Shear stress is a positive regulator of thimet oligopeptidase (EC3.4.24.15) in vascular endothelial cells: Consequences for MHC1 levels

Cardiovascular Research

Volumn 99, Issue 3, 2013, Pages 545-554

  Guinan, Anthony F ^a   Rochfort, Keith D ^a   Fitzpatrick, Paul A ^a,c   Walsh, Tony G ^a   Pierotti, Adrian R ^b   Phelan, Susan ^a   Murphy, Ronan P ^a   Cummins, Philip M ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b GLASGOW CALEDONIAN UNIVERSITY   (United Kingdom)

^c Sahlgrenska Cancer Center   (Sweden)

Author keywords

Endothelium; MHC1; NADPH oxidase; Shear stress; Thimet oligopeptidase

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; ACETYLCYSTEINE; APOCYNIN; CATALASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; SUPEROXIDE DISMUTASE; THIMET OLIGOPEPTIDASE; HLA ANTIGEN CLASS 1; METALLOPROTEINASE; NOX4 PROTEIN, HUMAN;

ANIMAL CELL; ANTIGEN PRESENTATION; AORTA; ARTICLE; BOVINE AORTIC ENDOTHELIAL CELL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HEMODYNAMICS; HUMAN; HUMAN AORTIC ENDOTHELIAL CELL; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LAMINAR FLOW; LUCIFERASE ASSAY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SHEAR STRESS; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANIMAL; CATTLE; CELL CULTURE; ENDOTHELIUM; GENETICS; IMMUNOLOGY; MECHANICAL STRESS; METABOLISM; MHC1; PHYSIOLOGY; RAT; SHEAR STRENGTH; BOVINAE;

ENDOTHELIUM; MHC1; NADPH OXIDASE; SHEAR STRESS; THIMET OLIGOPEPTIDASE;

ANIMALS; CATTLE; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; METALLOENDOPEPTIDASES; NADPH OXIDASE; PROMOTER REGIONS, GENETIC; RATS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SHEAR STRENGTH; STRESS, MECHANICAL;

EID: 84894468274     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt127     Document Type: Article

References (54)

