Cited by 248Muscle Physiology and DisordersTGF-β signaling in diseasesMeat and Animal Product Quality

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Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin

Gilson, Hélène, Schakman, Olivier, Kalista, Stéphanie, Lause, Pascale, Tsuchida, Kunihiro, Thissen, Jean-Paul·2009·American Journal of Physiology-Endocrinology and Metabolism

DOI 10.1152/ajpendo.00193.2009

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Abstract

Follistatin (FS) inhibits several members of the TGF-beta superfamily, including myostatin (Mstn), a negative regulator of muscle growth. Mstn inhibition by FS represents a potential therapeutic approach of muscle atrophy. The aim of our study was to investigate the mechanisms of the FS-induced muscle hypertrophy. To test the role of satellite cells in the FS effect, we used irradiation to destroy their proliferative capacity. FS overexpression increased the muscle weight by about 37% in control animals, but the increase reached only 20% in irradiated muscle, supporting the role of cell proliferation in the FS-induced hypertrophy. Surprisingly, the muscle hypertrophy caused by FS reached the same magnitude in Mstn-KO as in WT mice, suggesting that Mstn might not be the only ligand of FS involved in the regulation of muscle mass. To assess the role of activin (Act), another FS ligand, in the FS-induced hypertrophy, we electroporated FSI-I, a FS mutant that does not bind Act with high affinity. Whereas FS electroporation increased muscle weight by 32%, the muscle weight gain induced by FSI-I reached only 14%. Furthermore, in Mstn-KO mice, FSI-I overexpression failed to induce hypertrophy, in contrast to FS. Therefore, these results suggest that Act inhibition may contribute to FS-induced hypertrophy. Finally, the role of Act as a regulator of muscle mass was supported by the observation that ActA overexpression induced muscle weight loss (-15%). In conclusion, our results show that satellite cell proliferation and both Mstn and Act inhibition are involved in the FS-induced muscle hypertrophy.

