In Vitro Analyses of Interactions between Olfactory Receptor Growth Cones and Glial Cells That Mediate Axon Sorting and Glomerulus Formation

Journal of Comparative Neurology

Volumn 472, Issue 4, 2004, Pages 478-495

  Tucker, Eric S ^a,b   Oland, Lynne A ^b   Tolbert, Leslie P ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Development; Manduca sexta; Neuron glia interaction; Olfaction

Indexed keywords

ANIMAL CELL; ARTICLE; CELL INTERACTION; CELL SELECTION; COCULTURE; CYTOSKELETON; GLIA CELL; GROWTH CONE; INVERTEBRATE; LEPIDOPTERA; NERVE CELL; NERVE FIBER GROWTH; NEUROPIL; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; VERTEBRATE;

ANIMALS; AXONS; CELL COMMUNICATION; COCULTURE TECHNIQUES; COLORING AGENTS; CULTURE MEDIA; CYTOSKELETON; GROWTH CONES; IMMUNOHISTOCHEMISTRY; MANDUCA; MICROSCOPY, CONFOCAL; NEUROGLIA; OLFACTORY RECEPTOR NEURONS; PHALLOIDINE; SENSE ORGANS; SODIUM CHLORIDE;

EID: 1942420796     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20058     Document Type: Article

References (88)

