Novel dengue virus inhibitor 4-HPR activates ATF4 independent of protein kinase R-like Endoplasmic Reticulum Kinase and elevates levels of eIF2α phosphorylation in virus infected cells

Antiviral Research

Volumn 130, Issue , 2016, Pages 1-6

  Fraser, J E ^a   Wang, C ^a   Chan, K W K ^b   Vasudevan, S G ^b   Jans, D A ^a  

^a MONASH UNIVERSITY   (Australia)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Antiviral; Guanabenz; Integrated stress response; Key words Dengue virus; Translation attenuation; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; FENRETINIDE; INITIATION FACTOR 2ALPHA; PROTEIN KINASE R; PROTEIN KINASE R LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; ATF4 PROTEIN, MOUSE; PERK KINASE; SMALL INTERFERING RNA;

A549 CELL LINE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; DRUG MECHANISM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSLATION REGULATION; VIRUS PLAQUE; VIRUS TRANSCRIPTION; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL LINE; DENGUE VIRUS; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN SYNTHESIS; RNA INTERFERENCE; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CELLS, CULTURED; DENGUE VIRUS; EIF-2 KINASE; FENRETINIDE; MICE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION;

EID: 84962303147     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.03.006     Document Type: Article

References (34)

1. R.L. Ambrose, and J.M. Mackenzie West Nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion J. virology 85 2011 2723 2732
2. S. Bhatt, P.W. Gething, O.J. Brady, J.P. Messina, A.W. Farlow, C.L. Moyes, J.M. Drake, J.S. Brownstein, A.G. Hoen, O. Sankoh, M.F. Myers, D.B. George, T. Jaenisch, G.R. Wint, C.P. Simmons, T.W. Scott, J.J. Farrar, and S.I. Hay The global distribution and burden of dengue Nature 496 2013 504 507
3. M. Carocci, S.M. Hinshaw, M.A. Rodgers, V.A. Villareal, D.J. Burri, R. Pilankatta, N.P. Maharaj, M.U. Gack, E.J. Stavale, K.L. Warfield, and P.L. Yang The bioactive lipid 4-hydroxyphenyl retinamide inhibits flavivirus replication Antimicrob. Agents Chemother. 59 2015 85 95
4. J.E. Fraser, S.M. Rawlinson, C. Wang, D.A. Jans, and K.M. Wagstaff Investigating dengue virus nonstructural protein 5 (NS5) nuclear import Methods Mol. Biol. 1138 2014 301 328
5. J.E. Fraser, S. Watanabe, C. Wang, W.K. Chan, B. Maher, A. Lopez-Denman, C. Hick, K.M. Wagstaff, J.M. Mackenzie, P.M. Sexton, S.G. Vasudevan, and D.A. Jans A nuclear transport inhibitor that modulates the unfolded protein response and provides in vivo protection against lethal dengue virus infection J. Infect. Dis. 210 2014 1780 1791
6. A. Garaventa, R. Luksch, M.S. Lo Piccolo, E. Cavadini, P.G. Montaldo, M.R. Pizzitola, L. Boni, M. Ponzoni, A. Decensi, B. De Bernardi, F.F. Bellani, and F. Formelli Phase I trial and pharmacokinetics of fenretinide in children with neuroblastoma Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 9 2003 2032 2039
7. N. Hail Jr.; H.J. Kim, and R. Lotan Mechanisms of fenretinide-induced apoptosis Apoptosis: Int. J. Program. Cell Death 11 2006 1677 1694
8. H.P. Harding, H. Zeng, Y. Zhang, R. Jungries, P. Chung, H. Plesken, D.D. Sabatini, and D. Ron Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival Mol. cell 7 2001 1153 1163
9. A.G. Hinnebusch Mechanism and Regulation of Initiator Methionyl-tRNA Binding to Ribosomes 2000
10. H.Y. Jiang, and R.C. Wek GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation Biochem. J. 385 2005 371 380
11. T.P. Kingston, N.J. Lowe, J. Winston, and J. Heckenlively Visual and cutaneous toxicity which occurs during N-(4-hydroxyphenyl) retinamide therapy for psoriasis Clin. Exp. Dermatol. 11 1986 624 627
12. W.L. Lai, and N.S. Wong The PERK/eIF2 alpha signaling pathway of Unfolded Protein Response is essential for N-(4-hydroxyphenyl)retinamide (4HPR)-induced cytotoxicity in cancer cells Exp. cell Res. 314 2008 1667 1682
13. A. Marachelian, M. Kang, K. Hwang, J. Villablanca, S. Groshen, K. Matthay, J. Maris, K. DeSantes, C. Reynolds, and B. Maurer Phase I study of fenretinide (4-HPR) oral powder in patients with recurrent or resistant neuroblastoma: new approaches to Neuroblastoma Therapy (NANT) consortium trial J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 27 2009 10009
14. N.L. Mata, J.B. Lichter, R. Vogel, Y. Han, T.V. Bui, and L.J. Singerman Investigation of oral fenretinide for treatment of geographic atrophy in age-related macular degeneration Retina 33 2013 498 507
15. G.D. McIlroy, M. Delibegovic, C. Owen, P.N. Stoney, K.D. Shearer, P.J. McCaffery, and N. Mody Fenretinide treatment prevents diet-induced obesity in association with major alterations in retinoid homeostatic gene expression in adipose, liver, and hypothalamus Diabetes 62 2013 825 836
