Developmental and degenerative cardiac defects in the Taiwanese mouse model of severe spinal muscular atrophy

被引:19
作者
Maxwell, Gillian K. [1 ]
Szunyogova, Eva [1 ,2 ]
Shorrock, Hannah K. [2 ,3 ]
Gillingwater, Thomas H. [2 ,3 ]
Parson, Simon H. [1 ,2 ]
机构
[1] Univ Aberdeen, Inst Med Sci, Aberdeen AB25 2ZD, Scotland
[2] Univ Edinburgh, Euan MacDonald Ctr Motor Neurone Dis Res, Edinburgh, Midlothian, Scotland
[3] Univ Edinburgh, Edinburgh Med Sch Biomed Sci, Edinburgh, Midlothian, Scotland
关键词
cardiac; cardiovascular; cell death; septum; stress; ventricle; KUGELBERG-WELANDER-DISEASE; CONGENITAL HEART-DISEASE; MOTOR-NEURON; BASEMENT-MEMBRANE; MITOCHONDRIAL DYSFUNCTION; VENTRICULAR DYSFUNCTION; GLUCOSE-METABOLISM; LIVER DEVELOPMENT; ATP SYNTHASE; CELL-DEATH;
D O I
10.1111/joa.12793
中图分类号
R602 [外科病理学、解剖学]; R32 [人体形态学];
学科分类号
100101 ;
摘要
Spinal muscular atrophy (SMA), an autosomal recessive disease caused by a decrease in levels of the survival motor neuron (SMN) protein, is the most common genetic cause of infant mortality. Although neuromuscular pathology is the most severe feature of SMA, other organs and tissues, including the heart, are also known to be affected in both patients and animal models. Here, we provide new insights into changes occurring in the heart, predominantly at pre- and early symptomatic ages, in the Taiwanese mouse model of severe SMA. Thinning of the interventricular septum and dilation of the ventricles occurred at pre- and early symptomatic ages. However, the left ventricular wall was significantly thinner in SMA mice from birth, occurring prior to any overt neuromuscular symptoms. Alterations in collagen IV protein from birth indicated changes to the basement membrane and contributed to the abnormal arrangement of cardiomyocytes in SMA hearts. This raises the possibility that developmental defects, occurring prenatally, may contribute to cardiac pathology in SMA. In addition, cardiomyocytes in SMA hearts exhibited oxidative stress at pre-symptomatic ages and increased apoptosis during early symptomatic stages of disease. Heart microvasculature was similarly decreased at an early symptomatic age, likely contributing to the oxidative stress and apoptosis phenotypes observed. Finally, an increased incidence of blood retention in SMA hearts post-fixation suggests the likelihood of functional defects, resulting in blood pooling. These pathologies mirror dilated cardiomyopathy, with clear consequences for heart function that would likely contribute to potential heart failure. Our findings add significant additional experimental evidence in support of the requirement to develop systemic therapies for SMA capable of treating non-neuromuscular pathologies.
引用
收藏
页码:965 / 978
页数:14
相关论文
共 105 条
[1]   Mitochondrial Dysfunction in a Neural Cell Model of Spinal Muscular Atrophy [J].
Acsadi, Gyula ;
Lee, Icksoo ;
Li, Xingli ;
Khaidakov, Magomed ;
Pecinova, Alena ;
Parker, Graham C. ;
Huettemann, Maik .
JOURNAL OF NEUROSCIENCE RESEARCH, 2009, 87 (12) :2748-2756
[2]  
Collado-Ortiz MA, 2007, CIR CIR, V75, P117
[3]   Finger cold-induced vasodilatation, sympathetic skin response, and R-R interval variation in patients with progressive in spinal muscular atrophy [J].
Arai, H ;
Tanabe, Y ;
Hachiya, Y ;
Otsuka, E ;
Kumada, S ;
Furushima, W ;
Kohyama, J ;
Yamashita, S ;
Takanashi, JI ;
Kohno, Y .
