User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Onecut transcription factors are required for the second phase of development of the A13 dopaminergic nucleus in the mouse

Primary tabs

Espana-Bessy, Agnès [UCL] Clotman, Frédéric [UCL]

The A13 dopaminergic nucleus belongs to the incerto-hypothalamic area. It is thought to exert autonomous roles by integrating sensory input to autonomic, neuroendocrine, and motor output. Although its early development has been well characterized, the factors that contribute to later steps of its formation remain unknown. Transcription factors of the Onecut family have been detected in the A13 nucleus, raising the question of possible roles of these factors during A13 development. Using a combination of immunofluorescence analyses on sections and after whole-mount labeling followed by 3D reconstructions, we further characterized the second phase of development of the A13 nucleus in the mouse, described the distribution of the Onecut proteins throughout A13 development, and analyzed the phenotype of this nucleus in single or compound mutant embryos for the Onecut factors. Here we show that A13 development can be divided into two successive phases. First, during radial migration toward the pial surface the A13 cells differentiate into dopaminergic neurons. Second, these cells gather in the vicinity of the third ventricle. Onecut factors are dynamically and differentially expressed in the A13 nucleus during these two phases of development. In Onecut mutant embryos, the A13 neurons differentiate normally but scatter in the diencephalon and fail to properly gather close to the third ventricle. Hence, Onecut factors are markers of the A13 nucleus throughout embryonic development. They are dispensable for the first phase of A13 development but are required for the second phase of development and for maintenance of this nucleus. J. Comp. Neurol. 520:1424–1441, 2012. © 2011 Wiley Periodicals, Inc.

Document type Article de périodique (Journal article)
Access type Accès restreint
Publication date 2011
Language Anglais
Journal information "The Journal of Comparative Neurology" - Vol. 520, no. 7, p. 1424 -1441 (2012)
Peer reviewed yes
Publisher JohnWiley & Sons, Inc. ((United States) Hoboken)
issn 0021-9967
Publication status Publié
Affiliation UCL - SSS/IONS/CEMO - Pôle Cellulaire et moléculaire
Keywords HNF-6 ; OC-2 ; OC-3 ; Embryonic development ; Diencephalon ; 3D reconstructions of CNS nuclei
Links
  1. Akins Michael R., Benson Deanna L., Greer Charles A., Cadherin expression in the developing mouse olfactory system, 10.1002/cne.21270
  2. Andrews Gracie L, Yun Kyuson, Rubenstein John L.R, Mastick Grant S, Dlx transcription factors regulate differentiation of dopaminergic neurons of the ventral thalamus, 10.1016/s1044-7431(03)00016-2
  3. Rubenstein J. L. R., Briscoe J., Sussel L., Serup P., Hartigan-O'Connor D., Jessell T. M., Ericson J., 10.1038/19315
  4. Bulfone, J Neurosci, 13, 3155 (1993)
  5. Burglin, Int J Dev Biol, 46, 115 (2002)
  6. Carriere C, Plaza S, Martin P, Quatannens B, Bailly M, Stehelin D, Saule S, Characterization of quail Pax-6 (Pax-QNR) proteins expressed in the neuroretina., 10.1128/mcb.13.12.7257
  7. Cheong, Clin Cancer Res, 9, 5018 (2003)
  8. Clotman, Development, 129, 1819 (2002)
  9. Clotman F., Control of liver cell fate decision by a gradient of TGF  signaling modulated by Onecut transcription factors, 10.1101/gad.340305