1. Barrett AJ, Rawlings ND, O'Brien EA. The MEROPS database as a protease information system. J Struct Biol 2001;134:95-102.
2. Shrimpton CN, Smith AI, Lew RA. Soluble metalloendopeptidases and neuroendocrine signaling. Endocr Rev 2002;23:647-664.
3. Jeske NA, Glucksman MJ, Roberts JL. Metalloendopeptidase EC3.4.24.15 is constitutively released from the exofacial leaflet of lipid rafts in GT1-7 cells. J Neurochem 2004;90: 819-828.
4. Crack PJ, WuTJ, Cummins PM, Ferro ES, TullaiJW, Glucksman MJ et al. The association of metalloendopeptidase EC3.4.24.15 at the extracellular surface of the AtT-20 plasma membrane. Brain Res 1999;835:113-122.
5. Russo LC, Goñi CN, Castro LM, Asega AF, Camargo AC, Trujillo CA et al. Interaction with calmodulin is important for the secretion of thimet oligopeptidase following stimulation. FEBS J 2009;276:4358-4371.
6. Norman MU, Lew RA, Smith I, Hickey MJ. Metalloendopeptidases EC3.4.24.15/16 regulate bradykinin activity in the cerebral microvasculature. Am J Physiol Heart Circ Physiol 2003;284:H1942-H1948.
7. Rioli V, Gozzo FC, Heimann AS, Linardi A, Krieger JE, Shida CS et al. Novel natural peptide substrates for endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme. J Biol Chem 2003;278:8547-8555.
8. Wu TJ, Pagano E, Mani SK. A biological role for the gonadotrophin-releasing hormone (GnRH) metabolite, GnRH-(1-5). J Neuroendocrinol 2009;21:293-298.
9. Ferrario CM, Iyer SN. Angiotensin-(1-7): a bioactive fragment of the renin-angiotensin system. Regul Pept 1998;78:13-18.
10. Santos RA, Brosnihan KB, Jacobsen DW, Dicorleto PE, Ferrario CM. Production of angiotensin-(1-7) by human vascular endothelium. Hypertension 1992;19:1156-1161.
11. Chappell MC, Gomez MN, Pirro NT, Ferrario CM. Release of angiotensin-(1-7) from the rat hindlimb: influence of angiotensin-converting enzyme inhibition. Hypertension 2000;35:348-352.
12. Ferrario CM.ACE2: more of Ang-(1-7) or less Ang II?. Curr OpinNephrol Hypertens 2011; 20:1-6.
13. Tesanovic S, Vinh A, Gaspari TA, Casley D, Widdop RE. Vasoprotective and atheroprotective effects of angiotensin-(1-7) in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2010;30:1606-1163.
14. Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 1998;18:677-685.
15. Shinoki N, Kawasaki T, Minamino N, Okahara K, Ogawa A, Ariyoshi H et al. Shear stress down-regulates gene transcription and production of adrenomedullin in human aortic endothelial cells. J Cell Biochem 1998;71:109-115.
16. Fitzpatrick PA, Guinan AF, Walsh TG, Murphy RP, Killeen MT, Tobin NP et al. Downregulation of neprilysin expression in vascular endothelial cells by laminar shear stress involves NADPH oxidase-dependent ROS production. Int J Biochem Cell Biol 2009;41: 2287-2294.
17. Rieder MJ, Carmona R, Krieger JE, Pritchard KA, Greene AS. Suppression of angiotensinconverting enzyme expression and activity by shear stress. Circ Res 1997;80:312-319.
18. Masatsugu K, Itoh H, Chun TH, Saito T, Yamashita J, Doi K et al. Shear stress attenuates endothelin and endothelin-converting enzyme expression through oxidative stress. Regul Pept 2003;111:13-19.
19. Smith PK, Krohn RI, HermansonGT, Mallia AK, Gartner FH, ProvenzanoMDet al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985;150:76-85.
20. Walsh TG, Murphy RP, Fitzpatrick P, Rochfort KD, Guinan AF, Murphy A et al. Stabilization of brain microvascular endothelial barrier function by shear stress involves VE-cadherin signaling leading to modulation of pTyr-occludin levels. J Cell Physiol 2011; 226:3053-3063.
21. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156-159.
22. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
23. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979;76:4350-4354.
24. Morrison LS, Pierotti AR. Thimet oligopeptidase expression is differentially regulated in neuroendocrine and spermatid cell lines by transcription factor binding to SRY (sexdetermining region Y), CAAT and CREB (cAMP-response-element-binding protein) promoter consensus sequences. Biochem J 2003;376:189-197.
25. Godbole AS, Lu X, Guo X, Kassab GS. NADPH oxidase has a directional response to shear stress. Am J Physiol Heart Circ Physiol 2009;296:H152-H158.
26. Johnson DK, Schillinger KJ, Kwait DM, Hughes CV, McNamara EJ, Ishmael F et al. Inhibition of NADPH oxidase activation in endothelial cells by ortho-methoxy-substituted catechols. Endothelium 2002;9:191-203.
27. Miyano K, Sumimoto H. Role of the small GTPase Rac in p22phox-dependent NADPH oxidases. Biochimie 2007;89:1133-1144.
