Stress induces neurogenesis in non-neuronal cell cultures of adult olfactory epithelium

Neuroscience

Volumn 88, Issue 2, 1999, Pages 571-583

  Feron F ^a,b   MacKay Sim, A ^b   Andrieu, J L ^a   Matthaei, K I ^c   Holley, A ^a   Sicard, G ^a  

^a UNIVERSITÉ LYON 1   (France)

^b GRIFFITH UNIVERSITY   (Australia)

^c Biology and Environment   (Australia)

Author keywords

Cell culture; Cell lineage; Keratinocyte; Neurogenesis; Rodent; Stress

Indexed keywords

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL SURFACE; KERATINOCYTE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY EPITHELIUM; PRIORITY JOURNAL; RAT; STRESS;

AGE FACTORS; ANIMALS; ANTIBODIES; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELLS, CULTURED; EPITHELIAL CELLS; KERATINOCYTES; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; OLFACTORY MARKER PROTEIN; OLFACTORY MUCOSA; OLFACTORY RECEPTOR NEURONS; RATS; RATS, WISTAR; SPECIFIC PATHOGEN-FREE ORGANISMS; STRESS; STRESS, MECHANICAL; TUBULIN;

EID: 0342321814     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00233-4     Document Type: Article

References (78)

1. Andres K. H. Differenzierung und regeneration von zinneszellen in der regio olfactoria. Naturwissenschaften. 17:1965;500.
2. Boudreau N., Werb Z., Bissell M. J. Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc. natn. Acad. Sci. U.S.A. 93:1996;3509-3513.
3. Bouvet J. F., Godinot F., Croze S., Delaleu J. C. Trigeminal substance P-like fibres in the frog olfactory mucosa. Chem. Senses. 12:1985;499-505.
4. Brandt L., Brittebo E. B., Feil V. J., Bakke J. E. Irreversible binding and toxicity of the herbicide dichlobenil (2,6-dichlorobenzonitrile) in the olfactory mucosa of mice. Toxicol. appl. Pharmac. 103:1990;491-501.
5. Caggiano M., Kauer J. S., Hunter D. D. Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron. 13:1994;339-352.
6. Calof A. L., Chikaraishi D. M. Analysis of neurogenesis in mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron. 3:1989;115-127.
7. Camara C. G., Harding J. W. Thymidine incorporation in the olfactory epithelium of mice: early exponential response induced by olfactory neurectomy. Brain Res. 308:1984;63-68.
8. 4 and other chemicals. Tissue Cell. 14:1982;717-733.
9. Carr V. M., Farbman A. I. The dynamics of cell death in the olfactory epithelium. Expl Neurol. 124:1993;308-314.
10. Carr V. M., Farbman A. I. Effect of ketamine on stress protein immunoreactivities in rat olfactory mucosa. NeuroReport. 5:1993;197-200.
11. Chen C. S., Mrksich M., Huang S., Whitesides G. M., Ingber D. E. Geometric control of cell life and death. Science. 276:1997;1425-1428.
12. DeHamer M. K., Guevara J. L., Hannon K., Olwin B. B., Calof A. L. Genesis of olfactory receptor neurons in vitro: regulation of progenitor cell divisions by fibroblast growth factors. Neuron. 13:1994;1083-1097.
13. Delaleu J. C., Sicard G. Physiological and histological recovery of the olfactory mucosa of the frog after a dichlobenil injection. Chem. Senses. 20:1995;433-440.
14. Farbman A. I. Developmental biology of olfactory sensory neurons. Semin. Cell Biol. 5:1994;3-10.
15. Farbman A. I., Buchholz J. A. Transforming growth factor-α and other growth factors stimulate cell division in olfactory epithelium in vitro. J. Neurobiol. 30:1996;267-280.
16. Féron F., Lizard G., Sicard G. Isolation of mature olfactory neurones using retrograde labelling and flow cytometry. J. Neurosci. Meth. 57:1995;9-14.
17. Genter M. B., Deamer N. J., Cao Y., Levi P. E. Effects of P450 inhibition on the olfactory toxicity of β,β′-iminodipropionitrile (IDPN) in the rat. J. Biochem. Toxicol. 9:1994;31-39.
18. Goldstein B. J., Schwob J. E. Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J. Neurosci. 16(12):1996;4005-4016.
19. Goldstein B. J., Wolozin B. L., Schwob J. E. FGF2 suppresses neurogenesis of a cell lines derived from rat olfactory epithelium. J. Neurobiol. 33:1997;411-428.
20. Gong Q., Liu W.-L., Srodon M., Foster T. D., Shipley M. T. Olfactory epithelial organotypic slice cultures: a useful tool for investigating olfactory neural development. Int. J. dev. Neurosci. 14:1996;841-852.
21. Gordon M. K., Mumm J. S., Davis R. A., Holcomb J. D., Calof A. L. Dynamics of MASH-1 expression in vitro and in vivo suggest a non-stem cell site of MASH-1 action in the olfactory receptor neuron lineage. Molec. cell. Neurosci. 6:1995;363-379.
22. Graziadei P. P. C. Cell dynamics in the olfactory mucosa. Tissue Cell. 5:1973;113-131.
