The neuromuscular impact of symptomatic SMN restoration in a mouse model of spinal muscular atrophy

Neurobiology of Disease

Volumn 87, Issue , 2016, Pages 116-123

  Arnold, W David ^a   McGovern, Vicki L ^a   Sanchez, Benjamin ^b   Li, Jia ^b   Corlett, Kaitlyn M ^a   Kolb, Stephen J ^a   Rutkove, Seward B ^b   Burghes, Arthur H ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Antisense oligonucleotide; Biomarker; Clinical trials; Electrical impedance myography; Electromyography; Gene therapy; Motor unit number estimation; Pharmacodynamics; Spinal muscular atrophy; Survival motor neuron

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; SURVIVAL MOTOR NEURON PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DRUG EFFICACY; ELECTROMYOGRAPHY; GENE THERAPY; MOTOR UNIT POTENTIAL; MOUSE; MUSCLE ACTION POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMN GENE; SPINAL MUSCULAR ATROPHY; SURVIVAL RATE; TIME TO TREATMENT; TREATMENT RESPONSE; ANIMAL; ATROPHY; DISEASE MODEL; IMPEDANCE; LONGITUDINAL STUDY; MUSCULAR ATROPHY, SPINAL; MYOGRAPHY; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; REFLEX; SKELETAL MUSCLE; SURVIVAL ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; ATROPHY; DISEASE MODELS, ANIMAL; ELECTRIC IMPEDANCE; GENETIC THERAPY; LONGITUDINAL STUDIES; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR ATROPHY, SPINAL; MYOGRAPHY; OLIGONUCLEOTIDES, ANTISENSE; REFLEX; SURVIVAL ANALYSIS;

EID: 84952904811     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.12.014     Document Type: Article

References (70)

