Endothelial mitochondria regulate the intracellular Ca2+ response to fluid shear stress

American Journal of Physiology - Cell Physiology

Volumn 310, Issue 6, 2016, Pages C479-C490

  Scheitlin, Christopher G ^a   Julian, Justin A ^a   Shanmughapriya, Santhanam ^b   Madesh, Muniswamy ^b   Tsoukias, Nikolaos M ^c   Alevriadou, B Rita ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Florida International University   (United States)

Author keywords

Calcium oscillations; Endothelial cell; Fluid shear stress; Intracellular calcium; Mitochondria

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 7 CHLORO 5 (2 CHLOROPHENYL) 1,5 DIHYDRO 4,1 BENZOTHIAZEPIN 2(3H) ONE; ANTIMYCIN A1; CALCIUM ION; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; LANTHANUM; MEMBRANE PROTEIN; MITOCHONDRIAL CALCIUM ION UNIPORTER; OLIGOMYCIN; PHOSPHOLIPASE C; PHOSPHOLIPASE C INHIBITOR; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CALCIUM;

ARTERY BLOOD FLOW; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; FLUORESCENCE; HUMAN; HUMAN CELL; MECHANOTRANSDUCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OSCILLATION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SHEAR STRESS; CELL CULTURE; CYTOSOL; ENDOPLASMIC RETICULUM; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY; SECOND MESSENGER; VASCULAR ENDOTHELIUM;

CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MITOCHONDRIA; SECOND MESSENGER SYSTEMS; STRESS, MECHANICAL;

EID: 84983651862     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00171.2015     Document Type: Article

References (79)

