Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis

Journal of Clinical Investigation

Volumn 118, Issue 10, 2008, Pages 3343-3354

  Chun, Hyung J ^a   Ali, Ziad A ^a   Kojima, Yoko ^a   Kundu, Ramendra K ^a   Sheikh, Ahmad Y ^a   Agrawal, Rani ^a   Zheng, Lixin ^b   Leeper, Nicholas J ^a   Pearl, Nathan E ^a   Patterson, Andrew J ^a   Anderson, Joshua P ^a   Tsao, Philip S ^a   Lenardo, Michael J ^b   Ashley, Euan A ^a   Quertermous, Thomas ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; APELIN; APELIN 13; APELIN RECEPTOR; APOLIPOPROTEIN E; HYDRALAZINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ABDOMINAL AORTA ANEURYSM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; BIOAVAILABILITY; CONTROLLED STUDY; DRUG ANTAGONISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATION; INTIMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VEIN GRAFT;

ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM, ABDOMINAL; ATHEROSCLEROSIS; BLOOD VESSELS; CARRIER PROTEINS; CELL NUCLEUS; DIET; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, KNOCKOUT; NITRIC OXIDE; REACTIVE OXYGEN SPECIES; RECEPTORS, ANGIOTENSIN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; VASOCONSTRICTOR AGENTS;

EID: 55849094397     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI34871     Document Type: Article

References (55)

