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Development of a glial network in the olfactory nerve: role of calcium and neuronal activity

Published online by Cambridge University Press:  21 September 2011

Mounir A. Koussa
Affiliation:
Department of Neuroscience, University of Arizona, Tucson, AZ, USA
Leslie P. Tolbert
Affiliation:
Department of Neuroscience, University of Arizona, Tucson, AZ, USA
Lynne A. Oland*
Affiliation:
Department of Neuroscience, University of Arizona, Tucson, AZ, USA
*
Correspondence should be addressed to: Lynne A. Oland, Department of Neuroscience, University of Arizona, PO Box 210077, Tucson, AZ 85721, USA email: [email protected]

Abstract

In adult olfactory nerves of mammals and moths, a network of glial cells ensheathes small bundles of olfactory receptor axons. In the developing antennal nerve (AN) of the moth Manduca sexta, the axons of olfactory receptor neurons (ORNs) migrate from the olfactory sensory epithelium toward the antennal lobe. Here we explore developmental interactions between ORN axons and AN glial cells. During early stages in AN glial-cell migration, glial cells are highly dye coupled, dividing glia are readily found in the nerve and AN glial cells label strongly for glutamine synthetase. By the end of this period, dye-coupling is rare, glial proliferation has ceased, glutamine synthetase labeling is absent, and glial processes have begun to extend to enwrap bundles of axons, a process that continues throughout the remainder of metamorphic development. Whole-cell and perforated-patch recordings in vivo from AN glia at different stages of network formation revealed two potassium currents and an R-like calcium current. Chronic in vivo exposure to the R-type channel blocker SNX-482 halted or greatly reduced AN glial migration. Chronically blocking spontaneous Na-dependent activity by injection of tetrodotoxin reduced the glial calcium current implicating an activity-dependent interaction between ORNs and glial cells in the development of glial calcium currents.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Aigouy, B., Van de Bor, V., Boeglin, M. and Giangrande, A. (2004) Time-lapse and cell ablation reveal the role of cell interactions in fly glial migration and proliferation. Development 131, 51275138.CrossRefGoogle ScholarPubMed
Aigouy, B., Lepelletier, L. and Giangrande, A. (2008) Glial chain migration requires pioneer cells. Journal of Neuroscience 28, 1163511641.CrossRefGoogle ScholarPubMed
Antonov, I., Chang, S., Zakharenko, S. and Popov, S.V. (1999) Distribution of neurotransmitter secretion in growing axons. Neuroscience 90, 975984.CrossRefGoogle ScholarPubMed
Au, W.W., Treloar, H.B. and Greer, C.A. (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. Journal of Comparative Neurology 446, 6880.CrossRefGoogle ScholarPubMed
Bailey, M.S., Puche, A.C. and Shipley, M.T. (1999) Development of the olfactory bulb: evidence for glia-neuron interactions in glomerular formation. Journal of Comparative Neurology 415, 423448.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Banerjee, S., Pillai, A.M., Paik, R., Li, J. and Bhat, M.A. (2006) Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. Journal of Neuroscience 26, 33193329.CrossRefGoogle ScholarPubMed
Barber, P.C. and Lindsay, R.M. (1982) Schwann cells of the olfactory nerve contain glial fibrillary acidic protein and resemble astrocytes. Neuroscience 7, 30773090.CrossRefGoogle ScholarPubMed
Baumann, P.M., Oland, L.A. and Tolbert, L.P. (1996) Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta. Journal of Comparative Neurology 373, 118128.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Benquet, P., Guen, J.L., Dayanithi, G., Pichon, Y. and Tiaho, F. (1999) Omega-AgaIVA-sensitive (P/Q-type) and -resistant (R-type) high-voltage-activated Ba(2+) currents in embryonic cockroach brain neurons. Journal of Neurophysiology 82, 22842293.CrossRefGoogle ScholarPubMed
Benquet, P., Pichon, Y. and Tiaho, F. (2004) In vitro development of P- and R-like calcium currents in insect (Periplaneta americana) embryonic brain neurons. Neuroscience Letters 365, 228232.CrossRefGoogle ScholarPubMed
