Topography of somatostatin gene expression relative to molecular progenitor domains during ontogeny of the mouse hypothalamus

Frontiers in Neuroanatomy

Volumn , Issue FEB, 2011, Pages 1-15

  Morales Delgado, Nicanor ^a,b   Merchan, Paloma ^b   Bardet, Sylvia M ^b,c   Ferrán, José L ^b   Puelles, Luis ^b   Díaz, Carmen ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

^c UNIVERSITY OF LIMOGES   (France)

Author keywords

Dlk5; Forebrain; Hypothalamus; In situ hybridization; Nkx2.1; Otp; Shh; Sst

Indexed keywords

MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CELL GROWTH; CELL MIGRATION; CELL POPULATION; CELLULAR DISTRIBUTION; CEREBRAL PEDUNCLE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DEVELOPMENTAL STAGE; DISTAL LESS 5 GENE; EMBRYO; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCATION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; IN SITU HYBRIDIZATION; MOUSE; NK2 HOMEOBOX 1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; ORTHOPEDIA GENE; PARAVENTRICULAR THALAMIC NUCLEUS; SOMATOSTATIN GENE; SONIC HEDGEHOG GENE;

EID: 84855339889     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2011.00010     Document Type: Article

References (69)

1. Acampora, D., Postiglione, M. P., Avantaggiato, V., Di Bonito, M., andSimeone, A. (2000). The role of Otx and Otp genes in brain development. Int. J. Dev. Biol. 44, 669-677.
2. Acampora, D., Postiglione, M. P., Avantaggiato, V., Di Bonito, M., Vaccarino, F. M., Michaud, J., and Simeone A. (1999). Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev. 13, 2787-2800.
3. Altman, J., and Bayer, S. A. (1978). Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. J. Comp. Neurol. 182, 945-971.
4. Altman, J., and Bayer, S. A. (1986). The development of the rat hypothalamus. Adv. Anat. Embryol. Cell Biol. 100, 1-178.
5. Altman, J., and Bayer, S. A. (1995). Atlas of Prenatal Rat Brain Development. Boca Raton: CRC Press.
6. Alvarez-Bolado, G., Zhou, X., Cecconi, F., and Gruss, P. (2000). Expression of Foxb1 reveals two strategies for the formation of nuclei in the developing ventral diencephalon. Dev. Neurosci. 22, 197-206.
7. Anderson, S. A., Marín, O., Horn, C., Jennings, K., and Rubenstein, J. L. (2001). Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363.
8. Bardet, S. M. (2007). Organización morfológica y citogenética del hipotálamo del pollo sobre base de mapas moleculares. Doctoral thesis, Neuroscience Programme, University of Murcia, Spain.
9. Bardet, S. M., Cobos, I., Puelles, E., Martínez de-la-Torre, M, and Puelles, L. (2006). The chicken lateral septal organ and other circumventricular organs form in the striatal domain, abutting the molecular striatopallidal border. J. Comp. Neurol. 499, 745-767.
10. Bardet, S. M., Martínez de-la-Torre, M, Northcutt, R. G., Rubenstein, J. L., and Puelles, L. (2008). Conserved pattern of OTP-positive cells in the paraventricular nucleus and other hypothalamic sites of tetrapods. Brain Res. Bull. 75, 231-235.
11. Bendotti, C., Hohmann, C., Forloni, G., Reeves, R., Coyle, J. T., and Oster-Granite, M. L. (1990). Developmental expression of somatostatin in mouse brain. II. In situ hybridization. Brain Res. Dev. Brain Res. 53, 26-39.
12. Bertrand, N., and Dahmane, N. (2006). Sonic hedgehog signaling in forebrain development and its interactions with pathways that modify its effects. Trends Cell Biol. 16, 597-605.
13. Blechman, J., Borodovsky, N., Eisenberg, M., Nabel-Rosen, H., Grimm, J., and Levkowitz, G. (2007). Specification of hypothalamic neurons by dual regulation of the homeodomain protein Orthopedia. Development 134, 4417-4426.
