Ten-m2 is required for the generation of binocular visual circuits

Journal of Neuroscience

Volumn 33, Issue 30, 2013, Pages 12490-12509

  Young, Timothy R ^a   Bourke, Michael ^a   Zhou, Xiaohong ^b   Oohashi, Toshitaka ^b   Sawatari, Atomu ^a   Fässler, Reinhard ^b   Leamey, Catherine A ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR B1; GLYCOPROTEIN; PROTEIN C FOS; PROTEIN TEN M2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINOCULAR VISION; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LATERAL GENICULATE BODY; MOUSE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STRIATE CORTEX; SUPERIOR COLLICULUS; TASK PERFORMANCE; VISUAL DISCRIMINATION; VISUAL FIELD; VISUAL STIMULATION; VISUAL SYSTEM; WESTERN BLOTTING;

ANIMALS; DOMINANCE, OCULAR; FEMALE; GENICULATE BODIES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RECEPTOR, EPHB1; RETINAL GANGLION CELLS; SUPERIOR COLLICULI; VISION, BINOCULAR; VISUAL CORTEX; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 84880626107     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4708-12.2013     Document Type: Article

References (56)

1. Bagutti C, Forro G, Ferralli J, Rubin B, Chiquet-Ehrismann R (2003) The intracellular domain of teneurin-2 has a nuclear function and represses zic-1-mediated transcription. J Cell Sci 116:2957-2966. CrossRef Medline
2. Bovolenta P, Mason C (1987) Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J Neurosci 7:1447-1460. Medline
3. Brown LY, Kottmann AH, Brown S (2003) Immunolocalization of Zic2 expression in the developing mouse forebrain. Gene Expr Patterns 3:361-367. CrossRef Medline
4. Carreres MI, Escalante A, Murillo B, Chauvin G, Gaspar P, Vegar C, Herrera E (2011) Transcription factor foxd1 is required for the specification of the temporal retina in mammals. J Neurosci 31:5673-5681. CrossRef Medline
5. Chan SO, Guillery RW (1994) Changes in fiber order in the optic nerve and tract of rat embryos. J Comp Neurol 344:20-32. CrossRef Medline
6. Dharmaratne N, Glendining KA, Young TR, Tran H, Sawatari A, Leamey CA (2012) Ten-m3 is required for the development of topography in the ipsilateral retinocollicular pathway. PLoS One 7:e43083. CrossRef Medline
7. Dräger UC (1975) Receptive fields of single cells and topography in mouse visual cortex. J Comp Neurol 160:269-290. CrossRef Medline
8. Dräger UC (1985) Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proc R Soc Lond B Biol Sci 224:57-77. CrossRef Medline
9. Dräger UC, Olsen JF (1980) Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J Comp Neurol 191:383-412. CrossRef Medline
10. Dragunow M, Robertson HA (1988) Localization and induction of c-fos protein-like immunoreactive material in the nuclei of adult mammalian neurons. Brain Res 440:252-260. CrossRef Medline
11. Fabre PJ, Shimogori T, Charron F (2010) Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J Neurosci 30:266-275. CrossRef Medline
12. Feng K, Zhou XH, Oohashi T, Mörgelin M, Lustig A, Hirakawa S, Ninomiya Y, Engel J, Rauch U, Fässler R (2002) All four members of the Ten-m/ Odz family of transmembrane proteins form dimers. J Biol Chem 277: 26128-26135. CrossRef Medline
13. García-Frigola C, Herrera E (2010) Zic2 regulates the expression of Sert to modulate eye-specific refinement at the visual targets. EMBO J 29:3170-3183. CrossRef Medline
14. García-Frigola C, Carreres MI, Vegar C, Mason C, Herrera E (2008) Zic2 promotes axonal divergence at the optic chiasm midline by EphB1dependent and-independent mechanisms. Development 135:1833-1841. CrossRef Medline
15. Godement P, Salaun J, Imbert M (1984) Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230:552-575. CrossRef Medline