Blinder, K.J., Pumplin, D.W., Paul, D.L. and Keller, A. (2003) Intercellular interactions in the mammalian olfactory nerve. Journal of Comparative Neurology 466, 230239.CrossRefGoogle ScholarPubMed
Bruzzone, R. and Dermietzel, R. (2006) Structure and function of gap junctions in the developing brain. Cell and Tissue Research 326, 239248.CrossRefGoogle ScholarPubMed
Burd, G.D. (1991) Development of the olfactory nerve in the African clawed frog, Xenopus laevis: I. Normal development. Journal of Comparative Neurology 304, 123134.CrossRefGoogle ScholarPubMed
Carter, L.A. and Roskams, A.J. (2002) Neurotrophins and their receptors in the primary olfactory neuroaxis. Microscopy Research and Technique 58, 189196.CrossRefGoogle Scholar
Caveney, S. (1985) The role of gap junctions in development. Annual Review of Physiology 47, 319335.CrossRefGoogle ScholarPubMed
Chiu, S.Y. and Kriegler, S. (1994) Neurotransmitter-mediated signaling between axons and glial cells. Glia 11, 191200.CrossRefGoogle ScholarPubMed
Chung, K. and Coggeshall, R.E. (1979) Primary afferent axons in the tract of lissauer in the cat. Journal of Comparative Neurology 186, 451464.CrossRefGoogle ScholarPubMed
Cook, J.E. and Becker, D.L. (2009) Gap-junction proteins in retinal development: new roles for the ‘Nexus’. Physiology 24, 219230.CrossRefGoogle ScholarPubMed
Copenhaver, P.F. (2007) How to innervate a simple gut: familiar themes and unique aspects in the formation of the insect enteric nervous system. Developmental Dynamics 236, 18411864.CrossRefGoogle ScholarPubMed
Copenhaver, P.F. and Taghert, P.H. (1989) Development of the enteric nervous system in the moth. II. Stereotyped cell migration precedes the differentiation of embryonic neurons. Developmental Biology 131, 85101.CrossRefGoogle ScholarPubMed
Diochot, S., Richard, S., Baldy-Mounlinier, M., Nargeot, J. and Valmier, J. (1995) Dihydropyridines, phenylalkylamines and benzothiazepines block N-, P/Q- and R-type calcium currents. Pflugers Archives 431, 1019.CrossRefGoogle Scholar
Doengi, M., Deitmer, J.W. and Lohr, C. (2008) New evidence for purinergic signaling in the olfactory bulb: A2A and P2Y1 receptors mediate intracellular calcium release in astrocytes. FASEB Journal 22, 23682378.CrossRefGoogle ScholarPubMed
Doucette, J.R. (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anatomical Record 210, 385391.CrossRefGoogle ScholarPubMed
Gao, X.B. and van den Pol, A.N. (2000) GABA release from mouse axonal growth cones. Journal of Physiology 523, 629637.CrossRefGoogle ScholarPubMed
Ge, W.P., Zhou, W., Luo, Q., Jan, L.Y. and Jan, Y.N. (2009) Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proceedings of the National Academy of Sciences of the U.S.A. 106, 328333.CrossRefGoogle ScholarPubMed
Giangrande, A. (1994) Glia in the fly wing are clonally related to epithelial cells and use the nerve as a pathway for migration. Development 120, 523534.CrossRefGoogle Scholar
Gibson, N.J. and Nighorn, A.J. (2000) Expression of nitric oxide synthase and soluble guanylyl cyclase in the developing olfactory system of Manduca sexta. Journal of Comparative Neurology 422, 191205.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Gibson, N.J. and Tolbert, L.P. (2006) Activation of epidermal growth factor receptor mediates receptor axon sorting and extension in the developing olfactory system of the moth Manduca sexta. Journal of Comparative Neurology 495, 554572.CrossRefGoogle ScholarPubMed
Gibson, N.J., Hildebrand, J.G. and Tolbert, L.P. (2004) Glycosylation patterns are sexually dimorphic throughout development of the olfactory system in Manduca sexta. Journal of Comparative Neurology 476, 118.CrossRefGoogle ScholarPubMed
Gilmour, D.T., Maischen, H.M. and Nüsslein-Volhard, C. (2002) Migration and function of a glial subtype in the vertebrae peripheral nervous system. Neuron 34, 577588.CrossRefGoogle Scholar
Goodenough, D. A. and Paul, D. L. (2009) Gap junctions. Cold Spring Harbor Perspectives in Biology 1, a002576.CrossRefGoogle ScholarPubMed
