Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise

Benjamin I. Burke; Ahmed Ismaeel; Douglas E. Long; Lauren A. Depa; Peyton T. Coburn; Jensen Goh; Tolulope P. Saliu; Bonnie J. Walton; Ivan J. Vechetti; Bailey D. Peck; Taylor R. Valentino; C. Brooks Mobley; Hasiyet Memetimin; Dandan Wang; Brian S. Finlin; Philip A. Kern; Charlotte A. Peterson; John J. McCarthy; Yuan Wen

doi:10.1172/jci.insight.182589

Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise

Benjamin I. Burke, Ahmed Ismaeel, Douglas E. Long, Lauren A. Depa, Peyton T. Coburn, Jensen Goh, Tolulope P. Saliu, Bonnie J. Walton, Ivan J. Vechetti, Bailey D. Peck, Taylor R. Valentino, C. Brooks Mobley, Hasiyet Memetimin, Dandan Wang, Brian S. Finlin, Philip A. Kern, Charlotte A. Peterson, John J. McCarthy, Yuan Wen

Research output: Contribution to journal › Article › peer-review

Abstract

Extracellular vesicles (EVs) have emerged as important mediators of intertissue signaling and exercise adaptations. In this human study, we provide evidence that muscle-specific microRNA-1 (miR-1) was transferred to adipose tissue via EVs following an acute bout of resistance exercise. Using a multimodel machine learning automation tool, we discovered muscle primary miR-1 transcript and CD63⁺ EV count in circulation as top explanatory features for changes in adipose miR-1 levels in response to resistance exercise. RNA-Seq and in-silico prediction of miR-1 target genes identified caveolin 2 (CAV2) and tripartite motif containing 6 (TRIM6) as miR-1 target genes downregulated in the adipose tissue of a subset of participants with the highest increases in miR-1 levels following resistance exercise. Overexpression of miR-1 in differentiated human adipocyte-derived stem cells downregulated these miR-1 targets and enhanced catecholamine-induced lipolysis. These data identify a potential EV-mediated mechanism by which skeletal muscle communicates with adipose tissue and modulates lipolysis via miR-1.

Original language	English
Article number	e182589
Journal	JCI insight
Volume	9
Issue number	21
DOIs	https://doi.org/10.1172/jci.insight.182589
State	Published - Nov 8 2024

Bibliographical note

Publisher Copyright:
Copyright: © 2024, Burke et al. This is an open access article published under the terms of the Creative Commons Attribution 4.0 International License.

ASJC Scopus subject areas

General Medicine

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10.1172/jci.insight.182589

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Burke, B. I., Ismaeel, A., Long, D. E., Depa, L. A., Coburn, P. T., Goh, J., Saliu, T. P., Walton, B. J., Vechetti, I. J., Peck, B. D., Valentino, T. R., Brooks Mobley, C., Memetimin, H., Wang, D., Finlin, B. S., Kern, P. A., Peterson, C. A., McCarthy, J. J., & Wen, Y. (2024). Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise. JCI insight, 9(21), Article e182589. https://doi.org/10.1172/jci.insight.182589

@article{67bae91fec7841f8bc3e769c262ce38a,

title = "Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise",

abstract = "Extracellular vesicles (EVs) have emerged as important mediators of intertissue signaling and exercise adaptations. In this human study, we provide evidence that muscle-specific microRNA-1 (miR-1) was transferred to adipose tissue via EVs following an acute bout of resistance exercise. Using a multimodel machine learning automation tool, we discovered muscle primary miR-1 transcript and CD63+ EV count in circulation as top explanatory features for changes in adipose miR-1 levels in response to resistance exercise. RNA-Seq and in-silico prediction of miR-1 target genes identified caveolin 2 (CAV2) and tripartite motif containing 6 (TRIM6) as miR-1 target genes downregulated in the adipose tissue of a subset of participants with the highest increases in miR-1 levels following resistance exercise. Overexpression of miR-1 in differentiated human adipocyte-derived stem cells downregulated these miR-1 targets and enhanced catecholamine-induced lipolysis. These data identify a potential EV-mediated mechanism by which skeletal muscle communicates with adipose tissue and modulates lipolysis via miR-1.",

