Myoendothelial Contacts, Gap Junctions, and Microdomains: Anatomical Links to Function?

Microcirculation

Volumn 19, Issue 5, 2012, Pages 403-415

  Sandow, Shaun L ^a   Senadheera, Sevvandi ^a   Bertrand, Paul P ^a   Murphy, Timothy V ^a   Tare, Marianne ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Calcium channel; Electron microscopy; Endothelium; Endothelium derived hyperpolarization; Gap junction; Myoendothelial junctions; Potassium channel; Signaling microdomain; Smooth muscle; Vasodilation

Indexed keywords

ARTERIOLE; BASEMENT MEMBRANE; CELL COMMUNICATION; CELL COMPARTMENTALIZATION; CELL DENSITY; CELL ULTRASTRUCTURE; CHEEK POUCH; HYPERPOLARIZATION; INTERNAL ELASTIC LAMINA; MESENTERIC ARTERY; MITOCHONDRION; MYOENDOTHELIAL CLOSE CONTACT; MYOENDOTHELIAL GAP JUNCTION; MYOENDOTHELIAL MICRODOMAIN; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR ENDOTHELIUM;

ANIMALS; ARTERIES; ENDOTHELIUM, VASCULAR; GAP JUNCTIONS; HUMANS; MEMBRANE MICRODOMAINS; MUSCLE, SMOOTH, VASCULAR;

EID: 84863731508     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/j.1549-8719.2011.00146.x     Document Type: Review

References (100)