JOURNAL OF CHILD NEUROLOGY, 2005, 20 (11) :871-875
[4]   Early heart failure in the SMNΔ7 model of spinal muscular atrophy and correction by postnatal scAAV9-SMN delivery [J].
Bevan, Adam K. ;
Hutchinson, Kirk R. ;
Foust, Kevin D. ;
Braun, Lyndsey ;
McGovern, Vicki L. ;
Schmelzer, Leah ;
Ward, Jennifer G. ;
Petruska, Jeffrey C. ;
Lucchesi, Pamela A. ;
Burghes, Arthur H. M. ;
Kaspar, Brian K. .
HUMAN MOLECULAR GENETICS, 2010, 19 (20) :3895-3905
[5]   Physical exercise reduces cardiac defects in type 2 spinal muscular atrophy-like mice [J].
Biondi, Olivier ;
Lopes, Philippe ;
Desseille, Celine ;
Branchu, Julien ;
Chali, Farah ;
Ben Salah, Amina ;
Pariset, Claude ;
Chanoine, Christophe ;
Charbonnier, Frederic .
JOURNAL OF PHYSIOLOGY-LONDON, 2012, 590 (22) :5907-5925
[6]   Systemic, postsymptomatic antisense oligonucleotide rescues motor unit maturation delay in a new mouse model for type II/III spinal muscular atrophy [J].
Bogdanik, Laurent P. ;
Osborne, Melissa A. ;
Davis, Crystal ;
Martin, Whitney P. ;
Austin, Andrew ;
Rigo, Frank ;
Bennett, C. Frank ;
Lutz, Cathleen M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (43) :E5863-E5872
[7]   Defects in pancreatic development and glucose metabolism in SMN-depleted mice independent of canonical spinal muscular atrophy neuromuscular pathology [J].
Bowerman, Melissa ;
Michalski, John-Paul ;
Beauvais, Ariane ;
Murray, Lyndsay M. ;
DeRepentigny, Yves ;
Kothary, Rashmi .
HUMAN MOLECULAR GENETICS, 2014, 23 (13) :3432-3444
[8]   Glucose metabolism and pancreatic defects in spinal muscular atrophy [J].
Bowerman, Melissa ;
Swoboda, Kathryn J. ;
Michalski, John-Paul ;
Wang, Gen-Sheng ;
Reeks, Courtney ;
Beauvais, Ariane ;
Murphy, Kelley ;
Woulfe, John ;
Screaton, Robert A. ;
Scott, Fraser W. ;
Kothary, Rashmi .
ANNALS OF NEUROLOGY, 2012, 72 (02) :256-268
[9]   Bioenergetic status modulates motor neuron vulnerability and pathogenesis in a zebrafish model of spinal muscular atrophy [J].
Boyd, Penelope J. ;
Tu, Wen-Yo ;
Shorrock, Hannah K. ;
Groen, Ewout J. N. ;
Carter, Roderick N. ;
Powis, Rachael A. ;
Thomson, Sophie R. ;
Thomson, Derek ;
Graham, Laura C. ;
Motyl, Anna A. L. ;
Wishart, Thomas M. ;
Highley, J. Robin ;
Morton, Nicholas M. ;
Becker, Thomas ;
Becker, Catherina G. ;
Heath, Paul R. ;
Gillingwater, Thomas H. .
PLOS GENETICS, 2017, 13 (04)
[10]   Type IV collagen degradation in the myocardial basement membrane after unloading of the failing heart by a left ventricular assist device [J].
Bruggink, Annette H. ;
van Oosterhout, Matthijs F. M. ;
de Jonge, Nicolaas ;
Cleutjens, Jack P. M. ;
van Wichen, Dick F. ;
van Kuik, Joyce ;
Tilanus, Marcel G. J. ;
Gmelig-Meyling, Frits H. J. ;
van den Tweel, Jan G. ;
de Weger, Roel A. .
LABORATORY INVESTIGATION, 2007, 87 (11) :1125-1137