A simplified method to generate serotonergic neurons from mouse embryonic stem and induced pluripotent stem cells

Journal of Neurochemistry

Volumn 122, Issue 1, 2012, Pages 81-93

  Shimada, Takeshi ^a   Takai, Yoshihiro ^a   Shinohara, Kikuko ^a   Yamasaki, Atsushi ^a   Tominaga Yoshino, Keiko ^a   Ogura, Akihiko ^a   Toi, Akihiro ^a   Asano, Kouji ^a   Shintani, Norihito ^a   Hayata Takano, Atsuko ^a   Baba, Akemichi ^a,c   Hashimoto, Hitoshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

embryonic stem cells; in vitro differentiation; induced pluripotent stem cells; noggin; psychiatric disorders; serotonergic neurons

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; ENHANCED GREEN FLUORESCENT PROTEIN; NOGGIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENHANCER REGION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PET 1 GENE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; VOLTAGE CLAMP;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; COLLAGEN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; ELECTRIC STIMULATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INDUCED PLURIPOTENT STEM CELLS; LAMININ; MICE; ORGAN CULTURE TECHNIQUES; PROTEINS; PROTEOGLYCANS; RNA, MESSENGER; SEROTONERGIC NEURONS; SEROTONIN; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; TUBULIN; TYROSINE 3-MONOOXYGENASE;

ERINACEIDAE; IPS;

EID: 84862185062     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07724.x     Document Type: Article

References (50)