Grafe, P., Schaffer, V. and Rucker, F. (2006) Kinetics of ATP release following compression injury of a peripheral nerve trunk. Purinergic Signalling 2, 527536.CrossRefGoogle ScholarPubMed
Hartl, S., Heil, J.E., Hirsekorn, A. and Lohr, C. (2007) A novel neurotransmitter-independent communication pathway between axons and glial cells. European Journal of Neuroscience 25, 945956.CrossRefGoogle ScholarPubMed
Hayashi, J.H. and Levine, R.B. (1992) Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. Journal of Experimental Biology 171, 1542.CrossRefGoogle ScholarPubMed
Higgins, M.R., Gibson, N.J., Eckholdt, P.A., Nighorn, A., Copenhaver, P.F., Nardi, J. et al. (2002) Different isoforms of fasciclin II are expressed by a subset of developing olfactory receptor neurons and by olfactory-nerve glial cells during formation of glomeruli in the moth Manduca sexta. Developmental Biology 244, 134154.CrossRefGoogle ScholarPubMed
Jhaveri, D., Sen, A. and Rodrigues, V. (2000) Mechanisms underlying olfactory neuronal connectivity in Drosophila – the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. Developmental Biology 226, 7387.CrossRefGoogle ScholarPubMed
Kafitz, K.W. and Greer, C.A. (1999) Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro. Glia 25, 99110.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Kirschenbaum, S.R., Higgins, M.R., Tveten, M. and Tolbert, L.P. (1995) 20-Hydroxyecdysone stimulates proliferation of glial cells in the developing brain of the moth Manduca sexta. Journal of Neurobiology 28, 234247.CrossRefGoogle ScholarPubMed
Klämbt, C. (2009) Modes and regulation of glial migration in vertebrates and invertebrates. Nature Review 10, 769779.CrossRefGoogle ScholarPubMed
Kreutzberg, G.W. and Gross, G.W. (1977) General morphology and axonal ultrastructure of the olfactory nerve of the pike, Esox lucius. Cell Tissue Research 181, 443457.CrossRefGoogle ScholarPubMed
Kucenas, S., Takada, N., Park, H.C., Woodruff, E., Broadie, K. and Appel, B. (2008) CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nature Neuroscience 11, 143151.CrossRefGoogle ScholarPubMed
LeCaudey, V. and Gilmour, D. (2006) Organizing moving groups during morphogenesis. Current Opinion in Cell Biology 18, 102107.CrossRefGoogle ScholarPubMed
Leiserson, W.M., Harkins, E.W. and Keshishian, H. (2000) Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 28, 793806.CrossRefGoogle Scholar
Li, Y., Li, D. and Raisman, G. (2005) Interaction of olfactory ensheathing cells with astrocytes may be the key to repair of tract injuries in the spinal cord: the ‘pathway hypothesis’. Journal of Neurocytology 34, 343351.CrossRefGoogle ScholarPubMed
Lohr, C. and Deitmer, J.W. (2006) Calcium signaling in invertebrate glial cells. Glia 54, 642649.CrossRefGoogle ScholarPubMed
Lohr, C., Oland, L.A. and Tolbert, L.P. (2001) Olfactory receptor axons influence the development of glial potassium currents in the antennal lobe of the moth Manduca sexta. Glia 36, 309320.CrossRefGoogle ScholarPubMed
Lohr, C., Tucker, E., Oland, L.A. and Tolbert, L.P. (2002) Development of depolarization-induced calcium transients in insect glial cells is dependent on the presence of afferent axons. Journal of Neurobiology 52, 8598.CrossRefGoogle ScholarPubMed
Lohr, C., Heil, J.E. and Deitmer, J.W. (2005) Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo. Glia 50, 198211.CrossRefGoogle ScholarPubMed
Mackay-Sim, A. and Chuah, M.I. (2000) Neurotrophic factors in the primary olfactory pathway. Progress in Neurobiology 62, 527559.CrossRefGoogle Scholar
Morton, D.B. and Truman, J.W. (1985) Steroid regulation of the peptide-mediated increase in cyclic GMP in the nervous system of the hawkmoth, Manduca sexta. Journal of Comparative Physiology A 157, 423432.CrossRefGoogle ScholarPubMed
Murakami, S., Umetsu, D., Maeyama, Y., Sato, M., Yoshida, S. and Tabata, T. (2007) Focal adhesion kinase controls morphogenesis of the Drosophila optic stalk. Development 134, 15391548.CrossRefGoogle ScholarPubMed
