Anti-LRP4 autoantibodies in AChR- and MuSK-antibodynegative myasthenia gravis

Journal of Neurology

Volumn 259, Issue 3, 2012, Pages 427-435

  Pevzner, Alexandra ^a   Schoser, Benedikt ^b   Peters, Katja ^a   Cosma, Nicoleta Carmen ^a   Karakatsani, Andromachi ^a   Schalke, Berthold ^c   Melms, Arthur ^d   Kröger, Stephan ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Autoimmune disorder; Low density lipoprotein receptor related protein; LRP4; Myasthenia gravis

Indexed keywords

AGRIN; AUTOANTIBODY; CHOLINERGIC RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 4; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 4 AUTOANTIBODY; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ANIMAL TISSUE; ANTIBODY COMBINING SITE; ANTIBODY DETECTION; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; FEMALE; HUMAN; MALE; MOUSE; MYASTHENIA GRAVIS; MYOTUBE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; SKELETAL MUSCLE;

ADOLESCENT; ADULT; AGED; AGRIN; ANIMALS; AUTOANTIBODIES; BUNGAROTOXINS; CELLS, CULTURED; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; LDL-RECEPTOR RELATED PROTEINS; MALE; MICE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; MYASTHENIA GRAVIS; NEUROLOGIC EXAMINATION; NEUROMUSCULAR JUNCTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, NICOTINIC; TRANSFECTION; YOUNG ADULT;

EID: 84861855230     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-011-6194-7     Document Type: Article

References (44)

