Protein-anchoring strategy for delivering acetylcholinesterase to the neuromuscular junction

Molecular Therapy

Volumn 20, Issue 7, 2012, Pages 1384-1392

  Ito, Mikako ^a   Suzuki, Yumi ^a   Okada, Takashi ^b   Fukudome, Takayasu ^c   Yoshimura, Toshiro ^d   Masuda, Akio ^a   Takeda, Shin'Ichi ^b   Krejci, Eric ^e   Ohno, Kinji ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^c Nagasaki Kawatana Medical Center   (Japan)

^d NAGASAKI UNIVERSITY   (Japan)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; COLLAGEN; COLLAGEN Q; CYCLOPHOSPHAMIDE; ENHANCED GREEN FLUORESCENT PROTEIN; NEOSTIGMINE; UNCLASSIFIED DRUG;

ACETYLCHOLINESTERASE DEFICIENCY; ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS SEROTYPE 8; ANIMAL CELL; BASEMENT MEMBRANE; CONFERENCE PAPER; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; ENDPLATE POTENTIAL; ENZYME DEFICIENCY; ENZYME RELEASE; EXTRACELLULAR MATRIX; GENE THERAPY; GLUTEUS MAXIMUS MUSCLE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MOTOR PERFORMANCE; MOUSE; MUSCLE ACTION POTENTIAL; NEUROMUSCULAR SYNAPSE; NONHUMAN; PHENOTYPE; PROTEIN TRANSPORT; ROTAROD TEST; SEDIMENTATION; SEROTYPE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TIBIALIS ANTERIOR MUSCLE;

ADENO-ASSOCIATED VIRUS; MUS;

EID: 84863441080     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.34     Document Type: Article

References (46)