Myoga, M.H. and Regehr, W.G. (2011) Calcium microdomains near R-type calcium channels control the induction of presynaptic long-term potentiation at parallel fiber to purkinje cell synapses. Journal of Neuroscience 31, 52355243.CrossRefGoogle ScholarPubMed
Naidoo, V., Dai, X. and Galligan, J.J. (2010) R-type Ca(2+) channels contribute to fast synaptic excitation and action potentials in subsets of myenteric neurons in the guinea pig intestine. Neurogastroenterology Motility 22, 353363.CrossRefGoogle ScholarPubMed
Nave, K.-A. and Trapp, B.D. (2008) Axon-glial signaling and the glial support of axon function. Annual Review of Neuroscience 31, 535561.CrossRefGoogle ScholarPubMed
Oland, L.A. and Tolbert, L.P. (1987) Glial patterns during early development of antennal lobes of Manduca sexta: a comparison between normal lobes and lobes deprived of antennal axons. Journal of Comparative Neurology 255, 196207.CrossRefGoogle ScholarPubMed
Oland, L.A. and Tolbert, L.P. (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2, 1024.CrossRefGoogle ScholarPubMed
Oland, L.A. and Tolbert, L.P. (2011) Roles of gilal cells in neural circuit formation: Insights from insert. Glia 59, 12731295.CrossRefGoogle Scholar
Oland, L.A., Orr, G. and Tolbert, L.P. (1990) Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain. Journal of Neuroscience 10, 20962112.CrossRefGoogle ScholarPubMed
Oland, L.A., Pott, W.M., Bukhman, G., Sun, X.J. and Tolbert, L.P. (1996) Activity blockade does not prevent the construction of olfactory glomeruli in the moth Manduca sexta. International Journal of Developmental Neuroscience 14, 983996.CrossRefGoogle Scholar
Oland, L.A., Pott, W.M., Higgins, M.R. and Tolbert, L.P. (1998) Targeted ingrowth and glial relationships of olfactory receptor axons in the primary olfactory pathway of an insect. Journal of Comparative Neurology 398, 119138.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Oland, L.A., Marrero, H.M. and Burger, I. (1999) Glial cells in the developing and adult olfactory lobe of the moth Manduca sexta. Cell Tissue Research 297, 527545.CrossRefGoogle ScholarPubMed
Oland, L.A., Pott, W.M., Howard, C.T., Inlow, M. and Buckingham, J. (2003) A diffusible signal attracts olfactory sensory axons toward their target in the developing brain of the moth. Journal of Neurobiology 56, 2440.CrossRefGoogle ScholarPubMed
Peters, A., Palay, S.L. and Webster, H. de F. (eds) (1991) The Fine Structure of the Nervous System. 3rd ed. New York: Oxford University Press.Google Scholar
Piechotta, K., Lu, J. and Delpire, E. (2002) Cation chloride cotransporters interact with the stress-related kinases Ste20-related proline-alanine-rich kinase (SPAK) and oxidative stress response 1 (OSR 1). Journal of Biological Chemistry 297, 5081250819.CrossRefGoogle Scholar
Rela, L., Bordey, A. and Greer, C.A. (2010) Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia 58, 665678.CrossRefGoogle ScholarPubMed
Rieger, A., Deitmer, J.W. and Lohr, C. (2007) Axon-glia communication evokes calcium signaling in olfactory ensheathing cells of the developing olfactory bulb. Glia 55, 352359.CrossRefGoogle ScholarPubMed
Rodrigues, F., Schmidt, I. and Klämbt, C. (2011) Comparing peripheral glial cell differentiation in Drosophila and vertebrates. Cellular & Molecular Life Sciences 68, 5569.CrossRefGoogle ScholarPubMed
Rössler, W., Oland, L.A., Higgins, M.R., Hildebrand, J.G. and Tolbert, L.P. (1999) Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. Journal of Neuroscience 19, 98659877.CrossRefGoogle ScholarPubMed
Sanes, J.R. and Hildebrand, J.G. (1975) Nerves in the antenna of pupal Manduca sexta (Lepidoptera: Sphingidae). Wilhelm Roux' Archives 178, 7178.CrossRefGoogle Scholar
Sanes, J.R. and Hildebrand, J.G. (1976) Origin and morphogenesis of sensory neurons in an insect antenna. Developmental Biology 51, 300319.CrossRefGoogle Scholar
Sanes, J.R., Hildebrand, J.G. and Prescott, D.J. (1976) Differentiation of insect sensory neurons in the absence of their normal synaptic targets. Developmental Biology 52, 121127.CrossRefGoogle ScholarPubMed
