Neurochemical plasticity of the carotid body in hypertension.
carotid body
hypertension
neurochemical plasticity
neurotrophic factors
spontaneously hypertensive rat
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
20
04
2022
received:
22
02
2022
accepted:
05
05
2022
medline:
11
8
2023
pubmed:
10
8
2023
entrez:
10
8
2023
Statut:
ppublish
Résumé
The carotid body (CB), a main peripheral arterial chemoreceptor, has lately been implicated in the pathophysiology of various cardiovascular disorders. Emerging experimental evidence supports a causal relationship between CB dysfunction and augmented sympathetic outflow which is the common hallmark of human sympathetic-related diseases, including essential hypertension. To gain insight into the neurotransmitter profile of chemosensory cells in the hypertensive CB, we examined the expression and cellular localization of some classical neurotransmitters, neuropeptides, and gaseous signaling molecules as well as neurotrophic factors and their receptors in the CB of spontaneously hypertensive rats, a common animal model of hypertension. Our immunohistochemical experiments revealed an elevated catecholamine and serotonin content in the hypertensive CB compared to normotensive controls. GABA immunostaining was seen in some peripherally located glomus cells in the CB of SHR and it was significantly lower than in control animals. The density of substance P and vasoactive intestinal peptide-immunoreactive fibers was diminished whereas that of neuropeptide Y-immunostained nerve fibers was increased and that of calcitonin gene-related peptide-containing fibers remained almost unchanged in the hypertensive CB. We have further demonstrated that in the hypertensive state the production of nitric oxide is impaired and that the components of the neurotrophin signaling system display an abnormal enhanced expression. Our results provide immunohistochemical evidence that the altered transmitter phenotype of CB chemoreceptor cells and the elevated production of neurotrophic factors modulate the chemosensory processing in hypertensive animals which contributes to autonomic dysfunction and elicits sympathetic hyperactivity, consequently leading to elevated blood pressure.
Substances chimiques
Nerve Growth Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2366-2377Informations de copyright
© 2022 American Association for Anatomy.
Références
Abdala, A. P., McBryde, F. D., Marina, N., Hendy, E. B., Engelman, Z. J., Fudim, M., Sobotka, P. A., Gourine, A. V., & Paton, J. F. (2012). Hypertension is critically dependent on the carotid body input in the spontaneously hypertensive rat. Journal of Physiology, 590, 4269-4277.
Atanasova, D. Y., Dandov, A. D., Dimitrov, N. D., & Lazarov, N. E. (2020). Histochemical and immunohistochemical localization of nitrergic structures in the carotid body of spontaneously hypertensive rats. Acta Histochemica, 122, 151500.
Atanasova, D. Y., Iliev, M. E., & Lazarov, N. E. (2011). Morphology of the rat carotid body. Biomedical Reviews, 22, 41-55.
Atanasova, D. Y., & Lazarov, N. E. (2014). Expression of neurotrophic factors and their receptors in the carotid body of spontaneously hypertensive rats. Respiratory Physiology & Neurobiology, 202, 6-15.
Brognara, F., Felippe, I. S. A., Salgado, H. C., & Paton, J. F. R. (2021). Autonomic innervation of the carotid body as a determinant of its sensitivity: Implications for cardiovascular physiology and pathology. Cardiovascular Research, 117, 1015-1032.
De Caro, R., Macchi, V., Sfriso, M. M., & Porzionato, A. (2013). Structural and neurochemical changes in the maturation of the carotid body. Respiratory Physiology & Neurobiology, 185, 9-19.
De Castro, F. (1926). Sur la structure et l'innervation de la glande intercarotidienne (glomus caroticum) de l'homme et des mammifères, et sur un noveau système d'innervation autonome du nerf glossopharyngien. Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid, 24, 365-432.
Dutschmann, M., & Paton, J. F. (2002). Inhibitory synaptic mechanisms regulating upper airway patency. Respiratory Physiology & Neurobiology, 131, 57-63.
