Structural Plasticity of the Carotid Body.

Aging Cell hypertrophy Glomus cell volume Hyperplasia Neovascularization Neural crest-derived stem cells Structural plasticity Vasodilation

Journal

Advances in anatomy, embryology, and cell biology
ISSN: 0301-5556
Titre abrégé: Adv Anat Embryol Cell Biol
Pays: Germany
ID NLM: 0407712

Informations de publication

Date de publication:
2023
Historique:
medline: 13 11 2023
pubmed: 10 11 2023
entrez: 9 11 2023
Statut: ppublish

Résumé

The mammalian carotid body (CB) exhibits considerable plasticity of its structure during development and aging and as a consequence of environmental, metabolic and inflammatory stimuli. The structural changes during maturation include an enlargement of the total and vascular volume of the CB. Conversely, aging results in a reduction in the number and volume of glomus cells with progressive cellular degeneration and an apparent increase in the surrounding connective tissue. Age-related structural alterations are similar to those during chronic hypoxia. Long-term hypoxic exposure and sodium nitrate treatment enlarge several-fold the size of the rat CB causing glomus cell hypertrophy and hyperplasia, and evoke changes in its vascular structure, inducing marked vasodilation and neovascularization. In humans, such structural CB adaptation responses to prolonged hypoxia occur during acclimatization to high altitudes. On the other hand, the hyperoxic CB is significantly smaller than those of age-matched normoxic controls. Morphological alterations in the CB in both hypertensive animals and humans are characterized by a slightly enlarged parenchyma without apparent vascular expansion and/or dilation. The CB structural plasticity depends on the existence of a population of multipotent neural crest-derived stem cells, which are activated during hypoxia to proliferate and differentiate into new both neuronal (glomus) and vascular cell types.

Identifiants

pubmed: 37946076
doi: 10.1007/978-3-031-44757-0_4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

37-48

Informations de copyright

© 2023. The Author(s), under exclusive license to Springer Nature Switzerland AG.