Schweitzer, E.S., Sanes, J.R. and Hildebrand, J.G. (1976) Ontogeny of electroantennogram responses in the moth, Manduca sexta. Journal of Insect Physiology 22, 955960.CrossRefGoogle ScholarPubMed
Sen, A., Shetty, C., Jhaveri, D. and Rodrigues, V. (2005) Distinct types of glial cells populate the Drosophila antenna. BMC Developmental Biology 5, 2536.CrossRefGoogle ScholarPubMed
Sepp, K.J., Schulte, J. and Auld, V.J. (2000) Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30, 122133.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Shih, C.-H., Hsu, H.-T., Wang, K.-H. and Ko, W.-C. (2010) Calcium channel subtypes for cholinergic and nonadrenergic noncholinergic neurotransmission in isolated guinea pig trachea. Naunyn-Schmiedeberg's Archives of Pharmacology 382, 419432.CrossRefGoogle ScholarPubMed
Silies, M. and Klämbt, C. (2010) APC/CFzr/Cdh1-dependent regulation of cell adhesion controls glial migration in the Drosophila PNS. Nature Neuroscience 13, 13571364.CrossRefGoogle Scholar
Silies, M., Edenfeld, G., Engelen, D., Stork, T. and Klämbt, C. (2007) Development of peripheral glial cells in Drosophila. Neuron Glia Biology 3, 3543.CrossRefGoogle ScholarPubMed
Stebbings, L.A., Todman, M.G., Phillips, R., Greer, C.E., Tam, J., Phelan, P. et al. (2002) Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mechanisms of Development 113, 197205.CrossRefGoogle ScholarPubMed
Stevens, B. and Fields, R.D. (2000) Response of Schwann cells to action potentials in development. Science 287, 22672271.CrossRefGoogle ScholarPubMed
Su, Z. and He, C. (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Progress in Neurobiology 92, 517532.CrossRefGoogle ScholarPubMed
Thyssen, A. Hrinet, D., Wolburg, H., Schmalzing, G., Deitmer, J. W and Lohr, C. (2010) Ectopic vesicular neurotransmitter release along sensory axons mediates neurovascular coupling via glial calcium signaling. Proceedings of the National Academy of science of the U.S.A. 107, 1525815263.CrossRefGoogle ScholarPubMed
Treloar, H.B., Purcell, A.L. and Greer, C.A. (1999) Glomerular formation in the developing rat olfactory bulb. Journal of Comparative Neurology 413, 289304.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Tucker, E.S. and Tolbert, L.P. (2003) Reciprocal interactions between olfactory receptor axons and olfactory nerve glia cultured from the developing moth Manduca sexta. Developmental Biology 260, 930.CrossRefGoogle ScholarPubMed
van den Pol, A.N., Finkbeiner, S.M. and Cornell-Bell, A.H. (1992) Calcium excitability and oscillations in suprachiasmatic nucleus neurons and glia in vitro. Journal of Neuroscience 12, 26482664.CrossRefGoogle ScholarPubMed
von Hilchen, C.M., Beckervordersandforth, R.M., Rickert, C., Technau, G.M. and Altenhein, B. (2008) Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mechanisms of Development 125, 337352.CrossRefGoogle ScholarPubMed
von Hilchen, C.M., Hein, I., Technau, G.M. and Altenhein, B. (2010) Netrins guide migration of distinct glial cells in the Drosophila embryo. Development 137, 12511262.CrossRefGoogle ScholarPubMed
Waxman, S.G. and Black, J.A. (1995) Axoglial interactions at the cellular and molecular levels in central nervous system myelinated fibers. In Kettenmann, H. and Ransom, B.R. (eds) Neuroglia. New York: Oxford University Press, pp. 587610.Google Scholar
Wright, J.W. and Copenhaver, P.F. (2000) Different isoforms of fascicin II play distinct roles in the guidance of neuronal migration during insect embryogenesis. Developmental Biology 225, 5978.CrossRefGoogle ScholarPubMed
Young, S.H. and Poo, M.M. (1983) Spontaneous release of transmitter from growth cones of embryonic neurones. Nature 305, 634637.CrossRefGoogle ScholarPubMed
Zakharenko, S., Chang, S., O'Donoghue, M. and Popov, S.V. (1999) Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis. Journal of Cell Biology 144, 507518. Erratum in: Journal of Cell Biology (1999) 144: following 801.CrossRefGoogle ScholarPubMed
Zufall, F., Stengl, M., Franke, C., Hildebrand, J.G. and Hatt, H. (1991) Ionic currents of cultured olfactory receptor neurons from antennae of male Manduca sexta. Journal of Neuroscience 4, 956965.CrossRefGoogle Scholar