Nelson Michael D, Rosenberry Ryan, Barresi Rita, Tsimerinov Evgeny I, Rader Florian, Tang Xiu, Mason O'Neil, Schwartz Avery, Stabler Thomas, Shidban Sarah, Mobaligh Neigena, Hogan Shomari, Elashoff Robert, Allen Jason D, Victor Ronald G
Heart Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
NSCT Diagnostic & Advisory Service for Rare Neuromuscular Diseases, Institute of Genetic Medicine, Newcastle upon Tyne, UK.
J Physiol. 2015 Dec 1;593(23):5183-200. doi: 10.1113/JP271252. Epub 2015 Nov 2.
Becker muscular dystrophy (BMD) is a progressive X-linked muscle wasting disease for which there is no treatment. BMD is caused by in-frame mutations in the gene encoding dystrophin, a structural cytoskeletal protein that also targets other proteins to the sarcolemma. Among these is neuronal nitric oxide synthase mu (nNOSμ), which requires specific spectrin-like repeats (SR16/17) in dystrophin's rod domain and the adaptor protein α-syntrophin for sarcolemmal targeting. When healthy skeletal muscle is exercised, sarcolemmal nNOSμ-derived nitric oxide (NO) attenuates α-adrenergic vasoconstriction, thus optimizing perfusion. In the mdx mouse model of dystrophinopathy, this protective mechanism (functional sympatholysis) is defective, resulting in functional muscle ischaemia. Treatment with a NO-donating non-steroidal anti-inflammatory drug (NSAID) alleviates this ischaemia and improves the murine dystrophic phenotype. In the present study, we report that, in 13 men with BMD, sympatholysis is defective mainly in patients whose mutations disrupt sarcolemmal targeting of nNOSμ, with the vasoconstrictor response measured as a decrease in muscle oxygenation (near infrared spectroscopy) to reflex sympathetic activation. Then, in a single-arm, open-label trial in 11 BMD patients and a double-blind, placebo-controlled cross-over trial in six patients, we show that acute treatment with oral sodium nitrate, an inorganic NO donor without a NSIAD moiety, restores sympatholysis and improves post-exercise hyperaemia (Doppler ultrasound). By contrast, sodium nitrate improves neither sympatholysis, nor hyperaemia in healthy controls. Thus, a simple NO donor recapitulates the vasoregulatory actions of sarcolemmal nNOS in BMD patients, and constitutes a putative novel therapy for this disease.
贝克肌肉萎缩症(BMD)是一种进行性X连锁肌肉萎缩疾病,目前尚无治疗方法。BMD由编码抗肌萎缩蛋白的基因发生框内突变引起,抗肌萎缩蛋白是一种结构细胞骨架蛋白,它还能将其他蛋白质靶向至肌膜。其中包括神经元型一氧化氮合酶μ(nNOSμ),它需要抗肌萎缩蛋白杆状结构域中的特定血影蛋白样重复序列(SR16/17)以及衔接蛋白α-肌营养不良蛋白聚糖才能靶向至肌膜。当健康的骨骼肌进行运动时,肌膜上nNOSμ产生的一氧化氮(NO)会减弱α-肾上腺素能血管收缩,从而优化灌注。在抗肌萎缩蛋白病的mdx小鼠模型中,这种保护机制(功能性交感神经抑制)存在缺陷,导致功能性肌肉缺血。使用一种释放NO的非甾体抗炎药(NSAID)进行治疗可缓解这种缺血,并改善小鼠的营养不良表型。在本研究中,我们报告称,在13名BMD男性患者中,交感神经抑制缺陷主要出现在那些突变破坏了nNOSμ向肌膜靶向定位的患者中,血管收缩反应通过肌肉氧合(近红外光谱法)对反射性交感神经激活的降低来衡量。然后,在一项针对11名BMD患者的单臂开放标签试验以及一项针对6名患者的双盲、安慰剂对照交叉试验中,我们发现口服硝酸钠(一种不含NSIAD部分的无机NO供体)进行急性治疗可恢复交感神经抑制并改善运动后充血(多普勒超声)。相比之下,硝酸钠在健康对照中既不能改善交感神经抑制,也不能改善充血。因此,一种简单的NO供体概括了BMD患者肌膜nNOS的血管调节作用,并构成了一种针对该疾病的新型潜在疗法。