Cell-surface MuSK self-association: A crucial role for the putative signal sequence

Biochemistry

Volumn 44, Issue 49, 2005, Pages 16229-16238

  Bianchetta, Michael J ^a   Betensky, Rebecca A ^b   Cohen, Jonathan B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; ENZYMES; IMMUNOLOGY;

EXTRACELLULAR DOMAIN; MUTATIONAL ANALYSIS; NEUROMUSCULAR JUNCTIONS; PLASMA MEMBRANES;

ASSOCIATION REACTIONS;

COMPLEMENTARY DNA; MESSENGER RNA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE MUSK; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; EMBRYO; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MUTANT; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL MEMBRANE; DNA MUTATIONAL ANALYSIS; FIBROBLASTS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

EID: 28944436680     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051549j     Document Type: Article

References (41)

1. Sanes, J. R., and Lichtman, J. W. (2001) Induction, Assembly, Maturation and Maintenance of a Postsynaptic Apparatus, Nat. Rev. Neurosci. 2, 791-805.
2. Salpeter, M. M., and Loring, R. H. (1985) Nicotinic Acetylcholine Receptors in Vertebrate Muscle: Properties, Distribution and Neural Control, Prog. Neurobiol. 25, 297-325.
3. Salpeter, M. M., Marchaterre, M., and Harris, R. (1988) Distribution of Extrajunctional Acetylcholine Receptors on a Vertebrate Muscle: Evaluated by Using a Scanning Electron Microscope Autoradiographic Procedure, J. Cell Biol. 106, 2087-2093.
4. Merlie, J. P. (1984) Biogenesis of the Acetylcholine Receptor, a Multisubunit Integral Membrane Protein, Cell 36, 573-575.
5. Denzer, A. J., Hauser, D. M., Gesemann, M., and Ruegg, M. A. (2004) Synaptic Differentiation: the Role of Agrin in the Formation and Maintenance of the Neuromuscular Junction, Cell Tissue Res. 290, 357-365.
6. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P., and Sanes, J. R. (1996) Defective Neuromuscular Synaptogenesis in Agrin-Deficient Mutant Mice, Cell 85, 525-535.
7. Valenzuela, D. M., Stitt, T. N., Distefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nunez, L., Park, J. S., Stark, J. L., Gies, D. R., Thomas, S., Lebeau, M. M., Fernald, A. A., Copeland, N. G., Jenkins, N. A., Burden, S. J., Glass, D. J., and Yancopoulos, G. D. (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.
8. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J., Distefano, P. S., Valenzuela, D. M., Dechiara, T. M., and Yancopoulos, G. D. (1996) Agrin Acts via a MuSK Receptor Complex, Cell 85, 513-523.
9. Dechiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S., Smith, C., Distefano, P. S., Glass, D. J., Burden, S. J., and Yancopoulos, G. D. (1996) The Receptor Tyrosine Kinase MuSK Is Required for Neuromuscular Junction Formation in Vivo, Cell 85, 501-512.
10. Hopf, C., and 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.
11. Hopf, C., and Hoch, W. (1997) Heparin Inhibits Acetylcholine Receptor Aggregation at Two Distinct Steps in the Agrin-Induced Pathway, Eur. J. Neurosci. 9, 1170-1177.
12. Willmann, R., and Fuhrer, C. (2002) Neuromuscular Synaptogenesis: Clustering of Acetylcholine Receptors Revisited, Cell. Mol. Life Sci. 59, 1296-1316.
