Endothelial remodelling and intracellular calcium machinery

Current Molecular Medicine

Volumn 14, Issue 4, 2014, Pages 457-480

  Moccia, F ^a   Tanzi, F ^a   Munaron, L ^b  

^a Laboratory of General Physiology   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Connexin hemichannels; Endothelial dysfunction; Endothelial progenitor cells; Ischemic disease; Orai1; Stim1; TRPC1

Indexed keywords

CALCIUM CHANNEL; CALCIUM; GAP JUNCTION PROTEIN;

ARTICLE; CALCIUM CELL LEVEL; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GAP JUNCTION; HUMAN; NONHUMAN; PROEIN EXPRESSION; RISK FACTOR; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TRANSPLANTATION; ANIMAL; CALCIUM SIGNALING; CYTOLOGY; INTRACELLULAR SPACE; MECHANICS; METABOLISM; PATHOLOGY; REGENERATION; STEM CELL; VASCULAR ENDOTHELIUM;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CONNEXINS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INTRACELLULAR SPACE; MECHANICAL PROCESSES; REGENERATION; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84904039769     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524013666131118113410     Document Type: Article

References (249)

1. Vanhoutte PM, Shimokawa H, Tang EHC, Feletou M. Endothelial dysfunction and vascular disease. Acta Physiol 2009;196:193-222.
2. Khazaei M, Moien-Afshari F, Laher I. Vascular endothelial function in health and diseases. Pathophysiol 2008;15:49-67.
3. Mancardi D, Fiorio Pla A, Moccia F, Tanzi F, Munaron L. Old and New Gasotransmitters in the Cardiovascular System: Focus on the Role of Nitric Oxide and Hydrogen Sulfide in Endothelial Cells and Cardiomyocytes. Curr Pharm Biotechnol 2011;12:1406-15.
4. Munaron L, Fiorio Pla A. Endothelial Calcium Machinery and Angiogenesis: Understanding Physiology to Interfere with Pathology. Curr Med Chem 2009;16:4691-703.
5. Moccia F, Berra-Romani R, Tanzi F. Update on vascular endothelial Ca(2+) signalling: A tale of ion channels, pumps and transporters. World J Biol Chem 2012;3:127-58.
6. Moccia F, Everardo Avelino-Cruz J, Sanchez-Hernandez Y, Tanzi F. Ca2 Signalling in Damaged Endothelium: Do Connexin Hemichannels Aid in Filling the Gap? Curr Drug Ther 2010;5:277-87.
7. Kuruvilla L, Kartha CC. Molecular mechanisms in endothelial regulation of cardiac function. Mol Cell Biochem 2003;253:113-23.
8. Deanfield JE, Halcox JP, Rabelink TJ. Endothelial function and dysfunction-Testing and clinical relevance. Circulation 2007;115:1285-95.
9. Feletou M, Vanhoutte PM. Endothelial dysfunction: a multifaceted disorder. Am J Physiol Heart Circ Physiol 2006;291:H985-H1002.
10. Orford JL, Selwyn AP, Ganz P, Popma JJ, Rogers C. The comparative pathobiology of atherosclerosis and restenosis. Am J Cardiol 2000;86:6H-11H.
11. Marx SO, Totary-Jain H, Marks AR. Vascular Smooth Muscle Cell Proliferation in Restenosis. Circ-Cardiovasc Interv 2011;4:104-11.
12. Kim MS, Dean LS. In-Stent Restenosis. Cardiovasc Ther 2011;29:190-8.
13. Zargham R. Preventing restenosis after angioplasty: a multistage approach. Clin Sci 2008;114:257-64.
14. Tesfamariam B, DeFelice AF. Endothelial injury in the initiation and progression of vascular disorders. Vascul Pharmacol 2007;46:229-37.
15. Vanhoutte PM. Endothelial Dysfunction-The First Step Toward Coronary Arteriosclerosis. Circ J 2009;73:595-601.
16. Dignat-George F, Sampol J. Circulating endothelial cells in vascular disorders: new insights into an old concept. Eur J Haematol 2000;65:215-20.
17. Yoder M, Rounds S. Bad blood, bad endothelium: ill fate? Blood 2011;117:3479-80.
18. Watt J, Wadsworth R, Kennedy S, Oldroyd KG. Pro-healing drug-eluting stents: a role for antioxidants? Clin Sci 2008;114:265-73.
19. Finn AV, Nakazawa G, Joner M, et al. Vascular responses to drug eluting stents-Importance of delayed healing. Arterioscler Thromb Vasc Biol 2007;27:1500-10.
20. Otsuka F, Finn AV, Yazdani SK, Nakano M, Kolodgie FD, Virmani R. The importance of the endothelium in atherothrombosis and coronary stenting. Nature Rev Cardiol 2012;9:439-53.
21. Celik T, Iyisoy A, Kursaklioglu H, Celik M. The forgotten player of in-stent restenosis: Endothelial dysfunction. Int J Cardiol 2008;126:443-4.
22. Joner M, Finn AV, Farb A, et al. Pathology of drug-eluting stents in humans-Delayed healing and late thrombotic risk. J Am Coll Cardiol 2006;48:193-202.
23. Kipshidze N, Dangas G, Tsapenko M, et al. Role of the endothelium in modulating neointimal formation-Vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions. J Am Coll Cardiol 2004;44:733-9.
24. Asahara T, Bauters C, Pastore C, et al. Local-delivery of vascular endothelial growth-factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid-artery. Circulation 1995;91:2793-801.
