Myostatin: a Circulating Biomarker Correlating with Disease in Myotubular Myopathy Mice and Patients.

Koch, Catherine; Buono, Suzie; Menuet, Alexia; Robé, Anne; Djeddi, Sarah; Kretz, Christine; Gomez-Oca, Raquel; Depla, Marion; Monseur, Arnaud; Thielemans, Leen; Servais, Laurent; Laporte, Jocelyn; Cowling, Belinda S.

doi:10.1016/j.omtm.2020.04.022

Request a copy

Article (Scientific journals)

Myostatin: a Circulating Biomarker Correlating with Disease in Myotubular Myopathy Mice and Patients.

Koch, Catherine; Buono, Suzie; Menuet, Alexia et al.

2020 • In Molecular Therapy: Methods and Clinical Development, 17, p. 1178-1189

Permalink
https://hdl.handle.net/2268/256217

DOI
10.1016/j.omtm.2020.04.022

PubMed
32514412

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Myostatin_A circulating biomarker correlating with disease in myotubular myopathy mice and patients.pdf

Publisher postprint (1.87 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

GDF8; MSTN; antisense oligonucleotides; biomarker; centronuclear myopathies; dynamin; myotubular myopathy; therapy

Abstract :

[en] Myotubular myopathy, also called X-linked centronuclear myopathy (XL-CNM), is a severe congenital disease targeted for therapeutic trials. To date, biomarkers to monitor disease progression and therapy efficacy are lacking. The Mtm1 (-/y) mouse is a faithful model for XL-CNM, due to myotubularin 1 (MTM1) loss-of-function mutations. Using both an unbiased approach (RNA sequencing [RNA-seq]) and a directed approach (qRT-PCR and protein level), we identified decreased Mstn levels in Mtm1 (-/y) muscle, leading to low levels of myostatin in muscle and plasma. Myostatin (Mstn or growth differentiation factor 8 [Gdf8]) is a protein released by myocytes and inhibiting muscle growth and differentiation. Decreasing Dnm2 by genetic cross with Dnm2 (+/-) mice or by antisense oligonucleotides blocked or postponed disease progression and resulted in an increase in circulating myostatin. In addition, plasma myostatin levels inversely correlated with disease severity and with Dnm2 mRNA levels in muscles. Altered Mstn levels were associated with a generalized disruption of the myostatin pathway. Importantly, in two different forms of CNMs we identified reduced circulating myostatin levels in plasma from patients. This provides evidence of a blood-based biomarker that may be used to monitor disease state in XL-CNM mice and patients and supports monitoring circulating myostatin during clinical trials for myotubular myopathy.

Disciplines :

Neurology
Pediatrics

Author, co-author :

Koch, Catherine

Buono, Suzie

Menuet, Alexia

Robé, Anne

Djeddi, Sarah

Kretz, Christine

Gomez-Oca, Raquel

Depla, Marion

Monseur, Arnaud

Thielemans, Leen

More authors (3 more)

Language :

English

Title :

Myostatin: a Circulating Biomarker Correlating with Disease in Myotubular Myopathy Mice and Patients.

Publication date :

04 May 2020

Journal title :

Molecular Therapy: Methods and Clinical Development

eISSN :

2329-0501

Publisher :

Elsevier, United States

Volume :

Pages :

1178-1189

Commentary :

Available on ORBi :

since 01 February 2021

Statistics

Number of views

42 (7 by ULiège)

