Cell Death in the Olfactory System

doi:10.1017/CBO9780511976094.018

18 - Cell Death in the Olfactory System

from Part II - Cell Death in Tissues and Organs

Published online by Cambridge University Press: 07 September 2011

Edited by

Douglas R. Green: Affiliation:
St. Jude Children's Research Hospital, Memphis, Tennessee
Pawel Kermer: Affiliation:
DFG Research Center “Molecular Physiology of the Brain” (CMPB), Germany
John C. Reed: Affiliation:
Sanford-Burnham Medical Research Institute, La Jolla, California

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Summary

Introduction

The olfactory system is one of the most plastic regions in the brain, where neurons are continuously replaced and neuronal circuits are modulated throughout life. Although there is a constant replacement of receptor neurons in the adult olfactory epithelium, there is a perpetual integration of new neurons into the adult olfactory bulb. Hence a fine-tuned program to balance neuronal apoptosis and survival is necessary. This chapter summarizes current knowledge about life and death in the adult olfactory epithelium and olfactory bulb after illustrating normal olfactory anatomy. Finally, olfactory neuronal death is revisited in the context of neurodegenerative diseases.

Type: Chapter
Information: Apoptosis
Physiology and Pathology
, pp. 194 - 200

DOI: https://doi.org/10.1017/CBO9780511976094.018 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2011

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References

Altman, J.Autoradiographic and histological studies of postnatal neurogenesis (1969) IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol. 137(4):433–57.

Alvarez-Buylla, A, García-Verdugo, JM, Tramontin, AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci. 2(4):287–93.

Ansari, KA, Johnson, A (1975) Olfactory function in patients with Parkinson's disease. J Chronic Dis. 28(9):493–7.

Anton, ES, Ghashghaei, HT, Weber, JL, McCann, C, Fischer, TM, Cheung, ID, Gassmann, M, Messing, A, Klein, R, Schwab, MH, Lloyd, KC, Lai, C (2004) Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci. 7(12):1319–28.

Braak, H, Braak, E (1998) Evolution of neuronal changes in the course of Alzheimer's disease. J Neural Transm Suppl. 53:127–40.

Braak, H, Del Tredici, K, Rüb, U, de Vos, RA, Jansen Steur, EN, Braak, E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. 24(2):197–211.

Brazel, CY, Nuñez, JL, Yang, Z, Levison, SW (2005) Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience. 131(1):55–65.

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(2):339–52.

Corotto, FS, Henegar, JR, Maruniak, JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience. 61(4):739–44.

Cowan, CM, Thai, J, Krajewski, S, Reed, JC, Nicholson, DW, Kaufmann, SH, Roskams, AJ (2001) Caspases 3 and 9 send a pro-apoptotic signal from synapse to cell body in olfactory receptor neurons. J Neurosci. 21(18):7099–109.

Cowan, CM, Roskams, AJ (2002) Apoptosis in the mature and developing olfactory neuroepithelium. Microsc Res Tech. 58(3):204–15.

Cowan, CM, Roskams, AJ (2004) Caspase-3 and caspase-9 mediate developmental apoptosis in the mouse olfactory system. J Comp Neurol. 474(1):136–48.

Cremer, H, Lange, R, Christoph, A, Plomann, M, Vopper, G, Roes, J, Brown, R, Baldwin, S, Kraemer, P, Scheff, S, et al. (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 367(6462):455–9.

Crino, PB, Martin, JA, Hill, WD, Greenberg, B, Lee, VM, Trojanowski, JQ (1995) Beta-Amyloid peptide and amyloid precursor proteins in olfactory mucosa of patients with Alzheimer's disease, Parkinson's disease, and Down syndrome. Ann Otol Rhinol Laryngol. 104(8):655–61.

Daniel, SE, Hawkes, CH (1992) Preliminary diagnosis of Parkinson's disease by olfactory bulb pathology. Lancet. 340(8812):186.

Deckner, ML, Risling, M, Frisén, J (1997) Apoptotic death of olfactory sensory neurons in the adult rat. Exp Neurol. 143(1):132–40.

