SMAD4 is essential for generating subtypes of neurons during cerebellar development

Developmental Biology

Volumn 365, Issue 1, 2012, Pages 82-90

  Fernandes, Marie ^a   Antoine, Michelle ^a   Hébert, Jean M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Deep cerebellar nuclei; Granule cell precursor; Mouse; Rhombic lip; SMAD4; Unipolar brush cells

Indexed keywords

4 AMINOBUTYRIC ACID; BONE MORPHOGENETIC PROTEIN; GLUTAMIC ACID; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRUSH BORDER; CELL COUNT; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CEREBELLUM; CEREBELLUM NUCLEUS; CONTROLLED STUDY; EMBRYO; GRANULE CELL; MOUSE; MUTANT; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PURKINJE CELL; SIGNAL TRANSDUCTION;

MUS;

EID: 84859431030     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.017     Document Type: Article

References (41)

1. Alder J., Lee K.J., Jessell T.M., Hatten M.E. Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nat. Neurosci. 1999, 2:535-540.
2. Altman J., Bayer S.A. Time of origin and distribution of a new cell type in the rat cerebellar cortex. Exp. Brain Res. 1977, 29:265-274.
3. Altman J., Bayer S.A. Development of the cerebellar system in relation to its evolution, structures and functions 1997, CRC, New York.
4. Basson M.A., Echevarria D., Ahn C.P., Sudarov A., Joyner A.L., Mason I.J., Martinez S., Martin G.R. Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 2008, 135:889-898.
5. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., Matzuk M.M., Zoghbi H.Y. Math1 is essential for genesis of cerebellar granule neurons. Nature 1997, 390:169-172.
6. Chizhikov V.V., Lindgren A.G., Currle D.S., Rose M.F., Monuki E.S., Millen K.J. The roof plate regulates cerebellar cell-type specification and proliferation. Development 2006, 133:2793-2804.
7. Chizhikov V.V., Lindgren A.G., Mishima Y., Roberts R.W., Aldinger K.A., Miesegaes G.R., Currle D.S., Monuki E.S., Millen K.J. Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10725-10730.
8. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
9. Descargues P., Sil A.K., Karin M. IKKalpha, a critical regulator of epidermal differentiation and a suppressor of skin cancer. EMBO J. 2008, 27:2639-2647.
10. Englund C., Kowalczyk T., Daza R.A., Dagan A., Lau C., Rose M.F., Hevner R.F. Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J. Neurosci. 2006, 26:9184-9195.
11. Fernandes M., Gutin G., Alcorn H., McConnell S.K., Hebert J.M. Mutations in the BMP pathway in mice support the existence of two molecular classes of holoprosencephaly. Development 2007, 134:3789-3794.
12. Fink A.J., Englund C., Daza R.A., Pham D., Lau C., Nivison M., Kowalczyk T., Hevner R.F. Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J. Neurosci. 2006, 26:3066-3076.
13. Gutin G., Fernandes M., Palazzolo L., Paek H., Yu K., Ornitz D.M., McConnell S.K., Hebert J.M. FGF signalling generates ventral telencephalic cells independently of SHH. Development 2006, 133:2937-2946.
14. Hirsch M.R., Glover J.C., Dufour H.D., Brunet J.F., Goridis C. Forced expression of Phox2 homeodomain transcription factors induces a branchio-visceromotor axonal phenotype. Dev. Biol. 2007, 303:687-702.
15. Hoshino M., Nakamura S., Mori K., Kawauchi T., Terao M., Nishimura Y.V., Fukuda A., Fuse T., Matsuo N., Sone M., Watanabe M., Bito H., Terashima T., Wright C.V., Kawaguchi Y., Nakao K., Nabeshima Y. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 2005, 47:201-213.
16. Kendall S.E., Battelli C., Irwin S., Mitchell J.G., Glackin C.A., Verdi J.M. NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol. Cell. Biol. 2005, 25:7711-7724.
