Temporal-spatial changes in Sonic Hedgehog expression and signaling reveal different potentials of ventral mesencephalic progenitors to populate distinct ventral midbrain nuclei

Neural Development

Volumn 6, Issue 1, 2011, Pages

  Blaess, Sandra ^a,b   Bodea, Gabriela O ^b   Kabanova, Anna ^b   Chanet, Soline ^c   Mugniery, Emilie ^d   Derouiche, Amin ^b,e   Stephen, Daniel ^a   Joyner, Alexandra L ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c CNRS   (France)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; GLI PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; RNA; SHH PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN;

ANIMAL; ARTICLE; ASTROCYTE; BIOSYNTHESIS; BRAIN MAPPING; CELL DIFFERENTIATION; CYTOLOGY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; MESENCEPHALON; MOUSE; NERVE CELL; NEURAL STEM CELL; OCULOMOTOR NERVE; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; RED NUCLEUS; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

ANIMALS; ASTROCYTES; BRAIN MAPPING; CELL DIFFERENTIATION; DOPAMINE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MESENCEPHALON; MICE; NEURAL STEM CELLS; NEURONS; OCULOMOTOR NERVE; PREGNANCY; RED NUCLEUS; RNA; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

EID: 79959262926     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-6-29     Document Type: Article

References (43)

