Dscam promotes refinement in the mouse retina through cell death and restriction of exploring dendrites

Journal of Neuroscience

Volumn 35, Issue 14, 2015, Pages 5640-5654

  Li, Shuai ^a   Sukeena, Joshua M ^a   Simmons, Aaron B ^a   Hansen, Ethan J ^a   Nuhn, Renee E ^a,d   Samuels, Ivy S ^b,c   Fuerst, Peter G ^a,d  

^a UNIVERSITY OF IDAHO   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d NONE   (United States)

Author keywords

Apoptosis; Bax; Dendrite; ERG; Mosaic; Physiology

Indexed keywords

CELL ADHESION MOLECULE; DOWN SYNDROME CELL ADHESION MOLECULE; PROTEIN BAX; UNCLASSIFIED DRUG; BAX PROTEIN, MOUSE; DSCAM PROTEIN, MOUSE; EYE PROTEIN; HOMEODOMAIN PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; PHOTOPROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL CULTURE; CELL DEATH; CELL DENSITY; CONTROLLED STUDY; DENDRITE; DROSOPHILA; ELECTRON MICROSCOPY; GAIN OF FUNCTION MUTATION; GENE OVEREXPRESSION; GENOTYPE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; WESTERN BLOTTING; ANIMAL; CYTOLOGY; ELECTRORETINOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MACROGLIA; METABOLISM; MUTATION; NERVE CELL; NERVE CELL NETWORK; NEWBORN; PHYSIOLOGY; RETINA AMACRINE CELL; TRANSGENIC MOUSE; ULTRASTRUCTURE; VISUAL SYSTEM;

AMACRINE CELLS; ANIMALS; ANIMALS, NEWBORN; BCL-2-ASSOCIATED X PROTEIN; CELL ADHESION MOLECULES; CELL DEATH; CELLS, CULTURED; DENDRITES; ELECTRORETINOGRAPHY; EPENDYMOGLIAL CELLS; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MUTATION; NERVE NET; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; RETINA; VISUAL PATHWAYS;

EID: 84929347195     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2202-14.2015     Document Type: Article

References (77)

