Slit2 as a β-catenin/ctnnb1-dependent retrograde signal for presynaptic differentiation

eLife

Volumn 4, Issue JULY 2015, 2015, Pages 1-20

  Wu, Haitao ^a,b   Barik, Arnab ^b   Lu, Yisheng ^b   Shen, Chengyong ^b   Bowman, Andrew ^b   Li, Lei ^b   Sathyamurthy, Anupama ^b   Lin, Thiri W ^b   Xiong, Wen Cheng ^b,c   Mei, Lin ^b,c  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; SLIT2 PROTEIN; SYNAPTOPHYSIN; CTNNB1 PROTEIN, MOUSE; MUTANT PROTEIN; NERVE PROTEIN; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDPLATE POTENTIAL; FEMALE; GENE SEQUENCE; GENETIC TRANSFECTION; GENOTYPE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOLECULAR CLONING; MOTOR NERVE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PHRENIC NERVE; POLYMERASE CHAIN REACTION; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SPINAL CORD; SYNAPTOGENESIS; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUSCLE CELL; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS;

ANIMALS; BETA CATENIN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE CELLS; MUTANT PROTEINS; NERVE TISSUE PROTEINS; NEURONS;

EID: 84937393810     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07266     Document Type: Article

References (97)

1. Aberle H, Schwartz H, Hoschuetzky H, Kemler R. 1996a. Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to alpha-catenin. The Journal of Biological Chemistry 271:1520–1526. doi: 10.1074/jbc.271.3.1520
2. Aberle H, Schwartz H, Kemler R. 1996b. Cadherin-catenin complex: protein interactions and their implications for cadherin function. Journal of Cellular Biochemistry 61:514–523. doi: 10.1002/(SICI)1097-4644(19960616)61:4<514::AID-JCB4>3.0.CO;2-R.
3. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B, Reichardt LF. 2003 Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40:719–731. doi: 10.1016/S0896-6273(03)00718-9
4. Banerjee S, Gordon L, Donn TM, Berti C, Moens CB, Burden SJ, Granato M. 2011 A novel role for MuSK and noncanonical Wnt signaling during segmental neural crest cell migration. Development 138:3287–3296. doi: 10.1242/dev.067306
5. Barik A, Lu Y, Sathyamurthy A, Bowman A, Shen C, Li L, Xiong WC, Mei L. 2014a. LRP4 is critical for neuromuscular junction maintenance. The Journal of Neuroscience 34:13892–13905. doi: 10.1523/JNEUROSCI.1733-14.2014
6. Barik A, Zhang B, Sohal GS, Xiong WC, Mei L. 2014b. Crosstalk between Agrin and Wnt signaling pathways in development of vertebrate neuromuscular junction. Developmental Neurobiology 74:828–838. doi: 10.1002/dneu.22190
7. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996 Functional interaction of beta-catenin with the transcription factor LEF-1 Nature 382:638–642. doi: 10.1038/382638a0
8. Bozdagi O, Valcin M, Poskanzer K, Tanaka H, Benson DL. 2004 Temporally distinct demands for classic cadherins in synapse formation and maturation. Molecular and Cellular Neurosciences 27:509–521. doi: 10.1016/j.mcn.2004.08.008
9. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T. 1999 Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795–806. doi: 10.1016/S0092-8674(00)80590-5
10. Chedotal A. 2007 Slits and their receptors. Advances in Experimental Medicine and Biology 621:65–80. doi: 10.1007/978-0-387-76715-4_5
11. Chen SC, Mehrad B, Deng JC, Vassileva G, Manfra DJ, Cook DN, Wiekowski MT, Zlotnik A, Standiford TJ, Lira SA. 2001 Impaired pulmonary host defense in mice lacking expression of the CXC chemokine lungkine. Journal of Immunology 166:3362–3368. doi: 10.4049/jimmunol.166.5.3362
12. Coussens LM, Tinkle CL, Hanahan D, Werb Z. 2000 MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103:481–490. doi: 10.1016/S0092-8674(00)00139-2
13. Crawford GE, Faulkner JA, Crosbie RH, Campbell KP, Froehner SC, Chamberlain JS. 2000 Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. The Journal of Cell Biology 150:1399–1410. doi: 10.1083/jcb.150.6.1399
14. D’Arcangelo G, Miao GG, Curran T. 1996 Detection of the reelin breakpoint in reeler mice. Brain Research. Molecular Brain Research 39:234–236. doi: 10.1016/0169-328X(96)00046-0.
