A cell surface interaction network of neural leucine-rich repeat receptors

Genome Biology

Volumn 10, Issue 9, 2009, Pages

  Söllner, Christian ^a,b   Wright, Gavin J ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; EXTRACELLULAR LEUCINE RICH REPEAT AND FIBRONECTIN; LEUCINE RICH REPEAT NEURONAL; LEUCINE RICH REPEAT RECEPTOR; LEUCINE RICH REPEAT TRANSMEMBRANE PROTEIN; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG; LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; PROTEIN; ZEBRAFISH PROTEIN;

ARTICLE; CELL SURFACE; GENE EXPRESSION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BRAIN; CONFOCAL MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOMICS; IN SITU HYBRIDIZATION; METABOLISM; METHODOLOGY; PRENATAL DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY RECEPTOR; SPINAL CORD;

DANIO RERIO; VERTEBRATA;

ANIMALS; BRAIN; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENOMICS; IN SITU HYBRIDIZATION; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, CONFOCAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEINS; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SENSORY RECEPTOR CELLS; SPINAL CORD; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 76249121966     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-9-r99     Document Type: Article

References (49)

1. Lichtman JW, Smith SJ. Seeing circuits assemble. Neuron 2008, 60:441-448. 10.1016/j.neuron.2008.10.040, 18995818.
2. Akins MR, Biederer T. Cell-cell interactions in synaptogenesis. Curr Opin Neurobiol 2006, 16:83-89. 10.1016/j.conb.2006.01.009, 16427268.
3. Dickson BJ. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964. 10.1126/science.1072165, 12471249.
4. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176. 10.1038/nature05453, 17151600.
5. Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007, 10:19-26. 10.1038/nn1827, 17189949.
6. Chen Y, Aulia S, Li L, Tang BL. AMIGO and friends: an emerging family of brain-enriched, neuronal growth modulating, type I transmembrane proteins with leucine-rich repeats (LRR) and cell adhesion molecule motifs. Brain Res Rev 2006, 51:265-274. 10.1016/j.brainresrev.2005.11.005, 16414120.
7. Dolan J, Walshe K, Alsbury S, Hokamp K, O'Keeffe S, Okafuji T, Miller SF, Tear G, Mitchell KJ. The extracellular Leucine-Rich Repeat superfamily; a comparative survey and analysis of evolutionary relationships and expression patterns. BMC Genomics 2007, 8:320. 10.1186/1471-2164-8-320, 2235866, 17868438.
8. Bando T, Sekine K, Kobayashi S, Watabe AM, Rump A, Tanaka M, Suda Y, Kato S, Morikawa Y, Manabe T, Miyajima A. Neuronal leucine-rich repeat protein 4 functions in hippocampus-dependent long-lasting memory. Mol Cell Biol 2005, 25:4166-4175. 10.1128/MCB.25.10.4166-4175.2005, 1087730, 15870286.
9. Wolfe AD, Henry JJ. Neuronal leucine-rich repeat 6 (XlNLRR-6) is required for late lens and retina development in Xenopus laevis. Dev Dyn 2006, 235:1027-1041. 10.1002/dvdy.20691, 16456849.
10. Aruga J, Mikoshiba K. Identification and characterization of Slitrk, a novel neuronal transmembrane protein family controlling neurite outgrowth. Mol Cell Neurosci 2003, 24:117-129. 10.1016/S1044-7431(03)00129-5, 14550773.
11. Lin JC, Ho WH, Gurney A, Rosenthal A. The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons. Nat Neurosci 2003, 6:1270-1276. 10.1038/nn1148, 14595443.
12. Robinson M, Parsons Perez MC, Tebar L, Palmer J, Patel A, Marks D, Sheasby A, De Felipe C, Coffin R, Livesey FJ, Hunt SP. FLRT3 is expressed in sensory neurons after peripheral nerve injury and regulates neurite outgrowth. Mol Cell Neurosci 2004, 27:202-214. 10.1016/j.mcn.2004.06.008, 15485775.