1. Bjorklund A, Dunnett SB. Dopamine neuron systems in the brain: an update. Trends Neurosci 2007, 30:194-202. 10.1016/j.tins.2007.03.006, 17408759.
2. Bjorklund A, Dunnett SB. Fifty years of dopamine research. Trends Neurosci 2007, 30:185-187. 10.1016/j.tins.2007.03.004, 17397938.
3. Smidt MP, Burbach JP. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 2007, 8:21-32. 10.1038/nrn2039, 17180160.
4. Dagher A, Robbins TW. Personality, addiction, dopamine: insights from Parkinson's disease. Neuron 2009, 61:502-510. 10.1016/j.neuron.2009.01.031, 19249271.
5. Ono Y, Nakatani T, Sakamoto Y, Mizuhara E, Minaki Y, Kumai M, Hamaguchi A, Nishimura M, Inoue Y, Hayashi H, Takahashi J, Imai T. Differences in neurogenic potential in floor plate cells along an anteroposterior location: midbrain dopaminergic neurons originate from mesencephalic floor plate cells. Development 2007, 134:3213-3225. 10.1242/dev.02879, 17670789.
6. Kittappa R, Chang WW, Awatramani RB, McKay RD. The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol 2007, 5:e325. 10.1371/journal.pbio.0050325, 2121110, 18076286.
7. Bonilla S, Hall AC, Pinto L, Attardo A, Gotz M, Huttner WB, Arenas E. Identification of midbrain floor plate radial glia-like cells as dopaminergic progenitors. Glia 2008, 56:809-820. 10.1002/glia.20654, 18351630.
8. Joksimovic M, Yun BA, Kittappa R, Anderegg AM, Chang WW, Taketo MM, McKay RD, Awatramani RB. Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis. Nat Neurosci 2009, 12:125-131. 10.1038/nn.2243, 19122665.
9. Joksimovic M, Anderegg A, Roy A, Campochiaro L, Yun B, Kittappa R, McKay R, Awatramani R. Spatiotemporally separable Shh domains in the midbrain define distinct dopaminergic progenitor pools. Proc Natl Acad Sci USA 2009, 106:19185-19190. 10.1073/pnas.0904285106, 2776440, 19850875.
10. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002, 129:4753-4761.
11. Bai CB, Stephen D, Joyner AL. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 2004, 6:103-115. 10.1016/S1534-5807(03)00394-0, 14723851.
12. Ahn S, Joyner AL. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516. 10.1016/j.cell.2004.07.023, 15315762.
13. Blaess S, Corrales JD, Joyner AL. Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 2006, 133:1799-1809. 10.1242/dev.02339, 16571630.
14. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999, 21:70-71. 10.1038/5007, 9916792.
15. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 2001, 1:4. 10.1186/1471-213X-1-4, 31338, 11299042.
16. Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528. 10.1016/j.cell.2004.07.024, 15315763.
17. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 2000, 25:139-140. 10.1038/75973, 10835623.
18. Kimmel RA, Turnbull DH, Blanquet V, Wurst W, Loomis CA, Joyner AL. Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev 2000, 14:1377-1389. 316660, 10837030.
19. Sloan-Kettering Institute: Laboratory Protocols. , http://www.mskcc.org/mskcc/html/77387.cfm
20. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2007, Academic Press, Elsevier, 3.
21. Wallen A, Zetterstrom RH, Solomin L, Arvidsson M, Olson L, Perlmann T. Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp Cell Res 1999, 253:737-746. 10.1006/excr.1999.4691, 10585298.
22. Zervas M, Millet S, Ahn S, Joyner AL. Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 2004, 43:345-357. 10.1016/j.neuron.2004.07.010, 15294143.
23. Andersson E, Tryggvason U, Deng Q, Friling S, Alekseenko Z, Robert B, Perlmann T, Ericson J. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 2006, 124:393-405. 10.1016/j.cell.2005.10.037, 16439212.
24. Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol 1994, 162:402-413. 10.1006/dbio.1994.1097, 8150204.
25. Legue E, Joyner AL. Genetic fate mapping using site-specific recombinases. Methods Enzymol 2010, 477:153-181.
26. Feil R, Wagner J, Metzger D, Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 1997, 237:752-757. 10.1006/bbrc.1997.7124, 9299439.
27. Robinson SP, Langan-Fahey SM, Johnson DA, Jordan VC. Metabolites, pharmacodynamics, and pharmacokinetics of tamoxifen in rats and mice compared to the breast cancer patient. Drug Metab Dispos 1991, 19:36-43.
28. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 1998, 8:1323-1326. 10.1016/S0960-9822(07)00562-3, 9843687.
29. Sgaier SK, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL. Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 2005, 45:27-40.
30. Nakatani T, Kumai M, Mizuhara E, Minaki Y, Ono Y. Lmx1a and Lmx1b cooperate with Foxa2 to coordinate the specification of dopaminergic neurons and control of floor plate cell differentiation in the developing mesencephalon. Dev Biol 2010, 339:101-113. 10.1016/j.ydbio.2009.12.017, 20035737.
31. Prakash N, Puelles E, Freude K, Trumbach D, Omodei D, Di Salvio M, Sussel L, Ericson J, Sander M, Simeone A, Wurst W. Nkx6-1 controls the identity and fate of red nucleus and oculomotor neurons in the mouse midbrain. Development 2009, 136:2545-2555. 10.1242/dev.031781, 2729334, 19592574.
32. Nakatani T, Minaki Y, Kumai M, Ono Y. Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 2007, 134:2783-2793. 10.1242/dev.02870, 17611227.
33. Bentivoglio M, Morelli M. Dopamine. Handbook of Chemical Neuroanatomy 2005, 21. Amsterdam: Elsevier, Dunnett S, Bentivoglio M, Björklund A, Hökfelt T, 1, [Björklund A, Hökfelt T (Series Editor): The Handbook of Chemical Neuroanatomy]..
34. Bayer SA, Wills KV, Triarhou LC, Ghetti B. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp Brain Res 1995, 105:191-199.
35. Derouiche A, Frotscher M. Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: evidence for transmitter degradation. Brain Res 1991, 552:346-350. 10.1016/0006-8993(91)90103-3, 1680531.
36. Martinez-Hernandez A, Bell KP, Norenberg MD. Glutamine synthetase: glial localization in brain. Science 1977, 195:1356-1358. 10.1126/science.14400, 14400.
37. Bignami A, Eng LF, Dahl D, Uyeda CT. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 1972, 43:429-435. 10.1016/0006-8993(72)90398-8, 4559710.
38. Stecca B, Ruiz IAA. Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J Mol Cell Biol 2:84-95.
39. Dessaud E, McMahon AP, Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 2008, 135:2489-2503. 10.1242/dev.009324, 18621990.
40. Ribes V, Balaskas N, Sasai N, Cruz C, Dessaud E, Cayuso J, Tozer S, Yang LL, Novitch B, Marti E, Briscoe J. Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev 24:1186-1200.
41. Fedtsova N, Turner EE. Signals from the ventral midline and isthmus regulate the development of Brn3.0-expressing neurons in the midbrain. Mech Dev 2001, 105:129-144. 10.1016/S0925-4773(01)00399-9, 11429288.
42. Perez-Balaguer A, Puelles E, Wurst W, Martinez S. Shh dependent and independent maintenance of basal midbrain. Mech Dev 2009, 126:301-313. 10.1016/j.mod.2009.03.001, 19298856.
43. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773. 10.1016/j.neuron.2008.01.022, 18341995.