Expression of neurexin, neuroligin, and their cytoplasmic binding partners in the pancreatic β-cells and the involvement of neuroligin in insulin secretion

Endocrinology

Volumn 149, Issue 12, 2008, Pages 6006-6017

  Suckow, Arthur T ^a,b   Comoletti, Davide ^c   Waldrop, Megan A ^a   Mosedale, Merrie ^a,b   Egodage, Sonya ^a   Taylor, Palmer ^c   Chessler, Steven D ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; NEUREXIN; NEUROLIGIN;

ARTICLE; CELL SURFACE; CYTOPLASM; IN VITRO STUDY; INSULIN RELEASE; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SYNAPTOGENESIS;

ALTERNATIVE SPLICING; ANIMALS; BLOTTING, WESTERN; BRAIN; CARRIER PROTEINS; CELL ADHESION MOLECULES, NEURONAL; CELL LINE, TUMOR; GLYCOPROTEINS; GUANYLATE KINASE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEUROPEPTIDES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 57349156187     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0274     Document Type: Article

References (69)

1. Hori Y, Gu X, Xie X, Kim SK 2005 Differentiation of insulin-producing cells from human neural progenitor cells. PLoS Med 2:e103
2. Rulifson EJ, Kim SK, Nusse R 2002 Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118-1120
3. Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED 2001 The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94-116
4. Fujimoto K, Shibasaki T, Yokoi N, Kashima Y, Matsumoto M, Sasaki T, Tajima N, Iwanaga T, Seino S 2002 Piccolo, a Ca2+ sensor in pancreatic β-cells. Involvement of cAMP-GEFII.Rim2.Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497-50502
5. Ohara-Imaizumi M, Ohtsuka T, Matsushima S, Akimoto Y, Nishiwaki C, Nakamichi Y, Kikuta T, Nagai S, Kawakami H, Watanabe T, Nagamatsu S 2005 ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic β cells and functions in insulin exocytosis: interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Mol Biol Cell 16:3289-3300
6. Regazzi R, Wollheim CB, Lang J, Theler JM, Rossetto O, Montecucco C, Sadoul K, Weller U, Palmer M, Thorens B 1995 VAMP-2 and cellubrevin are expressed in pancreatic β-cells and are essential for Ca(2+ )-but not for GTP γ S-induced insulin secretion. EMBO J 14:2723-2730
7. Sadoul K, Lang J, Montecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA 1995 SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 128:1019-1028
8. Zhang W, Efanov A, Yang SN, Fried G, Kolare S, Brown H, Zaitsev S, Berggren PO, Meister B 2000 Munc-18 associates with syntaxin and serves as a negative regulator of exocytosis in the pancreatic β-cell. J Biol Chem 275:41521-41527
9. Zhang W, Lilja L, Bark C, Berggren PO, Meister B 2004 Mint1, a Munc-18-interacting protein, is expressed in insulin-secreting β-cells. Biochem Biophys Res Commun 320:717-721
10. Baekkeskov S, Aanstoot HJ, Christgau S, Reetz A, Solimena M, Cascalho M, Folli F, Richter-Olesen H, De Camilli P 1990 Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature 347:151-156
11. Suckow AT, Sweet IR, Van Yserloo B, Rutledge EA, Hall TR, Waldrop M, Chessler SD 2006 Identification and characterization of a novel isoform of the vesicular γ-aminobutyric acid transporter with glucose-regulated expression in rat islets. J Mol Endocrinol 36:187-199
12. Franklin IK, Wollheim CB 2004 GABA in the endocrine pancreas: its putative role as an islet cell paracrine-signalling molecule. J Gen Physiol 123:185-190
13. Craig AM, Kang Y 2007 Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17:43-52
14. Missler M, Sudhof TC 1998 Neurexins: three genes and 1001 products. Trends Genet 14:20-26
15. Bolliger MF, Pei J, Maxeiner S, Boucard AA, Grishin NV, Sudhof TC 2008 Unusually rapid evolution of Neuroligin-4 in mice. Proc Natl Acad Sci USA 105:6421-6426
16. Chih B, Gollan L, Scheiffele P 2006 Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51:171-178
17. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Sudhof TC 2002 SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531
18. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P 2003 Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708-716
19. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM 2004 Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026
20. Sara Y, Biederer T, Atasoy D, Chubykin A, Mozhayeva MG, Sudhof TC, Kavalali ET 2005 Selective capability of SynCAM and neuroligin for functional synapse assembly. J Neurosci 25:260-270
21. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T 2000 Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669
22. Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T 2007 SynCAMs organize synapses through heterophilic adhesion. J Neurosci 27:12516-12530
23. 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
24. Kang Y, Zhang X, Dobie F, Wu H, Craig AM 2008 Induction of GABAergic postsynaptic differentiation by α-neurexins. J Biol Chem 283:2323-2334
25. Song JY, Ichtchenko K, Sudhof TC, Brose N 1999 Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 96:1100-1105
26. Varoqueaux F, Jamain S, Brose N 2004 Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83:449-456
27. Chessler SD, Simonson WT, Sweet IR, Hammerle LP 2002 Expression of the vesicular inhibitory amino acid transporter in pancreatic islet cells: distribution of the transporter within rat islets. Diabetes 51:1763-1771
28. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, Sudhof TC 2003 α-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423:939-948
29. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Sudhof TC, Brose N 2006 Neuroligins determine synapse maturation and function. Neuron 51:741-754
30. Comoletti D, Flynn RE, Boucard AA, Demeler B, Schirf V, Shi J, Jennings LL, Newlin HR, Sudhof TC, Taylor P 2006 Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for β-neurexins. Biochemistry 45:12816-12827
31. Comoletti D, De Jaco A, Jennings LL, Flynn RE, Gaietta G, Tsigelny I, Ellisman MH, Taylor P 2004 The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J Neurosci 24:4889-4893
32. Comoletti D, Flynn R, Jennings LL, Chubykin A, Matsumura T, Hasegawa H, Sudhof TC, Taylor P 2003 Characterization of the interaction of a recombinant soluble neuroligin-1 with neurexin-1β. J Biol Chem 278:50497-50505
33. Reed NA, Oh DJ, Czymmek KJ, Duncan MK 2001 An immunohistochemical method for the detection of proteins in the vertebrate lens. J Immunol Methods 253:243-252
34. Sweet IR, Cook DL, DeJulio E, Wallen AR, Khalil G, Callis J, Reems J 2004 Regulation of ATP/ADP in pancreatic islets. Diabetes 53:401-409
35. Ichtchenko K, Nguyen T, Sudhof TC 1996 Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271:2676-2682
36. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Sudhof TC 1995 Neuroligin 1: a splice site-specific ligand for β-neurexins. Cell 81:435-443
37. 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 α- and β-neurexins. Neuron 48:229-236
38. Graf ER, Kang Y, Hauner AM, Craig AM 2006 Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 β LNS domain. J Neurosci 26:4256-4265
39. Sassoe-Pognetto M, Fritschy JM 2000 Mini-review: gephyrin, a major postsynaptic protein of GABAergic synapses. Eur J Neurosci 12:2205-2210
40. O'Brien RJ, Lau LF, Huganir RL 1998 Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8:364-369
41. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW, Sudhof TC 1997 Binding of neuroligins to PSD-95. Science 277:1511-1515
42. Poulopoulos A, Meyer G, Soykan T, Craig AM, Brose N, Varoqueaux F, Interaction of neuroligins with gephyrin is a critical link in inhibitory postsynaptic organization. Society for Neuroscience Meeting Planner, San Diego, CA, 2007, online:35.37/E16; available at www.abstractsonline.com/viewer/ viewAbstractPrintFriendly.asp?CKey={BDE0A39C-4622-401C-B16A-7A0B 0F903C19}&SKey={330F04B6-5567-486C-A696-B29C71969451}&MKey= {FF8B70E5-B7F9-4D07-A58A-C1068FDE9D25}&AKey={3A7DC0B9-D787-44AA-BD08- FA7BB2FE9004}
43. Tabuchi K, Biederer T, Butz S, Sudhof TC 2002 CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with caskin 1, a novel CASK-binding protein. J Neurosci 22:4264-4273
44. Prange O, Wong TP, Gerrow K, Wang YT, El-Husseini A 2004 A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci USA 101:13915-13920
45. Ohara-Imaizumi M, Nishiwaki C, Nakamichi Y, Kikuta T, Nagai S, Nagamatsu S 2004 Correlation of syntaxin-1 and SNAP-25 clusters with docking and fusion of insulin granules analysed by total internal reflection fluorescence microscopy. Diabetologia 47:2200-2207
46. Cirulli V, Baetens D, Rutishauser U, Halban PA, Orci L, Rouiller DG 1994 Expression of neural cell adhesion molecule (N-CAM) in rat islets and its role in islet cell type segregation. J Cell Sci 107(Pt 6):1429-1436
47. Craig AM, Graf ER, Linhoff MW 2006 How to build a central synapse: clues from cell culture. Trends Neurosci 29:8-20
