Neuronal Migration Generates New Populations of Neurons That Develop Unique Connections, Physiological Properties and Pathologies
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
Grantová podpora
R21 DC017589
NIDCD NIH HHS - United States
PubMed
31069224
PubMed Central
PMC6491807
DOI
10.3389/fcell.2019.00059
Knihovny.cz E-zdroje
- Klíčová slova
- differential function, neuronal functionality, neuronal migration, neuronal pathfinding, neuronal pathology,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Central nervous system neurons become postmitotic when radial glia cells divide to form neuroblasts. Neuroblasts may migrate away from the ventricle radially along glia fibers, in various directions or even across the midline. We present four cases of unusual migration that are variably connected to either pathology or formation of new populations of neurons with new connectivities. One of the best-known cases of radial migration involves granule cells that migrate from the external granule cell layer along radial Bergman glia fibers to become mature internal granule cells. In various medulloblastoma cases this migration does not occur and transforms the external granule cell layer into a rapidly growing tumor. Among the ocular motor neurons is one unique population that undergoes a contralateral migration and uniquely innervates the superior rectus and levator palpebrae muscles. In humans, a mutation of a single gene ubiquitously expressed in all cells, induces innervation defects only in this unique motor neuron population, leading to inability to elevate eyes or upper eyelids. One of the best-known cases for longitudinal migration is the facial branchial motor (FBM) neurons and the overlapping inner ear efferent population. We describe here molecular cues that are needed for the caudal migration of FBM to segregate these motor neurons from the differently migrating inner ear efferent population. Finally, we describe unusual migration of inner ear spiral ganglion neurons that result in aberrant connections with disruption of frequency presentation. Combined, these data identify unique migratory properties of various neuronal populations that allow them to adopt new connections but also sets them up for unique pathologies.
Department of Biological Sciences Western Michigan University Kalamazoo MI United States
Department of Biology University of Iowa Iowa City IA United States
Department of Otolaryngology University of Iowa Iowa City IA United States
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Allen N. J., Lyons D. A. (2018). Glia as architects of central nervous system formation and function. Science 362 181–185. 10.1126/science.aat0473 PubMed DOI PMC
Bixby J. L., Lilien J., Reichardt L. F. (1988). Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J. Cell Biol. 107 353–361. 10.1083/jcb.107.1.353 PubMed DOI PMC
Bjorke B., Shoja-Taheri F., Kim M., Robinson G. E., Fontelonga T., Kim K. T., et al. (2016). Contralateral migration of oculomotor neurons is regulated by Slit/Robo signaling. Neural Dev. 11:18. PubMed PMC
Cantone M., Kuspert M., Reiprich S., Lai X., Eberhardt M., Gottle P., et al. (2019). A gene regulatory architecture that controls region-independent dynamics of oligodendrocyte differentiation. Glia 67 825–843. 10.1002/glia.23569 PubMed DOI
Cheng L., Desai J., Miranda C. J., Duncan J. S., Qiu W., Nugent A. A., et al. (2014). Human CFEOM1 mutations attenuate KIF21A autoinhibition and cause oculomotor axon stalling. Neuron 82 334–349. 10.1016/j.neuron.2014.02.038 PubMed DOI PMC
Dallos P., Wu X., Cheatham M. A., Gao J., Zheng J., Anderson C. T., et al. (2008). Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58 333–339. 10.1016/j.neuron.2008.02.028 PubMed DOI PMC
Driver A., Shumrick C., Stottmann R. (2017). Ttc21b is required in bergmann glia for proper granule cell radial migration. J. Dev. Biol. 5:E18. 10.3390/jdb5040018 PubMed DOI PMC
