Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses

Nature

Volumn 489, Issue 7416, 2012, Pages 438-442

  Yumoto, Norihiro ^a   Kim, Natalie ^a   Burden, Steven J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 4; MUSCLE SPECIFIC KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

CLUSTER ANALYSIS; ENZYME ACTIVITY; MUSCLE; NEUROLOGY; PROTEIN; STABILIZATION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENZYME ACTIVITY; IN VIVO CULTURE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DIAPHRAGM; MICE; MOTOR NEURONS; MUSCLE, SKELETAL; NEURAL TUBE; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; PROTEIN BINDING; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, LDL; SARCOPENIA; SIGNAL TRANSDUCTION; SYNAPSINS; TISSUE CULTURE TECHNIQUES;

EID: 84866480273     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11348     Document Type: Article

References (30)

1. Sanes, J. R. & Lichtman, J. W. Induction, assembly, maturation andmaintenance of a postsynaptic apparatus. Nature Rev. Neurosci. 2, 791-805 (2001).
2. DeChiara, T. M. et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512 (1996).
3. Weatherbee, S. D., Anderson, K. V. & Niswander, L. A. LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133, 4993-5000 (2006).
4. Kim, N. et al. Lrp4 is a receptor for Agrin and forms a complex withMuSK. Cell 135, 334-342 (2008).
5. Zhang, B. et al. LRP4 serves as a coreceptor of agrin. Neuron 60, 285-297 (2008).
6. Arber, S., Burden, S. J. & Harris, A. J. Patterning of skeletal muscle. Curr. Opin. Neurobiol. 12, 100-103 (2002).
7. Yang, X. et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-410 (2001).
8. Yang, X., Li, W., Prescott, E. D., Burden, S. J. & Wang, J. C. DNA topoisomerase IIbeta and neural development. Science 287, 131-134 (2000).
9. Lin, W. et al. Distinct roles of nerve andmuscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057-1064 (2001).
10. Panzer, J. A. S. o. n. g. Y. & Balice-Gordon, R. J. In vivo imaging of preferentialmotor axon outgrowth to and synaptogenesis at prepatterned acetylcholine receptor clusters in embryonic zebrafish skeletalmuscle. J. Neurosci. 26, 934-947 (2006).
11. Flanagan-Steet, H.,Fox, M. A.,Meyer, D. & Sanes, J. R.Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132, 4471-4481 (2005).
12. Burden, S. J. SnapShot: neuromuscular junction. Cell 144, 826.e1 (2011).
13. Kummer, T. T., Misgeld, T. & Sanes, J. R. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr. Opin. Neurobiol. 16, 74-82 (2006).
14. Zhang, W., Coldefy, A. S., Hubbard, S. R. & Burden, S. J. Agrin binds to the N-terminal region of Lrp4 and stimulates association between Lrp4 and the first Ig-like domain in MuSK. J. Biol. Chem., (2011).
15. Gautam, M. et al. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535 (1996).
16. Lin, W. et al. Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron 46, 569-579 (2005).
17. Misgeld, T., Kummer, T. T., Lichtman, J. W. & Sanes, J. R. Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter. Proc. Natl Acad. Sci. USA 102, 11088-11093 (2005).
18. Kim, N. & Burden, S. J.MuSKcontrolswheremotor axons growandformsynapses. Nature Neurosci. 11, 19-27 (2008).
19. Gomez, A. M. & . B. u. r. d. e. n. S. J. The extracellular region of Lrp4 is sufficient to mediate neuromuscular synapse formation. Dev. Dynam. 240, 2626-2633 (2011).
20. Engel, A. G., Ohno, K. & Sine, S. M. Sleuthing molecular targets for neurological diseases at the neuromuscular junction. Nature Rev. Neurosci. 4, 339-352 (2003).
21. Higuchi, O., Hamuro, J., Motomura, M. & Yamanashi, Y. Autoantibodies to lowdensity lipoprotein receptor-related protein 4 in myasthenia gravis. Ann. Neurol. 69, 418-422 (2011).
22. Drescher, U. The Eph family in the patterning of neural development. Curr. Biol. 7, R799-R807 (1997).
23. Bao, J., Wolpowitz, D., Role, L. W. & Talmage, D. A. Back signaling by the Nrg-1 intracellular domain. J. Cell Biol. 161, 1133-1141 (2003).
24. Fox, M. A. et al. Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129, 179-193 (2007).
25. Higuchi, O., Hamuro, J., Motomura, M. & Yamanashi, Y. Autoantibodies to lowdensity lipoprotein receptor-related protein 4 in myasthenia gravis. Ann. Neurol. 69, 418-422 (2011).
26. Pun, S., Santos, A. F., Saxena, S., Xu, L. & Caroni, P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nature Neurosci. 9, 408-419 (2006).
27. Valdez, G. et al. Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc. Natl Acad. Sci. USA 107, 14863-14868 (2010).
28. Hata, K., Polo-Parada, L. & Landmesser, L. T.Selective targeting of different neural cell adhesion molecule isoforms during motoneuron myotube synapse formation in culture and the switch fromanimmature tomature formof synaptic vesicle cycling. J. Neurosci. 27, 14481-14493 (2007).
29. Umemori, H., Linhoff, M. W., Ornitz, D. M. & Sanes, J. R. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270 (2004).
30. Umemori, H. & Sanes, J. R. Signal regulatory proteins (SIRPS) are secreted presynaptic organizing molecules. J. Biol. Chem. 283, 34053-34061 (2008).