Statins stimulate the production of a soluble form of the receptor for advanced glycation end products

Journal of Lipid Research

Volumn 54, Issue 11, 2013, Pages 3052-3061

  Quade Lyssy, Patricia ^a   Kanarek, Anna Maria ^a   Baiersdörfer, Markus ^a   Postina, Rolf ^a   Kojro, Elzbieta ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

ADAM 10; Atherosclerosis; Diabetic complications; Hypercholesterolemia

Indexed keywords

ADAM10 ENDOPEPTIDASE; ADVANCED GLYCATION END PRODUCT RECEPTOR; ATORVASTATIN; FLUINDOSTATIN; MEVINOLIN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL LEVEL; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN SECRETION; RNA INTERFERENCE; STEROL SYNTHESIS;

ADAM 10; ATHEROSCLEROSIS; DIABETIC COMPLICATIONS; HYPERCHOLESTEROLEMIA;

ANIMALS; BETA-CYCLODEXTRINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE; CHOLESTEROL; DOSE-RESPONSE RELATIONSHIP, DRUG; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LOVASTATIN; MICE; RECEPTORS, IMMUNOLOGIC; SOLUBILITY; TRICARBOXYLIC ACIDS;

EID: 84885967163     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M038968     Document Type: Article

References (47)

1. Bierhaus, A., P. M. Humpert, M. Morcos, T. Wendt, T. Chavakis, B. Arnold, D. M. Stern, and P. P. Nawroth. 2005. Understanding RAGE, the receptor for advanced glycation end products. J. Mol. Med. 83: 876-886. (Pubitemid 41598688)
2. Bucciarelli, L. G., T. Wendt, L. Rong, E. Lalla, M. A. Hofmann, M. T. Goova, A. Taguchi, S. F. Yan, S. D. Yan, D. M. Stern, et al. 2002. RAGE is a multiligand receptor of the immunoglobulin superfamily: implications for homeostasis and chronic disease. Cell. Mol. Life Sci. 59: 1117-1128.
3. Bucciarelli, L. G., T. Wendt, W. Qu, Y. Lu, E. Lalla, L. L. Rong, M. T. Goova, B. Moser, T. Kislinger, D. C. Lee, et al. 2002. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 106: 2827-2835. (Pubitemid 35396983)
4. Soro-Paavonen, A., A. M. Watson, J. Li, K. Paavonen, A. Koitka, A. C. Calkin, D. Barit, M. T. Coughlan, B. G. Drew, G. I. Lancaster, et al. 2008. Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes. 57: 2461-2469.
5. Ueno, H., H. Koyama, T. Shoji, M. Monden, S. Fukumoto, S. Tanaka, Y. Otsuka, Y. Mima, T. Morioka, K. Mori, et al. 2010. Receptor for advanced glycation end-products (RAGE) regulation of adiposity and adiponectin is associated with atherogenesis in apoE-deficient mouse. Atherosclerosis. 211: 431-436.
6. Barlovic, D. P., M. C. Thomas, and K. Jandeleit-Dahm. 2010. Cardiovascular disease: what's all the AGE/RAGE about? Cardiovasc. Hematol. Disord. Drug Targets. 10: 7-15.
7. Li, J., and A. M. Schmidt. 1997. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 272: 16498-16506. (Pubitemid 27276477)
8. Wautier, J. L., C. Zoukourian, O. Chappey, M. P. Wautier, P. J. Guillausseau, R. Cao, O. Hori, D. Stern, and A. M. Schmidt. 1996. Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J. Clin. Invest. 97: 238-243.
9. Park, L., K. G. Raman, K. J. Lee, Y. Lu, L. J. Ferran, Jr., W. S. Chow, D. Stern, and A. M. Schmidt. 1998. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat. Med. 4: 1025-1031. (Pubitemid 28417334)
10. Goova, M. T., J. Li, T. Kislinger, W. Qu, Y. Lu, L. G. Bucciarelli, S. Nowygrod, B. M. Wolf, X. Caliste, S. F. Yan, et al. 2001. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am. J. Pathol. 159: 513-525. (Pubitemid 32751082)
11. Deane, R., Y. S. Du, R. K. Submamaryan, B. LaRue, S. Jovanovic, E. Hogg, D. Welch, L. Manness, C. Lin, J. Yu, et al. 2003. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med. 9: 907-913. (Pubitemid 36889934)
12. Yonekura, H., Y. Yamamoto, S. Sakurai, R. G. Petrova, M. J. Abedin, H. Li, K. Yasui, M. Takeuchi, Z. Makita, S. Takasawa, et al. 2003. Novel splice variants of the receptor for advanced glycation endproducts expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem. J. 370: 1097-1109. (Pubitemid 36399105)
13. Schlueter, C., S. Hauke, A. M. Flohr, P. Rogalla, and J. Bullerdiek. 2003. Tissue-specific expression patterns of the RAGE receptor and its soluble forms-a result of regulated alternative splicing? Biochim. Biophys. Acta. 1630: 1-6. (Pubitemid 37297971)