1. Ahad M.A., Rutkove S.B. Electrical impedance myography at 50kHz in the rat: technique, reproducibility, and the effects of sciatic injury and recovery. Clin. Neurophysiol. 2009, 120:1534-1538.
2. Ahad M., Rutkove S.B. Correlation between muscle electrical impedance data and standard neurophysiologic parameters after experimental neurogenic injury. Physiol. Meas. 2010, 31:1437-1448.
3. Ahad M.A., et al. Electrical characteristics of rat skeletal muscle in immaturity, adulthood and after sciatic nerve injury, and their relation to muscle fiber size. Physiol. Meas. 2009, 30:1415-1427.
4. Araujo A., et al. Vascular perfusion abnormalities in infants with spinal muscular atrophy. J. Pediatr. 2009, 155:292-294.
5. Arnold W.D., Burghes A.H. Spinal Muscular Atrophy: The Development and Implementation of Potential Treatments 2013, Ann Neurol.
6. Arnold W.D., et al. Electrophysiological biomarkers in spinal muscular atrophy: preclinical proof of concept. Ann. Clin. Transl. Neurol. 2014, 1:34-44.
7. Arnold S.K., Wier C.G., Kissel J.T., Burghes A.H., Kolb S.J. Electrophysiological motor unit number estimation (MUNE) measuring compound muscle action potential (CMAP) in mouse hindlimb muscles. J. Vis. Exp 2015, (Journal of Visualized Experiments. Accepted. 2015).
8. Arnold W.D., et al. Spinal muscular atrophy: diagnosis and management in a new therapeutic era. Muscle Nerve 2015, 51:157-167.
9. Baldwin T., et al. Wound healing response is a major contributor to the severity of cutaneous leishmaniasis in the ear model of infection. Parasite Immunol. 2007, 29:501-513.
10. Bevan A.K., et al. Early heart failure in the SMNDelta7 model of spinal muscular atrophy and correction by postnatal scAAV9-SMN delivery. Hum. Mol. Genet. 2010, 19:3895-3905.
11. Buchthal F., Olsen P.Z. Electromyography and muscle biopsy in infantile spinal muscular atrophy. Brain 1970, 93:15-30.
12. Burghes A.H., Beattie C.E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick?. Nat. Rev. Neurosci. 2009, 10:597-609.
13. Butchbach M.E., et al. Abnormal motor phenotype in the SMNDelta7 mouse model of spinal muscular atrophy. Neurobiol. Dis. 2007, 27:207-219.
14. Distefano G., et al. Heart involvement in progressive spinal muscular atrophy. a review of the literature and case histories in childhood. Pediatr. Med. Chir. 1994, 16:125-128.
15. Dominguez E., et al. Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum. Mol. Genet. 2011, 20:681-693.
16. Duque S.I., et al. A large animal model of spinal muscular atrophy and correction of phenotype. Ann. Neurol. 2015, 77:399-414.
17. Eisenberg R.S. Impedance Measurement of the Electrical Structure of Skeletal Muscle. Comprehensive Physiology 2010, John Wiley & Sons, Inc.
18. Elso C.M., et al. Leishmaniasis host response loci (lmr1-3) modify disease severity through a Th1/Th2-independent pathway. Genes Immun. 2004, 5:93-100.
19. Finkel R.S. Electrophysiological and motor function scale association in a pre-symptomatic infant with spinal muscular atrophy type I. Neuromuscul. Disord. 2013, 23:112-115.
20. Finkel R.S., et al. Candidate proteins, metabolites and transcripts in the biomarkers for spinal muscular atrophy (BforSMA) clinical study. PLoS One 2012, 7.
21. Finkel R.S., et al. Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology 2014, 83:810-817.
22. Foust K.D., et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 2010, 28:271-274.
23. Grimnes S., Martinsen Ø.G. Chapter 11 - history of bioimpedance and bioelectricity. Bioimpedance and Bioelectricity Basics (Third Edition) 2015, 495-504. Academic Press, Oxford. S.G.G. Martinsen (Ed.).
24. Harding B.N., et al. Spectrum of neuropathophysiology in spinal muscular atrophy type I. J. Neuropathol. Exp. Neurol. 2015, 74:15-24.
25. Hausmanowa-Petrusewicz I., Karwanska A. Electromyographic findings in different forms of infantile and juvenile proximal spinal muscular atrophy. Muscle Nerve 1986, 9:37-46.
26. Hsieh-Li H.M., et al. A mouse model for spinal muscular atrophy. Nat. Genet. 2000, 24:66-70.
27. Kang P.B., et al. The motor neuron response to SMN1 deficiency in spinal muscular atrophy. Muscle Nerve 2014, 49:636-644.
28. Kaufmann P., et al. Prospective cohort study of spinal muscular atrophy types 2 and 3. Neurology 2012, 79:1889-1897.
29. Kolb S.J., Kissel J.T. Spinal muscular atrophy: a timely review. Arch. Neurol. 2011, 68:979-984.
30. Kubicek W.G., et al. Development and evaluation of an impedance cardiac output system. Aerosp. Med. 1966, 37:1208-1212.
31. Le T.T., et al. SMNδ7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum. Mol. Genet. 2005, 14:845-857.
32. Lefebvre S., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
33. Lewelt A., et al. Compound muscle action potential and motor function in children with spinal muscular atrophy. Muscle Nerve 2010, 42:703-708.
34. Li J., et al. A technique for performing electrical impedance myography in the mouse hind limb: data in normal and ALS SOD1 G93A animals. PLoS One 2012, 7.
35. Li J., et al. Electrical impedance alterations in the rat hind limb with unloading. J. Musculoskelet. Neuronal Interact. 2013, 13:37-44.
36. Li J., et al. A comparison of three electrophysiological methods for the assessment of disease status in a mild spinal muscular atrophy mouse model. PLoS One 2014, 9.