Felippe, I. S. A., Zera, T., da Silva, M. P., Moraes, D. J. A., McBryde, F., & Paton, J. F. R. (2022). The sympathetic nervous system exacerbates carotid body sensitivity in hypertension. Cardiovascular Research. https://doi.org/10.1093/cvr/cvac008
Fisher, J. P., & Paton, J. F. R. (2012). The sympathetic nervous system and blood pressure in humans: Implications for hypertension. Journal of Human Hypertension, 26, 463-475.
González, C., Almaraz, L., Obeso, A., & Rigual, R. (1994). Carotid body chemoreceptors: From natural stimuli to sensory discharges. Physiological Reviews, 74, 829-898.
Ichikawa, H. (2002). Innervation of the carotid body: Immunohistochemical, denervation, and retrograde tracing studies. Microscopy Research and Technique, 59, 188-195.
Iturriaga, R. (2001). Nitric oxide and carotid body chemoreception. Biological Research, 34, 135-139.
Iturriaga, R., Alcayaga, J., Chapleau, M. W., & Somers, V. K. (2021). Carotid body chemoreceptors: Physiology, pathology, and implications for health and disease. Physiological Reviews, 101, 1177-1235.
Jacono, F. J., Peng, Y. J., Kumar, G. K., & Prabhakar, N. R. (2005). Modulation of the hypoxic sensory response of the carotid body by 5-hydroxytryptamine: Role of the 5-HT2 receptor. Respiratory Physiology & Neurobiology, 145, 135-142.
Kato, K., Wakai, J., Matsuda, H., Kusakabe, T., & Yamamoto, Y. (2012). Increased total volume and dopamine β-hydroxylase immunoreactivity of carotid body in spontaneously hypertensive rats. Autonomic Neuroscience, 169, 49-55.
Kondo, H. (1976). Innervation of the carotid body of the adult rat. A serial ultrathin section analysis. Cell and Tissue Research, 173, 1-15.
Kumar, P., & Prabhakar, N. R. (2012). Peripheral chemoreceptors: Function and plasticity of the carotid body. Comprehensive Physiology, 2, 141-219.
Kusakabe, T., Hayashida, Y., Matsuda, H., Gono, Y., Powell, F. L., Ellisman, M. H., Kawakami, T., & Takenaka, T. (1998). Hypoxic adaptation of the peptidergic innervation in the rat carotid body. Brain Research, 806, 165-174.
McBryde, F. D., Abdala, A. P., Hendy, E. B., Pijacka, W., Marvar, P., Moraes, D. J., Sobotka, P. A., & Paton, J. F. (2013). The carotid body as a putative therapeutic target for the treatment of neurogenic hypertension. Nature Communications, 4, 2395.
McDonald, D. M., & Mitchell, R. A. (1975). The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: A quantitative ultrastructural study. Journal of Neurocytology, 4, 177-230.
McQueen, D. S., & Ribeiro, J. A. (1981). Effect of β-endorphin, vasoactive intestinal polypeptide and cholecystokinin octapeptide on cat carotid chemoreceptor activity. Journal of Experimental Physiology, 66, 273-284.
Nurse, C. A. (2010). Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Experimental Physiology, 95, 657-667.
Ortega-Sáenz, P., & López-Barneo, J. (2020). Physiology of the carotid body: From molecules to disease. Annual Review of Physiology, 82, 127-149.
Paton, J. F. R., Sobotka, P. A., Fudim, M., Engelman, Z. J., Hart, E. C., McBryde, F. D., Abdala, A. P., Marina, N., Gourine, A. V., Lobo, M., Patel, N., Burchell, A., Ratcliffe, L., & Nightingale, A. (2013). The carotid body as a therapeutic target for the treatment of sympathetically mediated diseases. Hypertension, 61, 5-13.
