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Structural and functional characteristics of the special regulatory devices in the peripheral pulmonary circulation in rabbits

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Abstract

The present study intended to describe in detail the several blood vessels harboring special regulatory devices in rabbit’s pulmonary tissue using light and electron microscopy and immuno-histochemistry. Numerous throttle arteries were recorded within the adventitia of the segmental and sub-segmental bronchi and within pulmonary pleura. These arteries showed characteristic narrow or obliterated lumens and some of them bear longitudinal muscular intimal bolsters. For the first time, TEM revealed some structural modifications of the vascular endothelial cells of these arteries indicating that they become more activated to perform some additional functions. Arteriovenous anastomoses (AVAs) including direct shunt vessels and glomus organs were also recognized. Direct arteriovenous shunts appeared as small connecting devices communicating between small arteries and small veins while glomus organs consisted of the tortuous glomus vessels and the related afferent and efferent vessels. Several arteries and veins showing unique unusual structural characteristics were also described. For the first time, serotonin (5-HT) was strongly expressed in the vascular endothelium and muscle fibers of throttle arteries, in glomus cells of the glomus vessels, and in vascular endothelium of some veins and venules of special structure. The exact role of 5-HT is still unknown and further investigations are required to determine the types and distribution of 5-HT receptors present in these vascular devices. We concluded that these special vascular devices can play a critical role in controlling blood flow and pressure in the peripheral pulmonary circulation; however, the exact physiological mechanisms by which they work or are controlled remain unknown providing a ripe area for further investigation.

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Abbreviations

AVAs:

arteriovenous anastomoses

5 HT:

5-hydroxytryptamine or serotonin

SEM:

scanning electron microscopy

TEM:

transmission electron microscopy

References

  • Abushora MY, Bhatia N, Alnabki Z, Shenoy M, Alshaher M, Stoddard MF (2013) Intrapulmonary shunt is a potentially unrecognized cause of ischemic stroke and transient ischemic attack. J Am Soc Echocardiogr 26:683–690

    Article  PubMed  Google Scholar 

  • Alsip NL, Harris PD (1992) Serotonin-induced dilation of small arterioles is not mediated via endothelium-derived relaxing factor in skeletal muscle. Eur J Pharmacol 229:117–124

    Article  CAS  PubMed  Google Scholar 

  • Alsip NL, Schuschke DA, Miller FN (1996) Microvascular responses in the skeletal muscle of the diabetic rat. J Lab Clin Med 128:429–437

    Article  CAS  PubMed  Google Scholar 

  • Bancroft, J. D., and M. Gamble, 2002. Theory and practice of histological and histochemical techniques, 3rd edn

  • Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083–1152

    Article  CAS  PubMed  Google Scholar 

  • Berger M, Gray JA, Roth BL (2009) The expanded biology of serotonin. Annu Rev Med 60:355–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryan TL, van Diepen S, Bhutani M, Shanks M, Welsh RC, Stickland MK (2012) The effects of dobutamine and dopamine on intrapulmonary shunt and gas exchange in healthy humans. J Appl Physiol 113:541–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Centurio´n D, Sa´nchez-Lo´pez A, Ortiz MI, De Vries P, Saxena PR, and Villalo´n CM (2000) Mediation of 5-HT-induced internal carotid vasodilatation in GR127935-and ritanserin-pretreated dogs by 5-HT7 receptors. Naunyn Schmiedebergs Arch Pharmacol 362:169–176

  • Centurio’n D, Glusa E, Sa’nchez-Lo’pez A, Valdivia LF, Saxena PR, Villalo’n CM (2004) 5-HT7, but not 5-HT2B, receptors mediate hypotension in vagosympathectomized rats. Eur J Pharmacol 502:239–242

    Article  CAS  Google Scholar 

  • Cho A, Mitchell L, Koopmans D, Langille BL (1997) Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. Circ Res 81:328–337

    Article  CAS  PubMed  Google Scholar 

  • Dahme E (1957) €Uber die Beurteilung der Angiopathien bei chronischsklerosierenden Nierenerkrankungen des Hundes. Eine vergleichend morphologische Studie zum Problem der spontanen und experimentellen Arteriosklerose in der Tierheilkunde. Arch Exp Vet Med 11(611–636 u):752–812

    Google Scholar 

  • de Mello DE, Reid LM (1997) Arteries and veins. In: Crystal RG, West JB, Weibel ER, Barnes PJ (eds) The lung: scientific foundations. Lippincott-Raven, Philadelphia, pp 1117–1127

    Google Scholar 

  • Den Boer MO, Villaloa NCM, Saxena PR (1992) 5-HT1- like receptor mediated changes in porcine carotid haemody- namics: are 5-HT1D receptors involved? Naunyn Schmiedeberg's Arch Pharmacol 345:509–515

    Article  Google Scholar 

  • El-Etreby MF (1969) Morphological studies on the peripheral circulation of the genital organs in buffaloes with special reference to spontaneous arteriosclerosis in animals. Zentralbl Veterinarmed A 16:865–893

    Article  CAS  PubMed  Google Scholar 

  • Elliott JE, Nigam SM, Laurie SS, Beasley KM, Goodman RD, Hawn JA, Gladstone IM, Chesnutt MS, Lovering AT (2013) Prevalence of left heart contrast in healthy, young, asymptomatic humans at rest breathing room air. Respir Physiol Neurobiol 188:71–78

    Article  PubMed  Google Scholar 

  • Ellis ES, Byrne C, Murphy OE, Tilford NS, Baxter GS (1995) Mediation by 5-hydroxytryptamine2B receptors of endothelium-dependent relaxation in rat jugular vein. Br J Pharmacol 114:400–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fath El-Bab, M. R., 1970: A histological study on the respiratory system of camel. Thesis Ph D., Fac. Vet. Med. Egypt: Assuit University

  • Fath-Elbab, M. R. and Abou-Elhamd, A. S., (2016) Special cutaneous vascular elements in one-humped camel (Camelus dromedarius) Journal of Advanced Veterinary and Animal Research ISSN 2311-7710 (electronic)

  • Glusa E, Roos A (1996) Endothelial 5-HT receptors mediate relaxation of porcine pulmonary arteries in response to ergotamine and dihydroergotamine. Br J Pharmacol 119:330–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green AR (2006) Neuropharmacology of 5-hydroxytryptamine. Br J Pharmacol 147:S145–S152

    Article  PubMed  CAS  Google Scholar 

  • Haugen G, Mellembakken J, Stray-Pedersen S (1997) Characterization of the vasodilatatory response to serotonin in human umbilical arteries perfused in vitro. The influence of the endothelium. Early Hum Dev 47:185–193

    Article  CAS  PubMed  Google Scholar 

  • Heidenreich J (1960) Morphologische Studien am Blutkreislauf der Lunge des Pferdes. Zentralbl Veterinarmed A 8:794–825

    Google Scholar 

  • Hislop A, Reid L (1978) Normal structure and dimensions of the pulmonary arteries in the rat. J Anat:125, 71–183

  • Hoyer D, Hannon JP, Martin GR (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71:533–554

    Article  CAS  PubMed  Google Scholar 

  • Hussein MM, Hassan AHS (2018) Special Histological Features of the Angioarchitecture of the Ovaries in the Egyptian Buffaloes (Bubalus bubalis). J Adv Microsc Res 13:1–8

    Article  Google Scholar 

  • Jahnichen S, Glusa E, Pertz HH (2005) Evidence for 5-HT2B and 5-HT7 receptormediated relaxation in pulmonary arteries of weaned pigs. Naunyn Schmiedeberg's Arch Pharmacol 371:89–98

    Article  CAS  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27(137A)

  • Key BJ, Wigfield CC (1992) Changes in the tail surface temperature of the rat following injection of 5-hydroxytryptamine into the ventrolateral medulla. Neuropharmacology 31:717–723

    Article  CAS  PubMed  Google Scholar 

  • Kress H (1961) Strukturelle Besonderheiten und Altersver €anderungen an den nutritiven Blutgef€assen des Herzen bei Reh (Capreolus capreolus) und Rothirsch (Cervus elaphus). Arch Exp Vet Med 4:585–618

    Google Scholar 

  • Laurie SS, Elliott JE, Goodman RD, Lovering AT (2012) Catecholamineinduced opening of intrapulmonary arteriovenous anastomoses in healthy humans at rest. J Appl Physiol 113:1213–1222

    Article  CAS  PubMed  Google Scholar 

  • Andrew T. Lovering, R. Kirk Riemer, and Bernard The´ baud (2013) Intrapulmonary arteriovenous anastomoses physiological, pathophysiological, or both? Ann Am Thorac Soc Vol 10, 5, pp 504–508

  • Lovering AT, Stickland MK, Kelso AJ, Eldridge MW (2007a) Direct demonstration of 25- and 50-μm arteriovenous pathways in healthy human and baboon lungs. Am J Physiol Heart Circ Physiol 292:H1777–H1781

    Article  CAS  PubMed  Google Scholar 

  • Lovering AT, Stickland MK, Kelso AJ, Eldridge MW (2007b) Direct demonstration of 25- and 50-microm arteriovenous pathways in healthy human and baboon lungs. Am J Physiol Heart Circ Physiol 292:H1777–H1781

    Article  CAS  PubMed  Google Scholar 

  • Marini, K.J. , He, K., Hobbs, S.K. Kaproth-Joslin K. (2018) Pictorial review of the pulmonary vasculature: from arteries to veins Insights into Imaging 9:971–987

  • Masuda H, Kawamura K, Tohda K, Shozawa T, Sageshima M, Kamiya A (1989) Increase in endothelial cell density before artery enlargement in flow-loaded canine carotid artery. Arteriosclerosis 9:812–823

    Article  CAS  PubMed  Google Scholar 

  • Masuda H, Kawamura K, Nanjo H, Sho E , Komatsu M, Sugiyama T, Sugita, A Asari, Y Kobayashi, Ebina M (2003) Ultrastructure of endothelial cells under flow alteration microscopy research and technique 60:2–12

  • McMullan DM, Reddy VM, Gottliebson WM, Silverman NH, Perry SB, Chan F, Hanley FL, Riemer RK (2008) Morphological studies of pulmonary arteriovenous shunting in a lamb model of superiorcavopulmonary anastomosis. Pediatr Cardiol 29:706–712

    Article  PubMed  Google Scholar 

  • Mohammaden DM (2009) Angioarchitecture of the lungs of the camel (Camelus dromedarius). Assuit University, M.V.Sc. Egypt

    Google Scholar 

  • Mokthar, D.M. and Abd-Elhafez, E A. (2015) Morphological studies on the peripheral circulation of the ovary in one-humped camel (Camelus dromedarius). Anantomia Histologia Embryologia

  • Mankad PS, Chester AH, Yacoub MH (1991) 5-Hydroxytryptamine mediates endothelium dependent coronary vasodilatation in the isolated rat heart by the release of nitric oxide. Cardiovasc Res 25:244–248

  • Mylecharane EJ (1990) Mechanisms involved in serotonin-induced vasodilatation. Blood Vessels 27:116–126

    CAS  PubMed  Google Scholar 

  • Nichols CD (2009) Serotonin 5-HT2A receptor function as a contributing factor to both neuropsychiatric and cardiovascular diseases. Cardiovasc Psychiatry Neurol:2009, 475108

  • Ramage AG, Villalo’n CM (2008) 5-Hydroxytryptamine and cardiovascular regulation. Trends Pharmacol Sci 29:472–481

    Article  CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17:208–212

    Article  CAS  Google Scholar 

  • Saxena PR (1995) Cranial arteriovenous shunting, an in vivo animal model for migraine Experimental headache models. Lippincott-Raven Publishers, Philadelphia, pp 189–198

    Google Scholar 

  • Saxena APR, Verdouw PD (1982) Redistribution by 5-hydroxytryptamine of carotid arterial blood at the expense of arteriovenous anastomotic blood ¯ow. J Physiol 332:501–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena PR, Duncker DJ, Bom AH, Heiligers JPC, Verdouw PD (1986) Effects of MDL and methiothepin on carotid vascular responses to 5-hydroxytryptamine in the pig: evidence for the presence of ‘5-hydroxytryptamine1-like’ recep- tors. Naunyn Schmiedeberg's Arch Pharmacol 333:198–204

    Article  CAS  Google Scholar 

  • Schoeffter P, Ullmer C, Gutierrez M, Weitz-Schmidt G (1995) Lübbert HFunctional serotonin 5-HT1D receptors and 5-HT1D beta receptor mRNA expression in human umbilical vein endothelial cells. Naunyn Schmiedeberg's Arch Pharmacol 352(5):580–582

    CAS  Google Scholar 

  • Sho E, Sho M, Singh TM, Xu C, Zarins CK, Masuda H (2001) Blood flow decrease induces apoptosis of endothelial cells in previously dilated arteries resulting from chronic high blood flow. Arterioscler Thromb Vasc Biol 21:1139–1145

    Article  CAS  PubMed  Google Scholar 

  • Stephanie WW, Shaun FM, Robert PD, Barman SS (2012) Serotonin and Blood Pressure Regulation Pharmacol. Rev. 64:359–388

  • Stickland MK, Lovering AT, Eldridge MW (2007) Exercise-induced arteriovenous intrapulmonary shunting in dogs. Am J Respir Crit Care Med 176:300–305

    Article  PubMed  PubMed Central  Google Scholar 

  • Thurmon JC, Tranquilli WJ, Benson GJ (1996) Lumb & Jones Veterinary Anesthesia, third edn. Lea & Febiger, London

  • Tobin CE (1966) Arteriovenous shunts in the peropheral pulmonary circulation in the human lung. Thorax 21:197–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Townsley ML (2013) Structure and composition of pulmonary arteries, capillaries and veins. Compr Physiol 2:675–709

    Google Scholar 

  • Vanhoutte PM (1987) Serotonin and the vascular wall. Int J Cardiol 14(2):189–203

    Article  CAS  PubMed  Google Scholar 

  • Villalo’n CM, Centurio’n D (2007) Cardiovascular responses produced by 5 hydroxytriptamine: a pharmacological update on the receptors/mechanisms involved and therapeutic implications. Naunyn Schmiedeberg's Arch Pharmacol 376:45–63

    Article  CAS  Google Scholar 

  • Watts SW, Thompson JM (2004) Characterization of the contractile 5-hydroxytryptamine receptor in the renal artery of the normotensive rat. J Pharmacol Exp Ther 309:165–172

    Article  CAS  PubMed  Google Scholar 

  • Woodman OL, Dusting GJ (1994) Involvement of nitric oxide in coronary vascular responses to 5-hydroxytryptamine in the anaesthetized greyhound. Clin Exp Pharmacol Physiol 21:377–381

    Article  CAS  PubMed  Google Scholar 

  • Woods TD, Harmann L, Purath T, Ramamurthy S, Subramanian S, Jackson S, Tarima S (2010) Small- and moderate-size right-to-left shunts identified by saline contrast echocardiography are normal and unrelated to migraine headache. Chest 138:264–269

    Article  PubMed  Google Scholar 

  • Yuan G, Pan Y, Li H, Wang J (2016) Ultrastructure features of coronary artery endothelium in Bactrian camel (Camelus bactrianus). Int J Morphol 34(1):280–284

    Article  Google Scholar 

  • Zhuang Y-J, Singh CK, Zarins CK, Masuda H (1998) Sequential increase and decrease in blood flow stimulates progressive intimal thickening. Eur J Vasc Endovasc Surg 16:301–310

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I wish to express my appreciation to Prof. Doaa M Mokhtar, the professor of histology in Assiut University for her cooperation and advise.

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Authors and Affiliations

  1. Department of Anatomy and Histology, Faculty of Vet. Medicine, Assiut University, Asyut, 71526, Egypt

    Marwa M Hussein

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  1. Marwa M Hussein
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Marwa M. Hussein collected the samples, performed the electron microscopy study, analyzed the results, and prepared and reviewed the paper.

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Correspondence to Marwa M Hussein.

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The study was approved by the Ethics Committee of Assiut University, Egypt.

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Highlights

• This work is considered a detailed descriptive study of the structural components of the special regulatory devices in the peripheral pulmonary terminals in New Zealand white rabbits.

• The light and electron microscopic images identified different structural modifications in the vascular wall of some blood vessels to perform some additional functions.

• Vascular endothelium of some throttle arteries attained some unique characteristics and a strong expression of 5-HT suggesting an important role displayed by these cells in blood flow and pressure regulation.

• Variable types of intrapulmonary arteriovenous anastomoses were recognized in pulmonary tissue indicating that they have some vital physiological roles.

• For the first time, 5-HT is expressed strongly in vascular endothelium of some venous radicles and in glomus cells in AVAs.

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Hussein, M.M. Structural and functional characteristics of the special regulatory devices in the peripheral pulmonary circulation in rabbits. Protoplasma 257, 755–766 (2020). https://doi.org/10.1007/s00709-019-01459-y

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