1. Krejci, E, Thomine, S, Boschetti, N, Legay, C, Sketelj, J and Massoulié, J (1997). The mammalian gene of acetylcholinesterase- associated collagen. J Biol Chem 272: 22840-22847. (Pubitemid 27386105)
2. Rotundo, RL (1984). Asymmetric acetylcholinesterase is assembled in the Golgi apparatus. Proc Natl Acad Sci USA 81: 479-483. (Pubitemid 14186587)
3. Ruiz, CA and Rotundo, RL (2009). Limiting role of protein disulfide isomerase in the expression of collagen-tailed acetylcholinesterase forms in muscle. J Biol Chem 284: 31753-31763.
4. Deprez, P, Inestrosa, NC and Krejci, E (2003). Two different heparin-binding domains in the triple-helical domain of ColQ, the collagen tail subunit of synaptic acetylcholinesterase. J Biol Chem 278: 23233-23242. (Pubitemid 36830136)
5. Peng, HB, Xie, H, Rossi, SG and Rotundo, RL (1999). Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 145: 911-921. (Pubitemid 29240865)
6. Cartaud, A, Strochlic, L, Guerra, M, Blanchard, B, Lambergeon, M, Krejci, E et al. (2004). MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J Cell Biol 165: 505-515. (Pubitemid 38679616)
7. Ohno, K, Brengman, J, Tsujino, A and 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 USA 95: 9654-9659. (Pubitemid 28506287)
8. Donger, C, Krejci, E, Serradell, AP, Eymard, B, Bon, S, Nicole, S et al. (1998). Mutation in the human acetylcholinesterase-associated collagen gene, COLQ, is responsible for congenital myasthenic syndrome with end-plate acetylcholinesterase deficiency (Type Ic). Am J Hum Genet 63: 967-975. (Pubitemid 30418565)
9. Ohno, K, Engel, AG, Brengman, JM, Shen, XM, Heidenreich, F, Vincent, A et al. (2000). The spectrum of mutations causing end-plate acetylcholinesterase deficiency. Ann Neurol 47: 162-170. (Pubitemid 30078562)
10. Bestue-Cardiel, M, Sáenz de Cabezón-Alvarez, A, Capablo-Liesa, JL, López-Pisón, J, Peña-Segura, JL, Martin-Martinez, J et al. (2005). Congenital endplate acetylcholinesterase deficiency responsive to ephedrine. Neurology 65: 144-146. (Pubitemid 40967793)
11. Mihaylova, V, Müller, JS, Vilchez, JJ, Salih, MA, Kabiraj, MM, D'Amico, A et al. (2008). Clinical and molecular genetic findings in COLQ-mutant congenital myasthenic syndromes. Brain 131(Pt 3): 747-759. (Pubitemid 351294715)
12. Feng, G, Krejci, E, Molgo, J, Cunningham, JM, Massoulié, J and Sanes, JR (1999). Genetic analysis of collagen Q: roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J Cell Biol 144: 1349-1360. (Pubitemid 29157310)
13. Lee, HH, Choi, RC, Ting, AK, Siow, NL, Jiang, JX, Massoulié, J et al. (2004). Transcriptional regulation of acetylcholinesterase-associated collagen ColQ: differential expression in fast and slow twitch muscle fibers is driven by distinct promoters. J Biol Chem 279: 27098-27107. (Pubitemid 38812546)
14. Ruiz, CA and Rotundo, RL (2009). Dissociation of transcription, translation, and assembly of collagen-tailed acetylcholinesterase in skeletal muscle. J Biol Chem 284: 21488-21495.
15. Inagaki, K, Fuess, S, Storm, TA, Gibson, GA, Mctiernan, CF, Kay, MA et al. (2006). Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 14: 45-53. (Pubitemid 43899488)
16. Nakai, H, Fuess, S, Storm, TA, Muramatsu, S, Nara, Y and Kay, MA (2005). Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol 79: 214-224. (Pubitemid 39650967)
17. Bouma, SR, Drislane, FW and Huestis, WH (1977). Selective extraction of membranebound proteins by phospholipid vesicles. J Biol Chem 252: 6759-6763. (Pubitemid 8200434)
18. Kimbell, LM, Ohno, K, Engel, AG and Rotundo, RL (2004). C-terminal and heparin-binding domains of collagenic tail subunit are both essential for anchoring acetylcholinesterase at the synapse. J Biol Chem 279: 10997-11005. (Pubitemid 38401591)
19. Wang, Z, Zhu, T, Qiao, C, Zhou, L, Wang, B, Zhang, J et al. (2005). Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 23: 321-328. (Pubitemid 41094420)
20. Schnepp, BC, Clark, KR, Klemanski, DL, Pacak, CA and Johnson, PR (2003). Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J Virol 77: 3495-3504. (Pubitemid 36297269)
21. Kay, MA (2007). AAV vectors and tumorigenicity. Nat Biotechnol 25: 1111-1113. (Pubitemid 47538108)
22. Xiao, X, Li, J and Samulski, RJ (1996). Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol 70: 8098-8108. (Pubitemid 26339120)
23. Rivière, C, Danos, O and Douar, AM (2006). Long-term expression and repeated administration of AAV type 1, 2 and 5 vectors in skeletal muscle of immunocompetent adult mice. Gene Ther 13: 1300-1308. (Pubitemid 44264084)
24. Krejci, E, Legay, C, Thomine, S, Sketelj, J and Massoulié, J (1999). Differences in expression of acetylcholinesterase and collagen Q control the distribution and oligomerization of the collagen-tailed forms in fast and slow muscles. J Neurosci 19: 10672-10679. (Pubitemid 30235714)
