LG2 agrin mutation causing severe congenital myasthenic syndrome mimics functional characteristics of non-neural (z-) agrin

Human Genetics

Volumn 131, Issue 7, 2012, Pages 1123-1135

  Maselli, Ricardo A ^a   Fernandez, Jose M ^b   Arredondo, Juan ^a   Navarro, Carmen ^c   Ngo, Maian ^a   Beeson, David ^d   Cagney, Órla ^a   Williams, D Colette ^e   Wollmann, Robert L ^f   Yarov Yarovoy, Vladimir ^a   Ferns, Michael J ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University Hospital of Vigo   (Spain)

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

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; AGRIN; ALPHA DYSTROGLYCAN; CHOLINERGIC RECEPTOR; LAMININ G2 AGRIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CONGENITAL MYASTHENIC SYNDROME; CONTROLLED STUDY; CYTOPLASM; DISPERSION; GENE FUNCTION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MUSCLE CELL; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ACETYLCHOLINESTERASE; ADULT; AGRIN; BASE SEQUENCE; CELL LINE; CODON, NONSENSE; DYSTROGLYCANS; FEMALE; HEK293 CELLS; HUMANS; MALE; MODELS, MOLECULAR; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUTATION, MISSENSE; MYASTHENIC SYNDROMES, CONGENITAL; NEUROMUSCULAR JUNCTION; PEDIGREE; RECEPTORS, CHOLINERGIC; SEQUENCE ANALYSIS, DNA;

EID: 84862768198     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-011-1132-4     Document Type: Article

References (43)

