Reduction of the HIV protease inhibitor-induced ER stress and inflammatory response by raltegravir in macrophages

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Zhang, Xiaoxuan ^a,b   Cao, Risheng ^b   Liu, Runping ^a,b   Zhao, Renping ^a   Huang, Yi ^a,c   Gurley, Emily C ^b   Hylemon, Phillip B ^b,d   Pandak, William M ^d   Wang, Guangji ^a   Zhang, Luyong ^a   Li, Xiaokun ^c   Zhou, Huiping ^b,c,d  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c WENZHOU MEDICAL UNIVERSITY   (China)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; INTERLEUKIN 6; LOPINAVIR; LOPINAVIR PLUS RITONAVIR; RALTEGRAVIR; REACTIVE OXYGEN METABOLITE; RITONAVIR; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; INTEGRASE INHIBITOR; LIPID; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; ATF 4 GENE; CALCIUM CELL LEVEL; CHOP GENE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG UPTAKE; ENDOPLASMIC RETICULUM STRESS; FOAM CELL; GENE CONTROL; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; INFLAMMATION; LIPID METABOLISM; LIPID STORAGE; MACROPHAGE; MALE; MARKER GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN EXPRESSION; UNFOLDED PROTEIN RESPONSE; XBP 1 GENE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CARDIOVASCULAR DISEASES; CELL LINE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; ENDOPLASMIC RETICULUM; ENZYME LINKED IMMUNOSORBENT ASSAY; HIV INFECTIONS; HOMEOSTASIS; KUPFFER CELL; METABOLISM;

ANIMALS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CARDIOVASCULAR DISEASES; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOKINES; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIV INFECTIONS; HIV INTEGRASE INHIBITORS; HIV PROTEASE INHIBITORS; HOMEOSTASIS; HUMANS; INFLAMMATION; INTERLEUKIN-6; KUPFFER CELLS; LIPID METABOLISM; LIPIDS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; RALTEGRAVIR POTASSIUM; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84898740511     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090856     Document Type: Article

References (34)

