Autonomic microganglion cells: a source of acetylcholine in the rat carotid body

2004 ◽  
Vol 96 (1) ◽  
pp. 384-391 ◽  
Author(s):  
Estelle B. Gauda ◽  
Reed Cooper ◽  
Shereé M. Johnson ◽  
Gabrielle L. McLemore ◽  
Cathleen Marshall
Keyword(s):  
Carotid Body ◽  
Nerve Fibers ◽  
Hypoxic Exposure ◽  
Type I ◽  
Mrna Levels ◽  
Excitatory Neurotransmitter ◽  
Postnatal Maturation ◽  
Cervical Ganglion ◽  
Cholinergic Nerve Terminals ◽  
Peripheral Arterial

Hypoxic chemosensitivity of peripheral arterial chemoreceptors and the ventilatory response to O2 deprivation increases with postnatal development. Multiple putative neurotransmitters, which are synthesized in the carotid body (CB), are thought to mediate signals generated by hypoxia. Acetylcholine (ACh) is believed to be a major excitatory neurotransmitter participating in hypoxic chemosensitivity. However, it is not known whether ACh originates from type I cells in the CB. In these studies, we tested the hypothesis that choline acetyltransferase (ChAT) and vesicular ACh transporter (VAChT) mRNAs are expressed in the CB and that mRNA levels would increase with postnatal maturation or exposure to hypoxia. Semiquantitative in situ hybridization histochemistry and immunohistochemistry were used to localize cholinergic markers within neurons and cells of the rat CB, the nodose-petrosal-jugular ganglion complex, and the superior cervical ganglion up to postnatal day 28. We show that the pattern of distribution, in tissue sections, is similar for both ACh markers; however, the level of VAChT mRNA is uniformly greater than that of ChAT. VAChT mRNA and immunoreactivity are detected abundantly in the nodose-petrosal-jugular ganglion complex in a number of microganglion cells embedded in nerve fibers innervating the CB for all postnatal groups, whereas ChAT mRNA is detected in only a few of these cells. Contrary to our hypothesis, postnatal maturation caused a reduction in ACh trait expression, whereas hypoxic exposure did not induce the upregulation of VAChT and ChAT mRNA levels in the CB, microganglion, or within the ganglion complex. The present findings indicate that the source of ACh in the CB is likely within autonomic microganglion cells and cholinergic nerve terminals.

scholarly journals Immunohistochemical Characteristics of the Human Carotid Body in the Antenatal and Postnatal Periods of Development

2021 ◽  
Vol 22 (15) ◽  
pp. 8222
Author(s):  
Dmitry Otlyga ◽  
Ekaterina Tsvetkova ◽  
Olga Junemann ◽  
Sergey Saveliev
Keyword(s):  
Tyrosine Hydroxylase ◽  
Carotid Body ◽  
Nerve Fibers ◽  
Individual Development ◽  
Endocrine Function ◽  
Type I ◽  
Type I Cells ◽  
Carotid Bodies ◽  
I Cells ◽  
Human Carotid

The evolutionary and ontogenetic development of the carotid body is still understudied. Research aimed at studying the comparative morphology of the organ at different periods in the individual development of various animal species should play a crucial role in understanding the physiology of the carotid body. However, despite more than two centuries of study, the human carotid body remains poorly understood. There are many knowledge gaps in particular related to the antenatal development of this structure. The aim of our work is to study the morphological and immunohistochemical characteristics of the human carotid body in the antenatal and postnatal periods of development. We investigated the human carotid bodies from 1 embryo, 20 fetuses and 13 adults of different ages using samples obtained at autopsy. Immunohistochemistry revealed expression of βIII-tubulin and tyrosine hydroxylase in the type I cells and nerve fibers at all periods of ontogenesis; synaptophysin and PGP9.5 in the type I cells in some of the antenatal cases and all of the postnatal cases; 200 kDa neurofilaments in nerve fibers in some of the antenatal cases and all of the postnatal cases; and GFAP and S100 in the type II cells and Schwann cells in some of the antenatal cases and all of the postnatal cases. A high level of tyrosine hydroxylase in the type I cells was a distinctive feature of the antenatal carotid bodies. On the contrary, in the type I cells of adults, the expression of tyrosine hydroxylase was significantly lower. Our data suggest that the human carotid body may perform an endocrine function in the antenatal period, while in the postnatal period of development, it loses this function and becomes a chemosensory organ.

