Development of the olfactory bulb: Evidence for glia-neuron interactions in glomerular formation

Journal of Comparative Neurology

Volumn 415, Issue 4, 1999, Pages 423-448

  Bailey, Mary S ^a   Puche, Adam C ^a   Shipley, Michael T ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Differentiation; Gradient; Radial glia

Indexed keywords

CYTOPLASM PROTEIN; NEUROMODULIN;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; DENDRITE; EMBRYO; GLIA; JUXTAGLOMERULAR CELL; MITRAL CELL; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY RECEPTOR; PRIORITY JOURNAL; RAT; SCHWANN CELL;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; EMBRYO; GAP-43 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; OLFACTORY BULB; OLFACTORY MARKER PROTEIN; OLFACTORY RECEPTOR NEURONS; RATS; VIMENTIN;

EID: 0033611288     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19991227)415:4<423::AID-CNE2>3.0.CO;2-G     Document Type: Article

References (98)

1. Abd-el-Basset EM, Ahmed I, Kalnins VI, Fedoroff S. 1992. Immunoelectron microscopic localization of vimentin and glial fibrillary acidic protein in mouse astrocytes and their precursor cells in culture. Glia 6:149-153.
2. Astic L, Pellier-Monnin V, Godinot F. 1998. Spatio-temporal patters of ensheathing cell differentiation in the rat olfactory system during development. Neuroscience 84:295-307.
3. Autillo-Touati A, Chamak B, Araud D, Vuillet J, Seite R, Prochiantz A. 1988. Region-specific neuro-astroglial interactions: ultrastructural study of the in vitro expression of neuronal polarity. J Neurosci Res 19:326-342.
4. Bailey MS, Shipley MT. 1993. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526.
5. Baird DH, Hatten ME, Mason CA. 1992. Cerebellar target neurons provide a stop signal for afferent neurite extension in vitro. J Neurosci 12:619-634.
6. Baker H, Grillo M, Margolis FL. 1989. Biochemical and immunocytochemical characterization of olfactory marker protein in the rodent central nervous system. J Comp Neurol 285:246-261.
7. Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M. 1992. Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736-749.
8. Bayer SA. 1983. 3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329-340.
9. Belluscio L, Gold GH, Nemes A, Axel R. 1998. Mice deficient in G(olf) are anosmic. Neuron 20:69-81.
10. Brunet LJ, Gold GH, Ngai J. 1996. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693.
11. Bulfone A, Wang F, Hevner R, Anderson S, Cutforth T, Chen S, Meneses J, Pedersen R, Axel R, Rubenstein JL. 1998 . An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21:1273-1282.
12. Cooper NGF, Steindler DA. 1986. Lectins demarcate the barrel subfield in the somatosensory cortex of the early postnatal mouse. J Comp Neurol 249:157-169.
13. Crossin KL, Prieto AL, Hoffman S, Jones FS, Friedlander DR. 1990. Expression of adhesion molecules and the establishment of boundaries during embryonic and neural development. Exp Neurol 109:6-18.
14. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL. 1990. Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10:684-692.
15. De Carlos JA, Lopez-Mascaraque L, Valverde F. 1995. The telencephalic vesicles are innervated by olfactory placode-derived cells: a possible mechanism to induce neocortical development. Neuroscience 68:1167-1178.
16. Denis-Donini S, Glowinski J, Prochiantz A. 1984. Glial heterogeneity may define the three-dimensional shape of mouse mesencephalic dopaminergic neurons. Nature 307:641-643.
17. Doucette R. 1989. Development of the nerve fiber layer in the olfactory bulb of mouse embryos. J Comp Neurol 285:514-527.
18. Doucette R. 1991. PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 312:451-466.
19. Ekenhoff MF, Rakic P. 1984. Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 223:1-21.
20. Farbman AI, Margolis FL. 1980. Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol 74:205-215.
21. Farbman A, Scholz D, Emanuel D, Margolis F. 1980. Maturation of olfactory receptor cell terminals. In: van der Starre H, editor. Olfaction and taste. London: IRL Press, p 147-150.
22. Fok-Seang J, Smith-Thomas LC, Meiners S, Muir E, Du JS, Housden E, Johnson AR, Faissner A, Geller HM, Keynes RJ, Rogers JH, Fawcett JW. 1995. Analysis of astrocyte cell lines with different abilities to promote axon growth. Brain Res 689:207-223.
23. Frotscher M. 1997. Dual role for Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 290:315-322.
24. Fueshko SM, Key S, Wray S. 1998. GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J Neurosci 18:2560-2569.
25. Gasser UE, Hatten ME. 1990. Neuron-glial interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation. J Neurosci 10:1276-1285.
26. Gilbert SF. 1997. Developmental biology. 5th ed. Massachusetts: Sinauer Associates, p 113-114.
27. Gong Q, Shipley MT. 1995. Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14:91-101.
28. Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT. 1994. Localization and regeneration of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. J Comp Neurol 344:336-348.
29. Gonsalez MDL, Malemud CJ, Silver J. 1993. Role of astroglial extracellular matrix in the formation of rat olfactory bulb glomeruli. Exp Neurol 123:91-105.
30. Graziadei PPC, Kaplan MS. 1980. Re-growth of olfactory sensory axons into transplanted neural tissue. I. Development of connections with the occipital cortex. Brain Res 201:39-44.
31. Graziadei PPC, Monti-Graziadei GA. 1986. Principles of organization of the vertebrate olfactory glomerulus: a hypothesis. Neuroscience 19:1025-1035.
32. Gressens P, Richelme C, Kadhim HJ, Gadisseux J-F, Evrard P. 1992. The germinative zone produces the most cortical astrocytes after neuronal migration in the developing mammalian brain. Biol Neonate 61:4-24.
33. Guthrie KM, Gall CM. 1988. Differential expression of mRNAs for the NGF family of neurotrophic factors in the adult rat central olfactory system. J Comp Neurol 313:95-102.
34. Hatten ME. 1990. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. TINS 13:179-184.
35. Hatten ME, Lynch M, Rydel RE, Sanchez J, Joseph-Silverstein J, Moscatelli D. Rifkin DB. 1988. In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol 125:280-289.
36. Heredia M, Gascuel J, Ramon-Cueta A, Santacana M, Avila J, Masson C, Valverde F. 1998. Two novel monoclonal antibodies (1.9.E and 4.11.C) against olfactory bulb ensheathing glia. Glia 24:352-364.
37. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V. 1991. Mouse small eye results from mutations in a paired like homeobox continuing gene. Nature 354:522-525
38. Hinds JW. 1968a. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
39. Hinds JW. 1968b Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration. J Comp Neurol 134:305-322.
40. Hinds JW. 1972. Early neuron differentiation in the mouse olfactory bulb. I. Light microscopy. J Comp Neurol 146:233-252.
41. Hinds JW, Ruffett TL. 1973. Mitral cell development in the mouse olfactory bulb: reorientation of the perikaryon and maturation of the axon initial segment. J Comp Neurol 151:281-306.
42. Levitt P, Rakic P. 1980. Immunoperoxidase localization of glial fibrillary acid protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815-840.
43. Liesi P, Dahl D, Vaheri A. 1983. Laminin is produced by early rat astrocytes in primary culture. J Cell Biol 96:920-924.
44. Lochter A, Vaughn L, Kaplony A, Prochiantz A, Schachner M, Faissner A. 1991. J1/Tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J Cell Biol 113:1159-1171.
45. Lopez-Mascaraque L, Garcia C, Valverde F, DeCarlos JA. 1998. Central olfactory structures in Pax-6 mutant mice. Ann NY Acad Sci 855:83-94.
46. Malun D, Brunjes PC. 1996. Development of olfactory glomeruli: temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. J Comp Neurol 368:1-16.
47. Malun D, Oland LA, Tolbert LP. 1994. Uniglomerular projection neurons participate in early development of olfactory glomeruli in the moth Manduca sexta. J Comp Neurol 350:1-22.
48. Margolis FL. 1972. A brain protein unique to the olfactory bulb. Proc Natl Acad Sci USA 69:1221-1224.
49. Marin-Padilla M, Amieva MR. 1989. Early neurogenesis of the mouse olfactory nerve: Golgi and electron microscopic studies. J Comp Neurol 288:339-352.
50. Matus A. 1988. Microtubule-associated proteins: their potential role in determining neuronal morphology. Annu Rev Neurosci 11:29-44.
51. Meiri KF, Johnson MI, Willard M. 1988. Distribution and phosphorylation of the growth-associated protein GAP-43 in regenerating sympathetic neurons in culture. J Neurosci 8:2571-2581.
52. Meisami E, Safari L. 1981. A quantitative study of the effects of early unilateral olfactory deprivation on the number and distribution of mitral and tufted cells and of glomeruli in the rat olfactory bulb. Brain Res 221:81-107.
53. Meyer G, Soria JM, Martinez-Galan JR, Martin-Clemente B, Fairen A. 1998. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397:493-518.
54. 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.
55. Niswander L, Jeffery S, Martin GR, Tickle C. 1994. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371:609-612.
56. Norgren RB Jr, Brackenbury R. 1993. Cell adhesion molecules and the migration of LHRH neurons during development. Dev Biol 160:377-387.
57. Norgren RB Jr, Ratner N, Brackenbury R. 1992. Development of olfactory nerve glia defined by a monoclonal antibody specific for Schwann cells. Dev Dyn 194:231-238.
58. Norris CR, Kalil K. 1991. Guidance of callosal axons by radial glia in the developing cerebral cortex. J Neurosci 11:3481-3492.
59. O'Brien TF, Faissner A, Schachner M, Steindler DA. 1992. Afferent-boundary interactions in the developing neostriatal mosaic. Dev Brain Res 65:259-267.
60. 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.
61. 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.
