Synapse formation regulated by protein tyrosine phosphatase receptor T through interaction with cell adhesion molecules and Fyn

EMBO Journal

Volumn 28, Issue 22, 2009, Pages 3564-3578

  Lim, So Hee ^a,c   Kwon, Seok Kyu ^b   Lee, Myung Kyu ^a   Moon, Jeonghee ^a   Jeong, Dae Gwin ^a   Park, Eunha ^a   Kim, Seung Jun ^a   Park, Byung Chul ^a   Lee, Sang Chul ^a   Ryu, Seong Eon ^a   Yu, Dae Yeul ^a   Chung, Bong Hyun ^a   Kim, Eunjoon ^b   Myung, Pyung Keun ^c   Lee, Jae Ran ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c Chungnam National University   (South Korea)

Author keywords

Cell adhesion molecule; Fyn; PTPRT; Synapse formation; Tyrosine phosphorylation

Indexed keywords

CELL ADHESION MOLECULE; NEUROLIGIN; PROTEIN KINASE FYN; PROTEIN TYROSINE PHOSPHATASE RECEPTOR T; RECEPTOR PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; EXTRACELLULAR SPACE; GROWTH REGULATION; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SYNAPSE;

ANIMALS; BRAIN; CELL ADHESION MOLECULES; CELLS, CULTURED; GUINEA PIGS; HUMANS; MICE; MODELS, BIOLOGICAL; NEURONS; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; RNA, SMALL INTERFERING; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 70450222110     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.289     Document Type: Article

References (55)

