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

Neuron Glia Biology

Volumn 6, Issue 4, 2010, Pages 245-261

  Koussa, Mounir A ^a   Tolbert, Leslie P ^a   Oland, Lynne A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

antennal nerve; Calcium currents; Manduca sexta

Indexed keywords

CALCIUM; DYE; GLUTAMATE AMMONIA LIGASE; SNX 482; SODIUM; TETRODOTOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA (ORGAN); ARTICLE; CALCIUM CURRENT; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GLIA; IN VIVO STUDY; MANDUCA SEXTA; MOTH; NERVE CELL NETWORK; NONHUMAN; OLFACTORY NERVE; OLFACTORY RECEPTOR; PRIORITY JOURNAL;

ANIMALS; BIOPHYSICS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELL COMMUNICATION; CELLS, CULTURED; ELECTRIC STIMULATION; GAP JUNCTIONS; GLUTAMATE-AMMONIA LIGASE; HISTONES; MANDUCA; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON; NERVE NET; NEUROGLIA; OLFACTORY NERVE; OLFACTORY RECEPTOR NEURONS; ORGANIC CHEMICALS; PATCH-CLAMP TECHNIQUES; SODIUM CHANNEL BLOCKERS; SPIDER VENOMS; TETRODOTOXIN;

LEPIDOPTERA; MAMMALIA; MANDUCA SEXTA;

EID: 84857002154     PISSN: 1740925X     EISSN: 17410533     Source Type: Journal    
DOI: 10.1017/S1740925X11000081     Document Type: Article

References (92)

