J Korean Soc Hypertens.  2011 Dec;17(4):133-147. 10.5646/jksh.2011.17.4.133.

Cyclophilin A: A Mediator of Cardiovascular Pathology

Affiliations
  • 1Aab Cardiovascular Research Institute and Department of Medicine, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA. bradford_berk@urmc.rochester.edu

Abstract

Cyclophilin A (CyPA) is a 17 kDa, ubiquitously expressed multifunctional protein that possesses peptidylprolyl cis-trans isomerase activity and scaffold function. Its expression is increased in inflammatory conditions including rheumatoid arthritis, autoimmune disease and cancer. Intracellular CyPA regulates protein trafficking, signal transduction, transcription regulation and the activity of certain other proteins. Secreted CyPA activates cardiovascular cells resulting in a variety of cardiovascular diseases; including vascular remodeling, abdominal aortic aneurysms formation, atherosclerosis, cardiac hypertrophy and myocardial ischemic reperfusion injury.

Keyword

Cyclophilin A; Oxidative stress; Cardiovascular diseases

MeSH Terms

Aortic Aneurysm, Abdominal
Arthritis, Rheumatoid
Atherosclerosis
Autoimmune Diseases
Cardiomegaly
Cardiovascular Diseases
Cyclophilin A
Cyclophilins
Myocardial Reperfusion Injury
Oxidative Stress
Protein Transport
Proteins
Quaternary Ammonium Compounds
Signal Transduction
Cyclophilin A
Cyclophilins
Proteins
Quaternary Ammonium Compounds

Figure

  • Fig. 1. Cyclophilin A (CyPA) effects on vascular smooth muscle (VSMC), endothelial cells (EC) and T cells. VCAM-1, vascular cell adhesion molecule-1; IFN, interferon; IL, interleukin.

  • Fig. 2. Immune modulation of T cell function. (A) Th2 inhibits Th1 responses. (B) T regs regulate both Th1 and Th2 responses. IFN, interferon; IL, interleukin; TGF, transforming growth factor.

  • Fig. 3. Mechanism of cyclophilin A (CyPA) regulation on cardiovascular cells. ROS, reactive oxygen species; VSMC, vascular smooth muscle; EC, endothelial cells.


