Contributions of VLDLR and LRP8 in the establishment of retinogeniculate projections

Neural Development

Volumn 8, Issue 1, 2013, Pages

  Su, Jianmin ^a   Klemm, Michael A ^b   Josephson, Anne M ^c   Fox, Michael A ^a,b,c  

^a VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Axon; Intergeniculate nucleus; Lateral geniculate nucleus; Reelin; Retinal terminal; Retinogeniculate; Synaptic targeting

Indexed keywords

CHOLERA TOXIN B SUBUNIT; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 8; NEUROPEPTIDE Y; NUCLEAR FACTOR Y; REELIN; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER 2; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN 8; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; CYTOARCHITECTURE; GENE DELETION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LATERAL GENICULATE BODY; MOUSE; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; RETINA GANGLION CELL; RETINOTECTAL PROJECTION; ANIMAL; C57BL MOUSE; CELL MOTION; EMBRYOLOGY; GENETICS; GENICULATE BODY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; CELL MOVEMENT; GENICULATE BODIES; LDL-RECEPTOR RELATED PROTEINS; LIPOPROTEINS, VLDL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, LDL; RETINAL GANGLION CELLS;

EID: 84878816451     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-8-11     Document Type: Article

References (76)

1. Huberman AD, Feller MB, Chapman B. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 2008, 31:479-509. 10.1146/annurev.neuro.31.060407.125533, 2655105, 18558864.
2. Triplett JW, Feldheim DA. Eph and ephrin signaling in the formation of topographic maps. Semin Cell Dev Biol 2011, 23(1):7-15. 3288406, 22044886.
3. Sanes JR, Yamagata M. Many paths to synaptic specificity. Annu Rev Cell Dev Biol 2009, 25:161-195. 10.1146/annurev.cellbio.24.110707.175402, 19575668.
4. Pfeiffenberger C, Cutforth T, Woods G, Yamada J, Renteria RC, Copenhagen DR, Flanagan JG, Feldheim DA. Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. Nat Neurosci 2005, 8(8):1022-1027. 10.1038/nn1508, 1352169, 16025107.
5. Leamey CA, Merlin S, Lattouf P, Sawatari A, Zhou X, Demel N, Glendining KA, Oohashi T, Sur M, Fassler R. Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol 2007, 5(9):e241. 10.1371/journal.pbio.0050241, 1964777, 17803360.
6. Rebsam A, Petros TJ, Mason CA. Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. J Neurosci 2009, 29(47):14855-14863. 10.1523/JNEUROSCI.3462-09.2009, 2829946, 19940181.
7. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ. Functional requirement for class I MHC in CNS development and plasticity. Science 2000, 290(5499):2155-2159. 10.1126/science.290.5499.2155, 2175035, 11118151.
8. Bjartmar L, Huberman AD, Ullian EM, Renteria RC, Liu X, Xu W, Prezioso J, Susman MW, Stellwagen D, Stokes CC, Cho R, Worley P, Malenka RC, Ball S, Peachey NS, Copenhagen D, Chapman B, Nakamoto M, Barres BA, Perin MS. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 2006, 26(23):6269-6281. 10.1523/JNEUROSCI.4212-05.2006, 2579897, 16763034.
9. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131(6):1164-1178. 10.1016/j.cell.2007.10.036, 18083105.
10. Datwani A, McConnell MJ, Kanold PO, Micheva KD, Busse B, Shamloo M, Smith SJ, Shatz CJ. Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron 2009, 64(4):463-470. 10.1016/j.neuron.2009.10.015, 2787480, 19945389.
11. Hong YK, Kim IJ, Sanes JR. Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. J Comp Neurol 2011, 519(9):1691-1711. 10.1002/cne.22595, 3652686, 21452242.
12. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. Molecular identification of a retinal cell type that responds to upward motion. Nature 2008, 452(7186):478-482. 10.1038/nature06739, 18368118.
13. Kim IJ, Zhang Y, Meister M, Sanes JR. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci 2010, 30(4):1452-1462. 10.1523/JNEUROSCI.4779-09.2010, 2822471, 20107072.
14. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 2008, 59(3):425-438. 10.1016/j.neuron.2008.07.018, 18701068.
15. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 2009, 62(3):327-334. 10.1016/j.neuron.2009.04.014, 3140054, 19447089.
16. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, Barres BA, Huberman AD, Feller MB. Transgenic mice reveal unexpected diversity of on-off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 2011, 31(24):8760-8769. 10.1523/JNEUROSCI.0564-11.2011, 3139540, 21677160.
17. Yonehara K, Shintani T, Suzuki R, Sakuta H, Takeuchi Y, Nakamura-Yonehara K, Noda M. Expression of SPIG1 reveals development of a retinal ganglion cell subtype projecting to the medial terminal nucleus in the mouse. PLoS One 2008, 3(2):e1533. 10.1371/journal.pone.0001533, 2217595, 18253481.
18. Yonehara K, Ishikane H, Sakuta H, Shintani T, Nakamura-Yonehara K, Kamiji NL, Usui S, Noda M. Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS One 2009, 4(1):e4320. 10.1371/journal.pone.0004320, 2629575, 19177171.
19. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 2006, 497(3):326-349. 10.1002/cne.20970, 2885916, 16736474.
20. Fox MA, Guido W. Shedding light on class-specific wiring: development of intrinsically photosensitive retinal ganglion cell circuitry. Mol Neurobiol 2011, 44(3):321-329. 10.1007/s12035-011-8199-8, 3230729, 21861091.
21. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374(6524):719-723. 10.1038/374719a0, 7715726.
22. D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 1997, 17(1):23-31.
23. Rogers JT, Rusiana I, Trotter J, Zhao L, Donaldson E, Pak DT, Babus LW, Peters M, Banko JL, Chavis P, Rebeck GW, Hoe HS, Weeber EJ. Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density. Learn Mem 2011, 18(9):558-564. 10.1101/lm.2153511, 3166788, 21852430.
24. Ventruti A, Kazdoba TM, Niu S, D'Arcangelo G. Reelin deficiency causes specific defects in the molecular composition of the synapses in the adult brain. Neuroscience 2011, 189:32-42.
25. Hellwig S, Hack I, Kowalski J, Brunne B, Jarowyj J, Unger A, Bock HH, Junghans D, Frotscher M. Role for Reelin in neurotransmitter release. J Neurosci 2011, 31(7):2352-2360. 10.1523/JNEUROSCI.3984-10.2011, 21325502.
26. Matsuki T, Matthews RT, Cooper JA, van der Brug MP, Cookson MR, Hardy JA, Olson EC, Howell BW. Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell 2010, 143(5):826-836. 10.1016/j.cell.2010.10.029, 3033572, 21111240.
27. Leemhuis J, Bouche E, Frotscher M, Henle F, Hein L, Herz J, Meyer DK, Pichler M, Roth G, Schwan C, Bock HH. Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation. J Neurosci 2010, 30(44):14759-14772. 10.1523/JNEUROSCI.4036-10.2010, 3523719, 21048135.
28. Borrell V, Del Rio JA, Alcantara S, Derer M, Martinez A, D'Arcangelo G, Nakajima K, Mikoshiba K, Derer P, Curran T, Soriano E. Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J Neurosci 1999, 19(4):1345-1358.
29. Borrell V, Pujadas L, Simo S, Dura D, Sole M, Cooper JA, Del Rio JA, Soriano E. Reelin and mDab1 regulate the development of hippocampal connections. Mol Cell Neurosci 2007, 36(2):158-173. 10.1016/j.mcn.2007.06.006, 17720534.
30. Wu P, Li MS, Yu DM, Deng JB. Reelin, a guidance signal for the regeneration of the entorhino-hippocampal path. Brain Res 2008, 1208:1-7.
31. Su J, Haner CV, Imbery TE, Brooks JM, Morhardt DR, Gorse K, Guido W, Fox MA. Reelin is required for class-specific retinogeniculate targeting. J Neurosci 2011, 31(2):575-586. 10.1523/JNEUROSCI.4227-10.2011, 3257181, 21228166.
32. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999, 97(6):689-701. 10.1016/S0092-8674(00)80782-5, 10380922.
33. Benhayon D, Magdaleno S, Curran T. Binding of purified Reelin to ApoER2 and VLDLR mediates tyrosine phosphorylation of Disabled-1. Brain Res Mol Brain Res 2003, 112(1-2):33-45.
34. Howell BW, Hawkes R, Soriano P, Cooper JA. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 1997, 389(6652):733-737. 10.1038/39607, 9338785.
35. Howell BW, Herrick TM, Hildebrand JD, Zhang Y, Cooper JA. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr Biol 2000, 10(15):877-885. 10.1016/S0960-9822(00)00608-4, 10959835.
36. Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 1997, 389(6652):730-733. 10.1038/39601, 9338784.
37. Land PW, Kyonka E, Shamalla-Hannah L. Vesicular glutamate transporters in the lateral geniculate nucleus: expression of VGLUT2 by retinal terminals. Brain Res 2004, 996(2):251-254. 10.1016/j.brainres.2003.10.032, 14697503.
38. Singh R, Su J, Brooks JM, Terauchi A, Umemori H, Fox MA. Fibroblast Growth Factor 22 contributes to the development of retinal nerve terminals in the dorsal lateral geniculate nucleus. Front Mol Neurosci 2012, 4:61. 3306139, 22363257.
39. Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 2005, 22(5):661-676.
40. Bickford ME, Slusarczyk A, Dilger EK, Krahe TE, Kucuk C, Guido W. Synaptic development of the mouse dorsal lateral geniculate nucleus. J Comp Neurol 2010, 518(5):622-635. 10.1002/cne.22223, 20034053.
41. Fujiyama F, Hioki H, Tomioka R, Taki K, Tamamaki N, Nomura S, Okamoto K, Kaneko T. Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation. J Comp Neurol 2003, 465(2):234-249. 10.1002/cne.10848, 12949784.
42. Guido W. Refinement of the retinogeniculate pathway. J Physiol 2008, 586(Pt 18):4357-4362. 2614014, 18556365.
43. Rice DS, Nusinowitz S, Azimi AM, Martinez A, Soriano E, Curran T. The reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 2001, 31(6):929-941. 10.1016/S0896-6273(01)00436-6, 11580894.
44. Trotter JH, Klein M, Jinwal UK, Abisambra JF, Dickey CA, Tharkur J, Masiulis I, Ding J, Locke KG, Rickman CB, Birch DG, Weeber EJ, Herz J. ApoER2 function in the establishment and maintenance of retinal synaptic connectivity. J Neurosci 2011, 31(40):14413-14423. 10.1523/JNEUROSCI.3135-11.2011, 3224795, 21976526.
45. Botchkina GI, Morin LP. Specialized neuronal and glial contributions to development of the hamster lateral geniculate complex and circadian visual system. J Neurosci 1995, 15(1 Pt 1):190-201.
46. Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 2000, 27(1):33-44. 10.1016/S0896-6273(00)00007-6, 10939329.
47. Schmid RS, Jo R, Shelton S, Kreidberg JA, Anton ES. Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb Cortex 2005, 15(10):1632-1636. 10.1093/cercor/bhi041, 15703255.
48. Dong E, Caruncho H, Liu WS, Smalheiser NR, Grayson DR, Costa E, Guidotti A. A reelin-integrin receptor interaction regulates Arc mRNA translation in synaptoneurosomes. Proc Natl Acad Sci USA 2003, 100(9):5479-5484. 10.1073/pnas.1031602100, 154370, 12707415.
49. Rodriguez MA, Pesold C, Liu WS, Kriho V, Guidotti A, Pappas GD, Costa E. Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex. Proc Natl Acad Sci USA 2000, 97(7):3550-3555. 10.1073/pnas.97.7.3550, 16277, 10725376.
50. Stipp CS, Hemler ME. Transmembrane-4-superfamily proteins CD151 and CD81 associate with alpha 3 beta 1 integrin, and selectively contribute to alpha 3 beta 1-dependent neurite outgrowth. J Cell Sci 2000, 113(Pt 11):1871-1882.
51. Ivins JK, Yurchenco PD, Lander AD. Regulation of neurite outgrowth by integrin activation. J Neurosci 2000, 20(17):6551-6560.
52. Ivins JK, Colognato H, Kreidberg JA, Yurchenco PD, Lander AD. Neuronal receptors mediating responses to antibody activated laminin-1. J Neurosci 1998, 18(23):9703-9715.
53. Young-Pearse TL, Chen AC, Chang R, Marquez C, Selkoe DJ. Secreted APP regulates the function of full-length APP in neurite outgrowth through interaction with integrin beta1. Neural Dev 2008, 3:15. 10.1186/1749-8104-3-15, 2442059, 18573216.
54. Billnitzer AJ, Barskaya I, Yin C, Perez RG. APP independent and dependent effects on neurite outgrowth are modulated by the receptor associated protein (RAP). J Neurochem 2012, 124(1):123-132.
55. Caldwell JH, Klevanski M, Saar M, Müller UC. Roles of the amyloid precursor protein family in the peripheral nervous system. Mech Dev 2012, 29(12):112-118.
56. Hoe HS, Lee KJ, Carney RS, Lee J, Markova A, Lee JY, Howell BW, Hyman BT, Pak DT, Bu G, Rebeck GW. Interaction of reelin with amyloid precursor protein promotes neurite outgrowth. J Neurosci 2009, 29(23):7459-7473. 10.1523/JNEUROSCI.4872-08.2009, 2759694, 19515914.