1. 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, 5127-5138. (Pubitemid 39485368)
2. Aigouy B., Lepelletier L. and Giangrande A. (2008) Glial chain migration requires pioneer cells. Journal of Neuroscience 28, 11635-11641.
3. Antonov I., Chang S., Zakharenko S. and Popov S.V. (1999) Distribution of neurotransmitter secretion in growing axons. Neuroscience 90, 975-984. (Pubitemid 29156762)
4. 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, 68-80. (Pubitemid 34252851)
5. 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, 423-448.
6. 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, 3319-3329.
7. Barber P.C. and Lindsay R.M. (1982) Schwann cells of the olfactory nerve contain glial fibrillary acidic protein and resemble astrocytes. Neuroscience 7, 3077-3090. (Pubitemid 13175740)
8. 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, 118-128. (Pubitemid 26292123)
9. 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, 2284-2293.
10. Benquet P., Pichon Y. and Tiaho F. (2004) In vitro development of Pand R-like calcium currents in insect (Periplaneta americana) embryonic brain neurons. Neuroscience Letters 365, 228-232. (Pubitemid 38891788)
11. 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, 230-239. (Pubitemid 37255231)
12. Bruzzone R. and Dermietzel R. (2006) Structure and function of gap junctions in the developing brain. Cell and Tissue Research 326, 239-248. (Pubitemid 44435805)
13. Burd G.D. (1991) Development of the olfactory nerve in the African clawed frog, Xenopus laevis: I. Normal development. Journal of Comparative Neurology 304, 123-134.
14. Carter L.A. and Roskams A.J. (2002) Neurotrophins and their receptors in the primary olfactory neuroaxis. Microscopy Research and Technique 58, 189-196. (Pubitemid 34832824)
15. Caveney S. (1985) The role of gap junctions in development. Annual Review of Physiology 47, 319-335. (Pubitemid 15142385)
16. Chiu S.Y. and Kriegler S. (1994) Neurotransmitter-mediated signaling between axons and glial cells. Glia 11, 191-200. (Pubitemid 2116316)
17. Chung K. and Coggeshall R.E. (1979) Primary afferent axons in the tract of lissauer in the cat. Journal of Comparative Neurology 186, 451-464. (Pubitemid 9222530)
18. Cook J.E. and Becker D.L. (2009) Gap-junction proteins in retinal development: new roles for the 'Nexus'. Physiology 24, 219-230.
19. 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, 1841-1864. (Pubitemid 47078894)
20. 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, 85-101. (Pubitemid 19032127)
21. 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, 10-19.
22. 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, 2368-2378. (Pubitemid 351948655)
23. Doucette J.R. (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anatomical Record 210, 385-391. (Pubitemid 15209791)
24. Gao X.B. and van den Pol A.N. (2000) GABA release from mouse axonal growth cones. Journal of Physiology 523, 629-637. (Pubitemid 30153823)
25. 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, 328-333.
26. 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, 523-534. (Pubitemid 24071195)
27. 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, 191-205. (Pubitemid 30390164)
28. 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, 554-572.
29. 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, 1-18. (Pubitemid 38880229)
30. 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, 577-588. (Pubitemid 34628754)
31. Goodenough D. A. and Paul D. L. (2009) Gap junctions. Cold Spring Harbor Perspectives in Biology 1, a002576.
32. Grafe P., Schaffer V. and Rucker F. (2006) Kinetics of ATP release following compression injury of a peripheral nerve trunk. Purinergic Signalling 2, 527-536. (Pubitemid 44363749)
33. 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, 945-956.
34. 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, 15-42.
35. 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, 134-154. (Pubitemid 34271146)
36. 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, 73-87.
37. Kafitz K.W. and Greer C.A. (1999) Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro. Glia 25, 99-110. (Pubitemid 29032766)
38. 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, 234-247.
39. Klämbt C. (2009) Modes and regulation of glial migration in vertebrates and invertebrates. Nature Review 10, 769-779.
40. 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, 443-457. (Pubitemid 8146822)
41. 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, 143-151. (Pubitemid 351170490)
42. LeCaudey V. and Gilmour D. (2006) Organizing moving groups during morphogenesis. Current Opinion in Cell Biology 18, 102-107. (Pubitemid 43107615)
43. 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, 793-806. (Pubitemid 32038072)
44. 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, 343-351. (Pubitemid 44078242)
45. Lohr C. and Deitmer J.W. (2006) Calcium signaling in invertebrate glial cells. Glia 54, 642-649. (Pubitemid 44629627)
46. 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, 309-320. (Pubitemid 34010059)
47. 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, 85-98. (Pubitemid 34803901)
48. 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, 198-211. (Pubitemid 40769850)
49. Mackay-Sim A. and Chuah M.I. (2000) Neurotrophic factors in the primary olfactory pathway. Progress in Neurobiology 62, 527-559. (Pubitemid 30408160)
50. Morton D.B. and Truman J.W. (1985) Steroid regulation of the peptidemediated increase in cyclic GMP in the nervous system of the hawkmoth, Manduca sexta. Journal of Comparative Physiology A 157, 423-432.
51. 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, 1539-1548. (Pubitemid 46746306)
52. Myoga M.H. and Regehr W.G. (2011) Calcium microdomains near R-type calcium channels control the induction of presynaptic longterm potentiation at parallel fiber to purkinje cell synapses. Journal of Neuroscience 31, 5235-5243.
53. 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, 353-363.
54. Nave K.-A. and Trapp B.D. (2008) Axon-glial signaling and the glial support of axon function. Annual Review of Neuroscience 31, 535-561.
55. 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, 196-207. (Pubitemid 17000058)
56. Oland L.A. and Tolbert L.P. (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2, 10-24.
57. Oland L.A. and Tolbert L.P. (2011) Roles of gilal cells in neural circuit formation: Insights from insert. Glia 59, 1273-1295.
58. 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, 2096-2112.
59. 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, 983-996. (Pubitemid 27032535)
60. 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, 119-138. (Pubitemid 28373880)
61. 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, 527-545. (Pubitemid 29410541)
62. 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, 24-40. (Pubitemid 36682627)
63. 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.
64. 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, 50812-50819. (Pubitemid 36042246)
65. Rela L., Bordey A. and Greer C.A. (2010) Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia 58, 665-678.
66. 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, 352-359.
67. Rodrigues F., Schmidt I. and Klämbt C. (2011) Comparing peripheral glial cell differentiation in Drosophila and vertebrates. Cellular & Molecular Life Sciences 68, 55-69.
68. 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, 9865-9877. (Pubitemid 30226660)
69. Sanes J.R. and Hildebrand J.G. (1975) Nerves in the antenna of pupal Manduca sexta (Lepidoptera: Sphingidae). Wilhelm Roux' Archives 178, 71-78.
70. Sanes J.R. and Hildebrand J.G. (1976) Origin and morphogenesis of sensory neurons in an insect antenna. Developmental Biology 51, 300-319.
71. 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, 121-127.
72. 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, 955-960.
73. Sen A., Shetty C., Jhaveri D. and Rodrigues V. (2005) Distinct types of glial cells populate the Drosophila antenna. BMC Developmental Biology 5, 25-36.
74. Sepp K.J., Schulte J. and Auld V.J. (2000) Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 30, 122-133. (Pubitemid 30199426)
75. 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, 419-432.
76. Silies M. and Klämbt C. (2010) APC/CFzr/Cdh1-dependent regulation of cell adhesion controls glial migration in the Drosophila PNS. Nature Neuroscience 13, 1357-1364.
77. Silies M., Edenfeld G., Engelen D., Stork T. and Klämbt C. (2007) Development of peripheral glial cells in Drosophila. Neuron Glia Biology 3, 35-43. (Pubitemid 47345541)
78. 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, 197-205. (Pubitemid 34311751)
79. Stevens B. and Fields R.D. (2000) Response of Schwann cells to action potentials in development. Science 287, 2267-2271. (Pubitemid 30177032)
80. Su Z. and He C. (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Progress in Neurobiology 92, 517-532.
81. 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, 15258-15263.
82. Treloar H.B., Purcell A.L. and Greer C.A. (1999) Glomerular formation in the developing rat olfactory bulb. Journal of Comparative Neurology 413, 289-304. (Pubitemid 29462728)
83. 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, 9-30. (Pubitemid 36900332)
84. 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, 2648-2664.
85. 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, 337-352.
86. 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, 1251-1262.
87. 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. 587-610.
88. 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, 59-78.
89. Young S.H. and Poo M.M. (1983) Spontaneous release of transmitter from growth cones of embryonic neurones. Nature 305, 634-637. (Pubitemid 13013454)
90. 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, 507-518. (Pubitemid 29234530)
91. Erratum in: Journal of Cell Biology (1999) 144: following 801.
92. 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, 956-965.