Abstract
After exiting the hindbrain, branchial motor axons reach their targets in association with sensory ganglia. The trigeminal ganglion has been shown to promote motor axon growth from rhombomeres 2/3 and 4/5, but it is unknown whether this effect is ganglion specific and through which signals it is mediated. Here, we addressed these questions by co-cultures of ventral rhombomere 8 explants with cranial and spinal sensory ganglia in a collagen gel matrix. Our results show that all cranial sensory ganglia and even a trunk dorsal root ganglion can promote motor axon growth and that ganglia isolated from older embryos had a stronger effect on the axonal growth than younger ones. We found that brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) are necessary and sufficient for this effect. Altogether, our results demonstrate that the promoting effect of sensory ganglia on cranial motor axon growth is stage dependent, but not ganglion specific and is mediated by BDNF and NGF signals.
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Avivi C, Goldstein RS (2003) Differing patterns of neurotrophin-receptor expressing neurons allow distinction of the transient Frorieps’ ganglia from normal DRG before morphological differences appear. Brain Res Dev Brain Res 145:49–59
Avivi C, Cui S, Goren S, Goldstein RS (2002) Differences in neuronal differentiation between the transient cranial (Frorieps’) and normal dorsal root ganglia. Brain Res Dev Brain Res 135:19–28
Bai Z, Pu Q, Haque Z, Wang J, Huang R (2016) The unique axon trajectory of the accessory nerve is determined by intrinsic properties of the neural tube in the avian embryo. Ann Anat 205:85–89
Caton A, Hacker A, Naeem A, Livet J, Maina F, Bladt F, Klein R, Birchmeier C, Guthrie S (2000) The branchial arches and HGF are growth-promoting and chemoattractant for cranial motor axons. Development 127:1751–1766
Chandrasekhar A (2004) Turning heads: development of vertebrate branchiomotor neurons. Dev Dyn 229:143–161
Cho KH, Jang HS, Cheong JS, Rodriguez-Vazquez JF, Murakami G, Abe H (2015) Sensory pathways in the human embryonic spinal accessory nerve with special reference to the associated lower cranial nerve ganglia. Childs Nerv Syst 31:95–99
Clarke JD, Lumsden A (1993) Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. Development 118:151–162
Ernfors P, Ibanez CF, Ebendal T, Olson L, Persson H (1990) Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proc Natl Acad Sci USA 87:5454–5458
Fraser S, Keynes R, Lumsden A (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344:431–435
Froriep A (1882) Über ein Ganglion des Hypoglossus und Wirbelanlagen in der Occipitalregion. Arch Anat Physiol Anat Abt S:279–302
Froriep A, Beck W (1895) Über des Vorkommen dorsaler Hypoglossuswurzeln mit Ganglion, in der Reihe der Säugetiere. Anat Anz 10:688–696
Geffen R, Goldstein RS (1996) Rescue of sensory ganglia that are programmed to degenerate in normal development: evidence that NGF modulates proliferation of DRG cells in vivo. Dev Biol 178:51–62
Guthrie S (2007) Patterning and axon guidance of cranial motor neurons. Nat Rev Neurosci 8:859–871
Guthrie S, Lumsden A (1992) Motor neuron pathfinding following rhombomere reversals in the chick embryo hindbrain. Development 114:663–673
Guthrie S, Pini A (1995) Chemorepulsion of developing motor axons by the floor plate. Neuron 14:1117–1130
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Harlow DE, Yang H, Williams T, Barlow LA (2011) Epibranchial placode-derived neurons produce BDNF required for early sensory neuron development. Dev Dyn 240:309–323
His W (1888) Centralen u. peripherischen Nervenbahnen beim menschlichen Embryo. Abhandl math-phys Cl Kgl Sachs Ges Wiss 14
Hovorka MS, Uray NJ (2013) Microscopic clusters of sensory neurons in C1 spinal nerve roots and in the C1 level of the spinal accessory nerve in adult humans. Anat Rec (Hoboken) 296:1588–1593
Huang JK, Dorey K, Ishibashi S, Amaya E (2007) BDNF promotes target innervation of Xenopus mandibular trigeminal axons in vivo. BMC Dev Biol 7:59
Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230–232
Jacob J, Guthrie S (2000) Facial visceral motor neurons display specific rhombomere origin and axon pathfinding behavior in the chick. J Neurosci 20:7664–7671
Jacob J, Tiveron MC, Brunet JF, Guthrie S (2000) Role of the target in the pathfinding of facial visceral motor axons. Mol Cell Neurosci 16:14–26
