The ventral habenulae of zebrafish develop in prosomere 2 dependent on Tcf7l2 function

Neural Development

Volumn 8, Issue 1, 2013, Pages

  Beretta, Carlo A ^a   Dross, Nicolas ^a   Bankhead, Peter ^a   Carl, Matthias ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Asymmetry; Habenula; Neural network; Photoconversion; PSmOrange; Tcf; Time lapse imaging; Zebrafish

Indexed keywords

NEUROTRANSMITTER; TRANSCRIPTION FACTOR 7 LIKE 2; ZEBRAFISH PROTEIN; TCF7L2 PROTEIN, ZEBRAFISH;

ANIMAL CELL; ARTICLE; CELL TRACKING; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DIENCEPHALON; EMBRYO; FLUORESCENCE MICROSCOPY; GENOTYPE; HABENULA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LASER SURGERY; NONHUMAN; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY; ZEBRA FISH; ANIMAL; GENETICS; METABOLISM; MULTIPHOTON MICROSCOPY; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; DIENCEPHALON; HABENULA; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NEUROGENESIS; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84884554412     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-8-19     Document Type: Article

References (50)

1. Sutherland RJ. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 1982, 6:1-13. 10.1016/0149-7634(82)90003-3, 7041014.
2. Amo R, Aizawa H, Takahoko M, Kobayashi M, Takahashi R, Aoki T, Okamoto H. Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J Neurosci 2010, 30:1566-1574. 10.1523/JNEUROSCI.3690-09.2010, 20107084.
3. Gamse JT, Kuan YS, Macurak M, Brosamle C, Thisse B, Thisse C, Halpern ME. Directional asymmetry of the zebrafish epithalamus guides dorso-ventral innervation of the midbrain target. Development 2005, 132:4869-4881. 10.1242/dev.02046, 16207761.
4. Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O, Concha ML, Russell C, Wilson SW, Okamoto H. Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr Biol 2005, 15:238-243. 10.1016/j.cub.2005.01.014, 2790415, 15694307.
5. Bianco IH, Carl M, Russell C, Clark J, Wilson SW. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev 2008, 3:9. 10.1186/1749-8104-3-9, 2292717, 18377638.
6. Yang L-M, Hu B, Xia Y-H, Zhang B-L, Zhao H. Lateral habenula lesions improve the behavioral response in depressed rats via increasing the serotonin level in dorsal raphe nucleus. Behav Brain Res 2008, 188:84-90. 10.1016/j.bbr.2007.10.022, 18054396.
7. Concha ML, Bianco IH, Wilson SW. Encoding asymmetry within neural circuits. Nat Rev Neurosci 2012, 13:832-843. 10.1038/nrn3371, 23165260.
8. Hikosaka O. The habenula: from stress evasion to value-based decision-making. Nat Neurosci 2010, 11:503-513.
9. Okamoto H, Agetsuma M, Aizawa H. Genetic dissection of the zebrafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev Neurobiol 2012, 72:386-394. 10.1002/dneu.20913, 21567982.
10. Lecourtier L, Kelly PH. A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Behav Rev 2007, 31:658-672.
11. Aizawa H, Goto M, Sato T, Okamoto H. Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev Cell 2007, 12:87-98. 10.1016/j.devcel.2006.10.004, 17199043.
12. Gamse JT, Thisse C, Thisse B, Halpern ME. The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development 2003, 130:1059-1068. 10.1242/dev.00270, 12571098.
13. Concha ML, Wilson SW. Asymmetry in the epithalamus of vertebrates. J Anat 2001, 199:63-84. 10.1046/j.1469-7580.2001.19910063.x, 1594988, 11523830.
14. Roussigne M, Blader P, Wilson SW. The zebrafish epithalamus clears a path through the complexity of brain lateralization. Dev Neurobiol 2011, 72:269-281.
