Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia

Journal of Comparative Neurology

Volumn 461, Issue 2, 2003, Pages 151-165

  Yun, Kyuson ^a   Garel, Sonia ^a   Fischman, Seth ^a   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CNS development; Cortical axons; Dorsoventral patterning; Gsh1; Gsh2; LGE; Striatum; Telencephalon; Ventral pallium

Indexed keywords

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN REGION; CELL MIGRATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; EMBRYO; GENE FUNCTION; GENE MUTATION; HETEROTOPIA; HOMEOBOX; HYPOPLASIA; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; STEM CELL; TELENCEPHALON;

AFFERENT PATHWAYS; ANIMALS; BIOLOGICAL MARKERS; BODY PATTERNING; CELL MOVEMENT; CEREBRAL CORTEX; CHORISTOMA; CORPUS STRIATUM; DOPAMINE; EFFERENT PATHWAYS; GENES, HOMEOBOX; GROWTH CONES; HOMEODOMAIN PROTEINS; INTERNEURONS; MICE; MICE, KNOCKOUT; MUTATION; OLFACTORY BULB; RECEPTORS, DOPAMINE D2; STEM CELLS;

EID: 0037573477     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10685     Document Type: Article

References (53)

1. Anderson S, Qiu M, Bulfone A, Eisenstat D, Meneses JJ, Pedersen RA, Rubenstein JLR. 1997. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late-born striatal cells. Neuron 19:27-37.
2. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JLR. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
3. Bayer SA, Altman J, Russo RJ, Dai XF, Simmons JA. 1991. Cell migration in the rat embryonic neocortex. J Comp Neurol 307:499-516.
4. Bulfone A, Kim HJ, Puelles L, Porteus MH, Grippo JF, Rubenstein JL. 1993. The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev 40:129-140.
5. Casarosa S, Fode C, Guillemot F. 1999. Mashl regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
6. Corbin JG, Gaiano N, Machold RP, Langston A, Fishell G. 2000. The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development 127:5007-5020.
7. Crossley PH, Martinez S, Ohkubo Y, Rubenstein JLR. 2001. Evidence that coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon define patterning centers for the telencephalic and optic vesicles. Neuroscience 108:183-206.
8. Dellovade TL, Pfaff DW, Schwanzel-Fukuda M. 1998. Olfactory bulb development is altered in small-eye (Sey) mice. J Comp Neurol 402:402-418.
9. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JLR. 1999. DLX-1, DLX-2 and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217-237.
10. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F. 2000. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80.
11. Garel S, Yun K, Grosschedl R, Rubenstein JLR. 2002. Topography of connections between the neocortex and thalamus is regulated by intermediate structures. Development 129:5621-5634.
12. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133-139.
13. Godement P, Vanselow J, Thanos S, Bonhoeffer F. 1987. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101:697-713.
14. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. 2000. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22:6309-6314.
15. Graybiel AM. 2000. The basal ganglia. Curr Biol 10:R509-R511.
16. Grigoriou M, Tucker AS, Sharpe PT, Pachnis V. 1998. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 125:2063-2074.
17. Hallonet M, Hollemann T, Wehr R, Jenkins NA, Copeland NG, Pieler T, Gruss P. 1998. Vax1 is a novel homeobox-containing gene expressed in the developing anterior ventral forebrain. Development 125:2599-2610.
18. Hallonet M, Hollemann T, Pieler T, Gruss P. 1999. Vax1, a novel homeobox-containing gene, directs development of the basal forebrain and visual system. Genes Dev 13:3106-3114.
19. Heimer L, Zahm DS, Alheid GF. 1995. Basal ganglia. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press.
20. Hsieh-Li HM, Witte DP, Szucsik JC, Weinstein M, Li H, Potter SS. 1995. Gsh-2, a murine homeobox gene expressed in the developing brain. Mech Dev 50:177-186.
21. Li H, Zeitler PS, Valerius MT, Small K, Potter SS. 1996. Gsh-1, an orphan Hox gene, is required for normal pituitary development. EMBO J 15:714-724.
22. Long JE, Garel S, Depew MJ, Tobet S, Rubenstein JLR. 2003. DLX5 regulates development of peripheral and central components of the olfactory system. J Neurosci 23:568-578.
23. Lopez-Bendito G, Chan CH, Mallamaci A, Parnavelas J, Molnar Z. 2002. Role of Emx2 in the development of the reciprocal connectivity between cortex and thalamus. J Comp Neurol 451:153-169.
24. Marín O, Rubenstein JLR. 2001. A long, remarkable journey: cellular and molecular mechanisms of tangential migration in the telencephalon. Nat Neurosci Rev 2:780-790.