1. Riddle TM, Kuhel DG, Woollett LA, Fichtenbaum CJ, Hui DY (2001) HIV protease inhibitor induces fatty acid and sterol biosynthesis in liver and adipose tissues due to the accumulation of activated sterol regulatory element-binding proteins in the nucleus. J Biol Chem 276: 37514-37519.
2. Spector AA (2006) HIV protease inhibitors and hyperlipidemia: a fatty acid connection. Arterioscler Thromb Vasc Biol 26: 7-9.
3. Moyle G, Carr A (2002) HIV-associated lipodystrophy, metabolic complications, and antiretroviral toxicities. HIV Clin Trials 3: 89-98. (Pubitemid 34183098)
4. Chen L, Jarujaron S, Wu X, Sun L, Zha W, et al. (2009) HIV protease inhibitor lopinavir-induced TNF-alpha and IL-6 expression is coupled to the unfolded protein response and ERK signaling pathways in macrophages. Biochem Pharmacol 78: 70-77.
5. Zhou H, Gurley EC, Jarujaron S, Ding H, Fang Y, et al. (2006) HIV protease inhibitors activate the unfolded protein response and disrupt lipid metabolism in primary hepatocytes. AmJPhysiol GastrointestLiver Physiol 291: G1071-G1080. (Pubitemid 44904161)
6. Zhou H, Pandak WM, Jr., Lyall V, Natarajan R, Hylemon PB (2005) HIV protease inhibitors activate the unfolded protein response in macrophages: implication for atherosclerosis and cardiovascular disease. Mol Pharmacol 68: 690-700. (Pubitemid 41206022)
7. Koster JC, Remedi MS, Qiu H, Nichols CG, Hruz PW (2003) HIV protease inhibitors acutely impair glucose-stimulated insulin release. Diabetes 52: 1695-1700. (Pubitemid 36792459)
8. Vlahakis SR, Bennett SA, Whitehead SN, Badley AD (2007) HIV protease inhibitors modulate apoptosis signaling in vitro and in vivo. Apoptosis 12: 969-977. (Pubitemid 46653299)
9. Marchetti G, Bellistri GM, Borghi E, Tincati C, Ferramosca S, et al. (2008) Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIV-infected patients on long-term highly active antiretroviral therapy. Aids 22: 2035-2038.
10. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86: 1133-1149. (Pubitemid 44521649)
11. Nair V, Chi G (2007) HIV integrase inhibitors as therapeutic agents in AIDS. RevMedVirol 17: 277-295. (Pubitemid 47066639)
12. Steigbigel RT, Cooper DA, Kumar PN, Eron JE, Schechter M, et al. (2008) Raltegravir with optimized background therapy for resistant HIV-1 infection. N Engl J Med 359: 339-354.
13. Imaz A, del Saz SV, Ribas MA, Curran A, Caballero E, et al. (2009) Raltegravir, etravirine, and ritonavir-boosted darunavir: a safe and successful rescue regimen for multidrug-resistant HIV-1 infection. J Acquir Immune Defic Syndr 52: 382-386.
14. Cocohoba J, Dong BJ (2008) Raltegravir: the first HIV integrase inhibitor. Clin Ther 30: 1747-1765.
15. Cao R, Hu Y, Wang Y, Gurley EC, Studer EJ, et al. (2010) Prevention of HIV protease inhibitor-induced dysregulation of hepatic lipid metabolism by raltegravir via endoplasmic reticulum stress signaling pathways. J Pharmacol Exp Ther 334: 530-539.
16. Jacob A, Zhou M, Wu R, Halpern VJ, Ravikumar TS, et al. (2007) Proinflammatory cytokines from Kupffer cells downregulate hepatocyte expression of adrenomedullin binding protein-1. Biochim Biophys Acta 1772: 766-772. (Pubitemid 46891214)
17. Poirier JM, Robidou P, Jaillon P (2008) Quantification of the HIV-integrase inhibitor raltegravir (MK-0518) in human plasma by high-performance liquid chromatography with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci 867: 277-281.
18. Wu X, Zhang L, Gurley E, Studer E, Shang J, et al. (2008) Prevention of free fatty acid-induced hepatic lipotoxicity by 18beta-glycyrrhetinic acid through lysosomal and mitochondrial pathways. Hepatology 47: 1905-1915. (Pubitemid 351945558)
19. Mooser V, Carr A (2001) Antiretroviral therapy-associated hyperlipidaemia in HIV disease. Curr Opin Lipidol 12: 313-319. (Pubitemid 32521956)
20. Zhou H, Jarujaron S, Gurley EC, Chen L, Ding H, et al. (2007) HIV protease inhibitors increase TNF-alpha and IL-6 expression in macrophages: Involvement of the RNA-binding protein HuR. Atherosclerosis.
21. Hughes CA, Robinson L, Tseng A, MacArthur RD (2009) New antiretroviral drugs: a review of the efficacy, safety, pharmacokinetics, and resistance profile of tipranavir, darunavir, etravirine, rilpivirine, maraviroc, and raltegravir. Expert Opin Pharmacother 10: 2445-2466.
22. Kaplowitz N, Than TA, Shinohara M, Ji C (2007) Endoplasmic reticulum stress and liver injury. SeminLiver Dis 27: 367-377. (Pubitemid 350071837)
23. Jäger R, Bertrand MJM, Gorman AM, Vandenabeele P, Samali A (2012) The unfolded protein response at the crossroads of cellular life and death during ER stress. Biology of the Cell: n/a-n/a.
24. Zhang K, Kaufman RJ (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66: S102-109. (Pubitemid 43739994)
25. Kaplowitz N, Ji C (2006) Unfolding new mechanisms of alcoholic liver disease in the endoplasmic reticulum. J GastroenterolHepatol 21 Suppl 3: S7-S9. (Pubitemid 44266540)
26. Cnop M, Igoillo-Esteve M, Cunha DA, Ladriere L, Eizirik DL (2008) An update on lipotoxic endoplasmic reticulum stress in pancreatic beta-cells. BiochemSocTrans 36: 909-915.
27. Wu X, Sun L, Zha W, Studer E, Gurley E, et al. (2010) HIV protease inhibitors induce endoplasmic reticulum stress and disrupt barrier integrity in intestinal epithelial cells. Gastroenterology 138: 197-209.
28. Fan J, Watanabe T (2003) Inflammatory reactions in the pathogenesis of atherosclerosis. J Atheroscler Thromb 10: 63-71.
29. Kobayasi R, Akamine EH, Davel AP, Rodrigues MA, Carvalho CR, et al. (2011) Oxidative stress and inflammatory mediators contribute to endothelial dysfunction in high-fat diet-induced obesity in mice. J Hypertens 28: 2111-2119.
30. Tousoulis D, Zisimos K, Antoniades C, Stefanadi E, Siasos G, et al. (2009) Oxidative stress and inflammatory process in patients with atrial fibrillation: the role of left atrium distension. Int J Cardiol 136: 258-262.
31. Berg K, Jynge P, Bjerve K, Skarra S, Basu S, et al. (2005) Oxidative stress and inflammatory response during and following coronary interventions for acute myocardial infarction. Free Radic Res 39: 629-636. (Pubitemid 40846835)
32. Deng W, Baki L, Yin J, Zhou H, Baumgarten CM (2010) HIV protease inhibitors elicit volume-sensitive Cl- current in cardiac myocytes via mitochondrial ROS. J Mol Cell Cardiol 49: 746-752.
33. Feng B, Yao PM, Li Y, Devlin CM, Zhang D, et al. (2003) The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. NatCell Biol 5: 781-792. (Pubitemid 37087166)
34. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, et al. (2009) Autophagy regulates lipid metabolism. Nature 458: 1131-1135.