1. Bartolomei JC, Greer CA. 2000. Olfactory ensheathing cells: bridging the gap in spinal cord injury. Neurosurgery 47:1057-1069.
2. Baumann PM, Oland LA, Tolbert LP. 1996. Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta. J Comp Neurol 373:118-128.
3. Bozza T, Feinstein P, Zheng C, Mombaerts P. 2002. Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22:3033-3043.
4. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-338.
5. Crandall JE, Dibble C, Butler D, Pays L, Ahmad N., Kostek C, Puschel 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.
6. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K. 1999. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 19:8894-8908.
7. Dickson BJ. 2001. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11:103-110.
8. Doucette R. 1989. Development of the nerve fiber layer in the olfactory bulb of mouse embryos. J Comp Neurol 285:514-527.
9. Doucette R. 1991. PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 312:451-466.
10. Drazba J, Liljelund P, Smith C, Payne R, Lemmon V. 1997. Growth cone interactions with purified cell and substrate adhesion molecules visualized by interference reflection microscopy. Brain Res Dev Brain Res 100:183-197.
11. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F. 1995. In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
12. Dubuque SH, Schachtner J, Nighorn AJ, Menon KP, Zinn K, Tolbert LP. 2001. Immunolocalization of synaptotagmin for the study of synapses in the developing antennal lobe of Manduca sexta. J Comp Neurol 441:277-287.
13. Fischer RA. 1925. Statistical methods for research workers. Edinburgh: Oliver and Boyd.
14. Gao Q, Yuan B, Chess A. 2000. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780-785.
15. Gilbert M, Smith J, Roskams AJ, Auld VJ. 2001. Neuroligin 3 is a vertebrate gliotactin expressed in the olfactory ensheathing glia, a growth-promoting class of macroglia. Glia 34:151-164.
16. 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.
17. Gonzalez ML, Silver J. 1994. Axon-glia interactions regulate ECM patterning in the postnatal rat olfactory bulb. J Neurosci 14:6121-6131.
18. Grunwald IC, Klein R. 2002. Axon guidance: receptor complexes and signaling mechanisms. Curr Opin Neurobiol 12:250-259.
19. 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.
20. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
21. Hildebrand JG, Rössler WR, Tolbert LP. 1997. Postembryonic development of the olfactory system in the moth Manduca sexta: primary-afferent control of glomerular development. Semin Cell Dev Biol 8:163-170.
22. Hu H, Marton TF, Goodman CS. 2001. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32:39-51.
23. Isbister CM, O'Connor TP. 1999. Filopodial adhesion does not predict growth cone steering events in vivo. J Neurosci 19:2589-2600.
24. Kafitz KW, Greer CA. 1999. Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro. Glia 25:99-110.
25. Kent K. 1985. Metamorphosis of the antennal center and the influence of sensory innervation on the formation of glomeruli in the hawkmoth Manduca sexta. PhD dissertation, Harvard University.
26. Kent KS, Harrow ID, Quartararo P, Hildebrand JG. 1986. An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res 245:237-245.
27. Kent KS, Oland LA, Hildebrand JG. 1999. Development of the labial pit organ glomerulus in the antennal lobe of the moth Manduca sexta: the role of afferent projections in the formation of identifiable olfactory glomeruli. J Neurobiol 40:28-44.
28. Key B, St. John J. 2002. Axon navigation in the mammalian primary olfactory pathway: where to next? Chem Senses 27:245-260.
29. Lankford KL, Klein WL. 1990. Ultrastructure of individual neurons isolated from avian retina: occurrence of microtubule loops in dendrites. Brain Res Dev Brain Res 51:217-224.
30. Lemmon V, Burden SM, Payne HR, Elmslie GJ, Hlavin ML. 1992. Neurite growth on different substrates: permissive vs. instructive influences and the role of adhesive strength. J Neurosci 12:818-826.
31. Letourneau PC. 1975. Possible roles for cell-to-substratum adhesion in neuronal morphogenesis. Dev Biol 44:77-91.
32. Lin CH, Forscher P. 1993. Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121:1369-1383.
33. Lohr C, Tucker E, Oland LA, Tolbert LP. 2002. Development of depolarization-induced calcium transients in insect glial cells is dependent on the presence of afferent axons. J Neurobiol 52:85-98.
34. Luo Y, Raible D, Raper JA. 1993. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
35. Marin-Padilla M, Amieva MR. 1989. Early neurogenesis of the mouse olfactory nerve: Golgi and electron microscopic studies. J Comp Neurol 288:339-352.
36. Mason C, Erskine L. 2000. Growth cone form, behavior, and interactions in vivo: retinal axon pathfinding as a model. J Neurobiol 44:260-270.
37. Matheson SF, Levine RB. 1999. Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function. J Neurobiol 38:27-45.
38. 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.
39. Mori K, Nagao H, Yoshihara Y. 1999. The olfactory bulb: coding and processing of odor molecule information. Science 286:711-715.
40. Nikolic M. 2002. The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int J Biochem Cell Biol 34:731-745.
41. 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.
42. 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.
43. Oland LA, Tolbert LP. 1989. Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10-24.
44. Oland LA, Tolbert LP. 1996. Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J Neurobiol 30:92-109.