Références

Angell-James JE, Clarke JA, Daly MD, Taton A (1985) Respiratory and cardiovascular responses to hyperoxia, hypoxia and hypercapnia in renal hypertensive rabbit; role of carotid body chemoreceptors. J Hypertens 3:213–223
pubmed: 4020128 doi: 10.1097/00004872-198506000-00004
Arias-Stella J, Valcarcel J (1973) The human carotid body at high altitudes. Pathol Microbiol (Basel) 39:292–297
pubmed: 4578025
Arias-Stella J, Valcarcel J (1976) Chief cell hyperplasia in the human carotid body at high altitudes; physiologic and pathologic significance. Hum Pathol 7:361–373
pubmed: 939535 doi: 10.1016/S0046-8177(76)80052-4
Atanasova DY, Lazarov NE (2014) Expression of neurotrophic factors and their receptors in the carotid body of spontaneously hypertensive rats. Respir Physiol Neurobiol 202:6–15
pubmed: 25034384 doi: 10.1016/j.resp.2014.06.016
Atanasova DY, Lazarov NE (2016) Morphological changes in the rat carotid body following acute sodium nitrite treatment. Respir Physiol Neurobiol 221:11–18
pubmed: 26528896 doi: 10.1016/j.resp.2015.10.015
Bavis RW, Fallon SC, Dmitrieff EF (2013) Chronic hyperoxia and the development of the carotid body. Respir Physiol Neurobiol 185:94–104
pubmed: 22640932 doi: 10.1016/j.resp.2012.05.019
Bee D, Barer G, Wach R, Pallot D, Emery C, Jones S (1989) Structure and function of the carotid body in New Zealand genetically hypertensive rats. Q J Exp Physiol 74:691–701
pubmed: 2531903 doi: 10.1113/expphysiol.1989.sp003321
Chen J, Dinger B, Stensaas L, Fidone S (2001) Involvement of vascular endothelial growth factor (VEGF) in carotid body vascular remodeling induced by chronic hypoxia. FASEB J 15:A153
De Caro R, Macchi V, Sfriso MM, Porzionato A (2013) Structural and neurochemical changes in the maturation of the carotid body. Resp Physiol Neurobiol 185:9–19
doi: 10.1016/j.resp.2012.06.012
Del Rio R, Munoz C, Arias P, Court FA, Moya EA, Iturriaga R (2011) Chronic intermittent hypoxia-induced vascular enlargement and VEGF upregulation in the rat carotid body is not prevented by antioxidant treatment. Am J Physiol Lung Cell Mol Physiol 301:L702–L711
pubmed: 21821731 doi: 10.1152/ajplung.00128.2011
Di Giulio C (2018) Ageing of the carotid body. J Physiol 596:3021–3027
pubmed: 29319194 pmcid: 6068111 doi: 10.1113/JP275300
Di Giulio C, Cacchio M, Bianchi G, Rapino C, Di Ilio C (2003) Selected contribution: carotid body as a model for aging studies: is there a link between oxygen and aging? J Appl Physiol 95:1755–1758
pubmed: 12871967 doi: 10.1152/japplphysiol.00406.2003
Di Giulio C, Antosiewicz J, Walski M, Petruccelli G, Verratti V, Bianchi G, Pokorski M (2009) Physiological carotid body denervation during aging. Adv Exp Med Biol 648:257–263
pubmed: 19536488 doi: 10.1007/978-90-481-2259-2_29
Di Giulio C, Zara S, Mazzatenta A, Verratti V, Porzionato A, Cataldi A, Pokorski M (2023) Aging and the carotid body: a scoping review. Respir Physiol Neurobiol 313:104063
pubmed: 37076025 doi: 10.1016/j.resp.2023.104063
Erickson JT, Mayer C, Jawa A, Ling L, Olson EB Jr, Vidruk EH, Mitchell GS, Katz DM (1998) Chemoafferent degeneration and carotid body hypoplasia following chronic hyperoxia in newborn rats. J Physiol 509:519–552
pubmed: 9575300 pmcid: 2230960 doi: 10.1111/j.1469-7793.1998.519bn.x
Eyzaguirre C, Abudara V (1996) Reflection on the carotid nerve sensory discharge and coupling between glomus cells. Adv Exp Med Biol 10:159–167
doi: 10.1007/978-1-4615-5891-0_23
Felippe ISA, Zera T, da Silva MP, Moraes DJA, McBryde F, Paton JFR (2023) The sympathetic nervous system exacerbates carotid body sensitivity in hypertension. Cardiovasc Res 119:316–331
pubmed: 35048948 doi: 10.1093/cvr/cvac008
Habeck JO (1986) Morphological findings at the carotid bodies of humans suffering from different types of systemic hypertension or severe lung diseases. Anat Anz 162:17–27
pubmed: 3752531
Habeck JO (1991) Peripheral arterial chemoreceptors and hypertension. J Auton Nerv Syst 34:1–7
pubmed: 1940013 doi: 10.1016/0165-1838(91)90003-L
Habeck JO, Honig A, Pfeiffer C, Schmidt M (1981) The carotid bodies in spontaneously hypertensive (SHR) and normotensive rats—a study concerning size, location and blood supply. Anat Anz 150:374–384
pubmed: 7344555
Heath D, Smith P (1985) The pathology of the carotid body and sinus. Edward Arnold, London
Hoffman H, Birrel JHW (1958) The carotid body in normal and anoxic states: an electron microscopic study. Acta Anat (Basel) 32:297–311
pubmed: 13532241 doi: 10.1159/000141332
Hollinshead WH (1945) Effects of anoxia upon carotid body morphology. Anat Rec 92:255–261