Doetsch, F, García-Verdugo, JM, Alvarez-Buylla, A (1999) Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A. 96(20):11619–24.

Doty, RL, Shaman, P, Applebaum, SL, Giberson, R, Siksorski, L, Rosenberg, L (1984) Smell identification ability: changes with age. Science. 226(4681):1441–3.

Enwere, E, Shingo, T, Gregg, C, Fujikawa, H, Ohta, S, Weiss, S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci. 24(38):8354–65.

Farbman, AI (1990) Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci. 13(9):362–5.

Farbman, AI, Brunjes, PC, Rentfro, L, Michas, J, Ritz, S (1988) The effect of unilateral naris occlusion on cell dynamics in the developing rat olfactory epithelium. J Neurosci. 8(9):3290–5.

Farbman, AI, Buchholz, JA, Suzuki, Y, Coines, A, Speert, D (1999) A molecular basis of cell death in olfactory epithelium. J Comp Neurol. 414(3):306–14.

Gage, FH (2002) Neurogenesis in the adult brain. J Neurosci. 22(3):612–3.

Garcia, AD, Doan, NB, Imura, T, Bush, TG, Sofroniew, MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci. 7(11):1233–41.

Gascon, E, Vutskits, L, Jenny, B, Durbec, P, Kiss, JZ (2007) PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development. 134(6):1181–90.

Gheusi, G, Cremer, H, McLean, H, Chazal, G, Vincent, JD, Lledo, PM (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A. 97(4):1823–8.

Gould, E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci. 8(6):481–8.

Graves, AB, Bowen, JD, Rajaram, L, McCormick, WC, McCurry, SM, Schellenberg, GD, Larson, EB (1999) Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology. 53(7):1480–7

Graziadei, PP (1973) Cell dynamics in the olfactory mucosa. Tissue Cell. 5(1):113–31.

Graziadei, PP, Monti Graziadei, GA (1980) Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J Neurocytol. 9(2):145–62.

Hack, MA, Saghatelyan, A, de Chevigny, A, Pfeifer, A, Ashery-Padan, R, Lledo, PM, Götz, M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci. 8(7):865–72.

Haehner, A, Hummel, T, Hummel, C, Sommer, U, Junghanns, S, Reichmann, H (2007) Olfactory loss may be a first sign of idiopathic Parkinson's disease. Mov Disord. 22(6):839–42.

Hawkes, C (2006) Olfaction in neurodegenerative disorder. Adv Otorhinolaryngol. 63:133–51.

Hinds, JW, Hinds, PL, McNelly, NA (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat Rec. 210(2):375–83.

Holcomb, JD, Mumm, JS, Calof, AL (1995) Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro. Dev Biol. 172(1):307–23.

Jourdan, F, Moyse, E, De Bilbao, F, Dubois-Dauphin, M (1998) Olfactory neurons are protected from apoptosis in adult transgenic mice over-expressing the bcl-2 gene. Neuroreport 9(5):921–6.

Kim, WR, Kim, Y, Eun, B, Park, OH, Kim, H, Kim, K, Park, CH, Vinsant, S, Oppenheim, RW, Sun, W (2007) Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci. 27(52):14392–403.

Kovács, T, Cairns, NJ, Lantos, PL (2001) Olfactory centres in Alzheimer's disease: olfactory bulb is involved in early Braak's stages. Neuroreport 12(2):285–8.

Li, L, Liu, F, Salmonsen, RA, Turner, TK, Litofsky, NS, Di Cristofano, A, Pandolfi, PP, Jones, SN, Recht, LD, Ross, AH (2002) PTEN in neural precursor cells: regulation of migration, apoptosis, and proliferation. Mol Cell Neurosci. 20(1):21–9.

Lledo, PM, Saghatelyan, A (2005) Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 28(5):248–54.

Lledo, PM, Alonso, M, Grubb, MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 7(3):179–93.

Lois, C, García-Verdugo, JM, Alvarez-Buylla, A (1996) Chain migration of neuronal precursors. Science. 271(5251):978–81.

