Chemical phenotypes of intrinsic cardiac neurons in the newborn pig (Sus scrofa domesticus Erxleben, 1777).
epicardiac ganglionated plexus
heart
immunohistochemistry
innervation morphology
subplexi
Journal
Journal of morphology
ISSN: 1097-4687
Titre abrégé: J Morphol
Pays: United States
ID NLM: 0406125
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
28
09
2021
received:
21
07
2021
accepted:
30
10
2021
pubmed:
3
11
2021
medline:
24
12
2021
entrez:
2
11
2021
Statut:
ppublish
Résumé
Intrinsic cardiac neurons (ICNs) are crucial cells in the neural regulation of heart rhythm, myocardial contractility, and coronary blood flow. ICNs exhibit diversity in their morphology and neurotransmitters that probably are age-dependent. Therefore, neuroanatomical heart studies have been currently focused on the identification of chemical phenotypes of ICNs to disclose their possible functions in heart neural regulation. Employing whole-mount immunohistochemistry, we examined ICNs from atria of the newborn pigs (Sus scrofa domesticus) as ICNs at this stage of development have never been neurochemically characterized so far. We found that the majority of the examined ICNs (>60%) were of cholinergic phenotype. Biphenotypic neuronal somata (NS), that is, simultaneously positive for two neuronal markers, were also rather common and distributed evenly within the sampled ganglia. Simultaneous positivity for cholinergic and adrenergic neuromarkers was specific in 16.4%, for cholinergic and nitrergic-in 3.5% of the examined NS. Purely either adrenergic or nitrergic ICNs were observed at 13% and 3.1%, correspondingly. Purely adrenergic and nitrergic NS were the most frequent in the ventral left atrial subplexus. Similarly to neuronal phenotype, sizes of NS also varied depending on the atrial region providing insights into their functional implications. Axons, but not NS, positive for classic sensory neuronal markers (vesicular glutamate transporter 2 and calcitonin gene-related peptide) were identified within epicardiac nerves and ganglia. Moreover, a substantial number of ICNs could not be attributed to any phenotype as they were not immunoreactive for antisera used in this study. Numerous dendrites with putative peptidergic and adrenergic contacts on cholinergic NS contributed to neuropil of ganglia. Our observations demonstrate that intrinsic cardiac ganglionated plexus is not fully developed in the newborn pig despite of dense network of neuronal processes and numerous signs of neural contacts within ganglia.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
51-65Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Akamatsu, W., Fujihara, H., Mitsuhashi, T., Yano, M., Shibata, S., Hayakawa, Y., Okano, H. J., Sakakibara, S., Takano, H., Takano, T., Takahashi, T., Noda, T., & Okano, H. (2005). The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proceedings of the National Academy of Sciences of the United States of America, 102, 4625-4630. https://doi.org/10.1073/pnas.0407523102
Aksu, T., Gopinathannair, R., Gupta, D., & Pauza, D. H. (2021). Intrinsic cardiac autonomic nervous system: What do clinical electrophysiologists need to know about the “heart brain”? Journal of Cardiovascular Electrophysiology, 32, 1737-1747. https://doi.org/10.1111/jce.15058