scholarly journals ULTRASTRUCTURE OF THE CAROTID BODY

1966 ◽  
Vol 30 (3) ◽  
pp. 563-578 ◽  
Author(s):  
T. J. Biscoe ◽  
W. E. Stehbens
Keyword(s):  
Blood Vessels ◽  
Schwann Cells ◽  
Carotid Body ◽  
Nerve Fibers ◽  
Nerve Endings ◽  
Type I ◽  
Type Ii Cells ◽  
Type Ii ◽  
Type I Cells ◽  
I Cells

An electron microscope investigation was made of the carotid body in the cat and the rabbit. In thin-walled blood vessels the endothelium was fenestrated. Larger vessels were surrounded by a layer of smooth muscle fibers. Among the numerous blood vessels lay groups of cells of two types covered by basement membranes. Aggregates of Type I cells were invested by Type II cells, though occasionally cytoplasmic extensions were covered by basement membrane only. Type I cells contained many electron-opaque cored vesicles (350 to 1900 A in diameter) resembling those in endocrine secretory cells. Type II cells covered nerve endings terminating on Type I cells and enclosed nerve fibers in much the same manner as Schwann cells. The nerve endings contained numerous microvesicles (∼500 A in diameter), mitochondria, glycogen granules, and a few electron-opaque cored vesicles. Junctions between nerve endings and Type I cells were associated with regions of increased density in both intercellular spaces and the adjoining cytoplasm. Cilia of the 9 + 0 fibril pattern were observed in Type I and Type II cells and pericytes. Nonmyelinated nerve fibers, often containing microvesicles, mitochondria, and a few electron-opaque cored vesicles (650 to 1000 A in diameter) were present in Schwann cells, many of which were situated close to blood vessels Ganglion cells near the periphery of the gland, fibrocytes, and segments of unidentified cells were also seen. It was concluded that, according to present concepts of the structure of nerve endings, those endings related to Type I cells could be efferent or afferent.

Postnatal maturation of carotid body and type I cell chemoreception in the rat

1999 ◽  
Vol 276 (5) ◽  
pp. L875-L884 ◽  
Author(s):  
Owen S. Bamford ◽  
Laura M. Sterni ◽  
Michael J. Wasicko ◽  
Marshall H. Montrose ◽  
John L. Carroll
Keyword(s):  
Carotid Body ◽  
Carotid Sinus ◽  
Type I ◽  
Carotid Sinus Nerve ◽  
Postnatal Maturation ◽  
Cell Responses ◽  
Type I Cells ◽  
Intracellular Ca ◽  
I Cells

The site of postnatal maturation of carotid body chemoreception is unclear. To test the hypothesis that maturation occurs synchronously in type I cells and the whole carotid body, the development of changes in the intracellular Ca2+ concentration responses to hypoxia, CO2, and combined challenges was studied with fluorescence microscopy in type I cells and compared with the development of carotid sinus nerve (CSN) responses recorded in vitro from term fetal to 3-wk animals. Type I cell responses to all challenges increased between 1 and 8 days and then remained constant, with no multiplicative O2-CO2interaction at any age. The CSN response to hypoxia also matured by 8 days, but CSN responses to CO2 did not change significantly with age. Multiplicative O2-CO2interaction occurred in the CSN response at 2–3 wk but not in younger groups. We conclude that type I cell maturation underlies maturation of the CSN response to hypoxia. However, because development of responses to CO2 and combined hypoxia-CO2 challenges differed between type I cells and the CSN, responses to these stimuli must mature at other, unidentified sites within the developing carotid body.