17. Kim E.J., Battiste J., Nakagawa Y., Johnson J.E. Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol. Cell. Neurosci. 2008, 38:595-606.
18. Kimmel R.A., Turnbull D.H., Blanquet V., Wurst W., Loomis C.A., Joyner A.L. Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 2000, 14:1377-1389.
19. Leto K., Bartolini A., Yanagawa Y., Obata K., Magrassi L., Schilling K., Rossi F. Laminar fate and phenotype specification of cerebellar GABAergic interneurons. J. Neurosci. 2009, 29:7079-7091.
20. Li J.Y., Lao Z., Joyner A.L. Changing requirements for Gbx2 in development of the cerebellum and maintenance of the mid/hindbrain organizer. Neuron 2002, 36:31-43.
21. Liu A., Joyner A.L. Early anterior/posterior patterning of the midbrain and cerebellum. Annu. Rev. Neurosci. 2001, 24:869-896.
22. Machold R., Fishell G. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 2005, 48:17-24.
23. Miale I.L., Sidman R.L. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 1961, 4:277-296.
24. Pascual M., Abasolo I., Mingorance-Le Meur A., Martinez A., Del Rio J.A., Wright C.V., Real F.X., Soriano E. Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5193-5198.
25. Qin L., Wine-Lee L., Ahn K.J., Crenshaw E.B. Genetic analyses demonstrate that bone morphogenetic protein signaling is required for embryonic cerebellar development. J. Neurosci. 2006, 26:1896-1905.
26. Rajan P., Panchision D.M., Newell L.F., McKay R.D. BMPs signal alternately through a SMAD or FRAP-STAT pathway to regulate fate choice in CNS stem cells. J. Cell Biol. 2003, 161:911-921.
27. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 2001, 24:1005-1039.
28. Rios I., Alvarez-Rodriguez R., Marti E., Pons S. Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling. Development 2004, 131:3159-3168.
29. Sato T., Joyner A.L., Nakamura H. How does Fgf signaling from the isthmic organizer induce midbrain and cerebellum development?. Dev. Growth Differ. 2004, 46:487-494.
30. Schmahmann J.D. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin. Neurosci. 2004, 16:367-378.
31. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
32. Shim J.H., Greenblatt M.B., Xie M., Schneider M.D., Zou W., Zhai B., Gygi S., Glimcher L.H. TAK1 is an essential regulator of BMP signalling in cartilage. EMBO J. 2009, 28:2028-2041.
33. Wang V.Y., Rose M.F., Zoghbi H.Y. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 2005, 48:31-43.
34. Weisheit G., Gliem M., Endl E., Pfeffer P.L., Busslinger M., Schilling K. Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur. J. Neurosci. 2006, 24:466-478.
35. Xu J., Liu Z., Ornitz D.M. Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development 2000, 127:1833-1843.
36. Xu X., Han J., Ito Y., Bringas P., Deng C., Chai Y. Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGF-beta/BMP signaling during tooth and palate development. Dev. Cell 2008, 15:322-329.
37. Yang X., Li C., Herrera P.L., Deng C.X. Generation of Smad4/Dpc4 conditional knockout mice. Genesis 2002, 32:80-81.
38. Yang Z.J., Ellis T., Markant S.L., Read T.A., Kessler J.D., Bourboulas M., Schuller U., Machold R., Fishell G., Rowitch D.H., Wainwright B.J., Wechsler-Reya R.J. Medulloblastoma can be initiated be deletion of patched in lineage-restricted progenitors or stem cells. Cancer Cell 2008, 14:135-145.
39. Zhou Y.X., Zhao M., Li D., Shimazu K., Sakata K., Deng C.X., Lu B. Cerebellar deficits and hyperactivity in mice lacking Smad4. J. Biol. Chem. 2003, 278:42313-42320.
40. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Wilecke K.M., Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 2001, 31:85-94.
41. Zordan P., Croci L., Hawkes R., Consalez G.G. Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev. Dyn. 2008, 237:1726-1735.