Transformation of the cerebellum into more ventral brainstem fates causes cerebellar agenesis in the absence of Ptf1a function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 17, 2014, Pages

  Millen, Kathleen J ^a,b   Steshina, Ekaterina Y ^c   Iskusnykh, Igor Y ^c   Chizhikov, Victor V ^c  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Dorsal ventral patterning; Human cerebellar malformation; Mouse; Neuronal progenitors; Neuronal specification

Indexed keywords

HOMEODOMAIN PROTEIN; LIM HOMEOBOX TRANSCRIPTION FACTOR 1 ALPHA; T CELL LEUKEMIA HOMEOBOX 3; UNCLASSIFIED DRUG;

ARTICLE; BRAIN STEM; CELL FATE; CEREBELLUM AGENESIS; CONTROLLED STUDY; EMBRYO; GENE FUNCTION; GENE IDENTIFICATION; GENE INACTIVATION; GENE MAPPING; HUMAN; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

DORSAL-VENTRAL PATTERNING; HUMAN CEREBELLAR MALFORMATION; MOUSE; NEURONAL PROGENITORS; NEURONAL SPECIFICATION;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN STEM; CELL LINEAGE; CEREBELLUM; EMBRYO, MAMMALIAN; GLUTAMINE; HUMANS; MICE; MODELS, BIOLOGICAL; MUTATION; NEURONS; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84899650241     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315024111     Document Type: Article

References (49)

1. Wassarman KM, et al. (1997) Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124(15):2923-2934.
2. Broccoli V, Boncinelli E, Wurst W (1999) The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401(6749):164-168.
3. Marshall H, et al. (1992) Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360(6406):737-741.
4. Chisaka O, Musci TS, Capecchi MR (1992) Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 355(6360):516-520.
5. Mark M, et al. (1993) Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119(2):319-338.
6. Barkovich AJ, Millen KJ, Dobyns WB (2007) A developmental classification of malformations of the brainstem. Ann Neurol 62(6):625-639.
7. Barkovich AJ, Millen KJ, Dobyns WB (2009) A developmental and genetic classification for midbrain-hindbrain malformations. Brain 132(Pt 12):3199-3230.
8. Sillitoe RV, Joyner AL (2007) Morphology, molecular codes, and circuitry produce the threedimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23:549-577.
9. Wang VY, RoseMF, ZoghbiHY(2005)Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48(1):31-43.
10. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48(1):17-24.
11. Englund C, et al. (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26(36): 9184-9195.
12. Fink AJ, et al. (2006) Development of the deep cerebellar nuclei: Transcription factors and cell migration from the rhombic lip. J Neurosci 26(11):3066-3076.
13. Wingate R (2005) Math-Map(ic)s. Neuron 48(1):1-4.
14. Hagan N, Zervas M (2012) Wnt1 expression temporally allocates upper rhombic lip progenitors and defines their terminal cell fate in the cerebellum. Mol Cell Neurosci 49(2):217-229.
15. Hunter NL, Dymecki SM (2007) Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus. Development 134(19):3449-3460.
16. Hoshino M, et al. (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47(2):201-213.
17. Hori K, Hoshino M (2012) GABAergic neuron specification in the spinal cord, the cerebellum, and the cochlear nucleus. Neural Plast 2012:921732.
18. Martinez S, Andreu A, Mecklenburg N, Echevarria D (2013) Cellular and molecular basis of cerebellar development. Front Neuroanat 7:18.
19. Basson MA, et al. (2008) Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135(5):889-898.
20. Sellick GS, et al. (2004) Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat Genet 36(12):1301-1305.
21. Tutak E, et al. (2009) A Turkish newborn infant with cerebellar agenesis/neonatal diabetes mellitus and PTF1A mutation. Genet Couns 20(2):147-152.
22. Al-Shammari M, Al-Husain M, Al-Kharfy T, Alkuraya FS (2011) A novel PTF1A mutation in a patient with severe pancreatic and cerebellar involvement. Clin Genet 80(2): 196-198.
23. Pascual M, et al. (2007) Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc Natl Acad Sci USA 104(12):5193-5198.
24. Dymecki SM, Kim JC (2007) Molecular neuroanatomy's "Three Gs": A primer. Neuron 54(1):17-34.
25. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21(1):70-71.
26. Chizhikov VV, et al. (2010) Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proc Natl Acad Sci USA 107(23):10725-10730.
27. Hippenmeyer S, et al. (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3(5):e159.
28. Corrales JD, Blaess S, Mahoney EM, Joyner AL (2006) The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133(9): 1811-1821.
29. Battiste J, et al. (2007) Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 134(2): 285-293.
30. Parras CM, et al. (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev 16(3):324-338.
31. Pattyn A, Goridis C, Brunet JF (2000) Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol Cell Neurosci 15(3):235-243.
32. Schweizer H, Johnson RL, Brand-Saberi B (2004) Characterization of migration behavior of myogenic precursor cells in the limb bud with respect to Lmx1b expression. Anat Embryol (Berl) 208(1):7-18.
33. Dai JX, Hu ZL, Shi M, Guo C, Ding YQ (2008) Postnatal ontogeny of the transcription factor Lmx1b in the mouse central nervous system. J Comp Neurol 509(4):341-355.
34. Gray PA (2008) Transcription factors and the genetic organization of brain stem respiratory neurons. J Appl Physiol (1985) 104(5):1513-1521.
35. Miller RL, et al. (2012) Fos-activation of FoxP2 and Lmx1b neurons in the parabrachial nucleus evoked by hypotension and hypertension in conscious rats. Neuroscience 218: 110-125.
36. Zou HL, et al. (2009) Expression of the LIM-homeodomain gene Lmx1a in the postnatal mouse central nervous system. Brain Res Bull 78(6):306-312.
37. Hallonet ME, Le Douarin NM (1993) Tracing neuroepithelial cells of the mesencephalic and metencephalic alar plates during cerebellar ontogeny in quail-chick chimaeras. Eur J Neurosci 5(9):1145-1155.
38. Zervas M, Blaess S, Joyner AL (2005) Classical embryological studies and modern genetic analysis of midbrain and cerebellum development. Curr Top Dev Biol 69: 101-138.
39. Glasgow SM, Henke RM, Macdonald RJ, Wright CV, Johnson JE (2005) Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132(24):5461-5469.
40. Mizuguchi R, et al. (2006) Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat Neurosci 9(6):770-778.
41. Hori K, et al. (2008) A nonclassical bHLH Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes Dev 22(2):166-178.
42. Chiang C, et al. (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383(6599):407-413.
43. Roessler E, et al. (1996) Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 14(3):357-360.
44. Belloni E, et al. (1996) Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat Genet 14(3):353-356.
45. Fernandes M, Hébert JM (2008) The ups and downs of holoprosencephaly: Dorsal versus ventral patterning forces. Clin Genet 73(5):413-423.
46. Tischfield MA, et al. (2005) Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development. Nat Genet 37(10):1035-1037.
47. Yu T, et al. (2013) Deregulated FGF and homeotic gene expression underlies cerebellar vermis hypoplasia in CHARGE syndrome. Elife 2:e01305.
48. Kawaguchi Y, et al. (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32(1):128-134.
49. Burlison JS, Long Q, Fujitani Y, Wright CV, Magnuson MA (2008) Pdx-1 and Ptf1a concurrently determine fate specification of pancreatic multipotent progenitor cells. Dev Biol 316(1):74-86.