Drosophila Nesprin-1 controls glutamate receptor density at neuromuscular junctions

Cellular and Molecular Life Sciences

Volumn 71, Issue 17, 2014, Pages 3363-3379

  Morel, Véronique ^a   Lepicard, Simon ^b,c   Rey, Alexandre N ^a   Parmentier, Marie Laure ^b,c   Schaeffer, Laurent ^a,d,e  

^a UNIVERSITÉ DE LYON   (France)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^c INSERM   (France)

^d UNIVERSITÉ LYON 1   (France)

^e HOSPICES CIVILS DE LYON   (France)

Author keywords

Drosophila; GluRIIA; Msp 300; Nesprin 1; Neuromuscular junction

Indexed keywords

ENVELOPE PROTEIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 2A; MUSCLE PROTEIN; MUSCLE SPECIFIC PROTEIN 300; NESPRIN 1; NUCLEAR PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHROPOD LARVA; ARTICLE; CELLULAR PARAMETERS; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; FEMALE; GENE DELETION; GENE SILENCING; KLARSICHT ANC 1 SYNE HOMOLOGY; LINKER OF NUCLEOSKELETON AND CYTOSKELETON; MALE; MYASTHENIA; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; POSTSYNAPTIC DENSITY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RECEPTOR DENSITY; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXCITATORY POSTSYNAPTIC POTENTIALS; LARVA; LOCOMOTION; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MYASTHENIA GRAVIS, AUTOIMMUNE, EXPERIMENTAL; NEUROMUSCULAR JUNCTION; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUTAMATE; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 84906276267     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1566-7     Document Type: Article

References (59)

