Protocadherin-dependent dendritic selfavoidance regulates neural connectivity and circuit function

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Kostadinov, Dimitar ^a,b   Sanes, Joshua R ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CADHERIN; CHOLINE ACETYLTRANSFERASE; GAMMA PROTOCADHERIN; PROTOCADHERIN; UNCLASSIFIED DRUG; GAMMA-PROTOCADHERINS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; ELECTROPHYSIOLOGY; HISTOLOGY; IMMUNOFLUORESCENCE TEST; INFORMATION PROCESSING; MOUSE; NERVE CELL NETWORK; NERVOUS SYSTEM FUNCTION; NEURITE; NONHUMAN; PHOTORECEPTOR; PRESYNAPTIC POTENTIAL; RETINA AMACRINE CELL; RETINA GANGLION CELL; STIMULUS RESPONSE; SYNAPSE; SYNAPTIC POTENTIAL; VISUAL STIMULATION; ANIMAL; C57BL MOUSE; DENDRITE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

AMACRINE CELLS; ANIMALS; CADHERINS; DENDRITES; MICE, INBRED C57BL;

EID: 84940563410     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08964     Document Type: Article

References (90)

1. Ackman JB, Crair MC. 2014. Role of emergent neural activity in visual map development. Current Opinion in Neurobiology 24:166-175. doi: 10.1016/j.conb.2013.11.011.
2. Bacci A, Huguenard JR, Prince DA. 2003. Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex. The Journal of Neuroscience 23:859-866.
3. Baker MW, Macagno ER. 2000. The role of a LAR-like receptor tyrosine phosphatase in growth cone collapse and mutual-avoidance by sibling processes. Journal of Neurobiology 44:194-203. doi: 10.1002/1097-4695(200008) 44:2<194::AID-NEU9>3.0.CO;2-J.
4. Barlow HB, Hill RM. 1963. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139:412-414. doi: 10.1126/science.139.3553.412.
5. Bekkers JM, Stevens CF. 1991. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proceedings of the National Academy of Sciences of USA 88:7834-7838. doi: 10.1073/ pnas.88.17.7834.
6. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183-188. doi: 10.1038/nature09818.
7. Buffelli M, Burgess RW, Feng G, Lobe CG, Lichtman JW, Sanes JR. 2003. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424:430-434. doi: 10.1038/nature01844.
8. Burbridge TJ, Xu HP, Ackman JB, Ge X, Zhang Y, Ye MJ, Zhou ZJ, Xu J, Contractor A, Crair MC. 2014. Visual circuit development requires patterned activity mediated by retinal acetylcholine receptors. Neuron 84:1049-1064. doi: 10.1016/j.neuron.2014.10.051.
9. Chan YC, Chiao CC. 2013. The distribution of the preferred directions of the ON-OFF direction selective ganglion cells in the rabbit retina requires refinement after eye opening. Physiological Reports 1:e00013. doi: 10.1002/ phy2.13.
10. Chen H, Liu X, Tian N. 2014. Subtype-dependent postnatal development of direction-and orientation-selective retinal ganglion cells in mice. Journal of Neurophysiology 112:2092-2101. doi: 10.1152/jn.00320.2014.
11. Crepel F, Mariani J, Delhaye-Bouchard N. 1976. Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. Journal of Neurobiology 7:567-578. doi: 10.1002/neu.480070609.
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. doi: 10.1016/j.cell.2014.06.047.
13. Elstrott J, Anishchenko A, Greschner M, Sher A, Litke AM, Chichilnisky EJ, Feller MB. 2008. Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron 58:499-506. doi: 10.1016/j.neuron.2008.03.013.
14. Enciso GA, Rempe M, Dmitriev AV, Gavrikov KE, Terman D, Mangel SC. 2010. A model of direction selectivity in the starburst amacrine cell network. Journal of Computational Neuroscience 28:567-578. doi: 10.1007/s10827-010-0238-3.
15. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845-852. doi: 10.1038/nature00931.
16. Famiglietti EV. 1983. 'Starburst' amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261:138-144. doi: 10.1016/0006-8993(83)91293-3.
17. Ford KJ, Felix AL, Feller MB. 2012. Cellular mechanisms underlying spatiotemporal features of cholinergic retinal waves. The Journal of Neuroscience 32:850-863. doi: 10.1523/JNEUROSCI.5309-12.2012.
18. Fried SI, Munch TA, Werblin FS. 2002. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420:411-414. doi: 10.1038/nature01179.
19. 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. doi: 10.1016/j.neuron.2009.09.027.