1. Alves-Sampaio A, Troca-Marín JA, Montesinos ML (2010) NMDAmediated regulation of DSCAM dendritic local translation is lost in a mouse model of Down’s syndrome. J Neurosci 30:13537–13548.
2. Amano K, Fujii M, Arata S, Tojima T, Ogawa M, Morita N, Shimohata A, Furuichi T, Itohara S, Kamiguchi H, Korenberg JR, Arata A, Yamakawa K (2009) DSCAM deficiency causes loss of pre-inspiratory neuron synchroneity and perinatal death. J Neurosci 29:2984–2996.
3. Aylward EH, Habbak R, Warren AC, Pulsifer MB, Barta PE, Jerram M, Pearlson GD (1997) Cerebellar volume in adults with Down syndrome. Arch Neurol 54:209–212.
4. Blank M, Fuerst PG, Stevens B, Nouri N, Kirkby L, Warrier D, Barres BA, Feller MB, Huberman AD, Burgess RW, Garner CC (2011) The Down syndrome critical region regulates retinogeniculate refinement. J Neurosci 31:5764–5776.
5. Bruggen B, Meyer A, Boven F, Weiler R, Dedek K (2014) Type 2 wide-field amacrine cells in TH::GFP mice show a homogenous synapse distribution and contact small ganglion cells. Eur J Neurosci. Advanced online publication. doi: 10.1111/ejn.12813.
6. Chen BE, Kondo M, Garnier A, Watson FL, Püettmann-Holgado R, Lamar DR, Schmucker D (2006) The molecular diversity of Dscam is functionally required for neuronal wiring specificity in Drosophila. Cell 125:607– 620.
7. Chen SK, Chew KS, McNeill DS, Keeley PW, Ecker JL, Mao BQ, Pahlberg J, Kim B, Lee SC, Fox MA, Guido W, Wong KY, Sampath AP, Reese BE, Kuruvilla R, Hattar S (2013) Apoptosis regulates ipRGC spacing necessary for rods and cones to drive circadian photoentrainment. Neuron 77:503–515.
8. Claes E, Seeliger M, Michalakis S, Biel M, Humphries P, Haverkamp S (2004) Morphological characterizationoftheretinaoftheCNGA3(/)Rho(/)mutant mouse lacking functional cones and rods. Invest Ophthalmol Vis Sci 45:2039– 2048.
9. Creavin AL, Brown RD (2009) Ophthalmic abnormalities in children with Down syndrome. J Pediatr Ophthalmol Strabismus 46:76–82.
10. Cvetkovska V, Hibbert AD, Emran F, Chen BE (2013) Overexpression of Down syndrome cell adhesion molecule impairs precise synaptic targeting. Nat Neurosci 16:677–682.
11. de Andrade GB, Long SS, Fleming H, Li W, Fuerst PG (2014) DSCAM localization and function at the mouse cone synapse. J Comp Neurol 522: 2609–2633.
12. Duan X, Krishnaswamy A, De la Huerta I, Sanes JR (2014) Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158:793–807.
13. Fuerst PG, Koizumi A, Masland RH, Burgess RW (2008) Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451:470–474.
14. Fuerst PG, Bruce F, Tian M, Wei W, Elstrott J, Feller MB, Erskine L, Singer JH, Burgess RW (2009) DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64:484– 497.
15. Fuerst PG, Harris BS, Johnson KR, Burgess RW (2010) A novel null allele of mouse DSCAM survives to adulthood on an inbred C3H background with reduced phenotypic variability. Genesis 48:578–584.
16. Fuerst PG, Bruce F, Rounds RP, Erskine L, Burgess RW (2012) Cell autonomy of DSCAM function in retinal development. Dev Biol 361:326–337.
17. Grossman TR, Gamliel A, Wessells RJ, Taghli-Lamallem O, Jepsen K, Ocorr K, Korenberg JR, Peterson KL, Rosenfeld MG, Bodmer R, Bier E (2011) Over-expression of DSCAM and COL6A2 cooperatively generates congenital heart defects. PLoS Genet 7:e1002344.
18. Hahn P, Lindsten T, Ying GS, Bennett J, Milam AH, Thompson CB, Dunaief JL (2003) Proapoptotic bcl-2 family members, Bax and Bak, are essential for developmental photoreceptor apoptosis. Invest Ophthalmol Vis Sci 44:3598–3605.
19. Hattori D, Demir E, Kim HW, Viragh E, Zipursky SL, Dickson BJ (2007) Dscam diversity is essential for neuronal wiring and self-recognition. Nature 449:223–227.
20. Haydar TF, Reeves RH (2012) Trisomy 21 and early brain development. Trends Neurosci 35:81–91.
21. He H, Kise Y, Izadifar A, Urwyler O, Ayaz D, Parthasarthy A, Yan B, Erfurth ML, Dascenco D, Schmucker D (2014) Cell-intrinsic requirement of Dscam1 isoform diversity for axon collateral formation. Science 344: 1182–1186.
22. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen K, Sun Y, Carlson E, Alleva E, Epstein CJ, Mobley WC (1996) Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci U S A 93:13333–13338.
23. Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO (2009) Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12:35–43.