Arora, R. C., Waldmann, M., Hopkins, D. A., & Armour, J. A. (2003). Porcine intrinsic cardiac ganglia. The Anatomical Record, 271A, 249-258. https://doi.org/10.1002/ar.a.10030
Ashton, J. L., Burton, R. A. B., Bub, G., Smaill, B. H., & Montgomery, J. M. (2018). Synaptic plasticity in cardiac innervation and its potential role in atrial fibrillation. Frontiers in Physiology, 9, 240. https://doi.org/10.3389/fphys.2018.00240
Azevedo, E. R., & Parker, J. D. (1999). Parasympathetic control of cardiac sympathetic activity. Circulation, 100, 274-279. https://doi.org/10.1161/01
Batulevicius, D., Pauziene, N., & Pauza, D. H. (2003). Topographic morphology and age-related analysis of the neuronal number of the rat intracardiac nerve plexus. Annals of Anatomy = Anatomischer Anzeiger: Official Organ of the Anatomische Gesellschaft, 185, 449-459. https://doi.org/10.1016/S0940-9602(03)80105-X
Batulevicius, D., Pauziene, N., & Pauza, D. H. (2005). Architecture and age-related analysis of the neuronal number of the Guinea pig intrinsic cardiac nerve plexus. Annals of Anatomy-Anatomischer Anzeiger, 187, 225-243. https://doi.org/10.1016/j.aanat.2005.01.004
Batulevicius, D., Skripka, V., Pauziene, N., & Pauza, D. H. (2008). Topography of the porcine epicardiac nerve plexus as revealed by histochemistry for acetylcholinesterase. Autonomic Neuroscience, 138, 64-75. https://doi.org/10.1016/j.autneu.2007.10.005
Brack, K. E. (2015). The heart's “little brain” controlling cardiac function in the rabbit. Experimental Physiology, 100, 348-353. https://doi.org/10.1113/expphysiol.2014.080168
Brown, K. M., Gillette, T. A., & Ascoli, G. A. (2008). Quantifying neuronal size: Summing up trees and splitting the branch difference. Seminars in Cell and Developmental Biology, 19, 485-493. https://doi.org/10.1016/j.semcdb.2008.08.005
Chanson, P., Timsit, J., Masquet, C., Warnet, A., Guillausseau, P. J., Birman, P., Harris, A. G., & Lubetzki, J. (1990). Cardiovascular effects of the somatostatin analog octreotide in acromegaly. Annals of Internal Medicine, 113, 921-925. https://doi.org/10.7326/0003-4819-113-12-921
Choate, J. K., Murphy, S. M., Feldman, R., & Anderson, C. R. (2008). Sympathetic control of heart rate in nNOS knockout mice. American Journal of Physiology-Heart and Circulatory Physiology, 294, 354-361. https://doi.org/10.1152/ajpheart.00898.2007
Crick, S. J., Sheppard, M. N., Ho, S. Y., & Anderson, R. H. (1999). Localisation and quantitation of autonomic innervation in the porcine heart I: Conduction system. Journal of Anatomy, 195, 341-357.
Day, I. N. M., & Thompson, R. J. (2010). UCHL1 (PGP 9.5): Neuronal biomarker and ubiquitin system protein. Progress in Neurobiology, 90, 327-362. https://doi.org/10.1016/j.pneurobio.2009.10.020
Dickie, R., Bachoo, R. M., Rupnick, M. A., Dallabrida, S. M., DeLoid, G. M., Lai, J., Depinho, R. A., & Rogers, R. A. (2006). Three-dimensional visualization of microvessel architecture of whole-mount tissue by confocal microscopy. Microvascular Research, 72, 20-26. https://doi.org/10.1016/j.mvr.2006.05.003
Franke-Radowiecka, A., Zmijewska, N., Zubkiewicz, T., Zalecki, M., Klimczuk, M., Listowska, Ż., & Kaleczyc, J. (2020). Nerve structures of the heart and their immunohistochemical characterization in 10-week-old porcine foetuses. Comptes Rendus. Biologies, 343, 53-62. https://doi.org/10.5802/crbiol.4
