Comparative analysis of ER stress response into HIV protease inhibitors: Lopinavir but not darunavir induces potent ER stress response via ROS/JNK pathway

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 778-788

  Taura, Manabu ^a   Kariya, Ryusho ^a   Kudo, Eriko ^a   Goto, Hiroki ^a   Iwawaki, Takao ^b   Amano, Masayuki ^c   Suico, Mary Ann ^a   Kai, Hirofumi ^a   Mitsuya, Hiroaki ^c   Okada, Seiji ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

AIDS; CHOP; ER stress; HIV protease inhibitor; JNK; ROS

Indexed keywords

AMPRENAVIR; ATAZANAVIR; DARUNAVIR; INDINAVIR; LOPINAVIR; NELFINAVIR; REACTIVE OXYGEN METABOLITE; RITONAVIR; SAQUINAVIR; STRESS ACTIVATED PROTEIN KINASE; TIPRANAVIR; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; SULFONAMIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; COMPARATIVE STUDY; DRUG EFFECTS; HEK293 CELL LINE; HEPG2 CELL LINE; KIDNEY; LIVER; METABOLISM; MOUSE; SIGNAL TRANSDUCTION; SMALL INTESTINE;

MUS;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; HEK293 CELLS; HEP G2 CELLS; HIV PROTEASE INHIBITORS; HUMANS; INTESTINE, SMALL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KIDNEY; LIVER; LOPINAVIR; MALE; MICE; MICE, INBRED BALB C; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 84883633521     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.08.161     Document Type: Article

References (48)