1. Aiello VD, Gutierrez PS, Chaves MJ, Lopes AA, Higuchi ML, Ramires JA. Morphology of the internal elastic lamina in arteries from pulmonary hypertensive patients: a confocal laser microscopy study. Mod Pathol 16: 411-416, 2003.
2. Beacham WS, Konishi A, Hunt CC. Observations on the microcirculatory bed in rat mesocecum using differential interference contrast microscopy in vivo and electron microscopy. Am J Anat 146: 385-426, 1976.
3. Benfenati V, Caprini M, Nicchia GP, Rossi A, Dovizio M, Cervetto C, Nobile M, Ferroni S. Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia. Channels 3: 323-336, 2009.
4. Bennett MVL, Barrio LC, Bargiello TA, Spray DC, Hertzberg E, Saez JC. Gap junctions: new tools, new answers, new questions. Neuron 6: 305-320, 1991.
5. Berridge MJ. Calcium microdomains: organization and function. Cell Calcium 40: 405-412, 2006.
6. Billaud M, Lohman AW, Straub AC, Looft-Wilson R, Johnstone SR, Araj CA, Best AK, Chekeni FB, Ravichandran KS, Penuela S, Laird DW, Isakson BE. Pannexin1 regulates a1-adrenergic receptor-mediated vasoconstriction. Circ Res 109: 80-85, 2011.
7. 2+-release. Arch Pharmacol Res 28: 709-715, 2005.
8. Chadha PS, Haddock RE, Howitt L, Morris MJ, Murphy TV, Grayson TH, Sandow SL. Obesity upregulates IKCa and myoendothelial gap junctions to maintain endothelial vasodilator function. J Pharmacol Exp Ther 335: 284-293, 2010.
9. Ca and NO. J Pharmacol Exp Ther 336: 701-708, 2011.
10. Chaput N, Thery C. Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 33: 419-440, 2011.
11. + channels confer distinctive patterns of distribution in human tissues and differential cellular localisation in the colon and corpus cavernosum. Naunyn Schmiedebergs Arch Pharmacol 369: 602-615, 2004.
12. Choate JK, Klemm M, Hirst GDS. Sympathetic and parasympathetic neuromuscular junctions in the guinea-pig sino-atrial node. J Auton Nerv Syst 44: 1-16, 1993.
13. + currents underlying the action of endothelium-derived hyperpolarizing factor in guinea-pig, rat and human blood vessels. J Physiol 531: 359-373, 2001.
14. Conejo VA, De Haro R, Sosa-Melgarejo J, Mendez JD. New insights in endothelial and smooth muscle cell communication. Biomed Pharmacother 61: 173-179, 2007.
15. + channels in the rat isolated mesenteric artery. J Vasc Res 40: 159-168, 2003.
16. D'Hondt C, Ponsaerts R, De Smedt H, Vinken M, De Vuyst E, De Bock M, Wang N, Rogiers V, Leybaert L, Himpens B, Bultynck G. Pannexin channels in ATP release and beyond: an unexpected rendezvous at the endoplasmic reticulum. Cell Signal 23: 305-316, 2011.
17. Dahl E. The fine structure of intracerebral arteries. Zeit fur Zellforsch 145: 577-586, 1973.
18. Dahl E. The innervation of the cerebral arteries. J Anat 115: 53-63, 1973.
19. Davies P, Burke G, Reid L. The structure of the wall of the rat intracinar pulmonary artery: an electron microscopic study of microdissected preparations. Microvasc Res 32: 50-63, 1986.
20. de Wit C, Boettcher M, Schmidt VJ. Signaling across myoendothelial gap junctions-fact or fiction? Cell Comm Adhes 15: 231-245, 2008.
21. de Wit C, Griffith TM. Connexins and gap junctions in the EDHF phenomenon and conducted vasomotor responses. Pflugers Arch 459: 897-914, 2010.
22. Ca3.1 channels during endothelium-derived hyperpolarizing factor signaling in mesenteric resistance arteries. Circ Res 102: 1247-1255, 2008.
23. Dora KA, Sandow SL, Gallagher NT, Takano H, Rummery NM, Hill CE, Garland CJ. Myoendothelial gap junctions may provide the pathway for EDHF in mouse mesenteric artery. J Vasc Res 40: 480-490, 2003.
24. Ellis A, Goto K, Chaston DJ, Brackenbury TD, Meaney KR, Falck JR, Wojcikiewicz RJ, Hill CE. Enalapril treatment alters the contribution of epoxyeicosatrienoic acids but not gap junctions to endothelium-derived hyperpolarizing factor activity in mesenteric arteries of spontaneously hypertensive rats. J Pharmacol Exp Ther 330: 413-422, 2009.
25. Emerson GG, Segal SS. Electrical coupling between endothelial cells and smooth muscle cells in hamster feed arteries. Role in vasomotor control. Circ Res 87: 474-479, 2000.
26. Fawcett DW, Reynolds SRM, Zweifach RW. The fine structure of capillaries, arterioles and small arteries. In: The Microcirculation Urbana edited by Zweifach SRM, Reynolds BW, Chicago: University of Illinois Press, 1959, p. 1-27.