1. Ando J, Yamamoto K. Flow detection and calcium signaling in vascular endothelial cells. Cardiovasc Res 99: 260–268, 2013.
2. Andrews AM, Jaron D, Buerk DG, Barbee KA. Shear stress-induced NO production is dependent on ATP autocrine signaling and capacitative calcium entry. Cell Mol Bioeng 7: 510–520, 2014.
3. 2+ to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem 276: 29430–29439, 2001.
4. 2+ transients in rat cardiac myocytes: possible mechanisms and role of mitochondria. J Physiol 586: 1379–1397, 2008.
5. 2+ release and the role of mitochondria in rat cardiac myocytes. Ann NY Acad Sci 1123: 58–63, 2008.
6. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 1793: 933–940, 2009.
7. Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11–21, 2000.
8. Bezprozvanny I, Watras J, Ehrlich BE. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351: 751–754, 1991.
9. Cai H, Liu D, Garcia JG. CaM Kinase II-dependent pathophysiological signalling in endothelial cells. Cardiovasc Res 77: 30–34, 2008.
10. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100, 2006.
11. 2+ release is inhibited by mitochondrial depolarization. Biochem J 347: 593–600, 2000.
12. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnoczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174: 915–921, 2006.
13. 2+ exchange inhibitor 7-chloro-5-(2-chlorophenyl)- 1,5-dihydro-4,1-benzothiazepin-2(3H)-one (CGP-37157) in cerebellar granule cells. Biochem Pharmacol 66: 2409–2411, 2003.
14. 2+ affinity aequorin probe. Biochem J 445: 371–376, 2012.
15. dela Paz NG, Melchior B, Shayo FY, Frangos JA. Heparan sulfates mediate the interaction between platelet endothelial cell adhesion molecule- 1 (PECAM-1) and the Galphaq/11 subunits of heterotrimeric G proteins. J Biol Chem 289: 7413–7424, 2014.
16. 2+ in human airway smooth muscle cells. Am J Physiol Cell Physiol 303: C244–C256, 2012.
17. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature 399: 601–605, 1999.
18. 2+ in arterioles in situ: implications for coordination of vascular function. Am J Physiol Heart Circ Physiol 286: H2322–H2331, 2004.
19. Eisner V, Csordas G, Hajnoczky G. Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle–pivotal roles in Ca(2+) and reactive oxygen species signaling. J Cell Sci 126: 2965–2978, 2013.
20. Erb L, Liao Z, Seye CI, Weisman GA. P2 receptors: intracellular signaling. Pflügers Arch 452: 552–562, 2006.
21. 2+-calmodulin-dependent protein kinase II in dorsal root ganglion neurons. J Neurosci 21: 6694–6705, 2001.
22. Filippin L, Magalhaes PJ, Di Benedetto G, Colella M, Pozzan T. Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 278: 39224–39234, 2003.
23. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand 168: 81–88, 2000.
24. Gambillara V, Chambaz C, Montorzi G, Roy S, Stergiopulos N, Silacci P. Plaque-prone hemodynamics impair endothelial function in pig carotid arteries. Am J Physiol Heart Circ Physiol 290: H2320–H2328, 2006.
25. Giedt RJ, Pfeiffer DR, Matzavinos A, Kao CY, Alevriadou BR. Mitochondrial dynamics and motility inside living vascular endothelial cells: Role of bioenergetics. Ann Biomed Eng 52: 348–356, 2012.
26. Gorman MW, Feigl EO, Buffington CW. Human plasma ATP concentration. Clin Chem 53: 318–325, 2007.
27. 2+ signaling: old guests, new functions. Pflügers Arch 455: 375–396, 2007.
28. Gudi S, Nolan JP, Frangos JA. Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc Natl Acad Sci USA 95: 2515–2519, 1998.
29. Han Z, Chen YR, Jones CI, III Meenakshisundaram G, Zweier JL, Alevriadou BR. Shear-induced reactive nitrogen species inhibit mitochondrial respiratory complex activities in cultured vascular endothelial cells. Am J Physiol Cell Physiol 292: C1103–C1112, 2007.
30. Han Z, Varadharaj S, Giedt RJ, Zweier JL, Szeto HH, Alevriadou BR. Mitochondria-derived reactive oxygen species mediate heme oxygenase- 1 expression in sheared endothelial cells. J Pharmacol Exp Ther 329: 94–101, 2009.
31. Helmlinger G, Berk BC, Nerem RM. Calcium responses of endothelial cell monolayers subjected to pulsatile and steady laminar flow differ. Am J Physiol Cell Physiol 269: C367–C375, 1995.
32. 2+ oscillations. Cell Calcium 40: 53–61, 2006.
33. Hoffman NE, Chandramoorthy HC, Shanmughapriya S, Zhang X, Rajan S, Mallilankaraman K, Gandhirajan RK, Vagnozzi RJ, Ferrer LM, Sreekrishnanilayam K, Natarajaseenivasan K, Vallem S, Force T, Choi ET, Cheung JY, Madesh M. MICU1 motifs define mitochondrial calcium uniporter binding and activity. Cell Rep 5: 1576–1588, 2013.
34. Hong D, Jaron D, Buerk DG, Barbee KA. Heterogeneous response of microvascular endothelial cells to shear stress. Am J Physiol Heart Circ Physiol 290: H2498–H2508, 2006.
35. Hsiai TK, Hwang J, Barr ML, Correa A, Hamilton R, Alavi M, Rouhanizadeh M, Cadenas E, Hazen SL. Hemodynamics influences vascular peroxynitrite formation: Implication for low-density lipoprotein apo-B-100 nitration. Free Radic Biol Med 42: 519–529, 2007.
36. 2+]i oscillation frequency regulates agonist-stimulated NF-kappaB transcriptional activity. J Biol Chem 274: 33995–33998, 1999.
37. Hubbard KB, Hepler JR. Cell signalling diversity of the Gqalpha family of heterotrimeric G proteins. Cell Signal 18: 135–150, 2006.
38. 2+ release. Nature 360: 76–78, 1992.
39. 2+ oscillations. EMBO Rep 7: 390–396, 2006.