57. Ho T, Vessey KA, Cappai R, Dinet V, Mascarelli F, Ciccotosto GD, Fletcher EL. Amyloid precursor protein is required for normal function of the rod and cone pathways in the mouse retina. PLoS One 2012, 7(1):e29892. 10.1371/journal.pone.0029892, 3261162, 22279552.
58. Angst BD, Marcozzi C, Magee AI. The cadherin superfamily: diversity in form and function. J Cell Sci 2001, 114(Pt 4):629-641.
59. Senzaki K, Ogawa M, Yagi T. Proteins of the CNR family are multiple receptors for Reelin. Cell 1999, 99(6):635-647. 10.1016/S0092-8674(00)81552-4, 10612399.
60. Jossin Y, Ignatova N, Hiesberger T, Herz J, de Lambert RC, Goffinet AM. The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 2004, 24(2):514-521. 10.1523/JNEUROSCI.3408-03.2004, 14724251.
61. Sanes JR, Zipursky SL. Design principles of insect and vertebrate visual systems. Neuron 2010, 66(1):15-36. 10.1016/j.neuron.2010.01.018, 2871012, 20399726.
62. Zipursky SL, Sanes JR. Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 2010, 143(3):343-353. 10.1016/j.cell.2010.10.009, 21029858.
63. Honjo M, Tanihara H, Suzuki S, Tanaka T, Honda Y, Takeichi M. Differential expression of cadherin adhesion receptors in neural retina of the postnatal mouse. Invest Ophthalmol Vis Sci 2000, 41(2):546-551.
64. Lefebvre JL, Zhang Y, Meister M, Wang X, Sanes JR. gamma-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 2008, 135(24):4141-4151. 10.1242/dev.027912, 2644426, 19029044.
65. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 2012, 488(7412):517-521. 10.1038/nature11305, 3427422, 22842903.
66. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, Nguyen PL, Panagiotakos G, Inoue YU, Egusa SF, Volgyi B, Inoue T, Bloomfield SA, Barres BA, Berson DM, Feldheim DA, Huberman AD. Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 2011, 71(4):632-639. 10.1016/j.neuron.2011.07.006, 3513360, 21867880.
67. Hui DY, Basford JE. Distinct signaling mechanisms for apoE inhibition of cell migration and proliferation. Neurobiol Aging 2005, 26(3):317-323. 10.1016/j.neurobiolaging.2004.02.030, 15639309.
68. Blake SM, Strasser V, Andrade N, Duit S, Hofbauer R, Schneider WJ, Nimpf J. Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J 2008, 27(22):3069-3080. 10.1038/emboj.2008.223, 2585172, 18946489.
69. Oganesian A, Armstrong LC, Migliorini MM, Strickland DK, Bornstein P. Thrombospondins use the VLDL receptor and a nonapoptotic pathway to inhibit cell division in microvascular endothelial cells. Mol Biol Cell 2008, 19(2):563-571. 2230579, 18032585.
70. Volgyi B, Chheda S, Bloomfield SA. Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J Comp Neurol 2009, 512(5):664-687. 10.1002/cne.21912, 3373319, 19051243.
71. Coombs J, van der List D, Wang GY, Chalupa LM. Morphological properties of mouse retinal ganglion cells. Neuroscience 2006, 140(1):123-136. 10.1016/j.neuroscience.2006.02.079, 16626866.
72. Kong JH, Fish DR, Rockhill RL, Masland RH. Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 2005, 489(3):293-310. 10.1002/cne.20631, 16025455.
73. Sun W, Li N, He S. Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 2002, 451(2):115-126. 10.1002/cne.10323, 12209831.
74. Su J, Gorse K, Ramirez F, Fox MA. Collagen XIX is expressed by interneurons and contributes to the formation of hippocampal synapses. J Comp Neurol 2010, 518(2):229-253. 10.1002/cne.22228, 2913722, 19937713.
75. Yamamoto T, Sakakibara S, Mikoshiba K, Terashima T. Ectopic corticospinal tract and corticothalamic tract neurons in the cerebral cortex of yotari and reeler mice. J Comp Neurol 2003, 461(1):61-75. 10.1002/cne.10678, 12722105.
76. Su J, Stenbjorn RS, Gorse K, Su K, Hauser KF, Ricard-Blum S, Pihlajaniemi T, Fox MA. Target-derived matricryptins organize cerebellar synapse formation through alpha3beta1 integrins. Cell Rep 2012, 2(2):223-230. 10.1016/j.celrep.2012.07.001, 3432753, 22884367.