Site-specific connexin phosphorylation is associated with reduced heterocellular communication between smooth muscle and endothelium

Journal of Vascular Research

Volumn 47, Issue 4, 2010, Pages 277-286

  Straub, Adam C ^a   Johnstone, Scott R ^a   Heberlein, Katherine R ^a   Rizzo, Michael J ^a   Best, Angela K ^a   Boitano, Scott ^b   Isakson, Brant E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Endothelium; Gap junction; Heterocellular communication; Myoendothelial junction; Phosphorylation; Smooth muscle

Indexed keywords

CONNEXIN 43; FIBROBLAST GROWTH FACTOR 2; PHORBOL 13 ACETATE 12 MYRISTATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMMUNICATION; ENDOTHELIUM CELL; FIBROBLAST; MALE; MICROINJECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; ARTERIOLES; CALCIUM; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CONNEXIN 43; CYCLIC AMP; ENDOTHELIAL CELLS; FIBROBLAST GROWTH FACTOR 2; GAP JUNCTIONS; INOSITOL 1,4,5-TRISPHOSPHATE; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERINE; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS;

EID: 72049084553     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000265562     Document Type: Article

References (40)

1. de Wit C, Boettcher M, Schmidt VJ: Signaling across myoendothelial gap junction s-fact or f ic tion? Cel l C ommun Ad hes 20 0 8; 15: 231-245.
2. 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 20 09; 36: 67-76.
3. Heberlein K, Straub AC, Isakson BE: The myoendothelial junction: breaking through the matrix? Microcirculation 2009; 16:307-322.
4. Rhodin JA: The ultrastructure of mammalian arterioles and precapillary sphincters. J Ultrastruct Res 1967; 18:181-223.
5. Mather S, Dora KA, Sandow SL, Winter P, Garland CJ: Rapid endothelial cell-selective loading of connexin 40 antibody blocks en-dothelium-derived hyperpolarizing factor dilation in rat small mesenteric arteries. Circ Res 2005; 97:399-407.
6. 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 arter y. J Vasc Res 2003; 40: 480-490.
7. 2+ and inositol 1,4,5-trisphosphate-mediated signaling across the myoendothelial junction. Circ Res 2007; 100:246-254.
8. Isakson BE, Best AK, Duling BR: Incidence of protein on actin bridges between endo-thelium and smooth muscle in arterioles demonstrates heterogeneous connexin expression and phosphorylation. Am J Physiol Heart Circ Physiol 2008; 294:H2898-H2904.
9. Haddock RE, Grayson TH, Brackenbury TD, Meaney KR, Neylon CB, Sandow SL, Hill CE: Endothelial coordination of cerebral vasomo-tion via myoendothelial gap junctions containing connexins 37 and 40. Am J Physiol Heart Circ Physiol 2006; 291:H2047-H2056.
10. Sandow SL, Neylon CB, Chen MX, Garland CJ: Spatial separation of endothelial small-and intermediate-conductance calcium-activated potassium channels (K(Ca)) and con-nexins: possible relationship to vasodilator function? J Anat 2006; 209:689-698.
11. Lampe PD, Lau AF: Regulation of gap junctions by phosphorylation of connexins. Arch Biochem Biophys 2000; 384:205-215.
12. Lampe PD, Lau AF: The effects of connexin phosphorylation on gap junctional communication. Int J Biochem Cell Biol 2004; 36: 1171-1186.
13. Little TL, Xia J, Duling BR: Dye tracers define differential endothelial and smooth muscle coupli ng patterns withi n t he a r terio-lar wall. Circ Res 1995; 76: 498-504.
14. Siegl D, Koeppen M, Wolfle SE, Pohl U, de Wit C: Myoendothelial coupling is not prominent in arterioles within the mouse cremas-ter microcirculation in vivo. Circ Res 2005; 97: 781-788.
15. Lampe PD, TenBroek EM, Burt JM, Kurata WE, Johnson RG, Lau AF: Phosphorylation of connexin43 on serine368 by protein ki-nase C regulates gap junctional communication. J Cell Biol 2000; 14 9: 1503-1512.
16. Isakson BE, Duling BR: Heterocellular contact at the myoendothelial junction influences gap junction organization. Circ Res 2005; 97:44-51.
17. 2+ communication. J Cell Sci 2008; 121: 3664-3673.
18. Isakson BE, Damon DN, Day KH, Liao Y, Duling BR: Connexin40 and connexin43 in mouse aortic endothelium: evidence for coordinated regulation. Am J Physiol Heart Circ Physiol 2006; 290:H1199-H1205.
