Disruption of Basal Lamina Components in Neuromotor Synapses of Children with Spastic Quadriplegic Cerebral Palsy

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Robinson, Karyn G ^a   Mendonca, Janet L ^a   Militar, Jaimee L ^a   Theroux, Mary C ^a   Dabney, Kirk W ^a   Shah, Suken A ^a   Miller, Freeman ^a   Akins, Robert E ^a  

^a NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINERGIC RECEPTOR; LAMININ GAMMA1; MYOGENIN; MYOSIN; MYOSIN HEAVY CHAIN; SYNTROPHIN;

ARTICLE; ATAXIA; BASEMENT MEMBRANE; CEREBRAL PALSY; CHILD; DYSKINESIA; ELECTRON MICROSCOPY; HUMAN; MITOCHONDRION; MOTONEURON; MOTOR CONTROL; NEUROMUSCULAR SYNAPSE; PHENOTYPE; PROSPECTIVE STUDY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUADRIPLEGIA; SCOLIOSIS; TELOMERE; WEAKNESS;

ACETYLCHOLINESTERASE; ADOLESCENT; BASEMENT MEMBRANE; CASE-CONTROL STUDIES; CEREBRAL PALSY; CHILD; FEMALE; GENE EXPRESSION; HUMANS; LAMININ; MALE; MEMBRANE GLYCOPROTEINS; MICROSCOPY, ELECTRON; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PROSPECTIVE STUDIES; RECEPTORS, CHOLINERGIC; SYNAPSES;

EID: 84881592209     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070288     Document Type: Article

References (80)