14. Brazeau, P., Vale, W., Burgus, R., Ling, N., Butcher, M., Rivier, J., and Guillemin, R. (1973). Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science 179, 77-79.
15. Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R., and Rubenstein, J. L. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13, 3155-3172.
16. Caqueret, A., Yang, C., Duplan, S., Boucher, F., and Michaud, J. L. (2005). Looking for trouble: a search for developmental defects of the hypothalamus. Horm. Res. 64, 222-230.
17. Cobos, I., Shimamura, K., Rubenstein, J. L., Martinez, S., and Puelles, L. (2001). Fate map of the avian anterior forebrain at the four-somite stage, based on the analysis of quail-chick chimeras. Dev. Biol. 239, 46-67.
18. Cotter, J. R., and Laemle, L. K. (1987). Distribution of somatostatinlike immunoreactivity in the brain of the little brown bat (Myotis lucifugus). Am. J. Anat. 180, 280-294.
19. Dale, J. K., Vesque, C., Lints, T. J., Sampath, T. K., Furley, A., Dodd, J., and Placzek, M. (1997). Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90, 257-269
20. Dierickx, K., and Vandesande, F. (1979). Immunocytochemical localization of somatostatin-containing neurons in the rat hypothalamus. Cell Tissue Res. 201, 349-359.
21. Ericson, J., Muhr, J., Jessell, T. M., and Edlund, T. (1995). Sonic hedgehog: a common signal for ventral patterning along the rostrocaudal axis of the neural tube. Int. J. Dev. Biol. 39, 809-816.
22. Fan, C.-M., Kuwana, E., Bulfone, A., Fletcher, C. F., Copeland, N., Jenkins, A., Crews, S., Martinez, S., Puelles, L., Rubenstein, J. L. R., and Tessier-Lavigne, M. (1996). Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome. Mol. Cell. Neurosci. 7, 1-16.
23. Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L. R., Puelles, L., and Marín, O. (2007). Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27, 9682-9695.
24. Forloni, G., Hohmann, C., and Coyle, J. T. (1990). Developmental expression of somatostatin in mouse brain. I. Immunocytochemical studies. Brain Res. Dev. Brain Res. 53, 6-25.
25. Fuxe, K., Agnati, L. F., Kalia, M., Goldstein, M., Andersson, K., and Härfstrand, A. (1985). "The dopaminergic systems in the brain and in the pituitary," in Basic and Clinical Aspects of Neuroscience, eds E. Fluckiger, E. Muller, and M. Thorner (Amsterdam: Springer Press), 11-25.
26. García-Moreno, F., Pedraza, M., Di Giovannantonio, L. G., Di Salvio, M., López-Mascaraque, L., Simeone, A., and De Carlos, J. A. (2010). A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat. Neurosci. 13, 680-689.
27. Geng, X., Speirs C., Lagutin O., Inbal A., Liu W., Solnica-Krezel L., Jeong Y., Epstein D., and Oliver G. (2008). Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev. Cell 15, 236-247.
28. Goshu E., Jin H., Lovejoy J., Marion J.-F., Michaud J. L., and Fan C.-M. (2004). Sim2 contributes to neuroendocrine hormone gene expression in the anterior hypothalamus. Mol. Endocrinol. 18, 1251-1262.
29. Gross, D. S., and Longer, J. D. (1979). Developmental correlation between hypothalamic somatostatin and hypophysial growth hormone. Cell Tissue Res. 202, 251-261.
30. Hallonet, M., Hollemann, T., Wehr, R., Jenkins, N. A., Copeland, N. G., Pieler, T., and Gruss, P. (1998). Vax1 is a novel homeobox-containing gene expressed in the developing anterior ventral forebrain. Development 125, 2599-2610.
31. Hidalgo-Sánchez, M., Martínez de-la-Torre, M, Alvarado-Mallart, R. M., and Puelles, L. (2005). Distinct preisthmic domain, defined by overlap of Otx2 and Pax2 expression domains in the chicken caudal midbrain. J. Comp. Neurol. 483, 17-29.