62. 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.
63. Pellier V, Astic L. 1994. Histochemical and immunocytochemical study of the migration of neurons from the rat olfactory placode. Cell Tissue Res 275:587-598.
64. Pixley SK, de Vellis J. 1984. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Dev Brain Res 15:201-209.
65. Pomeroy SL, LaMantia A-S, Purves D. 1990. Postnatal construction of neural circuitry in the mouse olfactory bulb. J Neurosci 10:1952-1966.
66. Prochiantz A, Rousselet A, Chamak B. 1990. Adhesion and the in vitro development of axons and dendrites. In: Coleman P, Higgins G, Phelps C, editors. Progress in brain research. New York: Elsevier. p 331-336.
67. Raisman G. 1985. Specialized neuroglial arrangements may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
68. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-84.
69. Ramon-Cueto A, Avila J. 1998. Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175-177.
70. 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.
71. Rizvi TA, Murphy A, Ennis M, Behbehani M, Shipley MT. 1996. Medial preoptic afferents to periaqueductal gray medullo-output neurons: a combined fos and tract-tracing study. J Neurosci 16:333-344.
72. Rudge JS, Silver J. 1990. Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci 10:3594-3603.
73. Santacana M, Heredia M, Valverde F. 1992. Transient pattern of exuberant projections of olfactory axons during development in the rat. Brain Res Dev Brain Res 70:213-222.
74. Schmechel DE, Rakic P. 1979. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115-152.
75. Schwanzel-Fukuda M, Pfaff DW. 1989. Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161-164.
76. Sheppard AM, Hamilton SK, Pearlman AL. 1991. Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J Neurosci 11:3928-3942.
77. Shipley MT, Luna J, McLean JH. 1989. Processing and analysis of neuroanatomical images. In: Heimer L, Zaborsky L, editors. Neuroanatomical tract tracing methods 2. New York: Plenum, p 331-388.
78. Silver J, Ogawa MY. 1983. Postnatally induced formation of the corpus callosum in acallosal mice on glia-coated cellulose bridges. Science 1983:1067-1069.
79. Silver J, Lorenz SE, Wahlsten D, Coughlin J. 1982. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol 210:10-29.
80. Silver J, Poston M, Rutishauser U. 1987. Axon pathway boundaries in the developing brain. I. Cellular and molecular determinants that separate the optic and olfactory projections. J Neurosci 7:2264-2272.
81. Silver J, Edward MA, Levitt P. 1993. Immunocytochemical demonstration of early appearing astroglial structures that form boundaries and pathways along axon tracts in the fetal brain. J Comp Neurol 328:415-436.
82. Skene JHP. 1989. Axonal growth-associated proteins. Annu Rev Neurosci 12:127-156.
83. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J. 1990a. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130.
84. Snow DM, Steindler DA, Silver J. 1990b. Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier. Dev Biol 138:359-376.
85. Steindler DA. 1993. Glial boundaries in the developing nervous system. Annu Rev Neurosci 16:445-470.
86. Steindler D, Cooper NGF, Faissner A, Schachner M. 1989. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243-260.
87. Tolbert LP, Oland LA. 1989. A role for glia in the development of organized neuropilar structures. TINS 12:70-75.
88. Tolbert LP, Oland LA. 1990. Glial cells form boundaries for developing insect olfactory glomeruli. Exp Neurol 109:19-28.
89. Tolbert LP, Sirianni PA. 1990. Requirement for olfactory axons in the induction and stabilization of olfactory glomeruli in an insect. J Comp Neurol 298:69-82.
90. Tomaselli KJ, Neugebauer KM, Bixby JL, Lilien J, Reichardt LF. 1988. N-Cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1:33-43.
91. Treloar HB, Nurcombe V, Key B. 1996. Expression of extracellular matrix molecules in the embryonic rat olfactory pathway. J Neurobiol 31:41-55.
92. Valverde F, Santacana M, Heredia M. 1992. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49:255-275.
93. Valverde F, Heredia M, Santacana M. 1993. Characterization of neuronal cell varieties migrating from the olfactory epithelium during prenatal development in the rat. Immunocytochemical study using antibodies against olfactory marker protein (OMP) and luteinizing hormone-releasing hormone (LH-RH). Dev Brain Res 71:209-220.
94. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
95. Verhaagen J, Oestreicher AB, Grillo M, Khew-Goodall Y, Gispen WH, Margolis FL. 1990. Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J Neurosci Res 26:31-44.
96. Voight T. 1989. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74-88.
97. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
98. Whitlock KE, Westerfield M. 1998. A transient population of neurons pioneers the olfactory pathway in the zebrafish. J Neurosci 18:8919-8927.