16. Guillery RW, Mason CA, Taylor JS (1995) Developmental determinants at the mammalian optic chiasm. J Neurosci 15:4727-4737. Medline
17. Herrera E, Brown L, Aruga J, Rachel RA, Dolen G, Mikoshiba K, Brown S, Mason CA (2003) Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114:545-557. CrossRef Medline
18. Hofbauer A, Dräger UC (1985) Depth segregation of retinal ganglion cells projecting to mouse superior colliculus. J Comp Neurol 234:465-474. CrossRef Medline
19. Hong W, Mosca TJ, Luo L (2012) Teneurins instruct synaptic partner matching in an olfactory map. Nature 484:201-207. CrossRef Medline
20. Horng S, Kreiman G, Ellsworth C, Page D, Blank M, Millen K, Sur M (2009) Differential gene expression in the developing lateral geniculate nucleus and medial geniculate nucleus reveals novel roles for Zic4 and Foxp2 in visual and auditory pathway development. J Neurosci 29:13672-13683. CrossRef Medline
21. Kenzelmann D, Chiquet-Ehrismann R, Leachman NT, Tucker RP (2008) Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo. BMC Dev Biol 8:30. CrossRef Medline
22. Kenzelmann-Broz D, Tucker RP, Leachman NT, Chiquet-Ehrismann R (2010) The expression of teneurin-4 in the avian embryo: potential roles in patterning of the limb and nervous system. Int J Dev Biol 54;1509-16. Medline
23. LaVail JH, Nixon RA, Sidman RL (1978) Genetic control of retinal ganglion cell projections. J Comp Neurol 182:399-421. CrossRef Medline
24. Leamey CA, Glendining KA, Kreiman G, Kang ND, Wang KH, Fassler R, Sawatari A, Tonegawa S, Sur M (2008) Differential gene expression between sensory neocortical areas: potential roles for Ten_m3 and Bcl6 in patterning visual and somatosensory pathways. Cereb Cortex 18:53-66. CrossRef Medline
25. Leamey CA, Merlin S, Lattouf P, Sawatari A, Zhou X, Demel N, Glendining KA, Oohashi T, Sur M, Fässler R (2007) Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol 5:e241. CrossRef Medline
26. Leamey CA, Van Wart A, Sur M (2009) Intrinsic patterning and experiencedependent mechanisms that generate eye-specific projections and binocular circuits in the visual pathway. Curr Opin Neurobiol 19:181-187. CrossRef Medline
27. Lee R, Petros TJ, Mason CA (2008) Zic2 regulates retinal ganglion cell axon avoidance of ephrinB2 through inducing expression of the guidance receptor EphB1. J Neurosci 28:5910-5919. CrossRef Medline
28. Li H, Bishop KM, O'Leary DD (2006) Potential target genes of EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning. Mol Cell Neurosci 33:136-149. CrossRef Medline
29. Merlin S, Horng S, Marotte LR, Sur M, Sawatari A, Leamey CA (2013) Deletion of Ten-m3 induces the formation of eye dominance domains in mouse visual cortex. Cereb Cortex 23:763-774. CrossRef Medline
30. Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117. CrossRef Medline
31. Mosca TJ, Hong W, Dani VS, Favaloro V, Luo L (2012) Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 484:237-241. CrossRef Medline
32. Mui SH, Hindges R, O'Leary DD, Lemke G, Bertuzzi S (2002) The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129:797-804. Medline
33. Muir-Robinson G, Hwang BJ, Feller MB (2002) Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J Neurosci 22:5259-5264. Medline
34. Oohashi T, Zhou XH, Feng K, Richter B, Mörgelin M, Perez MT, Su WD, Chiquet-Ehrismann R, Rauch U, Fässler R (1999) Mouse ten-m/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues. J Cell Biol 145:563-577. CrossRef Medline
35. Pak W, Hindges R, Lim YS, Pfaff SL, O'Leary DD (2004) Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119:567-578. CrossRef Medline