doi: 10.1002/ar.1090920306
Honig A, Habeck JO, Pfeiffer C, Schmidt M, Huckstorf C, Rotter H, Eckermann P (1981) The carotid bodies of spontaneously hypertensive rats (SHR): a functional and morphologic study. Acta Biol Med Ger 40:1021–1030
pubmed: 6800171
Hurst G, Heath D, Smith P (1985) Histological changes associated with ageing of the human carotid body. J Pathol 147:181–187
pubmed: 4067736 doi: 10.1002/path.1711470306
Kato K, Yamaguchi-Yamada M, Yamamoto Y (2010) Short-term hypoxia increases tyrosine hydroxylase immunoreactivity in rat carotid body. J Histochem Cytochem 58:839–846
pubmed: 20530461 pmcid: 2924799 doi: 10.1369/jhc.2010.956250
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. Auton Neurosci 169:49–55
pubmed: 22546625 doi: 10.1016/j.autneu.2012.03.005
Kumar P (2012) The carotid body in cardiovascular disease: more chicken and egg than horse and cart? J Physiol 590:4123
pubmed: 22962032 pmcid: 3473269 doi: 10.1113/jphysiol.2012.239921
Kumar P, Prabhakar NR (2012) Peripheral chemoreceptors: function and plasticity of the carotid body. Compr Physiol 2:141–219
pubmed: 23728973 pmcid: 3919066 doi: 10.1002/cphy.c100069
Kusakabe T, Powell FL, Ellisman MH (1993) Ultrastructure of the glomus cells in the carotid body of chronically hypoxic rats: with a special reference to the similarity of the amphibian glomus cells. Anat Rec 237:220–227
pubmed: 8238973 doi: 10.1002/ar.1092370209
Kusakabe T, Hirakawa H, Oikawa S, Matsuda H, Kawakami T, Takenaka T, Hayashida Y (2004) Morphological changes in the rat carotid body 1, 2, 4, and 8 weeks after the termination of chronically hypocapnic hypoxia. Histol Histopathol 19:1133–1140
pubmed: 15375756
Kusakabe T, Matsuda H, Hayashida Y (2005) Hypoxic adaptation of the rat carotid body. Histol Histopathol 20:987–997
pubmed: 15944949
Lahiri S, Rozanov C, Cherniack NS (2000) Altered structure and function of the carotid body at high altitude and associated chemoreflexes. High Altitude Med Biol 1:63–74
doi: 10.1089/152702900320694
Laidler P, Kay JM (1975) A quantitative morphological study of the carotid bodies of rats living at a stimulated altitude of 4300 metres. J Pathol 117:183–191
pubmed: 55477 doi: 10.1002/path.1711170308
Lazarov N, Atanasova D (2022) The human carotid body and its role in ventilatory acclimatization to hypoxia. Acta Morphol Anthropol 29:63–68
Lazarov N, Reindl S, Fischer F, Gratzl M (2009) Histaminergic and dopaminergic traits in the human carotid body. Respir Physiol Neurobiol 165:131–136
pubmed: 19022410 doi: 10.1016/j.resp.2008.10.016
McDonald DM, Lurue DT (1983) The ultrastructure and connections of blood vessels supplying the rat carotid body and carotid sinus. J Neurocytol 12:117–153
pubmed: 6842269 doi: 10.1007/BF01148090
McGregor KH, Gil J, Lahiri S (1984) A morphometric study of the carotid body in chronically hypoxic rats. J Appl Physiol 57:1430–1438
pubmed: 6520037 doi: 10.1152/jappl.1984.57.5.1430
Peng YJ, Overholt JL, Kline D, Kumar GK, Prabhakar NR (2003) Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc Natl Acad Sci USA 100:10073–10078
pubmed: 12907705 pmcid: 187770 doi: 10.1073/pnas.1734109100
Prabhakar NR, Peng YJ, Kumar GK, Nanduri J (2015) Peripheral chemoreception and arterial pressure responses to intermittent hypoxia. Compr Physiol 5:561–577
pubmed: 25880505 pmcid: 4423746 doi: 10.1002/cphy.c140039
Schamel A, Chaouti A, Douma M, Sabour B (2016) Morphological and neurochemical plasticity of the carotid body after long-term hypoxia: vascular and cellular involvement, morphometric study in Meriones shawi rats. Der Pharma Chem 8:82–98
Smith P, Jago R, Heath D (1984a) Anatomical variation and quantitative histology of the normal and enlarged carotid body. J Physiol 137:287–304
Smith P, Jago R, Heath D (1984b) Glomic cells and blood vessels in the hyperplastic carotid bodies of spontaneously hypertensive rats. Cardiovasc Res 18:471–482
pubmed: 6467264 doi: 10.1093/cvr/18.8.471
Wang Z-Y, Bisgard GE (2002) Chronic hypoxia-induced morphological and neurochemical changes in the carotid body. Microsc Res Tech 59:168–177
pubmed: 12384961 doi: 10.1002/jemt.10191
Wang Z-Y, Bisgard GE (2005) Postnatal growth of carotid body. Respir Physiol Neurobiol 149:181–190
pubmed: 15914098 doi: 10.1016/j.resp.2005.03.016

Auteurs

Nikolai E Lazarov (NE)

Department of Anatomy and Histology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria. nlazarov@medfac.mu-sofia.bg.

Dimitrinka Y Atanasova (DY)

Institute of Neurobiology, Bulgarian Academy of Sciences, Sofia, Bulgaria.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH