Laminar shear stress regulates mitochondrial dynamics, bioenergetics responses and PRX3 activation in endothelial cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 11, 2014, Pages 2403-2413

  Bretón Romero, Rosa ^a   Acín Perez, Rebeca ^b   Rodríguez Pascual, Fernando ^a   Martínez Molledo, María ^c   Brandes, Ralf P ^d   Rial, Eduardo ^c   Enríquez, José A ^b   Lamas, Santiago ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

Bioenergetics; Fission; Flow; Mechanotransduction; Peroxiredoxins

Indexed keywords

CALCIUM ION; DRP1 PROTEIN; MITOCHONDRIAL PROTEIN; PEROXIREDOXIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOENERGY; BREATHING RATE; CALCIUM CELL LEVEL; CATTLE; CELL ORGANELLE; CONTROLLED STUDY; CYTOSOL; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; INTRACELLULAR SIGNALING; LAMINAR FLOW; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SHEAR STRESS; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

EID: 84905240725     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.07.003     Document Type: Article

References (63)

1. Hoffman B.D., Grashoff C., Schwartz M.A. Dynamic molecular processes mediate cellular mechanotransduction. Nature 2011, 475:316-323.
2. Mann G.E., Yudilevich D.L., Sobrevia L. Regulation of amino acid and glucose transporters in endothelial and smooth muscle cells. Physiol. Rev. 2003, 83:183-252.
3. Culic O., Gruwel M.L., Schrader J. Energy turnover of vascular endothelial cells. Am. J. Physiol. 1997, 273:C205-C213.
4. Groschner L.N., Waldeck-Weiermair M., Malli R., Graier W.F. Endothelial mitochondria-less respiration, more integration. Pflugers Arch. 2012, 464:63-76.
5. Quintero M., Colombo S.L., Godfrey A., Moncada S. Mitochondria as signaling organelles in the vascular endothelium. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5379-5384.
6. Kluge M.A., Fetterman J.L., Vita J.A. Mitochondria and endothelial function. Circ. Res. 2013, 112:1171-1188.
7. Monsalve M., Borniquel S., Valle I., Lamas S. Mitochondrial dysfunction in human pathologies. Front. Biosci. 2007, 12:1131-1153.
8. 2 generation play a key role in flow-mediated dilation in human coronary resistance arteries. Circ. Res. 2003, 93:573-580.
9. Lugus J.J., Ngoh G.A., Bachschmid M.M., Walsh K. Mitofusins are required for angiogenic function and modulate different signaling pathways in cultured endothelial cells. J. Mol. Cell. Cardiol. 2011, 51:885-893.
10. Twig G., Hyde B., Shirihai O.S. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim. Biophys. Acta 2008, 1777:1092-1097.
11. Erusalimsky J.D., Moncada S. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2524-2531.
12. Rajagopalan S., Meng X.P., Ramasamy S., Harrison D.G., Galis Z.S. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J. Clin. Invest. 1996, 98:2572-2579.
13. Kobayashi N., DeLano F.A., Schmid-Schonbein G.W. Oxidative stress promotes endothelial cell apoptosis and loss of microvessels in the spontaneously hypertensive rats. Arterioscler. Thromb. Vasc. Biol. 2005, 25:2114-2121.
14. Sen C.K., Roy S. Redox signals in wound healing. Biochim. Biophys. Acta 2008, 1780:1348-1361.
15. Ruiz-Gines J.A., Lopez-Ongil S., Gonzalez-Rubio M., Gonzalez-Santiago L., Rodriguez-Puyol M., Rodriguez-Puyol D. Reactive oxygen species induce proliferation of bovine aortic endothelial cells. J. Cardiovasc. Pharmacol. 2000, 35:109-113.
16. 2: relevance in inflammation and synergy with TNF-alpha. J. Immunol. 2007, 178:3893-3902.
17. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 2007, 87:245-313.
18. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
19. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 2008, 4:278-286.
20. 2 gradients across biomembranes. FEBS Lett. 2000, 475:121-126.
21. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 2008, 45:549-561.
22. Wood Z.A., Schroder E., Robin Harris J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28:32-40.
23. Breton-Romero R., Gonzalez de Orduna C., Romero N., Sanchez-Gomez F.J., de Alvaro C., Porras A., Rodriguez-Pascual F., Laranjinha J., Radi R., Lamas S. Critical role of hydrogen peroxide signaling in the sequential activation of p38 MAPK and eNOS in laminar shear stress. Free Radic. Biol. Med. 2012, 52:1093-1100.
24. Dewey C.F., Bussolari S.R., Gimbrone M.A., Davies P.F. The dynamic response of vascular endothelial cells to fluid shear stress. J. Biomech. Eng. 1981, 103:177-185.
25. Sanchez-Arago M., Chamorro M., Cuezva J.M. Selection of cancer cells with repressed mitochondria triggers colon cancer progression. Carcinogenesis 2010, 31:567-576.
26. Wu M., Neilson A., Swift A.L., Moran R., Tamagnine J., Parslow D., Armistead S., Lemire K., Orrell J., Teich J., Chomicz S., Ferrick D.A. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 2007, 292:C125-C136.
27. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
28. Vives-Bauza C., Yang L., Manfredi G. Assay of mitochondrial ATP synthesis in animal cells and tissues. Methods Cell Biol. 2007, 80:155-171.
29. Zhang M., Brewer A.C., Schroder K., Santos C.X., Grieve D.J., Wang M., Anilkumar N., Yu B., Dong X., Walker S.J., Brandes R.P., Shah A.M. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18121-18126.
30. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.
31. Cribbs J.T., Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007, 8:939-944.
32. Cereghetti G.M., Stangherlin A., Martins de Brito O., Chang C.R., Blackstone C., Bernardi P., Scorrano L. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15803-15808.
33. Ando J., Komatsuda T., Kamiya A. Cytoplasmic calcium response to fluid shear stress in cultured vascular endothelial cells. In Vitro Cell. Dev. Biol. 1988, 24:871-877.
34. Schwarz G., Callewaert G., Droogmans G., Nilius B. Shear stress-induced calcium transients in endothelial cells from human umbilical cord veins. J. Physiol. 1992, 458:527-538.
35. Jezek P., Plecita-Hlavata L. Mitochondrial reticulum network dynamics in relation to oxidative stress, redox regulation, and hypoxia. Int. J. Biochem. Cell Biol. 2009, 41:1790-1804.
36. Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim. Biophys. Acta 2012, 1817:1833-1838.
37. Giedt R.J., Yang C., Zweier J.L., Matzavinos A., Alevriadou B.R. Mitochondrial fission in endothelial cells after simulated ischemia/reperfusion: role of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 2012, 52:348-356.
38. Jones C.I., Han Z., Presley T., Varadharaj S., Zweier J.L., Ilangovan G., Alevriadou B.R. Endothelial cell respiration is affected by the oxygen tension during shear exposure: role of mitochondrial peroxynitrite. Am. J. Physiol. Cell Physiol. 2008, 295:C180-C191.
39. Han Z., Chen Y.R., Jones C.I., Meenakshisundaram G., Zweier J.L., Alevriadou B.R. Shear-induced reactive nitrogen species inhibit mitochondrial respiratory complex activities in cultured vascular endothelial cells. Am. J. Physiol. Cell Physiol. 2007, 292:C1103-C1112.
40. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
41. Darley-Usmar V. The powerhouse takes control of the cell; the role of mitochondria in signal transduction. Free Radic. Biol. Med. 2004, 37:753-754.
42. Rhee S.G., Chang T.S., Bae Y.S., Lee S.R., Kang S.W. Cellular regulation by hydrogen peroxide. J. Am. Soc. Nephrol. 2003, 14:S211-S215.
43. Mowbray A.L., Kang D.H., Rhee S.G., Kang S.W., Jo H. Laminar shear stress up-regulates peroxiredoxins (PRX) in endothelial cells: PRX 1 as a mechanosensitive antioxidant. J. Biol. Chem. 2008, 283:1622-1627.
44. Gourlay L.J., Bhella D., Kelly S.M., Price N.C., Lindsay J.G. Structure-function analysis of recombinant substrate protein 22kDa (SP-22). A mitochondrial 2-CYS peroxiredoxin organized as a decameric toroid. J. Biol. Chem. 2003, 278:32631-32637.
45. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 2012, 48:158-167.
46. Kuroda J., Ago T., Matsushima S., Zhai P., Schneider M.D., Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15565-15570.
47. Rhee S.G., Kang S.W., Jeong W., Chang T.S., Yang K.S., Woo H.A. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 2005, 17:183-189.
48. Jendrach M., Mai S., Pohl S., Voth M., Bereiter-Hahn J. Short- and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 2008, 8:293-304.
49. Detmer S.A., Chan D.C. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 2007, 8:870-879.
50. Sheridan C., Martin S.J. Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 2010, 10:640-648.
51. Ong S.B., Hausenloy D.J. Mitochondrial morphology and cardiovascular disease. Cardiovasc. Res. 2010, 88:16-29.
52. Soubannier V., McBride H.M. Positioning mitochondrial plasticity within cellular signaling cascades. Biochim. Biophys. Acta 2009, 1793:154-170.
53. Smirnova E., Griparic L., Shurland D.L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12:2245-2256.
54. Santel A., Frank S. Shaping mitochondria: the complex posttranslational regulation of the mitochondrial fission protein DRP1. IUBMB Life 2008, 60:448-455.
55. Kuipers A.J., Middelbeek J., van Leeuwen F.N. Mechanoregulation of cytoskeletal dynamics by TRP channels. Eur. J. Cell Biol. 2012, 91:834-846.
56. Picard M., Shirihai O.S., Gentil B.J., Burelle Y. Mitochondrial morphology transitions and functions: implications for retrograde signaling?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 304:R393-R406.
57. Yu T., Robotham J.L., Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2653-2658.
58. Shigenaga M.K., Hagen T.M., Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10771-10778.
59. Mueller C.F., Laude K., McNally J.S., Harrison D.G. ATVB in focus: redox mechanisms in blood vessels. Arterioscler. Thromb. Vasc. Biol. 2005, 25:274-278.
60. De Keulenaer G.W., Chappell D.C., Ishizaka N., Nerem R.M., Alexander R.W., Griendling K.K. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ. Res. 1998, 82:1094-1101.
61. Chatzizisis Y.S., Coskun A.U., Jonas M., Edelman E.R., Feldman C.L., Stone P.H. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 2007, 49:2379-2393.
62. Kirkinezos I.G., Moraes C.T. Reactive oxygen species and mitochondrial diseases. Semin. Cell Dev. Biol. 2001, 12:449-457.
63. Forman H.J., Davies K.J., Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic. Biol. Med. 2014, 66:24-35.