25. Lau, FT, Choi, RC, Xie, HQ, Leung, KW, Chen, VP, Zhu, JT et al. (2008). Myocyte enhancer factor 2 mediates acetylcholine-induced expression of acetylcholinesteraseassociated collagen ColQ in cultured myotubes. Mol Cell Neurosci 39: 429-438.
26. Arikawa-Hirasawa, E, Rossi, SG, Rotundo, RL and Yamada, Y (2002). Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat Neurosci 5: 119-123. (Pubitemid 34121578)
27. Stum, M, Girard, E, Bangratz, M, Bernard, V, Herbin, M, Vignaud, A et al. (2008). Evidence of a dosage effect and a physiological endplate acetylcholinesterase deficiency in the first mouse models mimicking Schwartz-Jampel syndrome neuromyotonia. Hum Mol Genet 17: 3166-3179.
28. Rotundo, RL, Rossi, SG and Anglister, L (1997). Transplantation of quail collagen-tailed acetylcholinesterase molecules onto the frog neuromuscular synapse. J Cell Biol 136: 367-374. (Pubitemid 27063086)
29. Moretti, FA, Chauhan, AK, Iaconcig, A, Porro, F, Baralle, FE and Muro, AF (2007). A major fraction of fibronectin present in the extracellular matrix of tissues is plasmaderived. J Biol Chem 282: 28057-28062. (Pubitemid 47529518)
30. Rooney, JE, Gurpur, PB and Burkin, DJ (2009). Laminin-111 protein therapy prevents muscle disease in the mdx mouse model for Duchenne muscular dystrophy. Proc Natl Acad Sci USA 106: 7991-7996.
31. Hall, ZW and Ralston, E (1989). Nuclear domains in muscle cells. Cell 59: 771-772. (Pubitemid 20022367)
32. Rossi, SG, Vazquez, AE and Rotundo, RL (2000). Local control of acetylcholinesterase gene expression in multinucleated skeletal muscle fibers: individual nuclei respond to signals from the overlying plasma membrane. J Neurosci 20: 919-928. (Pubitemid 30220448)
33. Miner, JH, Go, G, Cunningham, J, Patton, BL and Jarad, G (2006). Transgenic isolation of skeletal muscle and kidney defects in laminin beta2 mutant mice: implications for Pierson syndrome. Development 133: 967-975.
34. Somia, N and Verma, IM (2000). Gene therapy: trials and tribulations. Nat Rev Genet 1: 91-99.
35. Mueller, C and Flotte, TR (2008). Clinical gene therapy using recombinant adenoassociated virus vectors. Gene Ther 15: 858-863. (Pubitemid 351712619)
36. Helbling-Leclerc, A, Zhang, X, Topaloglu, H, Cruaud, C, Tesson, F, Weissenbach, J et al. (1995). Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat Genet 11: 216-218.
37. Nicole, S, Davoine, CS, Topaloglu, H, Cattolico, L, Barral, D, Beighton, P et al. (2000). Perlecan, the major proteoglycan of basement membranes, is altered in patients with Schwartz-Jampel syndrome (chondrodystrophic myotonia). Nat Genet 26: 480-483.
38. Kawahara, G, Okada, M, Morone, N, Ibarra, CA, Nonaka, I, Noguchi, S et al. (2007). Reduced cell anchorage may cause sarcolemma-specific collagen VI deficiency in Ullrich disease. Neurology 69: 1043-1049. (Pubitemid 47366059)
39. Okada, T, Nomoto, T, Yoshioka, T, Nonaka-Sarukawa, M, Ito, T, Ogura, T et al. (2005). Large-scale production of recombinant viruses by use of a large culture vessel with active gassing. Hum Gene Ther 16: 1212-1218. (Pubitemid 41443713)
40. Okada, T, Shimazaki, K, Nomoto, T, Matsushita, T, Mizukami, H, Urabe, M et al. (2002). Adeno-associated viral vector-mediated gene therapy of ischemia-induced neuronal death. Meth Enzymol 346: 378-393. (Pubitemid 41103149)
41. Okada, T, Nonaka-Sarukawa, M, Uchibori, R, Kinoshita, K, Hayashita-Kinoh, H, Nitahara-Kasahara, Y et al. (2009). Scalable purification of adeno-associated virus serotype 1 (AAV1) and AAV8 vectors, using dual ion-exchange adsorptive membranes. Hum Gene Ther 20: 1013-1021.
42. Rohr, UP, Wulf, MA, Stahn, S, Steidl, U, Haas, R and Kronenwett, R (2002). Fast and reliable titration of recombinant adeno-associated virus type-2 using quantitative realtime PCR. J Virol Methods 106: 81-88. (Pubitemid 35279652)
43. Engel, AG, Nagel, A, Walls, TJ, Harper, CM and Waisburg, HA (1993). Congenital myasthenic syndromes: I. Deficiency and short open-time of the acetylcholine receptor. Muscle Nerve 16: 1284-1292. (Pubitemid 23351078)
44. Engel, AG and Santa, T (1971). Histometric analysis of the ultrastructure of the neuromuscular junction in myasthenia gravis and in the myasthenic syndrome. Ann N Y Acad Sci 183: 46-63.
45. Engel, AG, Lindstrom, JM, Lambert, EH and Lennon, VA (1977). Ultrastructural localization of the acetylcholine receptor in myasthenia gravis and in its experimental autoimmune model. Neurology 27: 307-315. (Pubitemid 8200085)
46. Otterness, IG and Chang, YH (1976). Comparative study of cyclophosphamide, 6-mercaptopurine, azathiopurine and methotrexate. Relative effects on the humoral and the cellular immune response in the mouse. Clin Exp Immunol 26: 346-354.