Homeotic Transformations of Neuronal Cell Identities

Trends in Neurosciences

Volumn 38, Issue 12, 2015, Pages 751-762

  Arlotta, Paola ^a   Hobert, Oliver ^b  

^a Harvard University   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; CELL FATE; CELL TRANSFORMATION; DROSOPHILA; HOMEOSIS; HUMAN; MOLECULAR EVOLUTION; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; ZEBRA FISH; ANIMAL; BRAIN; EVOLUTION; MORPHOGENESIS; PHYSIOLOGY; PLANT; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL EVOLUTION; BRAIN; HUMANS; MORPHOGENESIS; NEURONS; PLANTS;

EID: 84961641087     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2015.10.005     Document Type: Review

References (84)

1. Bateson W. Materials for the Study of Variation, Treated with Especial Regard to Discontinuity in the Origin of Species 1894, Macmillan.
2. Meyerowitz E.M., et al. Abnormal flowers and pattern formation in floral development. Development 1989, 106:209-217.
3. Goldschmidt R. The Material Basis of Evolution 1940, Yale University Press.
4. Akam M. Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. Int. J. Dev. Biol. 1998, 42:445-451.
5. Stern D.L. Evolution, Development, and the Predictable Genome 2010, Roberts and Company Publishers.
6. Sattler R. Homeosis in plants. Am. J. Bot. 1988, 75:1606-1617.
7. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
8. Lewis E.B. Homeosis: the first 100 years. Trends Genet. 1994, 10:341-343.
9. Holmes S. Henderson's Dictionary of Biological Terms 1986, Van Nostrand Reinhold Co. 9th edn.
10. Riedl R. Order in Living Organisms: A Systems Analysis of Evolution 1978, Wiley.
11. Sternberg P.W., Horvitz H.R. The genetic control of cell lineage during nematode development. Annu. Rev. Genet. 1984, 18:489-524.
12. Slack J.M. Homoeotic transformations in man: implications for the mechanism of embryonic development and for the organization of epithelia. J. Theor. Biol. 1985, 114:463-490.
13. Sulston J.E., et al. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
14. Horvitz H.R., et al. Mutations that affect neural cell lineages and cell fates during the development of the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 1983, 48:453-463.
15. Zhao C., Emmons S.W. A transcription factor controlling development of peripheral sense organs in C. elegans. Nature 1995, 373:74-78.
16. Tomlinson A., Ready D.F. Sevenless: a cell-specific homeotic mutation of the Drosophila eye. Science 1986, 231:400-402.
17. Hobert O. Regulation of terminal differentiation programs in the nervous system. Annu. Rev. Cell Dev. Biol. 2011, 27:681-696.
18. Mann R.S., Carroll S.B. Molecular mechanisms of selector gene function and evolution. Curr. Opin. Genet. Dev. 2002, 12:592-600.
19. Vernay B., et al. Otx2 regulates subtype specification and neurogenesis in the midbrain. J. Neurosci. 2005, 25:4856-4867.
20. Di Giovannantonio L.G., et al. Otx2 cell-autonomously determines dorsal mesencephalon versus cerebellum fate independently of isthmic organizing activity. Development 2014, 141:377-388.
21. Jung H., et al. Global control of motor neuron topography mediated by the repressive actions of a single hox gene. Neuron 2010, 67:781-796.
22. Jung H., et al. Evolving Hox activity profiles govern diversity in locomotor systems. Dev. Cell 2014, 29:171-187.
23. Philippidou P., Dasen J.S. Hox genes: choreographers in neural development, architects of circuit organization. Neuron 2013, 80:12-34.
24. Francius C., Clotman F. Generating spinal motor neuron diversity: a long quest for neuronal identity. Cell. Mol. Life Sci. 2014, 71:813-829.
25. Srinivasan K., et al. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19071-19078.
26. Molyneaux B.J., et al. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 2005, 47:817-831.
27. Chen B., et al. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17184-17189.
28. Chen J.G., et al. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17792-17797.
29. Lodato S., et al. Gene co-regulation by Fezf2 selects neurotransmitter identity and connectivity of corticospinal neurons. Nat. Neurosci. 2014, 17:1046-1054.
30. Alcamo E.A., et al. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 2008, 57:364-377.
31. Britanova O., et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 2008, 57:378-392.
32. McKenna W.L., et al. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J. Neurosci. 2011, 31:549-564.
33. Rouaux C., Arlotta P. Fezf2 directs the differentiation of corticofugal neurons from striatal progenitors in vivo. Nat. Neurosci. 2010, 13:1345-1347.
34. De la Rossa A., et al. In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons. Nat. Neurosci. 2013, 16:193-200.
35. Rouaux C., Arlotta P. Direct lineage reprogramming of post-mitotic callosal neurons into corticofugal neurons in vivo. Nat. Cell Biol. 2013, 15:214-221.
36. Shim S., et al. Cis-regulatory control of corticospinal system development and evolution. Nature 2012, 486:74-79.
37. Ma Q. Transcriptional regulation of neuronal phenotype in mammals. J. Physiol. 2006, 575:379-387.
38. Duggan A., Chalfie M. Control of neuronal development in Caenorhabditis elegans. Curr. Opin. Neurobiol. 1995, 5:6-9.
39. Zhang Y., et al. Identification of genes expressed in C. elegans touch receptor neurons. Nature 2002, 418:331-335.