1. JA Anderson JJ Ng C Bowe C McDonald DP Richman RL Wollmann RA Maselli 2008 Variable phenotypes associated with mutations in DOK7 Muscle Nerve 37 4 448 456 10.1002/mus.20944 18161030 10.1002/mus.20944 1:CAS:528:DC%2BD1cXltlKrurg%3D
2. J Arredondo AI Chernyavsky DL Jolkovsky KE Pinkerton SA Grando 2008 Receptor-mediated tobacco toxicity: acceleration of sequential expression of alpha5 and alpha7 nicotinic receptor subunits in oral keratinocytes exposed to cigarette smoke FASEB J 22 5 1356 1368 10.1096/fj.07-9965.com 18450646 10.1096/fj.07-9965.com 1:CAS:528:DC%2BD1cXltlWksr8%3D
3. Bogdanik LP, Burgess RW (2011) A valid mouse model of AGRIN-associated congenital myasthenic syndrome. Hum Mol Genet. doi: 10.1093/hmg/ddr396
4. RW Burgess QT Nguyen YJ Son JW Lichtman JR Sanes 1999 Alternatively spliced isoforms of nerve- and muscle-derived agrin: their roles at the neuromuscular junction Neuron 23 1 33 44 10402191 10.1016/S0896-6273(00)80751-5 1:CAS:528:DyaK1MXjvVSjtLc%3D
5. RW Burgess DK Dickman L Nunez DJ Glass JR Sanes 2002 Mapping sites responsible for interactions of agrin with neurons J Neurochem 83 2 271 284 12423238 10.1046/j.1471-4159.2002.01102.x 1:CAS:528:DC%2BD38XotFyltLs%3D
6. F Chevessier B Faraut A Ravel-Chapuis P Richard K Gaudon S Bauche C Prioleau R Herbst E Goillot C Ioos JP Azulay S Attarian JP Leroy E Fournier C Legay L Schaeffer J Koenig M Fardeau B Eymard J Pouget D Hantai 2004 MUSK, a new target for mutations causing congenital myasthenic syndrome Hum Mol Genet 13 24 3229 3240 10.1093/hmg/ddh333 15496425 10.1093/hmg/ddh333 1:CAS:528: DC%2BD2cXhtVClu7vM
7. RN Cole SW Reddel OL Gervasio WD Phillips 2008 Anti-MuSK patient antibodies disrupt the mouse neuromuscular junction Ann Neurol 63 6 782 789 10.1002/ana.21371 18384168 10.1002/ana.21371
8. AG Engel 2006 Light on limb-girdle myasthenia Brain 129 Pt 8 1938 1939 10.1093/brain/awl198 16870882 10.1093/brain/awl198
9. AG Engel EH Lambert MR Gomez 1977 A new myasthenic syndrome with end-plate acetylcholinesterase deficiency, small nerve terminals, and reduced acetylcholine release Ann Neurol 1 4 315 330 10.1002/ana.410010403 214017 10.1002/ana.410010403 1:STN:280:DyaE1M%2FmtVygtA%3D%3D
10. M Ferns W Hoch JT Campanelli F Rupp ZW Hall RH Scheller 1992 RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes Neuron 8 1079 1086 1319184 10.1016/0896-6273(92)90129-2 1:CAS:528:DyaK38XkvVequ7c%3D
11. MJ Ferns JT Campanelli W Hoch RH Scheller Z Hall 1993 The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans Neuron 11 3 491 502 8398142 10.1016/0896-6273(93)90153-I 1:CAS:528:DyaK2cXht1Gkur0%3D
12. M Gautam PG Noakes L Moscoso F Rupp RH Scheller JP Merlie JR Sanes 1996 Defective neuromuscular synaptogenesis in agrin-deficient mutant mice Cell 85 4 525 535 8653788 10.1016/S0092-8674(00)81253-2 1:CAS:528:DyaK28XjtFyit7w%3D
13. M Gesemann AJ Denzer MA Ruegg 1995 Acetylcholine receptor aggregating activity of agrin isoforms and mapping of the active site J Cell Biol 128 4 625 636 7860635 10.1083/jcb.128.4.625 1:CAS:528:DyaK2MXjs1ehurk%3D
14. M Gesemann V Cavalli AJ Denzer A Brancaccio B Schumacher MA Ruegg 1996 Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor Neuron 16 4 755 767 8607994 10.1016/S0896-6273(00) 80096-3 1:CAS:528:DyaK28XislCms7s%3D
15. J Gingras S Rassadi E Cooper M Ferns 2002 Agrin plays an organizing role in the formation of sympathetic synapses J Cell Biol 158 6 1109 1118 12221070 10.1083/jcb.200203012 1:CAS:528:DC%2BD38Xnt1ensrY%3D