1. Romi F, Gilhus NE, Aarli JA (2006) Myasthenia gravis: disease severity and prognosis. Acta Neurol Scand Suppl 183:24-25
2. Newsom-Davis J (2007) The emerging diversity of neuromuscular junction disorders. Acta Myol 26:5-10 (Pubitemid 47400719)
3. Farrugia ME, Vincent A (2010) Autoimmune mediated neuromuscular junction defects. Curr Opin Neurol 23:489-495
4. Lindstrom JM, Einarson BL, Lennon VA, Seybold ME (1976) Pathological mechanisms in experimental autoimmune myasthenia gravis. I. Immunogenicity of syngeneic muscle acetylcholine receptor and quantitative extraction of receptor and antibodyreceptor complexes from muscles of rats with experimental automimmune myasthenia gravis. J Exp Med 144:726-738
5. Drachman DB, de Silva S, Ramsay D, Pestronk A (1987) Humoral pathogenesis of myasthenia gravis. Ann N Y Acad Sci 505:90-105
6. Engel AG (1979) The immunopathological basis of acetylcholine receptor deficiency in myasthenia gravis. Prog Brain Res 49:423-434
7. Burges J, Wray DW, Pizzighella S, Hall Z, Vincent A (1990) A myasthenia gravis plasma immunoglobulin reduces miniature endplate potentials at human endplates in vitro. Muscle Nerve 13:407-413 (Pubitemid 20173561)
8. Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A (2001) Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med 7:365-368 (Pubitemid 32224355)
9. Scuderi F, Marino M, Colonna L, Mannella F, Evoli A, Provenzano C, Bartoccioni E (2002) Anti-p110 autoantibodies identify a subtype of "seronegative" myasthenia gravis with prominent oculobulbar involvement. Lab Invest 82:1139-1146 (Pubitemid 35014847)
10. McConville J, Farrugia ME, Beeson D, Kishore U, Metcalfe R, Newsom-Davis J, Vincent A (2004) Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann Neurol 55:580-584 (Pubitemid 38391977)
11. Guptill JT, Sanders DB, Evoli A (2011) Anti-musk antibody myasthenia gravis: clinical findings and response to treatment in two large cohorts. Muscle Nerve 44:36-40
12. Valenzuela DM, Stitt TN, Distefano PS, Rojas E, Mattsson K, Compton DL, Nunez L, Park JS, Stark JL, Gies DR, Thomas S, Le Beau MM, Fernald AA, Copeland NG, Jenkins NA, Burden SJ, Glass DJ, Yancopoulos GD (1995) Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15:573-584
13. Glass DJ, DeChiara TM, Stitt TN, Distefano PS, Valenzuela DM, Yancopoulos GD (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation and is a functional receptor for agrin. Cold Spring Harb Symp Quant Biol 61:435-444 (Pubitemid 27257992)
14. Apel ED, Glass DJ, Moscoso LM, Yancopoulos GD, Sanes JR (1997) Rapsyn is required forMuSKsignaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18:623-635 (Pubitemid 27194642)
15. Sanders DB, Juel VC (2008) MuSK-antibody positive myasthenia gravis: questions from the clinic. J Neuroimmunol 201-202:85-89
16. Cenacchi G, Valentina P, Marina F, Elena P, Corrado A (2011) Comparison of muscle ultrastructure in myasthenia gravis with anti-MuSK and anti-AChR antibodies. J Neurol 258:746-752
17. Benveniste O, Jacobson L, Farrugia ME, Clover L, Vincent A (2005) MuSK antibody positive myasthenia gravis plasma modifies MURF-1 expression in C2C12 cultures and mouse muscle in vivo. J Neuroimmunol 170:41-48 (Pubitemid 41740905)
18. Boneva N, Frenkian-Cuvelier M, Bidault J, Brenner T, Berrih-Aknin S (2006) Major pathogenic effects of anti-MuSK antibodies in myasthenia gravis. J Neuroimmunol 177:119-131 (Pubitemid 44108241)
19. Farrugia ME, Bonifati DM, Clover L, Cossins J, Beeson D, Vincent A (2007) Effect of sera from AChR-antibody negative myasthenia gravis patients on AChR and MuSK in cell cultures. J Neuroimmunol 185:136-144 (Pubitemid 46497437)
20. Vincent A, Leite MI, Farrugia ME, Jacob S, Viegas S, Shiraishi H, Benveniste O, Morgan BP, Hilton-Jones D, Newsom-Davis J, Beeson D, Willcox N (2008) Myasthenia gravis seronegative for acetylcholine receptor antibodies. Ann N Y Acad Sci 1132:84-92 (Pubitemid 351841363)
21. Leite MI, Jacob S, Viegas S, Cossins J, Clover L, Morgan BP, Beeson D, Willcox N, Vincent A (2008) IgG1 antibodies to acetylcholine receptors in 'seronegative' myasthenia gravis. Brain 131:1940-1952 (Pubitemid 351957451)