28. Dworakowski R, Alom-Ruiz SP, Shah AM. NADPH oxidase-derived reactive oxygen species in the regulation of endothelial phenotype. Pharmacol Rep 2008;60:21-28.
29. Cotter EJ, vonOffenberg SweeneyN, CoenPM, Birney YA, Glucksman MJ, CahillPAet al. Regulation of endopeptidases EC3.4.24.15 and EC3.4.24.16 in vascular endothelial cells by cyclic strain: role of Gi protein signaling. Arterioscler Thromb Vasc Biol 2004;24: 457-463.
30. Chen K, Keaney J. Reactive oxygen species-mediated signal transduction in the endothelium. Endothelium 2004;11:109-121.
31. Lehoux S. Redoxsignaling in vascular responses to shear and stretch. Cardiovasc Res 2006; 71:269-279.
32. Benrahmoune M, Thérond P, Abedinzadeh Z. The reaction of superoxide radical with N-acetylcysteine. Free Radic Biol Med 2000;29:775-782.
33. Griendling KK, Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 2000;91:21-27.
34. Hahn C, Schwartz MA. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009;10:53-62.
35. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phox-dependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 2005;97:533-540.
36. Duerrschmidt N, Stielow C, Muller G, Pagano PJ, Morawietz H.NO-mediated regulation of NAD(P)H oxidase by laminar shear stress in human endothelial cells. J Physiol 2006; 576:557-567.
37. Bäumer AT, Ten Freyhaus H, Sauer H, Wartenberg M, Kappert K, Schnabel P et al. Phosphatidylinositol 3-kinase-dependent membrane recruitment of Rac-1 and p47phox is critical for alpha-platelet-derived growth factor receptor-induced production of reactive oxygen species. J Biol Chem 2008;283:7864-7876.
38. Bian H, Reed EF. Alloantibody-mediated class I signal transduction in endothelial cells and smooth muscle cells: enhancement by IFN-gamma and TNF-alpha. J Immunol 1999;163: 1010-1018.
39. Foglieni C, Maisano F, Dreas L, Giazzon A, Ruotolo G, Ferrero E et al. Mild inflammatory activation of mammary arteries in patients with acute coronary syndromes. Am J Physiol Heart Circ Physiol 2008;294:H2831-H2837.
40. Firner S, Onder L, Nindl V, Ludewig B. Tight control-decision-making during T cellvascular endothelial cell interaction. Front Immunol 2012;3:1-6.
41. Doebis C, Schu S, Ladhoff J, Busch A, Beyer F, Reiser J et al. An anti-major histocompatibility complex class I intrabody protects endothelial cells from an attack by immune mediators. Cardiovasc Res 2006;72:331-338.
42. SaricT, Beninga J, Graef CI, AkopianTN, Rock KL, Goldberg AL. Major histocompatibility complex class I-presented antigenic peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J Biol Chem 2001;276:36474-36481.
43. Kessler JH, Khan S, Seifert U, Le Gall S, ChowKM, PaschenA et al. Antigen processing by nardilysin and thimet oligopeptidase generates cytotoxic T cell epitopes. Nat Immunol 2011;12:45-53.
44. Rock KL, York IA, Goldberg AL. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat Immunol 2004;5:670-677.
45. Kim SI, Pabon A, SwansonTA, Glucksman MJ. Regulation of cell-surfacemajor histocompatibility complex class I expression by the endopeptidase EC3.4.24.15 (thimet oligopeptidase). Biochem J 2003;375:111-120.
46. Tsai YC, Hsieh HJ, Liao F, Ni CW, Chao YJ, Hsieh CY et al. Laminar flow attenuates interferon-induced inflammatory responses in endothelial cells. Cardiovasc Res 2007; 74:497-505.
47. York IA, Mo AX, Lemerise K, ZengW, Shen Y, Abraham CR et al. The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 2003;18:429-440.
48. Resnick N, Collins T, AtkinsonW, Bonthron DT, Dewey CF Jr, GimbronMAJr. Plateletderived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc Natl Acad Sci USA 1993;90:4591-4595.
49. MiyakawaAA, de Lourdes JunqueiraM, Krieger JE. Identification oftwo novel shear stress responsive elements in rat angiotensin I converting enzyme promoter. Physiol Genomics 2004;17:107-113.
50. Ohno M, Cooke JP, Dzau VJ, Gibbons GH. Fluid shear stress induces endothelial transforming growth factor beta-1 transcription and production: modulation by potassium channel blockade. J Clin Invest 1995;95:1363-1369.
51. Mahmoudi T, Katsani KR, Verrijzer CP.GAGAcan mediate enhancer function in trans by linking two separate DNA molecules. EMBO J 2002;21:1775-1781.
52. Goettsch C, GoettschW, Brux M, Haschke C, Brunssen C, Muller G et al. Arterial flow reduces oxidative stress via an antioxidant response element and Oct-1 binding site within the NADPH oxidase 4 promoter in endothelial cells. Basic Res Cardiol 2011; 106:551-561.
53. SenBanerjee S, Lin Z, Atkins GB, Greif DM, Rao RM, Kumar A et al. KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med 2004;199: 1305-1315.
54. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408.