15. de Wit J, Hong W, Luo L, Ghosh A. 2011 Role of leucine-rich repeat proteins in the development and function of neural circuits. Annual Review of Cell and Developmental Biology 27:697–729. doi: 10.1146/annurev-cellbio-092910-154111
16. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P. 2003 Neurexin mediates the assembly of presynaptic terminals. Nature Neuroscience 6:708–716. doi: 10.1038/nn1074
17. 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. doi: 10.1016/S0092-8674(00)81251-9
18. Erskine L, Williams SE, Brose K, Kidd T, Rachel RA, Goodman CS, Tessier-Lavigne M, Mason CA. 2000 Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. The Journal of Neuroscience 20:4975–4982
19. Fox MA, Sanes JR, Borza DB, Eswarakumar VP, Fässler R, Hudson BG, John SW, Ninomiya Y, Pedchenko V, Pfaff SL, Rheault MN, Sado Y, Segal Y, Werle MJ, Umemori H. 2007 Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129:179–193. doi: 10.1016/j.cell.2007.02.035
20. Glass DJ, Bowen DC, Stitt TN, Radziejewski C, Bruno J, Ryan TE, Gies DR, Shah S, Mattsson K, Burden SJ, DiStefano PS, Valenzuela DM, DeChiara TM, Yancopoulos GD. 1996 Agrin acts via a MuSK receptor complex. Cell 85:513–523. doi: 10.1016/S0092-8674(00)81252-0
21. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. 1998 Identification of c-MYC as a target of the APC pathway. Science 281:1509–1512. doi: 10.1126/science.281.5382.1509
22. Henriquez JP, Webb A, Bence M, Bildsoe H, Sahores M, Hughes SM, Salinas PC. 2008 Wnt signaling promotes AChR aggregation at the neuromuscular synapse in collaboration with agrin. Proceedings of the National Academy of Sciences of USA 105:18812–18817. doi: 10.1073/pnas.0806300105
23. Huang ZH, Wang Y, Su ZD, Geng JG, Chen YZ, Yuan XB, He C. 2011 Slit-2 repels the migration of olfactory ensheathing cells by triggering Ca2+-dependent cofilin activation and RhoA inhibition. Journal of Cell Science 124:186–197. doi: 10.1242/jcs.071357
24. Hussain SA, Piper M, Fukuhara N, Strochlic L, Cho G, Howitt JA, Ahmed Y, Powell AK, Turnbull JE, Holt CE, Hohenester E. 2006 A molecular mechanism for the heparan sulfate dependence of slit-robo signaling. The Journal of Biological Chemistry 281:39693–39698. doi: 10.1074/jbc.M609384200
25. Jaworski A, Tessier-Lavigne M. 2012 Autocrine/juxtaparacrine regulation of axon fasciculation by Slit-Robo signaling. Nature Neuroscience 15:367–369. doi: 10.1038/nn.3037
26. Jing L, Lefebvre JL, Gordon LR, Granato M. 2009 Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61:721–733. doi: 10.1016/j.neuron.2008.12.025
27. Keller-Peck CR, Feng G, Sanes JR, Yan Q, Lichtman JW, Snider WD. 2001 Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. The Journal of Neuroscience 21:6136–6146
28. Kidd T, Bland KS, Goodman CS. 1999 Slit is the midline repellent for the robo receptor in Drosophila. Cell 96: 785–794. doi: 10.1016/S0092-8674(00)80589-9
29. Kim CH, Xiong WC, Mei L. 2005 Inhibition of MuSK expression by CREB interacting with a CRE-like element and MyoD. Molecular and Cellular Biology 25:5329–5338. doi: 10.1128/MCB.25.13.5329-5338.2005
30. Kim N, Burden SJ. 2008 MuSK controls where motor axons grow and form synapses. Nature Neuroscience 11: 19–27. doi: 10.1038/nn2026
31. 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. doi: 10.1016/j.cell.2008.10.002