Reference

References

1. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003; 42:1075–81.
2. Griendling KK, Ushio-Fukai M. Redox control of vascular smooth muscle proliferation. J Lab Clin Med. 1998; 132:9–15.
Article
3. Berk BC. Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells. Circulation. 2008; 117:1082–9.
Article
4. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994; 74:1141–8.
Article
5. Frey RS, Masuko U-F, Malik AB. Forum review NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid Redox Signal. 2009; 11:791–810.
6. Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, et al. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROS-PK Cepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med. 2008; 45:1223–31.
7. Birukov KG. Cyclic stretch, reactive oxygen species, and vascular remodeling. Antioxid Redox Signal. 2009; 11:1651–67.
Article
8. Marks AR. Cellular functions of immunophilins. Physiol Rev. 1996; 76:631–49.
Article
9. Ryffel B, Woerly G, Greiner B, Haendler B, Mihatsch MJ, Foxwell BM. Distribution of the cyclosporine binding protein cyclophilin in human tissues. Immunology. 1991; 72:399–404.
10. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science. 1984; 226:544–7.
Article
11. Takahashi N, Hayano T, Suzuki M. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature. 1989; 337:473–5.
Article
12. Schreiber SL. Chemistry and biology of the im-munophilins and their immunosuppressive ligands. Science. 1991; 251:283–7.
Article
13. Zhu C, Wang X, Deinum J, Huang Z, Gao J, Modjtahedi N, et al. Cyclophilin A participates in the nuclear translocation of apoptosis-inducing factor in neurons after cerebral hypoxia-ischemia. J Exp Med. 2007; 204:1741–8.
Article
14. Brazin KN, Mallis RJ, Fulton DB, Andreotti AH. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc Natl Acad Sci U S A. 2002; 99:1899–904.
Article
15. Colgan J, Asmal M, Neagu M, Yu B, Schneidkraut J, Lee Y, et al. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity. 2004; 21:189–201.
Article
16. Krummrei U, Bang R, Schmidtchen R, Brune K, Bang H. Cyclophilin-A is a zinc-dependent DNA binding protein in macrophages. FEBS Lett. 1995; 371:47–51.
Article
17. Walter DH, Haendeler J, Galle J, Zeiher AM, Dimmeler S. Cyclosporin A inhibits apoptosis of human endothelial cells by preventing release of cytochrome C from mitochondria. Circulation. 1998; 98:1153–7.
Article
18. Jonasson L, Holm J, Hansson GK. Cyclosporin A inhibits smooth muscle proliferation in the vascular response to injury. Proc Natl Acad Sci U S A. 1988; 85:2303–6.
Article
19. Gregory CR, Huang X, Pratt RE, Dzau VJ, Shorthouse R, Billingham ME, et al. Treatment with rapamycin and mycophenolic acid reduces arterial intimal thickening produced by mechanical injury and allows endothelial replacement. Transplantation. 1995; 59:655–61.
Article
20. Andersen HO, Hansen BF, Holm P, Stender S, Nordestgaard BG. Effect of cyclosporine on arterial balloon injury lesions in cholesterol-clamped rabbits: T lymphocyte-mediated immune responses not involved in balloon injury-induced neointimal proliferation. Arterioscler Thromb Vasc Biol. 1999; 19:1687–94.
21. Ferns G, Reidy M, Ross R. Vascular effects of cyclosporine A in vivo and in vitro. Am J Pathol. 1990; 137:403–13.
22. Jin ZG, Lungu AO, Xie L, Wang M, Wong C, Berk BC. Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler Thromb Vasc Biol. 2004; 24:1186–91.
Article
23. Jin ZG, Melaragno MG, Liao DF, Yan C, Haendeler J, Suh YA, et al. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res. 2000; 87:789–96.
Article
24. Satoh K, Matoba T, Suzuki J, O’Dell MR, Nigro P, Cui Z, et al. Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation. 2008; 117:3088–98.
Article
