Synaptic defects in type i spinal muscular atrophy in human development

Journal of Pathology

Volumn 229, Issue 1, 2013, Pages 49-61

  Martínez Hernández, Rebeca ^a   Bernal, Sara ^a   Also Rallo, Eva ^a   Alías, Laura ^a,b   Barcelõ, Majesús ^a,b   Hereu, Marta ^c   Esquerda, Josep E ^c   Tizzano, Eduardo F ^a,b  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c UNIVERSITY OF LLEIDA   (Spain)

Author keywords

acetylcholine receptor; human development; neuromuscular junction; spinal muscular atrophy

Indexed keywords

CHOLINERGIC RECEPTOR; SURVIVAL MOTOR NEURON PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FETUS; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL MUSCULAR ATROPHY;

CASE-CONTROL STUDIES; GENETIC PREDISPOSITION TO DISEASE; GESTATIONAL AGE; HUMANS; INFANT; INFANT, NEWBORN; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MORPHOGENESIS; MOTOR ENDPLATE; MOTOR NEURONS; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; PHENOTYPE; PRESYNAPTIC TERMINALS; RECEPTORS, CHOLINERGIC; SEVERITY OF ILLNESS INDEX; SPINAL MUSCULAR ATROPHIES OF CHILDHOOD;

EID: 84872862067     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4080     Document Type: Article

References (53)