25. Asahara T, Chen DH, Tsurumi Y, et al. Accelerated restitution of endothelial integrity and endothelium-dependent function after phVEGF(165) gene transfer. Circulation 1996;94:3291-302.
26. Tada T, Reidy MA. Endothelial regeneration.9. arterial injury followed by rapid endothelial repair induces smooth-musclecell proliferation but not intimal thickening. Am J Pathol 1987;129:429-33.
27. 2+ Entry Is Expressed in Human Endothelial Progenitor Cells. Stem Cells Dev 2010;19:1967-81.
28. 2+ Waves: A Novel Target for Cell-based Therapy and Anti-cancer Treatment? Curr Signal Transduct Ther 2012;7:161-76.
29. Coomber BL, Gotlieb AI. In vitro endothelial wound repair-interaction of cell-migration and proliferation. Arteriosclerosis 1990;10:215-22.
30. Kawamoto A, Losordo DW. Endothelial progenitor cells for cardiovascular regeneration. Trends Cardiovasc Med 2008;18:33-7.
31. Leone AM, Valgimigli M, Giannico MB, et al. From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 2009;30:890-9.
32. Munaron L. Intracellular calcium, endothelial cells and angiogenesis. Recent Patents Anticancer Drug Discov 2006;1:105-19.
33. Nilius B, Droogmans G. Ion channels and their functional role in vascular endothelium. Physiol Rev 2001;81:1415-59.
34. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: Dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol 2003;4:517-29.
35. Clapham DE. Calcium signaling. Cell 2007;131:1047-58.
36. Fiorio Pla A, Avanzato D, Munaron L, Ambudkar IS. Ion channels and transporters in cancer. 6. Vascularizing the tumor: TRP channels as molecular targets. Am J Physiol Cell Physiol 2012;302:C9-C15.
37. Munaron L, Genova T, Avanzato D, Antoniotti S, Fiorio Pla A. Targeting Calcium Channels to Block Tumor Vascularization. Recent Patents Anticancer Drug Discov 2013;8:27-37.
38. Di A, Malik AB. TRP channels and the control of vascular function. Curr Opin Pharmacol 2010;10:127-32.
39. 2+-ATPase in rat microvascular endothelial cells. Biochem J 2002;364:235-44.
40. 2+ extrusion in ATP-stimulated endothelium of intact rat aorta. Biochem Biophys Res Commun 2010;395:126-30.
41. 2+ oscillations. Trends Biochem Sci 2011;36:78-87.
42. Gomez MF, Stevenson AS, Bonev AD, Hill-Eubanks DC, Nelson MT. Opposing actions of inositol 1,4,5-trisphosphate and ryanodine receptors on nuclear factor of activated T-cells regulation in smooth muscle. J Biol Chem 2002;277:37756-64.
43. Yao XQ, Garland CJ. Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 2005;97:853-63.
44. 2+ Signaling. Cold Spring Harb Perspect Biol 2010;2:31.
45. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol 2006;68:619-47.
46. Wu L-J, Sweet T-B, Clapham DE. International Union of Basic and Clinical Pharmacology. LXXVI. Current Progress in the Mammalian TRP Ion Channel Family. Pharmacol Rev 2010;62:381-404.
47. Cheng HW, James AF, Foster RR, Hancox JC, Bates DO. VEGF activates receptor-operated cation channels in human microvascular endothelial cells. Arterioscler Thromb Vasc Biol 2006;26:1768-76.
48. Hamdollah Zadeh MA, Glass CA, Magnussen A, Hancox JC, Bates DO. VEGF-Mediated Elevated Intracellular Calcium and Angiogenesis in Human Microvascular Endothelial Cells In Vitro are Inhibited by Dominant Negative TRPC6. Microcirculation 2008;15:605-14.
49. Ge RL, Tai YL, Sun YY, et al. Critical role of TRPC6 channels in VEGF-mediated angiogenesis. Cancer Lett 2009;283:43-51.
50. Antigny F, Girardin N, Frieden M. Transient Receptor Potential Canonical Channels Are Required for in Vitro Endothelial Tube Formation. J Biol Chem 2012;287:5917-27.
51. Fiorio Pla A, Ong HL, Cheng KT, et al. TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acidactivated actin remodeling. Oncogene 2012;31:200-12.
52. 2+ entry is involved in early steps of tumor angiogenesis. Mol Cancer Res 2008;6:535-45.
53. Hartmannsgruber V, Heyken WT, Kacik M, et al. Arterial Response to Shear Stress Critically Depends on Endothelial TRPV4 Expression. PLoS One 2007;2:9.
54. Schierling W, Troidi K, Apfelbeck H, et al. Cerebral Arteriogenesis is Enhanced by Pharmacological as Well as Fluid-Shear-Stress Activation of the Trpv4 Calcium Channel. Eur J Vasc Endovasc Surg 2011;41:589-96.
55. Baldoli E, Maier JAM. Silencing TRPM7 mimics the effects of magnesium deficiency in human microvascular endothelial cells. Angiogenesis 2012;15:47-57.
56. Beech DJ. Orai1 calcium channels in the vasculature. Pflugers Arch 2012;463:635-47.
57. Li J, Cubbon RM, Wilson LA, et al. Orai1 and CRAC Channel Dependence of VEGF-Activated Ca(2+) Entry and Endothelial Tube Formation. Circ Res 2011;108:1190-U131.
58. Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M. Stim1 and Orai1 Mediate CRAC Currents and Store-Operated Calcium Entry Important for Endothelial Cell Proliferation. Circ Res 2008;103:1289-U185.
59. Rinne A, Banach K, Blatter LA. Regulation of nuclear factor of activated T cells (NFAT) in vascular endothelial cells. J Mol Cell Cardiol 2009;47:400-10.