25. Sun J, Hemler ME. Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metal-loproteinase inducer interactions. Cancer Res. 2001; 61:2276–81.
26. Pushkarsky T, Zybarth G, Dubrovsky L, Yurchenko V, Tang H, Guo H, et al. CD147 facilitates HIV-1 infection by interacting with virus-associated cyclophilin A. Proc Natl Acad Sci U S A. 2001; 98:6360–5.
Article
27. Damsker JM, Bukrinsky MI, Constant SL. Preferential chemotaxis of activated human CD4+ T cells by extracellular cyclophilin A. J Leukoc Biol. 2007; 82:613–8.
28. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 2000; 6:435–42.
Article
29. Pakula R, Melchior A, Denys A, Vanpouille C, Mazurier J, Allain F. Syndecan-1/CD147 association is essential for cyclophilin B-induced activation of p44/42 mitogen- activated protein kinases and promotion of cell adhesion and chemotaxis. Glycobiology. 2007; 17:492–503.
30. Hanoulle X, Melchior A, Sibille N, Parent B, Denys A, Wieruszeski JM, et al. Structural and functional characterization of the interaction between Cyclophilin B and a heparin-derived oligosaccharide. J Biol Chem. 2007; 282:34148–58.
Article
31. Binder RJ, Han DK, Srivastava PK. CD91: a receptor for heat shock protein gp96. Nat Immunol. 2000; 1:151–5.
Article
32. Pushkarsky T, Yurchenko V, Laborico A, Bukrinsky M. CD147 stimulates HIV-1 infection in a signal-in-dependent fashion. Biochem Biophys Res Commun. 2007; 363:495–9.
Article
33. Suzuki J, Jin ZG, Meoli DF, Matoba T, Berk BC. Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ Res. 2006; 98:811–7.
Article
34. Colgan J, Asmal M, Yu B, Luban J. Cyclophilin A-deficient mice are resistant to immunosuppression by cyclosporine. J Immunol. 2005; 174:6030–8.
Article
35. Miller AT, Wilcox HM, Lai Z, Berg LJ. Signaling through Itk promotes T helper 2 differentiation via negative regulation of T-bet. Immunity. 2004; 21:67–80.
Article
36. Zhou X, Stemme S, Hansson GK. Evidence for a local immune response in atherosclerosis. CD4+ T cells infiltrate lesions of apolipoprotein-E-deficient mice. Am J Pathol. 1996; 149:359–66.
37. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005; 352:1685–95.
Article
38. Xu Q. Role of heat shock proteins in atherosclerosis. Arterioscler Thromb Vasc Biol. 2002; 22:1547–59.
Article
39. Al-Daraji WI, Grant KR, Ryan K, Saxton A, Reynolds NJ. Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J Invest Dermatol. 2002; 118:779–88.
Article
40. Arevalo-Rodriguez M, Heitman J. Cyclophilin A is localized to the nucleus and controls meiosis in Saccharomyces cerevisiae. Eukaryot Cell. 2005; 4:17–29.
41. Pan H, Luo C, Li R, Qiao A, Zhang L, Mines M, et al. Cyclophilin A is required for CXCR4-mediated nuclear export of heterogeneous nuclear ribonucleoprotein A2, activation and nuclear translocation of ERK1/2, and chemotactic cell migration. J Biol Chem. 2008; 283:623–37.
Article
42. Sherry B, Yarlett N, Strupp A, Cerami A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci U S A. 1992; 89:3511–5.
Article
43. Rietschel ET, Schletter J, Weidemann B, El-Samalouti V, Mattern T, Zahringer U, et al. Lipopolysaccharide and peptidoglycan: CD14-dependent bacterial inducers of inflammation. Microb Drug Resist. 1998; 4:37–44.
Article
44. Fujihara M, Muroi M, Tanamoto K, Suzuki T, Azuma H, Ikeda H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol Ther. 2003; 100:171–94.
Article
45. Billich A, Winkler G, Aschauer H, Rot A, Peichl P. Presence of cyclophilin A in synovial fluids of patients with rheumatoid arthritis. J Exp Med. 1997; 185:975–80.
Article
46. Tegeder I, Schumacher A, John S, Geiger H, Geisslinger G, Bang H, et al. Elevated serum cyclophilin levels in patients with severe sepsis. J Clin Immunol. 1997; 17:380–6.