27. Feletou M. The Endothelium: Part 2: EDHF-Mediated Responses "The Classical Pathway" San Rafael, CA: Morgan & claypool Life Sciences, 2011.
28. Francis NJ, Landis SC. Cellular and molecular determinants of sympathetic neuron development. Ann Rev Neurosci 22: 541-566, 1999.
29. 2+ in relation to generation of acetylcholine-induced endothelium-dependent hyperpolarization in rat mesenteric artery. Br J Pharmacol 120: 1328-1334, 1997.
30. 2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 107: 3811-3816, 2010.
31. Griffith TM. Endothelium-dependent smooth muscle hyperpolarization: do gap junctions provide a unifying hypothesis? Brit J Pharmacol 141: 881-903, 2004.
32. Griffith TM, Chaytor AT, Taylor HJ, Giddings BD, Edwards DH. cAMP facilitates EDHF-type relaxations in conduit arteries by enhancing electrotonic conduction via gap junctions. Proc Natl Acad Sci USA 99: 6392-6397, 2002.
33. Gustafsson F, Mikkelsen HB, Arensbak B, Thuneberg L, Neve S, Jensen LJ, Holstein-Rathlou NH. Expression of connexin 37, 40 and 43 in rat mesenteric arterioles and resistance arteries. Histochem Cell Biol 119: 139-148, 2003.
34. Haddock RE, Grayson TH, Brackenbury TD, Meaney KR, Neylon CB, Sandow SL, Hill CE. Endothelial coordination of cerebral vasomotion via myoendothelial gap junctions containing connexins37 and 40. Am J Physiol 291: H2047-H2056, 2006.
35. Haddock RE, Grayson TH, Morris MJ, Howitt L, Chadha PS, Sandow SL. Diet-induced obesity impairs endothelium-derived hyperpolarization via altered potassium channel signaling mechanisms. PloS One 6: e16423, 2011.
36. Haefliger JA, Demotz S, Braissant O, Suter E, Waeber B, Nicod P, Meda P. Connexins 40 and 43 are differentially regulated within the kidneys of rats with renovascular hypertension. Kidney Int 60: 190-201, 2001.
37. Hammersen F, Hammersen E. Some structural apsects of precapillary vessels. J Cardiovasc Pharmacol 6: S289-S303, 1984.
38. Hassler O. The windows of the internal elastic lamella of the cerebral arteries. Virchows Archiv fur Pathol Anat Physiol Klin Medizin 335: 127-132, 1962.
39. Heberlein KR, Straub AC, Best AK, Greyson MA, Looft-Wilson RC, Sharma PR, Meher A, Leitinger N, Isakson BE. Plasminogen activator inhibitor-1 regulates myoendothelial junction formation. Circ Res 106: 1092-1102, 2010.
40. + channels. Am J Physiol 291: H216-H222, 2006.
41. Hill CE. Long distance conduction of vasodilation: a passive or regenerative process? Microcirculation 19: 379-390, 2012.
42. Hill CE, Hickey H, Sandow SL. Role of gap junctions in acetylcholine-induced vasodilation of proximal and distal arteries of the rat mesentery. J Auton Nerv Syst 81: 122-127, 2000.
43. 2+ communication. J Cell Sci 121: 3664-3673, 2008.
44. 2+ and inositol 1, 4, 5-trisphosphate-mediated signaling across the myoendothelial junction. Circ Res 100: 246-254, 2007.
45. Kristek F, Gerova M. Myoendothelial relations in the conduit coronary artery of the dog and rabbit. J Vasc Res 29: 29-32, 1992.
46. Ledoux J, Taylor MS, Bonev AD, Hannah RM, Solodushko V, Shui B, Tallini Y, Kotlikoff MI, Nelson MT. Functional architecture of inositol 1, 4, 5-trisphosphate signaling in restricted spaces of myoendothelial projections. Proc Natl Acad Sci USA 105: 9627-9632, 2008.
47. Little TL, Xia J, Duling BR. Dye tracers define differential endothelial and smooth muscle coupling patterns within the arteriolar wall. Circ Res 76: 498-504, 1995.
48. Looft-Wilson RC, Billaud M, Johnstone SR, Straub AC, Isakson BE. Interaction between nitric oxide signaling and gap junctions: effects on vascular function. Biochim Biophys Acta 2011, doi:
49. Luksha L, Luksha N, Kublickas M, Nisell H, Kublickiene K. Diverse mechanisms of endothelium-derived hyperpolarizing factor-mediated dilatation in small myometrial arteries in normal human pregnancy and preeclampsia. Biol Reprod 83: 728-735, 2010.
50. Luksha L, Nisell H, Luksha N, Kublickas M, Hultenby K, Kublickiene K. Endothelium-derived hyperpolarizing factor in preeclampsia: heterogeneous contribution, mechanisms, and morphological prerequisites. Am J Physiol 294: R510-R519, 2008.
51. Mather S. Endothelial cell modulation of vascular tone by EDHF and gap junctional communication. PhD thesis, Department of Pharmacy and Pharmacology, University of Bath, Bath, UK, 2005.
52. Mather S, Dora KA, Sandow SL, Winter P, Garland CJ. Rapid endothelial cell-selective loading of connexin 40 antibody blocks endothelium-derived hyperpolarizing factor dilation in rat small mesenteric arteries. Circ Res 97: 399-407, 2005.
53. Ca channels in hyperpolarizing responses of the rat middle cerebral artery. Stroke 37: 1277-1282, 2006.
54. McSherry IN, Sandow SL, Campbell WB, Falck JR, Hill MA, Dora KA. A role for heterocellular coupling and EETs in dilation of rat cremaster arteries. Microcirculation 13: 119-130, 2006.
55. Michel RP, Hu F, Meyrick BO. Myoendothelial junctional complexes in postobstructive pulmonary vasculopathy: a quantitative electron microscopic study. Exp Lung Res 21: 437-452, 1995.
56. Moore DH, Ruska H. The fine structure of capillaries and small arteries. J Biophys Biochem Cytol 3: 457-461, 1957.
57. Newstead J, Munkacsi I. Electron microscopic observations on the juxtamedullary efferent arterioles and Arteriolae rectae in kidneys of rats. Z Zellforsch Mikrosk Anat 97: 465-490, 1969.
58. Nixon GF, Mignery GA, Somlyo AV. Immunogold localization of inositol 1, 4, 5-trisphosphate receptors and characterization of ultrastructural features of the sarcoplasmic reticulum in phasic and tonic smooth muscle. J Muscle Res Cell Motility 15: 682-700, 1994.
59. Perlin JR, Lush ME, Stephens WZ, Piotrowski T, Talbot WS. Neuronal neuregulin 1 type III directs Schwann cell migration. Development 138: 4639-4648, 2011, in press.
60. 2+ signalling in smooth muscle: why two mechanisms are better than one. Trends Pharmacol Sci 25: 8-15, 2004.
61. Reinila A, Blanchette-Mackie EJ, Scow RO. Uptake of plasma triacylglycerol by a muscular artery in the rat: an ultrastructural study. Virchows Archiv B Cell Pathol Mol Pathol 47: 67-78, 1984.
62. Rhodin JAG. The ultrastructure of mammalian arterioles and precapillary sphincters. J Ult Res 18: 181-223, 1967.
63. Roggendorf W, Cervos-Navarro J. Ultrastructure of arterioles in the cat brain. Cell Tiss Res 178: 495-515, 1977.
64. Ryan US, Ryan JW, Whitaker C. How do kinins affect vascular tone? Adv Exp Med Biol 120A: 375-391, 1979.
65. Sahoo S, Klychko E, Thorne T, Misener S, Schultz KM, Millay M, Ito A, Liu T, Kamide C, Agrawal H, Perlman H, Qin G, Kishore R, Losordo DW. Exosomes from human CD34+ stem cells mediate their proangiogenic paracrine activity. Circ Res 109: 724-728, 2011.
66. Sandow SL. Factors, fiction and endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol 31: 563-570, 2004.
67. Sandow SL, Bramich NJ, Bandi HP, Rummery N, Hill CE. Structure, function and EDHF in the caudal artery of the SHR and WKY Rat. Arterioscler Thromb Vasc Biol 23: 822-828, 2003.
68. Sandow SL, Bramich NJ, Bandi HP, Rummery NM, Hill CE. Structure, function, and endothelium-derived hyperpolarizing factor in the caudal artery of the SHR and WKY rat. Arterioscler Thromb Vasc Biol 23: 822-828, 2003.
69. Sandow SL, Goto K, Rummery N, Hill CE. Developmental changes in myoendothelial gap junction mediated vasodilator activity in the rat saphenous artery. J Physiol 556: 875-886, 2004.
70. Sandow SL, Gzik DJ, Lee RMKW. Arterial internal elastic lamina holes: relationship to function? J Anat 214: 258-266, 2009.
71. Sandow SL, Haddock RE, Hill CE, Chadha PS, Kerr PM, Welsh DG, Plane F. What's where and why at a vascular myoendothelial microdomain signalling complex? Clin Exp Pharmacol Physiol 36: 67-76, 2009.
72. Sandow SL, Hill CE. The incidence of myoendothelial gap junctions in the proximal and distal mesenteric arteries of the rat is suggestive of a role in EDHF-mediated responses. Circ Res 86: 341-346, 2000.
73. Sandow SL, Hill CE. Incidence of myoendothelial gap junctions in the proximal and distal mesenteric arteries of the rat is suggestive of a role in endothelium-derived hyperpolarizing factor-mediated responses. Circ Res 86: 341-346, 2000.
74. Sandow SL, Looft-Wilson RC, Grayson TH, Segal SS, Hill CE. Expression of homocellular and heterocellular gap junctions in hamster arterioles and feed arteries. Cardiovasc Res 60: 643-653, 2003.
75. Ca) and connexins: possible relationship to vasodilator function? J Anat 209: 689-698, 2006.
76. Sandow SL, Tare M. C-type natriuretic peptide: a new endothelium-derived hyperpolarizing factor? Trends Pharmacol Sci 28: 61-67, 2007.
77. Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC. Involvement of myoendothelial gap junctions in the actions of endothelium-derived hyperpolarizing factor. Circ Res 90: 1108-1113, 2002.
78. Sandow SL, Whitehouse D, Hill CE. Specialised sympathetic neuroeffector associations in rat iris arterioles. J Anat 192: 45-57, 1998.
79. Ca-dependent vasodilator activity in rat mesenteric artery. J Vasc Res 49(S1): 29, 2012.
80. Shimokawa H, Yasutake H, Fujii K, Owada K, Nakaike R, Fukumoto Y, Takayanagi T, Nagao T, Egashira K, Fujishima M, Takeshita A. The importance of the hyperpolarizing mechanism increases as the vessel size decreases in endothelium-dependent relaxations in rat mesenteric circulation. J Cardiovasc Pharmacol 28: 703-711, 1996.
81. Simionescu M, Simionescu N, Palade GE. Segmental differentiation of cell junctions in the vascular endothelium. The microvasculature. J Cell Biol 67: 863-885, 1975.
82. Simionescu M, Simionescu N, Palade GE. Segmental differentiations of cell junctions in the vascular endothelium: the microvasculature. J Cell Biol 67: 863-885, 1975.
83. Sims FH. The internal elastic lamina in normal and abnormal human arteries: a barrier to the diffusion of macromolecules from the lumen. Artery 16: 159-173, 1989.
84. IR channels function as electrical amplifiers in rat vascular smooth muscle. J Physiol 586: 1147-1160, 2008.
85. Smith EB, Staples EM. Distribution of plasma proteins across the human aortic wall-barrier functions of endothelium and internal elastic lamina. Atherosclerosis 37: 579-590, 1980.
86. Sokoya EM, Burns AR, Marrelli SP, Chen J. Myoendothelial gap junction frequency does not account for sex differences in EDHF responses in rat MCA. Microvasc Res 74: 39-44, 2007.
87. Soret MG, Peterson T, Block EM. Ultrastructural study of cytoplasmic bridges through the membrana elastica in the aorta of the Chinese hamster (Cricetulus griseus). Artery 2: 451-466, 1976.
88. Sosa-Melgarejo JA, Berry CL. Myoendothelial contacts on arteriolarsclerosis. J Pathol 167: 235-239, 1992.
89. Sosa-Melgarejo JA, Berry CL. Myoendothelial contacts on the thoracic aorta of rat fetuses. J Pathol 166: 311-316, 1992.
90. Sosa-Melgarejo JA, Berry CL. Myoendothelial contacts in the human fetal aorta. Arch Med Res 26: 431-435, 1995.
91. Sosa-Melgarejo JA, Berry CL, Dodd S. Myoendothelial contacts in the small arterioles of human kidney. Virchows Archiv A Path Anat Histopathol 413: 183-187, 1988.
92. Spagnoli LG, Villaschi S, Neri L, Palmeri G. Gap junctions in myoendothelial bridges of rabbit carotid arteries. Experientia 38: 124-125, 1982.
93. Svendsen E, Tindall AR. The internal elastic membrane and intimal folds in arteries: important but neglected structures? Acta Physiol Scand 133(S572): 1-71, 1988.
94. Tada S, Tarbell JM. Internal elastic lamina affects the distribution of macromolecules in the arterial wall: a computational study. Am J Physiol 287: H905-H913, 2004.
95. Tare M, Coleman HA, Parkington HC. Glycyrrhetinic derivatives inhibit hyperpolarization in endothelial cells of guinea pig and rat arteries. Am J Physiol 282: H335-H341, 2002.
96. Taugner R, Kirchheim H, Forssmann WG. Myoendothelial contacts in glomerular arterioles and in renal interlobular arteries of rat, mouse and Tupaia belangeri. Cell Tiss Res 235: 319-325, 1984.
97. von der Weid PY, Beny JL. Simultaneous oscillations in the membrane potential of pig coronary artery endothelial and smooth muscle cells. J Physiol 471: 13-24, 1993.
98. Wolfle SE, Chaston DJ, Goto K, Sandow SL, Edwards FR, Hill CE. Non-linear relationship between hyperpolarisation and relaxation enables long distance propagation of vasodilatation. J Physiol 589: 2607-2623, 2011.
99. Yamamoto Y, Klemm MF, Edwards FR, Suzuki H. Intercellular electrical communication among smooth muscle and endothelial cells in guinea-pig mesenteric arterioles. J Physiol 535: 181-195, 2001.
100. Yuste R. Dendritic spines and distributed circuits. Neuron 71: 772-781, 2011.