60. 2+ uptake in bovine vascular endothelial cells. J Physiol (Lond) 2002;539:77-91.
61. 2+ Entry in Endothelial Progenitor Cells As a Perspective Tool to Enhance Cell-Based Therapy and Adverse Tumour Vascularization. Curr Med Chem 2012;19:5802-18.
62. Lee KP, Yuan JP, So I, Worley PF, Muallem S. STIM1-dependent and STIM1-independent Function of Transient Receptor Potential Canonical (TRPC) Channels Tunes Their Store-operated Mode. J Biol Chem 2010;285:38666-73.
63. Worley PF, Zeng W, Huang GN, et al. TRPC channels as STIM1-regulated store-operated channels. Cell Calcium 2007;42:205-11.
64. Ong HL, Cheng KT, Liu XB, et al. Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in storeoperated calcium influx. Evidence for similarities in storeoperated and calcium release-activated calcium channel components (vol 282, pg 9105-16, 2007). J Biol Chem 2007;282:27556.
65. 2+ Entry Function of Transient Receptor Potential Canonical (TRPC) 1 and 4 Channels in Endothelial Cells. Mol Pharmacol 2012;81:510-26.
66. 2+ influx. Circ Res 2005;96:1282-90.
67. Bair AM, Thippegowda PB, Freichel M, et al. Ca(2+) Entry via TRPC Channels Is Necessary for Thrombin-induced NFkappa B Activation in Endothelial Cells through AMPactivated Protein Kinase and Protein Kinase C delta. J Biol Chem 2009;284:563-74.
68. Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, Tiruppathi C. Caveolin-1 scaffold domain interacts with TRPC1 and IP(3)R3 to regulate Ca(2+) store releaseinduced Ca(2+) entry in endothelial cells. Am J Physiol Cell Physiol 2009;296:C403-C13.
69. Xue J, Thippegowda PB, Hu G, et al. NF-kappa B regulates thrombin-induced ICAM-1 gene expression in cooperation with NFAT by binding to the intronic NF-kappa B site in the ICAM-1 gene. Physiol Genomics 2009;38:42-53.
70. Munaron L, Avanzato D, Moccia F, Mancardi D. Hydrogen sulfide as a regulator of calcium channels. Cell Calcium 2013;53:77-84.
71. Yoshida T, Inoue R, Morii T, et al. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2006;2:596-607.
72. Tomatis C, Fiorio Pla A, Munaron L. Cytosolic calcium microdomains by arachidonic acid and nitric oxide in endothelial cells. Cell Calcium 2007;41:261-9.
73. Pupo E, Pla AF, Avanzato D, et al. Hydrogen sulfide promotes calcium signals and migration in tumor-derived endothelial cells. Free Radic Biol Med 2011;51:1765-73.
74. Moccia F, Bertoni G, Fiorio Pla A, et al. Hydrogen Sulfide Regulates Intracellular Ca(2+) Concentration in Endothelial Cells From Excised Rat Aorta. Curr Pharm Biotechnol 2011;12:1416-26.
75. Drumheller PD, Hubbell JA. Local modulation of intracellular calcium levels near a single-cell wound in human endothelial monolayers. Arterioscler Thromb 1991;11:1258-65.
76. Hinman LE, Beilman GJ, Groehler KE, Sammak PJ. Woundinduced calcium waves in alveolar type II cells. Am J Physiol-Lung Cell Mol Physiol 1997;273:L1242-L8.
77. Sammak PJ, Hinman LE, Tran POT, Sjaastad MD, Machen TE. How do injured cells communicate with the surviving cell monolayer? J Cell Sci 1997;110:465-75.
78. 2+ waves in epithelial cells. J Cell Sci 2001;114:4185-95.
79. Sung YJ, Sung ZL, Ho CL, et al. Intercellular calcium waves mediate preferential cell growth toward the wound edge in polarized hepatic cells. Exp Cell Res 2003;287:209-18.
80. 2+ signaling in injured in situ endothelium of rat aorta. Cell Calcium 2008;44:298-309.
81. Berra-Romani R, Raqeeb A, Torres-Jacome J, et al. The Mechanism of Injury-Induced Intracellular Calcium Concentration Oscillations in the Endothelium of Excised Rat Aorta. J Vasc Res 2012;49:65-76.
82. Berrout J, Jin M, O'Neil RG. Critical role of TRPP2 and TRPC1 channels in stretch-induced injury of blood-brain barrier endothelial cells. Brain Res 2012;1436:1-12.
83. 2+ signals and pre-wound serum signals is required for proliferation after mechanical injury. Cell Prolif 1998;31:155-70.
84. 2+, increase and its transcriptional activation of immediate early genes is important in the regulation of motility. Exp Cell Res 1999;246:319-26.
85. Unger GM, Bellrichard RL, Trinh BI, Sammak PJ. Quantitative assessment of leading edge adhesion: Reattachment kinetics modulated by injury-derived intracellular calcium predict wound closure rates in endothelial monolayers. J Cell Physiol 1998;174:217-31.
86. 2+ signaling and reendothelialization. J Cell Physiol 2008;214:595-603.
87. Shabir S, Southgate J. Calcium signalling in woundresponsive normal human urothelial cell monolayers. Cell Calcium 2008;44:453-64.
88. Leiper LJ, Walczysko P, Kucerova R, et al. The roles of calcium signaling and ERK1/2 phosphorylation in a Pax6(+/-) mouse model of epithelial wound-healing delay. BMC Biol 2006;4:14.
