Specification of pharyngeal endoderm is dependent on early signals from axial mesoderm

Linda A. Barlow

doi:10.1242/dev.128.22.4573

Specification of pharyngeal endoderm is dependent on early signals from axial mesoderm

Development ◽

10.1242/dev.128.22.4573 ◽

2001 ◽

Vol 128 (22) ◽

pp. 4573-4583

Author(s):

Linda A. Barlow

Keyword(s):

Embryonic Development ◽

Taste Buds ◽

Taste Bud ◽

General View ◽

Bud Development ◽

Pharyngeal Endoderm ◽

Prechordal Mesoderm

The development of taste buds is an autonomous property of the pharyngeal endoderm, and this inherent capacity is acquired by the time gastrulation is complete. These results are surprising, given the general view that taste bud development is nerve dependent, and occurs at the end of embryogenesis. The pharyngeal endoderm sits at the dorsal lip of the blastopore at the onset of gastrulation, and because this taste bud-bearing endoderm is specified to make taste buds by the end of gastrulation, signals that this tissue encounters during gastrulation might be responsible for its specification. To test this idea, tissue contacts during gastrulation were manipulated systematically in axolotl embryos, and the subsequent ability of the pharyngeal endoderm to generate taste buds was assessed. Disruption of both putative planar and vertical signals from neurectoderm failed to prevent the differentiation of taste buds in endoderm. However, manipulations of contact between presumptive pharyngeal endoderm and axial mesoderm during gastrulation indicate that signals from axial mesoderm (the notochord and prechordal mesoderm) specify the pharyngeal endoderm, conferring upon the endoderm the ability to autonomously differentiate taste buds. These findings further emphasize that despite the late differentiation of taste buds, the tissue-intrinsic mechanisms that generate these chemoreceptive organs are set in motion very early in embryonic development.

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Embryonic taste buds develop in the absence of innervation

Development ◽

10.1242/dev.122.4.1103 ◽

1996 ◽

Vol 122 (4) ◽

pp. 1103-1111 ◽

Cited By ~ 2

Author(s):

L.A. Barlow ◽

C.B. Chien ◽

R.G. Northcutt

Keyword(s):

Embryonic Development ◽

Taste Receptor ◽

Nerve Fibers ◽

Taste Buds ◽

Taste Bud ◽

Taste Cells ◽

Experimental Approaches ◽

Well Differentiated ◽

Serotonin Immunoreactivity

It has been hypothesized that taste buds are induced by contact with developing cranial nerve fibers late in embryonic development, since descriptive studies indicate that during embryonic development taste cell differentiation occurs concomitantly with or slightly following the advent of innervation. However, experimental evidence delineating the role of innervation in taste bud development is sparse and equivocal. Using two complementary experimental approaches, we demonstrate that taste cells differentiate fully in the complete absence of innervation. When the presumptive oropharyngeal region was taken from a donor axolotl embryo, prior to its innervation and development of taste buds, and grafted ectopically on to the trunk of a host embryo, the graft developed well-differentiated taste buds. Although grafts were invaded by branches of local spinal nerves, these neurites were rarely found near ectopic taste cells. When the oropharyngeal region was raised in culture, numerous taste buds were generated in the complete absence of neural elements. Taste buds in grafts and in explants were identical to those found in situ both in terms of their morphology and their expression of calretinin and serotonin immunoreactivity. Our findings indicate that innervation is not necessary for complete differentiation of taste receptor cells. We propose that taste buds are either induced in response to signals from other tissues, such as the neural crest, or arise independently through intrinsic patterning of the local epithelium.

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How Do Taste Buds EAT?: Defining the Embryo‐to‐Adult Transition in Mouse Taste Bud Development and Regeneration

The FASEB Journal ◽

10.1096/fasebj.2019.33.1_supplement.81.1 ◽

2019 ◽

Vol 33 (S1) ◽

Author(s):

Linda A Barlow ◽

Erin J Golden ◽

Tim J Fellin

Keyword(s):

Taste Buds ◽

Taste Bud ◽

Bud Development ◽

Adult Transition ◽

Mouse Taste

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THE TONGUE AND TASTE IN FAMILIAL DYSAUTONOMIA

PEDIATRICS ◽

10.1542/peds.45.5.739 ◽

1970 ◽

Vol 45 (5) ◽

pp. 739-745

Author(s):

John Pearson ◽

Milton J. Finegold ◽

Gleb Budzilovich

Keyword(s):

Experimental Evidence ◽

Familial Dysautonomia ◽

Taste Buds ◽

Sensory Nerves ◽

Taste Bud ◽

Autonomic Ganglia ◽

Bud Development ◽

Neuron Populations ◽

Motor Nerves

The extreme paucity of subcutaneous sensory nerves in the small tongue of a 1-year-old child with familial dysautonomia was correlated with the absence of taste buds in the light of prior experimental evidence, indicating a trophic influence of nerves on taste bud development. Motor nerves in the tongue were normal. Reduced neuron populations were found in sensory and autonomic ganglia.

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Some Observations on Changes in Denervated Taste Buds of Circumvallate Papillae of Rabbits

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100063457 ◽

1969 ◽

Vol 27 ◽

pp. 308-309

Author(s):

Sunao Fujimoto ◽

Raymond G. Murray ◽

Assia Murray

Keyword(s):

Taste Buds ◽

Taste Bud ◽

Cell Type ◽

Dark Cells ◽

Type Iii ◽

Circumvallate Papillae ◽

Taste Bud Cells ◽

Light Cells

Taste bud cells in circumvallate papillae of rabbit have been classified into three groups: dark cells; light cells; and type III cells. Unilateral section of the 9th nerve distal to the petrosal ganglion was performed in 18 animals, and changes of each cell type in the denervated buds were observed from 6 hours to 10 days after the operation.Degeneration of nerves is evident at 12 hours (Fig. 1) and by 2 days, nerves are completely lacking in the buds. Invasion by leucocytes into the buds is remarkable from 6 to 12 hours but then decreases. Their extrusion through the pore is seen. Shrinkage and disturbance in arrangement of cells in the buds can be seen at 2 days. Degenerated buds consisting of a few irregular cells and remnants of degenerated cells are present at 4 days, but buds apparently normal except for the loss of nerve elements are still present at 6 days.