  10. Cobos Inma, Broccoli Vania, Rubenstein John L.R., The vertebrate ortholog ofAristaless is regulated byDlx genes in the developing forebrain, 10.1002/cne.20405
  11. Contini M., Raviola E., GABAergic synapses made by a retinal dopaminergic neuron, 10.1073/pnas.0337681100
  12. Dahlström, Acta Physiol Scand, 62, 1 (1964)
  13. Dellovade Tammy L., Pfaff Donald W., Schwanzel-Fukuda Marlene, Olfactory bulb development is altered in small-eye (Sey) mice, 10.1002/(sici)1096-9861(19981221)402:3<402::aid-cne8>3.0.co;2-0
  14. Demyanenko Galina P., Shibata Yoichiro, Maness Patricia F., Altered distribution of dopaminergic neurons in the brain of L1 null mice, 10.1016/s0165-3806(00)00129-2
  15. Luk�s Zdenek, Viklick� Vladim�r, Dr�ber Pavel, Dr�berov� E., Ivanyi Dagmar, Expression of class III ?-tubulin in normal and neoplastic human tissues, 10.1007/s004180050222
  16. Ferguson Kerry L, McClellan Kelly A, Vanderluit Jacqueline L, McIntosh William C, Schuurmans Carol, Polleux Franck, Slack Ruth S, A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration, 10.1038/sj.emboj.7600887
  17. Ferran J.L., de Oliveira E. Dutra, Merchán P., Sandoval J.E., Sánchez-Arrones L., Martínez-De-La-Torre M., Puelles L., Genoarchitectonic profile of developing nuclear groups in the chicken pretectum, 10.1002/cne.22115
  18. Francius C., Clotman F., Dynamic expression of the Onecut transcription factors HNF-6, OC-2 and OC-3 during spinal motor neuron development, 10.1016/j.neuroscience.2009.09.076
  19. Grimm J., Mueller A., Hefti F., Rosenthal A., Molecular basis for catecholaminergic neuron diversity, 10.1073/pnas.0405340101
  20. Haworth Kim E., Latinkic Branko, Expression of Xenopus tropicalis HNF6/Onecut-1, 10.1387/ijdb.072472ke
  21. Hodge Liberty K., Klassen Matthew P., Han Bao-Xia, Yiu Glenn, Hurrell Joanna, Howell Audrey, Rousseau Guy, Lemaigre Frederic, Tessier-Lavigne Marc, Wang Fan, Retrograde BMP Signaling Regulates Trigeminal Sensory Neuron Identities and the Formation of Precise Face Maps, 10.1016/j.neuron.2007.07.010
  22. Hong Sung-Kook, Kim Cheol-Hee, Yoo Kyeong-Won, Kim Hyung-Seok, Kudoh Tetsuhiro, Dawid Igor B., Huh Tae-Lin, Isolation and expression of a novel neuron-specific onecut homeobox gene in zebrafish, 10.1016/s0925-4773(01)00647-5
  23. Jacquemin Patrick, Lannoy Vincent J., Rousseau Guy G., Lemaigre Frédéric P., OC-2, a Novel Mammalian Member of the ONECUT Class of Homeodomain Transcription Factors Whose Function in Liver Partially Overlaps with That of Hepatocyte Nuclear Factor-6, 10.1074/jbc.274.5.2665
  24. Jacquemin P., Durviaux S. M., Jensen J., Godfraind C., Gradwohl G., Guillemot F., Madsen O. D., Carmeliet P., Dewerchin M., Collen D., Rousseau G. G., Lemaigre F. P., Transcription Factor Hepatocyte Nuclear Factor 6 Regulates Pancreatic Endocrine Cell Differentiation and Controls Expression of the Proendocrine Gene ngn3, 10.1128/mcb.20.12.4445-4454.2000
  25. Jacquemin Patrick, Lemaigre Frédéric P, Rousseau Guy G, The Onecut transcription factor HNF-6 (OC-1) is required for timely specification of the pancreas and acts upstream of Pdx-1 in the specification cascade, 10.1016/s0012-1606(03)00115-5
  26. Kania Artur, Johnson Randy L, Jessell Thomas M, Coordinate Roles for LIM Homeobox Genes in Directing the Dorsoventral Trajectory of Motor Axons in the Vertebrate Limb, 10.1016/s0092-8674(00)00022-2