author = "Burke, {Benjamin I.} and Ahmed Ismaeel and Long, {Douglas E.} and Depa, {Lauren A.} and Coburn, {Peyton T.} and Jensen Goh and Saliu, {Tolulope P.} and Walton, {Bonnie J.} and Vechetti, {Ivan J.} and Peck, {Bailey D.} and Valentino, {Taylor R.} and {Brooks Mobley}, C. and Hasiyet Memetimin and Dandan Wang and Finlin, {Brian S.} and Kern, {Philip A.} and Peterson, {Charlotte A.} and McCarthy, {John J.} and Yuan Wen",

note = "Publisher Copyright: Copyright: {\textcopyright} 2024, Burke et al. This is an open access article published under the terms of the Creative Commons Attribution 4.0 International License.",

year = "2024",

month = nov,

day = "8",

doi = "10.1172/jci.insight.182589",

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Burke, BI, Ismaeel, A, Long, DE, Depa, LA, Coburn, PT, Goh, J, Saliu, TP, Walton, BJ, Vechetti, IJ, Peck, BD, Valentino, TR, Brooks Mobley, C, Memetimin, H, Wang, D, Finlin, BS , Kern, PA, Peterson, CA, McCarthy, JJ & Wen, Y 2024, 'Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise', JCI insight, vol. 9, no. 21, e182589. https://doi.org/10.1172/jci.insight.182589

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T1 - Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise

AU - Burke, Benjamin I.

AU - Ismaeel, Ahmed

AU - Long, Douglas E.

AU - Depa, Lauren A.

AU - Coburn, Peyton T.

AU - Goh, Jensen

AU - Saliu, Tolulope P.

AU - Walton, Bonnie J.

AU - Vechetti, Ivan J.

AU - Peck, Bailey D.

AU - Valentino, Taylor R.

AU - Brooks Mobley, C.

AU - Memetimin, Hasiyet

AU - Wang, Dandan

AU - Finlin, Brian S.

AU - Kern, Philip A.

AU - Peterson, Charlotte A.

AU - McCarthy, John J.

AU - Wen, Yuan

PY - 2024/11/8

Y1 - 2024/11/8

N2 - Extracellular vesicles (EVs) have emerged as important mediators of intertissue signaling and exercise adaptations. In this human study, we provide evidence that muscle-specific microRNA-1 (miR-1) was transferred to adipose tissue via EVs following an acute bout of resistance exercise. Using a multimodel machine learning automation tool, we discovered muscle primary miR-1 transcript and CD63+ EV count in circulation as top explanatory features for changes in adipose miR-1 levels in response to resistance exercise. RNA-Seq and in-silico prediction of miR-1 target genes identified caveolin 2 (CAV2) and tripartite motif containing 6 (TRIM6) as miR-1 target genes downregulated in the adipose tissue of a subset of participants with the highest increases in miR-1 levels following resistance exercise. Overexpression of miR-1 in differentiated human adipocyte-derived stem cells downregulated these miR-1 targets and enhanced catecholamine-induced lipolysis. These data identify a potential EV-mediated mechanism by which skeletal muscle communicates with adipose tissue and modulates lipolysis via miR-1.

AB - Extracellular vesicles (EVs) have emerged as important mediators of intertissue signaling and exercise adaptations. In this human study, we provide evidence that muscle-specific microRNA-1 (miR-1) was transferred to adipose tissue via EVs following an acute bout of resistance exercise. Using a multimodel machine learning automation tool, we discovered muscle primary miR-1 transcript and CD63+ EV count in circulation as top explanatory features for changes in adipose miR-1 levels in response to resistance exercise. RNA-Seq and in-silico prediction of miR-1 target genes identified caveolin 2 (CAV2) and tripartite motif containing 6 (TRIM6) as miR-1 target genes downregulated in the adipose tissue of a subset of participants with the highest increases in miR-1 levels following resistance exercise. Overexpression of miR-1 in differentiated human adipocyte-derived stem cells downregulated these miR-1 targets and enhanced catecholamine-induced lipolysis. These data identify a potential EV-mediated mechanism by which skeletal muscle communicates with adipose tissue and modulates lipolysis via miR-1.

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Extracellular vesicle transfer of miR-1 to adipose tissue modifies lipolytic pathways following resistance exercise

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