20. Fuerst PG, Koizumi A, Masland RH, Burgess RW. 2008. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451:470-474. doi: 10.1038/nature06514.
21. Gao F-B, Kohwi M, Brenman JE, Jan LY, Jan YN. 2000. Control of dendritic formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 28:91-101. doi: 10.1016/S0896-6273(00) 00088-X.
22. Garrett AM, Schreiner D, Lobas MA, Weiner JA. 2012. γ-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 74:269-276. doi: 10.1016/j.neuron. 2012.01.028.
23. Gibson DA, Tymanskyj S, Yuan RC, Leung HC, Lefebvre JL, Sanes JR, Chedotal A, Ma L. 2014. Dendrite selfavoidance requires cell-autonomous slit/robo signaling in cerebellar purkinje cells. Neuron 81:1040-1056. doi: 10.1016/j.neuron.2014.01.009.
24. Grueber WB, Graubard K, Truman JW. 2001. Tiling of the body wall by multidendritic sensory neurons in Manduca sexta. The Journal of Comparative Neurology 440:271-283. doi: 10.1002/cne.1385.
25. Grueber WB, Sagasti A. 2010. Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harbor Perspectives in Biology 2:a001750. doi: 10.1101/cshperspect.a001750.
26. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN. 2003. Dendrites of distinct classes of Drosophila sensory neurons show different capacities of homotypic repulsion. Current Biology 13:618-626. doi: 10.1016/S0960-9822(03)00207-0.
27. Hattori D, Chen Y, Matthews BJ, Salwinski L, Sabatti C, Grueber WB, Zipursky SL. 2009. Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms. Nature 461:644-648. doi: 10.1038/ nature08431.
28. 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. doi: 10.1038/nature06099.
29. Hayden SA, Mills JW, Masland RH. 1980. Acetylcholine synthesis by displaced amacrine cells. Science 210: 435-437. doi: 10.1126/science.7433984.
30. Helmstaedter M, Briggman KL, Turaga SC, Jain V, Seung HS, Denk W. 2013. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500:168-174. doi: 10.1038/nature12346.
31. Hoggarth A, McLaughlin AJ, Ronellenfitch K, Trenholm S, Vasandani R, Sethuramanujam S, Schwab D, Briggman KL, Awatramani GB. 2015. Specific wiring of distinct amacrine cells in the directionally selective retinal circuit permit independent encoding of direction and size. Neuron 86:1-16. doi: 10.1016/j.neuron.2015.02.035.
32. Hughes ME, Bortnick R, Tsubouchi A, Baumer P, Kondo M, Uemura T, Schmucker D. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417-427. doi: 10.1016/j.neuron.2007.04.013.
33. Kaneko R, Kato H, Kawamura Y, Esumi S, Hirayama T, Hirabayashi T, Yagi T. 2006. Allelic gene regulation of Pcdhalpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. The Journal of Biological Chemistry 281:30551-30560. doi: 10.1074/jbc.M605677200.
34. Kano M, Hashimoto K. 2009. Synapse elimination in the central nervous system. Current Opinion in Neurobiology 19:154-161. doi: 10.1016/j.conb.2009.05.002.
35. Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, Chu MW, Meister M, Sanes JR. 2011. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. The Journal of Neuroscience 31:7753-7762. doi: 10.1523/JNEUROSCI.0907-11.2011.
36. Kim IJ, Zhang Y, Meister M, Sanes JR. 2010. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. The Journal of Neuroscience 30: 1452-1462. doi: 10.1523/JNEUROSCI.4779-09.2010.
37. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. 2008. Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478-482. doi: 10.1038/nature06739.
38. Kramer AP, Kuwada JY. 1983. Formation of receptive fields of leech mechanosensory neurons during embryonic development. The Journal of Neuroscience 3:2474-2486.
39. Kramer AP, Stent GS. 1985. Developmental arborization of sensory neurons in the leech Haementeria ghilianii. II. Experimentally induced variations in the branching pattern. The Journal of Neuroscience 5:768-775.
40. Lee S, Zhou ZJ. 2006. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51:787-799. doi: 10.1016/j.neuron.2006.08.007.
41. 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. doi: 10.1038/nature11305.
42. Lefebvre JL, Sanes JR, Kay JN. 2015. Development of dendritic form and function. Annual Review of Cell and Developmental Biology 31:(in press).
43. 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. doi: 10.1242/dev.027912.
44. Liu Y, Halloran MC. 2005. Central and peripheral axon branches from one neuron are guided differentially by Semaphorin3D and transient axonal glycoprotein-1. The Journal of Neuroscience 25:10556-10563. doi: 10.1523/ JNEUROSCI.2710-05.2005.
