Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells

Journal of Neuroscience

Volumn 32, Issue 18, 2012, Pages 6126-6137

  Omori, Yoshihiro ^a,b,c   Araki, Fumiyuki ^a,b,d   Chaya, Taro ^a,b   Kajimura, Naoko ^e   Irie, Shoichi ^a,b   Terada, Koji ^a   Muranishi, Yuki ^a,b   Tsujii, Toshinori ^a,b   Ueno, Shinji ^f   Koyasu, Toshiyuki ^f   Tamaki, Yasuhiro ^d   Kondo, Mineo ^g   Amano, Shiro ^d   Furukawa, Takahisa ^a,b  

^a OSAKA BIOSCIENCE INSTITUTE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c Precursory Research for Embryonic Science and Technology   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DYSTROGLYCAN; DYSTROPHIN; LAMININ; PROTEIN PIKACHURIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; B WAVE; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; ELECTRORETINOGRAM; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OLIGOMERIZATION; PHOTORECEPTOR; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RETINA BIPOLAR GANGLION CELL; SIGNAL TRANSDUCTION; SYNAPSE; WESTERN BLOTTING;

ANIMALS; CARRIER PROTEINS; DYSTROGLYCANS; FEMALE; MALE; MICE; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PHOTORECEPTOR CELLS, VERTEBRATE; PRESYNAPTIC TERMINALS; RETINAL BIPOLAR CELLS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84860335169     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0322-12.2012     Document Type: Article

References (46)

