The transcription factor Cux2 marks development of an A-delta sublineage of TrkA sensory neurons

Developmental Biology

Volumn 360, Issue 1, 2011, Pages 77-86

  Bachy, Isabelle ^a   Franck, Marina C M ^a   Li, Lili ^a   Abdo, Hind ^a   Pattyn, Alexandre ^b   Ernfors, Patrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Montpellier University Medical Center   (France)

Author keywords

Development; Differentiation; Neurotrophins; Nociceptive neurons; Sensation; Sensory modality

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; HOMEODOMAIN PROTEIN; MUTANT PROTEIN; NEUROFILAMENT 200 PROTEIN; NEUROFILAMENT PROTEIN; NEUROGENIN 1; PROTEIN TYROSINE KINASE A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CUX2; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL POPULATION; COLD SENSITIVITY; CONTROLLED STUDY; HEAT SENSITIVITY; INTERNEURON; MECHANICAL STIMULATION; MECHANORECEPTOR; MOUSE; MYELINATED NERVE; NOCICEPTIVE RECEPTOR; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL GANGLION;

MUS;

EID: 80755133572     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.09.007     Document Type: Article

References (44)

1. Anderson D.J. Lineages and transcription factors in the specification of vertebrate primary sensory neurons. Curr. Opin. Neurobiol. 1999, 9:517-524.
2. Bertrand N., Castro D.S., Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 2002, 3:517-530.
3. Cain D.M., Khasabov S.G., Simone D.A. Response properties of mechanoreceptors and nociceptors in mouse glabrous skin: an in vivo study. J. Neurophysiol. 2001, 85:1561-1574.
4. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 1999, 398:436-441.
5. Cubelos B., Sebastian-Serrano A., Beccari L., Calcagnotto M.E., Cisneros E., Kim S., Dopazo A., Alvarez-Dolado M., Redondo J.M., Bovolenta P., Walsh C.A., Nieto M. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 2010, 66:523-535.
6. Cubelos B., Sebastian-Serrano A., Kim S., Moreno-Ortiz C., Redondo J.M., Walsh C.A., Nieto M. Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. Cereb. Cortex 2008, 18:1758-1770.
7. Cubelos B., Sebastian-Serrano A., Kim S., Redondo J.M., Walsh C., Nieto M. Cux-1 and Cux-2 control the development of Reelin expressing cortical interneurons. Dev. Neurobiol. 2008, 68:917-925.
8. Djouhri L., Lawson S.N. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res. Brain Res. Rev. 2004, 46:131-145.
9. Ernfors P., Merlio J.P., Persson H. Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 1992, 4:1140-1158.
10. Farinas I., Wilkinson G.A., Backus C., Reichardt L.F., Patapoutian A. Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: direct NT-3 activation of TrkB neurons in vivo. Neuron 1998, 21:325-334.
11. George L., Chaverra M., Todd V., Lansford R., Lefcort F. Nociceptive sensory neurons derive from contralaterally migrating, fate-restricted neural crest cells. Nat. Neurosci. 2007, 10:1287-1293.
12. Hari L., Brault V., Kleber M., Lee H.Y., Ille F., Leimeroth R., Paratore C., Suter U., Kemler R., Sommer L. Lineage-specific requirements of beta-catenin in neural crest development. J. Cell Biol. 2002, 159:867-880.
13. Huang J.E., Wilkinson G.A., Farinas I., Backus C., Zang K., Wong S.L., Reichardt L.F. Expression of Trk receptors in the developing mouse trigeminal ganglion: in vivo evidence for NT-3 activation of trkA and TrkB in addition to TrkC. Development 1999, 126:2191-2203.
14. Iulianella A., Sharma M., Durnin M., Vanden Heuvel G.B., Trainor P.A. Cux2 (Cutl2) integrates neural progenitor development with cell-cycle progression during spinal cord neurogenesis. Development 2008, 135:729-741.
15. Iulianella A., Sharma M., Vanden Heuvel G.B., Trainor P.A. Cux2 functions downstream of Notch signaling to regulate dorsal interneuron formation in the spinal cord. Development 2009, 136:2329-2334.
16. Iulianella A., Vanden Heuvel G., Trainor P. Dynamic expression of murine Cux2 in craniofacial, limb, urogenital and neuronal primordia. Gene Expr. Patterns 2003, 3:571-577.
17. Kleber M., Lee H.Y., Wurdak H., Buchstaller J., Riccomagno M.M., Ittner L.M., Suter U., Epstein D.J., Sommer L. Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. J. Cell Biol. 2005, 169:309-320.
18. Kramer I., Sigrist M., de Nooij J.C., Taniuchi I., Jessell T.M., Arber S. A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron 2006, 49:379-393.
19. Lawson S.N., Biscoe T.J. Development of mouse dorsal root ganglia: an autoradiographic and quantitative study. J. Neurocytol. 1979, 8:265-274.
