A novel mechanism of γ/σ T-lymphocyte and endothelial activation by shear stress: The role of ecto-ATP synthase β chain

Circulation Research

Volumn 108, Issue 4, 2011, Pages 410-417

  Fu, Yi ^a,b   Hou, Yingjian ^a   Fu, Chenglai ^a   Gu, Mingxia ^a   Li, Chenghong ^a   Kong, Wei ^a   Wang, Xian ^a   Shyy, John Y J ^b   Zhu, Yi ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ATP synthase; blood flow; endothelial dysfunction; mechanotransduction; T lymphocyte

Indexed keywords

ANTIBODY; APOLIPOPROTEIN E; CHOLESTEROL; GAMMA INTERFERON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LAMINAR FLOW; LIPID DIET; LYMPHOCYTE ACTIVATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT; CAVEOLIN 1; CELL ADHESION; CELL COMMUNICATION; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; ENDOTHELIUM, VASCULAR; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, ANIMAL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; STRESS, MECHANICAL; T-LYMPHOCYTES;

EID: 79952071002     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.230151     Document Type: Article

References (32)

1. Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med. 2009;6:16-26.
2. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol. 2007;292: H1209-H1224. (Pubitemid 46377111)
3. Chien S. Effects of disturbed flow on endothelial cells. Ann Biomed Eng. 2008;36:554-562.
4. Champagne E, Martinez LO, Collet X, Barbaras R. Ecto-F1Fo ATP synthase/F1 ATPase: metabolic and immunological functions. Curr Opin Lipidol. 2006;17:279-284. (Pubitemid 43786062)
5. Martinez LO, Jacquet S, Esteve JP Rolland C, Cabezón E, Champagne E, Pineau T, Georgeaud V, Walker JE, Tercé F, Collet X, Perret B, Barbaras R. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature. 2003;421:75-79. (Pubitemid 36077087)
6. Beisiegel U, Weber W, Havinga JR, Ihrke G, Hui DY, Wernette-Hammond ME, Turck CW, Innerarity TL, Mahley RW. Apolipoprotein E-binding proteins isolated from dog and human liver. Arteriosclerosis. 1988;8:288-297.
7. Mahley RW, Hui DY, Innerarity TL, Beisiegel U. Chylomicron remnant metabolism. Role of hepatic lipoprotein receptors in mediating uptake. Arteriosclerosis. 1989;9(1 Suppl):I-14-I-18.
8. Moser TL, Kenan DJ, Ashley TA, Roy JA, Goodman MD, Misra UK, Cheek DJ, Pizzo SV. Endothelial cell surface F1-F0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc Natl Acad Sci U S A. 2001;98:6656-6661. (Pubitemid 32538272)
9. Moser TL, Stack MS, Asplin I, Enghild JJ, Højrup P, Everitt L, Hubchak S, Schnaper HW, Pizzo SV. Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc Natl Acad Sci U S A. 1999;96: 2811-2816. (Pubitemid 29148800)
10. Burwick NR, Wahl ML, Fang J, Zhong Z, Moser TL, Li B, Capaldi RA, Kenan DJ, Pizzo SV. An Inhibitor of the F1 subunit of ATP synthase (IF1) modulates the activity of angiostatin on the endothelial cell surface. J Biol Chem. 2005;280:1740-1745.
11. Wang T, Chen Z, Wang X, Shyy JY, Zhu Y. Cholesterol loading increases the translocation of ATP synthase beta chain into membrane caveolae in vascular endothelial cells. Biochim Biophys Acta. 2006;1761: 1182-1190. (Pubitemid 44540261)
12. Scotet E, Martinez LO, Grant E, Barbaras R, Jenö P, Guiraud M, Monsarrat B, Saulquin X, Maillet S, Estève JP, Lopez F, Perret B, Collet X, Bonneville M, Champagne E. Tumor recognition following Vgamma9Vdelta2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity. 2005;22:71-80. (Pubitemid 40143452)
13. Glass CK, Witztum JL. Atherosclerosis. the road ahead. Cell. 2001;104: 503-516.
14. Rader DJ, Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature. 2008;451:904-913. (Pubitemid 351301745)