45. Long H, Ou Y, Rao Y, van Meyel DJ. 2009. Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila. Development 136:3475-3484. doi: 10.1242/dev.040220.
46. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience 13:133-140. doi: 10.1038/nn.2467.
47. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO, Peachey NS, Chedotal A, Yau KW, Kolodkin AL. 2012. Guidance-cue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. The Journal of Neuroscience 32:6859-6868. doi: 10.1523/JNEUROSCI.0267-12.2012.
48. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC, Zipursky SL, Grueber WB. 2007. Dendrite selfavoidance is controlled by Dscam. Cell 129:593-604. doi: 10.1016/j.cell.2007.04.013.
49. Miura SK, Martins A, Zhang KX, Graveley BR, Zipursky SL. 2013. Probabilistic splicing of Dscam1 establishes identity at the level of single neurons. Cell 155:1166-1177. doi: 10.1016/j.cell.2013.10.018.
50. Montague PR, Friedlander MJ. 1991. Morphogenesis and territorial coverage by isolated mammalian retinal ganglion cells. The Journal of Neuroscience 11:1440-1457.
51. Murata Y, Hamada S, Morishita H, Mutoh T, Yagi T. 2004. Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha. The Journal of Biological Chemistry 279:49508-49516. doi: 10.1074/ jbc.M408771200.
52. Murthy VN. 2011. Olfactory maps in the brain. Annual Review of Neuroscience 34:233-258. doi: 10.1146/annurevneuro-061010-113738.
53. Neves G, Zucker J, Daly M, Chess A. 2004. Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nature Genetics 36:240-246. doi: 10.1038/ng1299.
54. Nicholls JG, Baylor DA. 1968. Specific modalities and receptive fields of sensory neurons in the CNS of the leech. Journal of Neurophysiology 31:740-756.
55. Oyster CW, Barlow HB. 1967. Direction-selective units in rabbit retina: distribution of preferred directions. Science 155:841-842. doi: 10.1126/science.155.3764.841.
56. Park SJ, Kim IJ, Looger LL, Demb JB, Borghuis BG. 2014. Excitatory synaptic inputs to mouse on-off directionselective retinal ganglion cells lack direction tuning. The Journal of Neuroscience 34:3976-3981. doi: 10.1523/ JNEUROSCI.5017-13.2014.
57. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M. 2013. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nature Neuroscience 16:1068-1076. doi: 10.1038/nn. 3446.
58. Prasad T, Wang X, Gray PA, Weiner JA. 2008. A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: insights from genetic analyses of the protocadherin-gamma gene cluster. Development 135:4153-4164. doi: 10.1242/dev.026807.
59. Purves D, Lichtman JW. 1980. Elimination of synapses in the developing nervous system. Science 210:153-157. doi: 10.1126/science.7414326.
60. Redfern PA. 1970. Neuromuscular transmission in new-born rats. The Journal of Physiology 209:701-709. doi: 10. 1113/jphysiol.1970.sp009187.
61. Rieubland S, Roth A, Hausser M. 2014. Structured connectivity in cerebellar inhibitory networks. Neuron 81: 913-929. doi: 10.1016/j.neuron.2013.12.029.
62. Rossi J, Balthasar N, Olson D, Scott M, Berglund E, Lee CE, Choi MJ, Lauzon D, Lowell BB, Elmquist JK. 2011. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metabolism 13:195-204. doi: 10.1016/j.cmet.2011.01.010.
63. Sagasti A, Guido MR, Raible DW, Schier AF. 2005. Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Current Biology 15:804-814. doi: 10.1016/j.cub.2005. 03.048.
64. Schmucker D, Clemens JE, Shu H, Worby CA, Xiao J, Zipursky SL. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671-684. doi: 10.1016/S0092-8674(00)80878-8.
65. Schreiner D, Weiner JA. 2010. Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proceedings of the National Academy of Sciences of USA 107:14893-14898. doi: 10.1073/pnas.1004526107.
66. Smith CJ, Watson JD, VanHoven MK, Colon-Ramos DA, Miller DM III. 2012. Netrin (UNC-6) mediates dendritic self-avoidance. Nature Neuroscience 15:731-737. doi: 10.1038/nn.3065.
67. 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 self-avoidance and proper dendritic field organization. Neuron 54:403-416. doi: 10. 1016/j.neuron.2007.03.029.
68. 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. doi: 10.1126/science. 1241974.
