Abstract
Expression and age-related changes of calbindin-D28k (CB), parvalbumin (PV), and calretinin (CR) in the main olfactory bulb of the dog were investigated by immunohistochemistry and western blot analysis. Neurons that expressed these calcium-binding proteins showed a characteristic laminar distribution. Most of CB-immunoreactive neurons were observed in the glomerular layer (GL) and the inner sublayer of the external plexiform layer (EPL). Most of PV-immunoreactive neurons were observed in the outer sublayer of the EPL. CR-immunoreactive neurons were mainly distributed in the GL and the granule cell layer. With regard to age-related changes, CB-immunoreactive neurons in the GL were stable among all age groups; however, in the EPL they decreased with age. PV-immunoreactive neurons decreased in middle-aged and aged groups. However, CR-immunoreactive neurons were not decreased in middle-aged and aged groups. These results suggest that CB-immunoreactive neurons in the EPL were most sensitive to aging, and that their reduction may be related to aging in the dog.
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Allison AC (1953) The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. J Comp Neurol 98(2):309–353
Alonso JR, Briñón JG, Crespo C, Bravo IG, Arévalo R, Aijón J (2001) Chemical organization of the macaque monkey olfactory bulb: II. Calretinin, calbindin D-28k, parvalbumin, and neurocalcin immunoreactivity. J Comp Neurol 432(3):389–407
Amenta F, Cavalotta D, Del Valle ME, Mancini M, Sabbatini M, Torres JM, Vega JA (1994) Calbindin D-28k immunoreactivity in the rat cerebellar cortex: age-related changes. Neurosci Lett 178(1):131–134
Araujo JA, Studzinski CM, Milgram NW (2005) Further evidence for the cholinergic hypothesis of aging and dementia from the canine model of aging. Prog Neuropsychopharmacol Biol Psychiatry 29(3):411–422
Bastianelli E, Polans AS, Hidaka H, Pochet R (1995) Differential distribution of six calcium-binding proteins in the rat olfactory epithelium during postnatal development and adulthood. J Comp Neurol 354(3):395–409
Bouvet JF, Delaleu JC, Holley A (1987) Olfactory receptor cell function is affected by trigeminal nerve activity. Neurosci Lett 77(2):181–186
Briñón JG, Martínez-Guijarro FJ, Bravo IG, Arévalo R, Crespo C, Okazaki K, Hidaka H, Aijón J, Alonso JR (1999) Coexpression of neurocalcin with other calcium-binding proteins in the rat main olfactory bulb. J Comp Neurol 407(3):404–414
Briñón JG, Weruaga E, Crespo C, Porteros A, Arévalo R, Aijón J, Alonso JR (2001) Calretinin-, neurocalcin-, and parvalbumin-immunoreactive elements in the olfactory bulb of the hedgehog (Erinaceus europaeus). J Comp Neurol 429(4):554–570
Bufler J, Zufall F, Franke C, Hatt H (1992) Patch-clamp recordings of spiking and nonspiking interneurons from rabbit olfactory bulb slices: membrane properties and ionic currents. J Comp Physiol [A] 170(2):145–152
Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35(2):375–475
Cummings BJ, Head E, Ruehl W, Milgram NW, Cotman CW (1996) The canine as an animal model of human aging and dementia. Neurobiol Aging 17(2):259–268
de Jong GI, Naber PA, Van der Zee EA, Thompson LT, Disterhoft JF, Luiten PG (1996) Age-related loss of calcium binding proteins in rabbit hippocampus. Neurobiol Aging 17(3):459–465
DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28k, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14(1):1–19
Finger TE, Böttger B (1993) Peripheral peptidergic fibers of the trigeminal nerve in the olfactory bulb of the rat. J Comp Neurol 334(1):117–124
Frasnelli J, Schuster B, Hummel T (2007) Interactions between olfaction and the trigeminal system: what can be learned from olfactory loss. Cereb Cortex 17(10):2268–2275
Gulyás AI, Hájos N, Freund TF (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16(10):3397–3411
Halász N, Shepherd GM (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10(3):579–619
Hamilton KA, Heinbockel T, Ennis M, Szabó G, Erdélyi F, Hayar A (2005) Properties of external plexiform layer interneurons in mouse olfactory bulb slices. Neuroscience 133(3):819–829
Heimer L (1968) Synaptic distribution of centripetal and centrifugal nerve fibres in the olfactory system of the rat. An experimental anatomical study. J Anat 103(Pt 3):413–432
Hwang IK, Kang TC, Lee JC, Lee IS, Park SK, An SJ, Jeong YG, Seo JG, Oh YS, Won MH (2002) Age-related change of calbindin D-28k immunoreactive neurons in the rat main olfactory bulb. Neurosci Lett 326(3):159–162
Hwang IK, Kim DS, Lee HY, Lee JY, Choi GP, Lee DI, Kim JD, Lee YB, Sohn HS, Kang TC, Won MH (2003) Age-related changes of parvalbumin immunoreactive neurons in the rat main olfactory bulb. Mol Cells 16(3):302–306
Hwang IK, Yoo KY, Nam YS, Choi JH, Seo K, Lee IS, Jung JY, Kang TC, Oh YS, Won MH (2006) Age-related changes in calretinin-immunoreactive periglomerular cells in the rat main olfactory bulb. J Vet Med Sci 68(5):465–469
Iacopino AM, Christakos S (1990) Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87(11):4078–4082
Iacopino AM, Rhoten WB, Christakos S (1990) Calcium binding protein (calbindin-D28k) gene expression in the developing and aging mouse cerebellum. Brain Res Mol Brain Res 8(4):283–290
Ichikawa H, Jacobowitz DM, Sugimoto T (1993) Calretinin-immunoreactive neurons in the trigeminal and dorsal root ganglia of the rat. Brain Res 617(1):96–102
Jacobowitz DM, Winsky L (1991) Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304(2):198–218
Kishimoto J, Tsuchiya T, Cox H, Emson PC, Nakayama Y (1998) Age-related changes of calbindin-D28k, calretinin, and parvalbumin mRNAs in the hamster brain. Neurobiol Aging 19(1):77–82
Kosaka K, Heizmann CW, Kosaka T (1994) Calcium-binding protein parvalbumin-immunoreactive neurons in the rat olfactory bulb. 1. Distribution and structural features in adult rat. Exp Brain Res 99(2):191–204
Kosaka K, Fujii M, Toida K, Kosaka T (1997) Differentiation of chemically defined neuronal populations in the transplanted olfactory bulb without olfactory receptor innervation. Neurosci Res 28(1):11–19
Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells. Neurosci Res 30(2):101–110
Kovács T (2004) Mechanisms of olfactory dysfunction in aging and neurodegenerative disorders. Ageing Res Rev 3(2):215–232
Kurobe N, Inaguma Y, Shinohara H, Semba R, Inagaki T, Kato K (1992) Developmental and age-dependent changes of 28-kDa calbindin-D in the central nervous tissue determined with a sensitive immunoassay method. J Neurochem 58(1):128–134
Lolova I, Davidoff M (1992) Age-related morphological and morphometrical changes in parvalbumin- and calbindin-immunoreactive neurons in the rat hippocampal formation. Mech Ageing Dev 66(2):195–211
McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86(4):1899–1907
Mirich JM, Williams NC, Berlau DJ, Brunjes PC (2002) Comparative study of aging in the mouse olfactory bulb. J Comp Neurol 454(4):361–372
Mori K, Shepherd GM (1994) Emerging principles of molecular signal processing by mitral/tufted cells in the olfactory bulb. Semin Cell Biol 5(1):65–74
Ohm TG, Müller H, Ulfig N, Braak E (1990) Glutamic-acid-decarboxylase-and parvalbumin-like-immunoreactive structures in the olfactory bulb of the human adult. J Comp Neurol 291(1):1–8
Ohm TG, Müller H, Braak E (1991) Calbindin-D-28k-like immunoreactive structures in the olfactory bulb and anterior olfactory nucleus of the human adult: distribution and cell typology—partial complementarity with parvalbumin. Neuroscience 42(3):823–840
Pinching AJ, Powell TP (1971) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9(2):305–345
Pressler RT, Strowbridge BW (2006) Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49(6):889–904
Price JL, Powell TP (1970) The mitral and short axon cells of the olfactory bulb. J Cell Sci 7(3):631–651
Pugliese M, Carrasco JL, Geloso MC, Mascort J, Michetti F, Mahy N (2004) Gamma-aminobutyric acidergic interneuron vulnerability to aging in canine prefrontal cortex. J Neurosci Res 77(6):913–920
Ramón y Cajal S (1909) Histologie du système nerveux de l’homme & des vertébrés, Maloine, Paris
Rawson NE (2006) Olfactory loss in aging. Sci Aging Knowledge Environ 2006(5):pe6
Résibois A, Rogers JH (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience 46(1):101–134
Rofina J, van Andel I, van Ederen AM, Papaioannou N, Yamaguchi H, Gruys E (2003) Canine counterpart of senile dementia of the Alzheimer type: amyloid plaques near capillaries but lack of spatial relationship with activated microglia and macrophages. Amyloid 10(2):86–96
Satoh J, Tabira T, Sano M, Nakayama H, Tateishi J (1991) Parvalbumin-immunoreactive neurons in the human central nervous system are decreased in Alzheimer’s disease. Acta Neuropathol (Berl) 81(4):388–395
Schaefer ML, Böttger B, Silver WL, Finger TE (2002) Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol 444(3):221–226
Schneider SP, Macrides F (1978) Laminar distributions of interneurons in the main olfactory bulb of the adult hamster. Brain Res Bull 3(1):73–82
Scott JW, McDonald JK, Pemberton JL (1987) Short axon cells of the rat olfactory bulb display NADPH-diaphorase activity, neuropeptide Y-like immunoreactivity, and somatostatin-like immunoreactivity. J Comp Neurol 260(3):378–391
Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. NeuroReport 6(18):2479–2482
Seto-Ohshima A, Emson PC, Lawson E, Mountjoy CQ, Carrasco LH (1988) Loss of matrix calcium-binding protein-containing neurons in Huntington’s disease. Lancet 1(8597):1252–1255
Shipley MT, Ennis M (1996) Functional organization of olfactory system. J Neurobiol 30(1):123–176
Stone H, Williams B, Carregal EJ (1968) The role of the trigeminal nerve in olfaction. Exp Neurol 21(1):11–19
Takahashi YK, Kurosaki M, Hirono S, Mori K (2004) Topographic representation of odorant molecular features in the rat olfactory bulb. J Neurophysiol 92(4):2413–2427
Villa A, Podini P, Panzeri MC, Racchetti G, Meldolesi J (1994) Cytosolic Ca2+ binding proteins during rat brain ageing: loss of calbindin and calretinin in the hippocampus, with no change in the cerebellum. Eur J NeuroSci 6(9):1491–1499
Wellis DP, Scott JW (1990) Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64(3):932–947
West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14(4):275–285
Wouterlood FG, Hrtig W (1995) Calretinin-immunoreactivity in mitral cells of the rat olfactory bulb. Brain Res 682(1–2):93–100
Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92(8):3371–3375
Zettel ML, Frisina RD, Haider SE, O’Neill WE (1997) Age-related changes in calbindin D-28k and calretinin immunoreactivity in the inferior colliculus of CBA/CaJ and C57Bl/6 mice. J Comp Neurol 386(1):92–110
Acknowledgments
The authors would like to thank Mr. Seok Han, Mr. Seung Uk Lee, and Ms. Hyun Sook Kim for their technical help in this study. This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD, Basic Research Promotion Fund; KRF-2007-412-J00502).
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Choi, J.H., Lee, C.H., Yoo, KY. et al. Age-related Changes in Calbindin-D28k, Parvalbumin, and Calretinin Immunoreactivity in the Dog Main Olfactory Bulb. Cell Mol Neurobiol 30, 1–12 (2010). https://doi.org/10.1007/s10571-009-9425-z
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DOI: https://doi.org/10.1007/s10571-009-9425-z