Skip to main content
SpringerLink
Log in

The Reciprocity of M- and N-Cholinergic Mechanisms in the Pulmonary Microcirculatory Changes in Case of Experimental Pulmonary Embolism

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

In acute experiments on isolated perfused rabbit’s lungs, the changes of pulmonary microhemodynamics were studied when modeling pulmonary embolism in the comparison group and under conditions of blockade or activation of M- and N-cholinergic receptors. In the case of pulmonary embolism with acetylcholine infusion combined with blockade of M1-cholinergic receptors with pirenzepine, the pulmonary artery pressure increased approximately to the same level as in the animals of comparison group. However, capillary hydrostatic pressure and capillary resistance did not change, indicating a decrease in sympathetic constrictor effects mainly on pulmonary venous vessels. The capillary filtration coefficient in group acetylcholine infusion combined with M1-cholinoreceptor blockade increased to a greater extent than in the comparison group, which was caused by an increase in the pulmonary vessels’ endothelial permeability. In response to embolization of the pulmonary artery under infusion of an N-mimetic cytisine in combination with blockade of alpha-adrenergic receptors with phentolamine and M-cholinergic receptors with atropine, the increase of pulmonary artery pressure and precapillary resistance was less pronounced than with acetylcholine infusion under blockade of M1-cholinergic receptors and in the comparison group. These data demonstrate a predominant dilatory effect of endothelial N-cholinergic receptor activation on pulmonary arterial vessels. Under these conditions, capillary hydrostatic pressure and postcapillary resistance increased approximately to the same as in the comparison group. However, the capillary filtration coefficient increased to a lesser extent than in the case of pulmonary embolism under conditions of acetylcholine infusion in combination with blockade of M1-cholinergic receptors, which indicates a decrease of endothelial permeability. The results of the experiments allow us to conclude that a reciprocal character of the interaction of M- and N-cholinergic mechanisms is revealed in the regulation of the permeability of pulmonary vessels: activation of endothelial M-cholinergic receptors in case of pulmonary thromboembolism promotes an increase of the capillary filtration coefficient, while activation of N-cholinergic receptors leads to its decrease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Aubry A, Paternot A, Vieillard-Baron A (2020) Cor pulmonale. Rev Mal Respir 37:257–266. https://doi.org/10.1016/j.rmr.2019.10.012

    Article  CAS  PubMed  Google Scholar 

  2. Kline JA, Puskarich MA, Jones AE, Mastouri RA, Hall CL, Perkins A, Gundert EE, Lahm T (2019) Inhaled nitric oxide to treat intermediate risk pulmonary embolism: A multicenter randomized comparisonled trial. Nitric Oxide 84:60–68. https://doi.org/10.1016/j.niox.2019.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Zhao S, Friedman O (2020) Management of Right Ventricular Failure in Pulmonary Embolism. Crit Care Clin 36:505–515. https://doi.org/10.1016/j.ccc.2020.02.006

    Article  PubMed  Google Scholar 

  4. Evlakhov VI, Berezina TP, Poyassov IZ, Ovsyannikov VI (2021) Pulmonary Microcirculation during Experimental Pulmonary Thromboembolism under Conditions of Activation and Blockade of Muscarinic Acetylcholine Receptors. Bull Exp Biol Med 171:198–201. https://doi.org/10.1007/s10517-021-05194-4

    Article  CAS  PubMed  Google Scholar 

  5. Zou Q, Leung SW, Vanhoutte PM (2012) Activation of nicotinic receptors can contribute to endothelium-dependent relaxations to acetylcholine in the rat aorta. J Pharmacol Exp Ther 341:756–763. https://doi.org/10.1124/jpet.112.192229

    Article  CAS  PubMed  Google Scholar 

  6. Fujii N, McGarr GW, Ghassa R, Schmidt MD, McCormick JJ, Nishiyasu T, Kenny GP (2020) Sex-differences in cholinergic, nicotinic, and β-adrenergic cutaneous vasodilation: Roles of nitric oxide synthase, cyclooxygenase, and K+ channels. Microvasc Res 131:104030. https://doi.org/10.1016/j.mvr.2020.104030

    Article  CAS  PubMed  Google Scholar 

  7. Cooke JP, Ghebremariam YT (2008) Endothelial nicotinic acetylcholine receptors and an-giogenesis. Trends Cardiovasc Med 18: 247–253. https://doi.org/10.1016/j.tcm.2008.11.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wessler I, Kirkpatrick CJ (2008) Acetylcholine beyond neurons: the non-neuronal cholin-ergic system in humans. Br J Pharmacol 154:1558–1571. https://doi.org/10.1038/bjp.2008.185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zoli M, Pucci S, Vilella A, Gotti C (2018) Neuronal and Extraneuronal Nicotinic Acetylcholine Receptors. Curr Neuropharmacol 16:338–349. https://doi.org/10.2174/1570159X15666170912110450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Evlakhov VI, Poyassov IZ, Shaidakov EV (2017) The role of venous vessels reactions in the pulmonary hemodynamics changes following experimental pulmonary embolism. Russ J Physiol 103:778–788. (In Russ).

  11. Mashkovsky MD (2012) The medical drugs, 16th ed. New Wave, M. (In Russ).

  12. Chen LY, Cheng CW, Liang JY (2015) Effect of esterification condensation on the Folin-Ciocalteu method for the quantitative measurement of total phenols. Food Chem 170:10–15. https://doi.org/10.1016/j.foodchem.2014.08.038

    Article  CAS  PubMed  Google Scholar 

  13. Saternos HC, Almarghalani DA, Gibson HM, Meqdad MA, Antypas RB, Lingired-dy A, AbouAlaiwi WA (2018) Distribution and function of the muscarinic receptor sub-types in the cardiovascular system. Physiol Genomics 50:1–9. https://doi.org/10.1152/physiolgenomics.00062.2017

    Article  CAS  PubMed  Google Scholar 

  14. Losev NA, Evlakhov VI, Shalkovskaya LN (2011) The reciprocal character of the muscarinic and nicotinic cholinergic mechanisms interaction in the systemic hemodynamics regulation. Med Acad J 11:236–248. (In Russ).

  15. Evlakhov VI, Poyassov IZ, Berezina TP (2020) The peculiarities of pulmonary macro- and microhemodynamics changes after treatment with agonists and blockers of cholinoreceptors. Med Acad J 20:35–44. (In Russ). https://doi.org/10.17816/MAJ55326

    Article  Google Scholar 

  16. Ding X, Murray PA (2005) Regulation of pulmonary venous tone in response to musca-rinic receptor activation. Am J Physiol Lung Cell Mol Physiol 288: L131–L140. https://doi.org/10.1152/ajplung.00230.2004.

    Article  CAS  PubMed  Google Scholar 

  17. Orii R, Sugawara Y, Sawamura S, Yamada Y (2010) M3-muscarinic receptors mediate acetylcholine-induced pulmonary vasodilation in pulmonary hypertension. BioScience Trends 4: 260–266. https://www.biosciencetrends.com

    CAS  PubMed  Google Scholar 

  18. Evlakhov VI, Poyassov IZ, Ovsyannikov VI (2019) Pulmonary Microcirculation in Ex-perimental Model of Pulmonary Thromboembolism under Conditions of α-Adrenoceptor Blockade. Bull Exp Biol Med 166: 313–316. https://doi.org/10.1007/s10517-019-04340-3

    Article  CAS  PubMed  Google Scholar 

  19. Noguchi M, Furukawa KT, Morimoto M (2020) Pulmonary neuroendocrine cells: physi-ology, tissue homeostasis and disease. Dis Model Mech 13:dmm046920. https://doi.org/10.1242/dmm.046920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kiyokawa H, Morimoto M (2020) Notch signaling in the mammalian respiratory system, specifically the trachea and lungs, in development, homeostasis, regeneration, and disease. Dev Growth Differ 62:67–79. https://doi.org/10.1111/dgd.12628

    Article  PubMed  Google Scholar 

  21. Schmeck J, Konrad C, Schöffel S, Wendel-Wellner M, Gluth H, Koch T, Krafft P (2000) Interaction of acetylcholine and endothelin-1 in the modulation of pulmonary arterial pressure. Crit Care Med 28:3869–3875. https://doi.org/10.1097/00003246-200012000-00022

    Article  CAS  PubMed  Google Scholar 

  22. Maniatis NA, Kotanidou A, Catravas JD, Orfanos SE (2008) Endothelial pathomecha-nisms in acute lung injury. Vascul Pharmacol 49: 119–133. https://doi.org/10.1016/j.vph.2008.06.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rimoldi SF, Yuzefpolskaya M, Allemann Y, Messerli F (2009) Flash pulmonary edema. Prog Cardiovasc Dis 52:249–259. https://doi.org/10.1016/j.pcad.2009.10.002

    Article  CAS  PubMed  Google Scholar 

  24. Moccia F, Frost C, Berra-Romani R,Tanzi F, Adams DJ (2004) Expression and function of neuronal nicotinic ACh receptors in rat microvascular endothelial cells. Am J Physiol Heart Circ Physiol 286:H486–H491. https://doi.org/10.1152/ajpheart.00620.2003

    Article  CAS  PubMed  Google Scholar 

  25. Hawkins BT, Egleton RD, Davis TP (2005) Modulation of cerebral microvascular permeability by endothelial nicotinic acetylcholine receptors. Am J Physiol Heart Circ Physiol 289:H212–H219. https://doi.org/10.1152/ajpheart.01210.2004

    Article  CAS  PubMed  Google Scholar 

  26. Kimura I, Dohgu S, Takata F, Matsumoto J, Kawahara Y, Nishihira M, Sakada S, Saisho T, Yamauchi A, Kataoka Y (2019) Activation of the α7 nicotinic acetylcholine receptor up-regulates blood-brain barrier function through increased claudin-5 and occludin expression in rat brain endothelial cells. Neurosci Lett 694:9–13. https://doi.org/ 10.1016/j.neulet.2018.11.022

  27. He Y, Ye ZQ, Li X, Zhu GS, Liu Y, Yao WF, Luo GJ (2016) Alpha7 nicotinic acetylcholine receptor activation attenuated intestine-derived acute lung injury. J Surg Res 201:258–265. https://doi.org/10.1016/j.jss.2015.10.046

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was performed within the 0557-2019-00012 state assignment of the Ministry of Science and Higher Education of the Russian Federation.

Author information

Authors and Affiliations

  1. Institute of Experimental Medicine, St. Petersburg, Russia

    V. I. Evlakhov, I. Z. Poyassov & T. P. Berezina

Authors
  1. V. I. Evlakhov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Z. Poyassov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. P. Berezina
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Idea of work and planning of experiments (Evlakhov V.I.), data collection (Evlakhov V.I., Poyasov I.Z., Berezina T.P.), statistical processing of data (Evlakhov V.I., Poyasov I.Z.), writing and editing the manuscript (Evlakhov V.I., Poyasov I.Z.).

Corresponding author

Correspondence to V. I. Evlakhov.

Ethics declarations

CONFLICT OF INTEREST

The authors declare that they have neither evident nor potential conflict of interest related to the publication of this article.

Additional information

Translated by A.V. Dyomina

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 2, pp. 249–261https://doi.org/10.31857/S0869813922020042.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Evlakhov, V.I., Poyassov, I.Z. & Berezina, T.P. The Reciprocity of M- and N-Cholinergic Mechanisms in the Pulmonary Microcirculatory Changes in Case of Experimental Pulmonary Embolism. J Evol Biochem Phys 58, 268–278 (2022). https://doi.org/10.1134/S0022093022010239

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093022010239

Keywords:

Search

Navigation