Development and further characterization of a small subclass of rat olfactory receptor neurons that shows immunoreactivity for the HSP70 heat shock protein

Journal of Comparative Neurology

Volumn 404, Issue 3, 1999, Pages 375-386

  Carr, Virginia Mcmillan ^a   Morimoto, Richard I ^a   Farbman, Albert I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Immunohistochemistry; Olfactory bulb; Olfactory epithelium; Olfactory neurogenesis; Stress proteins

Indexed keywords

HEAT SHOCK PROTEIN;

ANIMAL CELL; ARTICLE; GUINEA PIG; HAMSTER; IMMUNOREACTIVITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; RAT; SMELLING; SWINE;

ANIMALS; ANIMALS, NEWBORN; AUTORADIOGRAPHY; CELL COUNT; CRICETINAE; EPITHELIAL CELLS; EPITHELIUM; GERBILLINAE; GUINEA PIGS; HSP70 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; MESOCRICETUS; MICE; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0033557188     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990215)404:3<375::AID-CNE7>3.0.CO;2-8     Document Type: Article

References (69)

1. Agard D. 1993. To fold or not to fold. . . . Science 260:1903-1904.
2. Beckmann RP, Mizzen LA, Welch WJ. 1990. Interactions of hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science 248:850-854.
3. Beckmann RP, Lovett M, Welch WJ. 1992. Examining the function and regulation of hsp70 in cells subjected to metabolic stress. J Cell Biol 117:1137-1150.
4. Black MM, Chestnut MH, Pleasure IT, Keen JH. 1991. Stable clathrin: uncoating protein (hsp70) complexes in intact neurons and in their axonal transport. J Neurosci 11:1163-1172.
5. Brunjes PC, Frazier LL. 1986. Maturation and plasticity in the olfactory system of vertebrates. Brain Res Rev 11:1-45.
6. Byrd CA, Jones JT, Quattro JM, Rogers ME, Brunjes PC, Vogt RG. 1996. Ontogeny of odorant receptor gene expression in zebrafish, Danio rerio. J Neurobiol 29:445-458.
7. Caggiano M, Kauer JS, Hunter DD. 1994. Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13:339-352.
8. Carr VMcM, Farbman AI. 1995a. Development of rat olfactory receptor neurons subclass reactive with a monoclonal antibody to HSP70. Chem Senses 20:675.
9. Carr VMcM, Farbman AI. 1995b. Developmental study of a rat olfactory receptor neuron subclass reactive with an α-HSP70 monoclonal antibody. Soc Neurosci Abstr 21:572.
10. Carr VMcM, Farbman AI. 1997. Initial development of a small subclass of rat olfactory receptor neurons characterized by antigenicity to HSP70. Chem Senses 22: 57.
11. Carr VMcM, Farbman AI. 1998. Initial development of a small subclass of rat olfactory receptor neurons characterized by antigenicity to HSP70. Ann NY Acad Sci (in press).
12. Carr VMcM, Murphy SP, Morimoto RI, Farbman AI. 1994. Small subclass of rat olfactory neurons with specific bulbar projections is reactive with monoclonal antibodies to the HSP70 heat shock protein. J Comp Neurol 348:150-160.
13. Carr VMcM, Ring G, Youngentob SL, Schwob JE, Farbman AI. 1998. HSP(+)olfactory receptor neuron (ORN) bulbar projections following methyl bromide (meBr) lesion of the rat olfactory epithelium (OE). Neurosci Abstr 24:1144.
14. Chirico WJ, Walters MG, Bloel G. 1988. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332:805-810.
15. Craig EA. 1993. Chaperones: helpers along the pathways to protein folding. Science 260:1902-1903.
16. Deshaies RJ, Koch BD, Werner-Washburne M, Craig EA, Schekman R. 1988. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332:800-805.
17. Freeman BC, Morimoto RI. 1996. The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 15:2969-2979.
18. Gesteland RJ, Yancy RA, Farbman AI. 1982. Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience 7:3127-3136.
19. Graziadei PPC, Monti Graziadei GA. 1978. Continuous nerve cell renewal in the olfactory system. In: Jacobson M, editor. Handbook of sensory physiology, vol. IX. The development of sensory systems. Berlin: Springer-Verlag, p 55-82.
20. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-580.
21. Hightower LE. 1991. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66:191-197.
22. Johnson RN, Kucey BL. 1988. Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science 242:1551-1554.
23. Kasowski HJ, Kim H, Greer CA. 1996. Intrinsic organization of the olfactory bulb glomerulus. Chem Senses 21:621.
24. Kirstein CL, Coopersmith R; Bridges RJ, Leon M. 1991. Glutathione levels in olfactory and non-olfactory neural structures of rats. Brain Res 543:341-346.
25. Klenoff JR, Greer CA. 1998. Postnatal development of olfactory receptor cell axonal arbors. J Comp Neurol 390:256-267.
26. Kubick S, Strotmann J, Andreini I, Breer H. 1997. Subfamily of olfactory receptors characterized by unique structural features and expression patterns. J Neurochem 69:465-475.
27. LaMantia A-S, Purves D. 1989. Development of glomerular pattern visualized in the olfactory bulbs of living mice. Nature 341:646-649.
28. Li GC, Laszlo A. 1985. Amino acid analogs while inducing heat shock proteins sensitize CHO cells to thermal damage. J Cell Physiol 122:91-97.
29. Li GC, Werb Z. 1982. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci USA 79:3218-3222.
30. Liang R, MacRae TH. 1997. Molecular chaperones and the cytoskeleton. J Cell Sci 110:1431-1440.
31. Liebich HG. 1975. Zum Bau der oberen Luftwege der weissen Ratte (Mus rattus norvegicus, var. albinos). Anat Anz 138:170-179.
32. Manzerra P, Rush SJ, Brown IR. 1997. Tissue-specific differences in heat shock protein hsc70 and hsp70 in control and hyperthermic rabbit. J Cell Physiol 170:130-137.
33. Mehlen P, Hickey E, Weber LA, Arrigo A-P. 1997. Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFα in NIH-3T3-ras cells. Biochem Biophys Res Commun 241:187-192.
34. Mehlen P, Kretz-Remy C, Briolay J, Fostan P, Mirault M-E, Arrigo A-P. 1995. Intracellular reactive oxygen species as apparent modulators of heat-shock protein 27 (hsp27) structural organization and phosphorylation in basal and tumour necrosis factor α-treated T47D human carcinoma cells. Biochem J 312:367-375.
35. Mehlen P, Kretz-Remy C, Préville X, Arrigo A-P. 1996. Human hsp27, Drosophila hsp27 and human αB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFα-induced cell death. EMBO J 15:2695-2706.
36. Meisami E. 1979. The developing rat olfactory bulb: prospects of a new model system in developmental neurobiology. In: Meisami E, Brazier MAB, editors. Neural growth and differentiation. New York: Raven Press, p 183-206
37. 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 in glomeruli in the rat olfactory bulb. Brain Res 221:81-107.
38. Menco BPM, Jackson JE. 1997. Abanded topography in the developing rat's olfactory epithelial surface. J Comp Neurol 388:293-306.
39. 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.
40. Mori K, Fujita SC, Imamura K, Obata K. 1985. Immunohistochemical study of subclasses of olfactory nerve fibers and their projections to the olfactory bulb in the rabbit. J Comp Neurol 242:214-229.
41. Morimoto RI, Tissières A, Georgopoulos C. 1990. The stress response, function of proteins, and perspectives. In: Morimoto RI, Tissieres A, Georgopoulos C, editors. Stress proteins in biology and medicine. Cold Spring Harbor, NY: Cold Spring Laboratory Press, p 1-36.
42. Morimoto RI, Tissières A, Georgopoulos C, editors. 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
43. Moulton DG, Çelebi G, Fink RP. 1970. Olfaction in mammals - two aspects: proliferation of cells in the olfactory epithelium and sensitivity to odours. In: Wolstenholme GEW, Knight J, editors. Ciba Foundation Symposium on Taste and Smell in Vertebrates. London: Churchill Press, p 227-250.