47. Endrich MM, Gehring H. The V3 loop of human immunodeficiency virus type-1 envelope protein is a high-affinity ligand for immunophilins present in human blood. Eur J Biochem. 1998; 252:441–6.
Article
48. Liao DF, Jin ZG, Baas AS, Daum G, Gygi SP, Aebersold R, et al. Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells. J Biol Chem. 2000; 275:189–96.
Article
49. Baas AS, Berk BC. Differential activation of mitogen-activated protein kinases by H2O2 and O2- in vascular smooth muscle cells. Circ Res. 1995; 77:29–36.
50. Meloche S, Seuwen K, Pages G, Pouyssegur J. Biphasic and synergistic activation of p44mapk (ERK1) by growth factors: correlation between late phase activation and mitogenicity. Mol Endocrinol. 1992; 6:845–54.
Article
51. York RD, Yao H, Dillon T, Ellig CL, Eckert SP, McCleskey EW, et al. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature. 1998; 392:622–6.
Article
52. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, et al. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension. 1998; 32:488–95.
53. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest. 1996; 97:1916–23.
Article
54. Satoh K, Nigro P, Matoba T, O’Dell MR, Cui Z, Shi X, et al. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med. 2009; 15:649–56.
Article
55. Takapoo M, Chamseddine AH, Bhalla RC, Miller FJ Jr. Glutathione peroxidase-deficient smooth muscle cells cause paracrine activation of normal smooth muscle cells via cyclophilin A. Vascul Pharmacol. 2011; 55:143–8.
Article
56. Kim SH, Lessner SM, Sakurai Y, Galis ZS. Cyclophilin A as a novel biphasic mediator of endothelial activation and dysfunction. Am J Pathol. 2004; 164:1567–74.
Article
57. Seko Y, Tobe K, Ueki K, Kadowaki T, Yazaki Y. Hypoxia and hypoxia/reoxygenation activate Raf-1, mitogen- activated protein kinase kinase, mitogen-activated protein kinases, and S6 kinase in cultured rat cardiac myocytes. Circ Res. 1996; 78:82–90.
58. Seko Y, Tobe K, Takahashi N, Kaburagi Y, Kadowaki T, Yazaki Y. Hypoxia and hypoxia/reoxygenation activate Src family tyrosine kinases and p21ras in cultured rat cardiac myocytes. Biochem Biophys Res Commun. 1996; 226:530–5.
59. Satoh K, Nigro P, Zeidan A, Soe NN, Jaffre F, Oikawa M, et al. Cyclophilin A promotes cardiac hypertrophy in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2011; 31:1116–23.
Article
60. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, Salmona M, et al. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci U S A. 2002; 99:3505–10.
Article
61. Ghezzi P, Casagrande S, Massignan T, Basso M, Bellacchio E, Mollica L, et al. Redox regulation of cyclophilin A by glutathionylation. Proteomics. 2006; 6:817–25.
Article
62. Massignan T, Casoni F, Basso M, Stefanazzi P, Biasini E, Tortarolo M, et al. Proteomic analysis of spinal cord of presymptomatic amyotrophic lateral sclerosis G93A SOD1 mouse. Biochem Biophys Res Commun. 2007; 353:719–25.
Article
63. Lammers M, Neumann H, Chin JW, James LC. Acetylation regulates cyclophilin A catalysis, immunosuppression and HIV isomerization. Nat Chem Biol. 2010; 6:331–7.
Article
64. Bryant SR, Bjercke RJ, Erichsen DA, Rege A, Lindner V. Vascular remodeling in response to altered blood flow is mediated by fibroblast growth factor-2. Circ Res. 1999; 84:323–8.
Article
65. Chiang HY, Korshunov VA, Serour A, Shi F, Sottile J. Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol. 2009; 29:1074–9.
Article
66. Acevedo L, Yu J, Erdjument-Bromage H, Miao RQ, Kim JE, Fulton D, et al. A new role for Nogo as a regulator of vascular remodeling. Nat Med. 2004; 10:382–8.
Article
67. Carmeliet P, Moons L, Herbert JM, Crawley J, Lupu F, Lijnen R, et al. Urokinase but not tissue plasminogen activator mediates arterial neointima formation in mice. Circ Res. 1997; 81:829–39.
Article