Duncan J. S., Fritzsch B. (2013). Continued expression of GATA3 is necessary for cochlear neurosensory development. PLoS One 8:e62046. 10.1371/journal.pone.0062046 PubMed DOI PMC
Dupin E., Calloni G. W., Coelho-Aguiar J. M., Le Douarin N. M. (2018). The issue of the multipotency of the neural crest cells. Dev. Biol. 444(Suppl. 1) S47–S59. 10.1016/j.ydbio.2018.03.024 PubMed DOI
Elliott K. L., Fritzsch B., Duncan J. S. (2018). Evolutionary and developmental biology provide insights into the regeneration of organ of corti hair cells. Front. Cell. Neurosci. 12:252. 10.3389/fncel.2018.00252 PubMed DOI PMC
Flora A., Klisch T. J., Schuster G., Zoghbi H. Y. (2009). Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. Science 326 1424–1427. 10.1126/science.1181453 PubMed DOI PMC
Fritzsch B. (1998). Of mice and genes: evolution of vertebrate brain development. Brain Behav. Evol. 52 207–217. 10.1159/000006564 PubMed DOI
Fritzsch B., Beisel K., Jones K., Farinas I., Maklad A., Lee J., et al. (2002). Development and evolution of inner ear sensory epithelia and their innervation. J. Neurobiol. 53 143–156. 10.1002/neu.10098 PubMed DOI PMC
Fritzsch B., Elliott K. L. (2017). Evolution and development of the inner ear efferent system: transforming a motor neuron population to connect to the most unusual motor protein via ancient nicotinic receptors. Front. Cell. Neurosci. 11:114. 10.3389/fncel.2017.00114 PubMed DOI PMC
Fritzsch B., Elliott K. L., Glover J. C. (2017). Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature. Cell Tissue Res. 370 195–209. 10.1007/s00441-017-2676-y PubMed DOI PMC
Fritzsch B., Elliott K. L., Pavlinkova G. (2019). Primary sensory map formations reflect unique needs molecular cues specific to each sensory system. F1000Res. 8:345. 10.12688/f1000research.17717.1 PubMed DOI PMC
Fritzsch B., Glover J. (2007). “Evolution of the deuterostome central nervous system: an intercalation of developmental patterning processes with cellular specification processes,” in Evolution of Nervous Systems Vol. 2 ed. Kaas J. H. (Oxford: Academic Press; ), 1–24. 10.1016/b0-12-370878-8/00125-7 DOI
Fritzsch B., Nichols D. (1993). DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Hear. Res. 65 51–60. 10.1016/0378-5955(93)90200-k PubMed DOI
Fritzsch B., Nichols D., Echelard Y., McMahon A. (1995). Development of midbrain and anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice. J. Neurobiol. 27 457–469. 10.1002/neu.480270403 PubMed DOI
Fritzsch B., Northcutt R. G. (1993). Origin and migration of trochlear, oculomotor and abducent motor neurons in Petromyzon marinus L. Dev. Brain Res. 74 122–126. 10.1016/0165-3806(93)90091-n PubMed DOI
Fritzsch B., Pan N., Jahan I., Elliott K. L. (2015). Inner ear development: building a spiral ganglion and an organ of Corti out of unspecified ectoderm. Cell Tissue Res. 361 7–24. 10.1007/s00441-014-2031-5 PubMed DOI PMC
Fritzsch B., Sonntag R., Dubuc R., Ohta Y., Grillner S. (1990). Organization of the six motor nuclei innervating the ocular muscles in lamprey. J. Comp. Neurol. 294 491–506. 10.1002/cne.902940402 PubMed DOI
Frotscher M. (1997). Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res. 290 315–322. 10.1007/978-3-642-60905-3_17 PubMed DOI
Glasco D. M., Pike W., Qu Y., Reustle L., Misra K., Di Bonito M., et al. (2016). The atypical cadherin Celsr1 functions non-cell autonomously to block rostral migration of facial branchiomotor neurons in mice. Dev. Biol. 417 40–49. 10.1016/j.ydbio.2016.07.004 PubMed DOI PMC
Glover J. C., Elliott K. L., Erives A., Chizhikov V. V., Fritzsch B. (2018). Wilhelm His’ lasting insights into hindbrain and cranial ganglia development and evolution. Dev. Biol. 444(Suppl. 1) S14–S24. 10.1016/j.ydbio.2018.02.001 PubMed DOI PMC
Goodrich L. (2016). The Primary Auditory Neurons of the Mammalian Cochlea. Berlin: Springer.
