Mechanisms underlying spontaneous constrictions of postcapillary venules in the rat stomach

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• 作者：Retsu Mitsui ; Hikaru Hashitani
• 关键词：Microvasculature ; Contraction ; Smooth muscle ; Pericyte ; Rhythmicity
• 刊名：Pfl¨¹gers Archiv - European Journal of Physiology
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：468
• 期：2
• 页码：279-291
• 全文大小：2,826 KB
• 参考文献：1.Aickin CC, Brading AF (1990) The effect of loop diuretics on Cl− transport in smooth muscle of the guinea-pig vas deferens and taenia from the caecum. J Physiol 421:33–53PubMed PubMedCentral CrossRef
  2.Baluk P, Bolton P, Hirata A, Thurston G, McDonald DM (1998) Endothelial gaps and adherent leukocytes in allergen-induced early- and late-phase plasma leakage in rat airways. Am J Pathol 152:1463–1476PubMed PubMedCentral
  3.Bulley S, Jaggar JH (2014) Cl− channels in smooth muscle cells. Pflugers Arch 466:861–872PubMed PubMedCentral CrossRef
  4.Chen RY, Li DS, Guth PH (1992) Role of calcitonin gene-related peptide in capsaicin-induced gastric submucosal arteriolar dilation. Am J Physiol 262:H1350–H1355PubMed
  5.Davis AJ, Shi J, Pritchard HA, Chadha PS, Leblanc N, Vasilikostas G, Yao Z, Verkman AS, Albert AP, Greenwood IA (2013) Potent vasorelaxant activity of the TMEM16A inhibitor T16Ainh-A01. Br J Pharmacol 168:773–784PubMed PubMedCentral CrossRef
  6.Figini M, Emanueli C, Grady EF, Kirkwood K, Payan DG, Ansel J, Gerard C, Geppetti P, Bunnett N (1997) Substance P and bradykinin stimulate plasma extravasation in the mouse gastrointestinal tract and pancreas. Am J Physiol 272:G785–G793PubMed
  7.Fujiwara T, Uehara Y (1984) The cytoarchitecture of the wall and the innervation pattern of the microvessels in the rat mammary gland: a scanning electron microscopic observation. Am J Anat 170:39–54PubMed CrossRef
  8.Gannon B, Browning J, O’Brien P (1982) The microvascular architecture of the glandular mucosa of rat stomach. J Anat 135:667–683PubMed PubMedCentral
  9.Granger DN, Perry MA, Kvietys PR (1983) The microcirculation and fluid transport in digestive organs. Fed Proc 42:1667–1672PubMed
  10.Guth PH, Smith E (1975) Neural control of gastric mucosal blood flow in the rat. Gastroenterology 69:935–940PubMed
  11.Haddock RE, Hill CE (2002) Differential activation of ion channels by inositol 1,4,5-trisphosphate (IP3)- and ryanodine-sensitive calcium stores in rat basilar artery vasomotion. J Physiol 545:615–627PubMed PubMedCentral CrossRef
  12.Hashitani H, Takano H, Fujita K, Mitsui R, Suzuki H (2011) Functional properties of suburothelial microvessels in the rat bladder. J Urol 185:2382–2391PubMed CrossRef
  13.Hashitani H, Mitsui R, Masaki S, van Helden DF (2015) Pacemaker role of pericytes in generating synchronised spontaneous Ca2+ transients in the myenteric microvasculature of the guinea-pig gastric antrum. Cell Calcium 58:442–456PubMed CrossRef
  14.Hashitani H, Mitsui R, Shimizu Y, Higashi R, Nakamura K (2012) Functional and morphological properties of pericytes in suburothelial venules of the mouse bladder. Br J Pharmacol 167:1723–1736PubMed PubMedCentral CrossRef
  15.Hirose K, Iino M, Endo M (1993) Caffeine inhibits Ca2+-mediated potentiation of inositol 1,4,5-trisphosphate-induced Ca2+ release in permeabilized vascular smooth muscle cells. Biochem Biophys Res Commun 194:726–732PubMed CrossRef
  16.Hirst GD (1977) Neuromuscular transmission in arterioles of guinea-pig submucosa. J Physiol 273:263–275PubMed PubMedCentral CrossRef
  17.Holman ME, Kasby CB, Suthers MB, Wilson JA (1968) Some properties of the smooth muscle of rabbit portal vein. J Physiol 196:111–132PubMed PubMedCentral CrossRef
  18.Iino M (1989) Calcium-induced calcium release mechanism in guinea pig taenia caeci. J Gen Physiol 94:363–383PubMed CrossRef
  19.Jones TW (1852) Discovery that the veins of bat’s wing (which are furnished with valves) are endowed with rythmical contractility, and that the onward flow of blood is accelerated by each contraction. Philos Trans R Soc Lond 142:131–136CrossRef
  20.Joyce NC, DeCamilli P, Boyles J (1984) Pericytes, like vascular smooth muscle cells, are immunocytochemically positive for cyclic GMP-dependent protein kinase. Microvasc Res 28:206–219PubMed CrossRef