13. Glass, D. J., Apel, E. D., Shah, S., Bowen, D. C., Dechiara, T. M., Stitt, T. N., Sanes, J. R., and Yancopoulos, G. D. (1997) Kinase Domain of the Muscle-Specific Receptor Tyrosine Kinase (MuSK) Is Sufficient for Phosphorylation but Not Clustering of Acetylcholine Receptors: Required Role for the MuSK Ectodomain?, Proc. Natl. Acad. Sci. U.S.A. 94, 8848-8853.
14. Apel, E. D., Glass, D. J., Moscoso, L. M., Yancopoulos, G. D., and Sanes, J. R. (1997) Rapsyn Is Required for MuSK Signaling and Recruits Synaptic Components to a MuSK-Containing Scaffold, Neuron 18, 623-635.
15. Gautam, M., Dechiara, T. M., Glass, D. J., Yancopoulos, G. D., and Sanes, J. R. (1999) Distinct Phenotypes of Mutant Mice Lacking Agrin, MuSK, or Rapsyn, Dev. Brain Res. 114, 171-178.
16. Trinidad, J. C., Fischbach, G. D., and Cohen, J. B. (2000) The Agrin/MuSK Signaling Pathway Is Spatially Segregated From the Neuregulin/ErbB Receptor Signaling Pathway at the Neuromuscular Junction, J. Neurosci. 20, 8762-8770.
17. Pike, L. J. (2003) Lipid Rafts: Bringing Order to Chaos, J. Lipid Res. 44, 655-667.
18. van Deurs, B., Roepstorff, K., Hommelgaard, A. M., and Sandvig, K. (2003) Caveolae: Anchored, Multifunctional Platforms in Thelipid Ocean, Trends Cell Biol. 13, 92-100.
19. Ceresa, B. P., and Schmid, S. L. (2000) Regulation of Signal Transduction by Endocytosis, Curr. Opin. Cell Biol. 12, 204-210.
20. Herbst, R., and Burden, S. J. (2000) The Juxtamembrane Region of MuSK Has a Critical Role in Agrin-Mediated Signaling, EMBO J. 19, 67-77.
21. Zhou, H., Glass, D. J., Yancopoulos, G. D., and Sanes, J. R. (1999) Distinct Domains of MuSK Mediate Its Abilities to Induce and to Associate With Postsynaptic Specializations, J. Cell Biol. 146, 1133-1146.
22. Gillespie, S. K. H., Balasubramanian, S., Fung, E. T., and Huganir, R. L. (1996) Rapsyn Clusters and Activates the Synapse-Specific Receptor Tyrosine Kinase MuSK, Neuron 16, 953-962.
23. Kryl, D., Yacoubian, T., Haapasalo, A., Castren, E., Lo, D., and Barker, P. A. (1999) Subcellular Localization of Full-Length and Truncated Trk Receptor Isoforms in Polarized Neurons and Epithelial Cells, J. Neurosci. 19, 5823-5833.
24. Elenius, K., Corfas, G., Paul, S., Choi, C. J., Rio, C., Plowman, G. D., and Klagsbrun, M. (1997) A Novel Juxtamembrane Domain Isoform of HER4/ErbB4. Isoform-Specific Tissue Distribution and Differential Processing in Response to Phorbol Ester, J. Biol. Chem. 272, 26761-26768.
25. Ramarao, M. K., and Cohen, J. B. (1998) Mechanism of Nicotinic Acetylcholine Receptor Cluster Formation by Rapsyn, Proc. Natl. Acad. Sci. U.S.A. 95, 4007-4012.
26. Bailey, T. L., and Gribskov, M. (1998) Combining Evidence Using P-Values: Application to Sequence Homology Searches, Bioinformatics 14, 48-54.
27. Dautry-Varsat, A. (1986) Receptor-Mediated Endocytosis: The Intracellular Journey of Transferrin and Its Receptor, Biochimie 68, 375-381.
28. Brodsky, F. M. (1985) Clathrin Structure Characterized with Monoclonal Antibodies. II. Identification of in Vivo Forms of Clathrin, J. Cell Biol. 101, 2055-2062.
