Interactions of Wnt/β-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons

Journal of Neuroscience

Volumn 30, Issue 27, 2010, Pages 9280-9291

  Tang, Mianzhi ^a   Villaescusa, J Carlos ^b   Luo, Sarah X ^c   Guitarte, Camilla ^a   Lei, Simonia ^a   Miyamoto, Yasunori ^d   Taketo, Makoto M ^e   Arenas, Ernest ^b   Huang, Eric J ^a,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d OCHANOMIZU UNIVERSITY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; SONIC HEDGEHOG PROTEIN; TYROSINE 3 MONOOXYGENASE; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE PROGRESSION; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; GENE TARGETING; INTERNAL RIBOSOME ENTRY SITE; MESENCEPHALON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BETA CATENIN; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; DOPAMINE; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCEPHALON; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PYRIDINES; PYRIMIDINES; SIGNAL TRANSDUCTION; STEM CELLS; TYROSINE 3-MONOOXYGENASE; WNT1 PROTEIN;

EID: 77954497673     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0860-10.2010     Document Type: Article

References (41)

1. Andersson ER, Prakash N, Cajanek L, Minina E, Bryja V, Bryjova L, Yamaguchi TP, Hall AC, Wurst W, Arenas E (2008) Wnt5a regulates ventral midbrain morphogenesis and the development of A9-A10 dopaminergic cells in vivo. PLoS ONE 3:e3517.
2. Ang SL (2006) Transcriptional control of midbrain dopaminergic neuron development. Development 133:3499-3506.
3. Arenas E (2008) Foxa2: the rise and fall of dopamine neurons. Cell Stem Cell 2:110-112.
4. Barberi T, Klivenyi P, Calingasan NY, Lee H, Kawamata H, Loonam K, Perrier AL, Bruses J, Rubio ME, Topf N, Tabar V, Harrison NL, Beal MF, Moore MA, Studer L (2003) Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 21:1200-1207.
5. Bjorklund A, Lindvall O (1984) Dopamine-containing systems in the CNS. In: Handbook of chemical neuroanatomy. Amsterdam: Elsevier.
6. Castelo-Branco G, Arenas E (2006) Function of Wnts in dopaminergic neuron development. Neurodegener Dis 3:5-11.
7. Castelo-Branco G, Wagner J, Rodriguez FJ, Kele J, Sousa K, Rawal N, Pasolli HA, Fuchs E, Kitajewski J, Arenas E (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci U S A 100:12747-12752.
8. Castelo-Branco G, Andersson ER, Minina E, Sousa KM, Ribeiro D, Kokubu C, Imai K, Prakash N, Wurst W, Arenas E (2010) Delayed dopaminergic neuron differentiation in Lrp6 mutant mice. Dev Dyn 239:211-221.
9. Chung S, Leung A, Han BS, Chang MY, Moon JI, Kim CH, Hong S, Pruszak J, Isacson O, Kim KS (2009) Wnt1-lmx1a forms a novel autoregulatory loop and controls midbrain dopaminergic differentiation synergistically with the SHH-FoxA2 pathway. Cell Stem Cell 5:646-658.
10. Danielian PS, McMahon AP (1996) Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature 383:332-334.
11. Ferri AL, Lin W, Mavromatakis YE, Wang JC, Sasaki H, Whitsett JA, Ang SL (2007) Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner. Development 134:2761-2769.
12. Gulacsi AA, Anderson SA (2008) Beta-catenin-mediated Wnt signaling regulates neurogenesis in the ventral telencephalon. Nat Neurosci 11:1383-1391.
13. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, Taketo MM (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18:5931-5942.
14. Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ (2004) Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118:517-528.
15. Hedlund E, Pruszak J, Lardaro T, Ludwig W, Viñuela A, Kim KS, Isacson O (2008) Embryonic stem cell-derived Pitx3-enhanced green fluorescent protein midbrain dopamine neurons survive enrichment by fluorescence-activated cell sorting and function in an animal model of Parkinson's disease. Stem Cells 26:1526-1536.
16. Hynes M, Porter JA, Chiang C, Chang D, Tessier-Lavigne M, Beachy PA, Rosenthal A (1995) Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron 15:35-44.
17. Jeong Y, Epstein DJ (2003) Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130:3891-3902.
18. Joksimovic M, Yun BA, Kittappa R, Anderegg AM, Chang WW, Taketo MM, McKay RD, Awatramani RB (2009) Wnt antagonism of Shh facilitates midbrain floor plate neurogenesis. Nat Neurosci 12:125-131.