68. Filippov S, Koenig GC, Chun TH, Hotary KB, Ota I, Bugge TH, et al. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med. 2005; 202:663–71.
Article
69. Hassan GS, Jasmin JF, Schubert W, Frank PG, Lisanti MP. Caveolin-1 deficiency stimulates neointima formation during vascular injury. Biochemistry. 2004; 43:8312–21.
Article
70. Korshunov VA, Berk BC. Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol. 2003; 23:2185–91.
71. Korshunov VA, Berk BC. Strain-dependent vascular remodeling: the "Glagov phenomenon" is genetically determined. Circulation. 2004; 110:220–6.
72. Ruef J, Hu ZY, Yin LY, Wu Y, Hanson SR, Kelly AB, et al. Induction of vascular endothelial growth factor in balloon-injured baboon arteries. A novel role for reactive oxygen species in atherosclerosis. Circ Res. 1997; 81:24–33.
73. Ruef J, Liu SQ, Bode C, Tocchi M, Srivastava S, Runge MS, et al. Involvement of aldose reductase in vascular smooth muscle cell growth and lesion formation after arterial injury. Arterioscler Thromb Vasc Biol. 2000; 20:1745–52.
Article
74. Leite PF, Danilovic A, Moriel P, Dantas K, Marklund S, Dantas AP, et al. Sustained decrease in superoxide dismutase activity underlies constrictive remodeling after balloon injury in rabbits. Arterioscler Thromb Vasc Biol. 2003; 23:2197–202.
Article
75. Hsieh HJ, Cheng CC, Wu ST, Chiu JJ, Wung BS, Wang DL. Increase of reactive oxygen species (ROS) in endothelial cells by shear flow and involvement of ROS in shear-induced c-fos expression. J Cell Physiol. 1998; 175:156–62.
Article
76. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phox-dependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res. 2005; 97:533–40.
Article
77. Castier Y, Ramkhelawon B, Riou S, Tedgui A, Lehoux S. Role of NF-kappaB in flow-induced vascular remodeling. Antioxid Redox Signal. 2009; 11:1641–9.
78. Menshikov M, Plekhanova O, Cai H, Chalupsky K.
Parfyonova Y., Bashtrikov P, et al. Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol. 2006. 26:801–7.
79. Seki Y, Kai H, Shibata R, Nagata T, Yasukawa H, Yoshimura A, et al. Role of the JAK/STAT pathway in rat carotid artery remodeling after vascular injury. Circ Res. 2000; 87:12–8.
Article
80. Lambert CM, Roy M, Meloche J, Robitaille GA, Agharazii M, Richard DE, et al. Tumor necrosis factor inhibitors as novel therapeutic tools for vascular remodeling diseases. Am J Physiol Heart Circ Physiol. 2010; 299:H995–1001.
Article
81. El Mabrouk M, Touyz RM, Schiffrin EL. Differential ANG II-induced growth activation pathways in mesenteric artery smooth muscle cells from SHR. Am J Physiol Heart Circ Physiol. 2001; 281:H30–9.
Article
82. Paravicini TM, Touyz RM. Redox signaling in hypertension. Cardiovasc Res. 2006; 71:247–58.
Article
83. Berk BC. Redox signals that regulate the vascular response to injury. Thromb Haemost. 1999; 82:810–7.
Article
84. Touyz RM, Wu XH, He G, Park JB, Chen X, Vacher J, et al. Role of c-Src in the regulation of vascular contraction and Ca2+ signaling by angiotensin II in human vascular smooth muscle cells. J Hypertens. 2001; 19:441–9.
Article
85. Ishida M, Ishida T, Thomas SM, Berk BC. Activation of extracellular signal-regulated kinases (ERK1/2) by angiotensin II is dependent on c-Src in vascular smooth muscle cells. Circ Res. 1998; 82:7–12.
Article
86. Saito Y, Haendeler J, Hojo Y, Yamamoto K, Berk BC. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol. 2001; 21:6387–94.
Article
87. Yang H, Li M, Chai H, Yan S, Lin P, Lumsden AB, et al. Effects of cyclophilin A on cell proliferation and gene expressions in human vascular smooth muscle cells and endothelial cells. J Surg Res. 2005; 123:312–9.
88. Yang Y, Lu N, Zhou J, Chen ZN, Zhu P. Cyclophilin A up-regulates MMP-9 expression and adhesion of mono-cytes/macrophages via CD147 signalling pathway in rheumatoid arthritis. Rheumatology (Oxford). 2008; 47:1299–310.