Release of Dopamine from Carotid Sinus Nerve Fibers Innervating Type I Cells in the Cat Carotid Body

Neurosignals ◽  
1993 ◽  
Vol 2 (1) ◽  
pp. 16-26 ◽  
Author(s):  
L. Almaraz ◽  
Z.-Z. Wang ◽  
L.J. Stensaas ◽  
S.J. Fidone
Keyword(s):  
Carotid Body ◽  
Carotid Sinus ◽  
Nerve Fibers ◽  
Type I ◽  
Carotid Sinus Nerve ◽  
Type I Cells ◽  
I Cells

Sustained hypoxia-induced proliferation of carotid body type I cells in rats

2008 ◽  
Vol 104 (3) ◽  
pp. 803-808 ◽  
Author(s):  
Z.-Y. Wang ◽  
E. B. Olson ◽  
D. E. Bjorling ◽  
G. S. Mitchell ◽  
G. E. Bisgard
Keyword(s):  
Cell Proliferation ◽  
Carotid Body ◽  
Terminal Deoxynucleotidyl Transferase ◽  
Hypoxic Exposure ◽  
Type I ◽  
Body Type ◽  
Cellular Changes ◽  
And Function ◽  
I Cells ◽  
Sustained Hypoxia

Sustained hypoxia (SH) has been shown to cause profound morphological and cellular changes in carotid body (CB). However, results regarding whether SH causes CB type I cell proliferation are conflicting. By using bromodeoxyuridine, a uridine analog that is stably incorporated into cells undergoing DNA synthesis, we have found that SH causes the type I cell proliferation in the CB; the proliferation occurs mainly during the first 1–3 days of hypoxic exposure. Moreover, the new cells survive for at least 1 mo after the return to normoxia. Also, SH does not cause any cell death in CB as examined by the terminal deoxynucleotidyl transferase-mediated dUTP-X nick-end labeling assay. Taken together, our results suggest that SH stimulates CB type I cell proliferation, which may produce long-lasting changes in CB morphology and function.

Prenatal nicotine affects catecholamine gene expression in newborn rat carotid body and petrosal ganglion

2001 ◽  
Vol 91 (5) ◽  
pp. 2157-2165 ◽  
Author(s):  
Estelle B. Gauda ◽  
Reed Cooper ◽  
Patrice K. Akins ◽  
Guimei Wu
Keyword(s):  
Mrna Expression ◽  
Carotid Body ◽  
Ganglion Cells ◽  
Nicotine Exposure ◽  
Mrna Levels ◽  
Cardiorespiratory Control ◽  
Receptor Mrna ◽  
Prenatal Nicotine ◽  
Peripheral Arterial ◽  
Th Mrna

Nicotine exposure modifies the expression of catecholamine and opioid neurotransmitter systems involved in attenuation of hypoxic chemosensitivity. We used in situ hybridization histochemistry to determine the effect of prenatal and early postnatal nicotine exposure on tyrosine hydroxylase (TH), dopamine β-hydroxylase (DβH), preproenkephalin (PPE), and D2-dopamine receptor mRNA levels in the rat carotid body and petrosal ganglion during postnatal development. In the carotid body, nicotine increased TH mRNA expression in animals at 0 and 3 postnatal days (both, P < 0.05 vs. control) without affecting TH mRNA levels at 6 and 15 days. At 15 postnatal days, DβH mRNA levels were increased in the carotid body of nicotine-exposed animals. Dopamine D2-receptor mRNA levels in the carotid body increased with postnatal age but were unaffected by nicotine exposure. PPE was not expressed in the carotid body at any of the ages studied in control or treated animals. In the petrosal ganglion, nicotine increased the number of ganglion cells expressing TH mRNA in animals at 3 days ( P < 0.01 vs. control). DβH mRNA expression was not induced nor was PPE mRNA expression increased in the petrosal ganglion in treated animals. Prenatal nicotine exposure upregulates mRNAs involved in the synthesis of two inhibitory neuromodulators, dopamine and norepinephrine, in peripheral arterial chemoreceptors, which may contribute to abnormalities in cardiorespiratory control observed in nicotine exposed animals.