1. Agid Y., Buzsaki G., Diamond D. M., et al. (2007) How can drug discovery for psychiatric disorders be improved? Nat. Rev. Drug Discov. 6, 189-201. (Pubitemid 46344623)
2. Alenina N., Bashammakh S., and, Bader M., (2006) Specification and differentiation of serotonergic neurons. Stem Cell Rev. 2, 5-10. (Pubitemid 44195972)
3. Balemans W., and, Van Hul W., (2002) Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231-250. (Pubitemid 35216412)
4. Barberi T., Klivenyi P., Calingasan N. Y., et al. (2003) Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 21, 1200-1207. (Pubitemid 37186177)
5. Benninger F., Beck H., Wernig M., Tucker K. L., Brustle O., and, Scheffler B., (2003) Functional integration of embryonic stem cell-derived neurons in hippocampal slice cultures. J. Neurosci. 23, 7075-7083. (Pubitemid 36975872)
6. Bonaguidi M. A., Peng C. Y., McGuire T., Falciglia G., Gobeske K. T., Czeisler C., and, Kessler J. A., (2008) Noggin expands neural stem cells in the adult hippocampus. J. Neurosci. 28, 9194-9204.
7. Cazillis M., Gonzalez B. J., Billardon C., Lombet A., Fraichard A., Samarut J., Gressens P., Vaudry H., and, Rostene W., (2004) VIP and PACAP induce selective neuronal differentiation of mouse embryonic stem cells. Eur. J. Neurosci. 19, 798-808. (Pubitemid 38297017)
8. Chalazonitis A., Pham T. D., Li Z., Roman D., Guha U., Gomes W., Kan L., Kessler J. A., and, Gershon M. D., (2008) Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit. J. Comp. Neurol. 509, 474-492.
9. Cummings K. J., Pendlebury J. D., Sherwood N. M., and, Wilson R. J., (2004) Sudden neonatal death in PACAP-deficient mice is associated with reduced respiratory chemoresponse and susceptibility to apnoea. J. Physiol. 555, 15-26. (Pubitemid 38313059)
10. Gaspar P., Cases O., and, Maroteaux L., (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4, 1002-1012. (Pubitemid 37486676)
11. Gaulden J., and, Reiter J. F., (2008) Neur-ons and neur-offs: regulators of neural induction in vertebrate embryos and embryonic stem cells. Hum. Mol. Genet. 17, R60-R66.
12. Gratsch T. E., and, O'Shea K. S., (2002) Noggin and chordin have distinct activities in promoting lineage commitment of mouse embryonic stem (ES) cells. Dev. Biol. 245, 83-94. (Pubitemid 34461805)
13. Hampton D. W., Steeves J. D., Fawcett J. W., and, Ramer M. S., (2007) Spinally upregulated noggin suppresses axonal and dendritic plasticity following dorsal rhizotomy. Exp. Neurol. 204, 366-379. (Pubitemid 46335907)
14. Harland R., (2000) Neural induction. Curr. Opin. Genet. Dev. 10, 357-362. (Pubitemid 30450037)
15. Hashimoto H., Shintani N., and, Nishino A.,., et al. (2000) Mice with markedly reduced PACAP (PAC(1)) receptor expression by targeted deletion of the signal peptide. J. Neurochem. 75, 1810-1817.
16. Hashimoto H., Shintani N., Tanaka K., et al. (2001) Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc. Natl Acad. Sci. USA 98, 13355-13360. (Pubitemid 33051367)
17. Hashimoto H., Hashimoto R., Shintani N., et al. (2009) Depression-like behavior in the forced swimming test in PACAP-deficient mice: amelioration by the atypical antipsychotic risperidone. J. Neurochem. 110, 595-602.
18. Hattori T., Baba K., Matsuzaki S., et al. (2007) A novel DISC1-interacting partner DISC1-Zinc-finger Binding protein: implication in the modulation of DISC1-dependent neurite outgrowth. Mol. Psychiatry 12, 398-407. (Pubitemid 46496834)
19. Hendricks T., Francis N., Fyodorov D., and, Deneris E. S., (1999) The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J. Neurosci. 19, 10348-10356. (Pubitemid 30228042)
20. Hitz C., Wurst W., and, Kuhn R., (2007) Conditional brain-specific knockdown of MAPK using Cre/loxP regulated RNA interference. Nucleic Acids Res. 35, e90.
21. Hodges M. R., Wehner M., Aungst J., Smith J. C., and, Richerson G. B., (2009) Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J. Neurosci. 29, 10341-10349.
22. Hynes M., and, Rosenthal A., (1999) Specification of dopaminergic and serotonergic neurons in the vertebrate CNS. Curr. Opin. Neurobiol. 9, 26-36. (Pubitemid 29084087)
23. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S. I., and, Sasai Y., (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40.
24. Kim M., Habiba A., Doherty J. M., Mills J. C., Mercer R. W., and, Huettner J. E., (2009) Regulation of mouse embryonic stem cell neural differentiation by retinoic acid. Dev. Biol. 328, 456-471.
25. Kumar M., Kaushalya S. K., Gressens P., Maiti S., and, Mani S., (2009) Optimized derivation and functional characterization of 5-HT neurons from human embryonic stem cells. Stem Cells Dev. 18, 615-627.