Number of downloads

3 (3 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Cowling, B.S., Thielemans, L., Translational medicine in neuromuscular disorders: from academia to industry. Dis. Model. Mech., 13, 2019 dmm041434.
McPherron, A.C., Lawler, A.M., Lee, S.J., Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387 (1997), 83–90.
Mariot, V., Joubert, R., Hourdé, C., Féasson, L., Hanna, M., Muntoni, F., Maisonobe, T., Servais, L., Bogni, C., Le Panse, R., et al. Downregulation of myostatin pathway in neuromuscular diseases may explain challenges of anti-myostatin therapeutic approaches. Nat. Commun., 8, 2017, 1859.
Ravenscroft, G., Laing, N.G., Bönnemann, C.G., Pathophysiological concepts in the congenital myopathies: blurring the boundaries, sharpening the focus. Brain 138 (2015), 246–268.
Laporte, J., Hu, L.J., Kretz, C., Mandel, J.L., Kioschis, P., Coy, J.F., Klauck, S.M., Poustka, A., Dahl, N., A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat. Genet. 13 (1996), 175–182.
Nicot, A.S., Toussaint, A., Tosch, V., Kretz, C., Wallgren-Pettersson, C., Iwarsson, E., Kingston, H., Garnier, J.M., Biancalana, V., Oldfors, A., et al. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat. Genet. 39 (2007), 1134–1139.
Böhm, J., Biancalana, V., Malfatti, E., Dondaine, N., Koch, C., Vasli, N., Kress, W., Strittmatter, M., Taratuto, A.L., Gonorazky, H., et al. Adult-onset autosomal dominant centronuclear myopathy due to BIN1 mutations. Brain 137 (2014), 3160–3170.
Bitoun, M., Maugenre, S., Jeannet, P.Y., Lacène, E., Ferrer, X., Laforêt, P., Martin, J.J., Laporte, J., Lochmüller, H., Beggs, A.H., et al. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37 (2005), 1207–1209.
Wilmshurst, J.M., Lillis, S., Zhou, H., Pillay, K., Henderson, H., Kress, W., Müller, C.R., Ndondo, A., Cloke, V., Cullup, T., et al. RYR1 mutations are a common cause of congenital myopathies with central nuclei. Ann. Neurol. 68 (2010), 717–726.
Vandersmissen, I., Biancalana, V., Servais, L., Dowling, J.J., Vander Stichele, G., Van Rooijen, S., Thielemans, L., An Integrated Modelling Methodology for Estimating the Prevalence of Centronuclear Myopathy. Neuromuscul. Disord. 28 (2018), 766–777.
Cowling, B.S., Chevremont, T., Prokic, I., Kretz, C., Ferry, A., Coirault, C., Koutsopoulos, O., Laugel, V., Romero, N.B., Laporte, J., Reducing dynamin 2 expression rescues X-linked centronuclear myopathy. J. Clin. Invest. 124 (2014), 1350–1363.
Cowling, B.S., Toussaint, A., Amoasii, L., Koebel, P., Ferry, A., Davignon, L., Nishino, I., Mandel, J.L., Laporte, J., Increased expression of wild-type or a centronuclear myopathy mutant of dynamin 2 in skeletal muscle of adult mice leads to structural defects and muscle weakness. Am. J. Pathol. 178 (2011), 2224–2235.
Liu, N., Bezprozvannaya, S., Shelton, J.M., Frisard, M.I., Hulver, M.W., McMillan, R.P., Wu, Y., Voelker, K.A., Grange, R.W., Richardson, J.A., et al. Mice lacking microRNA 133a develop dynamin 2–dependent centronuclear myopathy. J. Clin. Invest. 121 (2011), 3258–3268.
Tasfaout, H., Buono, S., Guo, S., Kretz, C., Messaddeq, N., Booten, S., Greenlee, S., Monia, B.P., Cowling, B.S., Laporte, J., Antisense oligonucleotide-mediated Dnm2 knockdown prevents and reverts myotubular myopathy in mice. Nat. Commun., 8, 2017, 15661.