1. E.J. Arts, and D.J. Hazuda HIV-1 Antiretroviral drug therapy Cold Spring Harb. Perspect. Med. 2 2012 a007161
2. I.T. Weber, and J. Agniswamy HIV-1 protease: structural perspectives on drug resistance Viruses 1 2009 1110 1136
3. I. Dierynck, M. De Wit, E. Gustin, I. Keuleers, J. Vandersmissen, S. Hallenberger, and K. Hertogs Binding kinetics of darunavir to human immunodeficiency virus type 1 protease explain the potent antiviral activity and high genetic barrier J. Virol. 81 2007 13845 13851 (Pubitemid 350247878)
4. E. Bulgheroni, P. Citterio, F. Croce, M. Lo Cicero, O. Vigano, F. Soster, T.C. Chou, M. Galli, and S. Rusconi Analysis of protease inhibitor combinations in vitro: activity of lopinavir, amprenavir and tipranavir against HIV type 1 wild-type and drug-resistant isolates J. Antimicrob. Chemother. 53 2004 464 468 (Pubitemid 38380244)
5. A.K. Ghosh, Z.L. Dawson, and H. Mitsuya Darunavir, a conceptually new HIV-1 protease inhibitor for the treatment of drug-resistant HIV Bioorg. Med. Chem. 15 2007 7576 7580 (Pubitemid 47575929)
6. D.D. Richman, D.M. Margolis, M. Delaney, W.C. Greene, D. Hazuda, and R.J. Pomerantz The challenge of finding a cure for HIV infection Science 323 2009 1304 1307
7. R. Cao, Y. Hu, Y. Wang, E.C. Gurley, E.J. Studer, X. Wang, P.B. Hylemon, W.M. Pandak, A.J. Sanyal, L. Zhang, and H. Zhou Prevention of HIV protease inhibitor-induced dysregulation of hepatic lipid metabolism by raltegravir via endoplasmic reticulum stress signaling pathways J. Pharmacol. Exp. Ther. 334 2010 530 539
8. J.C. Koster, M.S. Remedi, H. Qiu, C.G. Nichols, and P.W. Hruz HIV protease inhibitors acutely impair glucose-stimulated insulin release Diabetes 52 2003 1695 1700 (Pubitemid 36792459)
9. H. Zhou, S. Jarujaron, E.C. Gurley, L. Chen, H. Ding, E. Studer, W.M. Pandak Jr, W. Hu, T. Zou, J.Y. Wang, and P.B. Hylemon HIV protease inhibitors increase TNF-alpha and IL-6 expression in macrophages: involvement of the RNA-binding protein HuR Atherosclerosis 195 2007 e134 143
10. X. Wu, L. Sun, W. Zha, E. Studer, E. Gurley, L. Chen, X. Wang, P.B. Hylemon, W.M. Pandak Jr, A.J. Sanyal, L. Zhang, G. Wang, J. Chen, J.Y. Wang, and H. Zhou HIV protease inhibitors induce endoplasmic reticulum stress and disrupt barrier integrity in intestinal epithelial cells Gastroenterology 138 2009 197 209
11. J.V. Madruga, D. Berger, M. McMurchie, F. Suter, D. Banhegyi, K. Ruxrungtham, D. Norris, E. Lefebvre, M.P. de Bethune, F. Tomaka, M. De Pauw, T. Vangeneugden, and S. Spinosa-Guzman Efficacy and safety of darunavir-ritonavir compared with that of lopinavir-ritonavir at 48 weeks in treatment-experienced, HIV-infected patients in TITAN: a randomised controlled phase III trial Lancet 370 2007 49 58 (Pubitemid 47023100)
12. R. Ortiz, E. Dejesus, H. Khanlou, E. Voronin, J. van Lunzen, J. Andrade-Villanueva, J. Fourie, S. De Meyer, M. De Pauw, E. Lefebvre, T. Vangeneugden, and S. Spinosa-Guzman Efficacy and safety of once-daily darunavir/ritonavir versus lopinavir/ritonavir in treatment-naive HIV-1-infected patients at week 48 AIDS 22 2008 1389 1397
13. A.M. Mills, M. Nelson, D. Jayaweera, K. Ruxrungtham, I. Cassetti, P.M. Girard, C. Workman, I. Dierynck, V. Sekar, C.V. Abeele, and L. Lavreys Once-daily darunavir/ritonavir vs. lopinavir/ritonavir in treatment-naive, HIV-1-infected patients: 96-week analysis AIDS 23 2009 1679 1688
14. C. Orkin, E. DeJesus, H. Khanlou, A. Stoehr, K. Supparatpinyo, E. Lathouwers, E. Lefebvre, M. Opsomer, T. Van de Casteele, and F. Tomaka Final 192-week efficacy and safety of once-daily darunavir/ritonavir compared with lopinavir/ritonavir in HIV-1-infected treatment-naive patients in the ARTEMIS trial HIV Med. 14 2013 49 59