23. Graziadei P. P. C. and Monti Graziadei G. A. (1978) Continuous nerve cell renewal in the olfactory system. In Development of Sensory Systems (ed. M. Jacobson), Vol. IX, pp. 55-83. Springer, Berlin.
24. Graziadei P. P. C., Monti Graziadei G. A. Neurogenesis and neurons regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8:1979;1-18.
25. Guillemot F., Lo L. C., Johnson J. E., Auerbach A., Anderson D. J., Joyner A. L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell. 75:1993;463-476.
26. Hempstead J. L., Morgan J. I. Monoclonal antibodies to the rat olfactory sustentacular cell. Brain Res. 288:1983;289-295.
27. Hildebrand A., Romaris M., Rasmussen L. M., Heinegard D., Twardzik D. R., Border W. A., Ruoslahti E. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem. J. 302:1994;527-534.
28. Hinds J. W., Hinds P. L., McNelly N. A. An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat. Rec. 210:1984;375-383.
29. Holbrook E. H., Szumowski K. E. M., Schwob J. E. An immunochemical, ultrastructural and developmental characterization of the horizontal basal cells of net olfactory epithelium. J. comp. Neurol. 363:1995;128-146.
30. Holcomb J. D., Mumm J. S., Calof A. L. Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and vitro. Devl Biol. 172:1995;307-323.
31. Huard J. M. T., Schwob J. E. Cell cycle of globose basal cells in rat olfactory epithelium. Devl Dynamics. 203:1995;17-26.
32. Hurtt M. E., Thomas D. A., Working P. K., Monticello T. M., Morgan K. T. Degeneration and regeneration of the olfactory epithelium following inhalation exposure to methyl bromide: pathology, cell kinetics and olfactory function. Toxicol. appl. Pharmac. 94:1988;311-328.
33. Keller A., Margolis F. Immunological studies of the rat olfactory marker protein. J. Neurochem. 24:1975;1101-1106.
34. Kindas-Mugge I., Trautinger F. Increased expression of the M(r) 27,000 heat shock protein (hsp27) in in vitro differentiated normal human keratinocytes. Cell Growth Differ. 5:1994;777-781.
35. Kudrycki K., Stein-Izsak C., Behn C., Grillo M., Akeson R., Margolis F. R. Olf-1-binding site: characterization of an olfactory neuron-specific promoter motif. Molec. cell. Biol. 13:1993;3002-3014.
36. Lindquist S., Craig E. A. The heat shock proteins. A. Rev. Genet. 22:1988;631-677.
37. MacDonald K. P. A., Murrell W. G., Bartlett P. F., Bushell G. R., Mackay-Sim A. FGF2 promotes neuronal differentiation in explant cultures of adult and embryonic mouse olfactory epithelium. J. Neurosci. Res. 44:1996;27-39.
38. Mackay-Sim A., Patel U. Regional differences in cell density and cell genesis in the olfactory epithelium of the salamander. Expl Brain Res. 57:1984;99-106.
39. Mackay-Sim A., Breipohl W., Kremer M. Cell dynamics in the olfactory epithelium of the tiger salamander: a morphometric analysis. Expl Brain Res. 71:1988;189-198.
40. Mackay-Sim A., Kittel P. Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J. Neurosci. 11:1991;979-984.
41. Mahanthappa N. K., Schwarting G. A. Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-βs. Neuron. 10:1993;293-305.
42. Maniotis A. J., Chen C. S., Ingber D. E. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. natn. Acd. Sci. U.S.A. 94:1997;849-854.
43. 4 and its subsequent regeneration. Am. J. Anat. 142:1975;67-90.
44. Menco B. P. M. Qualitative and quantitative freeze-fracture studies on olfactory and respiratory structures of frog, rat and dog. I. A general survey. Cell Tiss. Res. 207:1980;183-209.
45. Min Y. G., Rhee C. S., Choo M. J., Song H. K., Hong S. C. Histopathologic changes in the olfactory epithelium in mice after exposure to sulfur dioxide. Acta otolar. 114:1994;447-452.
46. Miragall F., Kadmon G., Husmann M., Schachner M. Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of NCAM. Devl Biol. 129:1988;516-531.
47. Moulton D. G. and Fink R. P. (1972) Cell proliferation and migration in the olfactory epithelium. In Olfaction and Taste IV, pp. 20-26. Verlags-Gesellschaft, Stuttgart.
48. Mumm J. S., Shou J., Calof A. L. Colony-forming progenitors from mouse olfactory epithelium: evidence for feedback regulation of neuron production. Proc. natn. Acad. Sci. U.S.A. 93:1996;11167-11172.
49. Murrell W., Bushell G. R., Livesey J., McGrath J., MacDonald K. P. A., Bates P. R., Mackay-Sim A. Neurogenesis in adult human. NeuroReport. 7:1996;1189-1194.
50. Nagahara Y. Experimentelle studien über die histologischen veränderungen des geruchsorgans nach der olfactoriusdurchschneidung. Beiträge zur kenntnis des feineren baus des geruchsorgans. Jap. J. med. Sci. V. Path. 5:1940;165-199.