Goodrich L. V., Milenković L., Higgins K. M., Scott M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 1109–1113. 10.1126/science.277.5329.1109 PubMed DOI
Gruner H. N., Kim M., Mastick G. S. (2019). Robo1 and 2 repellent receptors cooperate to guide facial neuron cell migration and axon projections in the embryonic mouse hindbrain. Neuroscience 402 116–129. 10.1016/j.neuroscience.2019.01.017 PubMed DOI PMC
Han A. Y., Gupta S., Novitch B. G. (2018). Molecular specification of facial branchial motor neurons in vertebrates. Dev. Biol. 436 5–13. 10.1016/j.ydbio.2018.01.019 PubMed DOI
Herculano-Houzel S. (2009). The human brain in numbers: a linearly scaled-up primate brain. Front. Hum. Neurosci. 3:31. 10.3389/neuro.09.031.2009 PubMed DOI PMC
Horn Z., Behesti H., Hatten M. E. (2018). N-cadherin provides a cis and trans ligand for astrotactin that functions in glial-guided neuronal migration. Proc. Natl. Acad. Sci. U.S.A. 115 10556–10563. 10.1073/pnas.1811100115 PubMed DOI PMC
Jacob A., Wüst H. M., Thalhammer J. M., Fröb F., Küspert M., Reiprich S., et al. (2018). The transcription factor prospero homeobox protein 1 is a direct target of SoxC proteins during developmental vertebrate neurogenesis. J. Neurochem. 146 251–268. 10.1111/jnc.14456 PubMed DOI
Jahan I., Kersigo J., Pan N., Fritzsch B. (2010). Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell Tissue Res. 341 95–110. 10.1007/s00441-010-0984-6 PubMed DOI PMC
Karis A., Pata I., van Doorninck J. H., Grosveld F., de Zeeuw C. I., de Caprona D., et al. (2001). Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J. Comp. Neurol. 429 615–630. 10.1002/1096-9861(20010122)429:4<615::AID-CNE8>3.0.CO;2-F PubMed DOI
Kousa Y. A., Zhu H., Fakhouri W. D., Lei Y., Kinoshita A., Roushangar R. R., et al. (2019). The TFAP2A–IRF6–GRHL3 genetic pathway is conserved in neurulation. Hum. Mol. Genet. PubMed PMC
Leto K., Arancillo M., Becker E. B., Buffo A., Chiang C., Ding B., et al. (2016). Consensus paper: cerebellar development. Cerebellum 15 789–828. PubMed PMC
Lilien J., Balsamo J. (2005). The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin. Curr. Opin. Cell Biol. 17 459–465. 10.1016/j.ceb.2005.08.009 PubMed DOI
Lindsley A., Snider P., Zhou H., Rogers R., Wang J., Olaopa M., et al. (2007). Identification and characterization of a novel Schwann and outflow tract endocardial cushion lineage-restricted periostin enhancer. Dev. Biol. 307 340–355. 10.1016/j.ydbio.2007.04.041 PubMed DOI PMC
Macova I., Pysanenko K., Chumak T., Dvorakova M., Bohuslavova R., Syka J., et al. (2019). Neurod1 is essential for the primary tonotopic organization and related auditory information processing in the midbrain. J. Neurosci. 39 984–1004. 10.1523/JNEUROSCI.2557-18.2018 PubMed DOI PMC
Manns M., Fritzsch B. (1992). Retinoic acid affects the organization of reticulospinal neurons in developing Xenopus. Neurosci. Lett. 139 253–256. 10.1016/0304-3940(92)90565-o PubMed DOI
Mao Y., Reiprich S., Wegner M., Fritzsch B. (2014). Targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in the mouse inner ear. PLoS One 9:e94580. 10.1371/journal.pone.0094580 PubMed DOI PMC
Matei V., Pauley S., Kaing S., Rowitch D., Beisel K. W., Morris K., et al. (2005). Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 234 633–650. 10.1002/dvdy.20551 PubMed DOI PMC
Morris J. K., Maklad A., Hansen L. A., Feng F., Sorensen C., Lee K. F., et al. (2006). A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res. 1091 186–199. 10.1016/j.brainres.2006.02.090 PubMed DOI PMC
Morrissy A. S., Cavalli F. M., Remke M., Ramaswamy V., Shih D. J., Holgado B. L., et al. (2017). Spatial heterogeneity in medulloblastoma. Nat. Genet. 49 780–788. 10.1038/ng.3838 PubMed DOI PMC
Müller M., Jabs N., Lork D. E., Fritzsch B., Sander M. (2003). Nkx6. 1 controls migration and axon pathfinding of cranial branchio-motoneurons. Development 130 5815–5826. 10.1242/dev.00815 PubMed DOI
Murakami Y., Uchida K., Rijli F. M., Kuratani S. (2005). Evolution of the brain developmental plan: insights from agnathans. Dev. Biol. 280 249–259. 10.1016/j.ydbio.2005.02.008 PubMed DOI