Mackay-Sim, A, Kittel, P (1991) Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci. 11(4):979–84.

Magrassi, L, Graziadei, PP (1995) Cell death in the olfactory epithelium. Anat Embryol (Berl). 192(1):77–87.

Miwa, N, Storm, DR (2005) Odorant-induced activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in the olfactory bulb promotes survival of newly formed granule cells. J Neurosci. 25(22):5404–12.

Pellier, V, Astic, L (1994) Cell death in the developing olfactory epithelium of rat embryos. Brain Res Dev Brain Res. 79(2):307–15.

Petreanu, L, Alvarez-Buylla, A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 22(14):6106–13.

Robinson, AM, Conley, DB, Shinners, MJ, Kern, RC (2002) Apoptosis in the aging olfactory epithelium. Laryngoscope. 112(8 Pt 1):1431–5.

Robinson, AM, Conley, DB, Kern, RC (2003) Olfactory neurons in bax knockout mice are protected from bulbectomy-induced apoptosis. Neuroreport. 14(15):1891–4.

Rochefort, C, Gheusi, G, Vincent, JD, Lledo, PM (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci. 22(7):2679–89.

Ross, GW, Abbott, RD, Petrovitch, H, Tanner, CM, Davis, DG, Nelson, J, Markesbery, WR, Hardman, J, Masaki, K, Launer, L, White, LR (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord. 21(12):2062–7.

Saghatelyan, A, Roux, P, Migliore, M, Rochefort, C, Desmaisons, D, Charneau, P, Shepherd, GM, Lledo, PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron. 46(1):103–16.

Sanai, N, Tramontin, AD, Quiñones-Hinojosa, A, Barbaro, NM, Gupta, N, Kunwar, S, Lawton, MT, McDermott, MW, Parsa, AT, Manuel-García Verdugo, J, Berger, MS, Alvarez-Buylla, A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 427(6976):740–4.

Schwob, JE, Szumowski, KE, Stasky, AA (1992) Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci. 12(10):3896–919.

Sommer, U, Hummel, T, Cormann, K, Mueller, A, Frasnelli, J, Kropp, J, Reichmann, H (2004) Detection of presymptomatic Parkinson's disease: combining smell tests, transcranial sonography, and SPECT. Mov Disord. 19(10):1196–202.

Stevens, JC, Cain, WS (1987) Old-age deficits in the sense of smell as gauged by thresholds, magnitude matching, and odor identification. Psychol Aging. 2(1):36–42.

Suzuki, Y (2004) Fine structural aspects of apoptosis in the olfactory epithelium. J Neurocytol. 33(6):693–702.

Suzuki, Y, Farbman, AI (2000) Tumor necrosis factor-alpha-induced apoptosis in olfactory epithelium in vitro: possible roles of caspase 1 (ICE), caspase 2 (ICH-1), and caspase 3 (CPP32). Exp Neurol. 165(1):35–45.

Suzuki, Y, Takeda, M (1991) Basal cells in the mouse olfactory epithelium after axotomy: immunohistochemical and electron-microscopic studies. Cell Tissue Res. 266(2):239–45.

Talamo, BR, Rudel, R, Kosik, KS, Lee, VM, Neff, S, Adelman, L, Kauer, JS (1989) Pathological changes in olfactory neurons in patients with Alzheimer's disease. Nature. 337(6209):736–9.

Tomasiewicz, H, Ono, K, Yee, D, Thompson, C, Goridis, C, Rutishauser, U, Magnuson, T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron. 11(6):1163–74.

Winner, B, Cooper-Kuhn, CM, Aigner, R, Winkler, J, Kuhn, HG (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci. 16(9):1681–9.

Yamada, M, Onodera, M, Mizuno, Y, Mochizuki, H (2004) Neurogenesis in olfactory bulb identified by retroviral labeling in normal and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated adult mice. Neuroscience. 124(1):173–81.

Yamagishi, M, Ishizuka, Y, Seki, K (1994) Pathology of olfactory mucosa in patients with Alzheimer's disease. Ann Otol Rhinol Laryngol. 103(6):421–7.