Tasfaout, H., Lionello, V.M., Kretz, C., Koebel, P., Messaddeq, N., Bitz, D., Laporte, J., Cowling, B.S., Single Intramuscular Injection of AAV-shRNA Reduces DNM2 and Prevents Myotubular Myopathy in Mice. Mol. Ther. 26 (2018), 1082–1092.
Cowling, B.S., Prokic, I., Tasfaout, H., Rabai, A., Humbert, F., Rinaldi, B., Nicot, A.S., Kretz, C., Friant, S., Roux, A., Laporte, J., Amphiphysin (BIN1) negatively regulates dynamin 2 for normal muscle maturation. J. Clin. Invest. 127 (2017), 4477–4487.
Buono, S., Ross, J.A., Tasfaout, H., Levy, Y., Kretz, C., Tayefeh, L., Matson, J., Guo, S., Kessler, P., Monia, B.P., et al. Reducing dynamin 2 (DNM2) rescues DNM2-related dominant centronuclear myopathy. Proc. Natl. Acad. Sci. USA 115 (2018), 11066–11071.
Lawlor, M.W., Read, B.P., Edelstein, R., Yang, N., Pierson, C.R., Stein, M.J., Wermer-Colan, A., Buj-Bello, A., Lachey, J.L., Seehra, J.S., Beggs, A.H., Inhibition of activin receptor type IIB increases strength and lifespan in myotubularin-deficient mice. Am. J. Pathol. 178 (2011), 784–793.
Lawlor, M.W., Viola, M.G., Meng, H., Edelstein, R.V., Liu, F., Yan, K., Luna, E.J., Lerch-Gaggl, A., Hoffmann, R.G., Pierson, C.R., et al. Differential muscle hypertrophy is associated with satellite cell numbers and Akt pathway activation following activin type IIB receptor inhibition in Mtm1 p.R69C mice. Am. J. Pathol. 184 (2014), 1831–1842.
Anderson, S.B., Goldberg, A.L., Whitman, M., Identification of a novel pool of extracellular pro-myostatin in skeletal muscle. J. Biol. Chem. 283 (2008), 7027–7035.
Allen, D.L., Loh, A.S., Posttranscriptional mechanisms involving microRNA-27a and b contribute to fast-specific and glucocorticoid-mediated myostatin expression in skeletal muscle. Am. J. Physiol. Cell Physiol. 300 (2011), C124–C137.
Allen, D.L., Cleary, A.S., Hanson, A.M., Lindsay, S.F., Reed, J.M., CCAAT/enhancer binding protein-delta expression is increased in fast skeletal muscle by food deprivation and regulates myostatin transcription in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299 (2010), R1592–R1601.
West, D.W., Baehr, L.M., Marcotte, G.R., Chason, C.M., Tolento, L., Gomes, A.V., Bodine, S.C., Baar, K., Acute resistance exercise activates rapamycin-sensitive and -insensitive mechanisms that control translational activity and capacity in skeletal muscle. J. Physiol. 594 (2016), 453–468.
Yang, H., Li, T.W., Zhou, Y., Peng, H., Liu, T., Zandi, E., Martínez-Chantar, M.L., Mato, J.M., Lu, S.C., Activation of a novel c-Myc-miR27-prohibitin 1 circuitry in cholestatic liver injury inhibits glutathione synthesis in mice. Antioxid. Redox Signal. 22 (2015), 259–274.
Li, X., Xu, M., Ding, L., Tang, J., MiR-27a: A Novel Biomarker and Potential Therapeutic Target in Tumors. J. Cancer 10 (2019), 2836–2848.
Lee, S.J., McPherron, A.C., Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. USA 98 (2001), 9306–9311.
Walker, R.G., Poggioli, T., Katsimpardi, L., Buchanan, S.M., Oh, J., Wattrus, S., Heidecker, B., Fong, Y.W., Rubin, L.L., Ganz, P., et al. Biochemistry and Biology of GDF11 and Myostatin: Similarities, Differences, and Questions for Future Investigation. Circ. Res. 118 (2016), 1125–1141, discussion 1142.
Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., Ambros, V., Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol., 5, 2004, R13.
Rachagani, S., Cheng, Y., Reecy, J.M., Myostatin genotype regulates muscle-specific miRNA expression in mouse pectoralis muscle. BMC Res. Notes, 3, 2010, 297.
Böhm, J., Biancalana, V., Dechene, E.T., Bitoun, M., Pierson, C.R., Schaefer, E., Karasoy, H., Dempsey, M.A., Klein, F., Dondaine, N., et al. Mutation spectrum in the large GTPase dynamin 2, and genotype-phenotype correlation in autosomal dominant centronuclear myopathy. Hum. Mutat. 33 (2012), 949–959.
Durieux, A.C., Vignaud, A., Prudhon, B., Viou, M.T., Beuvin, M., Vassilopoulos, S., Fraysse, B., Ferry, A., Lainé, J., Romero, N.B., et al. A centronuclear myopathy-dynamin 2 mutation impairs skeletal muscle structure and function in mice. Hum. Mol. Genet. 19 (2010), 4820–4836.
Burch, P.M., Pogoryelova, O., Palandra, J., Goldstein, R., Bennett, D., Fitz, L., Guglieri, M., Bettolo, C.M., Straub, V., Evangelista, T., et al. Reduced serum myostatin concentrations associated with genetic muscle disease progression. J. Neurol. 264 (2017), 541–553.
Dupont, J.B., Guo, J., Renaud-Gabardos, E., Poulard, K., Latournerie, V., Lawlor, M.W., Grange, R.W., Gray, J.T., Buj-Bello, A., Childers, M.K., Mack, D.L., AAV-Mediated Gene Transfer Restores a Normal Muscle Transcriptome in a Canine Model of X-Linked Myotubular Myopathy. Mol. Ther. 28 (2020), 382–393.
Egerman, M.A., Cadena, S.M., Gilbert, J.A., Meyer, A., Nelson, H.N., Swalley, S.E., Mallozzi, C., Jacobi, C., Jennings, L.L., Clay, I., et al. GDF11 Increases with Age and Inhibits Skeletal Muscle Regeneration. Cell Metab. 22 (2015), 164–174.
Yuasa, K., Hagiwara, Y., Ando, M., Nakamura, A., Takeda, S., Hijikata, T., MicroRNA-206 is highly expressed in newly formed muscle fibers: implications regarding potential for muscle regeneration and maturation in muscular dystrophy. Cell Struct. Funct. 33 (2008), 163–169.
Bachmann, C., Jungbluth, H., Muntoni, F., Manzur, A.Y., Zorzato, F., Treves, S., Cellular, biochemical and molecular changes in muscles from patients with X-linked myotubular myopathy due to MTM1 mutations. Hum. Mol. Genet. 26 (2017), 320–332.
Maani, N., Sabha, N., Rezai, K., Ramani, A., Groom, L., Eltayeb, N., Mavandadnejad, F., Pang, A., Russo, G., Brudno, M., et al. Tamoxifen therapy in a murine model of myotubular myopathy. Nat. Commun., 9, 2018, 4849.
Buj-Bello, A., Laugel, V., Messaddeq, N., Zahreddine, H., Laporte, J., Pellissier, J.F., Mandel, J.L., The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc. Natl. Acad. Sci. USA 99 (2002), 15060–15065.
Seth, P.P., Siwkowski, A., Allerson, C.R., Vasquez, G., Lee, S., Prakash, T.P., Kinberger, G., Migawa, M.T., Gaus, H., Bhat, B., Swayze, E.E., Design, synthesis and evaluation of constrained methoxyethyl (cMOE) and constrained ethyl (cEt) nucleoside analogs. Nucleic Acids Symp. Ser. (Oxf) 52 (2008), 553–554.
Annoussamy, M., Lilien, C., Gidaro, T., Gargaun, E., Chê, V., Schara, U., Gangfuß, A., D'Amico, A., Dowling, J.J., Darras, B.T., et al. X-linked myotubular myopathy: A prospective international natural history study. Neurology 92 (2019), e1852–e1867.