24. Hughes ME, Bortnick R, Tsubouchi A, Bäumer P, Kondo M, Uemura T, Schmucker D (2007) Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417–427.
25. Hutchinson KM, Vonhoff F, Duch C (2014) Dscam1 is required for normal dendrite growth and branching but not for dendritic spacing in Drosophila motoneurons. J Neurosci 34:1924–1931.
26. Kay JN, Chu MW, Sanes JR (2012) MEGF10 and MEGF11 mediate homotypic interactions required for mosaic spacing of retinal neurons. Nature 483:465–469.
27. Keeley PW, Reese BE (2010) Morphology of dopaminergic amacrine cells in the mouse retina: independence from homotypic interactions. J Comp Neurol 518:1220–1231.
28. Keeley PW, Sliff BJ, Lee SC, Fuerst PG, Burgess RW, Eglen SJ, Reese BE (2012) Neuronal clustering and fasciculation phenotype in Dscam- and Bax-deficient mouse retinas. J Comp Neurol 520:1349–1364.
29. Khiripet N, Khantuwan W, Jungck JR (2012) Ka-me: a Voronoi image analyzer. Bioinformatics 28:1802–1804.
30. Kim JH, Wang X, Coolon R, Ye B (2013) Dscam expression levels determine presynaptic arbor sizes in Drosophila sensory neurons. Neuron 78:827– 838.
31. Knop GC, Feigenspan A, Weiler R, Dedek K (2011) Inputs underlying the ON-OFF light responses of type 2 wide-field amacrine cells in TH::GFP mice. J Neurosci 31:4780–4791.
32. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96–99.
33. Kunzevitzky NJ, Willeford KT, Feuer WJ, Almeida MV, Goldberg JL (2013) Amacrine cell subtypes differ in their intrinsic neurite growth capacity. Invest Ophthalmol Vis Sci 54:7603–7613.
34. Laguna A, Barallobre MJ, Marchena MÁ, Mateus C, Ramírez E, Martínez Cue C, Delabar JM, Castelo-Branco M, de la Villa P, Arbonés ML (2013) Triplication of DYRK1A causes retinal structural and functional alterations in Down syndrome. Hum Mol Genet 22:2775–2784.
35. Lefebvre JL, Zhang Y, Meister M, Wang X, Sanes JR (2008) gamma Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135:4141–4151.
36. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR (2012) Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488:517–521.
37. Lejeune J, Turpin R, Gautier M (1959) [Chromosomic diagnosis of mongolism]. Arch Fr Pediatr 16:962–963.
38. Li HL, Huang BS, Vishwasrao H, Sutedja N, Chen W, Jin I, Hawkins RD, Bailey CH, Kandel ER (2009) Dscam mediates remodeling of glutamate receptors in Aplysia during de novo and learning-related synapse formation. Neuron 61:527–540.
39. Liets LC, Eliasieh K, van der List DA, Chalupa LM (2006) Dendrites of rod bipolar cells sprout in normal aging retina. Proc Natl Acad Sci U S A 103:12156–12160.
40. Liu G, Li W, Wang L, Kar A, Guan KL, Rao Y, Wu JY (2009) DSCAMfunctions as a netrin receptor in commissural axon pathfinding. Proc Natl Acad Sci U S A 106:2951–2956.
41. Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:56–62.
42. Ly A, Nikolaev A, Suresh G, Zheng Y, Tessier-Lavigne M, Stein E (2008) DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 133:1241–1254.
43. Masland RH (2012) The neuronal organization of the retina. Neuron 76: 266–280.
44. Matsuda T, Cepko CL (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 101:16–22.
45. Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chédotal A, Kolodkin AL (2011a) Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470:259–263.
46. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H, Katayama K, Kumar SR, Suto F, Chédotal A, Peachey NS, Nathans J, Yoshida Y, Giger RJ, Kolodkin AL (2011b) Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 71:460– 473.
47. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO, Peachey NS, Chédotal A, Yau KW, Kolodkin AL (2012) Guidance-cue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. J Neurosci 32:6859–6868.
48. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC, Zipursky SL, Grueber WB (2007) Dendrite self-avoidance is controlled by Dscam. Cell 129:593–604.
49. Maynard KR, Stein E (2012) DSCAM contributes to dendrite arborization and spine formation in the developing cerebral cortex. J Neurosci 32: 16637–16650.
50. Michalakis S, Schäferhoff K, Spiwoks-Becker I, Zabouri N, Koch S, Koch F, Bonin M, Biel M, Haverkamp S (2013) Characterization of neurite outgrowth and ectopic synaptogenesis in response to photoreceptor dysfunction. Cell Mol Life Sci 70:1831–1847.
51. Millard SS, Lu Z, Zipursky SL, Meinertzhagen IA (2010) Drosophila dscam proteins regulate postsynaptic specificity at multiple-contact synapses. Neuron 67:761–768.