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1 retracted

RETRACTED: Follistatin induction by nitric oxide through cyclic GMP: a tightly regulated signaling pathway that controls myoblast fusion
Pisconti, A., Brunelli, S., Padova, M. D., Palma, C. D., Deponti, D., Baesso, S., Sartorelli, V., Cossu, G., & Clementi, E. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200507083 · Cited by 107
Retracted
Regulation of skeletal muscle mass in mice by a new TGF-p superfamily member
McPherron, A. C., Lawler, A. M., & Lee, S.-J. (1997) · Nature · doi:10.1038/387083a0 · Cited by 4,013
Regulation of myostatin activity and muscle growth
Lee, S.-J., & McPherron, A. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.151270098 · Cited by 1,616
Myostatin, a Negative Regulator of Muscle Growth, Functions by Inhibiting Myoblast Proliferation
Thomas, M., Langley, B., Berry, C., Sharma, M., Kirk, S., Bass, J., & Kambadur, R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004356200 · Cited by 1,014
Myostatin Inhibits Myoblast Differentiation by Down-regulating MyoD Expression
Langley, B. C., Thomas, M., Bishop, A., Sharma, M., Gilmour, S., & Kambadur, R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204291200 · Cited by 910
Functional improvement of dystrophic muscle by myostatin blockade
Bogdanovich, S., Krag, T. O. B., Barton, E. R., Morris, L. D., Whittemore, L.-A., Ahima, R. S., & Khurana, T. S. (2002) · Nature · doi:10.1038/nature01154 · Cited by 831
Myostatin negatively regulates satellite cell activation and self-renewal
McCroskery, S., Thomas, M., Maxwell, L., Sharma, M., & Kambadur, R. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200207056 · Cited by 784
Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11
McPherron, A. C., Lawler, A. M., & Lee, S.-J. (1999) · Nature Genetics · doi:10.1038/10320 · Cited by 471
The transforming growth factor-β superfamily of receptors
de Caestecker, M. (2004) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2003.10.004 · Cited by 464
Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells
Taylor, W. E., Bhasin, S., Artaza, J., Byhower, F., Azam, M., Willard, D. H., Kull, F. C., & González-Cadavid, N. F. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.2.e221 · Cited by 410
Loss of myostatin attenuates severity of muscular dystrophy in mdx mice
Wagner, K. R., McPherron, A. C., Winik, N., & Lee, S. (2002) · Annals of Neurology · doi:10.1002/ana.10385 · Cited by 378
Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading
Carlson, C. J., Booth, F. W., & Gordon, S. E. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.2.r601 · Cited by 358
Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors
Minetti, G., Colussi, C., Adami, R., Serra, C., Mozzetta, C., Parente, V., Fortuni, S., Straino, S., Sampaolesi, M., Padova, M. D., et al. (2006) · Nature Medicine · doi:10.1038/nm1479 · Cited by 343
Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin
Reisz‐Porszasz, S., Bhasin, S., Artaza, J. N., Shen, R., Sinha‐Hikim, I., Hogue, A., Fielder, T. J., & González-Cadavid, N. F. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00107.2003 · Cited by 333
Quadrupling Muscle Mass in Mice by Targeting TGF-ß Signaling Pathways
Lee, S.-J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000789 · Cited by 316
Down-Regulation of Akt/Mammalian Target of Rapamycin Signaling Pathway in Response to Myostatin Overexpression in Skeletal Muscle
Amirouche, A., Durieux, A., Banzet, S., Koulmann, N., Bonnefoy, R., Mouret, C., Bigard, X. A., Peinnequin, A., & Freyssenet, D. G. (2008) · Endocrinology · doi:10.1210/en.2008-0959 · Cited by 301
Contribution of satellite cells to IGF‐I induced hypertrophy of skeletal muscle
Barton‐Davis, Shoturma, & Sweeney (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00618.x · Cited by 283
Long-term enhancement of skeletal muscle mass and strength by single gene administration of myostatin inhibitors
Haidet, A. M., Rizo, L., Handy, C. R., Umapathi, P., Eagle, A., Shilling, C., Boué, D. R., Martin, P. T., Sahenk, Z., Mendell, J. R., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709144105 · Cited by 274
Expression of growth/differentiation factor 11, a new member of the BMP/TGFβ superfamily during mouse embryogenesis
Nakashima, M., Toyono, T., Akamine, A., & Joyner, A. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00205-6 · Cited by 240
Biological activity of follistatin isoforms and follistatin-like-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins
Sidis, Y., Mukherjee, A., Keutmann, H., Delbaere, A., Sadatsuki, M., & Schneyer, A. (2006) · Endocrinology · doi:10.1210/en.2006-0089 · Cited by 211
Activin type IIA and IIB receptors mediate Gdf11 signaling in axial vertebral patterningPreprint
Oh, S. P., Yeo, C., Lee, Y. J., Schrewe, H., Whitman, M., & Li, E. (2002) · Genes & Development · doi:10.1101/gad.1021802 · Cited by 196
Transgenic expression of a myostatin inhibitor derived from follistatin increases skeletal muscle mass and ameliorates dystrophic pathology in mdx mice
Nakatani, M., Takehara, Y., Sugino, H., Matsumoto, M., Hashimoto, O., Hasegawa, Y., Murakami, T., Uezumi, A., Takeda, S., Noji, S., et al. (2007) · The FASEB Journal · doi:10.1096/fj.07-8673com · Cited by 191
Self-citation
Modulating skeletal muscle mass by postnatal, muscle‐specific inactivation of the myostatin gene
Grobet, L., Pirottin, D., Farnir, F., Poncelet, D. A., Royo, L. J., Brouwers, B., Christians, E., Desmecht, D. J.-M., Coignoul, F., Kahn, R., et al. (2003) · genesis · doi:10.1002/gene.10188 · Cited by 187
Redundancy of myostatin and growth/differentiation factor 11 function
McPherron, A. C., Huynh, T. V., & Lee, S.-J. (2009) · BMC Developmental Biology · doi:10.1186/1471-213x-9-24 · Cited by 168