Chronic hypoxia upregulates connexin43 expression in rat carotid body and petrosal ganglion

2002 ◽  
Vol 92 (4) ◽  
pp. 1480-1486 ◽  
Author(s):  
J. Chen ◽  
L. He ◽  
B. Dinger ◽  
L. Stensaas ◽  
S. Fidone
Keyword(s):  
Gap Junction ◽  
Carotid Body ◽  
Chronic Hypoxia ◽  
Type I ◽  
Mrna Levels ◽  
Cx43 Expression ◽  
Type I Cells ◽  
Oxygen Sensitive ◽  
Ganglion Neurons ◽  
I Cells

Recent studies have demonstrated that oxygen-sensitive type I cells in the carotid body express the gap junction-forming protein connexin43 (Cx43). In the present study, we examined the hypothesis that chronic exposure to hypoxia increases Cx43 expression in type I cells as well as in chemoafferent neurons in the petrosal ganglion. Immunocytochemical studies in tissues from normal rats revealed diffuse and granular Cx43-like immunoreactivity in the cytoplasm of type I cells and dense punctate spots of immunoreactive product at the margins of type I cells and near the borders of chemosensory cell lobules. Cx43-like immunoreactivity was not detectable in petrosal ganglion neurons from normal animals. After a 2-wk exposure to hypobaric (380 Torr) hypoxia, Cx43 immunostaining was substantially enhanced in and around type I cells. Moreover, chronic hypoxia elicited the expression of Cx43-like immunoreactivity in the cytoplasm of afferent neurons throughout the petrosal ganglion. Quantitative RT-PCR studies indicate that chronic hypoxia evokes a substantial increase in Cx43 mRNA levels in the carotid body, along with a marked elevation of Cx43 expression in the petrosal ganglion. Increased Cx43 expression and gap junction formation in type I cells and sensory neurons may contribute to carotid body adaptation during sustained stimulation in extreme physiological conditions.

Effect of chronic hypoxia on purinergic synaptic transmission in rat carotid body

2006 ◽  
Vol 100 (1) ◽  
pp. 157-162 ◽  
Author(s):  
L. He ◽  
J. Chen ◽  
B. Dinger ◽  
L. Stensaas ◽  
S. Fidone
Keyword(s):  
Carotid Body ◽  
Chronic Hypoxia ◽  
Cholinergic Receptor ◽  
Nerve Fibers ◽  
Receptor Expression ◽  
Type I ◽  
Simultaneous Exposure ◽  
Type I Cells ◽  
I Cells

Recent studies indicate that chemoafferent nerve fiber excitation in the rat carotid body is mediated by acetylcholine and ATP, acting at nicotinic cholinergic receptors and P2X2 purinoceptors, respectively. We previously demonstrated that, after a 10- to 14-day exposure to chronic hypoxia (CH), the nicotinic cholinergic receptor blocker mecamylamine no longer inhibits rat carotid sinus nerve (CSN) activity evoked by an acute hypoxic challenge. The present experiments examined the effects of CH (9–16 days at 380 Torr) on the expression of P2X2 purinoceptors in carotid body and chemoafferent neurons, as well as the effectiveness of P2X2 receptor blocking drugs on CSN activity evoked by hypoxia. In the normal carotid body, immunocytochemical studies demonstrated a dense plexus of P2X2-positive nerve fibers penetrating lobules of type I cells. In addition, type I cells were lightly stained, indicating P2X2 receptor expression. After CH, the intensity of P2X2 receptor immunostaining was maintained in chemosensory type I cells and in the soma of chemoafferent neurons. P2 receptor expression on type I cells was confirmed by demonstrations of ATP-evoked increased intracellular Ca2+; this response was modulated by simultaneous exposure to hypoxia. In normal preparations, CSN activity evoked by hypoxia in vitro was 65% inhibited in the presence of specific P2X2 receptor antagonists. However, unlike the absence of mecamylamine action after CH, P2X2 antagonists remained effective against hypoxia-evoked activity after CH. Our findings indicate that ATP acting at P2X2 receptors contributes to adjusted chemoreceptor activity after CH, indicating a possible role for purinergic mechanisms in the adaptation of the carotid body in a chronic low-O2 environment.