19. Lin W, Metzakopian E, Mavromatakis YE, Gao N, Balaskas N, Sasaki H, Briscoe J, Whitsett JA, Goulding M, Kaestner KH, Ang SL (2009) Foxa1 and Foxa2 function both upstream of and cooperatively with Lmx1a and Lmx1b in a feedforward loop promoting mesodiencephalic dopaminergic neuron development. Dev Biol 333:386-396.
20. Lindeberg J, Usoskin D, Bengtsson H, Gustafsson A, Kylberg A, Söderström S, Ebendal T (2004) Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40:67-73. (Pubitemid 39488502)
21. McMahon AP, Bradley A (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62:1073-1085. (Pubitemid 120035024)
22. Megason SG, McMahon AP (2002) A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129:2087-2098.
23. Omodei D, Acampora D, Mancuso P, Prakash N, Di Giovannantonio LG, Wurst W, Simeone A (2008) Anterior-posterior graded response to Otx2 controls proliferation and differentiation of dopaminergic progenitors in the ventral mesencephalon. Development 135:3459-3470.
24. Parish CL, Parisi S, Persico MG, Arenas E, Minchiotti G (2005) Cripto as a target for improving embryonic stem cell-based therapy in Parkinson's disease. Stem Cells 23:471-476.
25. Parish CL, Castelo-Branco G, Rawal N, Tonnesen J, Sorensen AT, Salto C, Kokaia M, Lindvall O, Arenas E (2008) Wnt5a-treated midbrain neural stem cells improve dopamine cell replacement therapy in parkinsonian mice. J Clin Invest 118:149-160.
26. Prakash N, Wurst W (2006) Genetic networks controlling the development of midbrain dopaminergic neurons. J Physiol 575:403-410.
27. Prakash N, Brodski C, Naserke T, Puelles E, Gogoi R, Hall A, Panhuysen M, Echevarria D, Sussel L, Weisenhorn DM, Martinez S, Arenas E, Simeone A, Wurst W (2006) A Wnt1-regulated genetic network controls the identity and fate of midbrain-dopaminergic progenitors in vivo. Development 133:89-98.
28. Puelles E, Annino A, Tuorto F, Usiello A, Acampora D, Czerny T, Brodski C, Ang SL, Wurst W, Simeone A (2004) Otx2 regulates the extent, identity and fate of neuronal progenitor domains in the ventral midbrain. Development 131:2037-2048.
29. Rodríguez-Gómez JA, Lu JQ, Velasco I, Rivera S, Zoghbi SS, Liow JS, Musachio JL, Chin FT, Toyama H, Seidel J, Green MV, Thanos PK, Ichise M, Pike VW, Innis RB, McKayRD (2007) Persistent dopamine functions of neurons derived from embryonic stem cells in a rodent model of Parkinson disease. Stem Cells 25:918-928.
30. Sasaki H, Hui C, Nakafuku M, Kondoh H (1997) A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124:1313-1322. (Pubitemid 27190104)
31. Schulte G, Bryja V, Rawal N, Castelo-Branco G, Sousa KM, Arenas E (2005) Purified Wnt-5a increases differentiation of midbrain dopaminergic cells and dishevelled phosphorylation. J Neurochem 92:1550-1553.
32. Smidt MP, Burbach JP (2007) How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 8:21-32.
33. Sousa KM, Villaescusa JC, Cajanek L, Ondr JK, Castelo-Branco G, Hofstra W, Bryja V, Palmberg C, Bergman T, Wainwright B, Lang RA, Arenas E (2010) WNT2 regulates progenitor proliferation in the developing ventral midbrain. J Biol Chem 285:7246-7253.
34. Stuebner S, Faus-Kessler T, Fischer T, Wurst W, Prakash N (2010) Fzd3 and Fzd6 deficiency results in a severe midbrain morphogenesis defect. Dev Dyn 239:246-260.
35. Takeshima T, Shimoda K, Johnston JM, Commissiong JW (1996) Standardized methods to bioassay neurotrophic factors for dopaminergic neurons. J Neurosci Methods 67:27-41.
36. Tang M, Miyamoto Y, Huang EJ (2009) Multiple roles of beta-catenin in controlling the neurogenic niche for midbrain dopamine neurons. Development 136:2027-2038.
37. Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847-850. (Pubitemid 120006010)
38. Vernay B, Koch M, Vaccarino F, Briscoe J, Simeone A, Kageyama R, Ang SL (2005) Otx2 regulates subtype specification and neurogenesis in the midbrain. J Neurosci 25:4856-4867.
39. Ye W, Shimamura K, Rubenstein JL, Hynes MA, Rosenthal A (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93:755-766.
40. Zhang J, Huang EJ (2006) Dynamic expression of neurotrophic factor receptors in postnatal spinal motoneurons and in mouse model of ALS. J Neurobiol 66:882-895.
41. Zhang J, Pho V, Bonasera SJ, Holtzman J, Tang AT, Hellmuth J, Tang S, Janak PH, Tecott LH, Huang EJ (2007) Essential function of HIPK2 in TGFbeta-dependent survival of midbrain dopamine neurons. Nat Neurosci 10:77-86.