Ectopic Expression of Myostatin Induces Atrophy of Adult Skeletal Muscle by Decreasing Muscle Gene Expression
Durieux, A., Amirouche, A., Banzet, S., Koulmann, N., Bonnefoy, R., Pasdeloup, M., Mouret, C., Bigard, X. A., Peinnequin, A., & Freyssenet, D. G. (2007) · Endocrinology · doi:10.1210/en.2006-1500 · Cited by 162
Human Follistatin-Related Protein: A Structural Homologue of Follistatin with Nuclear Localization
Tortoriello, D. V., Sidis, Y., Holtzman, D. A., Holmes, W. E., & Schneyer, A. L. (2001) · Endocrinology · doi:10.1210/endo.142.8.8319 · Cited by 152
Induction of MafBx and Murf ubiquitin ligase mRNAs in rat skeletal muscle after LPS injection
Dehoux, M., Beneden, R. V., Fernández-Celemı́n, L., Lause, P., & Thissen, J. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00505-2 · Cited by 148
Self-citation
Proteomic Identification and Functional Validation of Activins and Bone Morphogenetic Protein 11 as Candidate Novel Muscle Mass Regulators
Souza, T. A., Chen, X., Guo, Y., Sava, P., Zhang, J., Hill, J. J., Yaworsky, P. J., & Qiu, Y. (2008) · Molecular Endocrinology · doi:10.1210/me.2008-0290 · Cited by 147
Characterization of unique binding kinetics of follistatin and activin or inhibin in serum
Schneyer, A. L., Rzucidlo, D. A., Sluss, P. M., & Crowley, W. F. (1994) · Endocrinology · doi:10.1210/endo.135.2.8033815 · Cited by 143
Prolonged absence of myostatin reduces sarcopenia
Siriett, V., Platt, L., Salerno, M. S., Ling, N., Kambadur, R., & Sharma, M. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20778 · Cited by 139
Regulation of Myogenic Differentiation by Androgens: Cross Talk between Androgen Receptor/ β-Catenin and Follistatin/Transforming Growth Factor-β Signaling Pathways
Singh, R., Bhasin, S., Braga, M., Artaza, J. N., Pervin, S., Taylor, W. E., Krishnan, V., Sinha, S. K., Rajavashisth, T. B., & Jasuja, R. (2008) · Endocrinology · doi:10.1210/en.2008-0858 · Cited by 131
Plasmid DNA electrotransfer for intracellular and secreted proteins expression: new methodological developments and applications
Bloquel, C., Fabre, E. E., Bureau, M. F., & Scherman, D. (2004) · The Journal of Gene Medicine · doi:10.1002/jgm.508 · Cited by 129
Stimulation of skeletal muscle myofibrillar protein synthesis, p70 S6 kinase phosphorylation, and ribosomal protein S6 phosphorylation by inhibition of myostatin in mature mice
Welle, S. L., Burgess, K., & Mehta, S. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90862.2008 · Cited by 121
Insulin-Like Growth Factor-I Gene Transfer by Electroporation Prevents Skeletal Muscle Atrophy in Glucocorticoid-Treated Rats
Schakman, O., Gilson, H., de Coninck, V., Lause, P., Verniers, J., Havaux, X., Ketelslegers, J., & Thissen, J. (2005) · Endocrinology · doi:10.1210/en.2004-1594 · Cited by 95
Self-citation
Myofibrillar protein synthesis in myostatin-deficient mice
Welle, S. L., Bhatt, K. S., & Pinkert, C. A. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00433.2005 · Cited by 94
Gdf11 Is a Negative Regulator of Chondrogenesis and Myogenesis in the Developing Chick Limb
Gamer, L. W., Cox, K. A., Small, C. G., & Rosen, V. (2001) · Developmental Biology · doi:10.1006/dbio.2000.9981 · Cited by 92
Role of Akt/GSK-3β/β-Catenin Transduction Pathway in the Muscle Anti-Atrophy Action of Insulin-Like Growth Factor-I in Glucocorticoid-Treated Rats
Schakman, O., Kalista, S., Bertrand, L., Lause, P., Verniers, J., Ketelslegers, J. M., & Thissen, J. (2008) · Endocrinology · doi:10.1210/en.2008-0439 · Cited by 83
Self-citation
Molecular analysis of fiber type-specific expression of murine myostatin promoter
Salerno, M. S., Thomas, M., Forbes, D., Watson, T. J., Kambadur, R., & Sharma, M. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00492.2003 · Cited by 78
Hypotension inNKCC1null mice: role of the kidneys
Wall, S. M., Knepper, M. A., Hassell, K. A., Fischer, M. P., Shodeinde, A., Shin, W., Pham, T. D., Meyer, J. W., Lorenz, J. N., Beierwaltes, W. H., et al. (2005) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00309.2005 · Cited by 70
Follistatin and its role as an activin-binding protein.
Sugino, H., Sugino, K., Hashimoto, O., Shoji, H., & Nakamura, T. (1997) · PubMed · Cited by 61
Opposing Effects of Activin A and Follistatin on Developing Skeletal Muscle Cells
Link, B. A., & Nishi, R. (1997) · Experimental Cell Research · doi:10.1006/excr.1997.3575 · Cited by 56
Activin-type II receptor B (ACVR2B) and follistatin haplotype associations with muscle mass and strength in humans
Walsh, S., Metter, E. J., Ferrucci, L., & Roth, S. M. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01322.2006 · Cited by 53
Localization of the heparin binding site of follistatin
Inouye, S., LING, N. C., & Shimasaki, S. (1992) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(92)90094-m · Cited by 52
Crystal Structures of the Heparan Sulfate-binding Domain of Follistatin
Innis, C. A., & Hyvönen, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211284200 · Cited by 48
Expression of the TGF-β Family of Ligands Is Developmentally Regulated in Skeletal Muscle of Neonatal Rats
Suryawan, A., Frank, J. W., Nguyen, H. V., & Davis, T. A. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000196718.47935.6e · Cited by 42
Changes in striated muscle following single intense doses of x-rays.
Rb, L. (2003) · PubMed · Cited by 35
Activin A inhibits formation of skeletal muscle during chick development
He, L., Vichev, K., Macharia, R., Huang, R., Christ, B., Patel, K., & Amthor, H. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0454-1 · Cited by 26
Myostatin preferentially down-regulates the expression of fast 2x myosin heavy chain in cattle
Hayashi, S., MIYAKE, M., Watanabe, K., Aso, H., HAYASHI, S., Ohwada, S., & Yamaguchi, T. (2008) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.84.354 · Cited by 14

