Isl1 Is required for multiple aspects of motor neuron development

Molecular and Cellular Neuroscience

Volumn 47, Issue 3, 2011, Pages 215-222

  Liang, Xingqun ^a,b   Song, Mi Ryoung ^c   Xu, ZengGuang ^a   Lanuza, Guillermo M ^d   Liu, Yali ^a   Zhuang, Tao ^a   Chen, Yihan ^a   Pfaff, Samuel L ^e   Evans, Sylvia M ^b,c   Sun, Yunfu ^a,b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

^d FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Axon growth; Cell death; Cranial ganglia; Isl1; Motor neuron; V2 interneuron

Indexed keywords

LIM HOMEODOMAIN TRANSCRIPTION FACTOR ISLET1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GANGLION; MOTONEURON; MOUSE; MUTANT; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; SURVIVAL;

ANIMALS; AXONS; EMBRYONIC DEVELOPMENT; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; SPINAL CORD;

EID: 79957664709     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.04.007     Document Type: Article

References (49)

1. Ahlgren U., Pfaff S.L., Jessell T.M., Edlund T., Edlund H. Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 1997, 385:257-260.
2. Appel B., Korzh V., Glasgow E., Thor S., Edlund T., Dawid I.B., Eisen J.S. Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 1995, 121:4117-4125.
3. Arber S., Han B., Mendelsohn M., Smith M., Jessell T.M., Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 1999, 23:659-674.
4. Begbie J., Graham A. Integration between the epibranchial placodes and the hindbrain. Science 2001, 294:595-598.
5. Broihier H.T., Skeath J.B. Drosophila homeodomain protein dHb9 directs neuronal fate via crossrepressive and cell-nonautonomous mechanisms. Neuron 2002, 35:39-50.
6. Burgess R.W., Jucius T.J., Ackerman S.L. Motor axon guidance of the mammalian trochlear and phrenic nerves: dependence on the netrin receptor Unc5c and modifier loci. J. Neurosci. 2006, 26:5756-5766.
7. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 2003, 5:877-889.
8. Chen H., Bagri A., Zupicich J.A., Zou Y., Stoeckli E., Pleasure S.J., Lowenstein D.H., Skarnes W.C., Chedotal A., Tessier-Lavigne M. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 2000, 25:43-56.
9. Dickson B.J. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964.
10. Elshatory Y., Gan L. The LIM-homeobox gene Islet-1 is required for the development of restricted forebrain cholinergic neurons. J. Neurosci. 2008, 28:3291-3297.
11. Elshatory Y., Everhart D., Deng M., Xie X., Barlow R.B., Gan L. Islet-1 controls the differentiation of retinal bipolar and cholinergic amacrine cells. J. Neurosci. 2007, 27:12707-12720.
12. Ericson J., Thor S., Edlund T., Jessell T.M., Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 1992, 256:1555-1560.
13. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 1997, 90:169-180.
14. Giger R.J., Cloutier J.F., Sahay A., Prinjha R.K., Levengood D.V., Moore S.E., Pickering S., Simmons D., Rastan S., Walsh F.S., Kolodkin A.L., Ginty D.D., Geppert M. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 2000, 25:29-41.
15. Haase G., Dessaud E., Garces A., de Bovis B., Birling M., Filippi P., Schmalbruch H., Arber S., deLapeyriere O. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 2002, 35:893-905.
16. Inoue A., Takahashi M., Hatta K., Hotta Y., Okamoto H. Developmental regulation of islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev. Dyn. 1994, 199:1-11.
17. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
18. Kawasaki T., Kitsukawa T., Bekku Y., Matsuda Y., Sanbo M., Yagi T., Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999, 126:4895-4902.
19. Klein R. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr. Opin. Cell Biol. 2004, 16:580-589.
20. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., Lin L.Z., Cai C.L., Lu M.M., Reth M., Platoshyn O., Yuan J.X., Evans S., Chien K.R. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 433:647-653.
21. Lee S.K., Pfaff S.L. Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 2003, 38:731-745.
22. Lee S.K., Jurata L.W., Funahashi J., Ruiz E.C., Pfaff S.L. Analysis of embryonic motoneuron gene regulation: derepression of general activators function in concert with enhancer factors. Development 2004, 131:3295-3306.
