Epibranchial placode-derived neurons produce BDNF required for early sensory neuron development.
In mice, BDNF provided by the developing taste epithelium is required for gustatory neuron survival following target innervation. However, we find that expression of BDNF, as detected by BDNF-driven β-galactosidase, begins in the cranial ganglia before its expression in the central (hindbrain) or peripheral (taste papillae) targets of these sensory neurons, and before gustatory ganglion cells innervate either target. To test early BDNF function, we examined the ganglia of bdnf null mice before target innervation, and found that while initial neuron survival is unaltered, early neuron development is disrupted. In addition, fate mapping analysis in mice demonstrates that murine cranial ganglia arise from two embryonic populations, i.e., epibranchial placodes and neural crest, as has been described for these ganglia in non-mammalian vertebrates. Only placodal neurons produce BDNF, however, which indicates that prior to innervation, early ganglionic BDNF produced by placode-derived cells promotes gustatory neuron development.
Department of Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA.
Danielle E
DE
Harlow
Hui
H
Yang
Trevor
T
Williams
Linda A
LA
Barlow
D000818:Animals; D019208:Brain-Derived Neurotrophic Factor / Q000235:genetics / Q000378:metabolism*; D004848:Epithelium / Q000196:embryology / Q000294:innervation; D005260:Female; D005724:Ganglia / Q000166:cytology / Q000502:physiology; D051379:Mice; D008810:Mice, Inbred C57BL; D018345:Mice, Knockout; D055495:Neurogenesis / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000378:metabolism*; D011247:Pregnancy; D020813:Receptor, trkB / Q000235:genetics / Q000378:metabolism; D011984:Sensory Receptor Cells / Q000166:cytology / Q000502:physiology*; D013650:Taste Buds / Q000166:cytology* / Q000196:embryology* / Q000378:metabolism; D014059:Tongue / Q000196:embryology / Q000294:innervation / Q000502:physiology
D019208:Brain-Derived Neurotrophic Factor; D020813:Receptor, trkB
Development. 1996 Jun;122(6):1965-73
8674435
J Neurosci. 1999 May 1;19(9):3507-18
10212310
Dev Biol. 1998 Dec 15;204(2):327-44
9882474
J Neurosci. 1997 Dec 1;17(23):9113-21
9364058
Development. 1992 Sep;116(1):201-11
1483388
J Neural Transm (Vienna). 1998;105(2-3):253-63
9660103
Neurobiol Aging. 2007 Jul;28(7):1088-98
16769156
J Neurosci. 2005 Jun 29;25(26):6251-9
15987955
Science. 1991 Oct 11;254(5029):282-5
1925583
Acta Anat (Basel). 1997;160(3):139-58
9718388
Nature. 1995 Mar 30;374(6521):450-3
7700353
Dev Biol. 2010 Apr 15;340(2):419-29
20122917
Neuroscience. 2005;134(4):1301-8
16054764
Science. 2002 Nov 8;298(5596):1245-8
12424382
Mech Dev. 2000 May;93(1-2):161-4
10781949
J Neurosci. 1998 Sep 15;18(18):7336-50
9736654
Mol Endocrinol. 2001 Oct;15(10):1748-57
11579207
Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3247-51
8159733
Nature. 1995 May 18;375(6528):235-8
7746324
Anat Rec. 1946 Feb;94:239-47
21015608
Science. 2008 Apr 18;320(5874):369-73
18323418
J Neurosci. 2009 Mar 18;29(11):3354-64
19295142
J Neurosci. 2000 May 1;20(9):3165-74
10777780
Auton Neurosci. 2006 Jun 30;126-127:30-8
16632412
J Neurocytol. 2004 Dec;33(6):617-29
16217618
Dev Biol. 2003 Dec 15;264(2):467-81
14651931
Neuron. 1998 Mar;20(3):483-94
9539123
J Comp Neurol. 1981 Dec 20;203(4):555-73
7035504
Development. 2005 Oct;132(19):4285-98
16141221
Nat Neurosci. 2007 Sep;10(9):1089-93
17726474
Dev Biol. 1982 Dec;94(2):291-310
7152108
Development. 1994 Aug;120(8):2213-24
7925022
Dev Biol. 2006 Apr 15;292(2):457-68
16500639
Neuron. 1992 Sep;9(3):449-63
1345671
J Comp Neurol. 1985 Apr 8;234(2):192-200
3838758
J Comp Neurol. 1995 May 8;355(3):427-54
7636024
Mol Cell Neurosci. 2002 Nov;21(3):502-11
12498790
J Neurosci. 1997 Nov 15;17(22):8667-75
9348335
Brain Res Mol Brain Res. 1999 May 7;68(1-2):1-13
10320778