22. Leite MI, Strobel P, Jones M, Micklem K, Moritz R, Gold R, Niks EH, Berrih-Aknin S, Scaravilli F, Canelhas A, Marx A, Newsom-Davis J, Willcox N, Vincent A (2005) Fewer thymic changes in MuSK antibody-positive than in MuSK antibodynegative MG. Ann Neurol 57:444-448 (Pubitemid 40343969)
23. Romi F, Aarli JA, Gilhus NE (2005) Seronegative myasthenia gravis: disease severity and prognosis. Eur J Neurol 12:413-418 (Pubitemid 40768658)
24. Mossman S, Vincent A, Newsom-Davis J (1986) Myasthenia gravis without acetylcholine-receptor antibody: a distinct disease entity. Lancet 1:116-119
25. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L (2008) LRP4 serves as a coreceptor of agrin. Neuron 60:285-297
26. Kim N, Stiegler AL, Cameron TO, Hallock PT, Gomez AM, Huang JH, Hubbard SR, Dustin ML, Burden SJ (2008) Lrp4 is a receptor for agrin and forms a complex with MuSK. Cell 135:334-342
27. Higuchi O, Hamuro J, Motomura M, Yamanashi Y (2011) Autoantibodies to low-density lipoprotein receptor-related protein 4 in myasthenia gravis. Ann Neurol 69:418-422
28. Schröder JE, Tegeler MR, Grosshans U, Porten E, Blank M, Lee J, Esapa C, Blake DJ, Kröger S (2007) Dystroglycan regulates structure, proliferation and differentiation of neuroepithelial cells in the developing vertebrate CNS. Dev Biol 307:62-78 (Pubitemid 46890848)
29. Tsen G, Halfter W, Kröger S, Cole GJ (1995) Agrin is a heparan sulfate proteoglycan. J Biol Chem 270:3392-3399
30. Eusebio A, Oliveri F, Barzaghi P, Ruegg MA (2003) Expression of mouse agrin in normal, denervated and dystrophic muscle. Neuromuscul Disord 13:408-415 (Pubitemid 36687815)
31. Wallace BG (1990) Inhibition of agrin-induced acetylcholinereceptor aggregation by heparin, heparan sulfate, and other polyanions. J Neurosci 10:3576-3582
32. Gesemann M, Denzer AJ, Ruegg MA (1995) Acetylcholine receptor aggregating activity of agrin isoforms and mapping of the active site. J Cell Biol 128:625-636
33. Hopf C, Hoch W (1998) Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J Biol Chem 273:6467-6473 (Pubitemid 28144742)
34. Yamamoto T, Sato T, Sugita H (1987) Antifilamin, antivinculin, and antitropomyosin antibodies in myasthenia gravis. Neurology 37:1329-1333
35. Lu CZ, Lu L, Hao ZS, Xia DG, Qain J, Arnason BG (1993) Antibody-secreting cells to acetylcholine receptor and to presynaptic membrane receptor in seronegative myasthenia gravis. J Neuroimmunol 43:145-149
36. Simon-Chazottes D, Tutois S, Kuehn M, Evans M, Bourgade F, Cook S, Davisson MT, Guenet JL (2006) Mutations in the gene encoding the low-density lipoprotein receptor LRP4 cause abnormal limb development in the mouse. Genomics 87:673-677
37. Choi HY, Dieckmann M, Herz J, Niemeier A (2009) Lrp4, a novel receptor for Dickkopf 1 and sclerostin, is expressed by osteoblasts and regulates bone growth and turnover in vivo. PLoS One 4:e7930
38. Karner CM, Dietrich MF, Johnson EB, Kappesser N, Tennert C, Percin F, Wollnik B, Carroll TJ, Herz J (2010) Lrp4 regulates initiation of ureteric budding and is crucial for kidney formation-a mouse model for Cenani-Lenz syndrome. PLoS One 5:e10418
39. Johnson EB, Hammer RE, Herz J (2005) Abnormal development of the apical ectodermal ridge and polysyndactyly in Megf7-deficient mice. Hum Mol Genet 14:3523-3538 (Pubitemid 41672134)
40. Weatherbee SD, Anderson KV, Niswander LA (2006) LDLreceptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133:4993-5000 (Pubitemid 46085064)
41. Wu H, Xiong WC, Mei L (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137:1017-1033
42. DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, Kinetz E, Compton DL, Rojas E, Park JS, Smith C, Distefano PS, Glass DJ, Burden SJ, Yancopoulos GD (1996) The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85:501-512 (Pubitemid 26157189)
43. Li Y, Pawlik B, Elcioglu N, Aglan M, Kayserili H, Yigit G, Percin F, Goodman F, Nurnberg G, Cenani A, Urquhart J, Chung BD, Ismail S, Amr K, Aslanger AD, Becker C, Netzer C, Scambler P, Eyaid W, Hamamy H, Clayton-Smith J, Hennekam R, Nurnberg P, Herz J, Temtamy SA, Wollnik B (2010) LRP4 mutations alter Wnt/beta-catenin signaling and cause limb and kidney malformations in Cenani-Lenz syndrome. Am J Hum Genet 86:696-706
44. Wang WW, Hao HJ, Gao F (2010) Detection of multiple antibodies in myasthenia gravis and its clinical significance. Chin Med J (Engl) 123:2555-2558