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Taste bud development in the channel catfish

The Journal of Comparative Neurology ◽

10.1002/cne.20425 ◽

2004 ◽

Vol 482 (1) ◽

pp. 1-16 ◽

Cited By ~ 29

Author(s):

R. Glenn Northcutt

Keyword(s):

Channel Catfish ◽

Taste Bud ◽

Bud Development

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Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively

Development ◽

10.1242/dev.124.7.1333 ◽

1997 ◽

Vol 124 (7) ◽

pp. 1333-1342 ◽

Cited By ~ 1

Author(s):

C.A. Nosrat ◽

J. Blomlof ◽

W.M. ElShamy ◽

P. Ernfors ◽

L. Olson

Keyword(s):

Taste Buds ◽

Mutant Mice ◽

Taste Bud ◽

Physiological Data ◽

Clinical Implications ◽

Wild Type ◽

Severe Reduction ◽

Sensory Modalities ◽

Per Se ◽

Taste Discrimination

A combination of anatomical, histological and physiological data from wild-type and null-mutated mice have established crucial roles for BDNF and NT3 in gustatory and somatosensory innervation of the tongue, and indeed for proper development of the papillary surface of the tongue. BDNF is expressed in taste buds, NT3 in many surrounding epithelial structures. Absence of BDNF in mice leads to severely malformed taste bud-bearing papillae and severe reduction of taste buds, a loss of proper innervation of remaining taste buds and a loss of taste discrimination although not of the suckling reflex per se. In contrast, absence of NT3 leads to a massive loss of somatosensory innervation of lingual structures. These findings demonstrate distinct roles for BDNF and NT3 in the establishment of the complex innervation apparatus of the tongue with non-overlapping roles for the lingual gustatory and somatosensory systems. The distinction between different sensory modalities, being dependent on either BDNF or NT3 may also have clinical implications.

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Quantitative Analysis of Taste Bud Cell Numbers in the Circumvallate and Foliate Taste Buds of Mice

Chemical Senses ◽

10.1093/chemse/bjaa017 ◽

2020 ◽

Vol 45 (4) ◽

pp. 261-273

Author(s):

Takahiro Ogata ◽

Yoshitaka Ohtubo

Keyword(s):

Soft Palate ◽

Cell Types ◽

Taste Buds ◽

Taste Bud ◽

Type Ii ◽

Fungiform Papilla ◽

Cross Sectional ◽

Cell Numbers ◽

Type Iii ◽

Receptor Cells

Abstract A mouse single taste bud contains 10–100 taste bud cells (TBCs) in which the elongated TBCs are classified into 3 cell types (types I–III) equipped with different taste receptors. Accordingly, differences in the cell numbers and ratios of respective cell types per taste bud may affect taste-nerve responsiveness. Here, we examined the numbers of each immunoreactive cell for the type II (sweet, bitter, or umami receptor cells) and type III (sour and/or salt receptor cells) markers per taste bud in the circumvallate and foliate papillae and compared these numerical features of TBCs per taste bud to those in fungiform papilla and soft palate, which we previously reported. In circumvallate and foliate taste buds, the numbers of TBCs and immunoreactive cells per taste bud increased as a linear function of the maximal cross-sectional taste bud area. Type II cells made up approximately 25% of TBCs irrespective of the regions from which the TBCs arose. In contrast, type III cells in circumvallate and foliate taste buds made up approximately 11% of TBCs, which represented almost 2 times higher than what was observed in the fungiform and soft palate taste buds. The densities (number of immunoreactive cells per taste bud divided by the maximal cross-sectional area of the taste bud) of types II and III cells per taste bud are significantly higher in the circumvallate papillae than in the other regions. The effects of these region-dependent differences on the taste response of the taste bud are discussed.

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Genetics and functions of the retinoic acid pathway, with special emphasis on the eye

Human Genomics ◽

10.1186/s40246-019-0248-9 ◽

2019 ◽

Vol 13 (1) ◽

Author(s):

Brian Thompson ◽

Nicholas Katsanis ◽

Nicholas Apostolopoulos ◽

David C. Thompson ◽

Daniel W. Nebert ◽

...

Keyword(s):

Retinoic Acid ◽

Embryonic Development ◽

Normal Development ◽

Anterior Segment ◽

Limb Bud ◽

Optic Vesicle ◽

Bud Development ◽

Optic Cup ◽

Multistep Process ◽

Acid Pathway

AbstractRetinoic acid (RA) is a potent morphogen required for embryonic development. RA is formed in a multistep process from vitamin A (retinol); RA acts in a paracrine fashion to shape the developing eye and is essential for normal optic vesicle and anterior segment formation. Perturbation in RA-signaling can result in severe ocular developmental diseases—including microphthalmia, anophthalmia, and coloboma. RA-signaling is also essential for embryonic development and life, as indicated by the significant consequences of mutations in genes involved in RA-signaling. The requirement of RA-signaling for normal development is further supported by the manifestation of severe pathologies in animal models of RA deficiency—such as ventral lens rotation, failure of optic cup formation, and embryonic and postnatal lethality. In this review, we summarize RA-signaling, recent advances in our understanding of this pathway in eye development, and the requirement of RA-signaling for embryonic development (e.g., organogenesis and limb bud development) and life.

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