89. Moses S, Dreja K, Lindqvist A, Lovdahl C, Hellstrand P, Hultgardh-Nilsson A. Smooth muscle cell response to mechanical injury involves intracellular calcium release and ERK1/ERK2 phosphorylation. Exp Cell Res 2001;269:88-96.
90. Schalper KA, Sanchez HA, Lee SC, Altenberg GA, Nathanson MH, Saez JC. Connexin 43 hemichannels mediate the Ca(2+) influx induced by extracellular alkalinization. Am J Physiol Cell Physiol 2010;299:C1504-C15.
91. Yin J, Kuebler WM. Mechanotransduction by TRP Channels: General Concepts and Specific Role in the Vasculature. Cell Biochem Biophys 2010;56:1-18.
92. Kuipers AJ, Middelbeek J, van Leeuwen FN. Mechanoregulation of cytoskeletal dynamics by TRP channels. Eur J Cell Biol 2012;91:834-46.
93. Patel A, Sharif-Naeini R, Folgering JRH, Bichet D, Duprat F, Honore E. Canonical TRP channels and mechanotransduction: from physiology to disease states. Pflugers Arch 2010;460:571-81.
94. Boucher I, Kehasse A, Marcincin M, Rich C, Rahimi N, Trinkaus-Randall V. Distinct Activation of Epidermal Growth Factor Receptor by UTP Contributes to Epithelial Cell Wound Repair. Am J Pathol 2011;178:1092-105.
95. Weinger I, Klepeis VE, Trinkaus-Randall V. Tri-nucleotide receptors play a critical role in epithelial cell wound repair. Purinergic Signal 2005;1:281-92.
96. 2+ waves: mechanisms and function. Physiol Rev 2012;92:1359-92.
97. Sonnemann KJ, Bement WM. Wound Repair: Toward Understanding and Integration of Single-Cell and Multicellular Wound Responses. Annu Rev Cell Dev Biol 2011;27:237-63.
98. Zhao M. Electrical fields in wound healing-An overriding signal that directs cell migration. Sem Cell Dev Biol 2009;20:674-82.
99. Klepeis VE, Weinger I, Kaczmarek E, Trinkaus-Randal V. P2Y receptors play a critical role in epithelial cell communication and migration. J Cell Biochem 2004;93:1115-33.
100. Capiod T, Shuba Y, Skryma R, Prevarskaya N. Calcium signalling and cancer cell growth. Subcell Biochem 2007;45:405-27.
101. 2+ transport. Nature Rev Cancer 2007;7:519-30.
102. 2+ for cancer cell proliferation and survival. Nat Rev Cancer 2008;8:361-75.
103. Prevarskaya N, Skryma R, Shuba Y. Ion channels and the hallmarks of cancer. Trends Mol Med 2010;16:107-21.
104. Lehen'kyi V, Shapovalov G, Skryma R, Prevarskaya N. Ion channnels and transporters in cancer. 5. Ion channels in control of cancer and cell apoptosis. Am J Physiol-Cell Physiol 2011;301:C1281-C9.
105. Talarico EF. Plasma membrane calcium-ATPase isoform four distribution changes during corneal epithelial wound healing. Mol Vis 2010;16:2259-72.
106. Salido GM, Sage SO, Rosado JA. Biochemical and functional properties of the store-operated Ca(2+) channels. Cell Signal 2009;21:457-61.
107. 2+ entry in the immune system and beyond. Immunol Rev 2009;231:189-209.
108. Zhang W, Halligan KE, Zhang X, et al. Orai1-Mediated ICRAC Is Essential for Neointima Formation After Vascular Injury. Circ Res 2011;109:534-U189.
109. Berridge MJ. Calcium signaling and cell proliferation. Bioessays 1995;17:491-500.
110. Patton AM, Kassis J, Doong H, Kohn EC. Calcium as a molecular target in angiogenesis. Curr Pharm Des 2003;9:543-51.
111. 2+ signals are modulated by ectonucleotidases in in situ endothelial cells of rat aorta. J Vasc Res 2004;41:166-73.
112. Feldman ST, Ngyuyen V, Schonthal A, Feramisco J. Expression of c-jun in bovine corneal endothelial-cells. Inv Ophthal Vis Sci 1992;33 (Suppl):923.
113. Wei CL, Wang XH, Chen M, Ouyang K, Song LS, Cheng HP. Calcium flickers steer cell migration. Nature 2009;457:901-5.
114. Malinin NL, Pluskota E, Byzova TV. Integrin signaling in vascular function. Curr Opin Hematol 2012;19:206-11.
115. Born GV, Kratzer MA. Source and concentration of extracellular adenosine triphosphate during haemostasis in rats, rabbits and man. J Physiol (Lond) 1984;354:419-29.
116. Bai CX, Giamarchi A, Rodat-Despoix L, et al. Formation of a new receptor-operated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep 2008;9:472-9.
117. Kobori T, Smith GD, Sandford R, Edwardson JM. The Transient Receptor Potential Channels TRPP2 and TRPC1 Form a Heterotetramer with a 2:2 Stoichiometry and an Alternating Subunit Arrangement. J Biol Chem 2009;284:35507-13.
118. Kim I, Moon SO, Kim SH, Kim HJ, Koh YS, Koh GY. Vascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factorkappa B activation in endothelial cells. J Biol Chem 2001;276:7614-20.
119. Aird WC. Phenotypic heterogeneity of the endothelium I. Structure, function, and mechanisms. Circ Res 2007;100:158-73.
120. Aird WC. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med 2012;2:a006429.
121. Adams DJ, Barakeh J, Laskey R, Vanbreemen C. Ion channels and regulation of intracellular calcium in vascular endothelial-cells. FASEB J 1989;3:2389-400.