15. Wree A, Zilles K, Schleicher A. Growth of fresh volumes and spontaneous cell death in the nuclei habenulae of albino rats during ontogenesis. Anat Embryol (Berl) 1981, 161:419-431.
16. Barth KA, Miklosi A, Watkins J, Bianco IH, Wilson SW, Andrew RJ. Fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr Biol 2005, 15:844-850. 10.1016/j.cub.2005.03.047, 2790416, 15886103.
17. Facchin L, Burgess HA, Siddiqi M, Granato M, Halpern ME. Determining the function of zebrafish epithalamic asymmetry. Philos Trans R Soc Lond B Biol Sci 2009, 364:1021-1032. 10.1098/rstb.2008.0234, 2666080, 19064346.
18. Carl M, Bianco IH, Bajoghli B, Aghaallaei N, Czerny T, Wilson SW. Wnt/Axin1/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of CNS asymmetries. Neuron 2007, 55:393-405. 10.1016/j.neuron.2007.07.007, 1940036, 17678853.
19. Doll CA, Burkart JT, Hope KD, Halpern ME, Gamse JT. Subnuclear development of the zebrafish habenular nuclei requires ER translocon function. Dev Biol 2011, 360:44-57. 3215860, 21945073.
20. Roussigne M, Bianco IH, Wilson SW, Blader P. Nodal signaling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development 2009, 136:1549-1557. 10.1242/dev.034793, 2675782,2675782, 19363156.
21. Bortolato M, Pivac N, Muck SD, Nikolac PM, Pessia M, Di Giovanni G. The role of the serotonergic system at the interface of aggression and suicide. Neuroscience 2013, 236:160-185.
22. Tsai SJ, Chiu HJ, Wang YC, Hong CJ. Association study of serotonin-6 receptor variant (C267T) with schizophrenia and aggressive behavior. Neurosci Lett 1999, 271:135-137. 10.1016/S0304-3940(99)00542-X, 10477121.
23. Tsai SJ, Hong CJ, Yu YW, Lin CH, Song HL, Lai HC, Yang KH. Association study of a functional serotonin transporter gene polymorphism with schizophrenia, psychopathology and clozapine response. Schizophr Res 2000, 44:177-181. 10.1016/S0920-9964(99)00170-X, 10962219.
24. Matsumoto M, Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nat Geosci 2007, 447:1111-1115.
25. Matsumoto M, Hikosaka O. Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 2009, 12:77-84. 10.1038/nn.2233, 2737828, 19043410.
26. Matsumoto M, Hikosaka O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nat Geosci 2009, 459:837-841.
27. Bromberg-Martin ES, Hikosaka O. Lateral habenula neurons signal errors in the prediction of reward information. Nat Neurosci 2011, 14:1209-1216. 10.1038/nn.2902, 3164948, 21857659.
28. Zilles K, Schleicher A, Wingert F. Quantitative growth analysis of limbic nuclei areas fresh volume in diencephalon and mesencephalon of an albino mouse ontogenic series. J Hirnforsch 1976, 17:1-10.
29. Subach OM, Patterson GH, Ting L-M, Wang Y, Condeelis JS, Verkhusha VV. A photoswitchable orange-to-far-red fluorescent protein, PSmOrange. Nat Methods 2011, 8:771-777. 10.1038/nmeth.1664, 3164916, 21804536.
30. Ekstrom P, Ebbesson SO. The left habenular nucleus contains a discrete serotonin-immunoreactive subnucleus in the coho salmon (Oncorhynchus kisutch). Neurosci Lett 1988, 91:121-125. 10.1016/0304-3940(88)90754-9, 3185952.
31. Bianco IH, Wilson SW. The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Phil Trans R Soc B 2009, 364:1005-1020. 10.1098/rstb.2008.0213, 2666075, 19064356.
32. Kuan Y-S, Yu H-H, Moens CB, Halpern ME. Neuropilin asymmetry mediates a left-right difference in habenular connectivity. Development 2007, 134:857-865. 10.1242/dev.02791, 17251263.
33. Snelson CD, Santhakumar K, Halpern ME, Gamse JT. Tbx2b is required for the development of the parapineal organ. Development 2008, 135:1693-1702. 10.1242/dev.016576, 2810831, 18385257.