25. Marín O, Rubenstein JLR. 2002. Patterning, regionalization and cell differentiation in the forebrain. In: Rossant J, Tam P, editors. Mouse development. San Diego: Academic Press. p 75-106.
26. Marín O, Rubenstein JLR. 2003. Cell migration in the forebrain. Annu Rev Neurosci. Feb 26 [epub ahead of print].
27. Marín O, Anderson SA, Rubenstein JLR. 2000. Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076.
28. Marín O, Baker J, Puelles L, Rubenstein JLR. 2002. Patterning of the basal telencephalon and hypothalamus is essential for guidance of cortical projections. Development 129:761-773.
29. Marín O, Plump AS, Flames N, Sanchez-Camacho C, Tessier-Lavigne M, Rubenstein JL. 2003. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit 1/2-independent repulsion and cortical attraction. Development 130:1889-1901.
30. Martinez-Barbera JP, Rodriguez TA, Beddington RS. 2000. The homeobox gene Hesx1 is required in the anterior neural ectoderm for normal forebrain formation Dev Biol 223:422-430.
31. Mathers PH, Grinberg A, Mahon KA, Jamrich M. 1997. The Rx homeobox gene is essential for vertebrate eye development. Nature 387:603-607.
32. Metin C, Deleglise D, Serafini T, Kennedy TE, Tessier-Lavigne M. 1997. A role for netrin-1 in the guidance of cortical efferents. Development 124:5063-5074.
33. Miura H, Yanazawa M, Kato K, Kitamura K. 1997. Expression of a novel aristaless related homeobox gene 'Arx' in the vertebrate telencephalon, diencephalon and floor plate. Mech Dev 65:99-109.
34. Muhr J, Andersson E, Persson M, Jessell TM, Ericson J. 2001. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104:861-873.
35. Oliver G, Mailhos A, Wehr R, Copeland NG, Jenkins NA, Gruss P. 1995. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121:4045-4055.
36. Porteus MH, Bulfone A, Liu JK, Puelles L, Lo LC, Rubenstein JLR. 1994. DLX-2, MASH-1, MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J Neurosci 14:6370-6383.
37. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL. 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.
38. Qiu M, Bulfone A, Martinez S, Meneses JJ, Shimamura K, Pedersen RA, Rubenstein JLR. 1995. Role of Dlx-2 in head development and evolution: null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes and Development 9:2523-2538.
39. Shimamura K, Rubenstein JLR. 1997. Inductive interactions direct early regionalization of the mouse forebrain. Development 124:2709-2718.
40. Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JLR. 1995. Longitudinal organization of the anterior neural plate and neural tube. Development 121:3923-3933.
41. Simeone A, Acampora D, Gulisano M, Stornaiuolo A, Boncinelli E. 1992. Nested expression domains of four homeobox genes in developing rostral brain. Nature 358:687-690.
42. Simeone A, Acampora D, Mallamaci A, Stornaiuolo A, D'Apice MR, Nigro V, Boncinelli E. 1993. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 12:2735-2747.
43. Stenman J, Toresson H, Campbell K. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174.
44. Stoykova A, Treichel D, Hallonet M, Gruss P. 2000. Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J Neurosci 20:8042-8050.
45. Sussel L, Kimura S, Rubenstein JLR. 1999. Loss ofNkx2.1 homeobox gene function results in a ventral to dorsal respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359-3370.
46. Szucsik JC, Witte DP, Li H, Pixley SK, Small KM, Potter SS. 1997. Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev Biol 191:230-242.
47. Tole S, Ragsdale CW, Grove EA. 2000. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes (J). Dev Biol 217:254-265.
48. Toresson H, Campbell K. 2001. A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128:4769-4780.
49. Toresson H, Potter SS, Campbell K. 2000. Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127:4361-4371.
50. Valerius MT, Li H, Stock JL, Weinstein M, Kaur S, Singh G, Potter SS. 1995. Gsh-1: a novel murine homeobox gene expressed in the central nervous system. Dev Dyn 203:337-351.
51. Wichterle H, Alvarez-Dolado M, Erskine L, Alvarez-Buylla A. 2003. Permissive corridor and diffusible gradients direct medial ganglionic eminence cell migration to the neocortex. Proc Natl Acad Sci U S A 100:727-732.
52. Yun K, Potter S, Rubenstein JL. 2001. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128:193-205.
53. Yun K, Fischman S, Johnson J, Hrabe de Angelis M, Weinmaster G, Rubenstein JLR. 2002. Modulation of the Notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129:5029-5040.