10.1161/01.res.79.4.631
Crossref journal-article
Ovid Technologies (Wolters Kluwer Health)
Circulation Research (276)
Abstract

Integration and coordination of responses among vascular wall cells are critical to the local modulation of vasomotor tone and to the maintenance of circulatory homeostasis. This article reviews the vast literature concerning the principles that govern the initiation and propagation of vasoactive stimuli among vascular smooth muscle cells, which are nominally the final effectors of vasomotor tone. In light of the abundance of new information concerning the distribution and function of gap junctions between vascular wall cells throughout the vascular tree, particular attention is paid to this integral aspect of vascular physiology. Evidence is provided for the important contribution of intercellular communication to vascular function at all levels of the circulation, from the largest elastic artery to the terminal arterioles. The thesis of this review is that the presence of gap junctions, in concert with the autonomic nervous system, pacemaker cells, myogenic mechanisms, and/or electrotonic current spread (both hyperpolarizing and depolarizing waves through gap junctions), confers a plasticity, adaptability, and flexibility to vasculature that may well account for the observed diversity in regulation and function of vascular tissues throughout the vascular tree. It is hoped that the summary information provided here will serve as a launching pad for a new discourse on the mechanistic basis of the integrative regulation and function of vasculature, which painstakingly accounts for the undoubtedly complex and manifold role of gap junctions in vascular physiology/dysfunction.

Authors 5
  1. George J. Christ (first)
  2. David C. Spray (additional)
  3. Marwan El-Sabban (additional)
  4. Lisa K. Moore (additional)
  5. Peter R. Brink (additional)
References 154 Referenced 205
  1. 10.1152/physrev.1989.69.2.546
  2. 10.1161/res.27.3.325
  3. Gibbins IL Morris JL Furness JB Costa M. Innervation of systemic blood vessels. In: Burnstock G Griffith SG eds. Nonadrenergic Innervation of Blood Vessels. Boca Raton Fla: CRC Press; 1988.
  4. Burnstock G. Structure of smooth muscle and its innervation. In: Bulbring E Brading AF Jones AW Tomita T eds. Smooth Muscle. Baltimore Md: Williams & Wilkins; 1970:1-69.
  5. Burnstock G Relevic V. Neural-Endothelial Interactions in the Control of Local Vascular Tone. Austin Tex: RG Landes Co; 1993.
  6. Somlyo AP, Somlyo AV. Vascular smooth muscle, I: normal structure, pathology, biochemistry and biophysics. Pharmacol Rev. 1968;20:197-283. (10.1016/S0031-6997(25)07139-X) / Pharmacol Rev (1968)
  7. Speden RN. Excitation of vascular smooth muscle. In: Bulbring E Brading AF Jones AW Tomita T eds. Smooth Muscle. Baltimore Md: Williams & Wilkins; 1970:558-588.
  8. Nishimura J Moreland S Moreland RS van Breeman C. Regulation of the Ca2+-force relationship in permeabilized arterial smooth muscle. In: Morel RS ed. Regulation of Smooth Muscle Contraction. New York NY: Plenum Publishing Corp; 1991. (10.1007/978-1-4684-6003-2_11)
  9. 10.1161/res.63.4.2458859
  10. 10.1007/BF02144172
  11. Cohen RA, Weisbrod RM. Endothelium inhibits norepinephrine release from adrenergic nerves of rabbit carotid artery. Am J Physiol. 1988;254:H871-H878. / Am J Physiol (1988)
  12. 10.1139/y90-016
  13. Maxwell RA, Eckhardt SB, Wastilla WB. Concerning the distribution of endogenous norepinephrine in the adventitial and medi-intimal layers of the rabbit aorta and the capacity of these layers to bind tritiated norepinephrine. J Pharmacol Exp Ther. 1968;161:34-39. (10.1016/S0022-3565(25)27944-7) / J Pharmacol Exp Ther (1968)
  14. 10.1016/0306-4522(93)90354-I
  15. Kuriyama H, Kitamura K, Nabata H. Pharmacological and physiological significance of ion channels and factors that modulate them in vascular tissues. Pharmacol Rev. 1995;47:387-573. / Pharmacol Rev (1995)
  16. Brayden JE, Nelson MT. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science. 1992;256:533-535. / Science (1992)
  17. Nelson MT MacCarron JG Quayle JM. Ion channels in resistance arteries. In: Bevan JA Halpern W Mulvany MJ eds. The Resistance Vasculature. Tocowa NJ: Humana Press; 1991. (10.1007/978-1-4612-0403-9_16)