36. 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. CrossRef Medline
37. Petros TJ, Shrestha BR, Mason C (2009) Specificity and sufficiency of EphB1 in driving the ipsilateral retinal projection. J Neurosci 29:3463-3474. CrossRef Medline
38. Porciatti V, Pizzorusso T, Maffei L (1999) The visual physiology of the wild type mouse determined with pattern VEPs. Vis Res 39:3071-3081. CrossRef Medline
39. Prusky GT, West PW, Douglas RM (2000) Behavioral assessment of visual acuity in mice and rats. Vis Res 40:2201-2209. CrossRef Medline
40. Rebsam A, Petros TJ, Mason CA (2009) Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. J Neurosci 29:14855-14863. CrossRef Medline
41. Rebsam A, Bhansali P, Mason CA (2012) Eye-specific projections of retinogeniculate axons are altered in albino mice. J Neurosci 32:4821-4826. CrossRef Medline
42. Reese BE (1986) The topography of expanded uncrossed retinal projections following neonatal enucleation of one eye: differing effects in dorsal lateral geniculate nucleus and superior colliculus. J Comp Neurol 250:8-32. CrossRef Medline
43. Reese BE (1987) The position of the crossed and uncrossed optic axons, and the nonoptic axons, in the optic tract of the rat. Neuroscience 22:1025-1039. CrossRef Medline
44. Reese BE, Jeffery G (1983) Crossed and uncrossed visual topography in dorsal lateral geniculate nucleus of the pigmented rat. J Neurophysiol 49:877-885. Medline
45. Reese BE, Guillery RW, Mallarino C (1992) Time of ganglion cell genesis in relation to the chiasmatic pathway choice of retinofugal axons. J Comp Neurol 324:336-342. CrossRef Medline
46. Silva JP, Lelianova VG, Ermolyuk YS, Vysokov N, Hitchen PG, Berninghausen O, Rahman MA, Zangrandi A, Fidalgo S, Tonevitsky AG, Dell A, Volynski KE, Ushkaryov YA (2011) Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities. Proc Natl Acad Sci U S A 108:12113-12118. CrossRef Medline
47. Tian NM, Pratt T, Price DJ (2008) Foxg1 regulates retinal axon pathfinding by repressing an ipsilateral program in nasal retina and by causing optic chiasm cells to exert a net axonal growth-promoting activity. Development 135:4081-4089. CrossRef Medline
48. Trevelyan AJ, Upton AL, Cordery PM, Thompson ID (2007) An experimentally induced duplication of retinotopic mapping within the hamster primary visual cortex. Eur J Neurosci 26:3277-3290. CrossRef Medline
49. Tucker RP, Beckmann J, Leachman NT, Schöler J, Chiquet-Ehrismann R (2012) Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol Biol Evol 29:1019-1029. CrossRef Medline
50. Wagor E, Mangini NJ, Pearlman AL (1980) Retinotopic organization of striate and extrastriate visual cortex in the mouse. J Comp Neurol 193: 187-202. CrossRef Medline
51. Wang Q, Burkhalter A (2007) Area map of mouse visual cortex. J Comp Neurol 502:339-357. CrossRef Medline
52. Williams SE, Mann F, Erskine L, Sakurai T, Wei S, Rossi DJ, Gale NW, Holt CE, Mason CA, Henkemeyer M (2003) Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39:919-935. CrossRef Medline
53. Williams SE, Grumet M, Colman DR, Henkemeyer M, Mason CA, Sakurai T (2006) A role for Nr-CAM in the patterning of binocular visual pathways. Neuron 50:535-547. CrossRef Medline
54. Wong AA, Brown RE (2006) Visual detection, pattern discrimination and visual acuity in 14 strains of mice. Genes Brain Behav 5:389-403. CrossRef Medline
55. Young TR, Leamey CA (2009) Teneurins: important regulators of neural circuitry. Int J Biochem Cell Biol 41:990-993. CrossRef Medline
56. Zhou XH, Brandau O, Feng K, Oohashi T, Ninomiya Y, Rauch U, Fässler R (2003) The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Expr Patterns 3:397-405. CrossRef Medline