45. Oland LA, Tolbert LP, Mossman KL. 1988. Radiation-induced reduction of the glial population during development disrupts the formation of olfactory glomeruli in an insect. J Neurosci 8:353-367.
46. 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.
47. Oland LA, Muller T, Kettenmann H, Hayashi J. 1996. Preparation of primary cultures and acute slices of the nervous system of the moth Manduca sexta. J Neurosci Methods 69:103-112.
48. Oland LA, Pott WM, Higgins MR, Tolbert LP. 1998. Targeted ingrowth and glial relationships of olfactory receptor axons in the primary olfactory pathway of an insect. J Comp Neurol 398:119-138.
49. Payne HR, Burden SM, Lemmon V. 1992. Modulation of growth cone morphology by substrate-bound adhesion molecules. Cell Motil Cytoskeleton 21:65-73.
50. Puche AC, Shipley MT. 2001. Radial glia development in the mouse olfactory bulb. J Comp Neurol 434:1-12.
51. Puche AC, Poirier F, Hair M, Bartlett PF, Key B. 1996. Role of galectin-1 in the developing mouse olfactory system. Dev Biol 179:274-287.
52. Raisman G. 1985. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
53. Ramon-Cueto A, Avila J. 1998. Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175-187.
54. Ramon-Cueto A, Valverde F. 1995. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 14:163-173.
55. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
56. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1255.
57. Roos J, Hummel T, Ng N, Klambt C, Davis GW. 2000. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26:371-382.
58. Rössler WR, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP. 1999. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 19:9865-9877.
59. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D. 1991. Microtubule behavior during guidance of pioneer neuron growth cones in situ. J Cell Biol 115:381-395.
60. Sanes JR, Hildebrand JG. 1976. Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300-319.
61. Sanes JR, Prescott DJ, Hildebrand JG. 1977. Cholinergic neurochemical development of normal and deafferented antennal lobes during metamorphosis of the moth, Manduca sexta. Brain Res 119:389-402.
62. Schwarting GA, Kostek C, Ahmad N, Dibble C, Pays L, Puschel AW. 2000. Semaphorin 3A is required for guidance of olfactory axons in mice. J Neurosci 20:7691-7697.
63. Shamah SM, Lin MZ, Goldberg JL, Estrach S, Sahin M, Hu L, Bazalakova M, Neve RL, Corfas G, Debant A, Greenberg ME. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-244.
64. St. John JA, Key B. 1999. Expression of galectin-1 in the olfactory nerve pathway of rat. Brain Res Dev Brain Res 117:171-178.
65. St. John JA, Key B. 2001. EphB2 and two of its ligands have dynamic protein expression patterns in the developing olfactory system. Brain Res Dev Brain Res 126:43-56.
66. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115:345-363.
67. Tanaka EM, Kirschner MW. 1995. The role of microtubules in growth cone turning at substrate boundaries. J Cell Biol 128:127-137.
68. Tisay KT, Key B. 1999. The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells. J Neurosci 19:9890-9899.
69. Tisay KT, Bartlett PF, Key B. 2000. Primary olfactory axons form ectopic glomeruli in mice lacking p75NTR. J Comp Neurol 428:656-670.
70. Tolbert LP. 1998. Olfactory development in invertebrates: on the scent of central development issues. Ann N Y Acad Sci 855:95-103.
71. Tolbert LP, Matsumoto SG, Hildebrand JG. 1983. Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158-1175.
72. Treloar HB, Nurcombe V, Key B. 1996. Expression of extracellular matrix molecules in the embryonic rat olfactory pathway. J Neurobiol 31:41-55.
73. Treloar H, Tomasiewicz H, Magnuson T, Key B. 1997. The central pathway of primary olfactory axons is abnormal in mice lacking the N-CAM-180 isoform. J Neurobiol 32:643-658.
74. Treloar HB, Purcell AL, Greer CA. 1999. Glomerular formation in the developing rat olfactory bulb. J Comp Neurol 413:289-304.
75. Tsui HT, Lankford KL, Ris H, Klein WL. 1984. Novel organization of microtubules in cultured central nervous system neurons: formation of hairpin loops at ends of maturing neurites. J Neurosci 4:3002-3013.
76. Tucker ES, Tolbert LP. 2003. Reciprocal interactions between olfactory receptor axons and olfactory nerve glia cultured from the developing moth Manduca sexta. Dev Biol 260:9-30.
77. Tucker ES, Oland LA, Tolbert LP. 2000. In vitro study of interactions between olfactory receptor growth cones and glial cells of the axonal sorting zone. Soc Neurosci Abstr 26:1611.
78. Tucker ES, Oland LA, Tolbert LP. 2001. In vitro analysis of interactions between olfactory receptor growth cones and centrally derived glia. Assoc Chemorecept Sci Abstr 23:72.
79. Valverde F. 1999. Building an olfactory glomerulus. J Comp Neurol 415:419-422.
80. Valverde F, Santacana M, Heredia M. 1992. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49:255-275.
81. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
82. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall JB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
83. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
84. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
85. Walz A, Rodriguez I, Mombaerts P. 2002. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J Neurosci 22:4025-4035.
86. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
87. Xu XM, Fisher DA, Zhou L, White FA, Ng S, Snider WD, Luo Y. 2000. The transmembrane protein semaphorin 6A repels embryonic sympathetic axons. J Neurosci 20:2638-2648.
88. 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.