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Authors: Gilson, H., Schakman, O., Kalista, S., Lause, P., Tsuchida, K., & Thissen, J.-P.
Affiliations: UCLouvain (BE)
ORCID: Schakman, Olivier
Tsuchida, Kunihiro
Thissen, Jean-Paul
Venue: American Journal of Physiology-Endocrinology and Metabolism
Publisher: American Physiological Society
Published: 2009-07
Volume: 297
Issue: 1
Pages: E157-E164
ISSN: 0193-1849 (ISSN-L)
1522-1555
DOI: 10.1152/ajpendo.00193.2009
OpenAlex: W2169876318
Cited by: 248
References: 48
Citations by year: 2026: 6 · 2025: 12 · 2024: 6 · 2023: 13 · 2022: 11 · 2021: 14 · 2020: 16 · 2019: 13 · 2018: 19 · 2017: 17 · 2016: 13 · 2015: 17 · 2014: 22 · 2013: 17 · 2012: 17
FWCI: 6.95
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
PubMed (publishedVersion)
Digital Access to Libraries (submittedVersion)
Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
Funders: Fonds Spéciaux de Recherche
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
Keywords: follistatin, muscle hypertrophy, satellite cells, satellite cell proliferation, myostatin, activin, TGF-beta superfamily, muscle atrophy, muscle mass regulation
MeSH terms: Animals, Hypertrophy, Male, Muscular Atrophy, Up-Regulation, Rats, Wistar, Mice, Knockout, Activins, Satellite Cells, Skeletal Muscle, Follistatin, Cell Proliferation, Mice, Rats, Myostatin, Rats, Transgenic

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Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin

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