Naujoks-Manteuffel C., Sonntag R., Fritzsch B. (1991). Development of the amphibian oculomotor complex: evidences for migration of oculomotor motoneurons across the midline. Anat. Embryol. 183 545–552. PubMed
Northcott P. A., Korshunov A., Pfister S. M., Taylor M. D. (2012). The clinical implications of medulloblastoma subgroups. Nat. Rev. Neurol. 8 340–351. 10.1038/nrneurol.2012.78 PubMed DOI
Pan N., Jahan I., Lee J. E., Fritzsch B. (2009). Defects in the cerebella of conditional Neurod1 null mice correlate with effective Tg (Atoh1-cre) recombination and granule cell requirements for Neurod1 for differentiation. Cell Tissue Res. 337 407–428. 10.1007/s00441-009-0826-6 PubMed DOI PMC
Parker H. J., Bronner M. E., Krumlauf R. (2016). The vertebrate Hox gene regulatory network for hindbrain segmentation: evolution and diversification: coupling of a Hox gene regulatory network to hindbrain segmentation is an ancient trait originating at the base of vertebrates. Bioessays 38 526–538. 10.1002/bies.201600010 PubMed DOI
Puelles L. (1978). A Golgi-study of oculomotor neuroblasts migrating across the midline in chick embryos. Anat. Embryol. 152 205–215. 10.1007/bf00315925 PubMed DOI
Reiprich S., Wegner M. (2015). From CNS stem cells to neurons and glia: sox for everyone. Cell Tissue Res. 359 111–124. 10.1007/s00441-014-1909-6 PubMed DOI
Saito Y., Miranda-Rottmann S., Ruggiu M., Park C. Y., Fak J. J., Zhong R., et al. (2016). NOVA2-mediated RNA regulation is required for axonal pathfinding during development. eLife 5:e14371. 10.7554/eLife.14371 PubMed DOI PMC
Schuller U., Heine V. M., Mao J., Kho A. T., Dillon A. K., Han Y. G., et al. (2008). Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14 123–134. 10.1016/j.ccr.2008.07.005 PubMed DOI PMC
Sidman R. L., Rakic P. (1973). Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62 1–35. 10.1016/0006-8993(73)90617-3 PubMed DOI
Simmons D., Duncan J., de Caprona D. C., Fritzsch B. (2011). Development of the Inner Ear Efferent System, Auditory and Vestibular Efferents. Berlin: Springer, 187–216.
Tan I.-L., Wojcinski A., Rallapalli H., Lao Z., Sanghrajka R. M., Stephen D., et al. (2018). Lateral cerebellum is preferentially sensitive to high sonic hedgehog signaling and medulloblastoma formation. Proc. Natl. Acad. Sci. U.S.A. 115 3392–3397. 10.1073/pnas.1717815115 PubMed DOI PMC
Taylor M. D., Northcott P. A., Korshunov A., Remke M., Cho Y.-J., Clifford S. C., et al. (2012). Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 123 465–472. 10.1007/s00401-011-0922-z PubMed DOI PMC
Tomasetti C., Vogelstein B. (2015a). Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 347 78–81. 10.1126/science.1260825 PubMed DOI PMC
Tomasetti C., Vogelstein B. (2015b). Musings on the theory that variation in cancer risk among tissues can be explained by the number of divisions of normal stem cells. arXiv:1501.05035 [Preprint]. PubMed PMC
von Bartheld C. S., Bahney J., Herculano-Houzel S. (2016). The search for true numbers of neurons and glial cells in the human brain: a review of 150 years of cell counting. J. Comp. Neurol. 524 3865–3895. 10.1002/cne.24040 PubMed DOI PMC
Yang T., Bassuk A. G., Stricker S., Fritzsch B. (2014a). Prickle1 is necessary for the caudal migration of murine facial branchiomotor neurons. Cell Tissue Res. 357 549–561. 10.1007/s00441-014-1925-6 PubMed DOI PMC
Yang T., Jia Z., Bryant-Pike W., Chandrasekhar A., Murray J. C., Fritzsch B., et al. (2014b). Analysis of PRICKLE 1 in human cleft palate and mouse development demonstrates rare and common variants involved in human malformations. Mol. Genet. Genomic Med. 2 138–151. 10.1002/mgg3.53 PubMed DOI PMC
Yang T., Kersigo J., Jahan I., Pan N., Fritzsch B. (2011). The molecular basis of making spiral ganglion neurons and connecting them to hair cells of the organ of Corti. Hear. Res. 278 21–33. 10.1016/j.heares.2011.03.002 PubMed DOI PMC
Zarei S., Zarei K., Fritzsch B., Elliott K. L. (2017). Sonic hedgehog antagonists reduce size and alter patterning of the frog inner ear. Dev. Neurobiol. 77 1385–1400. 10.1002/dneu.22544 PubMed DOI PMC