52. Miyazaki J, Takaki S, Araki K, Tashiro F, Tominaga A, Takatsu K, Yamamura K (1989) Expression vector system based on the chicken beta-actin promoter directs efficient production of interleukin-5. Gene 79:269–277.
53. Morales Diaz HD (2014) Down syndrome cell adhesion molecule is important for early development in Xenopus tropicalis. Genesis 52:849–857.
54. Neves G, Zucker J, Daly M, Chess A (2004) Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat Genet 36:240– 246.
55. Okawa H, Hoon M, Yoshimatsu T, Della Santina L, Wong RO (2014) Illuminating the multifaceted roles of neurotransmission in shaping neuronal circuitry. Neuron 83:1303–1318.
56. Péquignot MO, Provost AC, Sallé S, Taupin P, Sainton KM, Marchant D, Martinou JC, Ameisen JC, Jais JP, Abitbol M (2003) Major role of BAX in apoptosis during retinal development and in establishment of a functional postnatal retina. Dev Dyn 228:231–238.
57. Purohit AA, Li W, Qu C, Dwyer T, Shao Q, Guan KL, Liu G (2012) Down syndrome cell adhesion molecule (DSCAM) associates with uncoordinated-5C (UNC5C) in netrin-1-mediated growth cone collapse. J Biol Chem 287:27126–27138.
58. Rahmani Z, Blouin JL, Créau-Goldberg N, Watkins PC, Mattei JF, Poissonnier M, Prieur M, Chettouh Z, Nicole A, Aurias A, et al. (1990) Down syndrome critical region around D21S55 on proximal 21q22.3. Am J Med Genet Suppl 7:98–103.
59. Ramon y Cajal S (1893) La retine des vertebres. La Cellule 9:119–257.
60. Randlett O, MacDonald RB, Yoshimatsu T, Almeida AD, Suzuki SC, Wong RO, Harris WA (2013) Cellular requirements for building a retinal neuropil. Cell Rep 3:282–290.
61. Reese BE, Keeley PW (2014) Design principles and developmental mechanisms underlying retinal mosaics. Biol Rev Camb Philos Soc. Advanced online publication. doi: 10.1111/brv.12139.
62. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, Schmidt C, Bronson RT, Davisson MT (1995) A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 11:177–184.
63. Rodieck RW (1991) The density recovery profile: a method for the analysis of points in the plane applicable to retinal studies. Vis Neurosci 6:95–111.
64. Samuel MA, Zhang Y, Meister M, Sanes JR (2011) Age-related alterations in neurons of the mouse retina. J Neurosci 31:16033–16044.
65. Samuel MA, Voinescu PE, Lilley BN, de Cabo R, Foretz M, Viollet B, Pawlyk B, Sandberg MA, Vavvas DG, Sanes JR (2014) LKB1 and AMPK regulate synaptic remodeling in old age. Nat Neurosci 17:1190–1197.
66. Schmucker D, Chen B (2009) Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev 23:147–156.
67. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–684.
68. Schramm RD, Li S, Harris BS, Rounds RP, Burgess RW, Ytreberg FM, Fuerst PG (2012) A novel mouse Dscam mutation inhibits localization and shedding of DSCAM. PLoS One 7:e52652.
69. Soba P, Zhu S, Emoto K, Younger S, Yang SJ, Yu HH, Lee T, Jan LY, Jan YN (2007) Drosophila sensory neurons require Dscam for dendritic selfavoidance and proper dendritic field organization. Neuron 54:403–416.
70. Stacy RC, Demas J, Burgess RW, Sanes JR, Wong RO (2005) Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci 25:9347–9357.
71. Sun LO, Jiang Z, Rivlin-Etzion M, Hand R, Brady CM, Matsuoka RL, Yau KW, Feller MB, Kolodkin AL (2013) On and off retinal circuit assembly by divergent molecular mechanisms. Science 342:1241974.
72. Yamagata M, Sanes JR (2008) Dscam and Sidekick proteins direct laminaspecific synaptic connections in vertebrate retina. Nature 451:465–469.
73. Yamagata M, Sanes JR (2010) Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins. J Neurosci 30: 3579–3588.
74. Yamagata M, Sanes JR (2012) Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J Neurosci 32:14402–14414.
75. Yamakawa K, Huot YK, Haendelt MA, Hubert R, Chen XN, Lyons GE, Korenberg JR (1998) DSCAM: a novel member of the immunoglobulin superfamily maps in a Down syndrome region and is involved in the development of the nervous system. Hum Mol Genet 7:227–237.
76. Yimlamai D, Konnikova L, Moss LG, Jay DG (2005) The zebrafish down syndrome cell adhesion molecule is involved in cell movement during embryogenesis. Dev Biol 279:44–57.
77. Zhu H, Hummel T, Clemens JC, Berdnik D, Zipursky SL, Luo L (2006) Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat Neurosci 9:349–355.