J Comp Neurol. 1983 Nov 10;220(4):378-95
6643734
Dev Biol. 2001 Apr 15;232(2):508-21
11401409
Brain Res Brain Res Rev. 2005 Jun;48(3):457-76
15914252
Brain Cell Biol. 2006 Jun;35(2-3):187-201
17957483
J Comp Neurol. 2000 Jul 10;422(4):579-93
10861527
Dev Dyn. 1999 Aug;215(4):332-43
10417822
J Neurocytol. 2004 May;33(3):331-43
15475688
Development. 2004 May;131(10):2257-68
15102710
J Mol Biol. 1995 Sep 22;252(3):289-95
7563050
Am J Anat. 1985 Oct;174(2):105-18
4061337
Dev Biol. 2001 Nov 15;239(2):323-37
11784038
Mol Cell Neurosci. 2008 Nov;39(3):372-83
18718867
Nature. 2001 Feb 8;409(6821):729-33
11217863
Genes Dev. 2001 Jan 1;15(1):66-78
11156606
Adv Anat Embryol Cell Biol. 1982;74:1-90
7090875
J Exp Zool. 1961 Nov;148:91-123
13904079
Nature. 1995 May 18;375(6528):238-41
7746325
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14661-8
11717413
Brain Res. 1984 Aug 13;308(2):354-9
6206923
Anat Embryol (Berl). 2001 Aug;204(2):135-51
11556529
J Comp Neurol. 1995 Oct 2;360(4):698-704
8801260
J Neurosci. 2003 Jul 30;23(17):6856-65
12890780
Mol Cell Neurosci. 1996 Feb;7(2):143-51
8731482
FASEB J. 1995 Oct;9(13):1277-87
7557017
Trends Neurosci. 1997 Apr;20(4):159-64
9106356
Dev Biol. 2001 Apr 1;232(1):1-61
11254347
EMBO J. 2000 Mar 15;19(6):1290-300
10716929
J Neurosci. 1999 Nov 15;19(22):9928-38
10559401
Chem Senses. 2008 Jul;33(6):531-9
18495654
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3957-61
15004273
Neuroreport. 1997 Mar 3;8(4):1013-7
9141083
Neuron. 1991 Nov;7(5):819-30
1742027
Dev Biol. 2008 Feb 1;314(1):171-88
18164701
Nature. 1994 Mar 10;368(6467):147-50
8139657
Neuron. 1995 Jul;15(1):89-103
7619533
Harvey Lect. 1984-1985;80:137-86
6400655
J Comp Neurol. 1994 Feb 22;340(4):515-30
8006215
Neuron. 2008 Aug 14;59(3):399-412
18701066
Dev Biol. 1988 Apr;126(2):420-32
2450797
Curr Biol. 1998 Dec 3;8(24):1323-6
9843687
J Comp Neurol. 1996 Dec 23;376(4):587-602
8978472
Neuron. 1992 Jul;9(1):139-50
1321644
Am J Anat. 1983 Apr;166(4):445-68
6858941
Invest Ophthalmol Vis Sci. 1999 Nov;40(12):2996-3005
10549663
Acta Neuropathol. 2001 May;101(5):483-90
11484820
Dev Cell. 2002 Jul;3(1):25-38
12110165
J Comp Neurol. 2003 Apr 21;459(1):15-24
12629664
Dev Biol. 2000 Jun 15;222(2):296-306
10837119
Dev Biol. 1995 May;169(1):273-85
7750643
Development. 2000 Mar;127(6):1161-72
10683170
Neuron. 1995 Jul;15(1):105-14
7619514
Curr Opin Neurobiol. 1997 Feb;7(1):110-8
9039802
Nat Genet. 1999 Jan;21(1):70-1
9916792
J Comp Neurol. 1991 Feb 8;304(2):172-86
2016415
Int J Dev Neurosci. 1997 Jul;15(4-5):563-76
9263033
Brain Res Bull. 2006 Jun 15;70(1):33-43
16750480
Development. 1993 Jul;118(3):989-1001
8076530
Development. 1997 Apr;124(7):1333-42
9118804
Physiol Rev. 1968 Jul;48(3):534-69
4875350
Curr Opin Genet Dev. 2002 Oct;12(5):565-71
12200162
J Anat. 1955 Apr;89(2):133-52
14367209
J Neurosci. 2002 Aug 1;22(15):6309-14
12151506
Development. 2000 Jul;127(14):3045-56
10862742
Dev Biol. 2007 Oct 15;310(2):317-28
17826760
J Comp Neurol. 1995 Jan 23;351(4):489-98
7536754
J Comp Neurol. 1999 Jun 21;409(1):13-24
10363708
J Anat. 1998 Jan;192 ( Pt 1):91-8
9568564
Arch Physiol Biochem. 1998 Jul;106(3):161-202
10099715
J Comp Neurol. 1984 Feb 10;223(1):124-37
6608534
Nat Neurosci. 2008 Nov;11(11):1283-93
18849985
Cell. 1994 Mar 25;76(6):989-99
8137432
Neuroscience. 2003;121(2):341-54
14521993
Anat Rec. 1997 May;248(1):137-41
9143677
Am J Physiol. 1987 Feb;252(2 Pt 2):R247-51
3812762
Nat Neurosci. 2008 Mar;11(3):269-76
18278043
J Comp Neurol. 2007 Jun 10;502(5):673-82
17436285
Development. 2000 Nov;127(22):4775-85
11044393
Science. 2001 Oct 19;294(5542):595-8
11641498
J Neurosci Res. 1999 Sep 15;57(6):759-69
10467247
Exp Brain Res. 1971 Nov 30;13(5):461-88
5137297
Eur J Neurosci. 1992 Oct;4(11):1140-1158
12106420
Neurosci Lett. 2002 Jul 12;327(1):49-52
12098498
Brain Res. 1977 Jan 31;121(1):21-41
64284
Dev Neurosci. 2008;30(1-3):33-5
18075252