scholarly journals Characterization of ectonucleotidase expression in the rat carotid body: regulation by chronic hypoxia

2017 ◽  
Vol 313 (3) ◽  
pp. C274-C284 ◽  
Author(s):  
Shaima Salman ◽  
Cathy Vollmer ◽  
Grant B. McClelland ◽  
Colin A. Nurse
Keyword(s):  
Carotid Body ◽  
Chronic Hypoxia ◽  
Purinergic Signaling ◽  
Sensory Nerve ◽  
Nerve Fibers ◽  
Type I ◽  
Type Ii Cells ◽  
Type Ii ◽  
Sensory Plasticity ◽  
Cervical Ganglia

The carotid body (CB) chemoreflex maintains blood Po2 and Pco2/H+ homeostasis and displays sensory plasticity during exposure to chronic hypoxia. Purinergic signaling via P1 and P2 receptors plays a pivotal role in shaping the afferent discharge at the sensory synapse containing catecholaminergic chemoreceptor (type I) cells, glial-like type II cells, and sensory (petrosal) nerve endings. However, little is known about the family of ectonucleotidases that control synaptic nucleotide levels. Using quantitative PCR (qPCR), we first compared expression levels of ectonucleoside triphosphate diphosphohydrolases (NTPDases1,2,3,5,6) and ecto-5′-nucleotidase (E5′Nt/CD73) mRNAs in juvenile rat CB vs. brain, petrosal ganglia, sympathetic (superior cervical) ganglia, and a sympathoadrenal chromaffin (MAH) cell line. In whole CB extracts, qPCR revealed a high relative expression of surface-located members NTPDase1,2 and E5′Nt/CD73, compared with low NTPDase3 expression. Immunofluorescence staining of CB sections or dissociated CB cultures localized NTPDase2,3 and E5′Nt/CD73 protein to the periphery of type I clusters, and in association with sensory nerve fibers and/or isolated type II cells. Interestingly, in CBs obtained from rats reared under chronic hypobaric hypoxia (~60 kPa, equivalent to 4,300 m) for 5–7 days, in addition to the expected upregulation of tyrosine hydroxylase and VEGF mRNAs, there was a significant upregulation of NTPDase3 and E5′Nt/CD73 mRNA, but a downregulation of NTPDase1 and NTPDase2 relative to normoxic controls. We conclude that NTPDase1,2,3 and E5′Nt/CD73 are the predominant surface-located ectonucleotidases in the rat CB and suggest that their differential regulation during chronic hypoxia may contribute to CB plasticity via control of synaptic ATP, ADP, and adenosine pools.

scholarly journals Vasoactive Intestinal Polypeptide in the Carotid Body—A History of Forty Years of Research. A Mini Review

2020 ◽  
Vol 21 (13) ◽  
pp. 4692 ◽  
Author(s):  
Slawomir Gonkowski
Keyword(s):  
Vasoactive Intestinal Polypeptide ◽  
Carotid Body ◽  
Nerve Fibers ◽  
Spontaneous Discharge ◽  
Type I ◽  
Amino Acid Residues ◽  
Internal Organs ◽  
Physiological Factors ◽  
History Of ◽  
Intestinal Polypeptide

Vasoactive intestinal polypeptide (VIP) consists of 28 amino acid residues and is widespreadin many internal organs and systems. Its presence has also been found in the nervous structuressupplying the carotid body not only in mammals but also in birds and amphibians. The numberand distribution of VIP in the carotid body clearly depends on the animal species studied;however, among all the species, this neuropeptide is present in nerve fibers around blood vesselsand between glomus cell clusters. It is also known that the number of nerves containing VIP locatedin the carotid body may change under various pathological and physiological factors. The knowledgeconcerning the functioning of VIP in the carotid body is relatively limited. It is known that VIP mayimpact the glomus type I cells, causing changes in their spontaneous discharge, but the main impactof VIP on the carotid body is probably connected with the vasodilatory eects of this peptide and itsinfluence on blood flow and oxygen delivery. This review is a concise summary of forty years ofresearch concerning the distribution of VIP in the carotid body.

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