A diffusible signal attracts olfactory sensory axons toward their target in the developing brain of the moth

Journal of Neurobiology

Volumn 56, Issue 1, 2003, Pages 24-40

  Oland, Lynne A ^a   Pott, Wendy M ^a   Howard, Charles T ^a   Inlow, Mark ^b   Buckingham, Jocelyn ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

Author keywords

Insect; Manduca sexta; Olfaction

Indexed keywords

ANIMAL TISSUE; ANTENNA; ARTICLE; ASSOCIATION; BRAIN DEVELOPMENT; BRAIN REGION; CELL CULTURE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; LEPIDOPTERA; MOTH; NERVE FIBER; NEUROEPITHELIUM; NONHUMAN; OLFACTORY BULB; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING;

ANIMALS; BRAIN; MANDUCA; MICROSCOPY, CONFOCAL; NERVE GROWTH FACTORS; NEURITES; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; ORGAN CULTURE TECHNIQUES;

EID: 0038279796     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10210     Document Type: Article

References (72)

1. Astic L, Pellier-Monnin V, Saucier D, Charrier C, Mehlen P. 2002. Expression of netrin-1 and netrin-1 receptor, DCC in the rat olfactory nerve pathway during development and axonal regeneration. Neuroscience 109:643-656.
2. Bickel P, Doksum K. 1977. Mathematical Statistics: Basic Ideas and Selected Topics. Oakland, CA: Holden-Day. p 387-388.
3. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG. 1995. Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371-381.
4. Chuah MI, Au C. 1991. Olfactory Schwann cells are derived from olfactory precursor cells in the olfactory epithelium. J Neurosci Res 29:172-180.
5. Conzelmann S, Malun D, Breer H, Strotmann J. 2001. Brain targeting and glomerulus formation of two olfactory neuron populations expressing related receptor types. Eur J Neurosci 14:1623-1632.
6. Crandall JE, Dibble C, Butler D, Pays L, Ahmad N, Kostek C, Püschel AW, Schwarting GA. 2000. Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb. J Neurobiol 45:195-206.
7. Croucher SJ, Tickle C. 1989. Characterization of epithelial domains in the nasal passages of chick embryos: spatial and temporal mapping of a range of extracellular matrix and cell surface molecules during development of the nasal placode. Development 106:493-509.
8. Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Srevetan DW. 1997. Netrin-1 and DCC mediate axon guidance locally at the optic disc: Loss of function leads to optic nerve hypoplasia. Neuron 19:575-589.
9. Doucette R. 1990. Glial influences on axonal growth in the primary olfactory system. Glia 3:433-449.
10. Dudewicz E, Misha S. 1988. Modern Mathematical Statistics. New York: John Wiley and Sons. p 215.
11. Ebendal T, Jacobson CO. 1977. Tissue explants affecting extension and orientation of axons in cultured chick embryo ganglia. Exp Cell Res 105:379-387.
12. Gad JM, Keeling SL, Wilks AF, Tan SS, Cooper HM. 1997. The expression patterns of guidance receptors, DCC and neogenin, are spatially and temporally distinct throughout mouse embryogenesis. Dev Biol 192:258-273.
13. Gan W-B, Bishop DL, Turney SG, Lichtman JW. 1999. Vital imaging and ultrastructural analysis of individual axon terminals labeled by iontophoretic application of lipophilic dye. J Neurosci Meth 93:13-20.
14. Gibson NJ, Hildebrand JG, Tolbert LP. 2002. Differences in lectin-binding constituents on olfactory receptor axons projecting to ordinary and sexually dimorphic glomeruli in male and female Manduca sexta. Assoc Chemoreception Sci Abstr #30.
15. Gong Q, Shipley MT. 1996. Expression of extracellular matrix molecules and cell surface molecules in the olfactory nerve pathway during early development. J Comp Neurol 366:1-14.
16. Higgins MR, Gibson NJ, Eckholdt PA, Nighorn A, Copenhaver PF, Nardi J, Tolbert LP. 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. Dev Biol 244:134-154.
17. 125I-labeled α-bungarotoxin in normal and deafferented antennal lobes of Manduca sexta. Proc Natl Acad Sci USA 76:499-503.
18. Holt CE, Harris WA. 1998. Target selection: invasion, mapping and cell choice. Curr Opin Cell Biol 8:98-105.
19. Kaneko M, Tucker ES, Nighorn A, Tolbert LP. 2001. A role for Eph/ephrin signaling in developing olfactory axons. Soc Neurosci Abstr #140.3.