23. Lee S., Lee B., Joshi K., Pfaff S.L., Lee J.W., Lee S.K. A regulatory network to segregate the identity of neuronal subtypes. Dev. Cell 2008, 14:877-889.
24. Lendahl U., Zimmerman L.B., McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 1990, 60:585-595.
25. Lundgren S.E., Callahan C.A., Thor S., Thomas J.B. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 1995, 121:1769-1773.
26. Nakano T., Windrem M., Zappavigna V., Goldman S.A. Identification of a conserved 125 base-pair Hb9 enhancer that specifies gene expression to spinal motor neurons. Dev. Biol. 2005, 283:474-485.
27. Pan L., Deng M., Xie X., Gan L. ISL1 and BRN3B co-regulate the differentiation of murine retinal ganglion cells. Development 2008, 135:1981-1990.
28. Pfaff S.L., Mendelsohn M., Stewart C.L., Edlund T., Jessell T.M. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 1996, 84:309-320.
29. Price S.R., De Marco Garcia N.V., Ranscht B., Jessell T.M. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 2002, 109:205-216.
30. Segawa H., Miyashita T., Hirate Y., Higashijima S., Chino N., Uyemura K., Kikuchi Y., Okamoto H. Functional repression of Islet-2 by disruption of complex with Ldb impairs peripheral axonal outgrowth in embryonic zebrafish. Neuron 2001, 30:423-436.
31. Sharma K., Sheng H.Z., Lettieri K., Li H., Karavanov A., Potter S., Westphal H., Pfaff S.L. LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 1998, 95:817-828.
32. Shirasaki R., Pfaff S.L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 2002, 25:251-281.
33. Shirasaki R., Lewcock J.W., Lettieri K., Pfaff S.L. FGF as a target-derived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 2006, 50:841-853.
34. Song M.R., Sun Y., Bryson A., Gill G.N., Evans S.M., Pfaff S.L. Islet-to-LMO stoichiometries control the function of transcription complexes that specify motor neuron and V2a interneuron identity. Development 2009, 136:2923-2932.
35. Sun Y., Liang X., Najafi N., Cass M., Lin L., Cai C.L., Chen J., Evans S.M. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev. Biol. 2007, 304:286-296.
36. Sun Y., Dykes I.M., Liang X., Eng S.R., Evans S.M., Turner E.E. A central role for Islet1 in sensory neuron development linking sensory and spinal gene regulatory programs. Nat. Neurosci. 2008, 11:1283-1293.
37. Takashima S., Kitakaze M., Asakura M., Asanuma H., Sanada S., Tashiro F., Niwa H., Miyazaki Ji J., Hirota S., Kitamura Y., Kitsukawa T., Fujisawa H., Klagsbrun M., Hori M. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3657-3662.
38. Tanabe Y., Jessell T.M. Diversity and pattern in the developing spinal cord. Science 1996, 274:1115-1123.
39. Tanabe Y., William C., Jessell T.M. Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 1998, 95:67-80.
40. Tanaka H., Nojima Y., Shoji W., Sato M., Nakayama R., Ohshima T., Okamoto H. Islet1 selectively promotes peripheral axon outgrowth in Rohon-Beard primary sensory neurons. Dev. Dyn. 2011, 240:9-22.
41. Thaler J., Harrison K., Sharma K., Lettieri K., Kehrl J., Pfaff S.L. Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 1999, 23:675-687.
42. Thaler J.P., Lee S.K., Jurata L.W., Gill G.N., Pfaff S.L. LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 2002, 110:237-249.
43. Thaler J.P., Koo S.J., Kania A., Lettieri K., Andrews S., Cox C., Jessell T.M., Pfaff S.L. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 2004, 41:337-350.
44. Thor S., Thomas J.B. The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 1997, 18:397-409.
45. Thor S., Ericson J., Brannstrom T., Edlund T. The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 1991, 7:881-889.
46. Thor S., Andersson S.G., Tomlinson A., Thomas J.B. A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 1999, 397:76-80.
47. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 1994, 79:957-970.
48. Wang H.F., Liu F.C. Developmental restriction of the LIM homeodomain transcription factor Islet-1 expression to cholinergic neurons in the rat striatum. Neuroscience 2001, 103:999-1016.
49. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.