37. Li J., et al. Electrical impedance myography for the in vivo and ex vivo assessment of muscular dystrophy (mdx) mouse muscle. Muscle Nerve 2014, 49:829-835.
38. Ling K.K., et al. Severe neuromuscular denervation of clinically relevant muscles in a mouse model of spinal muscular atrophy. Hum. Mol. Genet. 2012, 21:185-195.
39. Lungu C., et al. Quantifying muscle asymmetries in cervical dystonia with electrical impedance: a preliminary assessment. Clin. Neurophysiol. 2011, 122:1027-1031.
40. McComas A.J., et al. Electrophysiological estimation of the number of motor units within a human muscle. J. Neurol. Neurosurg. Psychiatry 1971, 34:121-131.
41. McGovern V.L., et al. SMN expression is required in motor neurons to rescue electrophysiological deficits in the SMNDelta7 mouse model of SMA. Hum. Mol. Genet. 2015.
42. Naryshkin N.A., et al. Motor neuron disease. SMN2 splicing modifiers improve motor function and longevity in mice with spinal muscular atrophy. Science 2014, 345:688-693.
43. NIH NIH consensus statement. Bioelectrical impedance analysis in body composition measurement. Nutrition 1996, 12:749-762.
44. Palacino J., et al. SMN2 splice modulators enhance U1-pre-mRNA association and rescue SMA mice. Nat. Chem. Biol. 2015, 11:511-517.
45. Passini M.A., et al. Antisense oligonucleotides delivered to the mouse CNS ameliorate symptoms of severe spinal muscular atrophy. Sci. Transl. Med. 2011, 3:72ra18.
46. Pillen S., et al. Assessing spinal muscular atrophy with quantitative ultrasound. Neurology 2011, 76:933. (author reply 933-4).
47. Porensky P.N., et al. A single administration of morpholino antisense oligomer rescues spinal muscular atrophy in mouse. Hum. Mol. Genet. 2012, 21:1625-1638.
48. Poruk K.E., et al. Observational study of caloric and nutrient intake, bone density, and body composition in infants and children with spinal muscular atrophy type I. Neuromuscul. Disord. 2012, 22:966-973.
49. Renusch S.R., et al. Spinal Muscular Atrophy Biomarker Measurements from Blood Samples in a Clinical Trial of Valproic Acid in Ambulatory Adults 2015, vol. 2:119-130. IOS Press.
50. Robbins K.L., et al. Defining the therapeutic window in a severe animal model of spinal muscular atrophy. Hum. Mol. Genet. 2014, 23:4559-4568.
51. Roberts D.F., et al. The genetic component in child mortality. Arch. Dis. Child. 1970, 45:33-38.
52. Rudnik-Schoneborn S., et al. Digital necroses and vascular thrombosis in severe spinal muscular atrophy. Muscle Nerve 2010, 42:144-147.
53. Rutkove S.B. Electrical impedance myography: background, current state, and future directions. Muscle Nerve 2009, 40:936-946.
54. Rutkove S.B., et al. Electrical impedance myography to assess outcome in amyotrophic lateral sclerosis clinical trials. Clin. Neurophysiol. 2007, 118:2413-2418.
55. Rutkove S.B., et al. Characterizing spinal muscular atrophy with electrical impedance myography. Muscle Nerve 2010, 42:915-921.
56. Rutkove S.B., et al. Electrical impedance myography as a biomarker to assess ALS progression. Amyotroph. Lateral Scler. 2012, 13:439-445.
57. Rutkove S.B., et al. Electrical impedance myography in spinal muscular atrophy: a longitudinal study. Muscle Nerve 2012, 45:642-647.
58. Rutkove S.B., et al. Cross-sectional evaluation of electrical impedance myography and quantitative ultrasound for the assessment of Duchenne muscular dystrophy in a clinical trial setting. Pediatr. Neurol. 2014, 51:88-92.
59. Sanchez B., et al. Novel approach of processing electrical bioimpedance data using differential impedance analysis. Med. Eng. Phys. 2013, 35:1349-1357.
60. Sekine K., et al. Numerical calculations for effects of structure of skeletal muscle on frequency-dependence of its electrical admittance and impedance. J. Phys. D. Appl. Phys. 2015, 48:255401.
61. Shababi M., et al. Partial restoration of cardio-vascular defects in a rescued severe model of spinal muscular atrophy. J. Mol. Cell. Cardiol. 2012, 52:1074-1082.
62. Shababi M., et al. Spinal muscular atrophy: a motor neuron disorder or a multi-organ disease?. J. Anat. 2014, 224:15-28.
63. Shefner J.M. Motor unit number estimation in human neurological diseases and animal models. Clin. Neurophysiol. 2001, 112:955-964.
64. Srivastava T., et al. Machine learning algorithms to classify spinal muscular atrophy subtypes. Neurology 2012, 79:358-364.
65. Sung M., et al. The effect of subcutaneous fat on electrical impedance myography when using a handheld electrode array: the case for measuring reactance. Clin. Neurophysiol. 2013, 124:400-404.
66. Swoboda K.J., et al. Natural history of denervation in SMA: relation to age, SMN2 copy number, and function. Ann. Neurol. 2005, 57:704-712.
67. Tarulli A.W., et al. Electrical impedance myography in the assessment of disuse atrophy. Arch. Phys. Med. Rehabil. 2009, 90:1806-1810.
68. Valori C.F., et al. Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci. Transl. Med. 2010, 2:35ra42.
69. Willmott A.D., et al. Fibrillation potential onset in peripheral nerve injury. Muscle Nerve 2012, 46:332-340.
70. Wu J.S., et al. Assessment OF aged mdx mice by electrical impedance myography and magnetic resonance imaging. Muscle Nerve 2015.