1. Razafsky D, Zang S, Hodzic D (2011) unLINCing the nuclear envelope: towards an understanding of the physiological significance of nuclear positioning. Biochem Soc Trans 39:1790-1794
2. Starr DA (2009) A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122:577-586
3. Wang N, Tytell JD, Ingber DE (2009) mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10:75-82
4. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M (2007) Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134:901-908 (Pubitemid 46795681)
5. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M (2009) SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64:173-187
6. Gros-Louis F, Dupre N, Dion P, Fox MA, Laurent S, Verreault S, Sanes JR, Bouchard JP, Rouleau GA (2007) Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet 39:80-85 (Pubitemid 46026505)
7. Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, Ragnauth CD, Yi Q, Mellad JA, Warren DT et al (2007) Nesprin-1 and -2 are involved in the pathogenesis of Emery - Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet 16:2816-2833 (Pubitemid 350048381)
8. Emery AE (2000) Emery-Dreifuss muscular dystrophy - a 40-year retrospective. Neuromuscul Disord 10:228-232
9. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805 (Pubitemid 33674061)
10. Schaeffer L, de Kerchove d'Exaerde A, Changeux JP (2001) Targeting transcription to the neuromuscular synapse. Neuron 31:15-22 (Pubitemid 32757085)
11. Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M (2005) Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc Natl Acad Sci USA 102:4359-4364 (Pubitemid 40397116)
12. Puckelwartz MJ, Kessler E, Zhang Y, Hodzic D, Randles KN, Morris G, Earley JU, Hadhazy M, Holaska JM, Mewborn SK et al (2009) Disruption of nesprin-1 produces an Emery-Dreifuss muscular dystrophy-like phenotype in mice. Hum Mol Genet 18:607-620
13. Zhang J, Felder A, Liu Y, Guo LT, Lange S, Dalton ND, Gu Y, Peterson KL, Mizisin AP, Shelton GD et al (2010) Nesprin 1 is critical for nuclear positioning and anchorage. Hum Mol Genet 19:329-341
14. Volk T (1992) A new member of the spectrin superfamily may participate in the formation of embryonic muscle attachments in Drosophila. Development 116:721-730
15. Zhang Q, Ragnauth C, Greener MJ, Shanahan CM, Roberts RG (2002) The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 80:473-481 (Pubitemid 35333789)
16. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S et al (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156 (Pubitemid 47067374)
17. Rohrbough J, Pinto S, Mihalek RM, Tully T, Broadie K (1999) latheo, a Drosophila gene involved in learning, regulates functional synaptic plasticity. Neuron 23:55-70 (Pubitemid 29262464)
18. Feng Y, Ueda A, Wu CF (2004) A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet 18:377-402 (Pubitemid 40052750)
19. Marrus SB, Portman SL, Allen MJ, Moffat KG, DiAntonio A (2004) Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24:1406-1415 (Pubitemid 38222992)
20. Bolte S, Cordelieres FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232 (Pubitemid 46010930)
21. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2003-2007
22. Rosenberg-Hasson Y, Renert-Pasca M, Volk T (1996) A Drosophila dystrophin-related protein, MSP-300, is required for embryonic muscle morphogenesis. Mech Dev 60:83-94 (Pubitemid 27008251)
23. Apel ED, Lewis RM, Grady RM, Sanes JR (2000) Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J Biol Chem 275:31986-31995
24. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM (2001) Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci 114:4485-4498 (Pubitemid 34082869)
25. Zhang Q, Ragnauth CD, Skepper JN, Worth NF, Warren DT, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM (2005) Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci 118:673-687 (Pubitemid 40372577)
26. Xie X, Fischer JA (2008) On the roles of the Drosophila KASH domain proteins Msp-300 and Klarsicht. Fly 2:74-81
27. Starr DA, Han M (2002) Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298:406-409 (Pubitemid 35176347)
28. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415 (Pubitemid 23214028)
29. Kim K, Lee YS, Harris D, Nakahara K, Carthew RW (2006) The RNAi pathway initiated by Dicer-2 in Drosophila. Cold Spring Harb Symp Quant Biol 71:39-44
30. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19:1237-1248 (Pubitemid 28030543)
31. DiAntonio A, Petersen SA, Heckmann M, Goodman CS (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19:3023-3032 (Pubitemid 29173998)
32. Qin G, Schwarz T, Kittel RJ, Schmid A, Rasse TM, Kappei D, Ponimaskin E, Heckmann M, Sigrist SJ (2005) Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25:3209-3218 (Pubitemid 40463556)
33. Featherstone DE, Rushton E, Rohrbough J, Liebl F, Karr J, Sheng Q, Rodesch CK, Broadie K (2005) An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25:3199-3208 (Pubitemid 40463555)
34. Schuster CM, Ultsch A, Schloss P, Cox JA, Schmitt B, Betz H (1991) Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254:112-114 (Pubitemid 21917329)
35. Sigrist SJ, Reiff DF, Thiel PR, Steinert JR, Schuster CM (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23:6546-6556 (Pubitemid 36909881)
36. Chen K, Featherstone DE (2005) Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 3:1-13f
37. Cantera R, Kozlova T, Barillas-Mury C, Kafatos FC (1999) Muscle structure and innervation are affected by loss of Dorsal in the fruit fly, Drosophila melanogaster. Mol Cell Neurosci 13:131-141 (Pubitemid 29210463)
38. Heckscher ES, Fetter RD, Marek KW, Albin SD, Davis GW (2007) NF-kappaB, IkappaB, and IRAK control glutamate receptor density at the Drosophila NMJ. Neuron 55:859-873 (Pubitemid 47391188)
39. Elhanany-Tamir H, Yu YV, Shnayder M, Jain A, Welte M, Volk T (2012) Organelle positioning in muscles requires cooperation between two KASH proteins and microtubules. J Cell Biol 198:833-846
40. Metzger T, Gache V, Xu M, Cadot B, Folker ES, Richardson BE, Gomes ER, Baylies MK (2012) MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 484:120-124
41. Lei K, Zhang X, Ding X, Guo X, Chen M, Zhu B, Xu T, Zhuang Y, Xu R, Han M (2009) SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci USA 106:10207-10212
42. Jungbluth H, Wallgren-Pettersson C, Laporte J (2008) Centronuclear (myotubular) myopathy. Orphanet J Rare Dis 3:26
43. Chen K, Merino C, Sigrist SJ, Featherstone DE (2005) The 4.1 protein coracle mediates subunit-selective anchoring of Drosophila glutamate receptors to the postsynaptic actin cytoskeleton. J Neurosci 25:6667-6675 (Pubitemid 40995299)
44. Puckelwartz MJ, Kessler EJ, Kim G, Dewitt MM, Zhang Y, Earley JU, Depreux FF, Holaska J, Mewborn SK, Pytel P et al (2010) Nesprin-1 mutations in human and murine cardiomyopathy. J Mol Cell Cardiol 48:600-608
45. Bupp J, Martin AE, Stensrud ES, Jaspersen SL (2007) Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J Cell Biol 179:845-854 (Pubitemid 350223483)
46. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113:370-378 (Pubitemid 38544181)
47. Lammerding J, Hsiao J, Schulze PC, Kozlov S, Stewart CL, Lee RT (2005) Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J Cell Biol 170:781-791 (Pubitemid 41242110)
48. Brosig M, Ferralli J, Gelman L, Chiquet M, Chiquet-Ehrismann R (2010) Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int J Biochem Cell Biol 42:1717-1728
49. Mejat A, Decostre V, Li J, Renou L, Kesari A, Hantai D, Stewart CL, Xiao X, Hoffman E, Bonne G et al (2009) Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J Cell Biol 184:31-44
50. Qiu S, Li X-Y, Zhuo M (2011) Post-translational modification of NMDA receptor GluN2B subunit and its roles in chronic pain and memory. Sem Cell Dev Biol 22:521-529
51. Voeltz GK, Rolls MM, Rapoport TA (2002) Structural organization of the endoplasmic reticulum. EMBO Rep 3:944-950 (Pubitemid 35256468)
52. Pendin D, McNew JA, Daga A (2011) Balancing ER dynamics: shaping, bending, severing, and mending membranes. Curr Opin Cell Biol 23:435-442
53. Park SH, Blackstone C (2010) Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep 11:515-521
54. Frescas D, Mavrakis M, Lorenz H, Delotto R, Lippincott-Schwartz J (2006) The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol 173:219-230
55. Gough LL, Fan J, Chu S, Winnick S, Beck KA (2003) Golgi Localization of Syne-1. Mol Biol Cell 14:2410-2424 (Pubitemid 36724330)
56. Lu Z, Joseph D, Bugnard E, Zaal KJ, Ralston E (2001) Golgi complex reorganization during muscle differentiation: visualization in living cells and mechanism. Mol Biol Cell 12:795-808 (Pubitemid 33051979)
57. Beck KA (2005) Spectrins and the Golgi. Biochim Biophys Acta 1744:374-382
58. Dupre N, Gros-Louis F, Chrestian N, Verreault S, Brunet D, de Verteuil D, Brais B, Bouchard JP, Rouleau GA (2007) Clinical and genetic study of autosomal recessive cerebellar ataxia type 1. Ann Neurol 62:93-98 (Pubitemid 47235284)
59. Attali R, Warwar N, Israel A, Gurt I, McNally E, Puckelwartz M, Glick B, Nevo Y, Ben-Neriah Z, Melki J (2009) Mutation of SYNE-1, encoding an essential component of the nuclear lamina, is responsible for autosomal recessive arthrogryposis. Hum Mol Genet 18:3462-3469