Pijacka, W., Katayama, P. L., Salgado, H. C., Lincevicius, G. S., Campos, R. R., McBryde, F. D., & Paton, J. F. R. (2018). Variable role of carotid bodies in cardiovascular responses to exercise, hypoxia and hypercapnia in spontaneously hypertensive rats. Journal of Physiology, 596, 3201-3216.
Porzionato, A., Macchi, V., Parenti, A., & De Caro, R. (2008). Trophic factors in the carotid body. International Review of Cell and Molecular Biology, 269, 1-58.
Prabhakar, N. R. (1999). NO and CO as second messengers in oxygen sensing in the carotid body. Respiratory Physiology, 115, 161-168.
Prabhakar, N. R., & Jacono, F. J. (2005). Cellular and molecular mechanisms associated with carotid body adaptations to chronic hypoxia. High Altitude Medicine & Biology, 6, 112-120.
Prabhakar, N. R., & Peng, Y. J. (2004). Peripheral chemoreceptors in health and disease. Journal of Applied Physiology, 96, 359-366.
Prabhakar, N. R., Peng, Y. J., Kumar, G. K., & Nanduri, J. (2015). Peripheral chemoreception and arterial pressure responses to intermittent hypoxia. Comprehensive Physiology, 5, 561-577.
Przybylski, J., Janicki, P., & Trzebski, A. (1990). The increased catecholamine content in the carotid bodies of spontaneously hypertensive rats. In H. Acker, A. Trzebski, & R. G. O'Regan (Eds.), Chemoreceptors and chemoreceptor reflexes (pp. 363-376). Springer.
Scherer-Singler, U., Vincent, S. R., Kimura, H., & McGeer, E. G. (1983). Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. Journal of Neuroscience Methods, 9, 229-234.
Sinski, M., Lewandowski, J., Przybylski, J., Bidiuk, J., Abramczyk, P., Ciarka, A., & Gaciong, Z. (2012). Tonic activity of carotid body chemoreceptors contributes to the increases sympathetic drive in essential hypertension. Hypertension Research, 35, 487-491.
Stocco, E., Barbon, S., Tortorella, C., Macchi, V., De Caro, R., & Porzionato, A. (2020). Growth factors in the carotid body-An update. International Journal of Molecular Sciences, 21, E7267.
Takahashi, M., Matsuda, H., Hayashida, Y., Yamamoto, Y., Tsukuda, M., & Kusakabe, T. (2011). Morphological characteristics and peptidergic innervation in the carotid body of spontaneously hypertensive rats. Histology and Histopathology, 26, 369-375.
Verna, A. (1997). The mammalian carotid body: Morphological data. In C. Gonzalez (Ed.), The carotid body chemoreceptors (pp. 1-29). Landes Bioscience.
Wang, Z. Z., Stensaas, L. J., Bredt, D. S., Dinger, B., & Fidone, S. J. (1994). Localization and actions of nitric oxide in the cat carotid body. Neuroscience, 60, 275-286.
Wang, Z.-Y., & Bisgard, G. E. (2002). Chronic hypoxia-induced morphological and neurochemical changes in the carotid body. Microscopy Research and Technique, 59, 168-177.
Wang, Z. Z., Bredt, D. S., Fidone, S. J., & Stensaas, L. J. (1993). Neurons synthesizing nitric oxide innervate the mammalian carotid body. Journal of Comparative Neurology, 336, 419-432.
Watson, S. E., Supowit, S. C., Zhao, H., Katki, K. A., & DiPette, D. J. (2002). Role of sensory nervous system vasoactive peptides in hypertension. Brazilian Journal of Medical and Biological Research, 35, 1033-1045.
Zhang, M., Fearon, I. M., Zhong, H., & Nurse, C. A. (2003). Presynaptic modulation of rat arterial chemoreceptor function by 5-HT: Role of K+ channel inhibition via protein kinase C. Journal of Physiology, 551, 825-842.