  27. Kao Hung-Teh, Li Ping, Chao Helen M., Janoschka Stephen, Pham Kara, Feng Jian, Mcewen Bruce S., Greengard Paul, Pieribone Vincent A., Porton Barbara, Early involvement of synapsin III in neural progenitor cell development in the adult hippocampus, 10.1002/cne.21643
  28. Lannoy Vincent J., Bürglin Thomas R., Rousseau Guy G., Lemaigre Frédéric P., Isoforms of Hepatocyte Nuclear Factor-6 Differ in DNA-binding Properties, Contain a Bifunctional Homeodomain, and Define the New ONECUT Class of Homeodomain Proteins, 10.1074/jbc.273.22.13552
  29. Margagliotti Sabrina, Clotman Frédéric, Pierreux Christophe E., Beaudry Jean-Bernard, Jacquemin Patrick, Rousseau Guy G., Lemaigre Frédéric P., The Onecut transcription factors HNF-6/OC-1 and OC-2 regulate early liver expansion by controlling hepatoblast migration, 10.1016/j.ydbio.2007.09.013
  30. Marín Faustino, Herrero María-Trinidad, Vyas Sheela, Puelles Luis, Ontogeny of tyrosine hydroxylase mRNA expression in mid- and forebrain: Neuromeric pattern and novel positive regions, 10.1002/dvdy.20467
  31. Mastick Grant S., Andrews Gracie L., Pax6 Regulates the Identity of Embryonic Diencephalic Neurons, 10.1006/mcne.2000.0924
  32. Matsunami Hiroaki, Takeichi Masatoshi, Fetal Brain Subdivisions Defined by R- and E-Cadherin Expressions: Evidence for the Role of Cadherin Activity in Region-Specific, Cell–Cell Adhesion, 10.1006/dbio.1995.8029
  33. Merlo Giorgio R., Mantero Stefano, Zaghetto Ambra A., Peretto Paolo, Paina Sara, Gozzo Marianna, The role of Dlx homeogenes in early development of the olfactory pathway, 10.1007/s10735-007-9154-x
  34. Mitrofanis J., Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta, 10.1016/j.neuroscience.2004.08.017
  35. Moore K Lookingland K 2000 www.acnp.org/g4/GN401000022/CH.html
  36. Nakagawa, J Neurosci, 21, 2711 (2001)
  37. Nguyen Duc N.T., Rohrbaugh Margaret, Lai Zhi-Chun, The Drosophila homolog of Onecut homeodomain proteins is a neural-specific transcriptional activator with a potential role in regulating neural differentiation, 10.1016/s0925-4773(00)00431-7
  38. Nural Hikmet F., Mastick Grant S., Pax6 guides a relay of pioneer longitudinal axons in the embryonic mouse forebrain, 10.1002/cne.20317
  39. Otim Ochan, Amore Gabriele, Minokawa Takuya, McClay David R., Davidson Eric H., SpHnf6, a transcription factor that executes multiple functions in sea urchin embryogenesis, 10.1016/j.ydbio.2004.05.033
  40. Otim Ochan, Hinman Veronica F., Davidson Eric H., Expression of AmHNF6, a sea star orthologue of a transcription factor with multiple distinct roles in sea urchin development, 10.1016/j.modgep.2004.09.009
  41. Pierreux Christophe E., Vanhorenbeeck Vinciane, Jacquemin Patrick, Lemaigre Frédéric P., Rousseau Guy G., The Transcription Factor Hepatocyte Nuclear Factor-6/Onecut-1 Controls the Expression of Its Paralog Onecut-3 in Developing Mouse Endoderm, 10.1074/jbc.m409038200
  42. Pierreux Christophe E., Poll Aurélie V., Kemp Caroline R., Clotman Frédéric, Maestro Miguel A., Cordi Sabine, Ferrer Jorge, Leyns Luc, Rousseau Guy G., Lemaigre Frédéric P., The Transcription Factor Hepatocyte Nuclear Factor-6 Controls the Development of Pancreatic Ducts in the Mouse, 10.1053/j.gastro.2005.12.005
  43. Poll A. V., Pierreux C. E., Lokmane L., Haumaitre C., Achouri Y., Jacquemin P., Rousseau G. G., Cereghini S., Lemaigre F. P., A vHNF1/TCF2-HNF6 Cascade Regulates the Transcription Factor Network That Controls Generation of Pancreatic Precursor Cells, 10.2337/diabetes.55.01.06.db05-0681