48. Easom RA 2000 β-Granule transport and exocytosis. Semin Cell Dev Biol 11:253-266
49. De Jaco A, Kovarik Z, Comoletti D, Jennings LL, Gaietta G, Ellisman MH, Taylor P 2005 A single mutation near the C-terminus in α/β hydrolase fold protein family causes a defect in protein processing. Chem Biol Interact 157-158:371-372
50. Weir GC, Halban PA, Meda P, Wollheim CB, Orci L, Renold AE 1984 Dispersed adult rat pancreatic islet cells in culture: A, B, and D cell function. Metabolism 33:447-453
51. Chessler SD, Lernmark A 2000 Alternative splicing of GAD67 results in the synthesis of a third form of glutamic-acid decarboxylase in human islets and other non-neural tissues. J Biol Chem 275:5188-5192
52. Gammelsaeter R, Froyland M, Aragon C, Danbolt NC, Fortin D, Storm-Mathisen J, Davanger S, Gundersen V 2004 Glycine, GABA and their transporters in pancreatic islets of Langerhans: evidence for a paracrine transmitter interplay. J Cell Sci 117:3749-3758
53. Cabrera O, Jacques-Silva MC, Speier S, Yang SN, Kohler M, Fachado A, Vieira E, Zierath JR, Kibbey R, Berman DM, Kenyon NS, Ricordi C, Caicedo A, Berggren PO 2008 Glutamate is a positive autocrine signal for glucagon release. Cell Metab 7:545-554
54. Maffei A, Liu Z, Witkowski P, Moschella F, Del Pozzo G, Liu E, Herold K, Winchester RJ, Hardy MA, Harris PE 2004 Identification of tissue-restricted transcripts in human islets. Endocrinology 145:4513-4521
55. von Blankenfeld G, Turner J, Ahnert-Hilger G, John M, Enkvist MO, Stephenson F, Kettenmann H, Wiedenmann B 1995 Expression of functional GABAA receptors in neuroendocrine gastropancreatic cells. Pflugers Arch 430:381-388
56. Kennedy MB 1997 The postsynaptic density at glutamatergic synapses. Trends Neurosci 20:264-268
57. Fabrichny IP, Leone P, Sulzenbacher G, Comoletti D, Miller MT, Taylor P, Bourne Y, Marchot P 2007 Structural analysis of the synaptic protein neuroligin and its β-neurexin complex: determinants for folding and cell adhesion. Neuron 56:979-991
58. Comoletti D, Grishaev A, Whitten AE, Tsigelny I, Taylor P, Trewhella J 2007 Synaptic arrangement of the neuroligin/β-neurexin complex revealed by Xray and neutron scattering. Structure 15:693-705
59. Konstantinova I, Nikolova G, Ohara-Imaizumi M, Meda P, Kucera T, Zarbalis K, Wurst W, Nagamatsu S, Lammert E 2007 EphA-Ephrin-A-mediated β cell communication regulates insulin secretion from pancreatic islets. Cell 129:359-370
60. Hooghe-Peters EL, Meda P, Orci L 1981 Co-culture of nerve cells and pancreatic islets. Brain Res 227:287-292
61. Moller CJ, Christgau S, Williamson MR, Madsen OD, Niu ZP, Bock E, Baekkeskov S 1992 Differential expression of neural cell adhesion molecule and cadherins in pancreatic islets, glucagonomas, and insulinomas. Mol Endocrinol 6:1332-1342
62. Lise MF, El-Husseini A 2006 The neuroligin and neurexin families: from structure to function at the synapse. Cell Mol Life Sci 63:1833-1849
63. Watanabe RC, Chen W-M, Erdos MR, Saxena R, Jackson AU, Lyssenko V, Uda M, Buchanan TA, Schlessingor D, Groop L, Collins FS, Altshuler D, Abecasis G, Boehnke M, Scuteri A, Novel genetic loci for fasting glucose and insulin identified by genome-wide association in Caucasians. Proc 68th American Diabetes Association Annual Meeting, Philadelphia, PA, 2008 (Abstract 137-OR)
64. Sons MS, Busche N, Strenzke N, Moser T, Ernsberger U, Mooren FC, Zhang W, Ahmad M, Steffens H, Schomburg ED, Plomp JJ, Missler M 2006 α-Neurexins are required for efficient transmitter release and synaptic homeostasis at the mouse neuromuscular junction. Neuroscience 138:433-446
65. Bosco D, Orci L, Meda P 1989 Homologous but not heterologous contact increases the insulin secretion of individual pancreatic B-cells. Exp Cell Res 184:72-80
66. Hauge-Evans AC, Squires PE, Persaud SJ, Jones PM 1999 Pancreatic β-cell-to-α-cell interactions are required for integrated responses to nutrient stimuli: enhanced Ca2+ and insulin secretory responses of MIN6 pseudoislets. Diabetes 48:1402-1408
67. Luther MJ, Hauge-Evans A, Souza KL, Jorns A, Lenzen S, Persaud SJ, Jones PM 2006 MIN6 β-cell-β-cell interactions influence insulin secretory responses to nutrients and non-nutrients. Biochem Biophys Res Commun 343:99-104
68. ΔΔCT method. Methods 25:402-408
69. Hamaguchi K, Guskins HR, Leiter EH 1991 NIT-1, a pancreatic β-cell line established from a transgenic NOD/Lt mouse. Diabetes 40:842-849