20. Kennedy TE. 2000. Cellular mechanisms of netrin function: long-range and short-range actions. Biochem Cell Biol 78:569-575.
21. Kent KS. 1985. Metamorphosis of the antennal center and the influence of sensory innervation on the formation of glomeruli in the hawk moth Manduca sexta. [thesis] Cambridge, MA: Harvard University.
22. Key B. 1998. Molecular development of the olfactory nerve pathway. Ann NY Acad Sci 855:76-82.
23. Key B, Akeson RA. 1990. Olfactory neurons express a unique glycosylated form of the neural cell adhesion molecule NCAM. J Cell Biol 110:1729-1743.
24. Key B, Akeson RA. 1993. Distinct subsets of sensory olfactory neurons in mouse: possible role in the formation of the mosaic olfactory projection. J Comp Neurol 335:355-368.
25. Kirschenbaum S, Higgins MR, Tveten M, Tolbert LP. 1995. 20-hydroxyecdysone stimulates proliferation of glial cells in the developing brain of the moth Manduca sexta. J Neurobiol 28:234-247.
26. Knoll B, Zarbalis K, Wurst W, Drescher U. 2001. A role for the EphA family in the topographic targeting of vomeronasal axons. Development 128:895-906.
27. Kobayashi H, Koppel AM, Luo Y, Raper JA. 1997. A role for collapsin-1 in olfactory and cranial axon guidance. J Neurosci 17:8339-8352.
28. LaMantia A-S, Bhasin N, Rhodes K, Heemskerk J. 2000. Mesenchymal/epithelia induction mediates olfactory pathway formation. Neuron 28:411-425.
29. LaMantia A-S, Colbert MC, Linney E. 1993. Retinoic acid induction and regional differentiation prefigure olfactory pathway formation in the mammalian forebrain. Neuron 10:1035-1048.
30. Li H, Chen J, Fagaly T, Zhou L, Yuan W, Dupuis S, Jiang Z, Nash W, Gick C, Ornitz D, Wu J, Rao Y. 1999. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96:807-818.
31. Lipscomb BW, Treloar HB, Greer CA. 2002. Cell surface carbohydrates reveal heterogeneity in olfactory receptor axons in the mouse. Cell Tissue Res 308:7-17.
32. Mammem E. 1992. When Does Bootstrap Work? Asymptotic Results and Simulations. New York: Springer-Verlag. p 9-13.
33. Miragall F, Dermeitzel R. 1992. Immunocytochemical localization of cell adhesion molecules in the developing and mature olfactory system. Microsc Res Tech 23:157-172.
34. Miragall F, Kadmon M, Husmann M, Schnachner M. 1989. Expression of L1 and NCAM cell adhesion molecules during development of the mouse olfactory system. Dev Biol 135:272-286.
35. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
36. Oland LA, Müller T, Kettenmann H, Hayashi JH. 1996. Preparation of primary cultures and acute slices of the nervous system of the moth Manduca sexta. J Neurosci Meth 69:103-112.
37. Oland LA, Orr G, Tolbert LP. 1990. Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain. J Neurosci 10:2096-2112.
38. Oland LA, Pott WM. 2000. An attractive diffusible signal helps to guide olfactory axons to the antennal lobe of the moth Manduca sexta. Soc Neurosci Abstr #604.10.
39. Oland LA, Pott WM, Higgins MR, Tolbert LP. 1998. Targeted ingrowth and axon-glial cell relationships of olfactory axons in the primary olfactory pathway of an insect. J Comp Neurol 398:119-138.
40. Oland LA, Pott WM, Lai M. 1997. Glomerular development in slice and organotypic cultures from moth olfactory lobe. Chem Senses 22:764.
41. Oland LA, Pott WM, Tolbert LP. 2001. Behavior of olfactory receptor axons growing near and in explants of the axon sorting zone of the moth olfactory system. Assoc Chemoreception Sci Abstr #291.
42. Oland LA, Tolbert LP. 1987. Glial patterns during early development of antennal lobes of Manduca sexta: A comparison between normal lobes and lobes deprived of antennal axons. J Comp Neurol 255:196-207.
43. Oland LA, Tolbert LP. 1988. Effects of hydroxyurea parallel the effects of radiation in developing olfactory glomeruli in insects. J Comp Neurol 278:377-387.
44. Oland LA, Tolbert LP. 1989. Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10-24.
45. Pasterkamp RJ, DeWinter F, Holtmaat AJGD, Verhaagen J. 1998. Evidence for a role of the chemorepellant semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J Neurosci 18:9962-9976.
