Top

Published in:

01-09-2018 | Original Article

Mash1-expressing cells could differentiate to type III cells in adult mouse taste buds

Authors: Hiroki Takagi, Yuji Seta, Shinji Kataoka, Mitsushiro Nakatomi, Takashi Toyono, Tatsuo Kawamoto

Published in: Anatomical Science International | Issue 4/2018

Abstract

The gustatory cells in taste buds have been identified as paraneuronal; they possess characteristics of both neuronal and epithelial cells. Like neurons, they form synapses, store and release transmitters, and are capable of generating an action potential. Like epithelial cells, taste cells have a limited life span and are regularly replaced throughout life. However, little is known about the molecular mechanisms that regulate taste cell genesis and differentiation. In the present study, to begin to understand these mechanisms, we investigated the role of Mash1-positive cells in regulating adult taste bud cell differentiation through the loss of Mash1-positive cells using the Cre-loxP system. We found that the cells expressing type III cell markers—aromatic L-amino acid decarboxylase (AADC), carbonic anhydrase 4 (CA4), glutamate decarboxylase 67 (GAD67), neural cell adhesion molecule (NCAM), and synaptosomal-associated protein 25 (SNAP25)—were significantly reduced in the circumvallate taste buds after the administration of tamoxifen. However, gustducin and phospholipase C beta2 (PLC beta2)—markers of type II taste bud cells—were not significantly changed in the circumvallate taste buds after the administration of tamoxifen. These results suggest that Mash1-positive cells could be differentiated to type III cells, not type II cells in the taste buds.

Beidler LM, Smallman RI (1965) Renewal of cells within taste buds. J Cell Biol 27:263–272CrossRefPubMedPubMedCentral

Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD (1996) Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers and Mash-1-dependence. Development 122:309–320PubMed

Clapp TR, Stone LM, Margolskee RF, Kinnamon SC (2001) Immunocytochemical evidence for co-expression of type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci 2:6CrossRefPubMedPubMedCentral

Delay RJ, Kinnamon JC, Roper SD (1986) Ultrastructure of mouse vallate taste buds: II. Cell types and cell lineage. J Comp Neurol 253:242–252

Farbman AI (1980) Renewal of taste bud cells in rat circumvallate papillae. Cell Tissue Kinet 13:349–357PubMed

Finger TE, Simon SA (2000) Cell biology of taste epithelium. In: Finger TE, Silver WL, Restrepo D (eds) The neurobiology of taste and smell. Wiley-Liss, New York, pp 287–314

Guillemot F, Joyner AL (1993) Dynamic expression of the murine achaete-scute homologue Mash-1 in the developing nervous system. Mech Dev 42:171–185

Guillemot F, Lo LC, Johnson JE, Auerbach A, Anderson DJ, Joyner AL (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463–476CrossRefPubMed

Johnson JE, Birren SJ, Anderson DJ (1990) Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346:858–861

Kim EJ, Ables JL, Dickel LK, Eisch AJ, Johnson JE (2011) Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS ONE 6(3):e18472

Kito-Shingaki A, Seta Y, Toyono T, Kataoka S, Kakinoki Y, Yanagawa Y, Toyoshima K (2014) Expression of GAD67 and Dlx5 in the taste buds of mice genetically lacking Mash1. Chem Senses 39:403–414CrossRefPubMed

Kusakabe Y, Miura H, Hashimoto R, Sugiyama C, Ninomiya Y, Hino A (2002) The neural differentiation gene Mash-1 has a distinct pattern of expression from the taste reception-related genes gustducin and T1R2 in the taste buds. Chem Senses 27:445–451CrossRefPubMed

Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ (1991) Mammalian achaete-scute homolog 1 is transiently expressed by specially-restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524–1537

Lo L, Tiveron MC, Anderson DJ (1998) Mash1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125:609–620

Matsumura H, Hasuwa H, Inoue N, Ikawa M, Okabe M (2004) Lineage-specific cell disruption in living mice by Cre-mediated expression of diphtheria toxin A chain. Biochem Biophys Res Commun 321:275–279

Miura H, Kusakabe Y, Kato H, Miura-Ohnuma J, Tagami M, Ninomiya Y, Hino A (2003) Co-expression pattern of Shh with Prox1 and that of Nkx2.2 with Mash1 in mouse taste bud. Gene Expr Patterns 3:427–430CrossRefPubMed

Miura H, Kato H, Kusakabe Y, Ninomiya Y, Hino A (2005) Temporal changes in NCAM immunoreactivity during taste cell differentiation and cell lineage relationships in taste buds. Chem Senses 30:367–375CrossRefPubMed

Murray RG (1986) The mammalian taste bud type III cell: a critical analysis. J Ultrastruct Mol Struct Res 95: 175-88

Nakayama A, Miura H, Shindo Y, Kusakabe Y, Tomonari H, Harada S (2008) Expression of the basal cell markers of taste buds in the anterior tongue and soft palate of the mouse embryo. J Comp Neurol 509:211–224CrossRefPubMed

Seta Y, Toyono T, Takeda S, Toyoshima K (1999) Expression of Mash1 in basal cells of rat circumvallate taste buds is dependent upon gustatory innervation. FEBS Lett 444:43–46CrossRefPubMed

Seta Y, Stoick-Cooper CL, Toyono T, Kataoka S, Toyoshima K, Barlow LA (2006) The bHLH transcription factors, Hes6 and Mash1, are expressed in distinct subsets of cells within adult mouse taste buds. Arch Histol Cytol 69:189–198CrossRefPubMed

Seta Y, Oda M, Kataoka S, Toyono T, Toyoshima K (2011) Mash1 is required for the differentiation of AADC-positive type III cells in mouse taste buds. Dev Dyn 240:775–784CrossRefPubMed

Sommer L, Ma Q, Anderson DJ (1996) Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci 8:221–241

Stone LM, TanS-S Tam PPL, Finger TE (2002) Analysis of cell lineage relationships in taste buds. J Neurosci 22:4522–4529CrossRefPubMed

Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, paravalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60–79CrossRefPubMed

Yee CL, Yang R, Bottger B, Finger TE, Kinnamon JC (2001) “Type III” cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol 440:97–108CrossRefPubMed

Yee CL, Jones KR, Finger TE (2003) Brain-derived neurotrophic factor is present in adult mouse taste cells with synapses. J Comp Neurol 459:15–24CrossRefPubMed

Title: Mash1-expressing cells could differentiate to type III cells in adult mouse taste buds
Authors: Hiroki Takagi
Yuji Seta
Shinji Kataoka
Mitsushiro Nakatomi
Takashi Toyono
Tatsuo Kawamoto
Publication date: 01-09-2018
Publisher: Springer Singapore
Published in: Anatomical Science International / Issue 4/2018
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI: https://doi.org/10.1007/s12565-018-0431-4

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Mash1-expressing cells could differentiate to type III cells in adult mouse taste buds

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Effects of streptozotocin-induced diabetes on leg muscle contractile properties and motor neuron morphology in rats

Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study

Clinical significance of understanding lateral and medial circumflex femoral artery origin variability

The middle rectal artery arising from the lateral sacral artery

Anatomical relation between the accessory process and pedicle in the lumbar vertebrae

Lumbosacral loadbearing, sagittal shift in the line of gravity and joint surface areas