1. Alonso A, Sasin J, Bottini N, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phospha-tases in the human genome. Cell 117: 699-711
2. Anders L, Mertins P, Lammich S, Murgia M, Hartmann D, Saftig P, Haass C, Ullrich A (2006) Furin-, ADAM 10-, and g-secretase-mediated cleavage of a receptor tyrosine phosphatase and regulation of b-catenin's transcriptional activity. Mol Cell Biol 26: 3917-3934
3. Arac D, Boucard AA, Ozkan E, Strop P, Newell E, Sudhof TC, Byunger AT (2007) Structures of neuroligin-1 and the neuroli-gin-1/neurexin-1b complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron 56: 992-1003
4. Aricescu AR, Siebold C, Choudhuri K, Chang VT, Lu W, Davis SJ, Anton van Merwe P, Jones EY (2007) Structure of a tyrosine phosphatase adhesive interaction reveals a spacer-clamp mechanism. Science 317: 1217-1220
5. Barford ZJ, Flint AJ, Tonks NK (1995) Structural basis for phospho-tyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268: 1754-1758
6. Berman-Golan D, Elson A (2007) Neu-meditated phosphorylation of protein tyrosine phosphatase epsilon is critical for activation of Src in mammary tumor cells. Oncogene 26: 7028-7037
7. Besco J, Huijsduijnen R, Frostholm A, Rotter A (2006) Intracellular substrates of brain-enriched receptor protein tyrosine phospha-tase rho (RPTPr/PTPRT). Brain Res 1116: 50-57
8. Besco J, Popesco MC, Davuluri RV, Frostthlm A, Rotter A (2004) Genomic structure and alternative splicing of murine R2B receptor protein tyrosine phosphatases (PTPk, m, r and PCP-2). BMC Genomics 5: 14-32
9. Bilwes AM, den Hertog J, Hunter T, Noel JP (1996) Structural basis for inhibition of receptor protein-tyrosine phosphatase-a by di-merization. Nature 382: 555-559
10. Blanchetot C, Tertoolen LGJ, den Hertog J (2002) Regulation of receptor protein-tyrosine phosphatase a by oxidative stress. EMBO J 21: 493-503 (Pubitemid 34174031)
11. Bodrikov V, Leshchyns'ka I, Sytnyk V, Overvoorde J, den Hertog J, Schachner M (2005) RPTPa is essential for NCAM-mediated p59fyn activation and neurite elongation. J Cell Biol 168: 127-139
12. Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanism. Science 296: 1308-1313
13. Boucard AA, Chubykin AA, Comoletti D, Taylor P, Sudhof TC (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to a-and b-neurexins. Neuron 48: 229-236
14. Brady-Kalnay SM, Rimm DL, Tonks NK (1995) Receptor protein tyrosine phosphatase PTPm associates with cadherins in vivo. J Cell Biol 130: 977-986
15. Burden-Gulley SM, Brady-Kalnay SM (1999) PTPm regulates N-cadherin-dependent neurite outgrowth. J Cell Biol 144: 1323-1336
16. Chih B, Engelman H, Scheiffele P (2005) Control of excitatory and inhibitory synapse formation by neuroligins. Science 307: 1324-1328
17. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, Sudhof TC (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54: 919-931
18. Comoletti D, Grishaev A, Whitten AE, Tsigelny I, Taylor P, Trewhella J (2007) Synaptic arrangement of the neuroligin/b-neurexin complex revealed by X-ray and neutron scattering. Structure 15: 693-705
19. Craig AM, Kang Y (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurol 17: 43-52
20. Dean C, Dresbach T (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci 29: 21-29
21. Dean C, Sholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6: 708-716
22. Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8: 458-467
23. Eswaran J, Debreczeni JE, Longman E, Barr AJ, Knapp S (2006) The crystal structure of human receptor protein tyrosine phosphatase k phosphatase domain 1. Protein Sci 15: 1500-1505 (Pubitemid 43800021)
24. Gebbink MFBG, Zondag GCM, Koningstein GM, Feiken E, Wubbolts RW, Moolenaar WH (1995) Cell surface expression of receptor protein tyrosine phosphatase RPTPm is regulated by cell-cell contact. J Cell Biol 131: 251-260
25. Graf ER, Zhang X, Jin SX, Linoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119: 1013-1026
26. Harroch S, Palmeri M, Rosenbluth J, Custer A, Okigaki M, Shrager P, Blum M, Buxbaum JD, Schlessinger J (2000) No obvious abnormality in mice deficient in receptor protein tyrosine phosphatse b. Mol Cell Biol 20: 7706-7715
27. Hoffmann K, Tonks NK, Barford D (1997) The crystal structure of domain 1 of receptor protein-tyrosine phsophatase m. J Biol Chem 272: 27505-27508
28. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SGN (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3: 661-669
29. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C (2003) Mutations of the X-linked genes encoding neuroligins NLG3 and NLG4 are associated with autism. Nat Genet 34: 27-29
30. Jiang YP, Wang H, D'Eustachio P, Musacchio JM, Schlessinger J, Sap J (1993) Cloning and characterization of R-PTP-k, a new member of the receptor protein tyrosine phosphatase family with a proteolytically cleaved cellular adhesion molecule-like extracellular region. Mol Cell Biol 13: 2942-2951
31. Johnson KG, Van Vactor D (2003) Receptor protein tyrosine phos-phatases in nervous system development. Physiol Rev 83: 1-24
32. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, Kim E (2006) NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9: 1294-1301
33. Krasnoperov V, Bittner M, Mo W, Buryanovsky L, Neubert T, Holz RW, Ichtchenko K, Petrenko AG (2002) Protein-tyrosine phosphatase-s is a novel member of the functional family of a-latrotoxin receptors. J Biol Chem 277: 35887-35895
34. Lee JR, Shin H, Choi J, Ko J, Kim S, Lee HW, Kim K, Rho SH, Lee JH, Song HE, Eom SH, Kim E (2004) An intramolecular interaction between the FHA domain and a coiled coil negatively regulates the kinesin motor KIF1A. EMBO J 23: 1506-1515
35. Liu H, Nakazawa T, Tezuka T, Yamamoto T (2006) Physical and functional interaction of Fyn tyrosine kinase with a brain-enriched Rho GTPase-activating protein TCGAP. J Biol Chem 281: 23611-23619
36. McAndrew PE, Frostholm A, Evans JE, Zdilar D, Goldowitz D, Chiu IM, Burghes AHM, Rotter A (1998) Novel receptor protein tyrosine phosphatase (RPTPr) and acidic fibroblast growth factor (FGF-1) transcripts delineate a rostrocaudal boundary in the granule cell layer of the murine cerebellar cortex. J Comp Neurol 391: 444-455
37. Mustelin T, Altman A (1990) Dephosphorylation and activation of the T cell tyrosine kinase pp56lck by the leukocyte common antigen(CD45). Oncogene 5: 809-813
38. Nam HJ, Poy F, Krueger NX, Saito H, Frederick CA (1999) Crystal structure of the tandem phosphatase domains of RPTP LAR. Cell 97: 449-457
39. Nam HJ, Poy F, Krueger NX, Saito H, Frederick CA (2005) Structural basis for the function and regulation of the receptor protein tyrosine phosphatase CD45. J Exp Med 201: 441-452
40. Paul S, Lombroso PJ (2003) Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci 60: 2465-2482
41. Petrone A, Battaglia F, Wang C, Dusa A, Su J, Zagzag D, Bianchi R, Casaccia-Bonnefil P, Arancio O, Sap J (2003) Receptor protein tyrosine phosphatase a is essential for hippo-campal neuronal migraton and long-term potentiation. EMBO J 22: 4121-4131
42. Sallee JL, Wittchen ES, Burridge K (2006) Regulation of cell adhesion by protein-tyrosine phosphatases. II. Cell-cell adhesion. J Biol Chem 281: 16189-16192 (Pubitemid 43909565)
43. Shintani T, Ihara M, Sakuta H, Takahashi H, Watakabe I, Noda M (2006) Eph receptors are negatively controlled by protein tyrosine phosphatase receptor type O. Nat Neurosci 9: 761-769
44. Sudhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911
45. Tsujikawa K, Ichijo T, Moriyama K, Tadotsu N, Sakamoto K, Sakane N, Fukada S, Furukawa T, Saito H, Yamamoto H (2002) Regulation of Lck and Fyn tyrosine kinase activities by trans-membrane protein tyrosine phosphatase leukocyte common antigen-related molecule. Mol Cancer Res 1: 155-163
46. Uetani N, Chagnon MJ, Kennedy TE, Iwakura Y, Tremblay ML (2006) Mammalian motoneuron axon targeting requires receptor protein tyrosine phosphatase s and d. J Neurosci 2006: 5872-5880
47. van Montfort RLM, Congreve M, Tisi D, Carr R, Jhoti H (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423: 773-777
48. Vogel W, Lammers R, Huang J, Ullrich A (1993) Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science 259: 1611-1614
49. Wang Z, Shen D, Parsons DW, Bardelli A, Sager J, Szabo S, Ptak J, Silliman N, Peters BA, van der Heijden MS, Parmigiani G, Yan H, Wang TL, Riggins G, Powell SM, Wilson KV, Markowitz S, Kinzler KW, Vogelstein B, Velculescu VE (2004) Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 304: 1164-1166
50. Woo J, Kwon SK, Choi S, Kim S, Lee JR, Dunah A, Sheng M, Kim E (2009) Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat Neurosci 12: 428-437
51. Xie Y, Yeo TT, Zhang C, Yang T, Tisi MA, Massa SM, Longo FM (2001) The leukocyte common antigne-related tyrosine phospha-tase receptor regulates regenerative outgrowth in vivo. J Neurosci 21: 5130-5138
52. Zeng L, D'Alessamdri L, Kalousek MB, Vaughan L, Pallen CJ (1999) Protein tyrosine phosphatase a (PTPa) and contactin form a novel neuronal receptor complex linked to the intracellular tyrosine kinase Fyn. J Cell Biol 147: 707-713
53. Zhang X, Guo A, Yu J, Possemato A, Chen Y, Zheng W, Polakiewicz RD, Kinzler KW, Vogelstein B, Velculescu VE, Wang ZJ (2007) Identification of STAT3 as a substrate of receptor protein tyrosine phosphatase T. Proc Natl Acad Sci 104: 4060-4064
54. Zheng XM, Resnick RJ, Shalloway D (2000) A phosphotyrosine displacement mechanism for activation of Src by PTPa. EMBO J 19: 964-978
55. Zondag GCM, Koningstein GM, Jiang YP, Sap J, Moolenaar WH, Gebbink MFBG (1995) Homophilic interactions mediated by receptor tyrosine phosphatase m and k. J Biol Chem 270: 14247-14250