13. Wang CY, Chang K, Petralia RS, Wang YX, Seabold GK, Wenthold RJ. A novel family of adhesion-like molecules that interacts with the NMDA receptor. J Neurosci 2006, 26:2174-2183. 10.1523/JNEUROSCI.3799-05.2006, 16495444.
14. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 2006, 9:1294-1301. 10.1038/nn1763, 16980967.
15. Ko J, Kim S, Chung HS, Kim K, Han K, Kim H, Jun H, Kaang BK, Kim E. SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 2006, 50:233-245. 10.1016/j.neuron.2006.04.005, 16630835.
16. Linhoff MW, Lauren J, Cassidy RM, Dobie FA, Takahashi H, Nygaard HB, Airaksinen MS, Strittmatter SM, Craig AM. An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 2009, 61:734-749. 10.1016/j.neuron.2009.01.017, 19285470.
17. Kuja-Panula J, Kiiltomaki M, Yamashiro T, Rouhiainen A, Rauvala H. AMIGO, a transmembrane protein implicated in axon tract development, defines a novel protein family with leucine-rich repeats. J Cell Biol 2003, 160:963-973. 10.1083/jcb.200209074, 2173769, 12629050.
18. Yiu G, He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 2006, 7:617-627. 10.1038/nrn1956, 2693386, 16858390.
19. Francks C, Maegawa S, Lauren J, Abrahams BS, Velayos-Baeza A, Medland SE, Colella S, Groszer M, McAuley EZ, Caffrey TM, Timmusk T, Pruunsild P, Koppel I, Lind PA, Matsumoto-Itaba N, Nicod J, Xiong L, Joober R, Enard W, Krinsky B, Nanba E, Richardson AJ, Riley BP, Martin NG, Strittmatter SM, Moller HJ, Rujescu D, St Clair D, Muglia P, Roos JL, et al. LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol Psychiatry 2007, 12:1129-1139. 10.1038/sj.mp.4002053, 17667961.
20. Majercak J, Ray WJ, Espeseth A, Simon A, Shi XP, Wolffe C, Getty K, Marine S, Stec E, Ferrer M, Strulovici B, Bartz S, Gates A, Xu M, Huang Q, Ma L, Shughrue P, Burchard J, Colussi D, Pietrak B, Kahana J, Beher D, Rosahl T, Shearman M, Hazuda D, Sachs AB, Koblan KS, Seabrook GR, Stone DJ. LRRTM3 promotes processing of amyloid-precursor protein by BACE1 and is a positional candidate gene for late-onset Alzheimer's disease. Proc Natl Acad Sci USA 2006, 103:17967-17972. 10.1073/pnas.0605461103, 1635650,1635650, 17098871.
21. Abelson JF, Kwan KY, O'Roak BJ, Baek DY, Stillman AA, Morgan TM, Mathews CA, Pauls DL, Rasin MR, Gunel M, Davis NR, Ercan-Sencicek AG, Guez DH, Spertus JA, Leckman JF, Dure L, Kurlan R, Singer HS, Gilbert DL, Farhi A, Louvi A, Lifton RP, Sestan N, State MW. Sequence variants in SLITRK1 are associated with Tourette's syndrome. Science 2005, 310:317-320. 10.1126/science.1116502, 16224024.
22. Kalachikov S, Evgrafov O, Ross B, Winawer M, Barker-Cummings C, Martinelli Boneschi F, Choi C, Morozov P, Das K, Teplitskaya E, Yu A, Cayanis E, Penchaszadeh G, Kottmann AH, Pedley TA, Hauser WA, Ottman R, Gilliam TC. Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat Genet 2002, 30:335-341. 10.1038/ng832, 2606053, 11810107.
23. Merwe PA, Barclay AN. Transient intercellular adhesion: the importance of weak protein-protein interactions. Trends Biochem Sci 1994, 19:354-358. 10.1016/0968-0004(94)90109-0, 7985226.
24. Bushell KM, Sollner C, Schuster-Boeckler B, Bateman A, Wright GJ. Large-scale screening for novel low-affinity extracellular protein interactions. Genome Res 2008, 18:622-630. 10.1101/gr.7187808, 2279249, 18296487.
25. Karaulanov EE, Bottcher RT, Niehrs C. A role for fibronectin-leucine-rich transmembrane cell-surface proteins in homotypic cell adhesion. EMBO Rep 2006, 7:283-290. 10.1038/sj.embor.7400614, 1456895, 16440004.
26. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999, 96:795-806. 10.1016/S0092-8674(00)80590-5, 10102268.
27. Liu BP, Fournier A, GrandPre T, Strittmatter SM. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002, 297:1190-1193. 10.1126/science.1073031, 12089450.
28. Karaulanov E, Bottcher RT, Stannek P, Wu W, Rau M, Ogata S, Cho KW, Niehrs C. Unc5B interacts with FLRT3 and Rnd1 to modulate cell adhesion in Xenopus embryos. PLoS One 2009, 4:e5742. 10.1371/journal.pone.0005742, 2683942, 19492039.
29. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838. 10.1038/386833a0, 9126742.
30. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999, 97:927-941. 10.1016/S0092-8674(00)80804-1, 10399920.
31. Haines BP, Wheldon LM, Summerbell D, Heath JK, Rigby PW. Regulated expression of FLRT genes implies a functional role in the regulation of FGF signalling during mouse development. Dev Biol 2006, 297:14-25. 10.1016/j.ydbio.2006.04.004, 16872596.
32. Mumm JS, Godinho L, Morgan JL, Oakley DM, Schroeter EH, Wong RO. Laminar circuit formation in the vertebrate retina. Prog Brain Res 2005, 147:155-169. full_text, 15581704.
33. Jontes JD, Buchanan J, Smith SJ. Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo. Nat Neurosci 2000, 3:231-237. 10.1038/72936, 10700254.
34. Ross CA, Margolis RL, Reading SA, Pletnikov M, Coyle JT. Neurobiology of schizophrenia. Neuron 2006, 52:139-153. 10.1016/j.neuron.2006.09.015, 17015232.
35. Kurusu M, Cording A, Taniguchi M, Menon K, Suzuki E, Zinn K. A screen of cell-surface molecules identifies leucine-rich repeat proteins as key mediators of synaptic target selection. Neuron 2008, 59:972-985. 10.1016/j.neuron.2008.07.037, 2630283, 18817735.
36. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78. 10.1038/nature01176, 12422217.
37. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S, Timm J, Mintzlaff S, Abraham C, Bock N, Kietzmann S, Goedde A, Toksoz E, Droege A, Krobitsch S, Korn B, Birchmeier W, Lehrach H, Wanker EE. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005, 122:957-968. 10.1016/j.cell.2005.08.029, 16169070.
38. Barrios-Rodiles M, Brown KR, Ozdamar B, Bose R, Liu Z, Donovan RS, Shinjo F, Liu Y, Dembowy J, Taylor IW, Luga V, Przulj N, Robinson M, Suzuki H, Hayashizaki Y, Jurisica I, Wrana JL. High-throughput mapping of a dynamic signaling network in mammalian cells. Science 2005, 307:1621-1625. 10.1126/science.1105776, 15761153.
39. Wojtowicz WM, Wu W, Andre I, Qian B, Baker D, Zipursky SL. A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 2007, 130:1134-1145. 10.1016/j.cell.2007.08.026, 2707357, 17889655.
40. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, Levesque M, Allaire N, Perrin S, Sands B, Crowell T, Cate RL, McCoy JM, Pepinsky RB. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004, 7:221-228. 10.1038/nn1188, 14966521.
41. Dustin ML, Golan DE, Zhu DM, Miller JM, Meier W, Davies EA, Merwe PA. Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J Biol Chem 1997, 272:30889-30898. 10.1074/jbc.272.49.30889, 9388235.
42. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310.
43. Ensembl. , http://www.ensembl.org/
44. Durocher Y, Perret S, Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res 2002, 30:E9. 10.1093/nar/30.2.e9, 99848, 11788735.
45. The International Molecular Exchange Consortium (IMEx). , http://imex.sf.net
46. Wright GJ, Puklavec MJ, Willis AC, Hoek RM, Sedgwick JD, Brown MH, Barclay AN. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 2000, 13:233-242. 10.1016/S1074-7613(00)00023-6, 10981966.
47. Clay H, Ramakrishnan L. Multiplex fluorescent in situ hybridization in zebrafish embryos using tyramide signal amplification. Zebrafish 2005, 2:105-111. 10.1089/zeb.2005.2.105, 18248170.
48. A Neuroreceptor Network. , http://www.sanger.ac.uk/Teams/Team30/network.shtml
49. The Zebrafish Model Organism Database. , http://zfin.org/cgi-bin/webdriver?MIval=aa-ZDB_home.apg