  18. 10.1016/0006-2952(92)90659-7
  19. 10.1002/med.2610120202
  20. Weston AH Hamilton TC eds. Potassium Channel Modulators. London England: Blackwell Scientific Publications; 1992.
  21. 10.1002/j.1939-4640.1993.tb00392.x
  22. 10.1152/ajpcell.1993.265.1.C299
  23. Bolotina VM, Palacino PJ, Cohen RA. Direct effect of nitric oxide on Ca2+-dependent K+ channels in vascular smooth muscle cells. FASEB J. 1994;8:A364. Abstract. / FASEB J (1994)
  24. 10.1152/ajpcell.1995.268.4.C799
  25. 10.1126/science.270.5236.633
  26. Sperelakis N Kuriyama H eds. Ion Channels of Vascular Smooth Muscle Cells and Endothelial Cells. New York NY: Elsevier Science Publishing Co; 1991:27-38.
  27. 10.1007/BF00370950
  28. Kitazawa T Somlyo AP. Modulation of Ca2+-sensitivity by agonists in smooth muscle. In: Morel RS ed. Regulation of Smooth Muscle Contraction. New York NY: Plenum Publishing Corp; 1991. (10.1007/978-1-4684-6003-2_10)
  29. Somlyo AP Somlyo AV. Smooth muscle structure and function. In: Fozzard HA ed. The Heart and Cardiovascular System. 2nd ed. New York NY: Raven Press Publishers; 1992.
  30. 10.1111/j.1476-5381.1991.tb12438.x
  31. 10.1113/jphysiol.1985.sp015900
  32. Rembold CM, Murphy RA. Muscle length, shortening, myoplasmic [Ca2+], and activation of arterial smooth muscle. Circ Res. 1991;66:1354-1361. / Circ Res (1991)
  33. Worley JF, Quayle JM, Standen NB, Nelson MT. Regulation of single calcium channels in cerebral arteries by voltage, serotonin, and dihydropyridines. Am J Physiol. 1991;261:H1951-H1960. / Am J Physiol (1991)
  34. 10.1152/ajpcell.1992.263.2.C373
  35. 10.1007/BF00374516
  36. 10.1152/ajprenal.1992.262.5.F799
  37. Christ GJ, Brink PR, Melman A, Spray DC. The role of gap junctions and ion channels in the modulation of electrical and chemical signals in human corpus cavernosum smooth muscle. Int J Impot Res. 1993;5:77-96. / Int J Impot Res (1993)
  38. 10.1016/0014-2999(90)90624-F
  39. 10.1113/jphysiol.1983.sp014565
  40. 10.1113/jphysiol.1981.sp013999
  41. 10.1113/jphysiol.1982.sp014418
  42. Harder DR, Sperelakis N. Action potential generation in reaggregates of rat aortic smooth muscle cells in primary culture. Blood Vessels. 1979;16:186-201. / Blood Vessels (1979)
  43. 10.1113/jphysiol.1981.sp013818
  44. 10.1113/jphysiol.1981.sp014000
  45. 10.1113/jphysiol.1983.sp014970
  46. Kitamura K Suzuki H Ito Y Kuriyama H. Similarity and diversity of electrical activity in vascular smooth muscles. In: Sperelakis N Wood JD eds. Frontiers in Smooth Muscle Research. New York NY: Wiley-Liss; 1990:257-276.
