sung, P., et al. (2026) · Science Advances · doi:10.1126/sciadv.aea6453 · Cited by 1 · see citing works
“In myogenic differentiation, IGF2 promotes MYOD1 induction and myogenic commitment via IGF1R–mediated PI3K/AKT and mitogen-activated protein kinase (MAPK) signaling, as well as recruitment of MYOD1-associated transcriptional machinery at target promoters ( 41 – 44 ).”
MasterPATH: network analysis of functional genomics screening dataPreprint
Rubanova, N., Polesskaya, A., Campalans, A., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/264119
Additional file 1 of MasterPATH: network analysis of functional genomics screening data
Rubanova, N., Pinna, G., Kropp, J., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12955721
MasterPATH : l'analyse de réseau des données expérimentales de la génomique fonctionnelle
Rubanova, N. (2018) · doi:10.70675/7e3495d1z5f52z44e7za9d8z1f847314122c
“…ACTA1, MYH1, MYLPF, ARF6, CD81, CD9, CDC42, EHD2, MYOF proteins responsible for inhibition, activation, and facilitating of fusion of myotubes (Alzhanov et al., 2010; Bourmoum et al., 2016; Doherty et al., 2008; Gunning et al., 2001; S.-J. Lee, 2004; Tachibana et al., 1999; Vasyutina et al.,…”
Background
- Authors
- Alzhanov, D. T., McInerney, S. F., & Rotwein, P.
- Affiliations
- Oregon Health & Science University (US)
- Corresponding author
- Rotwein, Peter
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 285
- Issue
- 50
- Pages
- 38969-38977
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2998108
- OpenAlex
- W2079701322
- Semantic Scholar
- 1ec3f28d0e85c1a99bd386a9b065b0df2163f15c
- Cited by
- 44
- References
- 54
- Citations by year
- 2026: 1 · 2025: 2 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 2 · 2016: 5 · 2015: 5 · 2014: 1 · 2013: 5 · 2012: 5
- FWCI
- 1.82
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007680, R01DK042748, R01 DK42748-21, T32DK007674)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- insulin-like growth factor II, skeletal muscle differentiation, Igf2/H19 locus, genomic imprinting, distal enhancers, chromatin looping, open chromatin, myoblasts, muscle regeneration, enhancer conservation, transcriptional regulation
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Chromatin, Female, Gene Expression Regulation, Humans, Insulin-Like Growth Factor II, Male, Mice, Inbred C57BL, Models, Genetic, Promoter Regions, Genetic, Transcription, Genetic, Muscle, Skeletal, Reverse Transcriptase Polymerase Chain Reaction, Mice
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