122. Nicosia RF. The aortic ring model of angiogenesis: a quarter century of search and discovery. J Cell Mol Med 2009;13:4113-36.
123. Parekh AB. Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 2010;9:399-410.
124. 2+-dependent signal transduction. Traffic 2003;4:717-23.
125. Kahl CR, Means AR. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 2003;24:719-36.
126. 2+](i)) in migrating human umbilical vein endothelial cells (HUVECs) stimulated by shear-stress. Life Sci 1999;65:2643-51.
127. 2+ influxand phosphatidylinositol 3-kinase-mediated m-calpain activity for shear stress-induced endothelial cell polarity. Am J Physiol-Cell Physiol 2007;293:C1216-C25.
128. Gotlieb AI, Spector W. Migration into an in vitro experimental wound: a comparison of porcine aortic endothelial and smooth muscle cells and the effect of culture irradiation. Am J Pathol 1981;103:271-82.
129. Poppa V, Miyashiro JK, Corson MA, Berk BC. Endothelial NO synthase is increased in regenerating endothelium after denuding injury of the rat aorta. Arterioscler Thromb Vasc Biol 1998;18:1312-21.
130. Zheng JQ, Poo MM. Calcium signaling in neuronal motility. Annu Rev Cell Dev Biol 2007; 23: 375-404.
131. Marchenko SM, Sage SO. Electrical-properties of resting and acetylcholine-stimulated endothelium in intact rat aorta. J Physiol-London 1993;462:735-51.
132. Moccia F, Berra-Romani R, Baruffi S, et al. Basal nonselective cation permeability in rat cardiac microvascular endothelial cells. Microvasc Res 2002;64:187-97.
133. Tracey WR, Peach MJ. Differential muscarinic receptor messenger-RNA expression by freshly isolated and cultured bovine aortic endothelial-cells. Circ Res 1992;70:234-40.
134. Kohler R, Brakemeier S, Kuhn M, et al. Expression of ryanodine receptor type 3 and TRP channels in endothelial cells: comparison of in situ and cultured human endothelial cells. Cardiovasc Res 2001;51:160-8.
135. Hansson GK, Chao S, Schwartz SM, Reidy MA. Aortic endothelial-cell death and replication in normal and lipopolysaccharide-treated rats. Am J Pathol 1985;121:123-7.
136. Schwartz SM, Benditt EP. Clustering of replicating cells in aortic endothelium. Proc Natl Acad Sci U S A 1976;73:651-3.
137. Contreras JE, Sanchez HA, Veliz LP, Bukauskas FF, Bennett MVL, Saez JC. Role of connexin-based gap junction channels and hemichannels in ischemia-induced cell death in nervous tissue. Brain Res Rev 2004;47:290-303.
138. Lohman AW, Billaud M, Isakson BE. Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc Res 2012;95:269-80.
139. Liu CL, Mather S, Huang Y, Garland CJ, Yao XQ. Extracellular ATP facilitates flow-induced vasodilatation in rat small mesenteric arteries. Am J Physiol-Heart Circul Physiol 2004;286:H1688-H95.
140. Lodola F, Laforenza U, Bonetti E, et al. Store-operated ca(2+) entry is remodelled and controls in vitro angiogenesis in endothelial progenitor cells isolated from tumoral patients. PLoS One 2012;7:e42541.
141. Dhein S. Pharmacology of gap junctions in the cardiovascular system. Cardiovasc Res 2004;62:287-98.
142. Herve JC, Sarrouilhe D. Connexin-made channels as pharmacological targets. Curr Pharm Des 2005;11:1941-58.
143. Johnstone S, Isakson B, Locke D. Biological and biophysical properties of vascular connexin channels. Int Rev Cell Mol Biol 2009;278:69-118.
144. Goodenough DA, Paul DL. Gap Junctions. Cold Spring Harb Perspect Biol 2009;1:19.
145. Brisset AC, Isakson BE, Kwak BR. Connexins in Vascular Physiology and Pathology. Antioxid Redox Signal 2009;11:267-82.
146. de Wit C, Woelfle SE, Hoepfl B. Connexin-dependent communication within the vascular wall: Contribution to the control of arteriolar diameter. Adv Cardiol 2006;42:268-83.
147. Figueroa XF, Duling BR. Gap Junctions in the Control of Vascular Function. Antioxid Redox Signal 2009;11:251-66.
148. Morel S, Kwak BR. Roles of Connexins in Atherosclerosis and Ischemia-Reperfusion Injury. Curr Pharm Biotechnol 2012;13:17-26.
149. Scemes E, Spray DC, Meda P. Connexins, pannexins, innexins: novel roles of hemi-channels. Pflugers Arch 2009;457:1207-26.
150. Saez JC, Retamal MA, Basilio D, Bukauskas FF, Bennett MVL. Connexin-based gap junction hemichannels: Gating mechanisms. Biochim Biophys Acta-Biomembr 2005;1711:215-24.
151. Stout C, Goodenough DA, Paul DL. Connexins: functions without junctions. Curr Opin Cell Biol 2004;16:507-12.
152. Okamoto T, Akiyama M, Takeda M, Gabazza EC, Hayashi T, Suzuki K. Connexin32 is expressed in vascular endothelial cells and participates in gap-junction intercellular communication. Biochem Biophys Res Commun 2009;382:264-8.
153. Gabriels JE, Paul DL. Connexin43 is highly localized to sites of disturbed flow in rat aortic endothelium but connexin37 and connexin40 are more uniformly distributed. Circ Res 1998;83:636-43.