51. Oriol R., Mancilla-Jimenez R. Fluorescent staining of nuclei and amyloid substance. Two useful properties of p-phenylenediamine. J. immun. Meth. 62:1983;185-192.
52. Pixley S. K. Purified cultures of keratin-positive olfactory epithelial cells: identification of a subset as neuronal supporting (sustentacular) cells. J. Neurosci. Res. 31:1992;693-707.
53. Pixley S. K. CNS glial cells support in vitro survival, division and differentiation of dissociated olfactory neuronal progenitor cells. Neuron. 8:1992;1191-1204.
54. Rama Krishna N. S., Little S. S., Getchell T. V. Epidermal growth factor receptor mRNA and protein are expressed in progenitor cells of the olfactory epithelium. J. comp. Neurol. 373:1996;297-307.
55. Reh T. A., Nagy T., Gretton H. Retinal pigmented epithelial cells induced to transdifferentiate to neurons by laminin. Nature. 330:1987;68-71.
56. Reh T. A., Kljavin I. J. Age of differentiation determines rat germinal cell phenotype: induction of differentiation by dissociation. J. Neurosci. 9:1989;4179-4189.
57. Reynolds B. A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1992;1707-1710.
58. Roberts G. P., Brunt J. Identification of an epidermal cell-adhesion glycoprotein. Biochem. J. 232:1985;67-70.
59. Rougon G., Dubois C., Buckley N., Magnani J. L., Zoolinger W. A monoclonal antibody against meningococcus group B polysaccharide distinguishes embryonic from adult NCAM. J. Cell Biol. 103:1986;2429-2437.
60. Ruoslahti E., Yamaguchi Y. Proteoglycans as modulators of growth factor activities. Cell. 64:1991;867-869.
61. Sakakibara S., Imai T., Hamaguchi K., Okabe M., Aruga J., Nakajima K., Yasutomi D., Nagata T., Kurihara Y., Uesugi S., Miyata T., Ogawa M., Mikoshiba K., Okano H. Mouse-Mushashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Devl Biol. 176:1996;230-242.
62. Satoh M., Takeuchi M. Induction of NCAM expression in mouse olfactory keratin-positive basal cells in vitro. Devl Brain Res. 87:1995;111-119.
63. Saucier D., Astic L. Morpho-functional alterations in the olfactory system of rainbow trout (Oncorhynchus mykiss) and possible acclimation in response to long-lasting exposure to low copper levels. Comp. Biochem. Physiol. 112A:1995;273-284.
64. Schultz E. W. Repair of the olfactory mucosa. Am. J. Path. 37:1960;1-19.
65. Schwob J. E., Huard J. M. T., Luskin M. B., Yougentob S. L. Retroviral lineage studies of the rat olfactory epithelium. Chem. Senses. 19:1994;671-682.
66. Schwob J. E., Yougentob S. L., Mezza R. C. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. comp. Neurol. 359:1995;15-37.
67. Smith C. G. Regeneration of sensory olfactory epithelium and nerves in adult frogs. Anat. Rec. 109:1951;661-671.
68. Suzuki Y., Takeda M. Basal cells in the mouse olfactory epithelium after axotomy: immunohistochemical and electron-microscopic studies. Cell Tiss. Res. 266:1991;239-245.
69. Suzuki Y., Takeda M. Keratins in the developing olfactory epithelia. Devl Brain Res. 59:1991;171-178.
70. Suzuki Y., Takeda M. Basal cells in the mouse olfactory epithelium during development: immunohistochemical and electron-microscopic studies. Devl Brain Res. 73:1993;107-113.
71. Verhaagen J., Oestreicher A. B., Grillo M., Khew-Goodall Y. S., Gispen W. H., Margolis F. L. 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. 26:1990;31-44.
72. Vescovi A. L., Reynolds B. A., Fraser D. D., Weiss S. bFGF regulates the proliferative rate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron. 11:1993;951-966.
73. Vollrath M., Altmannsberger M., Weber K., Osborn M. An ultrastructural and immunohistological study of the rat olfactory epithelium: unique properties of olfactory sensory cells. Differentiation. 29:1985;243-253.
74. Walters E., Grillo M., Oestreicher A. B., Margolis F. Lac Z and OMP are co-expressed during ontogeny and regeneration in olfactory receptor neurons of OMP promoter-lacZ transgenic mice. Int. J. dev. Neurosci. 14:1996;813-822.
75. Weaver V. M., Petersen O. W., Wang F., Larabell C. A., Briand P., Damsky C., Bissell M. J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137:1997;231-245.
76. Welch W. J. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72:1992;1063-1081.
77. Westerman R. A., von Baumgarten R. Regeneration of olfactory paths in carp. Experientia. 20:1964;519-520.
78. Yamagishi M., Hasegawa S., Takahashi S., Nakano Y., Iwanaga T. Immunohistochemical analysis of the olfactory mucosa by use of antibodies to brain proteins and cytokeratin. Ann. Otorhinolar. 98:1989;348-388.