32. Hoffman, G. E., and Hayes, T. A. (1979). Somatostatin neurons and their projections in dog diencephalon. J. Comp. Neurol. 186, 371-391.
33. Johansson, O., Hökfelt, T., and Elde, R. P. (1984). Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13, 265-339.
34. Kimura, S., Hara, Y., Pineau, T., Fernandez-Salguero, P., Fox, C. H., Ward, J. M., and Gonzalez, F. J. (1996). The T/ebp null mouse: thyroid specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 10, 60-69.
35. Lagutin, O. V., Zhu, C. C., Kobayashi, D., Topczewski, J., Shimamura, K., Puelles, L., Russell, H. R. C., McKinnon, P. J., Solnica-Krezel, L., and Oliver, G. (2003). Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17, 368-379.
36. Lechan, R. M., and Fekete, C. (2006). The TRH neuron: a hypothalamic integrator of energy metabolism. Prog. Brain Res. 153, 209-235.
37. Le Verche, V., Kaindl, A. M., Verney, C., Csaba, Z., Peineau, S., Olivier, P., Adle-Biassette, H., Leterrier, C., Vitalis, T., Renaud, J., Dargent, B., and Gressens, P. (2009). The somatostatin 2A receptor is enriched in migrating neurons during rat and human brain development and stimulates migration and axonal outgrowth. PLoS ONE 4, e5509. doi: 10.1371/journal.pone.0005509
38. Martí, E., Takada, R., Bumcrot, D. A., Sasaki, H., and McMahon, A. P. (1995). Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121, 2537-2547.
39. Michaud, J. L. (2001). The developmental program of the hypothalamus and its disorders. Clin. Genet. 60, 255-263.
40. Nery, S., Fishell, G., and Corbin, J. G. (2002). The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5, 1279-1287.
41. Nieuwenhuys, R. (2009). The structural organization of the forebrain: a commentary on the papers presented at the 20th Annual Karger Workshop 'Forebrain Evolution in Fishes'. Brain Behav. Evol. 74, 77-85.
42. Nieuwenhuys, R., Voogd, J., and van Huijzen, C. (2008). "Development," in The Human Central Nervous System, 4th Edn. (Berlin/Heidelberg: Springer), 55-56.
43. Pabst, O., Herbrand, H., Takuma, N., and Arnold, H. H. (2000). NKX2 gene expression in neuroectoderm but not in mesendodermally derived structures depends on sonic hedgehog in mouse embryos. Dev. Genes Evol. 210,47-50.
44. Pera, E. M., and Kessel, M. (1997). Patterning of the chick forebrain anlage by the prechordal plate. Development 124, 4153-4162.
45. Puelles, L. (1995). A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav. Evol. 46, 319-337.
46. Puelles, L. (2001). Brain segmentation and forebrain development in amniotes. Brain Res. Bull. 55, 695-710.
47. Puelles, L., Amat, J. A., and Martínez de-la Torre, M.,. (1987). Segment-related, mosaic neurogenetic pattern in the forebrain and mesencephalon of early chick embryos. I. Topography of AChE-positive neuroblasts up to stage HH18. J. Comp. Neurol. 266, 147-268.
48. Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J., Smiga, S., and Rubenstein, J. L. (2000). Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol. 424, 409-438.
49. Puelles, L., Martinez, S., Martínez de-la-Torre, M, and Rubenstein, J. L. (2004). "Gene maps and related histogenetic domains in the forebrain and midbrain," in The Rat Nervous System, 3rd Edn., ed. G. Paxinos (San Diego: Elsevier), 3-25.
50. Puelles, L., Martínez de-la-Torre, M, Paxinos, G., Watson, C., and Martinez, S. (2007). The Chick Brain in Stereotaxic Coordinates. An Atlas Featuring Neuromeric Subdivisions and Mammalian Homologies. San Diego: Academic Press-Elsevier.
51. Puelles, L., and Rubenstein, J. L. (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci. 26, 469-476.