44. Nef S, Allaman I, Fiumelli H, De Castro E, Nef P. 1996. Olfaction in birds: differential embryonic expression of nine putative odorant receptor genes in the avian olfactory system. Mech Dev 55:65-77.
45. Plumier J-CL, Hopkins DA, Robertson HA, Currie RW. 1987. Constitutive expression of the 27-kDa heat shock protein (Hsp27) in sensory and motor neurons of the rat nervous system. J Comp Neurol 384:409-428.
46. Rama Krishna NS, Getchell ML, Tate SS, Margolis FL, Getchell TV. 1992. Glutathione and γ-glutamyl transpeptidase are differentially distributed in the olfactory mucosa of rats. Cell Tissue Res 270:475-484.
47. Rassow J, Voos W, Pfanner N. 1995. Partner proteins determine multiple functions of Hsp70. Trends Cell Biol 5:207-212.
48. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
49. 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.
50. Riabowol KT, Mizzen LA, Welch WJ. 1988. Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 242: 433-436.
51. Ring G, Mezza RJ, Schwob JE. 1997. Immunohistochemical identification of discrete subsets of rat olfactory neurons and the glomeruli they innervate. J Comp Neurol 388:415-434.
52. Sato K, Saito H, Matsuli N. 1996. HSP70 is essential to the neuroprotective effect of heat shock. Brain Res 740:117-123.
53. Schwob JE, Gottlieb DI. 1986. The primary olfactory projection has two chemically distinct zones. J Neurosci 6:3393-3404.
54. Schwob JE, Gottlieb DI. 1988. Purification and characterization of an antigen that is spatially segregated in the primary olfactory projection. J Neurosci 8:3470-3480.
55. Starcevic SL, Zielinski BS. 1997. Neuroprotective effects of glutathione on rainbow trout olfactory receptor neurons during exposure to copper sulfate. Comp Biochem Physiol 117C:211-219.
56. Strotmann J, Wanner I, Krieger J, Earning K, Breer H. 1992. Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. Neuroreport 3:1053-1056.
57. Strotmann J, Wanner I, Helfrich T, Beck A, Meinken C, Kubick S, Breer H. 1994a. Olfactory neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal neuroepithelium. Cell Tissue Res 276:429-438.
58. Strotmann J, Wanner I, Helfrich T, Beck A, Breer H. 1994b. Rostro-caudal patterning of receptor-expressing olfactory neurones in the rat nasal cavity. Cell Tissue Res 278:11-20.
59. Strotmann J, Wanner I, Helfrich T, Breer H. 1995. Receptor expression in olfactory neurons during rat development: in situ hybridization studies. Eur J Neurosci 7:492-500.
60. Strotmann J, Konzelmann S, Breer H. 1996. Laminar segregation of odorant receptor expression in the olfactory epithelium. Cell Tissue Res 284:347-354.
61. Sullivan S, Bohm S, Ressler KJ, Horowitz LF, Buck LB. 1995. Target-independent pattern specification in the olfactory epithelium. Neuron 15 779-789.
62. Tytell M. 1994. Heat shock proteins in the retina and optic nerve. In: Mayer RJ, Brown IR, editors. Heat shock proteins in the nervous system. New York: Academic Press, p 83-100.
63. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
64. Vassar R, Chao SK, Sitcheran R, Nuñoz JM, Vosshail LB, Axel. R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
65. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
66. Weiler E, Farbman AI. 1997. Proliferation in the rat olfactory epithelium: age-dependent changes. J Neurosci 17:3620-3622.
67. Welsh WJ. 1993. Heat shock proteins functioning as molecular chaperones: their roles in normal and stressed cells. Phil Trans R Soc London (Biol) 339 327-333.
68. Williams NE, Nelson EM. 1997. HSP70 and HSP90 homologs are associated with tubulin in hetero-oligomeric complexes, cilia, and the cortex of Tetrahymena. J Cell Sci 110:1665-1672.
69. 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 to olfactory and vomeronasal axons. J Neurosci 17:5830-5842.