  44. Prakash N., Wurst W., Development of dopaminergic neurons in the mammalian brain, 10.1007/s00018-005-5387-6
  45. Prakash Nilima, Wurst Wolfgang, Genetic networks controlling the development of midbrain dopaminergic neurons : Genetic control of midbrain dopaminergic neuron development, 10.1113/jphysiol.2006.113464
  46. Rousseau, Bull Mem Acad R Med Belg, 158, 207 (2003)
  47. Sammeta Neeraja, McClintock Timothy S., Chemical stress induces the unfolded protein response in olfactory sensory neurons, 10.1002/cne.22305
  48. Sanghera Manjit K., Anselmo-Franci Janete, McCann Samuel M., Effect of Medial Zona Incerta Lesions on the Ovulatory Surge of Gonadotrophins and Prolactin in the Rat, 10.1159/000125931
  49. Sasakura Yasunori, Makabe Kazuhiro W., A gene encoding a new ONECUT class homeodomain protein in the ascidian Halocynthia roretzi functions in the differentiation and specification of neural cells in ascidian embryogenesis, 10.1016/s0925-4773(01)00352-5
  50. Singh Sushma R., Hileman Stanley M., Connors John M., McManus Christina J., Coolen Lique M., Lehman Michael N., Goodman Robert L., Estradiol Negative Feedback Regulation by Glutamatergic Afferents to A15 Dopaminergic Neurons: Variation with Season, 10.1210/en.2009-0432
  51. Sita Luciane V., Elias Carol F., Bittencourt Jackson C., Dopamine and melanin-concentrating hormone neurons are distinct populations in the rat rostromedial zona incerta, 10.1016/s0006-8993(03)02345-x
  52. Sita L.V., Elias C.F., Bittencourt J.C., Connectivity pattern suggests that incerto-hypothalamic area belongs to the medial hypothalamic system, 10.1016/j.neuroscience.2007.07.010
  53. Stanke Jennifer, Moose Holly E., El-Hodiri Heithem M., Fischer Andy J., Comparative study of Pax2 expression in glial cells in the retina and optic nerve of birds and mammals, 10.1002/cne.22335
  54. Thaler Joshua P, Koo Sonya J, Kania Artur, Lettieri Karen, Andrews Shane, Cox Christopher, Jessell Thomas M, Pfaff Samuel L, A Postmitotic Role for Isl-Class LIM Homeodomain Proteins in the Assignment of Visceral Spinal Motor Neuron Identity, 10.1016/s0896-6273(04)00011-x
  55. Thor Stefan, Ericson Johan, Brännström Thomas, Edlund Thomas, The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat, 10.1016/0896-6273(91)90334-v
  56. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L., Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes, 10.1016/0092-8674(94)90027-2
  57. Vanhorenbeeck Vinciane, Jacquemin Patrick, Lemaigre Frédéric P., Rousseau Guy G., OC-3, a Novel Mammalian Member of the ONECUT Class of Transcription Factors, 10.1006/bbrc.2002.6760
  58. Vanhorenbeeck Vinciane, Jenny Marjorie, Cornut Jean-François, Gradwohl Gérard, Lemaigre Frédéric P., Rousseau Guy G., Jacquemin Patrick, Role of the Onecut transcription factors in pancreas morphogenesis and in pancreatic and enteric endocrine differentiation, 10.1016/j.ydbio.2007.02.027
  59. Vitalis, J Neurosci, 20, 6501 (2000)
  60. Ye Weilan, Shimamura Kenji, Rubenstein John L.R, Hynes Mary A, Rosenthal Arnon, FGF and Shh Signals Control Dopaminergic and Serotonergic Cell Fate in the Anterior Neural Plate, 10.1016/s0092-8674(00)81437-3
Bibliographic reference Espana-Bessy, Agnès ; Clotman, Frédéric. Onecut transcription factors are required for the second phase of development of the A13 dopaminergic nucleus in the mouse. In: The Journal of Comparative Neurology, Vol. 520, no. 7, p. 1424 -1441 (2012)
Permanent URL http://hdl.handle.net/2078.1/109029