15. B. Clotet, N. Bellos, J.M. Molina, D. Cooper, J.C. Goffard, A. Lazzarin, A. Wohrmann, C. Katlama, T. Wilkin, R. Haubrich, C. Cohen, C. Farthing, D. Jayaweera, M. Markowitz, P. Ruane, S. Spinosa-Guzman, and E. Lefebvre Efficacy and safety of darunavir-ritonavir at week 48 in treatment-experienced patients with HIV-1 infection in POWER 1 and 2: a pooled subgroup analysis of data from two randomised trials Lancet 369 2007 1169 1178 (Pubitemid 46541620)
16. C. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat. Rev. Mol. Cell. Biol. 13 2012 89 102
17. I. Tabas, and D. Ron Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress Nat. Cell Biol. 13 2011 184 190
18. M. Schroder, and R.J. Kaufman The mammalian unfolded protein response Annu. Rev. Biochem. 74 2005 739 789 (Pubitemid 40995523)
19. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat. Rev. Mol. Cell. Biol. 8 2007 519 529 (Pubitemid 46985379)
20. P. Pyrko, A. Kardosh, W. Wang, W. Xiong, A.H. Schonthal, and T.C. Chen HIV-1 protease inhibitors nelfinavir and atazanavir induce malignant glioma death by triggering endoplasmic reticulum stress Cancer Res. 67 2007 10920 10928 (Pubitemid 350145921)
21. M. Kraus, E. Malenke, J. Gogel, H. Muller, T. Ruckrich, H. Overkleeft, H. Ovaa, E. Koscielniak, J.T. Hartmann, and C. Driessen Ritonavir induces endoplasmic reticulum stress and sensitizes sarcoma cells toward bortezomib-induced apoptosis Mol. Cancer Ther 7 2008 1940 1948
22. O. Touzet, and A. Philips Resveratrol protects against protease inhibitor-induced reactive oxygen species production, reticulum stress and lipid raft perturbation AIDS 24 2010 1437 1447
23. K. Ide, M. Aoki, M. Amano, Y. Koh, R.S. Yedidi, D. Das, S. Leschenko, B. Chapsal, A.K. Ghosh, and H. Mitsuya Novel HIV-1 protease inhibitors (PIs) containing a bicyclic P2 functional moiety, tetrahydropyrano-tetrahydrofuran, that are potent against multi-PI-resistant HIV-1 variants Antimicrob. Agents Chemother. 55 2011 1717 1727
24. T. Iwawaki, and R. Akai Analysis of the XBP1 splicing mechanism using endoplasmic reticulum stress-indicators Biochem. Biophys. Res. Commun. 350 2006 709 715 (Pubitemid 44547905)
25. M. Taura, M.A. Suico, K. Koyama, K. Komatsu, R. Miyakita, C. Matsumoto, E. Kudo, R. Kariya, H. Goto, S. Kitajima, C. Takahashi, T. Shuto, M. Nakao, S. Okada, and H. Kai Rb/E2F1 regulates the innate immune receptor Toll-like receptor 3 in epithelial cells Mol. Cell. Biol. 32 2012 1581 1590
26. A. Samali, U. Fitzgerald, S. Deegan, and S. Gupta Methods for monitoring endoplasmic reticulum stress and the unfolded protein response Int. J. Cell Biol 2010 2010 830307
27. M. Taura, M.A. Suico, R. Fukuda, T. Koga, T. Shuto, T. Sato, S. Morino-Koga, S. Okada, and H. Kai MEF/ELF4 transactivation by E2F1 is inhibited by p53 Nucleic Acids Res. 39 2011 76 88
28. H. Goto, R. Kariya, M. Shimamoto, E. Kudo, M. Taura, H. Katano, and S. Okada Antitumor effect of berberine against primary effusion lymphoma via inhibition of NF-kappaB pathway Cancer Sci. 103 2012 775 781
29. T. Koga, H. Harada, T.S. Shi, S. Okada, M.A. Suico, T. Shuto, and H. Kai Hyperthermia suppresses the cytotoxicity of NK cells via down-regulation of perforin/granzyme B expression Biochem. Biophys. Res. Commun. 337 2005 1319 1323 (Pubitemid 41505266)
30. M. Taura, R. Fukuda, M.A. Suico, A. Eguma, T. Koga, T. Shuto, T. Sato, S. Morino-Koga, and H. Kai TLR3 induction by anticancer drugs potentiates poly I: C-induced tumor cell apoptosis Cancer Sci. 101 2010 1610 1617
31. T. Iwawaki, R. Akai, K. Kohno, and M. Miura A transgenic mouse model for monitoring endoplasmic reticulum stress Nat. Med 10 2004 98 102 (Pubitemid 38524705)