1. Beltran-Valero de Bernabe D, Currier S, Steinbrecher A, Celli J, van Beusekom E, van der Zwaag B, Kayserili H, Merlini L, Chitayat D, Dobyns WB, Cormand B, Lehesjoki AE, Cruces J, Voit T, Walsh CA, van Bok-hoven H, Brunner HG (2002) Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 71:1033-1043.
2. Blank M, Koulen P, Blake DJ, Kroger S (1999) Dystrophin and beta-dystroglycan in photoreceptor terminals from normal and mdx3Cv mouse retinae. EurJNeurosci 11:2121-2133.
3. Blank M, Blake DJ, Kroger S (2002) Molecular diversity of the dystrophin-like protein complex in the developing and adult avian retina. Neurosci-ence 111:259-273.
4. Blanks JC, Adinolfi AM, Lolley RN (1974) Synaptogenesis in the photoreceptor terminal of the mouse retina. J Comp Neurol 156:81-93.
5. Bogdanik L, Framery B, Frolich A, Franco B, Mornet D, Bockaert J, Sigrist SJ, Grau Y, Parmentier ML (2008) Muscle dystroglycan organizes the post-synapse and regulates presynaptic neurotransmitter release at the Dro-sophila neuromuscular junction. PLoS One 3:e2084.
6. Brockington M, Blake DJ, Prandini P, Brown SC, Torelli S, Benson MA, Ponting CP, Estournet B, Romero NB, Mercuri E, Voit T, Sewry CA, Guicheney P, Muntoni F (2001) Mutations in the fukutin related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin alpha2 deficiency and abnormal glycosylation of alpha-dystroglycan. Am J Hum Genet 69:1198-1209.
7. Carter-Dawson LD, LaVail MM (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245-262.
8. Chen S, Kadomatsu K, Kondo M, Toyama Y, Toshimori K, Ueno S, Miyake Y, Muramatsu T (2004) Effects of flanking genes on the phenotypes of mice deficient in basigin/CD147. Biochem Biophys Res Commun 324:147-153.
9. Cibis GW, Fitzgerald KM, Harris DJ, Rothberg PG, Rupani M (1993) The effects of dystrophin gene mutations on the ERG in mice and humans. Invest Ophthalmol Vis Sci 34:3646-3652.
10. D'Souza VN, Nguyen TM, Morris GE, Karges W, Pillers DA, Ray PN (1995) A novel dystrophin isoform is required for normal retinal electrophysiol-ogy. Hum Mol Genet 4:837-842.
11. Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122:809-823.
12. Fitzgerald KM, Cibis GW, Giambrone SA, Harris DJ (1994) Retinal signal transmission in Duchenne muscular dystrophy: evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. J Clin Invest 93:2425-2430.
13. Furukawa A, Koike C, Lippincott P, Cepko CL, Furukawa T (2002) The mouse Crx 5'-upstream transgene sequence directs cell-specific and developmentally regulated expression in retinal photoreceptor cells. J Neu-rosci 22:1640-1647.
14. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S (1994) Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
15. Haenggi T, Fritschy JM (2006) Role of dystrophin and utrophin for assembly and function of the dystrophin glycoprotein complex in non muscle tissue. Cell Mol Life Sci 63:1614-1631.
16. Henry MD, Campbell KP (1996) Dystroglycan: an extra cellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 8:625-631.
17. Hoffman EP, Kunkel LM (1989) Dystrophin abnormalities in Duchenne/ Becker muscular dystrophy. Neuron 2:1019-1029.
18. Hu H, Li J, Zhang Z, Yu M (2011) Pikachurin interaction with dystroglycan is diminished by defective O-mannosyl glycosylation in congenital muscular dystrophy models and rescued by LARGE overexpression. Neurosci Lett 489:10-15.
19. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
20. Jastrow H, Koulen P, Altrock WD, Kröger S (2006) Identification of a beta-dystroglycan immunoreactive subcompartment in photoreceptor terminals. Invest Ophthalmol Vis Sci 47:17-24.
21. Kanagawa M, Omori Y, Sato S, Kobayashi K, Miyagoe-Suzuki Y, Takeda S, Endo T, Furukawa T, Toda T (2010) Post-translational maturation of dystroglycan is necessary for pikachurin binding and ribbon synaptic localization. J Biol Chem 285:31208-31216.
22. Kobayashi K, Nakahori Y, Miyake M, Matsumura K, Kondo-Iida E, Nomura Y, Segawa M, Yoshioka M, Saito K, Osawa M, Hamano K, Sakakihara Y, Nonaka I, Nakagome Y, Kanazawa I, Nakamura Y, Tokunaga K, Toda T (1998) An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394:388-392.
23. Koike C, Obara T, Uriu Y, Numata T, Sanuki R, Miyata K, Koyasu T, Ueno S, Funabiki K, Tani A, Ueda H, Kondo M, Mori Y, Tachibana M, Furukawa T (2010) TRPM1 is a component of the retinal ON bipolar cell trans-duction channel in the mGluR6 cascade. Proc Natl Acad Sci U S A 107:332-337.
24. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76.
25. Lee Y, Kameya S, Cox GA, Hsu J, Hicks W, Maddatu TP, Smith RS, Naggert JK, Peachey NS, Nishina PM (2005) Ocular abnormalities in Large-(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol Cell Neurosci 30:160-172.
26. Liu J, Ball SL, Yang Y, Mei P, Zhang L, Shi H, Kaminski HJ, Lemmon VP, Hu H (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech Dev 123:228-240.
27. Longman C, Brockington M, Torelli S, Jimenez-Mallebrera C, Kennedy C, Khalil N, Feng L, Saran RK, Voit T, Merlini L, Sewry CA, Brown SC, Muntoni F (2003) Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Hum Mol Genet 12:2853-2861.
28. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, Hoshi T, Campbell KP (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418:422-425.
29. Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, Matsuo I, Furukawa T (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 6:1255-1263.
30. Peng HB, Ali AA, Daggett DF, Rauvala H, Hassell JR, Smalheiser NR (1998) The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes Commun 5:475-489.
31. Pillers DA, Bulman DE, Weleber RG, Sigesmund DA, Musarella MA, Powell BR, Murphey WH, Westall C, Panton C, Becker LE, Worton RG, Ray PN (1993) Dystrophin expression inthe human retinais required for normal function as defined by electroretinography. Nat Genet 4:82-86.
32. Pillers DA, Weleber RG, Woodward WR, Green DG, Chapman VM, Ray PN (1995) mdxCv3 mouse is a model for electroretinography of Duchenne/Becker muscular dystrophy. Invest Ophthalmol Vis Sci 36:462-466.
33. Robson JG, Frishman LJ (1995) Response linearity and kinetics of the cat retina: the bipolar cell component of the dark-adapted electroretinogram. Vis Neurosci 12:837-850.
34. Robson JG, Frishman LJ (1996) Photoreceptor and bipolar cell contributions to the cat electroretinogram: a kinetic model for the early part of the flash response. J Opt Soc Am A Opt Image Sci Vis 13:613-622.
35. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T (2008) Pikachurin, a dys-troglycan ligand,is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923-931.
36. Satz JS, Philp AR, Nguyen H, Kusano H, Lee J, Turk R, Riker MJ, Hernández J, Weiss RM, Anderson MG, Mullins RF, Moore SA, Stone EM, Campbell KP (2009) Visual impairment in the absence of dystroglycan. J Neurosci 29:13136-13146.
37. Schmitz F, Drenckhahn D (1997a) Localization of dystrophin and beta-dystroglycan inbovine retinal photoreceptor processes extending into the postsynaptic dendritic complex. Histochem Cell Biol 108:249-255.
38. Schmitz F, Drenckhahn D (1997b) Dystrophin in the retina. Prog Neuro-biol 53:547-560.
39. Sugita S, Saito F, Tang J, Satz J, Campbell K, Südhof TC (2001) A stoichio metric complex of neurexins and dystroglycan in brain. J Cell Biol 154:435-445.
40. Takaoka A, Hasegawa T, Yoshida K, Mori H (2008) Microscopic tomography with ultra-HVEM and applications. Ultramicroscopy 108:230-238.
41. tom Dieck S, Brandstätter JH (2006) Ribbon synapses of the retina. Cell Tissue Res 326:339-346.
42. Ueda H, Gohdo T, Ohno S (1998) Beta dystroglycan localization in the photoreceptor and Muller cells in the rat retina revealed by immuno electron microscopy. J Histochem Cytochem 46:185-191.
43. Ueda H, Baba T, Ohno S (2000) Current knowledge of dystrophin and dystrophin-associated proteins in the retina. Histol Histopathol 15:753-760.
44. van Reeuwijk J, Janssen M, van den Elzen C, Beltran-Valero de Bernabe ́ D, Sabatelli P, Merlini L, Boon M, Scheffer H, Brockington M, Muntoni F, Huynen MA, Verrips A, Walsh CA, Barth PG, Brunner HG, van Bokhoven H (2005) POMT2 mutations cause alpha dystroglycan hypoglycosylation and Walker-Warburg syndrome. J Med Genet 42:907-912.
45. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, Mizuno M, Inazu T, Mitsuhashi H, Takahashi S, Takeuchi M, Herrmann R, Straub V, Talim B, Voit T, Topaloglu H, Toda T, Endo T (2001) Muscular dystrophy and neuronal migration disorder caused by mutationsina glycosyltransferase, POMGnT1. Dev Cell 1:717-724.
46. Zelhof AC, Hardy RW, Becker A, Zuker CS (2006) Transforming the architecture of compound eyes. Nature 443:696-699.