1. O'Dowd, B.F., et al. 1993. A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene. 136:355-360.
2. Tatemoto, K., et al. 1998. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun. 251:471-476.
3. Chen, M.M., et al. 2003. A novel role for the potent endogenous inotrope apelin in human cardiac dysfunction. Circulation. 108:1432-1439.
4. Kleinz, M.J., and Davenport, A.P. 2004. Immunocytochemical localization of the endogenous vasoactive peptide apelin to human vascular and endocardial endothelial cells. Regul. Pept. 118:119-125.
5. Kleinz, M.J., Skepper, J.N., and Davenport, A.P. 2005. Immunocytochemical localisation of the apelin receptor, APJ, to human cardiomyocytes, vascular smooth muscle and endothelial cells. Regul. Pept. 126:233-240.
6. Sheikh, A.Y., et al. 2007. In vivo genetic profiling and cellular localization of apelin reveals a hypoxiasensitive, endothelial-centered pathway activated in ischemic heart failure. Am. J. Physiol. Heart Circ. Physiol. 294:H88-H98.
7. Ashley, E.A., et al. 2005. The endogenous peptide apelin potently improves cardiac contractility and reduces cardiac loading in vivo. Cardiovasc. Res. 65:73-82.
8. Atluri, P., et al. 2007. Ischemic heart failure enhances endogenous myocardial apelin and APJ receptor expression. Cell. Mol. Biol. Lett. 12:127-138.
9. Farkasfalvi, K., et al. 2007. Direct effects of apelin on cardiomyocyte contractility and electrophysiology. Biochem. Biophys. Res. Commun. 357:889-895.
10. Szokodi, I., et al. 2002. Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ. Res. 91:434-440.
11. Jia, Y.X., et al. 2006. Apelin protects myocardial injury induced by isoproterenol in rats. Regul. Pept. 133:147-154.
12. Cheng, X., Cheng, X.S., and Pang, C.C. 2003. Venous dilator effect of apelin, an endogenous peptide ligand for the orphan APJ receptor, in conscious rats. Eur. J. Pharmacol. 470:171-175.
13. Ishida, J., et al. 2004. Regulatory roles for APJ, a seven-transmembrane receptor related to AT1, in blood pressure in vivo. J. Biol. Chem. 279:26274-26279.
14. Lee, D.K., et al. 2000. Characterization of apelin, the ligand for the APJ receptor. J. Neurochem. 74:34-41.
15. Tatemoto, K., et al. 2001. The novel peptide apelin lowers blood pressure via a nitric oxide-dependent mechanism. Regul. Pept. 99:87-92.
16. O'Carroll, A.M., Don, A.L., and Lolait, S.J. 2003. APJ receptor mRNA expression in the rat hypothalamic paraventricular nucleus: regulation by stress and glucocorticoids. J. Neuroendocrinol. 15:1095-1101.
17. De Mota, N., et al. 2004. Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity and vasopressin release. Proc. Natl. Acad. Sci. U. S. A. 101:10464-10469.
18. Lee, D.K., George, S.R., and O'Dowd, B.F. 2006. Unravelling the roles of the apelin system: prospective therapeutic applications in heart failure and obesity. Trends Pharmacol. Sci. 27:190-194.
19. Iwanaga, Y., Kihara, Y., Takenaka, H., and Kita, T. 2006. Down-regulation of cardiac apelin system in hypertrophied and failing hearts: Possible role of angiotensin II-angiotensin type 1 receptor system. J. Mol. Cell. Cardiol. 41:798-806.
20. Daugherty, A., Manning, M.W., and Cassis, L.A. 2000. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J. Clin. Invest. 105:1605-1612.
21. Dietrich, H., et al. 2000. Rapid development of vein graft atheroma in ApoE-deficient mice. Am. J. Pathol. 157:659-669.
22. Piedrahita, J.A., Zhang, S.H., Hagaman, J.R., Oliver, P.M., and Maeda, N. 1992. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 89:4471-4475.
23. Zhang, S.H., Reddick, R.L., Piedrahita, J.A., and Maeda, N. 1992. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 258:468-471.
24. Xu, Q., Zhang, Z., Davison, F., and Hu, Y. 2003. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ. Res. 93:e76-e86.
25. Abbasi, S., Su, B., Kellems, R.E., Yang, J., and Xia, Y. 2005. The essential role of MEKK3 signaling in angiotensin II-induced calcineurin/nuclear factor of activated T-cells activation. J. Biol. Chem. 280:36737-36746.
26. Han, Y., Runge, M.S., and Brasier, A.R. 1999. Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. Circ. Res. 84:695-703.
27. Lu, D., Yang, H., and Raizada, M.K. 1996. Angiotensin II regulation of neuromodulation: downstream signaling mechanism from activation of mitogen-activated protein kinase. J. Cell Biol. 135:1609-1617.
28. AbdAlla, S., Lother, H., Abdel-tawab, A.M., and Quitterer, U. 2001. The angiotensin II AT2 receptor is an AT1 receptor antagonist. J. Biol. Chem. 276:39721-39726.
29. AbdAlla, S., Lother, H., and Quitterer, U. 2000. AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature. 407:94-98.
30. Minneman, K.P. 2007. Heterodimerization and surface localization of G protein coupled receptors. Biochem. Pharmacol. 73:1043-1050.
31. Bafford, R., Sui, X.X., Wang, G., and Conte, M. 2006. Angiotensin II and tumor necrosis factor-alpha upregulate survivin and Kruppel-like factor 5 in smooth muscle cells: Potential relevance to vein graft hyperplasia. Surgery. 140:289-296.
32. Gavazzi, G., et al. 2007. NOX1 deficiency protects from aortic dissection in response to angiotensin II. Hypertension. 50:189-196.
33. Miller, F.J., Jr., et al. 2002. Oxidative stress in human abdominal aortic aneurysms: a potential mediator of aneurysmal remodeling. Arterioscler. Thromb. Vasc. Biol. 22:560-565.
34. Tham, D.M., et al. 2002. Angiotensin II is associated with activation of NF-kappaB-mediated genes and downregulation of PPARs. Physiol. Genomics. 11:21-30.
35. Schmieder, R.E., Hilgers, K.F., Schlaich, M.P., and Schmidt, B.M. 2007. Renin-angiotensin system and cardiovascular risk. Lancet. 369:1208-1219.
36. Mehta, P.K., and Griendling, K.K. 2006. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am. J. Physiol. Cell Physiol. 292:C82-C97.
37. Zhong, J.C., et al. 2007. Apelin modulates aortic vascular tone via endothelial nitric oxide synthase phosphorylation pathway in diabetic mice. Cardiovasc. Res. 74:388-395.
38. Daugherty, A., Rateri, D.L., Lu, H., Inagami, T., and Cassis, L.A. 2004. Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation. 110:3849-3857.
39. Hayek, T., Attias, J., Smith, J., Breslow, J.L., and Keidar, S. 1998. Antiatherosclerotic and antioxidative effects of captopril in apolipoprotein E-deficient mice. J. Cardiovasc. Pharmacol. 31:540-544.
40. AbdAlla, S., Lother, H., el Massiery, A., and Quitterer, U. 2001. Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat. Med. 7:1003-1009.
41. Katugampola, S.D., Kuc, R.E., Maguire, J.J., and Davenport, A.P. 2002. G-protein-coupled receptors in human atherosclerosis: comparison of vasoconstrictors (endothelin and thromboxane) with recently de-orphanized (urotensin-II, apelin and ghrelin) receptors. Clin. Sci. (Lond.) 103(Suppl. 48):171S-175S.
42. Choe, W., et al. 2000. Functional expression of the seven-transmembrane HIV-1 co-receptor APJ in neural cells. J. Neurovirol. 6(Suppl. 1):S61-S69.
43. Hashimoto, T., et al. 2007. Requirement of apelinapelin receptor system for oxidative stress-linked atherosclerosis. Am. J. Pathol. 171:1705-1712.
44. Harmon, K.J., Couper, L.L., and Lindner, V. 2000. Strain-dependent vascular remodeling phenotypes in inbred mice. Am. J. Pathol. 156:1741-1748.
45. Knowles, J.W., and Maeda, N. 2000. Genetic modifiers of atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 20:2336-2345.
46. Zou, Y., Dietrich, H., Hu, Y., Metzler, B., Wick, G., and Xu, Q. 1998. Mouse model of venous bypass graft arteriosclerosis. Am. J. Pathol. 153:1301-1310.
47. Johns, C., Gavras, I., Handy, D.E., Salomao, A., and Gavras, H. 1996. Models of experimental hypertension in mice. Hypertension. 28:1064-1069.
48. Tabibiazar, R., et al. 2005. Mouse strain-specific differences in vascular wall gene expression and their relationship to vascular disease. Arterioscler. Thromb. Vasc. Biol. 25:302-308.
49. Paigen, B., Morrow, A., Holmes, P.A., Mitchell, D., and Williams, R.A. 1987. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 68:231-240.
50. Ali, Z.A., et al. 2005. Gene transfer of a broad spectrum CC-chemokine inhibitor reduces vein graft atherosclerosis in apolipoprotein E-knockout mice. Circulation. 112:I235-I241.
51. Kleschyov, A.L., and Munzel, T. 2002. Advanced spin trapping of vascular nitric oxide using colloid iron diethyldithiocarbamate. Methods Enzymol. 359:42-51.
52. Alp, N.J., et al. 2003. Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP-cyclohydrolase I overexpression. J. Clin. Invest. 112:725-735.
53. Sista, A.K., et al. 2005. Increased aortic stiffness in the insulin-resistant Zucker fa/fa rat. Am. J. Physiol. Heart Circ. Physiol. 289:H845-H851.
54. Chan, F.K., et al. 2000. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science. 288:2351-2354.
55. Siegel, R.M., et al. 2000. Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein. Sci. STKE. 2000:PL1.