69. Tasic B, Nabholz CE, Baldwin KK, Kim Y, Rueckert EH, Ribich SA, Cramer P, Wu Q, Axel R, Maniatis T. 2002. Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Molecular Cell 10:21-33. doi: 10.1016/S1097-2765(02)00578-6.
70. Taylor WR, Smith RG. 2012. The role of starburst amacrine cells in visual signal processing. Visual Neuroscience 29: 73-81. doi: 10.1017/S0952523811000393.
71. Taylor WR, Vaney DI. 2002. Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. The Journal of Neuroscience 22:7712-7720.
72. Taylor WR, Wassle H. 1995. Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7:2308-2321. doi: 10.1111/j.1460-9568.1995.tb00652.x.
73. Thu CA, Chen WV, Rubinstein R, Chevee M, Wolcott HN, Felsovalyi KO, Tapia JC, Shapiro L, Honig B, Maniatis T. 2014. Single-cell identity generated by combinatorial homophilic interactions between alpha, beta, and gamma protocadherins. Cell 158:1045-1059. doi: 10.1016/j.cell.2014.07.012.
74. Toyoda S, Kawaguchi M, Kobayashi T, Tarusawa E, Toyama T, Okano M, Oda M, Nakauchi H, Yoshimura Y, Sanbo M, Hirabayashi M, Hirayama T, Hirabayashi T, Yagi T. 2014. Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity. Neuron 82:94-108. doi: 10.1016/j.neuron.2014.02.005.
75. Trenholm S, Johnson K, Li X, Smith RG, Awatramani GB. 2011. Parallel mechanisms encode direction in the retina. Neuron 71:683-694. doi: 10.1016/j.neuron.2011.06.020.
76. Vaney DI, Sivyer B, Taylor WR. 2012. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nature Reviews. Neuroscience 13:194-208. doi: 10.1038/nrn3165.
77. Wang J, Zugates CT, Liang IH, Lee C-HJ, Lee T. 2002a. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33:559-571. doi: 10.1016/S0896-6273(02) 00570-6.
78. Wang X, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR. 2002b. Gamma Protocadherins are required for survival of spinal interneurons. Neuron 36:843-854. doi: 10.1016/S0896-6273(02)01090-5.
79. Wassle H, Puller C, Muller F, Haverkamp S. 2009. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. The Journal of Neuroscience 29:106-117. doi: 10.1523/JNEUROSCI.4442-08.2009.
80. Weiner JA, Wang X, Tapia JC, Sanes JR. 2005. Gamma protocadherins are required for synaptic development in the spinal cord. Proceedings of the National Academy of Sciences of USA 102:8-14. doi: 10.1073/pnas. 0407931101.
81. Wichterle H, Lieberam I, Porter JA, Jessell TM. 2002. Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397. doi: 10.1016/S0092-8674(02)00835-8.
82. Wojtowicz WM, Flanagan JJ, Millard SS, Zipursky SL, Clemens JC. 2004. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118:619-633. doi: 10. 1016/j.cell.2004.08.021.
83. Wojtowicz WM, Wu W, Andre I, Qian B, Baker D, Zipursky SL. 2007. A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130:1134-1145. doi: 10.1016/j.cell. 2007.08.026.
84. Yau K-W. 1976. Receptive fields, geometry and conduction block of sensory neurones in the central nervous system of the leech. The Journal of Physiology 263:513-538. doi: 10.1113/jphysiol.1976.sp011643.
85. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B. 2011. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469:407-410. doi: 10.1038/nature09711.
86. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K, Teixeira M, Juttner J, Noda M, Neve RL, Conzelmann KK, Roska B. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79:1078-1085. doi: 10.1016/j.neuron.2013.08.005.
87. Yoshida K, Watanabe D, Ishikane K, Tachibana M, Pastan I, Nakanishi S. 2001. A key role of starburst amacrine cells in originating retina directional selectivity and optokinetic eye movement. Neuron 30:771-780. doi: 10.1016/ S0896-6273(01)00316-6.
88. Zhan XL, Clemens JC, Neves G, Hattori D, Flanagan JJ, Hummel T, Vasconcelos ML, Chess A, Zipursky SL. 2004. Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron 43:673-686. doi: 10.1016/j.neuron.2004.07.020.
89. Zheng JJ, Lee S, Zhou ZJ. 2004. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44:851-864. doi: 10.1016/j.neuron.2004.11.015.
90. Zipursky SL, Grueber WB. 2013. The molecular basis of self-avoidance. Annual Review of Neuroscience 36: 547-568. doi: 10.1146/annurev-neuro-062111-150414.