  47. 10.1159/000159059
  48. Chen X-L, Rembold CM. Phenylephrine contracts rat tail artery by one electromechanical and three pharmacomechanical mechanisms. Am J Physiol. 1995;268:H74-H81. / Am J Physiol (1995)
  49. 10.1177/000331975500600403
  50. Meyer J-U, Lindbom L, Intaglietta M. Coordinated diameter oscillations at arteriolar bifurcations in skeletal muscle. Am J Physiol. 1987;253:H568-H573. / Am J Physiol (1987)
  51. 10.1161/res.33.2.244
  52. 10.1038/1911102a0
  53. Johnson PC. The myogenic response. In: Bohr DF Somlyo AP Sparks HV eds. Handbook of Physiology Section 2: The Cardiovascular System. Baltimore Md: Williams & Wilkins; 1980:409-442. (10.1002/cphy.cp020215)
  54. Siegel G Hofer HW Schnalke F Adler A Walter A Koepchen HP. Membrane physiological basis of vascular autorhythmicity: vasomotion and flow modulation in the microcirculation. Prog Appl Microcirc. 1989;15:10-31. (10.1159/000417696)
  55. Intaglietta M. Wave-like characteristics of vasomotion. Prog Appl Microcirc. 1983;3:83-94. / Prog Appl Microcirc (1983)
  56. 10.1111/j.1365-201X.1968.tb10889.x
  57. Johansson B Somlyo AP. Electrophysiological and excitation-contraction coupling. In: Bohr DF Somlyo AP Sparks HV eds. Handbook of Physiology Section 2: The Cardiovascular System. Baltimore Md: Williams & Wilkins; 1980:301-323. (10.1002/cphy.cp020212)
  58. 10.1152/ajpcell.1987.252.5.C555
  59. 10.1113/jphysiol.1978.sp012374
  60. 10.1113/jphysiol.1991.sp018609
  61. 10.1113/jphysiol.1974.sp010698
  62. Kitamura K, Itoh T, Suzuki H, Ito Y, Kuriyama H. Properties of sympathetic neuromuscular transmission and smooth muscle membranes in vascular beds. Comp Biochem Physiol. 1991;98:181-192. / Comp Biochem Physiol (1991)
  63. Holman ME Neild TO Lang RJ. On the passive properties of smooth muscle. In: Sperelakis N Wood JD eds. Frontiers in Smooth Muscle Research. New York NY: Wiley-Liss; 1990:379-398.
  64. Tomita T. Spread of excitation in smooth muscle. In: Sperelakis N Wood JD eds. Frontiers in Smooth Muscle Research. New York NY: Wiley-Liss; 1990:361-373.
  65. 10.1113/jphysiol.1984.sp015043
  66. 10.1152/ajpcell.1989.257.2.C323
  67. Cole WC, Picone JB, Sperelakis N. Gap junction uncoupling and discontinuous propagation in the heart. Biophys J. 1988;53:908-818. / Biophys J (1988)
  68. Hille B. Ionic Channels of Excitable Membranes. 2nd ed. Sunderland Mass: Sinauer Associates Inc; 1992.
  69. Hodgkin AL. The Conduction of the Nervous Impulse. Liverpool England: Liverpool University Press; 1967.
  70. Katz B. Nerve Muscle and Synapse. New York NY: McGraw-Hill Publishing Co; 1966.
  71. Xia J, Duling BR. Electromechanical coupling and the conducted vasomotor response. Am J Physiol. 1995;269:H2022-H2030. / Am J Physiol (1995)
  72. Xia J, Duling BR. Cellular pathways of the conducted electrical response in arterioles of hamster cheek pouch in vitro. Am J Physiol. 1995;269:H2031-H2038. / Am J Physiol (1995)
  73. Beny J-L, Pacicca C. Bidirectional electrical communication between smooth muscle and endothelial cells in the pig coronary artery. Am J Physiol. 1994;266:H1465-H1472. / Am J Physiol (1994)
  74. Christ GJ, Brink PR, Ramanan SV. The impact of innervation density on syncytial responses in tissues containing gap junctions. FASEB J. 1995;9:A913. Abstract. / FASEB J (1995)
  75. 10.1016/S0022-5347(01)66468-1
  76. 10.1126/science.137.3531.670-a
  77. Hall JE Zampighi GA Davis RM eds. Gap Junctions: Progress in Cell Research Volume 3. Amsterdam Netherlands: Elsevier Science Publishing Co; 1993.
  78. 10.1016/0896-6273(91)90241-Q
  79. 10.1523/JNEUROSCI.11-05-01421.1991
  80. Barr L, Berger W, Dewey MM. Electrical transmission at the nexus between smooth muscle cells. J Gen Physiol. 1968;52:347-368. / J Gen Physiol (1968)
  81. 10.1111/j.1540-8167.1991.tb01333.x
  82. Spray DC Moreno AP Rook M Christ G Saez JC Campos de Carvalho AC Fishman GI. Cardiovascular gap junctions: gating properties function and dysfunction. In: Ion Channels in the Cardiovascular Systems. New York NY: Academic Press; 1994:185-214.
  83. Burnstock G Gannon B Iwayama T. Sympathetic innervation of vascular smooth muscle in normal and hypertensive animals. Circ Res. 1970;26-27(suppl II):II-5-II-24.
  84. 10.1111/j.1699-0463.1963.tb03440.x
  85. Cliff WJ. The aortic tunica media in growing rats studied with the electron microscope. Lab Invest. 1967;17:599-615. / Lab Invest (1967)
  86. 10.1016/S0022-5320(67)80239-9
  87. 10.1113/jphysiol.1968.sp008498
  88. 10.1111/j.1748-1716.1967.tb03631.x
  89. Christ GJ, Zhao W, Moss J, Gondre CM, Roy C, Brink PR, Spray DC. Gap junctions modulate tissue contractility and α1-adrenergic agonist efficacy in isolated rat aorta. J Pharmacol Exp Ther. 1993;266:1054-1065. (10.1016/S0022-3565(25)38361-8) / J Pharmacol Exp Ther (1993)
  90. 10.1161/res.66.4.1690612
  91. Moore LK Beyer EC Burt JM. Characterization of gap junction channels in A7r5 vascular smooth muscle cells. Am J Physiol. 1991;260(Cell Physiol 29):C975-C981. (10.1152/ajpcell.1991.260.5.C975)
  92. 10.1126/science.3775368
  93. 10.1083/jcb.92.1.183
  94. 10.1007/BF00232759
  95. Christ GJ, Moreno AP, Parker ME, Gondre CM, Valcic M, Melman A, Spray DC. Intercellular communication through gap junctions: a potential role in pharmacomechanical coupling and syncytial tissue contraction in vascular smooth muscle isolated from the human corpus cavernosum. Life Sci. 1991;49:PL-195-PL-200. / Life Sci (1991)
  96. Blennerhassett MG, Kannan MS, Garfield RE. Functional characterization of cell-to-cell coupling in cultured rat aortic smooth muscle. Cell Physiol. 1987;21:C555-C569. / Cell Physiol (1987)
  97. Little TL, Beyer EC, Duling BR. Endothelial and smooth muscle cells of microvessels express connexins 43 and 40 in situ. FASEB J. 1993;2:A893. Abstract. / FASEB J (1993)
  98. 10.1161/res.70.1.1309317
  99. 10.1016/S0022-5347(17)36455-8
  100. 10.1161/01.hyp.23.6.1113
  101. 10.1159/000159057
  102. 10.1161/res.76.3.498
  103. Segal SS. Communication among endothelial and smooth muscle cells coordinates blood flow control during exercise. News Physiol Sci. 1992;7:152-156. / News Physiol Sci (1992)
  104. 10.1152/ajpheart.1995.268.2.H729
  105. 10.1091/mbc.6.4.459
  106. 10.1083/jcb.129.3.805
  107. Dermietzel R. Junctions in the central nervous system of the cat, IV: inter-endothelial junctions of cerebral blood vessels from selected areas of the brain. Cell Tissue Res. 1975;164:45-62. / Cell Tissue Res (1975)
  108. Davies PF, Ganz P, Diehl PS. Reversible microcarrier-mediated junctional communication between endothelial and smooth muscle cell monolayers: an in vitro model of vascular cell interactions. Lab Invest. 1985;85:710-718. / Lab Invest (1985)
  109. Nagy Z, Peters H, Huttner I. Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab Invest. 1984;50:313-322. / Lab Invest (1984)
  110. Shivers RR, Arthur FE, Bowman PD. Induction of gap junctions and brain endothelium-like tight junctions in cultured bovine endothelial cells: local control of cell specialization. J Submicrosc Cytol Pathol. 1988;20:1-14. / J Submicrosc Cytol Pathol (1988)
  111. 10.1083/jcb.67.3.863
  112. 10.1161/res.26.2.163
  113. Rivers RJ. Remote effects of pressure changes in arterioles. Am J Physiol. 1995;268:H1379-H1382. / Am J Physiol (1995)
  114. Christ GJ Brink PR Davis-Joseph B Spray DC. Presence and physiological significance of gap junctions in vascular smooth muscle. In: Kanno Y ed. Gap Junctions: Progress in Cell Research. Amsterdam Netherlands: Elsevier Science Publishing Co; 1995;4:211-215. (10.1016/B978-0-444-81929-1.50043-5)
  115. 10.1152/ajpcell.1993.264.1.C80
  116. 10.1016/0024-3205(95)00001-M
  117. 10.1016/S0006-3495(94)80605-8
  118. 10.1016/S0094-0143(21)00692-3
  119. 10.1152/ajpcell.1996.271.1.C321
  120. 10.1152/ajpcell.1993.265.6.C1517
  121. Bhattacharya S, Ying X, Bhattacharya J. Intercellular communication in lung vascular myocytes. FASEB J. 1993;1:A330. Abstract. / FASEB J (1993)
  122. 10.1007/BF00370421
  123. 10.1016/0006-2952(83)90134-X
  124. Hollenberg NK. Collateral arterial tree and responses to serotonin. J Cardiovasc Pharmacol. 1987;10:S35-S38. / J Cardiovasc Pharmacol (1987)
  125. Van Zweiten PA. Pathophysiological relevance of serotonin. J Cardiovasc Pharmacol. 1988;10(suppl 3):S19-S25. (10.1097/00005344-198700103-00006)
  126. Vanhoutte PM. Cardiovascular effects of serotonin. J Cardiovasc Pharmacol. 1987;10(suppl 3):S8-S11. (10.1097/00005344-198700103-00004)
  127. Christ GJ, Jean-Jacques MJ-J. Mutual-effect amplification of contractile responses elicited by simultaneous activation of α1-adrenergic and 5-HT2 receptors in isolated rat aorta. J Pharmacol Exp Ther. 1991;256:553-561. / J Pharmacol Exp Ther (1991)
  128. 10.1016/S0006-3495(94)80985-3
  129. 10.1016/S0006-3495(89)82705-5
  130. 10.1161/res.75.3.7520372
  131. 10.1038/317331a0
  132. 10.1152/ajpcell.1994.266.1.C293
  133. 10.1016/S0006-3495(85)83783-8
  134. 10.1111/j.2042-7158.1980.tb13086.x
  135. Bevan JA, Su C. Variation of intra- and perisynaptic adrenergic transmitter concentrations with width of synaptic cleft in vascular tissue. J Pharmacol Exp Ther. 1974;190:30-38. (10.1016/S0022-3565(25)29891-3) / J Pharmacol Exp Ther (1974)
  136. 10.1152/ajpcell.1995.268.6.C1537
  137. 10.1126/science.1967852
  138. 10.1016/0006-291X(88)90169-6
  139. 10.1073/pnas.86.8.2708
  140. 10.1091/mbc.1.8.585
  141. 10.1113/jphysiol.1976.sp011507
  142. 10.1073/pnas.85.10.3431
  143. 10.1097/00004872-198906000-00011
  144. 10.1016/0014-4800(82)90091-0
  145. 10.1016/S0022-5347(17)36359-0
  146. Christ GJ, Valcic M, Gondre CM, Parker M, Janis M, Schwartz K, Stone BA, Melman A. Kinetic characteristics of α1-adrenergic contractions in human corpus cavernosum smooth muscle. Am J Physiol. 1992;263:H15-H19. / Am J Physiol (1992)
  147. 10.1111/j.1476-5381.1990.tb12717.x
  148. 10.1139/y91-138
  149. 10.1111/j.1475-097X.1992.tb00294.x
  150. 10.1091/mbc.4.1.7
  151. 10.1172/JCI116321
  152. Moore LK, Burt JM. Gap junction function in vascular smooth muscle: influence of serotonin. Am J Physiol. 1995;269:H481-H489. / Am J Physiol (1995)
  153. Gabriel JE, Paul DL. Characterization of connexin expression in rat aortic endothelial cells during in vitro wounding. Mol Biol Cell. 1993;4:329a. Abstract. / Mol Biol Cell (1993)
  154. Giraldi A, Wen Y, Geliebter J, Christ GJ. Altered gap junction (connexin43) mRNA expression in human corpus cavernosum vascular smooth muscle. FASEB J. 1995;9:A913. Abstract. / FASEB J (1995)
Dates
Type When
Created 13 years, 2 months ago (June 11, 2012, 8:47 p.m.)
Deposited 5 months ago (March 30, 2025, 6:22 p.m.)
Indexed 1 month, 4 weeks ago (July 2, 2025, 2:34 p.m.)
Issued 28 years, 10 months ago (Oct. 1, 1996)
Published 28 years, 10 months ago (Oct. 1, 1996)
Published Print 28 years, 10 months ago (Oct. 1, 1996)
Funders 0

None

@article{Christ_1996, title={Gap Junctions in Vascular Tissues: Evaluating the Role of Intercellular Communication in the Modulation of Vasomotor Tone}, volume={79}, ISSN={1524-4571}, url={http://dx.doi.org/10.1161/01.res.79.4.631}, DOI={10.1161/01.res.79.4.631}, number={4}, journal={Circulation Research}, publisher={Ovid Technologies (Wolters Kluwer Health)}, author={Christ, George J. and Spray, David C. and El-Sabban, Marwan and Moore, Lisa K. and Brink, Peter R.}, year={1996}, month=oct, pages={631–646} }