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Comparative morphological and molecular studies on the oxygen-chemoreceptive cells in the carotid body and fish gills

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Abstract

Oxygen-chemoreceptive cells play critical roles for the respiration control. This review summarizes the chemoreceptive cells in the carotid body and fish gills from a morphological and molecular perspective. The cells synthesize and secrete biogenic amines, neuropeptides, and neuroproteins and also express many signaling molecules and transcription factors. In mammals, birds, reptiles, and amphibians, the carotid body primordium is consistently formed in the wall of the third arch artery which gives rise to the common carotid artery and the basal portion of the internal carotid artery. Consequently, the carotid body is located in the carotid bifurcation region, except birds in which the organ is situated at the lateral side of the common carotid artery. The carotid body receives branches of the cranial nerves IX and/or X dependent on the location of the organ. The glomus cell progenitors in mammals and birds are derived from the neighboring ganglion, i.e., the superior cervical sympathetic ganglion and the nodose ganglion, respectively, and immigrate into the carotid body primordium, constituting a solid cell cluster. In other animal species, the glomus cells are dispersed singly or forming small cell groups in intervascular stroma of the carotid body. In fishes, the neuroepithelial cells, corresponding to the glomus cells, are distributed in the gill filaments and lamellae. All oxygen-chemoreceptive cells sensitively respond to acute or chronic hypoxia, exhibiting degranulation, hypertrophy, hyperplasia, and upregulated expression of many genes.

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Fig. 1

Modified from Kameda et al. (2008). Bars 110 μm a, c, d, 140 μm b

Fig. 2

Modified from Kameda et al. (2003). b Schematic drawing of the topographical relationships of the carotid body (dark blue), endocrine glands, arteries, and nerves in the chicken cervicothoracic region. Ventral view of the left side. The 14th cervical sympathetic ganglion (5) lies close to the vertebral artery (VA) and issues branches to the artery (arrow). 1 thyroid gland, 2 cranial and caudal parathyroid glands, 3 ultimobranchial gland, 4 distal vagal (nodose) ganglion, CCA common carotid artery, BP brachial plex, R rib, RN recurrent laryngeal nerve, SCA subclavian artery, ST sympathetic trunk, TP transverse process of cervical vertebra, VN vagus nerve. *Common trunk of each artery supplying the endocrine organs. Modified from Kameda (1999). c, d Schematic drawings showing the location and arterial supply of the carotid body (dark blue) on the right c and left d sides. A ventral view. 1 ascending esophageal artery, 2 inferior thyroid artery, 3 carotid body artery, 4 esophagotracheobronchial artery, *Superior thyroid artery, **artery to the sternotracheal muscle, CCA common carotid artery, PT parathyroid glands, SCA subclavian artery, T thyroid gland, UB ultimobranchial gland. Modified from Kameda (1990a)

Fig. 3
Fig. 4

Modified from Kameda et al. (1994). b The carotid body (CB) and glomus cells (allows) distributed in the wall of the common carotid artery (CCA) and around the common trunk (CT) are intensely immunoreactive for TuJ1 in a chick embryo at E14. NG nodose ganglion. Modified from Kameda et al. (1994). c The carotid body from a chicken under normoxia shows many TH-immunoreactive glomus cells. d The carotid body from a chicken exposed to isocapnic hypoxia for 35 days. The volume is markedly increased, blood vessels (VB) are enlarged, and TH-immunoreactive cells are conspicuously decreased. Modified from Kameda et al. (1998). Bars 50 μm a, 80 μm b, 70 μm c, d

Fig. 5

Modified from Kameda et al. (1998). Bars 0.8 μm a, 1 μm b, and 0.7 μm c

Fig. 6

Modified from Kameda (2017)

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Abbreviations

5-HT:

Serotonin

AT1 receptor:

Angiotensin II type 1 receptor

bFGF:

Basic fibroblast growth factor

BDNF:

Brain-derived neurotrophic factor

CGRP:

Calcitonin gene–related peptide

Cbln1:

Cerebellin 1 precursor

CNTF:

Ciliary neurotrophic factor

Cox4i2:

Cytochrome c oxidase subunit IV isoform 2

CSN:

Carotid sinus nerve

DBH:

Dopamine β-hydroxylase

EGF:

Epidermal growth factor

EGFR:

EGF receptor

ET-1:

Endothelin-1

ETA-R:

Endothelin receptor type A

ETC:

Electron transport chain

Gcm2:

Glial cells missing 2

GDNF:

Glial cell line–derived neurotrophic factor

GFAP:

Glial fibrillary acidic protein

HIF:

Hypoxia-inducible factor

PHD2:

HIF prolyl hydroxylase 2

IGF-1:

Insulin-like growth factor-1

Ndufa4l2:

NADH dehydrogenase (ubiquinone)1 alpha subcomplex 4-like 2

NECs:

Neuroepithelial cells

Olfr:

Olfactory receptor gene

Pcx:

Pyruvate carboxylase

PDGFR-α:

Platelet-derived growth factor receptor-alpha

PGP 9.5.:

Protein gene product 9.5

NPY:

Neuropeptide Y

SCG:

Superior cervical ganglion of sympathetic trunk

SDHD:

Succinate dehydrogenase

SV2:

Synaptic vesicle protein 2

TGF-α:

Transforming growth factor-alpha

TH:

Tyrosine hydroxylase

TuJ1:

Neuron-specific class III β-tubulin isotype

trkB:

Tyrosine receptor kinase B

VEGF:

Vascular endothelial growth factor

VHL:

Von Hippel-Lindau

VIP:

Vasoactive intestinal polypeptide

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  1. Department of Anatomy, Kitasato University School of Medicine, Sagamihara, Kanagawa, 252-0374, Japan

    Yoko Kameda

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Correspondence to Yoko Kameda.

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All animal procedures were approved by the Animal Use and Care Committee of Kitasato University School of Medicine and conformed to NIH guidelines. This article does not contain any studies with human participants.

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Kameda, Y. Comparative morphological and molecular studies on the oxygen-chemoreceptive cells in the carotid body and fish gills. Cell Tissue Res 384, 255–273 (2021). https://doi.org/10.1007/s00441-021-03421-y

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