15. Wick G, Knoflach M, Xu Q. Autoimmune and inflammatory mechanisms in atherosclerosis. Annu Rev Immunol. 2004;22:361-403. (Pubitemid 38680427)
16. Galea P, Brezinschek R, Lipsky PE, Oppenheimer-Marks N. Phenotypic characterization of CD4-/alpha beta TCR+ and gamma delta TCR+ T cells with a transendothelial migratory capacity. J Immunol. 1994;153: 529-542.
17. Dyugovskaya L, Lavie P, Lavie L. Phenotypic and functional characterization of blood gammadelta T cells in sleep apnea. Am J Respir Crit Care Med. 2003;168:242-249. (Pubitemid 36920981)
18. Zhu M, Fu Y, Hou Y, Wang N, Guan Y, Tang C, Shyy JY, Zhu Y. Laminar shear stress regulates liver X receptor in vascular endothelial cells. Arterioscler Thromb Vasc Biol. 2008;28:527-533.
19. Frangos JA, Eskin SG, McIntire LV, Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science. 1985; 227:1477-1479. (Pubitemid 15146990)
20. Guo D, Chien S, Shyy JY. Regulation of endothelial cell cycle by laminar versus oscillatory flow: distinct modes of interactions of AMP-activated protein kinase and Akt pathways. Circ Res. 2007;100:564-571. (Pubitemid 46673266)
21. Laufs U, Liao JK. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem. 1998;273: 24266-24271. (Pubitemid 28435775)
22. Zhu Y, Liao HL, Wang N, Yuan Y, Ma KS, Verna L, Stemerman MB. Lipoprotein promotes caveolin-1 and Ras translocation to caveolae: role of cholesterol in endothelial signaling. Arterioscler Thromb Vasc Biol. 2000;20:2465-2470.
23. Gonzalez E, Nagiel A, Lin AJ, Golan DE, Michel T. Small interfering RNA-mediated down-regulation of caveolin-1 differentially modulates signaling pathways in endothelial cells. J Biol Chem. 2004;279: 40659-40669. (Pubitemid 39287660)
24. Schilbach K, Geiselhart A, Handgretinger R. Induction of proliferation and augmented cytotoxicity of gammadelta T lymphocytes by bisphosphonate clodronate. Blood. 2001;97:2917-2918.
25. Iiyama K, Hajra L, Iiyama M, Li H, DiChiara M, Medoff BD, Cybulsky MI. Patterns of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 expression in rabbit and mouse atherosclerotic lesions and at sites predisposed to lesion formation. Circ Res. 1999;85: 199-207. (Pubitemid 29343319)
26. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol. 2009;297:H1535-H1543.
27. Nakashima Y, Raines EW, Plump AS, Breslow JL, Ross R. Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler Thromb Vasc Biol. 1998; 18:842-851. (Pubitemid 28267666)
28. Stannard AK, Riddell DR, Sacre SM, Tagalakis AD, Langer C, von Eckardstein A, Cullen P, Athanasopoulos T, Dickson G, Owen JS. Cell-derived apolipoprotein E (ApoE) particles inhibit vascular cell adhesion molecule-1 (VCAM-1) expression in human endothelial cells. J Biol Chem. 2001;276:46011-46016.
29. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP. Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vasc Biol. 2007;27:346-351. (Pubitemid 46143050)
30. Yamamoto K, Shimizu N, Obi S, Kumagaya S, Taketani Y, Kamiya A, Ando J. Involvement of cell surface ATP synthase in flow-induced ATP release by vascular endothelial cells. Am J Physiol Heart Circ Physiol. 2007;293:H1646-H1653. (Pubitemid 47367211)
31. Wick G, Romen M, Amberger A, Metzler B, Mayr M, Falkensammer G, Xu Q. Atherosclerosis, autoimmunity, and vascular-associated lymphoid tissue. FASEB J. 1997;11:1199-1207. (Pubitemid 27481444)
32. Vantourout P, Martinez LO, Fabre A, Collet X, Champagne E. Ecto-F1-ATPase and MHC-class I close association on cell membranes. Mol Immunol. 2008;45:485-492. (Pubitemid 47332634)