16. J Gingras S Rassadi E Cooper M Ferns 2007 Synaptic transmission is impaired at neuronal autonomic synapses in agrin-null mice Dev Neurobiol 67 5 521 534 17443806 10.1002/dneu.20304 1:CAS:528:DC%2BD2sXls1Kmur4%3D
17. DJ Glass DC Bowen TN Stitt C Radziejewski J Bruno TE Ryan DR Gies S Shah K Mattsson SJ Burden PS Distefano DM Valenzuela TM DeChiara GD Yancopoulos 1996 Agrin acts via a MuSK receptor complex Cell 85 4 513 523 8653787 10.1016/S0092-8674(00)81252-0 1:CAS:528:DyaK28XjtFyit78%3D
18. D Hantai P Richard J Koenig B Eymard 2004 Congenital myasthenic syndromes Curr Opin Neurol 17 5 539 551 00019052-200410000-00004[pii] 15367858 10.1097/00019052-200410000-00004 1:CAS:528:DC%2BD2cXhtVWrsLjN
19. +-ATPase is a neuronal receptor for agrin Cell 125 2 359 369 10.1016/j.cell.2006.01.052 16630822 10.1016/j.cell.2006.01.052 1:CAS:528:DC%2BD28Xkt1Oqur0%3D
20. W Hoch JT Campanelli S Harrison RH Scheller 1994 Structural domains of agrin required for clustering of nicotinic acetylcholine receptors EMBO J 13 12 2814 2821 8026466 1:CAS:528:DyaK2cXkslCju78%3D
21. C Huze S Bauche P Richard F Chevessier E Goillot K Gaudon A Ben Ammar A Chaboud I Grosjean HA Lecuyer V Bernard A Rouche N Alexandri T Kuntzer M Fardeau E Fournier A Brancaccio MA Ruegg J Koenig B Eymard L Schaeffer D Hantai 2009 Identification of an agrin mutation that causes congenital myasthenia and affects synapse function Am J Hum Genet 85 2 155 167 10.1016/j.ajhg.2009.06.015 19631309 10.1016/j.ajhg.2009.06.015 1:CAS:528:DC%2BD1MXhsVGku7%2FN
22. C Jacobson F Montanaro M Lindenbaum S Carbonetto M Ferns 1998 Alpha-dystroglycan functions in acetylcholine receptor aggregation but is not a coreceptor for agrin-MuSK signaling J Neurosci 18 16 6340 6348 9698325 1:CAS:528:DyaK1cXlsVahur4%3D
23. MJ Karnovsky 1964 The localization of cholinesterase activity in rat cardiac muscle by electron microscopy J Cell Biol 23 217 232 14222810 10.1083/jcb.23.2.217 1:CAS:528:DyaF2MXhslemsA%3D%3D
24. N Kim AL Stiegler TO Cameron PT Hallock AM Gomez JH Huang SR Hubbard ML Dustin SJ Burden 2008 Lrp4 is a receptor for Agrin and forms a complex with MuSK Cell 135 2 334 342 10.1016/j.cell.2008.10.002 18848351 10.1016/j.cell.2008.10. 002 1:CAS:528:DC%2BD1cXhtlWhsrzK
25. I Ksiazek C Burkhardt S Lin R Seddik M Maj G Bezakova M Jucker S Arber P Caroni JR Sanes B Bettler MA Ruegg 2007 Synapse loss in cortex of agrin-deficient mice after genetic rescue of perinatal death J Neurosci 27 27 7183 7195 10.1523/JNEUROSCI.1609-07.2007 17611272 10.1523/JNEUROSCI.1609-07.2007 1:CAS:528:DC%2BD2sXot1egt7Y%3D
26. W Lin RW Burgess B Dominguez SL Pfaff JR Sanes KF Lee 2001 Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse Nature 410 6832 1057 1064 11323662 10.1038/35074025 1:CAS:528: DC%2BD3MXjsVCksLs%3D
27. W Lin B Dominguez J Yang P Aryal EP Brandon FH Gage KF Lee 2005 Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism Neuron 46 4 569 579 15944126 10.1016/j.neuron.2005.04.002 1:CAS:528:DC%2BD2MXkslyktbk%3D
28. AO Martin G Alonso NC Guerineau 2005 Agrin mediates a rapid switch from electrical coupling to chemical neurotransmission during synaptogenesis J Cell Biol 169 3 503 514 15883200 10.1083/jcb.200411054 1:CAS:528:DC%2BD2MXktFOjsbo%3D
29. RA Maselli JJ Ng JA Anderson O Cagney J Arredondo C Williams HB Wessel H Abdel-Hamid RL Wollmann 2009 Mutations in LAMB2 causing a severe form of synaptic congenital myasthenic syndrome J Med Genet 46 3 203 208 10.1136/jmg.2008.063693 19251977 10.1136/jmg.2008.063693 1:CAS:528: DC%2BD1MXktlKktbg%3D