154. Faigle M, Seessle J, Zug S, El Kasmi KC, Eltzschig HK. ATP Release from Vascular Endothelia Occurs Across Cx43 Hemichannels and Is Attenuated during Hypoxia. PLoS One. 2008;3:9.
155. Cherian PP, Siller-Jackson AJ, Gu SM, et al. Mechanical strain opens connexin 43 hemichannels in osteocytes: A novel mechanism for the release of prostaglandin. Mol Biol Cell 2005;16:3100-6.
156. Gomes P, Srinivas SP, Van Driessche W, Vereecke J, Himpens B. ATP release through connexin hemichannels in corneal endothelial cells. Invest Ophthal Vis Sci 2005;46:1208-18.
157. Braet K, Aspeslagh S, Vandamme W, et al. Pharmacological sensitivity of ATP release triggered by photoliberation of inositol-1,4,5-trisphosphate and zero extracellular calcium in brain endothelial cells. J Cell Physiol 2003;197:205-13.
158. 2+-dependent proinflammatory responses in lung capillaries. J Clin Invest 2006;116:2193-200.
159. Yi F-X, Boeldt DS, Gifford SM, et al. Pregnancy Enhances Sustained Ca(2+) Bursts and Endothelial Nitric Oxide Synthase Activation in Ovine Uterine Artery Endothelial Cells Through Increased Connexin 43 Function. Biol Reprod 2010;82:66-75.
160. 2+/PKC, p44/42 and p38 MAPKs pathways. Cell Prolif 2008;41:786-802.
161. Verma V, Hallett MB, Leybaert L, Martin PE, Evans WH. Perturbing plasma membrane hemichannels attenuates calcium signalling in cardiac cells and HeLa cells expressing connexins. Eur J Cell Biol 2009;88:90.
162. 2+ Entry Pathway. J Biol Chem 2012;287:12250-66.
163. De Bock M, Culot M, Wang N, et al. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability. J Cereb Blood Flow Metab 2011;31:1942-57.
164. Shintani-Ishida K, Uemura K, Yoshida KI. Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia. Am J Physiol-Heart Circul Physiol 2007;293:H1714-H20.
165. Bukauskas FF, Verselis VK. Gap junction channel gating. Biochim Biophys Acta-Biomembr 2004;1662:42-60.
166. Thompson RJ, MacVicar BA. Connexin and pannexin hemichannels of neurons and astrocytes. Channels 2008;2:81-6.
167. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E. Pannexin 1: The Molecular Substrate of Astrocyte Hemichannels. J Neurosci 2009;29:7092-7.
168. Shestopalov VI, Panchin Y. Pannexins and gap junction protein diversity. Cell Mol Life Sci 2008;65:376-94.
169. Schalper KA, Palacios-Prado N, Orellana JA, Saez JC. Currently used methods for identification and characterization of hemichannels. Cell Commun Adhes 2008;15:207-18.
170. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 2009;1793:933-40.
171. 2+ oscillations in microvascular endothelial cells. J Cell Physiol 2003;194:139-50.
172. Pal S, Wu J, Murray JK, et al. An antiangiogenic neurokinin-B/thromboxane A2 regulatory axis. J Cell Biol 2006;174:1047-58.
173. Mi LY, Ettenson DS, Edelman ER. Phospholipase C-delta extends intercellular signalling range and responses to injuryreleased growth factors in non-excitable cells. Cell Prolif 2008;41:671-90.
174. Cooke JP. NO and angiogenesis. Atheroscler Suppl 2003;4:53-60.
175. Morel S, Burnier L, Kwak BR. Connexins participate in the initiation and progression of atherosclerosis. Semin Immunopathol 2009;31:49-61.
176. Burnier L, Fontana P, Angelillo-Scherrer A, Kwak BR. Intercellular Communication in Atherosclerosis. Physiology 2009;24:36-44.
177. Yeh HI, Lai YJ, Chang HM, Ko YS, Severs NJ, Tsai CH. Multiple connexin expression in regenerating arterial endothelial gap junctions. Arterioscler Thromb Vasc Biol 2000;20:1753-62.
178. Kwak BR, Pepper MS, Gros DB, Meda P. Inhibition of endothelial wound repair by dominant negative connexin inhibitors. Mol Biol Cell 2001;12:831-45.
179. Pepper MS, Montesano R, Elaoumari A, Gros D, Orci L, Meda P. Coupling and connexin-43 expression in microvascular and large vessel endothelial-cells. Am J Physiol 1992;262:C1246-C57.
180. Chadjichristos CE, Matter CM, Roth I, et al. Reduced connexin43 expression limits neointima formation after balloon distension injury in hypercholesterolemic mice. Circulation 2006;113:2835-43.
181. Wang HH, Kung CI, Tseng YY, et al. Activation of endothelial cells to pathological status by down-regulation of connexin43. Cardiovasc Res 2008;79:509-18.
182. Hou CJY, Tsai CH, Su CH, et al. Diabetes reduces aortic endothelial gap junctions in ApoE-deficient mice: Simvastatin exacerbates the reduction. J Histochem Cytochem 2008;56:745-52.
183. Wong CW, Christen T, Roth I, et al. Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 2006;12:950-4.
184. Evans WH, Boitano S. Connexin mimetic peptides: specific inhibitors of gap-junctional intercellular communication. Biochem Soc Trans 2001;29:606-12.
185. Evans WH, De Vuyst E, Leybaert L. The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 2006;397:1-14.
186. Griffith TM. Endothelium-dependent smooth muscle hyperpolarization: do gap junctions provide a unifying hypothesis? Br J Pharmacol 2004;141:881-903.