46. Puche AC, Key B. 1996. N-acetyl-lactosamine in the rat olfactory system: expression and potential role in neurite growth. J Comp Neurol 364:267-278.
47. Renzi MJ, Wexler TL, Raper JA. 2000. Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target. Neuron 28:437-447.
48. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
49. Rössler W, Randolph P, Tolbert LP, Hildebrand JG. 1999. Axons of olfactory receptor cells of transsexually grafted antennae induce development of sexually dimorphic glomeruli in Manduca sexta. J Neurobiol 38:521-541.
50. Rössler W, Tolbert LP, Hildebrand JG. 1998. Early formation of sexually dimorphic glomeruli in the developing olfactory lobe of the brain of the moth Manduca sexta. J Comp Neurol 396:415-428.
51. Sanes JR, Hildebrand JG. 1975. Nerves in the antennae of pupal Manduca sexta Johanssen (Lepidoptera: Sphingidae). Wilhelm Roux' Archiv 178:71-78.
52. Sanes JR, Hildebrand JG. 1976. Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300-319.
53. Schneiderman AM, Matsumoto SG, Hildebrand JG. 1982. Trans-sexually grafted antennae influence development of sexually dimorphic neurones in moth brain. Nature 298:844-846.
54. Schwarting G, Crandall JE. 1991. Subsets of olfactory vomeronasal sensory epithelial cells and axons revealed by monoclonal antibodies to carbohydrate antigens. Br Res 547:239-248.
55. Schwarting GA, Deutsch G, Gattey DM, Crandall JE. 1992a. Glycoconjugates are stage- and position-specific cell surface molecules in the developing olfactory system. 1: The CC1 immunoreactive glycolipid defines a rostrocaudal gradient in the rat vomeronasal system. J Neurobiol 23:120-129.
56. Schwarting GA, Deutsch G, Gattey DM, Crandall JE. 1992b. Glycoconjugates are stage- and position-specific cell surface molecules in the developing olfactory system. 2. Unique carbohydrate antigens are topographic markers for selective projection patterns of olfactory axons. J Neurobiol 23:130-142.
57. Schwarting GA, Kostek C, Ahmed N, Dibble C, Pays L, Püschel AW. 2000. Semaphorin 3A is required for guidance of olfactory axons in mice. J Neurosci 20:7691-7697.
58. Schwarting GA, Kostek C, Bless EP, Ahmad N, Tobet SA. 2001. Deleted in colorectal cancer (DCC) regulates the migration of luteinizing hormone-releasing hormone neurons to the basal forebrain. J Neurosci 21:911-919.
59. Shu T, Valentino KM, Seaman C, Cooper HM, Richards LJ. 2000. Expression of the netrin-1 receptor, deleted in colorectal cancer (DCC), is largely confined to projecting neurons in the developing forebrain. J Comp Neurol 416:201-212.
60. St John J, Pasquale E, Key B. 2002. EphA receptors and ephrin-A ligands exhibit highly regulated spatial and temporal expression patterns in the developing olfactory system. Dev Br Res 138:1-14.
61. St John JA, Key B. 2001. EphB2 and two of its ligands have dynamic protein expression patterns in the developing olfactory system. Dev Br Res 126:43-56.
62. StataCorp. 2001. Stata statistical software. Release 7.0. College Station, TX: Stata.
63. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274:1123-1133.
64. Tessier-Lavigne M, Placzek M, Lumsden AGS, Dodd J, Jessell TM. 1988. Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336:775-778.
65. Tolbert LP, Hildebrand JG. 1981. Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze fracture. Proc Roy Soc Lond B 213:279-301.
66. Treloar HB, Nurcombe V, Key B. 1996. Expression of extracellular matrix molecules in the embryonic rat olfactory pathway. J Neurobiol 31:41-55.
67. Vassalli A, Rothman A, Feinstein P, Zapotocky M, Mombaerts P. 2002. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35:681-696.
68. Wadsworth WG, Bhatt H, Hedgecock EM. 1996. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16:35-46.
69. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
70. Williams-Hogarth LC, Puche AC, Torrey C, Cai X, Song I, Kolodkin AL, Shipley MT, Ronnett GV. 2000. Expression of semaphorins in developing and regenerating olfactory epithelium. J Comp Neurol 423:565-578.
71. Winberg ML, Mitchell KJ, Goodman CS. 1998. Genetic analysis of mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 93:581-591.
72. Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842.