40. Serrano-Saiz E., et al. Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 2013, 155:659-673.
41. Gordon P.M., Hobert O. A competition mechanism for a homeotic neuron identity transformation in C. elegans. Dev. Cell 2015, 34:206-219.
42. Way J.C., Chalfie M. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 1988, 54:5-16.
43. Nokes E.B., et al. Cis-regulatory mechanisms of gene expression in an olfactory neuron type in Caenorhabditis elegans. Dev. Dyn. 2009, 238:3080-3092.
44. Sagasti A., et al. Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes Dev. 1999, 13:1794-1806.
45. Alqadah A., et al. Postmitotic diversification of olfactory neuron types is mediated by differential activities of the HMG-box transcription factor SOX-2. EMBO J. 2015, 34:2574-2589.
46. Hobert O. Development of left/right asymmetry in the Caenorhabditis elegans nervous system: from zygote to postmitotic neuron. Genesis 2014, 52:528-543.
47. Sen S., et al. Genetic transformation of structural and functional circuitry rewires the Drosophila brain. Elife 2014, 3.
48. Morey M., et al. Coordinate control of synaptic-layer specificity and rhodopsins in photoreceptor neurons. Nature 2008, 456:795-799.
49. Leone D.P., et al. Satb2 regulates the differentiation of both callosal and subcerebral projection neurons in the developing cerebral cortex. Cereb. Cortex 2014, 25:3406-3419.
50. Morgan T.H., et al. The Genetics of Drosophila 1988, Garland.
51. Altun-Gultekin Z., et al. A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 2001, 128:1951-1969.
52. Uchida O., et al. The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development 2003, 130:1215-1224.
53. Saucedo-Cardenas O., et al. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:4013-4018.
54. Wallen A., et al. Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp. Cell Res. 1999, 253:737-746.
55. Ohno S. Evolution by Gene Duplication 1970, Springer.
56. Smith C.J., et al. Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization. Neuron 2013, 79:266-280.
57. Casares F., Mann R.S. The ground state of the ventral appendage in Drosophila. Science 2001, 293:1477-1480.
58. Gehring W.J., et al. Evolution of the Hox gene complex from an evolutionary ground state. Curr. Top. Dev. Biol. 2009, 88:35-61.
59. Petryniak M.A., et al. Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 2007, 55:417-433.
60. Puelles E., et al. Otx2 controls identity and fate of glutamatergic progenitors of the thalamus by repressing GABAergic differentiation. J. Neurosci. 2006, 26:5955-5964.
61. Sussel L., et al. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 1999, 126:3359-3370.
62. McKinsey G.L., et al. Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 2013, 77:83-98.
63. Nakatani T., et al. Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 2007, 134:2783-2793.
64. Mangale V.S., et al. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 2008, 319:304-309.
65. Gowan K., et al. Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 2001, 31:219-232.
66. Fode C., et al. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000, 14:67-80.
67. Glasgow S.M., et al. Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 2005, 132:5461-5469.
68. Hoshino M., et al. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 2005, 47:201-213.
69. Helms A.W., et al. Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 2005, 132:2709-2719.
70. Kriks S., et al. Gsh2 is required for the repression of Ngn1 and specification of dorsal interneuron fate in the spinal cord. Development 2005, 132:2991-3002.
71. Cheng L., et al. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 2004, 7:510-517.
72. Lopes R., et al. Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3119-3124.
73. Kala K., et al. Gata2 is a tissue-specific post-mitotic selector gene for midbrain GABAergic neurons. Development 2009, 136:253-262.
74. D'Autreaux F., et al. Homeoprotein Phox2b commands a somatic-to-visceral switch in cranial sensory pathways. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20018-20023.
75. Dasen J.S., et al. Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 2008, 134:304-316.
76. Rousso D.L., et al. Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 2008, 59:226-240.
77. Mears A.J., et al. Nrl is required for rod photoreceptor development. Nat. Genet. 2001, 29:447-452.
78. Daniele L.L., et al. Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Invest. Ophthalmol. Vis. Sci. 2005, 46:2156-2167.
79. Akimoto M., et al. Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3890-3895.
80. Ng L., et al. Two transcription factors can direct three photoreceptor outcomes from rod precursor cells in mouse retinal development. J. Neurosci. 2011, 31:11118-11125.
81. Skromne I., et al. Repression of the hindbrain developmental program by Cdx factors is required for the specification of the vertebrate spinal cord. Development 2007, 134:2147-2158.
82. Li Q., et al. Combinatorial rules of precursor specification underlying olfactory neuron diversity. Curr. Biol. 2013, 23:2481-2490.
83. Udolph G. Notch signaling and the generation of cell diversity in Drosophila neuroblast lineages. Adv. Exp. Med. Biol. 2012, 727:47-60.
84. Johnston R.J., Hobert O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 2003, 426:845-849.