40. James NL, Harrison DG, Nerem RM. Effects of shear on endothelial cell calcium in the presence and absence of ATP. FASEB J 9: 968–973, 1995.
41. Jones CI 3rd, Han Z, Presley T, Varadharaj S, Zweier JL, Ilangovan G, Alevriadou BR. Endothelial cell respiration is affected by the oxygen tension during shear exposure: role of mitochondrial peroxynitrite. Am J Physiol Cell Physiol 295: C180–C191, 2008.
42. Kim B, Lee H, Kawata K, Park JY. Exercise-mediated wall shear stress increases mitochondrial biogenesis in vascular endothelium. PLoS One 9: e111409, 2014.
43. Kokoska ER, Wolff AB, Smith GS, Miller TA. Epidermal growth factor-induced cytoprotection in human intestinal cells involves intracellular calcium signaling. J Surg Res 88: 97–103, 2000.
44. Kuchan MJ, Frangos JA. Role of calcium and calmodulin in flowinduced nitric oxide production in endothelial cells. Am J Physiol Cell Physiol 266: C628–C636, 1994.
45. Kupzig S, Walker SA, Cullen PJ. The frequencies of calcium oscillations are optimized for efficient calcium-mediated activation of Ras and the ERK/MAPK cascade. Proc Natl Acad Sci USA 102: 7577–7582, 2005.
46. 2+ influx in rat endothelial cells. Circ Res 92: 286–292, 2003.
47. Lemasters JJ, Qian T, He L, Kim JS, Elmore SP, Cascio WE, Brenner DA. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal 4: 769–781, 2002.
48. Li R, Beebe T, Cui J, Rouhanizadeh M, Ai L, Wang P, Gundersen M, Takabe W, Hsiai TK. Pulsatile shear stress increased mitochondrial membrane potential: implication of Mn-SOD. Biochem Biophys Res Commun 388: 406–412, 2009.
49. Liu B, Lu S, Zheng S, Jiang Z, Wang Y. Two distinct phases of calcium signalling under flow. Cardiovasc Res 91: 124–133, 2011.
50. 2+ store refilling. J Biol Chem 278: 44769–44779, 2003.
51. 2+ refilling of the endoplasmic reticulum. J Biol Chem 280: 12114–12122, 2005.
52. 2+ signals in cochlear supporting cells. Cell Calcium 46: 136–146, 2009.
53. Markoulaki S, Matson S, Ducibella T. Fertilization stimulates longlasting oscillations of CaMKII activity in mouse eggs. Dev Biol 272: 15–25, 2004.
54. 2+ influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol 298: H466–H776, 2010.
55. 2+ signaling. EMBO J 20: 1674–1680, 2001.
56. 2+ signaling of vascular endothelial cells: effect of shear stress and ATP. Am J Physiol Heart Circ Physiol 260: H1698–H1707, 1991.
57. Nollert MU, Eskin SG, McIntire LV. Shear stress increases inositol trisphosphate levels in human endothelial cells. Biochem Biophys Res Commun 170: 281–287, 1990.
58. 2+ oscillations. Trends Biochem Sci 36: 78–87, 2011.
59. + currents in bovine aortic endothelial cells. Pflügers Arch 443: 344–352, 2002.
60. Patil VV, Kulkarni HV. Comparison of confidence intervals for the Poisson mean: some new aspects. REVSTAT Stat J 10: 211–227, 2012.
61. 2+) mobilization, membrane hyperpolarization and nitric oxide production in human vascular endothelial cells. Cell Calcium 49: 240–248, 2011.
62. Rizzuto R, De Stefani D, Raffaello A, Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13: 566–578, 2012.
63. 2+ responses. Science 280: 1763–1766, 1998.
64. Salazar C, Politi AZ, Hofer T. Decoding of calcium oscillations by phosphorylation cycles: analytic results. Biophys J 94: 1203–1215, 2008.
65. 2+-dependent gene expression in response to receptor stimulation. PLoS One 9: e101188, 2014.
66. Shen J, Luscinskas FW, Connolly A, Dewey CF, Gimbrone MA. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am J Physiol Cell Physiol 262: C384–C390, 1992.
67. 2+ signaling and apoptosis. J Bioenerg Biomembr 32: 35–46, 2000.
68. Smedler E, Uhlen P. Frequency decoding of calcium oscillations. Biochim Biophys Acta 1840: 964–969, 2014.
69. 2+ signaling in endothelial cell tubes of mouse resistance arteries. Microcirculation 19: 757–770, 2012.
70. Takabe W, Jen N, Ai L, Hamilton R, Wang S, Holmes K, Dharbandi F, Khalsa B, Bressler S, Barr ML, Li R, Hsiai TK. Oscillatory shear stress induces mitochondrial superoxide production: implication of NADPH oxidase and c-Jun NH2-terminal kinase signaling. Antioxid Redox Signal 15: 1379–1388, 2011.
71. Uhlen P, Fritz N. Biochemistry of calcium oscillations. Biochem Biophys Res Commun 396: 28–32, 2010.
72. 2+ uniporter stimulation. J Physiol 580: 39–49, 2007.
73. Walsh C, Barrow S, Voronina S, Chvanov M, Petersen OH, Tepikin A. Modulation of calcium signalling by mitochondria. Biochim Biophys Acta 1787: 1374–1382, 2009.
74. Wang C, Baker BM, Chen CS, Schwartz MA. Endothelial cell sensing of flow direction. Arterioscler Thromb Vasc Biol 33: 2130–216, 2013.
75. Wang S, Iring A, Strilic B, Albarran Juarez J, Kaur H, Troidl K, Tonack S, Burbiel JC, Muller CE, Fleming I, Lundberg JO, Wettschureck N, Offermanns S. P2Y(2) and Gq/G(11) control blood pressure by mediating endothelial mechanotransduction. J Clin Invest 125: 3077–3086, 2015.
76. 2+ waves at caveolae in vascular endothelial cells. J Cell Sci 124: 3477–3483, 2011.
77. 2+ influx into human endothelial cells via P2X4 purinoceptors. Circ Res 87: 385–391, 2000.
78. Yeh LH, Park YJ, Hansalia RJ, Ahmed IS, Deshpande SS, Goldschmidt- Clermont PJ, Irani K, Alevriadou BR. Shear-induced tyrosine phosphorylation in endothelial cells requires Rac1-dependent production of ROS. Am J Physiol Cell Physiol 276: C838–C847, 1999.
79. 2+ oscillation frequency regulates agonist-stimulated gene expression in vascular endothelial cells. J Cell Sci 121: 2511–2518, 2008.