26. Lee S. H., Lumelsky N., Studer L., Auerbach J. M., and, McKay R. D., (2000) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18, 675-679. (Pubitemid 30415305)
27. Liu A., and, Niswander L. A., (2005) Bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev. Neurosci. 6, 945-954. (Pubitemid 41753088)
28. Mabuchi T., Shintani N., Matsumura S., Okuda-Ashitaka E., Hashimoto H., Muratani T., Minami T., Baba A., and, Ito S., (2004) Pituitary adenylate cyclase-activating polypeptide is required for the development of spinal sensitization and induction of neuropathic pain. J. Neurosci. 24, 7283-7291. (Pubitemid 39100698)
29. Martinowich K., and, Lu B., (2008) Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology 33, 73-83. (Pubitemid 350191318)
30. Meltzer H. Y., and, Huang M., (2008) In vivo actions of atypical antipsychotic drug on serotonergic and dopaminergic systems. Prog. Brain Res. 172, 177-197.
31. Mikawa S., and, Sato K., (2011) Noggin expression in the adult rat brain. Neuroscience 184, 38-53.
32. Mira H., Andreu Z., and, Suh H.,., et al. (2010) Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89.
33. Miyazaki S., Miyazaki T., Tashiro F., Yamato E., and, Miyazaki J., (2005) Development of a single-cassette system for spatiotemporal gene regulation in mice. Biochem. Biophys. Res. Commun. 338, 1083-1088. (Pubitemid 41597749)
34. Nakamachi T., Farkas J., Watanabe J., Ohtaki H., Dohi K., Arata S., and, Shioda S., (2011) Role of PACAP in neural stem/progenitor cell and astrocyte - from neural development to neural repair. Curr. Pharm. Des. 17, 973-984.
35. Okita K., Ichisaka T., and, Yamanaka S., (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317. (Pubitemid 47080336)
36. Sakaue M., Somboonthum P., Nishihara B., Koyama Y., Hashimoto H., Baba A., and, Matsuda T., (2000) Postsynaptic 5-hydroxytryptamine1A receptor activation increases in vivo dopamine release in rat prefrontal cortex. Br. J. Pharmacol. 129, 1028-1034. (Pubitemid 30142918)
37. Salli U., Reddy A. P., Salli N., Lu N. Z., Kuo H. C., Pau F. K., Wolf D. P., and, Bethea C. L., (2004) Serotonin neurons derived from rhesus monkey embryonic stem cells: similarities to CNS serotonin neurons. Exp. Neurol. 188, 351-364. (Pubitemid 38891596)
38. Scott M. M., Krueger K. C., and, Deneris E. S., (2005a) A differentially autoregulated Pet-1 enhancer region is a critical target of the transcriptional cascade that governs serotonin neuron development. J. Neurosci. 25, 2628-2636. (Pubitemid 40365174)
39. Scott M. M., Wylie C. J., Lerch J. K., et al. (2005b) A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc. Natl Acad. Sci. USA 102, 16472-16477. (Pubitemid 41688938)
40. Soriano P., (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71. (Pubitemid 29036285)
41. Srinivas S., Watanabe T., Lin C. S., William C. M., Tanabe Y., Jessell T. M., and, Costantini F., (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
42. Tanaka K., Shintani N., Hashimoto H., et al. (2006) Psychostimulant- induced attenuation of hyperactivity and prepulse inhibition deficits in Adcyap1-deficient mice. J. Neurosci. 26, 5091-5097. (Pubitemid 44315290)
43. Tang J., Song M., Wang Y., Fan X., Xu H., and, Bai Y., (2009) Noggin and BMP4 co-modulate adult hippocampal neurogenesis in the APP(swe)/PS1(DeltaE9) transgenic mouse model of Alzheimer's disease. Biochem. Biophys. Res. Commun. 385, 341-345.
44. Tokuyama Y., Ingram S. L., Woodward J. S., and, Bethea C. L., (2010) Functional characterization of rhesus embryonic stem cell-derived serotonin neurons. Exp. Biol. Med. (Maywood) 235, 649-657.
45. Tominaga-Yoshino K., Urakubo T., Okada M., Matsuda H., and, Ogura A., (2008) Repetitive induction of late-phase LTP produces long-lasting synaptic enhancement accompanied by synaptogenesis in cultured hippocampal slices. Hippocampus 18, 281-293. (Pubitemid 351399631)
46. Vaudry D., Falluel-Morel A., Bourgault S., et al. (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol. Rev. 61, 283-357.
47. Waschek J. A., Dicicco-Bloom E., Nicot A., and, Lelievre V., (2006) Hedgehog signaling: new targets for GPCRs coupled to cAMP and protein kinase A. Ann. N Y Acad. Sci. 1070, 120-128. (Pubitemid 44126629)
48. Wylie C. J., Hendricks T. J., Zhang B., Wang L., Lu P., Leahy P., Fox S., Maeno H., and, Deneris E. S., (2010) Distinct transcriptomes define rostral and caudal serotonin neurons. J. Neurosci. 30, 670-684.
49. Ye W., Shimamura K., Rubenstein J. L., Hynes M. A., and, Rosenthal A., (1998) FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766. (Pubitemid 28257582)
50. Zimmerman L. B., De Jesus-Escobar J. M., and, Harland R. M., (1996) Spemann The organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606. (Pubitemid 26299491)