Androgen receptor agonists increase lean mass, improve cardiopulmonary functions and extend survival in preclinical models of Duchenne muscular dystrophy

被引:23
作者
Ponnusamy, Suriyan [1 ]
Sullivan, Ryan D. [2 ]
You, Dahui [3 ]
Zafar, Nadeem [4 ]
Yang, Chuan He [4 ]
Thiyagarajan, Thirumagal [1 ]
Johnson, Daniel L. [5 ]
Barrett, Maron L. [1 ]
Koehler, Nikki J. [1 ]
Star, Mayra [1 ]
Stephenson, Erin J. [3 ,6 ]
Bridges, Dave [3 ,6 ,8 ]
Cormier, Stephania A. [3 ]
Pfeffer, Lawrence M. [4 ]
Narayanan, Ramesh [1 ,7 ]
机构
[1] Univ Tennessee, Ctr Hlth Sci, Dept Med, 19,South Manassas,Room 120, Memphis, TN 38103 USA
[2] Univ Tennessee, Ctr Hlth Sci, Dept Comparat Med, Memphis, TN 38163 USA
[3] Univ Tennessee, Ctr Hlth Sci, Dept Pediat, Memphis, TN 38163 USA
[4] Univ Tennessee, Ctr Hlth Sci, Dept Pathol & Lab Med, Memphis, TN 38163 USA
[5] Univ Tennessee, Ctr Hlth Sci, Mol Informat Core, Memphis, TN 38163 USA
[6] Univ Tennessee, Ctr Hlth Sci, Dept Physiol, Memphis, TN 38163 USA
[7] West Canc Ctr, Memphis, TN USA
[8] Univ Michigan, Sch Publ Hlth, Dept Nutr Sci, Ann Arbor, MI 48109 USA
关键词
NITRIC-OXIDE SYNTHASE; GENE-EXPRESSION; MUSCLE; SKELETAL; UTROPHIN; MODULATOR; MICE; SARCOLEMMA; PHENOTYPE; DISCOVERY;
D O I
10.1093/hmg/ddx150
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Duchenne muscular dystrophy (DMD) is a neuromuscular disease that predominantly affects boys as a result of mutation(s) in the dystrophin gene. DMD is characterized by musculoskeletal and cardiopulmonary complications, resulting in shorter life-span. Boys afflicted by DMD typically exhibit symptoms within 3-5 years of age and declining physical functions before attaining puberty. We hypothesized that rapidly deteriorating health of pre-pubertal boys with DMD could be due to diminished anabolic actions of androgens in muscle, and that intervention with an androgen receptor (AR) agonist will reverse musculoskeletal complications and extend survival. While castration of dystrophin and utrophin double mutant (mdx-dm) mice to mimic pre-pubertal nadir androgen condition resulted in premature death, maintenance of androgen levels extended the survival. Non-steroidal selective-AR modulator, GTx-026, which selectively builds muscle and bone was tested in X-linked muscular dystrophy mice (mdx). GTx-026 significantly increased body weight, lean mass and grip strength by 60-80% over vehicle-treated mdx mice. While vehicle-treated castrated mdx mice exhibited cardiopulmonary impairment and fibrosis of heart and lungs, GTx-026 returned cardiopulmonary function and intensity of fibrosis to healthy control levels. GTx-026 elicits its musculoskeletal effects through pathways that are distinct from dystrophin-regulated pathways, making AR agonists ideal candidates for combination approaches. While castration of mdx-dm mice resulted in weaker muscle and shorter survival, GTx-026 treatment increased the muscle mass, function and survival, indicating that androgens are important for extended survival. These preclinical results support the importance of androgens and the need for intervention with AR agonists to treat DMD-affected boys.
引用
收藏
页码:2526 / 2540
页数:15
相关论文
共 61 条
[1]   Oxandrolone enhances skeletal muscle myosin synthesis and alters global gene expression profile in Duchenne muscular dystrophy [J].
Balagopal, P ;
Olney, R ;
Darmaun, D ;
Mougey, E ;
Dokler, M ;
Sieck, G ;
Hammond, D .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 2006, 290 (03) :E530-E539
[2]   Spermine oxidase maintains basal skeletal muscle gene expression and fiber size and is strongly repressed by conditions that cause skeletal muscle atrophy [J].
Bongers, Kale S. ;
Fox, Daniel K. ;
Kunkel, Steven D. ;
Stebounova, Larissa V. ;
Murry, Daryl J. ;
Pufall, Miles A. ;
Ebert, Scott M. ;
Dyle, Michael C. ;
Bullard, Steven A. ;
Dierdorff, Jason M. ;
Adams, Christopher M. .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 2015, 308 (02) :E144-E158
[3]   NITRIC-OXIDE SYNTHASE COMPLEXED WITH DYSTROPHIN AND ABSENT FROM SKELETAL-MUSCLE SARCOLEMMA IN DUCHENNE MUSCULAR-DYSTROPHY [J].
BRENMAN, JE ;
CHAO, DS ;
XIA, HH ;
ALDAPE, K ;
BREDT, DS .
CELL, 1995, 82 (05) :743-752
[4]   Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy [J].
Chang, WJ ;
Iannaccone, ST ;
Lau, KS ;
Masters, BSS ;
McCabe, TJ ;
McMillan, K ;
Padre, RC ;
Spencer, MJ ;
Tidball, JG ;
Stull, JT .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1996, 93 (17) :9142-9147
[5]   Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice [J].
Chrisam, Martina ;
Pirozzi, Marinella ;
Castagnaro, Silvia ;
Blaauw, Bert ;
Polishchuck, Roman ;
Cecconi, Francesco ;
Grumati, Paolo ;
Bonaldo, Paolo .
AUTOPHAGY, 2015, 11 (12) :2142-2152
[6]   GLPG0492, a novel selective androgen receptor modulator, improves muscle performance in the exercised-mdx mouse model of muscular dystrophy [J].
Cozzoli, Anna ;
Capogrosso, Roberta Francesca ;
Sblendorio, Valeriana Teresa ;
Dinardo, Maria Maddalena ;
Jagerschmidt, Catherine ;
Namour, Florence ;
Camerino, Giulia Maria ;
De Luca, Annamaria .
PHARMACOLOGICAL RESEARCH, 2013, 72 :9-24
[7]   Sarcospan, the 25-kDa transmembrane component of the dystrophin-glycoprotein complex [J].
Crosbie, RH ;
Heighway, J ;
Venzke, DP ;
Lee, JC ;
Campbell, KP .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1997, 272 (50) :31221-31224
[8]   Discovery of nonsteroidal androgens [J].
Dalton, JT ;
Mukherjee, A ;
Zhu, ZX ;
Kirkovsky, L ;
Miller, DD .
BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 1998, 244 (01) :1-4
[9]   Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy [J].
Deconinck, AE ;
Rafael, JA ;
Skinner, JA ;
Brown, SC ;
Potter, AC ;
Metzinger, L ;
Watt, DJ ;
Dickson, JG ;
Tinsley, JM ;
Davies, KE .
CELL, 1997, 90 (04) :717-727
[10]   Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice [J].
Deconinck, N ;
Tinsley, J ;
DeBacker, F ;
Fisher, R ;
Kahn, D ;
Phelps, S ;
Davies, K ;
Gillis, JM .
NATURE MEDICINE, 1997, 3 (11) :1216-1221