  21.Kito Y, Suzuki H (2003) Properties of pacemaker potentials recorded from myenteric interstitial cells of Cajal distributed in the mouse small intestine. J Physiol 15:803–818CrossRef
  22.Mazzone A, Eisenman ST, Strege PR, Yao Z, Ordog T, Gibbons SJ, Farrugia G (2012) Inhibition of cell proliferation by a selective inhibitor of the Ca2+-activated Cl− channel, Ano1. Biochem Biophys Res Commun 427:248–253PubMed PubMedCentral CrossRef
  23.Mitsui R (2009) Characterisation of calcitonin gene-related peptide-immunoreactive neurons in the myenteric plexus of rat colon. Cell Tissue Res 337:37–43PubMed CrossRef
  24.Mitsui R, Hashitani H (2013) Immunohistochemical characteristics of suburothelial microvasculature in the mouse bladder. Histochem Cell Biol 140:189–200PubMed CrossRef
  25.Mitsui R, Hashitani H (2015) Functional properties of submucosal venules in the rat stomach. Pflugers Arch 467:1327–1342PubMed CrossRef
  26.Mitsui R, Miyamoto S, Takano H, Hashitani H (2013) Properties of submucosal venules in the rat distal colon. Br J Pharmacol 170:968–977PubMed PubMedCentral CrossRef
  27.Neild TO (1989) Measurement of arteriole diameter changes by analysis of television images. Blood Vessels 26:48–52PubMed
  28.Neild TO, Shen KZ, Surprenant A (1990) Vasodilatation of arterioles by acetylcholine released from single neurones in the guinea-pig submucosal plexus. J Physiol 420:247–265PubMed PubMedCentral CrossRef
  29.Namkung W, Phuan PW, Verkman AS (2011) TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. J Biol Chem 286:2365–2374PubMed PubMedCentral CrossRef
  30.Peng H, Matchkov V, Ivarsen A, Aalkjær C, Nilsson H (2001) Hypothesis for the initiation of vasomotion. Circ Res 88:810–815PubMed CrossRef
  31.Peti-Peterdi J, Kovács G, Hamar P, Rosivall L (1998) Hemodynamics of gastric microcirculation in rats. Am J Physiol 275:H1404–H1410PubMed
  32.Pifferi S, Dibattista M, Menini A (2009) TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch 458:1023–1038PubMed CrossRef
  33.Piper AS, Large WA (2003) Multiple conductance states of single Ca2+-activated Cl− channels in rabbit pulmonary artery smooth muscle cells. J Physiol 547:181–196PubMed PubMedCentral CrossRef
  34.Piper AS, Large WA (2004) Single cGMP-activated Ca2+-dependent Cl− channels in rat mesenteric artery smooth muscle cells. J Physiol 555:397–408PubMed PubMedCentral CrossRef
  35.Rhodin JA (1968) Ultrastructure of mammalian venous capillaries, venules, and small collecting veins. J Ultrastruct Res 25:452–500PubMed CrossRef
  36.Shimizu Y, Mochizuki S, Mitsui R, Hashitani H (2014) Neurohumoral regulation of spontaneous constrictions in suburothelial venules of the rat urinary bladder. Vascul Pharmacol 60:84–94PubMed CrossRef
  37.Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, Neubauer G, Wang GX, Allescher HD, Korth M, Wilm M, Hofmann F, Ruth P (2000) Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Iβ. Nature 404:197–201PubMed CrossRef
  38.Surks HK (2007) cGMP-dependent protein kinase I and smooth muscle relaxation: a tale of two isoforms. Circ Res 101:1078–1080PubMed CrossRef
  39.van Helden DF (1993) Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol 471:465–479PubMed PubMedCentral CrossRef
  40.Vanner S (1994) Corelease of neuropeptides from capsaicin-sensitive afferents dilates submucosal arterioles in guinea pig ileum. Am J Physiol 267:G650–G655PubMed
  41.von der Weid PY, Rahman M, Imtiaz MS, van Helden DF (2008) Spontaneous transient depolarizations in lymphatic vessels of the guinea pig mesentery: pharmacology and implication for spontaneous contractility. Am J Physiol Heart Circ Physiol 295:H1989–H2000PubMed CrossRef
  42.Wouters M, De Laet A, Donck LV, Delpire E, van Bogaert PP, Timmermans JP, de Kerchove d’Exaerde A, Smans K, Vanderwinden JM (2006) Subtractive hybridization unravels a role for the ion cotransporter NKCC1 in the murine intestinal pacemaker. Am J Physiol Gastrointest Liver Physiol 290:G1219–G1227PubMed CrossRef
  43.Yamamoto Y, Klemm MF, Edwards FR, Suzuki H (2001) Intercellular electrical communication among smooth muscle and endothelial cells in guinea-pig mesenteric arterioles. J Physiol 535:181–195PubMed PubMedCentral CrossRef
  44.Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210–1215PubMed CrossRef
  
