Abstract
This study was designed to clarify development and the neural regulation of longitudinal smooth muscle in the chicken posterior mesenteric artery to generate new hypotheses for the roles of arterial longitudinal muscles. The existence of longitudinal muscles was examined with hematoxylin-eosin staining. A well-developed longitudinal muscle layer exists in the posterior mesenteric artery of adult female chickens but not adult male chickens. The muscle layer is poorly developed in chickens aged < 15 weeks, even in female chickens. Mechanical responses of muscles were recorded and perivascular nerves were stimulated by electrical field stimulation (EFS). EFS induced monophasic contractions in longitudinal muscle of the posterior mesenteric artery segment, and those responses were inhibited by pretreatment with tetrodotoxin. Blockers for cholinoceptors and adrenoceptors did not affect EFS-evoked contractions but an antagonist for P2X purinoceptors blocked them. The present study demonstrated that the longitudinal muscle in the posterior mesenteric artery of the domestic fowl develops between the 5th and 15th week of life, suggesting that its development is involved in oviposition. The longitudinal muscle might have a role in resisting extensional stress from the oviduct containing eggs. Moreover, the arterial longitudinal muscle is regulated by purinergic neurons via P2X purinoceptors.
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Abbreviations
- EFS:
-
Electrical field stimulation
- HE:
-
Hematoxylin and eosin
- NANC:
-
Non-adrenergic non-cholinergic
- NF279:
-
8,8′-[Carbonylbis(imino-4,1-phenylenecarbonylimino-4,1-phenylenecarbonylimino)]bis-1,3,5-naphthalenetrisulfonic acid hexasodium salt
- RT-PCR:
-
Reverse transcription-polymerase chain reaction
- SD:
-
Standard deviation
References
Agianniotis A, Rachev A, Stergiopulos N (2012) Active axial stress in mouse aorta. J Biomech 45:1924–1927
Alkayed F, Boudaka A, Shiina T, Takewaki T, Shimizu Y (2009) P2X purinoceptors mediate an endothelium-dependent hyperpolarization in longitudinal smooth muscle of anterior mesenteric artery in young chickens. Br J Pharmacol 158:888–895
Alkayed F, Shiina T, Takewaki T, Shimizu Y (2011) Postnatal development of excitatory innervations in longitudinal smooth muscle of the chicken anterior mesenteric artery. Life Sci 88:400–405
Ball RA, Sautter JH, Katter MS (1963) Morphological characteristics of the anterior mesenteric artery of fowl. Anat Rec 146:251–255
Bell C (1969) Indirect cholinergic vasomotor control of intestinal blood flow in the domestic chicken. J Physiol 205:317–327
Bennett T, Malmfors T (1975) Autonomic control of renal portal blood flow in the domestic fowl. Experientia 31:1177–1178
Bolton TB (1968) Studies on the longitudinal muscle of the anterior mesentric artery of the domestic fowl. J Physiol 196:273–281
Bolton TB (1969) Spontaneous and evoked release of neurotransmitter substances in the longitudinal muscle of the anterior mesenteric artery of the domestic fowl. Br J Pharmacol 35:112–120
Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483
Burnstock G, Warland JJ (1987a) P2-purinoceptors of two subtypes in the rabbit mesenteric artery: reactive blue 2 selectively inhibits responses mediated via the P2y-but not the P2x-purinoceptor. Br J Pharmacol 90:383–391
Burnstock G, Warland JJ (1987b) A pharmacological study of the rabbit saphenous artery in vitro: a vessel with a large purinergic contractile response to sympathetic nerve stimulation. Br J Pharmacol 90:111–120
Draid M, Shiina T, El-Mahmoudy A, Boudaka A, Shimizu Y, Takewaki T (2005) Neurally released ATP mediates endothelium-dependent hyperpolarization in the circular smooth muscle cells of chicken anterior mesenteric artery. Br J Pharmacol 146:983–989
Erlinge D (1998) Extracellular ATP: a growth factor for vascular smooth muscle cells. Gen Pharmacol 31:1–8
Frøbert O, Mikkelsen EO, Bagger JP (1999) The influence of transmural pressure and longitudinal stretch on K + - and Ca2+ -induced coronary artery constriction. Acta Physiol Scand 165:379–385
Furchgott RF (1955) The pharmacology of vascular smooth muscle. Pharmacol Rev 7:183–265
Gooden BA (1980) The effect of hypoxia on vasoconstrictor responses of isolated mesenteric arterial vasculature from chicken and duckling. Comp Biochem Physiol C 67C:219–222
Johnson A (2000) Reproduction in the female. In: Whittow G (ed) Avian physiology. Academic Press, San Diego, pp 569–596
Keatinge WR (1966) Electrical and mechanical response of arteries to stimulation of sympathetic nerves. J Physiol 185:701–715
Khalifa M, El-Mahmoudy A, Shiina T, Shimizu Y, Nikami H, El-Sayed M, Kobayashi H, Takewaki T (2005) An electrophysiological study of excitatory purinergic neuromuscular transmission in longitudinal smooth muscle of chicken anterior mesenteric artery. Br J Pharmacol 144:830–839
Lu X, Yang J, Zhao JB, Gregersen H, Kassab GS (2003) Shear modulus of porcine coronary artery: contributions of media and adventitia. Am J Physiol Heart Circ Physiol 285:H1966–H1975
Ralevic V, Burnstock G (1991) Roles of P2-purinoceptors in the cardiovascular system. Circulation 84:1–14
Rummery NM, Brock JA, Pakdeechote P, Ralevic V, Dunn WR (2007) ATP is the predominant sympathetic neurotransmitter in rat mesenteric arteries at high pressure. J Physiol 582:745–754
Smith F, West N, Jones D (2000) The cardiovascular system. In: Whittow G (ed) Avian physiology. Academic Press, San Diego, pp 141–231
Smyth L, Bobalova J, Ward SM, Keef KD, Mutafova-Yambolieva VN (2000) Cotransmission from sympathetic vasoconstrictor neurons: differences in guinea-pig mesenteric artery and vein. Auton Neurosci 86:18–29
Takamizawa K, Hayashi K, Matsuda T (1992) Isometric biaxial tension of smooth muscle in isolated cylindrical segments of rabbit arteries. Am J Physiol 263:H30–H34
Thapaliya S, Matsuyama H, Takewaki T (1999) ATP released from perivascular nerves hyperpolarizes smooth muscle cells by releasing an endothelium-derived factor in hamster mesenteric arteries. J Physiol 521(Pt 1):191–199
Wu X, Davis MJ (2001) Characterization of stretch-activated cation current in coronary smooth muscle cells. Am J Physiol Heart Circ Physiol 280:H1751–H1761
Acknowledgments
This work was supported in part by Grants-in-Aid for Scientific Research (KAKENHI) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan [Research Project Number: 15580256, 16580238, 24580423]. All experiments were conducted according to the Gifu University guidelines for proper animal experiments.
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T. Shiina and M. Koga contributed equally to this work.
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Shiina, T., Koga, M., Saito, S. et al. Development of longitudinal smooth muscle in the posterior mesenteric artery and purinergic regulation of its contractile responses in chickens. J Comp Physiol A 199, 857–865 (2013). https://doi.org/10.1007/s00359-013-0848-0
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DOI: https://doi.org/10.1007/s00359-013-0848-0