30. RA Maselli J Arredondo O Cagney JJ Ng JA Anderson C Williams BJ Gerke B Soliven RL Wollmann 2010 Mutations in MUSK causing congenital myasthenic syndrome impair MuSK-Dok-7 interaction Hum Mol Genet 19 12 2370 2379 10.1093/hmg/ddq110 20371544 10.1093/hmg/ddq110 1:CAS:528:DC%2BC3cXms1Oktr8%3D
31. K Matsumoto-Miyai E Sokolowska A Zurlinden CE Gee D Luscher S Hettwer J Wolfel AP Ladner J Ster U Gerber T Rulicke B Kunz P Sonderegger 2009 Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage Cell 136 6 1161 1171 10.1016/j.cell.2009. 02.034 19303856 10.1016/j.cell.2009.02.034 1:CAS:528:DC%2BD1MXltFSnt7g%3D
32. T Misgeld TT Kummer JW Lichtman JR Sanes 2005 Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter Proc Natl Acad Sci USA 102 31 11088 11093 16043708 10.1073/pnas.0504806102 1:CAS:528:DC%2BD2MXnvVWju7c%3D
33. JS Muller A Herczegfalvi JJ Vilchez J Colomer LL Bachinski V Mihaylova M Santos U Schara M Deschauer M Shevell C Poulin A Dias A Soudo M Hietala T Aarimaa R Krahe V Karcagi A Huebner D Beeson A Abicht H Lochmuller 2007 Phenotypical spectrum of DOK7 mutations in congenital myasthenic syndromes Brain 130 Pt 6 1497 1506 10.1093/brain/awm068 17439981 10.1093/brain/awm068
34. ST Ngo PG Noakes WD Phillips 2007 Neural agrin: a synaptic stabiliser Int J Biochem Cell Biol 39 5 863 867 17126587 10.1016/j.biocel.2006.10.012 1:CAS:528:DC%2BD2sXksFaisLs%3D
35. J Palace D Lashley J Newsom-Davis J Cossins S Maxwell R Kennett S Jayawant Y Yamanashi D Beeson 2007 Clinical features of the DOK7 neuromuscular junction synaptopathy Brain 130 Pt 6 1507 1515 10.1093/brain/awm072 17452375 10.1093/brain/awm072
36. JR Sanes JW Lichtman 2001 Induction, assembly, maturation and maintenance of a postsynaptic apparatus Nat Rev Neurosci 2 11 791 805 11715056 10.1038/35097557 1:CAS:528:DC%2BD38Xmt1WitL0%3D
37. CR Slater PR Fawcett TJ Walls PR Lyons SJ Bailey D Beeson C Young D Gardner-Medwin 2006 Pre- and post-synaptic abnormalities associated with impaired neuromuscular transmission in a group of patients with 'limb-girdle myasthenia' Brain 129 Pt 8 2061 2076 10.1093/brain/awl200 16870884 10.1093/brain/awl200 1:STN:280:DC%2BD28vks1Oisw%3D%3D
38. J Stetefeld AT Alexandrescu MW Maciejewski M Jenny K Rathgeb-Szabo T Schulthess R Landwehr S Frank MA Ruegg RA Kammerer 2004 Modulation of agrin function by alternative splicing and Ca2+ binding Structure 12 3 503 515 10.1016/j.str.2004.02.001 15016366 10.1016/j.str.2004.02.001 1:CAS:528:DC%2BD2cXitFKksrw%3D
39. J Sugiyama DC Bowen ZW Hall 1994 Dystroglycan binds nerve and muscle agrin Neuron 13 1 20 10.1016/0896-6273(94)90462-6
40. Vitkup D, Sander C, Church GM (2003) The amino-acid mutational spectrum of human genetic disease. Genome Biol 4 (11):R72. doi: 10.1186/gb-2003-4-11-r72
41. BP Vohra JS Groshong RA Maselli MA Verity RL Wollmann CM Gomez 2004 Focal caspase activation underlies the endplate myopathy in slow-channel syndrome Ann Neurol 55 3 347 352 10.1002/ana.10823 14991812 10.1002/ana.10823 1:CAS:528:DC%2BD2cXisFKntb0%3D
42. X Yang S Arber C William L Li Y Tanabe TM Jessell C Birchmeier SJ Burden 2001 Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation Neuron 30 2 399 410 11395002 10.1016/S0896-6273(01)00287-2 1:CAS:528:DC%2BD3MXktFeitr0%3D
43. B Zhang S Luo Q Wang T Suzuki WC Xiong L Mei 2008 LRP4 serves as a coreceptor of agrin Neuron 60 2 285 297 10.1016/j.neuron.2008.10.006 18957220 10.1016/j.neuron.2008.10.006 1:CAS:528:DC%2BD1cXhtlCgtrjI