187. Christ GJ, Spektor M, Brink PR, Barr L. Further evidence for the selective disruption of intercellular communication by heptanol. Am J Physiol Heart Circ Physiol 1999;276:H1911-H7.
188. Figueroa XF, Isakson BE, Duling BR. Connexins: Gaps in our knowledge of vascular function. Physiology 2004;19:277-84.
189. Asahara T, Kawamoto A, Masuda H. Concise Review: Circulating Endothelial Progenitor Cells for Vascular Medicine. Stem Cells 2011;29:1650-5.
190. Yoder MC. Human endothelial progenitor cells. Cold Spring Harbor Perspect Med 2012;2:a006692.
191. Dimmeler S. Regulation of Bone Marrow-Derived Vascular Progenitor Cell Mobilization and Maintenance. Arterioscler Thromb Vasc Biol 2010;30:1088-93.
192. Ghadge SK, Muhlstedt S, Ozcelik C, Bader M. SDF-1 alpha as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol Ther 2011;129:97-108.
193. Weidt C, Niggemann B, Kasenda B, Drell TL, Zanker KS, Dittmar T. Stem cell migration: a quintessential stepping stone to successful therapy. Curr Stem Cell Res Ther 2007;2:89-103.
194. Yoder MC. Is Endothelium the Origin of Endothelial Progenitor Cells? Arterioscler Thromb Vasc Biol 2010;30:1094-103.
195. Hristov M, Zernecke A, Liehn EA, Weber C. Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost 2007;98:274-7.
196. Kong DL, Melo LG, Gnecchi M, et al. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation 2004;110:2039-46.
197. Werner N, Junk S, Laufs U, et al. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 2003;93:E17-E24.
198. Kawamoto A, Asahara T. Role of progenitor endothelial cells in cardiovascular disease and upcoming therapies. Catheter Cardiovasc Interv 2007;70:477-84.
199. Alev C, Ii M, Asahara T. Endothelial Progenitor Cells: A Novel Tool for the Therapy of Ischemic Diseases. Antioxid Redox Signal 2011;15:949-65.
200. Chavakis E, Koyanagi M, Dimmeler S. Enhancing the Outcome of Cell Therapy for Cardiac Repair Progress From Bench to Bedside and Back. Circulation 2010;121:325-35.
201. 2+ Signalling in Endothelial Progenitor Cells: A Novel Means to Improve Cell-Based Therapy and Impair Tumour Vascularisation. Curr Vasc Pharmacol 2014;12:87-105.
202. Ben-Shoshan J, George J. Endothelial progenitor cells as therapeutic vectors in cardiovascular disorders: From experimental models to human trials. Pharmacol Ther 2007;115:25-36.
203. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008;28:1584-95.
204. Asahara T. Cell therapy and gene therapy using endothelial progenitor cells for vascular regeneration. Handb Exp Pharmacol 2007;(180):181-94.
205. Maeng YS, Choi HJ, Kwon JY, et al. Endothelial progenitor cell homing: prominent role of the IGF2-IGF2R-PLC beta 2 axis. Blood 2009;113:233-43.
206. 2+ mobilizing properties in migrating endothelial cells. Am J Physiol-Heart Circul Physiol 2001;281:H745-H54.
207. 2+ channels. J Biol Chem 2008;283:25296-304.
208. Parekh AB, Putney JW. Store-operated calcium channels. Physiol Rev 2005;85:757-810.
209. 2+ Signals Required for Specific Cell Functions. PLoS Biol 2011;9:13.
210. 2+ Concentration. Stem Cells 2011;29:1898-907.
211. Benameur T, Tual-Chalot S, Andriantsitohaina R, Martinez MC. PPARalpha is essential for microparticle-induced differentiation of mouse bone marrow-derived endothelial progenitor cells and angiogenesis. PLoS One 2010;5:e12392.
212. Troidl C, Nef H, Voss S, et al. Calcium-dependent signalling is essential during collateral growth in the pig hind limbischemia model. J Mol Cell Cardiol 2010;49:142-51.
213. Troidl C, Troidl K, Schierling W, et al. Trpv4 induces collateral vessel growth during regeneration of the arterial circulation. J Cell Mol Med 2009;13:2613-21.
214. Baumgartner I, Isner JM. Somatic gene therapy in the cardiovascular system. Annu Rev Physiol 2001;63:427-50.
215. Gennaro G, Menard C, Michaud SE, Rivard A. Agedependent impairment of reendothelialization after arterial injury-Role of vascular endothelial growth factor. Circulation 2003;107:230-3.
216. Faehling M, Kroll J, Fohr KJ, et al. Essential role of calcium in vascular endothelial growth factor A-induced signaling: mechanism of the antiangiogenic effect of carboxyamidotriazole. FASEB J 2002;16:1805-7.
217. Munaron L, Fiorio Pla A. Calcium influx induced by activation of tyrosine kinase receptors in cultured bovine aortic endothelial cells. J Cell Physiol 2000;185:454-63.
218. 2+-activated K+ channels inhibits proliferation of human endothelial cells induced by basic fibroblast growth factor. J Vasc Res 1998;35:363-71.
219. 2+/Calmodulin-Dependent Protein Kinase II. Invest Ophthalmol Vis Sci 2011;52:3103-11.
220. Yeh HI, Lu SK, Tian TY, Hong RC, Lee WH, Tsai CH. Comparison of endothelial cells grown on different stent materials. J Biomed Mater Res Part A 2006;76A:835-41.
221. De Vuyst E, Boengler K, Antoons G, Sipido KR, Schulz R, Leybaert L. Pharmacological modulation of connexin-formed channels in cardiac pathophysiology. Br J Pharmacol 2011;163:469-83.