52. Rubenstein, J. L., Shimamura, K., Martinez, S., and Puelles, L. (1998). Regionalization of the prosencephalic neural plate. Annu. Rev. Neurosci. 21, 445-477.
53. Scanlan, N., Dufourny, L., and Skinner, D. C. (2003). Somatostatin-14 neurons in the ovine hypothalamus: colocalization with estrogen receptor alpha and somatostatin-28(1-12) immunoreactivity, and activation in response to estradiol. Biol. Reprod. 69, 1318-1324.
54. Schwanzel-Fukuda, M., and Pfaff, D. W. (1989). Origin of luteinizing hormone-releasing hormone neurons. Nature 338, 161-164.
55. Shimada, M., and Nakamura, T. (1973). Time of neuron origin in mouse hypothalamic nuclei. Exp. Neurol. 41, 163-173.
56. Shimamura, K., Hartigan, D. J., Martinez, S., Puelles, L., and Rubenstein, J. L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923-3933.
57. Shimamura, K., and Rubenstein, J. L. (1997). Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709-2718.
58. Shimogori, T., Lee, D. A., Miranda-Angulo, A., Yang, Y., Wang, H., Jiang, L., Yoshida, A. C., Kataoka, A., Mashiko, H., Avetisyan, M., Qi, L., Qian, J., and Blackshaw, S. (2010). A genomic atlas of mouse hypothalamic development. Nat. Neurosci. 13, 767-775.
59. Shiosaka, S., Takatsuki, K., Sakanaka, M., Inagaki, S., Takagi, H., Senba, E., Kawai, Y., Iida, H., Minagawa, H., Hara, Y., Matsuzaki, T., and Tohyama, M. (1982). Ontogeny of somatostatin-containing neuron system of the rat: immunohisto-chemical analysis. II. Forebrain and diencephalon. J. Comp. Neurol. 204, 211-224.
60. Shiosaka, S., Takatsuki, K., Sakanaka, M., Inagaki, S., Takagi, H., Senba, E., Kawai, Y., and Tohyama, M. (1981). Ontogeny of somatostatin-containing neuron system of the rat: immune-histochemical observations. I. Lower brainstem. J. Comp. Neurol. 203, 173-188.
61. Stühmer, T., Anderson, S. A., Ekker, M., and Rubenstein, J. L. R. (2002). Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129, 245-252.
62. Vale, W., Rivier, C., Brown, M., and Rivier, J. (1977). Pharmacology of thyrotropin releasing factor (TRF), luteinizing hormone releasing factor (LRF), and somatostatin. Adv. Exp. Med. Biol. 87, 123-156.
63. Viollet, C., Lepousez, G., Loudes, C., Videau, C., Simon, A., and Epelbaum, J. (2008). Somatostatinergic systems in brain: networks and functions. Mol. Cell. Endocrinol. 286, 75-87.
64. Wang, W., and Lufkin, T. (2000). The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev. Biol. 227, 432-449.
65. Wray, S., Grant, P., and Gainer, H. (1989). Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. Natl. Acad. Sci. U.S.A. 86, 8132-8136.
66. Yacubova, E., and Komuro, H. (2002). Stage-specific control of neuronal migration by somatostatin. Nature 415, 77-81.
67. Yee, C. L., Wang, Y., Anderson, S., Ekker, M., and Rubenstein, J. L. (2009). Arcuate nucleus expression of NKX2.1 and DLX and lineages expressing these transcription factors in neuropeptide Y(+), proopiomelanocortin(+), and tyrosine hydroxylase(+) neurons in neonatal and adult mice. J. Comp. Neurol. 517, 37-50.
68. Zhao, T., Szabó, N., Ma, J., Luo, L., Zhou, X., and Alvarez-Bolado, G. (2008). Genetic mapping of Foxb1-cell lineage shows migration from caudal diencephalon to telencephalon and lateral hypothalamus. Eur. J. Neurosci. 28, 1941-1955.
69. Zoli, M., Fuxe, K., Agnati, L. F., Härfstrand, A., Terenius, L., Toni, R., and Goldstein, M. (1986). "Computer-assisted morphometry of transmitter-identified neurons: new opening for understanding of peptide-monoamine interactions in the mediobasal hypothalamus," in Neurohistochemistry. Modern Methods and Applications, eds P. Panula, H. Päivarinta, and S. Soimila (New York: Alan R. Liss), 137-174.