Garg, S., Singh, P., Sharma, A., & Gupta, G. (2013). A gross comparative anatomical study of hearts in human cadavers and pigs. International Journal of Medical and Dental Sciences, 2, 170. https://doi.org/10.19056/ijmdsjssmes/2013/v2i2/86776
Gill, S. S., Pulido, O. M., Mueller, R. W., & McGuire, P. F. (1998). Molecular and immunochemical characterization of the ionotropic glutamate receptors in the rat heart. Brain Research Bulletin, 46, 429-434. https://doi.org/10.1016/S0361-9230(98)00012-4
Haberberger, R., & Kummer, W. (1996). β2-adrenoreceptor immunoreactivity in cardiac ganglia of the Guinea pig. The Histochemical Journal, 28, 827-833. https://doi.org/10.1007/BF02272155
Hanna, P., Dacey, M. J., Brennan, J., Moss, A., Robbins, S., Achanta, S., Biscola, N. P., Swid, M. A., Rajendran, P. S., Mori, S., Hadaya, J. E., Smith, E. H., Peirce, S. G., Chen, J., Hafton, L. A., Cheng, Z., Vadigepalli, V., Schwaber, J., Lux, R. L., … Shivkumar, K. (2021). Innervation and neuronal control of the mammalian sinoatrial node: A comprehensive atlas. Circulation Research, 128, 1279-1296. https://doi.org/10.1161/circresaha.120.318458
Hasan, W. (2013). Autonomic cardiac innervation: Development and adult plasticity. Organogenesis, 9, 176-193. https://doi.org/10.4161/org.24892
Hoover, D. B., Isaacs, E. R., Jacques, F., Hoard, J. L., Pagé, P., & Armour, J. A. (2009). Localization of multiple neurotransmitters in surgically derived specimens of human atrial ganglia. Neuroscience, 164, 1170-1179. https://doi.org/10.1016/j.neuroscience.2009.09.001
Horackova, M., Armour, J. A., & Byczko, Z. (1999). Distribution of intrinsic cardiac neurons in whole-Mount Guinea pig atria identified by multiple neurochemical coding. A confocal microscope study. Cell and Tissue Research, 297, 409-421.
Inokaitis, H., Pauziene, N., Rysevaite-Kyguoliene, K., & Pauza, D. H. (2016). Innervation of sinoatrial nodal cells in the rabbit. Annals of Anatomy, 205, 113-121. https://doi.org/10.1016/j.aanat.2016.03.007
Karnovsky, M. J., & Roots, L. (1964). A “direct-color” thiocholine method for cholinesterases. The Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society, 12, 219-221. https://doi.org/10.1177/12.3.219
Kruger, L., Mantyh, P. W., Sternini, C., Brecha, N. C., & Mantyh, C. R. (1988). Calcitonin gene-related peptide (CGRP) in the rat central nervous system: Patterns of immunoreactivity and receptor binding sites. Brain Research, 463, 223-244. https://doi.org/10.1016/0006-8993(88)90395-2
Levett, J. M., Murphy, D. A., Mcguirt, A. S., Ardell, J. L., & Armour, J. A. (1996). Cardiac augmentation can be maintained by continuous exposure of intrinsic cardiac neurons to a β-adrenergic agonist or angiotensin II. Journal of Surgical Research, 66, 167-173. https://doi.org/10.1006/jsre.1996.0390
Muscholl, E. (1980). Peripheral muscarinic control of norepinephrine release in the cardiovascular system. The American Journal of Physiology, 239, 713-720. https://doi.org/10.1152/ajpheart.1980.239.6.H713
Patil, J., Stucki, S., Nussberger, J., Schaffner, T., Gygax, S., Bohlender, J., & Imboden, H. (2011). Angiotensinergic and noradrenergic neurons in the rat and human heart. Regulatory Peptides, 167, 31-41. https://doi.org/10.1016/j.regpep.2010.11.011
Pauza, D. H., Skripka, V., Pauziene, N., & Stropus, R. (2000). Morphology, distribution, and variability of the epicardiac neural ganglionated subplexuses in the human heart. The Anatomical Record, 259, 353-382.