222. Dhein S, Hagen A, Jozwiak J, et al. Improving cardiac gap junction communication as a new antiarrhythmic mechanism: the action of antiarrhythmic peptides. Naunyn-Schmiedebergs Arch Pharmacol 2010;381:221-34.
223. Salameh A, Dhein S. Pharmacology of Gap junctions. New pharmacological targets for treatment of arrhythmia, seizure and cancer? Biochim Biophys Acta-Biomembr 2005;1719:36-58.
224. Lewandowski R, Procida K, Vaidyanathan R, et al. RXP-E A Connexin43-Binding Peptide That Prevents Action Potential Propagation Block. Circ Res 2008;103:519-26.
225. Shibayama J, Lewandowski R, Kieken F, et al. Identification of a novel peptide that interferes with the chemical regulation of connexin43. Circ Res 2006;98:1365-72.
226. Verma V, Larsen BD, Coombs W, et al. Novel Pharmacophores of Connexin43 Based on the RXP Series of Cx43-Binding Peptides. Circ Res 2009;105:176-84.
227. Verma V, Larsen BD, Coombs W, et al. Design and characterization of the first peptidomimetic molecule that prevents acidification-induced closure of cardiac gap junctions. Heart Rhythm 2010;7:1491-8.
228. 2+] oscillation patterns in cultured ventricular myocytes of neonatal rats. Toxicol In Vitro 2007;21:1476-85.
229. Bikou O, Thomas D, Trappe K, et al. Connexin 43 gene therapy prevents persistent atrial fibrillation in a porcine model. Cardiovasc Res 2011;92:218-25.
230. Igarashi T, Finet JE, Takeuchi A, et al. Connexin Gene Transfer Preserves Conduction Velocity and Prevents Atrial Fibrillation. Circulation 2012;125:216-25.
231. Greener ID, Sasano T, Wan XP, et al. Connexin43 Gene Transfer Reduces Ventricular Tachycardia Susceptibility After Myocardial Infarction. J Am Coll Cardiol 2012;60:1103-10.
232. Iyer RK, Odedra D, Chiu LLY, Vunjak-Novakovic G, Radisic M. Vascular Endothelial Growth Factor Secretion by Nonmyocytes Modulates Connexin-43 Levels in Cardiac Organoids. Tissue Eng Part A 2012;18:1771-83.
233. Pimentel RC, Yamada KA, Kleber AG, Saffitz JE. Autocrine regulation of myocyte CA3 expression by VEGF. Circ Res 2002;90:671-7.
234. Van Belle E, Bauters C, Asahara T, Isner JM. Endothelial regrowth after arterial injury: from vascular repair to therapeutics. Cardiovasc Res 1998;38:54-68.
235. VanBelle E, Maillard L, Tio FO, Isner JM. Accelerated endothelialization by local delivery of recombinant human vascular endothelial growth factor reduces in-stent intimal formation. Biochem Biophys Res Commun 1997;235:311-6.
236. Yoon YS, Johnson IA, Park JS, Diaz L, Losordo DW. Therapeutic myocardial angiogenesis with vascular endothelial growth factors. Mol Cell Biochem 2004;264:63-74.
237. Iwaguro H, Yamaguchi J, Kalka C, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 2002;105:732-8.
238. Das H, George JC, Joseph M, et al. Stem Cell Therapy with Overexpressed VEGF and PDGF Genes Improves Cardiac Function in a Rat Infarct Model. PLoS One 2009;4:10.
239. Hutter R, Carrick FE, Valdiviezo C, et al. Vascular endothelial growth factor regulates reendothelialization and neointima formation in a mouse model of arterial injury. Circulation 2004;110:2430-5.
240. Walter DH, Cejna M, Diaz-Sandoval L, et al. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents-An alternative strategy for inhibition of restenosis. Circulation 2004;110:36-45.
241. Hedman M, Hartikainen J, Syvanne M, et al. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia-Phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 2003;107:2677-83.
242. Park HJ, Yang F, Cho SW. Nonviral delivery of genetic medicine for therapeutic angiogenesis. Adv Drug Deliv Rev 2012;64:40-52.
243. Swanson N, Hogrefe K, Javed Q, Gershlick AH. In vitro evaluation of vascular endothelial growth factor (VEGF)-eluting stents. Int J Cardiol 2003;92:247-51.
244. Decrock E, Vinken M, De Vuyst E, et al. Connexin-related signaling in cell death: to live or let die? Cell Death Differ 2009;16:524-36.
245. Voelkers M, Salz M, Herzog N, et al. Orai1 and Stim1 regulate normal and hypertrophic growth in cardiomyocytes. J Mol Cell Cardiol 2010;48:1329-34.
246. Wolkowicz PE, Huang J, Umeda PK, et al. Pharmacological evidence for Orai channel activation as a source of cardiac abnormal automaticity. Eur J Pharmacol 2011;668:208-16.
247. McBride W, Lange RA, Hillis LD. Restenosis after successful coronary angioplasty-patho-physiology and prevention. N Engl J Med 1988;318:1734-7.
248. Takeshita S, Isshiki T, Ochiai M, et al. Endotheliumdependent relaxation of collateral microvessels after intramuscular gene transfer of vascular endothelial growth factor in a rat model of hindlimb ischemia. Circulation 1998;98:1261-3.
249. Germani A, Di Campli C, Pompilio G, Biglioli P, Capogrossi MC. Regenerative Therapy in Peripheral Artery Disease. Cardiovasc Ther 2009;27:289-304.