1. O'Shea TM, (2008) Diagnosis, treatment, and prevention of cerebral palsy. Clin Obstet Gynecol 51: 816-828.
2. Badawi N, Watson L, Petterson B, Blair E, Slee J, et al. (1998) What constitutes cerebral palsy? Dev Med Child Neurol 40: 520-527.
3. Koman LA, Smith BP, Shilt JS, (2004) Cerebral palsy. Lancet 363: 1619-1631.
4. Odding E, Roebroeck ME, Stam HJ, (2006) The epidemiology of cerebral palsy: incidence, impairments and risk factors. Disabil Rehabil 28: 183-191.
5. Rotundo RL, Rossi SG, Kimbell LM, Ruiz C, Marrero E, (2005) Targeting acetylcholinesterase to the neuromuscular synapse. Chem Biol Interact 157-158: 15-21.
6. Hepaguslar H, Ozzeybek D, Elar Z, (1999) The effect of cerebral palsy on the action of vecuronium with or without anticonvulsants. Anaesthesia 54: 593-596.
7. Theroux MC, Brandom BW, Zagnoev M, Kettrick RG, Miller F, et al. (1994) Dose response of succinylcholine at the adductor pollicis of children with cerebral palsy during propofol and nitrous oxide anesthesia. Anesth Analg 79: 761-765.
8. Smith LR, Ponten E, Hedstrom Y, Ward SR, Chambers HG, et al. (2009) Novel transcriptional profile in wrist muscles from cerebral palsy patients. BMC Med Genomics 2: 44.
9. Theroux MC, Akins RE, Barone C, Boyce B, Miller F, et al. (2002) Neuromuscular junctions in cerebral palsy: presence of extrajunctional acetylcholine receptors. Anesthesiology 96: 330-335.
10. Theroux MC, Oberman KG, Lahaye J, Boyce BA, Duhadaway D, et al. (2005) Dysmorphic neuromuscular junctions associated with motor ability in cerebral palsy. Muscle Nerve 32: 626-632.
11. Sanes JR, Lichtman JW, (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389-442.
12. Sanes JR, Lichtman JW, (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2: 791-805.
13. Taniguchi M, Kurahashi H, Noguchi S, Fukudome T, Okinaga T, et al. (2006) Aberrant neuromuscular junctions and delayed terminal muscle fiber maturation in alpha-dystroglycanopathies. Hum Mol Genet 15: 1279-1289.
14. Levitt-Gilmour TA, Salpeter MM, (1986) Gradient of extrajunctional acetylcholine receptors early after denervation of mammalian muscle. J Neurosci 6: 1606-1612.
15. Kramarcy NR, Sealock R, (2000) Syntrophin isoforms at the neuromuscular junction: developmental time course and differential localization. Mol Cell Neurosci 15: 262-274.
16. Gu Y, Hall ZW, (1988) Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1: 117-125.
17. Leinwand LA, Saez L, McNally E, Nadal-Ginard B, (1983) Isolation and characterization of human myosin heavy chain genes. Proc Natl Acad Sci U S A 80: 3716-3720.
18. Mishina M, Takai T, Imoto K, Noda M, Takahashi T, et al. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321: 406-411.
19. Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP, (1996) Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev Biol 179: 223-238.
20. Wright WE, Sassoon DA, Lin VK, (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607-617.
21. Brooke MH, Kaiser KK, (1970) Three "myosin adenosine triphosphatase" systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18: 670-672.
22. Biral D, Betto R, Danieli-Betto D, Salviati G, (1988) Myosin heavy chain composition of single fibres from normal human muscle. Biochem J 250: 307-308.
23. Cawthon RM, (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30: e47.
24. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
25. Modla S, Mendonca J, Czymmek KJ, Akins RE, (2010) Identification of neuromuscular junctions by correlative confocal and transmission electron microscopy. J Neurosci Methods 191: 158-165.
26. Rasband WS (2010) ImageJ. U. S. National Institutes of Health, Bethesda, MD, USA. Available: http://imagej.nih.gov/ij/.
27. Banks GB, Chamberlain JS, Froehner SC, (2009) Truncated dystrophins can influence neuromuscular synapse structure. Mol Cell Neurosci 40: 433-441.
28. Rotundo RL, (2003) Expression and localization of acetylcholinesterase at the neuromuscular junction. J Neurocytol 32: 743-766.
29. Nishimune H, Valdez G, Jarad G, Moulson CL, Muller U, et al. (2008) Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. J Cell Biol 182: 1201-1215.
30. Patton BL, (2000) Laminins of the neuromuscular system. Microsc Res Tech 51: 247-261.
31. Patton BL, (2003) Basal lamina and the organization of neuromuscular synapses. J Neurocytol 32: 883-903.
32. Karpati G, Engel WK, (1968) Histochemical investigation of fiber type ratios with the myofibrillar ATP-ase reaction in normal and denervated skeletal muscles of guinea pig. Am J Anat 122: 145-155.
33. Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL, (2011) Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol 589: 2625-2639.
34. Johnson DL, Miller F, Subramanian P, Modlesky CM, (2009) Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr 154: 715-720.
35. Marbini A, Ferrari A, Cioni G, Bellanova MF, Fusco C, et al. (2002) Immunohistochemical study of muscle biopsy in children with cerebral palsy. Brain Dev 24: 63-66.
36. Ito J, Araki A, Tanaka H, Tasaki T, Cho K, et al. (1996) Muscle histopathology in spastic cerebral palsy. Brain Dev 18: 299-303.
37. Coers C, Telerman-Toppet N, (1977) Morphological changes of motor units in Duchenne's muscular dystrophy. Arch Neurol 34: 396-402.
38. Kihira S, Nonaka I, (1985) Congenital muscular dystrophy. A histochemical study with morphometric analysis on biopsied muscles. J Neurol Sci 70: 139-149.
39. Karsch-Mizrachi I, Travis M, Blau H, Leinwand LA, (1989) Expression and DNA sequence analysis of a human embryonic skeletal muscle myosin heavy chain gene. Nucleic Acids Res 17: 6167-6179.
40. Marinou M, Tzartos SJ, (2003) Identification of regions involved in the binding of alpha-bungarotoxin to the human alpha7 neuronal nicotinic acetylcholine receptor using synthetic peptides. Biochem J 372: 543-554.
41. Fischer U, Reinhardt S, Albuquerque EX, Maelicke A, (1999) Expression of functional alpha7 nicotinic acetylcholine receptor during mammalian muscle development and denervation. Eur J Neurosci 11: 2856-2864.
42. Nizri E, Wirguin I, Brenner T, (2007) The role of cholinergic balance perturbation in neurological diseases. Drug News Perspect 20: 421-429.
43. Mouly V, Aamiri A, Bigot A, Cooper RN, Di Donna S, et al. (2005) The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy. Acta Physiol Scand 184: 3-15.
44. Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, et al. (1997) Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther 8: 1429-1438.
45. Lee CW, Peng HB, (2006) Mitochondrial clustering at the vertebrate neuromuscular junction during presynaptic differentiation. J Neurobiol 66: 522-536.
46. Lee CW, Peng HB, (2008) The function of mitochondria in presynaptic development at the neuromuscular junction. Mol Biol Cell 19: 150-158.
47. Kann O, Kovacs R, (2007) Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292: C641-657.
48. Wallace BG, (1989) Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J Neurosci 9: 1294-1302.
49. Strochlic L, Cartaud A, Mejat A, Grailhe R, Schaeffer L, et al. (2004) 14-3-3 gamma associates with muscle specific kinase and regulates synaptic gene transcription at vertebrate neuromuscular synapse. Proc Natl Acad Sci U S A 101: 18189-18194.
50. Wewer UM, Thornell LE, Loechel F, Zhang X, Durkin ME, et al. (1997) Extrasynaptic location of laminin beta 2 chain in developing and adult human skeletal muscle. Am J Pathol 151: 621-631.
51. Patton BL, Miner JH, Chiu AY, Sanes JR, (1997) Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139: 1507-1521.
52. Nishimune H, Sanes JR, Carlson SS, (2004) A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432: 580-587.
53. Chen J, Billings SE, Nishimune H, (2011) Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J Neurosci 31: 512-525.
54. Patton BL, Chiu AY, Sanes JR, (1998) Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393: 698-701.
55. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP, (1995) Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374: 258-262.
56. Maselli RA, Ng JJ, Anderson JA, Cagney O, Arredondo J, et al. (2009) Mutations in LAMB2 causing a severe form of synaptic congenital myasthenic syndrome. J Med Genet 46: 203-208.
57. Ohno K, Brengman J, Tsujino A, Engel AG, (1998) Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like tail subunit (ColQ) of the asymmetric enzyme. Proc Natl Acad Sci U S A 95: 9654-9659.
58. Stackhouse SK, Binder-Macleod SA, Stackhouse CA, McCarthy JJ, Prosser LA, et al. (2007) Neuromuscular electrical stimulation versus volitional isometric strength training in children with spastic diplegic cerebral palsy: a preliminary study. Neurorehabil Neural Repair 21: 475-485.
59. Stackhouse SK, Binder-Macleod SA, Lee SC, (2005) Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 31: 594-601.
60. Foran JR, Steinman S, Barash I, Chambers HG, Lieber RL, (2005) Structural and mechanical alterations in spastic skeletal muscle. Dev Med Child Neurol 47: 713-717.
61. Nishizawa T, Tamaki H, Kasuga N, Takekura H, (2003) Degeneration and regeneration of neuromuscular junction architecture in rat skeletal muscle fibers damaged by bupivacaine hydrochloride. J Muscle Res Cell Motil 24: 527-537.
62. Decary S, Hamida CB, Mouly V, Barbet JP, Hentati F, et al. (2000) Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 10: 113-120.
63. Rose J, Haskell WL, Gamble JG, Hamilton RL, Brown DA, et al. (1994) Muscle pathology and clinical measures of disability in children with cerebral palsy. J Orthop Res 12: 758-768.
64. Tsuneki H, Salas R, Dani JA, (2003) Mouse muscle denervation increases expression of an alpha7 nicotinic receptor with unusual pharmacology. J Physiol 547: 169-179.
65. Compton AG, Cooper ST, Hill PM, Yang N, Froehner SC, et al. (2005) The syntrophin-dystrobrevin subcomplex in human neuromuscular disorders. J Neuropathol Exp Neurol 64: 350-361.
66. Okuhira K, Fitzgerald ML, Tamehiro N, Ohoka N, Suzuki K, et al. Binding of PDZ-RhoGEF to ATP-binding cassette transporter A1 (ABCA1) induces cholesterol efflux through RhoA activation and prevention of transporter degradation. J Biol Chem 285: 16369-16377.
67. Slater C, Fawcett P, Walls T, Lyons P, Bailey S, et al. (2006) Pre- and post-synaptic abnormalities associated with impaired neuromuscular transmission in a group of patients with 'limb-girdle myasthenia'. Brain 129: 2061-2076.
68. Nelson PG, Fields RD, Yu C, Liu Y, (1993) Synapse elimination from the mouse neuromuscular junction in vitro: a non-Hebbian activity-dependent process. J Neurobiol 24: 1517-1530.
69. Yang YM, Liu GT, (2003) Injury of mouse brain mitochondria induced by cigarette smoke extract and effect of vitamin C on it in vitro. Biomed Environ Sci 16: 256-266.
70. Todd KJ, Robitaille R, (2006) Purinergic modulation of synaptic signalling at the neuromuscular junction. Pflugers Arch 452: 608-614.
71. Slater C, Lyons P, Walls T, Fawcett P, Young C, (1992) Structure and function of neuromuscular junctions in the vastus lateralis of man. A motor point biopsy study of two groups of patients. Brain 115: 451-478.
72. Patton BL, Cunningham JM, Thyboll J, Kortesmaa J, Westerblad H, et al. (2001) Properly formed but improperly localized synaptic specializations in the absence of laminin alpha4. Nat Neurosci 4: 597-604.
73. Knight D, Tolley LK, Kim DK, Lavidis NA, Noakes PG, (2003) Functional analysis of neurotransmission at beta2-laminin deficient terminals. J Physiol 546: 789-800.
74. Miner JH, Cunningham J, Sanes JR, (1998) Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol 143: 1713-1723.
75. Cho SI, Ko J, Patton BL, Sanes JR, Chiu AY, (1998) Motor neurons and Schwann cells distinguish between synaptic and extrasynaptic isoforms of laminin. J Neurobiol 37: 339-358.
76. Patton BL, Connoll AM, Martin PT, Cunningham JM, Mehta S, et al. (1999) Distribution of ten laminin chains in dystrophic and regenerating muscles. Neuromuscul Disord 9: 423-433.
77. Bewick GS, Nicholson LV, Young C, O'Donnell E, Slater CR, (1992) Different distributions of dystrophin and related proteins at nerve-muscle junctions. Neuroreport 3: 857-860.
78. Peters MF, Sadoulet-Puccio HM, Grady MR, Kramarcy NR, Kunkel LM, et al. (1998) Differential membrane localization and intermolecular associations of alpha-dystrobrevin isoforms in skeletal muscle. J Cell Biol 142: 1269-1278.
79. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, et al. (1997) Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 136: 883-894.
80. Grady RM, Merlie JP, Sanes JR, (1997) Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 136: 871-882.