29. Carter, A. R., Chen, C., Schwartz, P. M., and Segal, R. A. (2002) Brain-Derived Neurotrophic Factor Modulates Cerebellar Plasticity and Synaptic Ultrastructure, J. Neurosci. 22, 1316-1327.
30. Keenan, R. J., Freymann, D. M., Stroud, R. M., and Walter, P. (2001) The Signal Recognition Particle, Annu. Rev. Biochem. 70, 755-775.
31. Stroud, R. M., and Walter, P. (1999) Signal Sequence Recognition and Protein Targeting, Curr. Opin. Struct. Biol. 9, 754-759.
32. Ullrich, A., Coussens, L., Hayflick, J. S., Dull, T. J., Gray, A., Tam, A. W., Lee, J., Yarden, Y., Libermann, T. A., Schlessinger, J., Downward, J., Mayes, E. L. V., Whittle, N., Waterfield, M. D., and Seeburg, P. H. (1984) Human Epidermal Growth Factor Receptor CDNA Sequence and Aberrant Expression of the Amplified Gene in A431 Epidermoid Carcinoma Cells, Nature 309, 418-425.
33. Ebina, Y., Ellis, L., Jarnagin, K., Edery, M., Graf, L., Clauser, E., Ou, J. H., Masiarz, F., Kan, Y. W., Goldfine, I. D., Roth, R. A., and Rutter, W. J. (1985) The Human Insulin Receptor CDNA: The Structural Basis for Hormone-Activated Transmembrane Signalling, Cell 40, 747-758.
34. Yarden, Y., Escobedo, J. A., Kuang, W. J., Yang-Feng, T. L., Daniel, T. O., Tremble, P. M., Chen, E. Y., Ando, M. E., Harkins, R. N., Francke, U., Fried, V. A., Ullrich, A., and Williams, L. T. (1986) Structure of the Receptor for Platelet-Derived Growth Factor Helps Define a Family of Closely Related Growth Factor Receptors, Nature 323, 226-232.
35. Gewurz, G. E., Ploegh, H. L., and Tortorella, D. (2002) US2, a Human Cytomegalovirus-Encoded Type I Membrane Protein, Contains a Non-Cleavable Amino-Terminal Signal Peptide, J. Biol. Chem. 277, 11306-11313.
36. Xia, J., Zhang, X., Staudinger, J., and Huganir, R. L. (1999) Clustering of AMPA Receptors by the Synaptic PDZ Domain-Containing Protein PICK1, Neuron 22, 179-187.
37. Strochlic, L., Cartaud, A., Labas, V., Hoch, W., Rossier, J., and Cartaud, J. (2001) MAGI-1c: A Synaptic MAGUK Interacting with MuSK at the Vertebrate Neuromuscular Junction, J. Cell Biol. 53, 1127-1132.
38. Luo, Z. G., Wang, Q., Zhou, J. Z., Wang, J. B., Luo, Z. J., Liu, M. Y., He, X., WynshawBoris, A., Xiong, W. C., Lu, B., and Mei, L. (2002) Regulation of AChR Clustering by Dishevelled Interacting With MuSK and PAK1, Neuron 35, 489-505.
39. Nagy, P., Jenei, A., Kirsch, A. K., Szollosi, J., Damjanovich, S., and Jovin, T. M. (1999) Activation-Dependent Clustering of the ErbB2 Receptor Tyrosine Kinase Detected by Scanning Near-Field Optical Microscopy, J. Cell Sci. 112, 1733-1741.
40. Torres, R., Firestein, B. L., Dong, H., Staudinger, J., Olson, E. N., Huganir, R. L., Bredt, D. S., Gale, N. W., and Yancopoulos, G. D. (1998) PDZ Proteins Bind, Cluster, and Synaptically Colocalize With Eph Receptors and Their Ephrin Ligands, Neuron 21, 1453-1463.
41. Capozza, F., Cohen, A. W., Cheung, M., Sotgia, F., Schubert, W., Battista, M., Lee, H., Frank, P. G., and Lisanti, M. P. (2005) Muscle-specific Interactions of Caveolin Isoforms: Differential Complex Formation between Caveolins in Fibroblastic vs. Muscle Cells, Am. J. Physiol: Cell Physiol. 288, C677-C691.