1. Cusin V, Clermont O, Gerard B, et al., Prevalence of SMN1 deletion and duplication in carrier and normal populations: implication for genetic counselling. J Med Genet 2003; 40: E39.
2. Munsat TL, Davies KE,. International SMA consortium meeting (26-28 June 1992, Bonn, Germany). Neuromuscul Disord 1992; 2: 423-428.
3. Zerres K, Rudnik-Schoneborn S,. Natural history in proximal spinal muscular atrophy. Clinical analysis of 445 patients and suggestions for a modification of existing classifications. Arch Neurol 1995; 52: 518-523.
4. Fidzianska A,. Ultrastructural changes in muscle in spinal muscular atrophy. Werdnig-Hoffmann's disease. Acta Neuropathol 1974; 27: 247-256.
5. Fidzianska A,. Morphological differences between the atrophied small muscle fibres in amyotrophic lateral sclerosis and Werdnig-Hoffmann disease. Acta Neuropathol 1976; 34: 321-327.
6. Crawford TO, Pardo CA,. The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis 1996; 3: 97-110.
7. Lippa CF, Smith TW,. Chromatolytic neurons in Werdnig-Hoffmann disease contain phosphorylated neurofilaments. Acta Neuropathol 1988; 77: 91-94.
8. Lefebvre S, Burglen L, Reboullet S, et al., Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995; 80: 155-165.
9. Brahe C,. Copies of the survival motor neuron gene in spinal muscular atrophy: the more, the better. Neuromuscul Disord 2000; 10: 274-275.
10. Liu Q, Dreyfuss G,. A novel nuclear structure containing the survival of motor neurons protein. EMBO J 1996; 15: 3555-3565.
11. Burlet P, Huber C, Bertrandy S, et al., The distribution of SMN protein complex in human fetal tissues and its alteration in spinal muscular atrophy. Hum Mol Genet 1998; 7: 1927-1933.
12. Coovert DD, Le TT, McAndrew PE, et al., The survival motor neuron protein in spinal muscular atrophy. Hum Mol Genet 1997; 6: 1205-1214.
13. Soler-Botija C, Cusco I, Caselles L, et al., Implication of fetal SMN2 expression in type I SMA pathogenesis: protection or pathological gain of function? J Neuropathol Exp Neurol 2005; 64: 215-223.
14. Hausmanowa-Petrusewicz I, Vrbova G,. Spinal muscular atrophy: a delayed development hypothesis. Neuroreport 2005; 16: 657-661.
15. Martinez-Hernandez R, Soler-Botija C, Also E, et al., The developmental pattern of myotubes in spinal muscular atrophy indicates prenatal delay of muscle maturation. J Neuropathol Exp Neurol 2009; 68: 474-481.
16. Lewelt A, Krosschell KJ, Scott C, et al., Compound muscle action potential and motor function in children with spinal muscular atrophy. Muscle Nerve 2010; 42: 703-708.
17. Swoboda KJ, Prior TW, Scott CB, et al., Natural history of denervation in SMA: relation to age, SMN2 copy number, and function. Ann Neurol 2005; 57: 704-712.
18. Greensmith L, Vrbova G,. Disturbances of neuromuscular interaction may contribute to muscle weakness in spinal muscular atrophy. Neuromuscul Disord 1997; 7: 369-372.
19. Sleigh JN, Gillingwater TH, Talbot K,. The contribution of mouse models to understanding the pathogenesis of spinal muscular atrophy. Dis Model Mech 2011; 4: 457-467.
20. van der Steege G, Grootscholten PM, van der Vlies P, et al., PCR-based DNA test to confirm clinical diagnosis of autosomal recessive spinal muscular atrophy. Lancet 1995; 345: 985-986.
21. Hesselmans LF, Jennekens FG, Van den Oord CJ, et al., Development of innervation of skeletal muscle fibers in man: relation to acetylcholine receptors. Anat Rec 1993; 236: 553-562.
22. Liu Y, Padgett D, Takahashi M, et al., Essential roles of the acetylcholine receptor gamma-subunit in neuromuscular synaptic patterning. Development 2008; 135: 1957-1967.
23. Cusco I, Barcelo MJ, Rojas-Garcia R, et al., SMN2 copy number predicts acute or chronic spinal muscular atrophy but does not account for intrafamilial variability in siblings. J Neurol 2006; 253: 21-25.
24. Feldkotter M, Schwarzer V, Wirth R, et al., Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet 2002; 70: 358-368.
25. Sanes JR, Lichtman JW,. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nature Rev Neurosci 2001; 2: 791-805.
26. Witzemann V,. Development of the neuromuscular junction. Cell Tissue Res 2006; 326: 263-271.
27. Kong L, Wang X, Choe DW, et al., Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 2009; 29: 842-851.
28. Dachs E, Hereu M, Piedrafita L, et al., Defective neuromuscular junction organization and postnatal myogenesis in mice with severe spinal muscular atrophy. J Neuropathol Exp Neurol 2011; 70: 444-461.
29. Ling KK, Lin MY, Zingg B, et al., Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS One 2010; 5: e15457.
30. 2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J Neurosci 2010; 30: 849-857.
31. Coërs C, Woolf AL,. The Innervation of Muscle. A Biopsy Study. Blackwell Scientific Publications: Oxford, 1959.
32. Tarrade A, Fassier C, Courageot S, et al., A mutation of spastin is responsible for swellings and impairment of transport in a region of axon characterized by changes in microtubule composition. Hum Mol Genet 2006; 15: 3544-3558.
33. Rossoll W, Jablonka S, Andreassi C, et al., Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 2003; 163: 801-812.
34. Zhang H, Xing L, Rossoll W, et al., Multiprotein complexes of the survival of motor neuron protein SMN with Gemins traffic to neuronal processes and growth cones of motor neurons. J Neurosci 2006; 26: 8622-8632.
35. Gattenlohner S, Schneider C, Thamer C, et al., Expression of foetal type acetylcholine receptor is restricted to type 1 muscle fibres in human neuromuscular disorders. Brain 2002; 125: 1309-1319.
36. Arnold AS, Gueye M, Guettier-Sigrist S, et al., Reduced expression of nicotinic AChRS in myotubes from spinal muscular atrophy I patients. Lab Invest 2004; 84: 1271-1278.
37. Kariya S, Park GH, Maeno-Hikichi Y, et al., Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet 2008; 17: 2552-2569.
38. Cifuentes-Diaz C, Nicole S, Velasco ME, et al., Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum Mol Genet 2002; 11: 1439-1447.
39. Ling KK, Gibbs RM, Feng Z, et al., Severe neuromuscular denervation of clinically relevant muscles in a mouse model of spinal muscular atrophy. Hum Mol Genet 2012; 21: 185-195.
40. Mcgovern VL, Gavrilina TO, Beattie CE, et al., Embryonic motor axon development in the severe SMA mouse. Hum Mol Genet 2008; 17: 2900-2909.
41. Murray LM, Comley LH, Thomson D, et al., Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum Mol Genet 2008; 17: 949-962.
42. Lefebvre S, Burlet P, Liu Q, et al., Correlation between severity and SMN protein level in spinal muscular atrophy. Nature Genet 1997; 16: 265-269.
43. Young PJ, Le TT, Dunckley M, et al., Nuclear gems and Cajal (coiled) bodies in fetal tissues: nucleolar distribution of the spinal muscular atrophy protein, SMN. Exp Cell Res 2001; 265: 252-261.
44. Fan L, Simard LR,. Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development. Hum Mol Genet 2002; 11: 1605-1614.
45. Casanovas A, Ribera J, Hukkanen M, et al., Prevention by lamotrigine, MK-801 and N omega-nitro-L-arginine methyl ester of motoneuron cell death after neonatal axotomy. Neuroscience 1996; 71: 313-325.
46. Lowrie MB, Vrbova G,. Dependence of postnatal motoneurones on their targets: review and hypothesis. Trends Neurosci 1992; 15: 80-84.
47. Sendtner M, Kreutzberg GW, Thoenen H,. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 1990; 345: 440-441.
48. Fidzianska A, Rafalowska J,. Motoneuron death in normal and spinal muscular atrophy-affected human fetuses. Acta Neuropathol 2002; 104: 363-368.
49. Soler-Botija C, Ferrer I, Alvarez JL, et al., Downregulation of Bcl-2 proteins in type I spinal muscular atrophy motor neurons during fetal development. J Neuropathol Exp Neurol 2003; 62: 420-426.
50. Soler-Botija C, Ferrer I, Gich I, et al., Neuronal death is enhanced and begins during foetal development in type I spinal muscular atrophy spinal cord. Brain 2002; 125: 1624-1634.
51. Soler-Botija C, Cusco I, Lopez E, et al., Choline acetyltransferase expression does not identify early pathogenic events in fetal SMA spinal cord. Neuromuscul Disord 2005; 15: 253-258.
52. Parra J, Martinez-Hernandez R, Also-Rallo E, et al., Ultrasound evaluation of fetal movements in pregnancies at risk for severe spinal muscular atrophy. Neuromuscul Disord 2011; 21: 97-101.
53. Rosenthal JL, Taraskevich PS,. Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. J Physiol 1977; 270: 299-310.