Pauza, D. H., Pauziene, N., Pakeltyte, G., & Stropus, R. (2002). Comparative quantitative study of the intrinsic cardiac ganglia and neurons in the rat, Guinea pig, dog and human as revealed by histochemical staining for acetylcholinesterase. Annals of Anatomy = Anatomischer Anzeiger: Official Organ of the Anatomische Gesellschaft, 184, 125-136. https://doi.org/10.1016/S0940-9602(02)80005-X
Pauziene, N., Rysevaite-Kyguoliene, K., Alaburda, P., Pauza, A. G., Skukauskaite, M., Masaityte, A., Laucaityte, G., Saburkina, I., Inokaitis, H., Plisiene, J., & Pauza, D. H. (2017). Neuroanatomy of the pig cardiac ventricles. A stereomicroscopic, confocal and electron microscope study. Anatomical Record, 300, 1756-1780. https://doi.org/10.1002/ar.23619
Richardson, R. J., Grkovic, I., & Anderson, C. R. (2003). Immunohistochemical analysis of intracardiac ganglia of the rat heart. Cell and Tissue Research, 314, 337-350. https://doi.org/10.1007/s00441-003-0805-2
Rysevaite, K., Saburkina, I., Pauziene, N., Vaitkevicius, R., Noujaim, S. F., Jalife, J., & Pauza, D. H. (2011). Immunohistochemical characterization of the intrinsic cardiac neural plexus in whole-mount mouse heart preparations. Heart Rhythm, 8, 731-738. https://doi.org/10.1016/j.hrthm.2011.01.013
Saburkina, I., Pauziene, N., & Pauza, D. H. (2009). Prenatal development of the human epicardiac ganglia. Anatomia, Histologia, Embryologia, 38, 194-199. https://doi.org/10.1111/j.1439-0264.2008.00919.x
Schwarz, P., Diem, R., Dun, N. J., & Förstermann, U. (1995). Endogenous and exogenous nitric oxide inhibits norepinephrine release from rat heart sympathetic nerves. Circulation Research, 77, 841-848. https://doi.org/10.1161/01.res.77.4.841
Singh, S., Johnson, P. I., Javed, A., Gray, T. S., Lonchyna, V. A., & Wurster, R. D. (1999). Monoamine- and histamine-synthesizing enzymes and neurotransmitters within neurons of adult human cardiac ganglia. Circulation, 99, 411-419. https://doi.org/10.1161/01.CIR.99.3.411
Smith, F. M. (1999). Extrinsic inputs to intrinsic neurons in the porcine heart in vitro. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 276(2), 455-467. https://doi.org/10.1152/ajpregu.1999.276.2.R455
Suzuki, Y., Yeung, A. C., & Ikeno, F. (2011). The representative porcine model for human cardiovascular disease. Journal of Biomedicine and Biotechnology, 2011, 1-10. https://doi.org/10.1155/2011/195483
Végh, A., Duim, S., Smits, A., Poelmann, R., ten Harkel, A., DeRuiter, M., Goumans, M. J., & Jongbloed, M. (2016). Part and parcel of the cardiac autonomic nerve system: Unravelling its cellular building blocks during development. Journal of Cardiovascular Development and Disease, 3, 28. https://doi.org/10.3390/jcdd3030028
Wang, L., Li, D., Plested, C. P., Dawson, T., Teschemacher, A. G., & Paterson, D. J. (2006). Noradrenergic neuron-specific overexpression of nNOS in cardiac sympathetic nerves decreases neurotransmission. Journal of Molecular and Cellular Cardiology, 41, 364-370. https://doi.org/10.1016/j.yjmcc.2006.05.007
Wang, L., Li, D., Dawson, T. A., & Paterson, D. J. (2009). Long-term effect of neuronal nitric oxide synthase over-expression on cardiac neurotransmission mediated by a lentiviral vector. The Journal of Physiology, 587, 3629-3637. https://doi.org/10.1113/jphysiol.2009.172866
Woods, J. R., Dandavino, A., Murayama, K., Brinkman, C. R., & Assali, N. S. (1977). Autonomic control of cardiovascular functions during neonatal development and in adult sheep. Circulation Research, 40, 401-407. https://doi.org/10.1161/01.RES.40.4.401
Yiallourou, S. R., Sands, S. A., Walker, A. M., & Horne, R. S. C. (2012). Maturation of heart rate and blood pressure variability during sleep in term-born infants. Sleep, 35, 177-186. https://doi.org/10.5665/sleep.1616