• 作者单位：Retsu Mitsui (1)
  Hikaru Hashitani (1)
  
  1. Department of Cell Physiology, Nagoya City University Graduate School of Medical Sciences, 1, Kawasumi, Mizuho-cho, Mizuho-Ku, Nagoya, 467-8601, Japan
  
• 刊物主题：Human Physiology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1432-2013

文摘

Postcapillary venules (PCVs) play a critical role in regulating capillary hydrostatic pressure, but their contractile mechanisms are not well understood. We examined the properties of spontaneous vasomotion and corresponding Ca2+ transients in gastric PCV. In the rat gastric submucosa, changes in PCV diameter and intracellular Ca2+ dynamics were visualised by video tracking system and fluorescent Ca2+ imaging, respectively, while PCV morphology was examined by immunohistochemistry. Stellate-shaped PCV mural cells expressing α-smooth muscle actin exhibited synchronised spontaneous Ca2+ transients to develop vasomotion which was abolished by nifedipine (1 μM), cyclopiazonic acid (10 μM), or Ca2+-activated Cl− channel inhibitors (100 μM niflumic acid, 1 μM T16Ainh-A01). A gap junction blocker (3 μM carbenoxolone) disrupted the synchrony of spontaneous Ca2+ transients amongst PCV mural cells and attenuated spontaneous vasomotion. Low chloride solution ([Cl−]₀ = 12.4 mM) also disrupted the synchrony of spontaneous Ca2+ transients and abolished vasomotion. Na+-K+-Cl− co-transporter inhibitors (10 μM bumetanide, 30 μM furosemide) suppressed spontaneous Ca2+ transients and vasoconstrictions. A phosphodiesterase type 5 (PDE5) inhibitor (1 μM tadalafil) disrupted the spontaneous Ca2+ transient synchrony and abolished vasomotion in a nitric oxide (NO)-dependent manner. Thus, gastric PCVs exhibit spontaneous vasomotion, resulting from synchronised spontaneous Ca2+ transients within a network of stellate-shaped PCV mural cells. An active Cl− accumulation partly via Na+-K+-Cl− co-transport appears to be fundamental in maintaining depolarisation upon the opening of Ca2+-activated Cl− channels that triggers Ca2+ influx via voltage-dependent L-type Ca2+ channels. Basal PDE5 activity may continuously counteract vaso-relaxing effects of endothelial NO to maintain spontaneous vasomotion.