Article
89. Yurchenko V, Zybarth G, O’Connor M, Dai WW, Franchin G, Hao T, et al. Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J Biol Chem. 2002; 277:22959–65.
Article
90. Obchoei S, Weakley SM, Wongkham S, Wongkham C, Sawanyawisuth K, Yao Q, et al. Cyclophilin A enhances cell proliferation and tumor growth of liver fluke-associated cholangiocarcinoma. Mol Cancer. 2011; 10:102.
Article
91. Yang H, Chen J, Yang J, Qiao S, Zhao S, Yu L. Cyclophilin A is upregulated in small cell lung cancer and activates ERK1/2 signal. Biochem Biophys Res Commun. 2007; 361:763–7.
Article
92. Li M, Zhai Q, Bharadwaj U, Wang H, Li F, Fisher WE, et al. Cyclophilin A is overexpressed in human pancreatic cancer cells and stimulates cell proliferation through CD147. Cancer. 2006; 106:2284–94.
Article
93. Artus C, Boujrad H, Bouharrour A, Brunelle MN, Hoos S, Yuste VJ, et al. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J. 2010; 29:1585–99.
Article
94. Elbaz B, Valitsky M, Davidov G, Rahamimoff H. Cyclophilin A is involved in functional expression of the Na(+)-Ca(2+) exchanger NCX1. Biochemistry. 2010; 49:7634–42.
Article
95. Gerthoffer WT. Mechanisms of vascular smooth muscle cell migration. Circ Res. 2007; 100:607–21.
Article
96. Xu Q, Leiva MC, Fischkoff SA, Handschumacher RE, Lyttle CR. Leukocyte chemotactic activity of cyclophilin. J Biol Chem. 1992; 267:11968–71.
Article
97. Wang L, Wang CH, Jia JF, Ma XK, Li Y, Zhu HB, et al. Contribution of cyclophilin A to the regulation of inflammatory processes in rheumatoid arthritis. J Clin Immunol. 2010; 30:24–33.
Article
98. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000; 105:1605–12.
Article
99. Feldman DS, Zamah AM, Pierce KL, Miller WE, Kelly F, Rapacciuolo A, et al. Selective inhibition of hetero-trimeric Gs signaling. Targeting the receptor-G protein interface using a peptide minigene encoding the Galpha(s) carboxyl terminus. J Biol Chem. 2002; 277:28631–40.
100. Alexis JD, Wang N, Che W, Lerner-Marmarosh N, Sahni A, Korshunov VA, et al. Bcr kinase activation by angiotensin II inhibits peroxisome-proliferator-activated receptor gamma transcriptional activity in vascular smooth muscle cells. Circ Res. 2009; 104:69–78.
101. McCormick ML, Gavrila D, Weintraub NL. Role of oxidative stress in the pathogenesis of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2007; 27:461–9.
Article
102. Bruemmer D, Collins AR, Noh G, Wang W, Territo M, Arias-Magallona S, et al. Angiotensin II-accelerated atherosclerosis and aneurysm formation is attenuated in osteopontin-deficient mice. J Clin Invest. 2003; 112:1318–31.
Article
103. Pyo R, Lee JK, Shipley JM, Curci JA, Mao D, Ziporin SJ, et al. Targeted gene disruption of matrix metal-loproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J Clin Invest. 2000; 105:1641–9.
Article
104. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002; 110:625–32.
Article
105. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res. 2003; 92:827–39.
106. Aartsen WM, Hilgers RH, Schiffers PM, Daemen MJ, De Mey JG, Smits JF. Changes in vascular distensibility during angiotensin-converting enzyme inhibition involve bradykinin type 2 receptors. J Vasc Res. 2004; 41:18–27.
Article
107. Police SB, Thatcher SE, Charnigo R, Daugherty A, Cassis LA. Obesity promotes inflammation in periaortic adipose tissue and angiotensin II-induced abdominal aortic aneurysm formation. Arterioscler Thromb Vasc Biol. 2009; 29:1458–64.
Article
108. Browatzki M, Larsen D, Pfeiffer CA, Gehrke SG, Schmidt J, Kranzhofer A, et al. Angiotensin II stimulates matrix metalloproteinase secretion in human vascular smooth muscle cells via nuclear factor-kappaB and activator protein 1 in a redox-sensitive manner. J Vasc Res. 2005; 42:415–23.