20. Ledford A.W., Brantley J.G., Kemeny G., Foreman T.L., Quaggin S.E., Igarashi P., Oberhaus S.M., Rodova M., Calvet J.P., Vanden Heuvel G.B. Deregulated expression of the homeobox gene Cux-1 in transgenic mice results in downregulation of p27(kip1) expression during nephrogenesis, glomerular abnormalities, and multiorgan hyperplasia. Dev. Biol. 2002, 245:157-171.
21. Lee H.Y., Kleber M., Hari L., Brault V., Suter U., Taketo M.M., Kemler R., Sommer L. Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 2004, 303:1020-1023.
22. Lei L., Ma L., Nef S., Thai T., Parada L.F. mKlf7, a potential transcriptional regulator of TrkA nerve growth factor receptor expression in sensory and sympathetic neurons. Development 2001, 128:1147-1158.
23. Liu Q., Tang Z., Surdenikova L., Kim S., Patel K.N., Kim A., Ru F., Guan Y., Weng H.J., Geng Y., Undem B.J., Kollarik M., Chen Z.F., Anderson D.J., Dong X. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 2009, 139:1353-1365.
24. Liu Y., Ma Q. Generation of somatic sensory neuron diversity and implications on sensory coding. Curr. Opin. Neurobiol. 2011, 21:52-60.
25. Lo L., Dormand E., Greenwood A., Anderson D.J. Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 2002, 129:1553-1567.
26. Luo W., Wickramasinghe S.R., Savitt J.M., Griffin J.W., Dawson T.M., Ginty D.D. A hierarchical NGF signaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron 2007, 54:739-754.
27. Ma Q., Chen Z., del Barco Barrantes I., de la Pompa J.L., Anderson D.J. Neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 1998, 20:469-482.
28. Ma Q., Fode C., Guillemot F., Anderson D.J. Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev. 1999, 13:1717-1728.
29. Marmigere F., Ernfors P. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat. Rev. Neurosci. 2007, 8:114-127.
30. Marmigere F., Montelius A., Wegner M., Groner Y., Reichardt L.F., Ernfors P. The Runx1/AML1 transcription factor selectively regulates development and survival of TrkA nociceptive sensory neurons. Nat. Neurosci. 2006, 9:180-187.
31. Martin-Zanca D., Barbacid M., Parada L.F. Expression of the trk proto-oncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev. 1990, 4:683-694.
32. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997, 19:849-861.
33. Nagy I., Rang H. Noxious heat activates all capsaicin-sensitive and also a sub-population of capsaicin-insensitive dorsal root ganglion neurons. Neuroscience 1999, 88:995-997.
34. Ozen I., Galichet C., Watts C., Parras C., Guillemot F., Raineteau O. Proliferating neuronal progenitors in the postnatal hippocampus transiently express the proneural gene Ngn2. Eur. J. Neurosci. 2007, 25:2591-2603.
35. Perez S.E., Rebelo S., Anderson D.J. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 1999, 126:1715-1728.
36. Quaggin S.E., Heuvel G.B., Golden K., Bodmer R., Igarashi P. Primary structure, neural-specific expression, and chromosomal localization of Cux-2, a second murine homeobox gene related to Drosophila cut. J. Biol. Chem. 1996, 271:22624-22634.
37. Rifkin J.T., Todd V.J., Anderson L.W., Lefcort F. Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation. Dev. Biol. 2000, 227:465-480.
38. Shibasaki K., Murayama N., Ono K., Ishizaki Y., Tominaga M. TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. J. Neurosci. 2010, 30:4601-4612.
39. Snider W.D., McMahon S.B. Tackling pain at the source: new ideas about nociceptors. Neuron 1998, 20:629-632.
40. Tender G.C., Li Y.Y., Cui J.G. Vanilloid receptor 1-positive neurons mediate thermal hyperalgesia and tactile allodynia. Spine J. 2008, 8:351-358.
41. Tender G.C., Walbridge S., Olah Z., Karai L., Iadarola M., Oldfield E.H., Lonser R.R. Selective ablation of nociceptive neurons for elimination of hyperalgesia and neurogenic inflammation. J. Neurosurg. 2005, 102:522-525.
42. Treede R.D., Meyer R.A., Raja S.N., Campbell J.N. Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J. Physiol. 1995, 483(Pt 3):747-758.
43. White F.A., Silos-Santiago I., Molliver D.C., Nishimura M., Phillips H., Barbacid M., Snider W.D. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J. Neurosci. 1996, 16:4662-4672.
44. Zirlinger M., Lo L., McMahon J., McMahon A.P., Anderson D.J. Transient expression of the bHLH factor neurogenin-2 marks a subpopulation of neural crest cells biased for a sensory but not a neuronal fate. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:8084-8089.