32. Korkut C, Budnik V. 2009 WNTs tune up the neuromuscular junction. Nature Reviews Neuroscience 10:627–634. doi: 10.1038/nrn2681
33. Latvanlehto A, Fox MA, Sormunen R, Tu H, Oikarainen T, Koski A, Naumenko N, Shakirzyanova A, Kallio M, Ilves M, Giniatullin R, Sanes JR, Pihlajaniemi T. 2010 Muscle-derived collagen XIII regulates maturation of the skeletal neuromuscular junction. The Journal of Neuroscience 30:12230–12241. doi: 10.1523/JNEUROSCI.5518-09.2010
34. Li XM, Dong XP, Luo SW, Zhang B, Lee DH, Ting AK, Neiswender H, Kim CH, Carpenter-Hyland E, Gao TM, Xiong WC, Mei L. 2008 Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nature Neuroscience 11:262–268. doi: 10.1038/nn2053
35. Lin W, Sanchez HB, Deerinck T, Morris JK, Ellisman M, Lee KF. 2000 Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proceedings of the National Academy of Sciences of USA 97: 1299–1304. doi: 10.1073/pnas.97.3.1299
36. Liu Y, Sugiura Y, Wu F, Mi W, Taketo MM, Cannon S, Carroll T, Lin W. 2012. beta-Catenin stabilization in skeletal muscles, but not in motor neurons, leads to aberrant motor innervation of the muscle during neuromuscular development in mice. Developmental Biology 366: 255–267. doi: 10.1016/j.ydbio.2012.04.003
37. Luo S, Zhang B, Dong XP, Tao Y, Ting A, Zhou Z, Meixiong J, Luo J, Chiu FC, Xiong WC, Mei L. 2008 HSP90 beta regulates rapsyn turnover and subsequent AChR cluster formation and maintenance. Neuron 60:97–110. doi: 10.1016/j.neuron.2008.08.013
38. Luo ZG, Je HS, Wang Q, Yang F, Dobbins GC, Yang ZH, Xiong WC, Lu B, Mei L. 2003 Implication of geranylgeranyltransferase I in synapse formation. Neuron 40:703–717. doi: 10.1016/S0896-6273(03)00695-0
39. Luo ZG, Wang Q, Zhou JZ, Wang J, Luo Z, Liu M, He X, Wynshaw-Boris A, Xiong WC, Lu B, Mei L. 2002 Regulation of AChR clustering by Dishevelled interacting with MuSK and PAK1 Neuron 35:489–505. doi: 10.1016/S0896-6273(02)00783-3
40. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, van de Wetering M, Clevers H, Schlag PM, Birchmeier W, Behrens J. 2002 Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Molecular and Cellular Biology 22:1184–1193. doi: 10.1128/MCB.22.4.1184-1193.2002
41. MacDonald BT, Tamai K, He X. 2009 Wnt/beta-catenin signaling: components, mechanisms, and diseases. Developmental Cell 17:9–26. doi: 10.1016/j.devcel.2009.06.016
42. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C, Tessier-Lavigne M, Chedotal A. 2004 The slit receptor Rig- 1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 43:69–79. doi: 10.1016/j.neuron.2004.06.018
43. Marinescu VD, Kohane IS, Riva A. 2005 The MAPPER database: a multi-genome catalog of putative transcription factor binding sites. Nucleic Acids Research 33:D91–D97. doi: 10.1093/nar/gki103
44. Marques MJ, Conchello JA, Lichtman JW. 2000 From plaque to pretzel: fold formation and acetylcholine receptor loss at the developing neuromuscular junction. The Journal of Neuroscience 20:3663–3675
45. Masiakowski P, Yancopoulos GD. 1998 The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Current Biology 8:R407. doi: 10.1016/S0960-9822(98)70263-5
46. McCabe BD, Hom S, Aberle H, Fetter RD, Marques G, Haerry TE, Wan H, O’Connor MB, Goodman CS, Haghighi AP. 2004 Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41:891–905. doi: 10.1016/S0896-6273(04)00073-X.