34. Concha ML, Russell C, Regan JC, Tawk M, Sidi S, Gilmour DT, Kapsimali M, Sumoy L, Goldstone K, Amaya E, et al. Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron 2003, 39:423-438. 10.1016/S0896-6273(03)00437-9, 12895418.
35. Heisenberg CP, Houart C, Take-uchi M, Rauch GJ, Young N, Coutinho P, Masai I, Caneparo L, Concha ML, Geisler R, et al. A mutation in the Gsk3-binding domain of zebrafish Masterblind/Axin1 leads to a fate transformation of telencephalon and eyes to diencephalon. Genes Dev 2001, 15:1427-1434. 10.1101/gad.194301, 312705,312705, 11390362.
36. Hüsken U, Carl M. The Wnt/beta-catenin signaling pathway establishes neuroanatomical asymmetries and their laterality. Mech Dev 2013, 130:330-335. 10.1016/j.mod.2012.09.002, 23022991.
37. Hagemann AIH, Scholpp S. The tale of the three brothers - Shh, Wnt, and Fgf during development of the thalamus. Front Neurosci 2012, 6:76. 3361129, 22654733.
38. Mattes B, Weber S, Peres J, Chen Q, Davidson G, Houart C, Scholpp S. Wnt3 and Wnt3a are required for induction of the mid-diencephalic organizer in the caudal forebrain. Neural Dev 2012, 7:12. 10.1186/1749-8104-7-12, 3349543, 22475147.
39. Peukert D, Weber S, Lumsden A, Scholpp S. Lhx2 And Lhx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating Wnt signaling. PLoS Biol 2011, 9(12):e1001218. 10.1371/journal.pbio.1001218, 3236734, 22180728.
40. Ogawa S, Ramadasan PN, Goschorska M, Anantharajah A, Ng KW, Parhar IS. Cloning and expression of tachykinins and their association with kisspeptins in the brains of zebrafish. J Comp Neurol 2012, 520:2991-3012. 10.1002/cne.23103, 22430310.
41. Muncan V, Faro A, Haramis A-PG, Hurlstone AFL, Wienholds E, van Es J, Korving J, Begthel H, Zivkovic D, Clevers H. T-cell factor 4 (Tcf7l2) maintains proliferative compartments in zebrafish intestine. EMBO Rep 2007, 8:966-973. 10.1038/sj.embor.7401071, 2002560, 17823612.
42. Young R, Reyes A, Allende M. Expression and splice variant analysis of the zebrafish tcf4 transcription factor. Mech Dev 2002, 117:269-273. 10.1016/S0925-4773(02)00180-6, 12204269.
43. Clevers H, Nusse R. Wnt/b-catenin signaling and disease. Cell 2012, 149:1192-1205. 10.1016/j.cell.2012.05.012, 22682243.
44. Beretta CA, Brinkmann I, Carl M. All four zebrafish Wnt7 genes are expressed during early brain development. Gene Expr Patterns 2011, 11:277-284. 10.1016/j.gep.2011.01.004, 21300182.
45. Hansen T, Ingason A, Djurovic S, Melle I, Fenger M, Gustafsson O, Jakobsen KD, Rasmussen HB, Tosato S, Rietschel M, et al. At-risk variant in TCF7L2 for type II diabetes increases risk of schizophrenia. Biol Psychiatry 2011, 70:60-64.
46. Alkelai A, Greenbaum L, Lupoli S, Kohn Y, Sarner-Kanyas K, Ben-Asher E, Lancet D, Macciardi F, Lerer B. Association of the type 2 diabetes mellitus susceptibility gene, TCF7L2, with schizophrenia in an Arab-Israeli family sample. PLoS One 2012, 7(1):e29228. 10.1371/journal.pone.0029228, 3256145, 22247771.
47. Westerfield M. The zebrafish book 1995, Eugene, OR: The University of Oregon Press, 3.
48. Macdonald R, Xu Q, Barth KA, Mikkola I, Holder N, Fjose A, Krauss S, Wilson SW. Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain. Neuron 1994, 13:1039-1053. 10.1016/0896-6273(94)90044-2, 7946344.
49. Shanmugalingam S, Houart C, Picker A, Reifers F, Macdonald R, Barth A, Griffin K, Brand M, Wilson SW. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development 2000, 127:2549-2561.
50. Kapsimali M, Kaushik AL, Gibon G, Dirian L, Ernest S, Rosa FM. Fgf signaling controls pharyngeal taste bud formation through miR-200 and Delta-Notch activity. Development 2011, 138:3473-3484. 10.1242/dev.058669, 21791527.