14. Galichet, A., M. Weibel, and C. W. Heizmann. 2008. Calciumregulated intramembrane proteolysis of the RAGE receptor. Biochem. Biophys. Res. Commun. 370: 1-5.
15. Raucci, A., S. Cugusi, A. Antonelli, S. M. Barabino, L. Monti, A. Bierhaus, K. Reiss, P. Saftig, and M. E. Bianchi. 2008. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J. 22: 3716-3727.
16. Zhang, L., M. Bukulin, E. Kojro, A. Roth, V. V. Metz, F. Fahrenholz, P. P. Nawroth, A. Bierhaus, and R. Postina. 2008. Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J. Biol. Chem. 283: 35507-35516.
17. Kojro, E., G. Gimpl, S. Lammich, W. Marz, and F. Fahrenholz. 2001. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc. Natl. Acad. Sci. USA. 98: 5815-5820. (Pubitemid 32435725)
18. Matthews, V., B. Schuster, S. Schutze, I. Bussmeyer, A. Ludwig, C. Hundhausen, T. Sadowski, P. Saftig, D. Hartmann, K. J. Kallen, et al. 2003. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J. Biol. Chem. 278: 38829-38839. (Pubitemid 37221782)
19. Zimina, E. P., L. Bruckner-Tuderman, and C. W. Franzke. 2005. Shedding of collagen XVII ectodomain depends on plasma membrane microenvironment. J. Biol. Chem. 280: 34019-34024. (Pubitemid 41443123)
20. Colhoun, H. M., D. J. Betteridge, P. N. Durrington, G. A. Hitman, H. A. Neil, S. J. Livingstone, M. J. Thomason, M. I. Mackness, V. Charlton-Menys, and J. H. Fuller. 2004. Primary prevention of cardiovascular disease with atorvastatin in type 2 diabetes in the Collaborative Atorvastatin Diabetes Study (CARDS): multicentre randomised placebo-controlled trial. Lancet. 364: 685-696. (Pubitemid 39140624)
21. Abbas, A., J. Milles, and S. Ramachandran. 2012. Rosuvastatin and atorvastatin: comparative effects on glucose metabolism in nondiabetic patients with dyslipidaemia. Clin. Med. Insights Endocrinol. Diabetes. 5: 13-30.
22. Ridker, P. M., A. Pradhan, J. G. MacFadyen, P. Libby, and R. J. Glynn. 2012. Cardiovascular benefits and diabetes risks of statin therapy in primary prevention: an analysis from the JUPITER trial. Lancet. 380: 565-571.
23. Hoettecke, N., A. Ludwig, S. Foro, and B. Schmidt. 2010. Improved synthesis of ADAM10 inhibitor GI254023X. Neurodegener. Dis. 7: 232-238.
24. Cutts, J. L., and G. Melnykovych. 1988. Defective utilization of cholesterol esters from low-density lipoprotein in a human acute lymphoblastic leukemia T cell line. Biochim. Biophys. Acta. 961: 65-72.
25. Metz, V. V., E. Kojro, D. Rat, and R. Postina. 2012. Induction of RAGE shedding by activation of G protein-coupled receptors. PLoS ONE. 7: e41823.
26. Kojro, E., P. Fuger, C. Prinzen, A. M. Kanarek, D. Rat, K. Endres, F. Fahrenholz, and R. Postina. 2010. Statins and the squalene synthase inhibitor zaragozic acid stimulate the non-amyloidogenic pathway of amyloid-beta protein precursor processing by suppression of cholesterol synthesis. J. Alzheimers Dis. 20: 1215-1231.
27. Taraboulos, A., M. Scott, A. Semenov, D. Avrahami, L. Laszlo, and S. B. Prusiner. 1995. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129: 121-132. [Erratum. 1995. J. Cell Biol. 130: 501.]
28. Butterfield, D. A., E. Barone, and C. Mancuso. 2011. Cholesterolindependent neuroprotective and neurotoxic activities of statins: perspectives for statin use in Alzheimer disease and other agerelated neurodegenerative disorders. Pharmacol. Res. 64: 180-186.
29. Corsini, A., S. Bellosta, R. Baetta, R. Fumagalli, R. Paoletti, and F. Bernini. 1999. New insights into the pharmacodynamic and pharmacokinetic properties of statins. Pharmacol. Ther. 84: 413-428.
30. Pan, H. Y., A. R. DeVault, D. Wang-Iverson, E. Ivashkiv, B. N. Swanson, and A. A. Sugerman. 1990. Comparative pharmacokinetics and pharmacodynamics of pravastatin and lovastatin. J. Clin. Pharmacol. 30: 1128-1135.
31. Tse, F. L., J. M. Jaffe, and A. Troendle. 1992. Pharmacokinetics of fluvastatin after single and multiple doses in normal volunteers. J. Clin. Pharmacol. 32: 630-638.
32. Posvar, E. L., L. L. Radulovic, D. D. Cilla, Jr., L. R. Whitfield, and A. J. Sedman. 1996. Tolerance and pharmacokinetics of single-dose atorvastatin, a potent inhibitor of HMG-CoA reductase, in healthy subjects. J. Clin. Pharmacol. 36: 728-731. (Pubitemid 26295777)
33. Colhoun, H. M., D. J. Betteridge, P. Durrington, G. Hitman, A. Neil, S. Livingstone, V. Charlton-Menys, W. Bao, D. A. DeMicco, G. M. Preston, et al. 2011. Total soluble and endogenous secretory receptor for advanced glycation end products as predictive biomarkers of coronary heart disease risk in patients with type 2 diabetes: an analysis from the CARDS trial. Diabetes. 60: 2379-2385.
34. Fujisawa, K., N. Katakami, H. Kaneto, T. Naka, M. Takahara, F. Sakamoto, Y. Irie, K. Miyashita, F. Kubo, T. Yasuda, et al. 2013. Circulating soluble RAGE as a predictive biomarker of cardiovascular event risk in patients with type 2 diabetes. Atherosclerosis. 227: 425-428.
35. Lindsey, J. B., J. A. de Lemos, F. Cipollone, C. R. Ayers, A. Rohatgi, D. A. Morrow, A. Khera, and D. K. McGuire. 2009. Association between circulating soluble receptor for advanced glycation end products and atherosclerosis: observations from the Dallas Heart Study. Diabetes Care. 32: 1218-1220.
36. Hudson, B. I., Y. P. Moon, A. Z. Kalea, M. Khatri, C. Marquez, A. M. Schmidt, M. C. Paik, M. Yoshita, R. L. Sacco, C. DeCarli, et al. 2011. Association of serum soluble receptor for advanced glycation endproducts with subclinical cerebrovascular disease: the Northern Manhattan Study (NOMAS). Atherosclerosis. 216: 192-198.
37. Selvin, E., M. K. Halushka, A. M. Rawlings, R. C. Hoogeveen, C. M. Ballantyne, J. Coresh, and B. C. Astor. 2013. sRAGE and risk of diabetes, cardiovascular disease, and death. Diabetes. 62: 2116-2121.
38. Ilangumaran, S., and D. C. Hoessli. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335: 433-440. (Pubitemid 28491081)
39. Cuccurullo, C., A. Iezzi, M. L. Fazia, C. D. De, F. A. Di, R. Muraro, R. Bei, S. Ucchino, F. Spigonardo, F. Chiarelli, et al. 2006. Suppression of RAGE as a basis of simvastatin-dependent plaque stabilization in type 2 diabetes. Arterioscler. Thromb. Vasc. Biol. 26: 2716-2723.
40. Jinnouchi, Y., S. Yamagishi, M. Takeuchi, S. Ishida, Y. Jinnouchi, J. Jinnouchi, and T. Imaizumi. 2006. Atorvastatin decreases serum levels of advanced glycation end products (AGEs) in patients with type 2 diabetes. Clin. Exp. Med. 6: 191-193. (Pubitemid 46025593)
41. Feng, B., L. Xu, H. Wang, X. Yan, J. Xue, F. Liu, and J. F. Hu. 2011. Atorvastatin exerts its anti-atherosclerotic effects by targeting the receptor for advanced glycation end products. Biochim. Biophys. Acta. 1812: 1130-1137.
42. Lu, L., W. H. Peng, W. Wang, L. J. Wang, Q. J. Chen, and W. F. Shen. 2011. Effects of atorvastatin on progression of diabetic nephropathy and local RAGE and soluble RAGE expressions in rats. J. Zhejiang Univ. Sci. B. 12: 652-659.
43. Santilli, F., L. Bucciarelli, D. Noto, A. B. Cefalu, V. Davi, E. Ferrante, C. Pettinella, M. R. Averna, G. Ciabattoni, and G. Davi. 2007. Decreased plasma soluble RAGE in patients with hypercholesterolemia: effects of statins. Free Radic. Biol. Med. 43: 1255-1262. (Pubitemid 47429934)
44. Tam, H. L., S. W. Shiu, Y. Wong, W. S. Chow, D. J. Betteridge, and K. C. Tan. 2010. Effects of atorvastatin on serum soluble receptors for advanced glycation end-products in type 2 diabetes. Atherosclerosis. 209: 173-177.
45. Jick, H., G. L. Zornberg, S. S. Jick, S. Seshadri, and D. A. Drachman. 2000. Statins and the risk of dementia. Lancet. 356: 1627-1631.
46. Wolozin, B., W. Kellman, P. Rousseau, G. G. Celesia, and G. Siegel. 2000. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3- methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57: 1439-1443.
47. Haag, M. D., A. Hofman, P. J. Koudstaal, B. H. Stricker, and M. M. Breteler. 2009. Statins are associated with a reduced risk of Alzheimer disease regardless of lipophilicity. The Rotterdam Study. J. Neurol. Neurosurg. Psychiatry. 80: 13-17.