19. Looft-Wilson RC, Payne GW, Segal SS: Con-nexin expression and conducted vasodilation along arteriolar endothelium in mouse skeletal muscle. J Appl Physiol 2004; 97: 1152-1158.
20. Cooper CD, Lampe PD: Casein kinase 1 regulates connexin-43 gap junction assembly. J Biol Chem 2002; 277:44962-44968.
21. Desaphy JF, De Luca A, Camerino DC: Blockade by cAMP of native sodium channels of adult rat skeletal muscle fibers. Am J Physiol 1998; 275:C1465-C1472.
22. Figueroa XF, Paul DL, Simon AM, Good-enough DA, Day KH, Damon DN, Duling BR: Central role of connexin40 in the propagation of electrically activated vasodilation in mouse cremasteric arterioles in vivo. Circ Res 2003; 92:793-800.
23. Wiedeman MP: Blood flow through terminal arterial vessels after denervation of the bat wing. Circ Res 1968; 22: 83-89.
24. Langlands JM, Diamond J: The effect of phenylephrine on inositol 1,4,5-trisphos-phate levels in vascular smooth muscle measured using a protein binding assay system. Biochem Biophys Res Commun 1990; 173: 1258-1265.
25. 2+ signaling between smooth muscle and endothe-lium of resistance vessels. Circ Res 2000; 87: 1048-1054.
26. Oka T, Sato K, Hori M, Ozaki H, Karaki H: Xestospongin C, a novel blocker of IP3 receptor, attenuates the increase in cytosolic calcium level and degranulation that is induced by antigen in RBL-2H3 mast cells. Br J Pharmacol 2002; 135:1959-1966.
27. Albright CD, Kuo J, Jeong S: cAMP enhances Cx43 gap junction formation and function and reverses choline deficiency apoptosis. Exp Mol Pat hol 2001; 71: 34-39.
28. Somekawa S, Fukuhara S, Nakaoka Y, Fujita H, Saito Y, Mochizuki N: Enhanced functional gap junction neoformation by protein kinase A-dependent and Epac-dependent signals downstream of cAMP in cardiac my-ocytes. Circ Res 2005; 97: 655-662.
29. Paulson AF, Lampe PD, Meyer RA, Ten-Broek E, Atkinson MM, Walseth TF, Johnson RG: Cyclic AMP and LDL trigger a rapid enhancement in gap junction assembly through a stimulation of connexin trafficking. J Cell Sci 2000; 113:3037-3049.
30. Abudara V, Garces G, Saez JC: Cells of the carotid body express connexin43 which is up-reg ulated by cAMP. Brain Res 1999; 849: 25-33.
31. Dora KA, Gallagher NT, McNeish A, Garland CJ: Modulation of endothelial cell KCa3.1 channels during endothelium-de-rived hyperpolarizing factor signaling in mesenteric resistance ar teries. Circ Res 20 08; 102: 1247-1255.
32. Lamboley M, Pittet P, Koenigsberger M, Sau-ser R, Beny JL, Meister JJ: Evidence for signaling via gap junctions from smooth muscle to endothelial cells in rat mesenteric arteries: possible implication of a second messenger. Cell Calcium 2005; 37:311-320.
33. Ek-Vitorin JF, King TJ, Heyman NS, Lampe PD, Burt JM: Selectivity of connexin 43 channels is regulated through protein kinase C-dependent phosphorylation. Circ Res 2006; 98: 14 9 8-15 0 5.
34. Lampe PD, Cooper CD, King TJ, Burt JM: Analysis of Connexin43 phosphorylated at S325, S328 and S330 in normoxic and isch-emic heart. J Cell Sci 2006; 119:3435-3442.
35. Fujii T, Yonemitsu Y, Onimaru M, Inoue M, Hasegawa M, Kuwano H, Sueishi K: VEGF function for upregulation of endogenous PlGF expression during FGF-2-mediated therapeutic angiogenesis. Atherosclerosis 2008; 200:51-57.
36. Xu H, Czerwinski P, Hortmann M, Sohn HY, Forstermann U, Li H: Protein kinase C alpha promotes angiogenic activity of human en-dothelial cells via induction of vascular en-dothelial growth factor. Cardiovasc Res 2008; 78: 349-355.
37. 2+ oscillations by phosphorylation of Ins(1,4,5)P3 receptors. Biochem Soc Trans 2003; 31:954-957.
38. Hansra G, Garcia-Paramio P, Prevostel C, Whelan RD, Bornancin F, Parker PJ: Multi-site dephosphorylation and desensitization of conventional protein kinase C isotypes. Biochem J 1999; 342: 337-344.
39. 2+-activated K+ channels in arteriolar muscle cells. Am J Physiol 1998; 274:H27-H34.
40. Benham CD, Bolton TB, Lang RJ, Takewaki T: Calcium-activated potassium channels in single smooth muscle cells of rabbit jejunum and guinea-pig mesenteric artery. J Physiol 1986; 371:45-67.