The Suramin Derivative NF449 Interacts with the 5-fold Vertex of the Enterovirus A71 Capsid to Prevent Virus Attachment to PSGL-1 and Heparan Sulfate

PLoS Pathogens

Volumn 11, Issue 10, 2015, Pages

  Nishimura, Yorihiro ^a,b   McLaughlin, Noel P ^c   Pan, Jieyan ^a   Goldstein, Sara ^c   Hafenstein, Susan ^d   Shimizu, Hiroyuki ^b   Winkler, Jeffrey D ^c   Bergelson, Jeffrey M ^a,e  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4',4'',4''' [CARBONYLBISIMINO 1,3,5 BENZENETRIYLBIS(CARBONYLIMINO)]TETRAKISBENZENE 1,3 DISUFONIC ACID; GREEN FLUORESCENT PROTEIN; HEPARAN SULFATE; INTERLEUKIN ENHANCER BINDING FACTOR 3; P SELECTIN GLYCOPROTEIN LIGAND 1; SURAMIN; UNCLASSIFIED DRUG; 4,4,',4'',4'''-(CARBONYLBIS(IMINO-5,1,3-BENZENETRIYLBIS(CARBONYLIMINO)))TETRAKIS(BENZENE-1,3-DISULFONATE); ANTIVIRUS AGENT; BENZENESULFONIC ACID DERIVATIVE; MEMBRANE PROTEIN; P-SELECTIN LIGAND PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENTEROVIRUS 71; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR DOCKING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RECEPTOR BINDING ASSAY; SEQUENCE ANALYSIS; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS REPLICATION; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMISTRY; DRUG EFFECTS; ENTEROVIRUS A; ENTEROVIRUS INFECTION; HELA CELL LINE; JURKAT CELL LINE; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; VIROLOGY;

ANTIVIRAL AGENTS; BENZENESULFONATES; BINDING SITES; CAPSID; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; HELA CELLS; HEPARITIN SULFATE; HUMANS; JURKAT CELLS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SURAMIN; VIRUS ATTACHMENT;

EID: 84946074002     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005184     Document Type: Article

References (38)

1. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH, Virology, epidemiology, pathogenesis, and control of enterovirus 71. The Lancet Infectious Diseases. 2010;10(11):778–90. 20961813. doi: 10.1016/S1473-3099(10)70194-8
2. Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, et al. Hand, foot, and mouth disease in China, 2008–12: an epidemiological study. The Lancet Infectious Diseases. 2014;14(4):308–18. 24485991. doi: 10.1016/S1473-3099(13)70342-6
3. Zhu FC, Meng FY, Li JX, Li XL, Mao QY, Tao H, et al. Efficacy, safety, and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2013;381(9882):2024–32. 23726161. doi: 10.1016/S0140-6736(13)61049-1
4. Li R, Liu L, Mo Z, Wang X, Xia J, Liang Z, et al. An inactivated enterovirus 71 vaccine in healthy children. The New England Journal of Medicine. 2014;370(9):829–37. 24571755. doi: 10.1056/NEJMoa1303224
5. Zhu F, Xu W, Xia J, Liang Z, Liu Y, Zhang X, et al. Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. The New England Journal of Medicine. 2014;370(9):818–28. 24571754. doi: 10.1056/NEJMoa1304923
6. McMinn PC, Enterovirus vaccines for an emerging cause of brain-stem encephalitis. The New England Journal of Medicine. 2014;370(9):792–4. 24571750. doi: 10.1056/NEJMp1400601
7. Wang JN, Yao CT, Yeh CN, Huang CC, Wang SM, Liu CC, et al. Critical management in patients with severe enterovirus 71 infection. Pediatrics international: official journal of the Japan Pediatric Society. 2006;48(3):250–6. 16732789.
8. Fu YC, Chi CS, Jan SL, Wang TM, Chen PY, Chang Y, et al. Pulmonary edema of enterovirus 71 encephalomyelitis is associated with left ventricular failure: implications for treatment. Pediatr Pulmonol. 2003;35(4):263–8. 12629622.
9. Jan SL, Lin SJ, Fu YC, Chi CS, Wang CC, Wei HJ, et al. Extracorporeal life support for treatment of children with enterovirus 71 infection-related cardiopulmonary failure. Intensive Care Med. 2010;36(3):520–7. 20033668. doi: 10.1007/s00134-009-1739-2
10. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minawa T, Takemura T, et al. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nature Medicine. 2009;15:798–801. doi: 10.1038/nm.1992 19543282
11. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shizumi H, Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nature Medicine. 2009;15:794–7. doi: 10.1038/nm.1961 19543284
12. Tan CW, Poh CL, Sam IC, Chan YF, Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol. 2013;87(1):611–20. 23097443. doi: 10.1128/JVI.02226-12
13. Yang SL, Chou YT, Wu CN, Ho MS, Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J Virol. 2011;85(22):11809–20. 21900167. doi: 10.1128/JVI.00297-11
14. Du N, Cong H, Tian H, Zhang H, Zhang W, Song L, et al. Cell surface vimentin is an attachment receptor for enterovirus 71. J Virol. 2014. 24623428. doi: 10.1128/JVI.02636-14
15. Su PY, Wang YF, Huang SW, Lo YC, Wang YH, Wu SR, et al. Cell surface nucleolin facilitates enterovirus 71 binding and infection. J Virol. 2015. 25673703.
16. Nishimura Y, Wakita T, Shimizu H, Tyrosine sulfation of the amino terminus of PSGL-1 is critical for enterovirus 71 infection. PLoS Pathog. 2010;6(11):e1001174. 21079683. doi: 10.1371/journal.ppat.1001174
17. Nishimura Y, Lee H, Hafenstein S, Kataoka C, Wakita T, Bergelson JM, et al. Enterovirus 71 binding to PSGL-1 on leukocytes: VP1-145 acts as a molecular switch to control receptor interaction. PLoS Pathog. 2013;9(7):e1003511. 23935488. doi: 10.1371/journal.ppat.1003511
18. Arita M, Wakita T, Shimizu H, Characterization of pharmacologically active compounds that inhibit poliovirus and enterovirus 71 infectivity. The Journal of General Virology. 2008;89(Pt 10):2518–30. 18796721.
19. Bergelson JM, Coyne CB, Picornavirus entry. Advances in Experimental Medicine and Biology. 2013;790:24–41. 23884584. doi: 10.1007/978-1-4614-7651-1_2
20. Hohenegger M, Waldhoer M, Beindl W, Boing B, Kreimeyer A, Nickel P, et al. Gsalpha-selective G protein antagonists. Proc Natl Acad Sci U S A. 1998;95(1):346–51. 9419378.
21. Dewey HM, Wormall A, Studies on suramin (Antrypol: Bayer 205): 5. The combination of the drug with the plasma and other proteins. The Biochemical Journal. 1946;40(1):119–24. 16747958.
22. Chen P, Song Z, Qi Y, Feng X, Xu N, Sun Y, et al. Molecular determinants of enterovirus 71 viral entry: cleft around GLN-172 on VP1 protein interacts with variable region on scavenge receptor B 2. J Biol Chem. 2012;287(9):6406–20. 22219187. doi: 10.1074/jbc.M111.301622
23. Lee H, Cifuente JO, Ashley RE, Conway JF, Makhov AM, Tano Y, et al. A strain-specific epitope of enterovirus 71 identified by cryo-electron microscopy of the complex with fab from neutralizing antibody. J Virol. 2013;87(21):11363–70. 23946455. doi: 10.1128/JVI.01926-13
24. Liu CC, Chou AH, Lien SP, Lin HY, Liu SJ, Chang JY, et al. Identification and characterization of a cross-neutralization epitope of enterovirus 71. Vaccine. 2011;29(26):4362–72. 21501643. doi: 10.1016/j.vaccine.2011.04.010
25. Andries K, Dewindt B, Snoeks J, Willebrords R, van Eemeren K, Stokbroekx R, et al. In vitro activity of pirodavir (R 77975), a substituted phenoxy-pyridazinamine with broad-spectrum antipicornaviral activity. Antimicrobial Agents and Chemotherapy. 1992;36(1):100–7. 1317142.
26. Ji XY, Wang HQ, Hao LH, He WY, Gao RM, Li YP, et al. Synthesis and antiviral activity of N-phenylbenzamide derivatives, a novel class of enterovirus 71 inhibitors. Molecules. 2013;18(3):3630–40. 23519203. doi: 10.3390/molecules18033630 23519203
27. Wang Y, Qing J, Sun Y, Rao Z, Suramin inhibits EV71 infection. Antiviral Res. 2013;103C:1–6. 24374150.
28. Ren P, Zou G, Bailly B, Xu S, Zeng M, Chen X, et al. The approved pediatric drug suramin identified as a clinical candidate for the treatment of EV71 infection—suramin inhibits EV71 infection in vitro and in vivo. Emerging Microbes & Infections 2014;3:e62.
29. Pearson RD, Weller PF, Guerant RL, Guerant RL, Walker DH, Weller PF, Chemotherapy of Parasitic Diseases. In: Tropical Infectious Diseases. 3 ed: Elsevier; 2011.
30. La Rocca RV, Meer J, Gilliatt RW, Stein CA, Cassidy J, Myers CE, et al. Suramin-induced polyneuropathy. Neurology. 1990;40(6):954–60. 2161094.
31. Nagata N, Shimizu H, Ami Y, Tano Y, Harashima A, Suzaki Y, et al. Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol. 2002;67(2):207–16. 11992581.
32. Pan J, Narayanan B, Shah S, Yoder JD, Cifuente JO, Hafenstein S, et al. Single amino acid changes in the virus capsid permit coxsackievirus B3 to bind decay-accelerating factor. J Virol. 2011;85(14):7436–43. 21561916. doi: 10.1128/JVI.00503-11
33. Chow M, Newman J, Filman D, Hogle J, Rowlands D, Brown F, Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature. 1987;327:482–6. 3035380
34. Bergelson JM, Chan M, Solomon K, St. John NF, Lin H, Finberg RW, Decay-accelerating factor, a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci USA. 1994;91:6245–8. 7517044
35. Kassack MU, Braun K, Ganso M, Ullmann H, Nickel P, Boing B, et al. Structure-activity relationships of analogues of NF449 confirm NF449 as the most potent and selective known P2X1 receptor antagonist. European Journal of Medicinal Chemistry. 2004;39(4):345–57. 15072843.
36. Bergelson JM, St. John N, Kawaguchi S, Chan M, Stubdal H, Modlin J, et al. Infection by echoviruses 1 and 8 depends on the α2 subunit of human VLA-2. J Virol. 1993;67:6847–52. 8411387
37. Molecular Operating Environment (MOE). 2014.09. Chemical Computing Group Inc., 1010 Sherbooke St. West, Suite 910, Montreal, QC, Canada, H3A 2R. 2014.
38. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG, Crystal structure of human enterovirus 71. Science. 2012;336(6086):1274. 22383808. doi: 10.1126/science.1218713