109. Luchtefeld M, Grote K, Grothusen C, Bley S, Bandlow N, Selle T, et al. Angiotensin II induces MMP-2 in a p47phox-dependent manner. Biochem Biophys Res Commun. 2005; 328:183–8.
Article
110. Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS. 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; 98:2572–9.
111. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006; 6:508–19.
Article
112. Libby P. Inflammation in atherosclerosis. Nature. 2002; 420:868–74.
Article
113. Ross R. Atherosclerosis–an inflammatory disease. N Engl J Med. 1999; 340:115–26.
114. Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol. 2008; 8:802–15.
Article
115. Rahman A, Kefer J, Bando M, Niles WD, Malik AB. E-selectin expression in human endothelial cells by TNF-alpha-induced oxidant generation and NF-kappaB activation. Am J Physiol. 1998; 275:L533–44.
116. Tricot O, Mallat Z, Heymes C, Belmin J, Leseche G, Tedgui A. Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation. 2000; 101:2450–3.
Article
117. Ostergaard L, Simonsen U, Eskildsen-Helmond Y, Vorum H, Uldbjerg N, Honore B, et al. Proteomics reveals lowering oxygen alters cytoskeletal and endoplasmatic stress proteins in human endothelial cells. Proteomics. 2009; 9:4457–67.
Article
118. Nigro P, Satoh K, O’Dell MR, Soe NN, Cui Z, Mohan A, et al. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med. 2011; 208:53–66.
Article
119. Izumo S, Aoki H. Calcineurin–the missing link in cardiac hypertrophy. Nat Med. 1998; 4:661–2.
Article
120. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007; 292:C82–97.
Article
121. Sadoshima J, Izumo S. Molecular characterization of angiotensin II–induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res. 1993; 73:413–23.
122. Nakamura K, Fushimi K, Kouchi H, Mihara K, Miyazaki M, Ohe T, et al. Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation. 1998; 98:794–9.
123. Akki A, Zhang M, Murdoch C, Brewer A, Shah AM. NADPH oxidase signaling and cardiac myocyte function. J Mol Cell Cardiol. 2009; 47:15–22.
Article
124. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension. 2007; 49:241–8.
Article
125. Weber KT, Brilla CG. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin-angiotensin-aldosterone system. Circulation. 1991; 83:1849–65.
126. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007; 357:1121–35.
Article
127. Turer AT, Hill JA. Pathogenesis of myocardial ischemia-reperfusion injury and rationale for therapy. Am J Cardiol. 2010; 106:360–8.
Article
128. Prasad A, Stone GW, Holmes DR, Gersh B. Reperfusion injury, microvascular dysfunction, and cardioprotection: the "dark side" of reperfusion. Circulation. 2009; 120:2105–12.
129. Hess ML, Manson NH. Molecular oxygen: friend and foe. The role of the oxygen free radical system in the calcium paradox, the oxygen paradox and ischemia/reperfusion injury. J Mol Cell Cardiol. 1984; 16:969–85.
130. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res. 2004; 61:461–70.
Article
131. Braunersreuther V, Jaquet V. Reactive oxygen species in myocardial reperfusion injury: from physiopathology to therapeutic approaches. Curr Pharm Biotechnol. 2011; Apr 6 [Epub].
Article
132. Otani H. The role of nitric oxide in myocardial repair and remodeling. Antioxid Redox Signal. 2009; 11:1913–28.
Article
133. Seizer P, Ochmann C, Schonberger T, Zach S, Rose M, Borst O, et al. Disrupting the EMMPRIN (CD147)-cyclophilin A interaction reduces infarct size and preserves systolic function after myocardial ischemia and reperfusion. Arterioscler Thromb Vasc Biol. 2011; 31:1377–86.
Article
Full Text Links
  • JKSH
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr