Abstract
Sall3 is a member of a gene family with homology to the spalt gene of Drosophila melanogaster, encoding transcription factors, and acts as downstream target of hedgehog. Vertebrate homologues of spalt have been shown to be involved in development of the limbs and nervous system and several organs including the kidney and heart; mutations in the genes are implicated in several human genetic disorders. Recent studies have shown a total loss of olfactory bulb (OB) dopaminergic (DA) neurons in Sall3-null mice. We assume that tyrosine hydroxylase (TH) may be regulated by Sall3 in OB. In this study, we find that Sall3 and TH co-localize in glomerular layer (GL) of OB. Furthermore, we demonstrate a significant induction of the proximal TH promoter transcription activity by Sall3 in dual-luciferase reporter assay and a reduction of TH expression level in Sall3-deficient cell lines. Collectively, these findings support the notion that Sall3 correlates with the expression of TH in mouse OB and may have a role in OB DA neuron development by regulating TH gene expression. The results from this study may advance our understanding of the molecular pathways of OB in the DA neuron development and differentiation.
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Adler CH (2005) Nonmotor complications in Parkinson’s disease. Mov Disord 20(Suppl 11):S23–S29
Allen ZJ 2nd, Waclaw RR, Colbert MC, Campbell K (2007) Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomerular neuron subtypes. J Mol Histol 38:517–525
Anderson S, Mione M, Yun K, Rubenstein JL (1999) Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis. Cereb Cortex 9:646–654
Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69–78
Belzunegui S, San Sebastian W, Garrido-Gil P et al (2007) The number of dopaminergic cells is increased in the olfactory bulb of monkeys chronically exposed to MPTP. Synapse 61:1006–1012
Carpaneto A, Accardi A, Pisciotta M, Gambale F (1999) Chloride channels activated by hypotonicity in N2A neuroblastoma cell line. Exp Brain Res 124:193–199
Cave JW, Akiba Y, Banerjee K, Bhosle S, Berlin R, Baker H (2010) Differential regulation of dopaminergic gene expression by Er81. J Neurosci 30:4717–4724
Crawford GD Jr, Le WD, Smith RG, Xie WJ, Stefani E, Appel SH (1992) A novel N18TG2 x mesencephalon cell hybrid expresses properties that suggest a dopaminergic cell line of substantia nigra origin. J Neurosci 12:3392–3398
Datiche F, Cattarelli M (1996) Catecholamine innervation of the piriform cortex: a tracing and immunohistochemical study in the rat. Brain Res 710:69–78
De Marchis S, Bovetti S, Carletti B et al (2007) Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657–664
Dellovade TL, Pfaff DW, Schwanzel-Fukuda M (1998) Olfactory bulb development is altered in small-eye (Sey) mice. J Comp Neurol 402:402–418
Harrison SJ, Parrish M, Monaghan AP (2008) Sall3 is required for the terminal maturation of olfactory glomerular interneurons. J Comp Neurol 507:1780–1794
Huisman E, Uylings HB, Hoogland PV (2004) A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson’s disease. Mov Disord 19:687–692
Kawakami Y, Uchiyama Y, Rodriguez Esteban C et al (2009) Sall genes regulate region-specific morphogenesis in the mouse limb by modulating Hox activities. Development 136:585–594
Kiefer SM, McDill BW, Yang J, Rauchman M (2002) Murine Sall1 represses transcription by recruiting a histone deacetylase complex. J Biol Chem 277:14869–14876
Kuhnlein RP, Frommer G, Friedrich M et al (1994) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J 13:168–179
Le W, Conneely OM, Zou L et al (1999) Selective agenesis of mesencephalic dopaminergic neurons in Nurr1-deficient mice. Exp Neurol 159:451–458
Li D, Tian Y, Ma Y, Benjamin T (2004) p150(Sal2) is a p53-independent regulator of p21(WAF1/CIP). Mol Cell Biol 24:3885–3893
Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189
Luskin MB, Zigova T, Soteres BJ, Stewart RR (1997) Neuronal progenitor cells derived from the anterior subventricular zone of the neonatal rat forebrain continue to proliferate in vitro and express a neuronal phenotype. Mol Cell Neurosci 8:351–366
Ott T, Parrish M, Bond K, Schwaeger-Nickolenko A, Monaghan AP (2001) A new member of the spalt like zinc finger protein family, Msal-3, is expressed in the CNS and sites of epithelial/mesenchymal interaction. Mech Dev 101:203–207
Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825–836
Quinn NP, Rossor MN, Marsden CD (1987) Olfactory threshold in Parkinson’s disease. J Neurol Neurosurg Psychiatry 50:88–89
Saino-Saito S, Cave JW, Akiba Y et al (2007) ER81 and CaMKIV identify anatomically and phenotypically defined subsets of mouse olfactory bulb interneurons. J Comp Neurol 502:485–496
Schnaufer C, Breer H, Fleischer J (2009) Outgrowing olfactory axons contain the Reelin receptor VLDLR and navigate through the Reelin-rich cribriform mesenchyme. Cell Tissue Res 337:393–406
Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167–174
Sweetman D, Smith T, Farrell ER, Chantry A, Munsterberg A (2003) The conserved glutamine-rich region of chick csal1 and csal3 mediates protein interactions with other spalt family members. Implications for Townes-Brocks syndrome. J Biol Chem 278:6560–6566
Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759–3771
Wilson DA, Sullivan RM (1995) The D2 antagonist spiperone mimics the effects of olfactory deprivation on mitral/tufted cell odor response patterns. J Neurosci 15:5574–5581
Acknowledgments
This study was supported by research funds from the Nature Science Foundation of China (No. 30730096 and 39070925), from the National Basic Research Program of China (2011CB510003 and 2010CB945200), and a grant awarded by the “Shanghai-Baden-Wüertternberg program” from Shanghai Pujiang Research Program (09PJD014). The authors thank Andrea Bader (Institute of Physiology, University of Hohenheim, Stuttgart, Germany) for her excellent technical support of in situ hybridization experiment.
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Heng, X., Breer, H., Zhang, X. et al. Sall3 Correlates with the Expression of TH in Mouse Olfactory Bulb. J Mol Neurosci 46, 293–302 (2012). https://doi.org/10.1007/s12031-011-9563-x
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DOI: https://doi.org/10.1007/s12031-011-9563-x