16. N. Mody, and G.D. McIlroy The mechanisms of Fenretinide-mediated anti-cancer activity and prevention of obesity and type-2 diabetes Biochem. Pharmacol. 91 2014 277 286
17. N.J. Moreland, M.Y. Tay, E. Lim, A.P. Rathore, A.P. Lim, B.J. Hanson, and S.G. Vasudevan Monoclonal antibodies against dengue NS2B and NS3 proteins for the study of protein interactions in the flaviviral replication complex J. Virol. Methods 179 2012 97 103
18. I. Novoa, Y. Zhang, H. Zeng, R. Jungreis, H.P. Harding, and D. Ron Stress-induced gene expression requires programmed recovery from translational repression EMBO J. 22 2003 1180 1187
19. J. Pena, and E. Harris Dengue virus modulates the unfolded protein response in a time-dependent manner J. Biol. Chem. 286 2011 14226 14236
20. M.J. Pryor, S.M. Rawlinson, R.E. Butcher, C.L. Barton, T.A. Waterhouse, S.G. Vasudevan, P.G. Bardin, P.J. Wright, D.A. Jans, and A.D. Davidson Nuclear localization of dengue virus nonstructural protein 5 through its importin alpha/beta-recognized nuclear localization sequences is integral to viral infection Traffic 8 2007 795 807
21. M. Rahmaniyan, R.W. Curley Jr.; L.M. Obeid, Y.A. Hannun, and J.M. Kraveka Identification of dihydroceramide desaturase as a direct in vitro target for fenretinide J. Biol. Chem. 286 2011 24754 24764
22. R. Rajamanonmani, C. Nkenfou, P. Clancy, Y.H. Yau, S.G. Shochat, S. Sukupolvi-Petty, W. Schul, M.S. Diamond, S.G. Vasudevan, and J. Lescar On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes J. Gen. Virol. 90 2009 799 809
23. A.P. Rathore, M.L. Ng, and S.G. Vasudevan Differential unfolded protein response during Chikungunya and Sindbis virus infection: CHIKV nsP4 suppresses eIF2alpha phosphorylation Virology J. 10 2013 36
24. S.M. Rawlinson, M.J. Pryor, P.J. Wright, and D.A. Jans CRM1-mediated nuclear export of dengue virus RNA polymerase NS5 modulates interleukin-8 induction and virus production J. Biol. Chem. 284 2009 15589 15597
25. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response. Nature reviews Mol. Cell Biol. 8 2007 519 529
26. A.L. Sabichi, S.P. Lerner, E.N. Atkinson, H.B. Grossman, N.P. Caraway, C.P. Dinney, D.F. Penson, S. Matin, A. Kamat, L.L. Pisters, D.W. Lin, R.L. Katz, D.E. Brenner, G.P. Hemstreet 3rd, M. Wargo, A. Bleyer, W.H. Sanders, J.L. Clifford, H.L. Parnes, and S.M. Lippman Phase III prevention trial of fenretinide in patients with resected non-muscle-invasive bladder cancer Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 14 2008 224 229
27. M.Y. Tay, J.E. Fraser, W.K. Chan, N.J. Moreland, A.P. Rathore, C. Wang, S.G. Vasudevan, and D.A. Jans Nuclear localization of dengue virus (DENV) 1-4 non-structural protein 5; protection against all 4 DENV serotypes by the inhibitor Ivermectin Antivir. Res. 99 2013 301 306
28. P. Tsaytler, H.P. Harding, D. Ron, and A. Bertolotti Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis Science 332 2011 91 94
29. I. Umareddy, O. Pluquet, Q.Y. Wang, S.G. Vasudevan, E. Chevet, and F. Gu Dengue virus serotype infection specifies the activation of the unfolded protein response Virology J. 4 2007 91
30. K.M. Vattem, and R.C. Wek Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells Proceedings of the National Academy of Sciences of the United States of America vol. 101 2004 11269 11274
31. U. Veronesi, G. De Palo, E. Marubini, A. Costa, F. Formelli, L. Mariani, A. Decensi, T. Camerini, M.R. Del Turco, M.G. Di Mauro, M.G. Muraca, M. Del Vecchio, C. Pinto, G. D'Aiuto, C. Boni, T. Campa, A. Magni, R. Miceli, M. Perloff, W.F. Malone, and M.B. Sporn Randomized trial of fenretinide to prevent second breast malignancy in women with early breast cancer J. Natl. Cancer Inst. 91 1999 1847 1856
32. U. Veronesi, L. Mariani, A. Decensi, F. Formelli, T. Camerini, R. Miceli, M.G. Di Mauro, A. Costa, E. Marubini, M.B. Sporn, and G. De Palo Fifteen-year results of a randomized phase III trial of fenretinide to prevent second breast cancer Ann. Oncol. Off. J. Eur. Soc. Med. Oncol./ESMO 17 2006 1065 1071
33. J.G. Villablanca, W.B. London, A. Naranjo, P. McGrady, M.M. Ames, J.M. Reid, R.M. McGovern, S.A. Buhrow, H. Jackson, E. Stranzinger, B.J. Kitchen, P.M. Sondel, M.T. Parisi, B. Shulkin, G.A. Yanik, S.L. Cohn, and C.P. Reynolds Phase II study of oral capsular 4-hydroxyphenylretinamide (4-HPR/fenretinide) in pediatric patients with refractory or recurrent neuroblastoma: a report from the Children's Oncology Group Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 17 2011 6858 6866
34. K.M. Wagstaff, H. Sivakumaran, S.M. Heaton, D. Harrich, and D.A. Jans Ivermectin is a specific inhibitor of importin alpha/beta-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus Biochem. J. 443 2012 851 856