Jacob J, Hacker A, Guthrie S (2001) Mechanisms and molecules in motor neuron specification and axon pathfinding. BioEssays 23:582–595
Kuratani S, Tanaka S, Ishikawa Y, Zukeran C (1988) Early development of the hypoglossal nerve in the chick embryo as observed by the whole-mount nerve staining method. Am J Anat 182:155–168
Lewin GR, Barde YA (1996) Physiology of the neurotrophins. Annu Rev Neurosci 19:289–317
Lim TM, Lunn ER, Keynes RJ, Stern CD (1987) The differing effects of occipital and trunk somites on neural development in the chick embryo. Development 100:525–533
Lumsden A (2004) Segmentation and compartition in the early avian hindbrain. Mech Dev 121:1081–1088
Lumsden A, Keynes R (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424–428
Lumsden A, Sprawson N, Graham A (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113:1281–1291
Moody SA, Heaton MB (1983a) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. I. Ganglion development is necessary for motoneuron migration. J Comp Neurol 213:327–343
Moody SA, Heaton MB (1983b) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. II. Ganglion axon ingrowth guides motoneuron migration. J Comp Neurol 213:344–349
Moody SA, Heaton MB (1983c) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. III. Ganglion perikarya direct motor axon growth in the periphery. J Comp Neurol 213:350–364
Moody SA, Heaton MB (1983d) Ultrastructural observations of the migration and early development of trigeminal motoneurons in chick embryos. J Comp Neurol 216:20–35
Naeem A, Abbas L, Guthrie S (2002) Comparison of the effects of HGF, BDNF, CT-1, CNTF, and the branchial arches on the growth of embryonic cranial motor neurons. J Neurobiol 51:101–114
Pu Q, Bai Z, Haque Z, Wang J, Huang R (2013a) Occipital somites guide motor axons of the accessory nerve in the avian embryo. Neuroscience 246:22–27
Pu Q, Patel K, Berger J, Christ B, Huang R (2013b) Scanning electron microscopic evidence for physical segmental boundaries in the anterior presomitic mesoderm. Ann Anat 195:484–487
Robinson M, Adu J, Davies AM (1996) Timing and regulation of trkB and BDNF mRNA expression in placode-derived sensory neurons and their targets. Eur J Neurosci 8:2399–2406
Steljes TP, Kinoshita Y, Wheeler EF, Oppenheim RW, von Bartheld CS (1999) Neurotrophic factor regulation of developing avian oculomotor neurons: differential effects of BDNF and GDNF. J Neurobiol 41:295–315
Tucker A, Lumsden A, Guthrie S (1996) Cranial motor axons respond differently to the floor plate and sensory ganglia in collagen gel co-cultures. Eur J Neurosci 8:906–916
Tucker KL, Meyer M, Barde YA (2001) Neurotrophins are required for nerve growth during development. Nat Neurosci 4:29–37
Wang L, Klein R, Zheng B, Marquardt T (2011) Anatomical coupling of sensory and motor nerve trajectory via axon tracking. Neuron 71:263–277
Wetmore C, Elde R (1991) Detection and characterization of a sensory microganglion associated with the spinal accessory nerve: a scanning laser confocal microscopic study of the neurons and their processes. J Comp Neurol 305:148–163
Yao L, Zhang D, Bernd P (1994) The onset of neurotrophin and trk mRNA expression in early embryonic tissues of the quail. Dev Biol 165:727–730
Zhou J, Pliego-Rivero B, Bradford HF, Stern GM (1996) The BDNF content of postnatal and adult rat brain: the effects of 6-hydroxydopamine lesions in adult brain. Brain Res Dev Brain Res 97:297–303
Zhou XF, Chie ET, Rush RA (1998) Distribution of brain-derived neurotrophic factor in cranial and spinal ganglia. Exp Neurol 149:237–242
Acknowledgements
We are grateful for the technical assistance of Sandra Graefe in the Institute of Anatomy and Mr. Heinz Bioernsen in the Institute of Animal Science. We thank Developmental Studies Hybridoma Bank, Iowa City, IA, USA, for the antibody. This work was supported by grant of the DFG-Hu 729/10 and DFG-Hu 729/13 to R.H. and by the China Scholarship Council to J.W. and L.L.
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Li, L., Pu, Q., Hintze, M. et al. BDNF and NGF signals originating from sensory ganglia promote cranial motor axon growth. Exp Brain Res 238, 111–119 (2020). https://doi.org/10.1007/s00221-019-05694-w
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DOI: https://doi.org/10.1007/s00221-019-05694-w