32. M. Shamoto-Nagai, W. Maruyama, H. Yi, Y. Akao, F. Tribl, M. Gerlach, T. Osawa, P. Riederer, and M. Naoi Neuromelanin induces oxidative stress in mitochondria through release of iron: mechanism behind the inhibition of 26S proteasome J. Neural Transm. 113 2006 633 644 (Pubitemid 43673603)
33. R. Oerlemans, N.E. Franke, Y.G. Assaraf, J. Cloos, I. van Zantwijk, C.R. Berkers, G.L. Scheffer, K. Debipersad, K. Vojtekova, C. Lemos, J.W. van der Heijden, B. Ylstra, G.J. Peters, G.L. Kaspers, B.A. Dijkmans, R.J. Scheper, and G. Jansen Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein Blood 112 2008 2489 2499
34. M. Boyce, K.F. Bryant, C. Jousse, K. Long, H.P. Harding, D. Scheuner, R.J. Kaufman, D. Ma, D.M. Coen, D. Ron, and J. Yuan A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress Science 307 2005 935 939 (Pubitemid 40229232)
35. T. Ishimoto, O. Nagano, T. Yae, M. Tamada, T. Motohara, H. Oshima, M. Oshima, T. Ikeda, R. Asaba, H. Yagi, T. Masuko, T. Shimizu, T. Ishikawa, K. Kai, E. Takahashi, Y. Imamura, Y. Baba, M. Ohmura, M. Suematsu, H. Baba, and H. Saya CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth Cancer Cell 19 2011 387 400
36. I. Takac, K. Schroder, L. Zhang, B. Lardy, N. Anilkumar, J.D. Lambeth, A.M. Shah, F. Morel, and R.P. Brandes The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4 J. Biol. Chem. 286 2011 13304 13313
37. E. Anuurad, A. Bremer, and L. Berglund HIV protease inhibitors and obesity Curr. Opin. Endocrinol. Diabetes Obes 17 2010 478 485
38. D. Lindholm, H. Wootz, and L. Korhonen ER stress and neurodegenerative diseases Cell Death Differ. 13 2006 385 392
39. D. Morito, and K. Nagata ER stress proteins in autoimmune and inflammatory diseases Front. Immunol 3 2012 48
40. M. McLaughlin, and K. Vandenbroeck The endoplasmic reticulum protein folding factory and its chaperones: new targets for drug discovery? Br. J. Pharmacol 162 2011 328 345
41. T. Namba, K.I. Tanaka, Y. Ito, T. Hoshino, M. Matoyama, N. Yamakawa, Y. Isohama, A. Azuma, and T. Mizushima Induction of EMT-like phenotypes by an active metabolite of leflunomide and its contribution to pulmonary fibrosis Cell Death Differ. 17 2010 1882 1895
42. H. Tanjore, T.S. Blackwell, and W.E. Lawson Emerging evidence for endoplasmic reticulum stress in the pathogenesis of idiopathic pulmonary fibrosis Am. J. Physiol. Lung Cell Mol. Physiol 302 2012 L721 L729
43. F. Maingat, B. Halloran, S. Acharjee, G. van Marle, D. Church, M.J. Gill, R.R. Uwiera, E.A. Cohen, J. Meddings, K. Madsen, and C. Power Inflammation and epithelial cell injury in AIDS enteropathy: involvement of endoplasmic reticulum stress FASEB J 25 2011 2211 2220
44. L.M. Tiede, E.A. Cook, B. Morsey, and H.S. Fox Oxygen matters: tissue culture oxygen levels affect mitochondrial function and structure as well as responses to HIV viroproteins Cell Death Dis. 2 2011 e246
45. W. Deng, L. Baki, J. Yin, H. Zhou, and C.M. Baumgarten HIV protease inhibitors elicit volume-sensitive Cl- current in cardiac myocytes via mitochondrial ROS J. Mol. Cell. Cardiol. 49 2010 746 752
46. Y. Koh, H. Nakata, K. Maeda, H. Ogata, G. Bilcer, T. Devasamudram, J.F. Kincaid, P. Boross, Y.F. Wang, Y. Tie, P. Volarath, L. Gaddis, R.W. Harrison, I.T. Weber, A.K. Ghosh, and H. Mitsuya Novel bis-tetrahydrofuranylurethane- containing nonpeptidic protease inhibitor (PI) UIC-94017 (TMC114) with potent activity against multi-PI-resistant human immunodeficiency virus in vitro Antimicrob. Agents Chemother. 47 2003 3123 3129 (Pubitemid 37229567)
47. J.S. Murray, M.R. Elashoff, L.C. Iacono-Connors, T.A. Cvetkovich, and K.A. Struble The use of plasma HIV RNA as a study endpoint in efficacy trials of antiretroviral drugs AIDS 13 1999 797 804 (Pubitemid 29224581)
48. P.A. Volberding, and S.G. Deeks Antiretroviral therapy and management of HIV infection Lancet 376 2010 49 62