47. McCabe BD, Marques G, Haghighi AP, Fetter RD, Crotty ML, Haerry TE, Goodman CS, O’Connor MB. 2003 The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39:241–254. doi: 10.1016/S0896-6273(03)00426-4
48. McMahan UJ. 1990 The agrin hypothesis. Cold Spring Harbor Symposia on Quantitative Biology 55:407–418. doi: 10.1101/SQB.1990.055.01.041
49. Messé ant J, Dobbertin A, Girard E, Delers P, Manuel M, Mangione F, Schmitt A, Le Denmat D, Molgó J, Zytnicki D, Schaeffer L, Legay C, Strochlic L. 2015 MuSK frizzled-like domain is critical for mammalian neuromuscular junction formation and maintenance. Journal of Neuroscience 35:4926–4941. doi: 10.1523/JNEUROSCI.3381-14.2015
50. Miniou P, Tiziano D, Frugier T, Roblot N, Le Meur M, Melki J. 1999 Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Research 27:e27. doi: 10.1093/nar/27.19.e27
51. Miyashita T, Yeo SY, Hirate Y, Segawa H, Wada H, Little MH, Yamada T, Takahashi N, Okamoto H. 2004 PlexinA4 is necessary as a downstream target of Islet2 to mediate Slit signaling for promotion of sensory axon branching. Development 131:3705–3715. doi: 10.1242/dev.01228
52. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O, Clevers H. 1996 XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391–399. doi: 10.1016/S0092-8674(00)80112-9
53. Monks DA, Johansen JA, Mo K, Rao P, Eagleson B, Yu Z, Lieberman AP, Breedlove SM, Jordan CL. 2007 Overexpression of wild-type androgen receptor in muscle recapitulates polyglutamine disease. Proceedings of the National Academy of Sciences of USA 104:18259–18264. doi: 10.1073/pnas.0705501104
54. Murase S, Mosser E, Schuman EM. 2002 Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35:91–105. doi: 10.1016/S0896-6273(02)00764-X.
55. Nelson WJ, Nusse R. 2004 Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303:1483–1487. doi: 10.1126/science.1094291
56. Nguyen Ba-Charvet KT, Brose K, Ma L, Wang KH, Marillat V, Sotelo C, Tessier-Lavigne M, Chedotal A. 2001 Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. The Journal of Neuroscience 21:4281–4289
57. Nguyen Ba-Charvet KT, Brose K, Marillat V, Kidd T, Goodman CS, Tessier-Lavigne M, Sotelo C, Chedotal A. 1999 Slit2-Mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22:463–473. doi: 10.1016/S0896-6273(00)80702-3
58. Nguyen-Ba-Charvet KT, Plump AS, Tessier-Lavigne M, Chedotal A. 2002 Slit1 and slit2 proteins control the development of the lateral olfactory tract. The Journal of Neuroscience 22:5473–5480
59. Niclou SP, Jia L, Raper JA. 2000 Slit2 is a repellent for retinal ganglion cell axons. The Journal of Neuroscience 20: 4962–4974
60. Nishimune H, Sanes JR, Carlson SS. 2004 A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432:580–587. doi: 10.1038/nature03112
61. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995 Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2 Nature 374:258–262. doi: 10.1038/374258a0
62. Nuriya M, Huganir RL. 2006 Regulation of AMPA receptor trafficking by N-cadherin. Journal of Neurochemistry 97:652–661. doi: 10.1111/j.1471-4159.2006.03740.x.
63. Oppenheim RW, Houenou LJ, Johnson JE, Lin LF, Li L, Lo AC, Newsome AL, Prevette DM, Wang S. 1995 Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373: 344–346. doi: 10.1038/373344a0
64. Prakash S, Caldwell JC, Eberl DF, Clandinin TR. 2005 Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets. Nature Neuroscience 8:443–450. doi: 10.1038/nn1415
65. Ringstedt T, Braisted JE, Brose K, Kidd T, Goodman C, Tessier-Lavigne M, O’Leary DD. 2000 Slit inhibition of retinal axon growth and its role in retinal axon pathfinding and innervation patterns in the diencephalon. The Journal of Neuroscience 20:4983–4991
66. Rotundo RL, Ruiz CA, Marrero E, Kimbell LM, Rossi SG, Rosenberry T, Darr A, Tsoulfas P. 2008 Assembly and regulation of acetylcholinesterase at the vertebrate neuromuscular junction. Chemico-Biological Interactions 175: 26–29. doi: 10.1016/j.cbi.2008.05.025
67. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M. 2004 The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117:157–169. doi: 10.1016/S0092-8674(04)00303-4
68. Sanes JR, Lichtman JW. 2001 Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nature Reviews. Neuroscience 2:791–805. doi: 10.1038/35097557
69. Schuman EM, Murase S. 2003 Cadherins and synaptic plasticity: activity-dependent cyclin-dependent kinase 5 regulation of synaptic beta-catenin-cadherin interactions. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 358:749–756. doi: 10.1098/rstb.2002.1256
70. Schwander M, Shirasaki R, Pfaff SL, Muller U. 2004 Beta1 integrins in muscle, but not in motor neurons, are required for skeletal muscle innervation. The Journal of Neuroscience 24:8181–8191. doi: 10.1523/JNEUROSCI.1345-04.2004
71. Shu T, Sundaresan V, McCarthy MM, Richards LJ. 2003 Slit2 guides both precrossing and postcrossing callosal axons at the midline in vivo. The Journal of Neuroscience 23:8176–8184
72. Strochlic L, Falk J, Goillot E, Sigoillot S, Bourgeois F, Delers P, Rouvière J, Swain A, Castellani V, Schaeffer L, Legay C. 2012 Wnt4 participates in the formation of vertebrate neuromuscular junction. PLOS ONE 7:e29976. doi: 10.371/journal.pone.0029976
73. Tai CY, Mysore SP, Chiu C, Schuman EM. 2007 Activity-regulated N-cadherin endocytosis. Neuron 54:771–785. doi: 10.1016/j.neuron.2007.05.013
74. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X. 2000 LDL-receptorrelated proteins in Wnt signal transduction. Nature 407:530–535. doi: 10.1038/35035117
75. Timpl R, Tisi D, Talts JF, Andac Z, Sasaki T, Hohenester E. 2000 Structure and function of laminin LG modules. Matrix Biology 19:309–317. doi: 10.1016/S0945-053X(00)00072-X.
76. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H. 1997 Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789–799. doi: 10.1016/S0092-8674(00)81925-X.
77. Vleminckx K, Kemler R, Hecht A. 1999 The C-terminal transactivation domain of beta-catenin is necessary and sufficient for signaling by the LEF-1/beta-catenin complex in Xenopus laevis. Mechanisms of Development 81: 65–74. doi: 10.1016/S0925-4773(98)00225-1
78. Wang CY, Yang F, He XP, Je HS, Zhou JZ, Eckermann K, Kawamura D, Feng L, Shen L, Lu B. 2002 Regulation of neuromuscular synapse development by glial cell line-derived neurotrophic factor and neurturin. The Journal of Biological Chemistry 277:10614–10625. doi: 10.1074/jbc.M106116200
79. Wang J, Jing Z, Zhang L, Zhou G, Braun J, Yao Y, Wang ZZ. 2003 Regulation of acetylcholine receptor clustering by the tumor suppressorAPC. Nature Neuroscience 6:1017–1018. doi: 10.1038/nn1128
80. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS, Henzel W, Tessier-Lavigne M. 1999 Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96:771–784. doi: 10.1016/S0092-8674(00)80588-7
81. Wang L, Marquardt T. 2012 Direct live monitoring of heterotypic axon-axon interactions in vitro. Nature Protocols 7:351–363. doi: 10.1038/nprot.2011.442
82. Weatherbee SD, Anderson KV, Niswander LA. 2006 LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133:4993–5000. doi: 10.1242/dev.02696
83. Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M, Chedotal A, Ghosh A. 2002 Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33:47–61. doi: 10.1016/S0896-6273(01)00566-9
84. Wong V, Glass DJ, Arriaga R, Yancopoulos GD, Lindsay RM, Conn G. 1997 Hepatocyte growth factor promotes motor neuron survival and synergizes with ciliary neurotrophic factor. The Journal of Biological Chemistry 272: 5187–5191. doi: 10.1074/jbc.272.8.5187
85. Wu H, Lu Y, Barik A, Joseph A, Taketo MM, Xiong WC, Mei L. 2012a. beta-Catenin gain of function in muscles impairs neuromuscular junction formation. Development 139:2392–2404. doi: 10.1242/dev.080705
86. Wu H, Lu Y, Shen C, Patel N, Gan L, Xiong WC, Mei L. 2012b. Distinct roles of muscle and motoneuron LRP4 in neuromuscular junction formation. Neuron 75:94–107. doi: 10.1016/j.neuron.2012.04.033
87. Wu H, Xiong WC, Mei L. 2010 To build a synapse: signaling path ays in neuromuscular junction assembly. Development 137:1017–1033. doi: 10.1242/dev.038711
88. Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, Rao Y. 1999 Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400:331–336. doi: 10.1038/22477
89. Xu L, Corcoran RB, Welsh JW, Pennica D, Levine AJ. 2000 WISP-1 is a Wnt-1- and beta-catenin-responsive oncogene. Genes & Development 14:585–595
90. Yamamoto Y, Livet J, Pollock RA, Garces A, Arce V, deLapeyriere O, Henderson CE. 1997 Hepatocyte growth factor (HGF/SF) is a muscle-derived survival factor for a subpopulation of embryonic motoneurons. Development 124:2903–2913
91. Yan D, Wiesmann M, Rohan M, Chan V, Jefferson AB, Guo L, Sakamoto D, Caothien RH, Fuller JH, Reinhard C, Garcia PD, Randazzo FM, Escobedo J, Fantl WJ, Williams LT. 2001 Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta -catenin signaling is activated in human colon tumors. Proceedings of the National Academy of Sciences of USA 98:14973–14978. doi: 10.1073/pnas.261574498
92. Yumoto N, Kim N, Burden SJ. 2012 Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature 489:438–442. doi: 10.1038/nature11348
93. Zhang B, Liang C, Bates R, Yin Y, Xiong WC, Mei L. 2012 Wnt proteins regulate acetylcholine receptor clustering in muscle cells. Molecular Brain 5:7. doi: 10.1186/1756-6606-5-7
94. Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. 2008 LRP4 serves as a coreceptor of agrin. Neuron 60: 285–297. doi: 10.1016/j.neuron.2008.10.006
95. Zhang B, Xiong WC, Mei L. 2009 Get ready to Wnt: prepatterning in neuromuscular junction formation. Developmental Cell 16:325–327. doi: 10.1016/j.devcel.2009.03.001
96. Zhang J, Lefebvre JL, Zhao S, Granato M. 2004 Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nature Neuroscience 7:1303–1309. doi: 10.1038/nn1350
97. Zinyk DL, Mercer EH, Harris E, Anderson DJ, Joyner AL. 1998 Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Current Biology 8:665–668. doi: 10.1016/S0960-9822(98)70255-6.