Molecular mechanism of SCARB2-mediated attachment and uncoating of EV71

详细信息    查看全文

• 作者：Minghao Dang (1)
  Xiangxi Wang (1)
  Quan Wang (3)
  Yaxin Wang (1)
  Jianping Lin (3)
  Yuna Sun (1)
  Xuemei Li (1)
  Liguo Zhang (1)
  Zhiyong Lou (2)
  Junzhi Wang (4)
  Zihe Rao (1) (2) (3)
  
• 关键词：viral entry ; uncoating ; picornaviruses ; receptor binding ; SCARB2 ; EV71 ; lipid transfer tunnel
• 刊名：Protein & Cell
• 出版年：2014
• 出版时间：September 2014
• 年：2014
• 卷：5
• 期：9
• 页码：692-703
• 全文大小：3,716 KB
• 参考文献：1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213鈥?21 CrossRef
  2. Arita M, Koike S, Aoki J, Horie H, Nomoto A (1998) Interaction of poliovirus with its purified receptor and conformational alteration in the virion. J Virol 72:3578鈥?586
  3. Bergelson JM, Coyne CB (2013) Picornavirus entry. In: Viral entry into host cells. Springer, New York, pp 24鈥?1
  4. Chen P, Song Z, Qi Y, Feng X, Xu N, Sun Y, Wu X, Yao X, Mao Q, Li X (2012) 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 287:6406鈥?420 CrossRef
  5. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh J-T, Bergelson JM (2001) The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA 98:15191鈥?5196 CrossRef
  6. Crowell RL, Philipson L (1971) Specific alterations of coxsackievirus B3 eluted from HeLa cells. J Virol 8:509鈥?15
  7. De Colibus L, Wang X, Spyrou JA, Kelly J, Ren J, Grimes J, Puerstinger G, Stonehouse N, Walter TS, Hu Z (2014) More-powerful virus inhibitors from structure-based analysis of HEV71 capsid-binding molecules. Nat Struct Mol Biol 21(3):282鈥?88 CrossRef
  8. De Sena J, Mandel B (1977) Studies on the in vitro uncoating of poliovirus II. Characteristics of the membrane-modified particle. Virology 78:554鈥?66 CrossRef
  9. DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, Palo Alto
  10. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126鈥?132 CrossRef
  11. Fricks CE, Hogle JM (1990) Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol 64:1934鈥?945
  12. Fry EE, Lea SM, Jackson T, Newman JW, Ellard FM, Blakemore WE, Abu-Ghazaleh R, Samuel A, King AM, Stuart DI (1999) The structure and function of a foot-and-mouth disease virus鈥搊ligosaccharide receptor complex. EMBO J 18:543鈥?54 CrossRef
  13. Grant RA, Hiremath CN, Filman DJ, Syed R, Andries K, Hogle JM (1994) Structures of poliovirus complexes with anti-viral drugs: implications for viral stability and drug design. Curr Biol 4:784鈥?97 CrossRef
  14. Ho BK, Gruswitz F (2008) HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct Biol 8:49 CrossRef
  15. Hogle JM (2002) Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu Rev Microbiol 56:677鈥?02 CrossRef
  16. Huang C-C, Liu C-C, Chang Y-C, Chen C-Y, Wang S-T, Yeh T-F (1999) Neurologic complications in children with enterovirus 71 infection. N Engl J Med 341:936鈥?42 CrossRef
  17. Iwata H, Hirasawa T, Roy P (1991) Complete nucleotide sequence of segment 5 of epizootic haemorrhagic disease virus; the outer capsid protein VP5 is homologous to the VP5 protein of bluetongue virus. Virus Res 20:273鈥?81 CrossRef
  18. Kim J-JP, Olson LJ, Dahms NM (2009) Carbohydrate recognition by the mannose-6-phosphate receptors. Curr Opin Struct Biol 19:534鈥?42 CrossRef
  19. Leong KLJ, Ng MM-L, Chu JJH (2011) The essential role of clathrin-mediated endocytosis in the infectious entry of human enterovirus 71. J Biol Chem 286:309鈥?21 CrossRef
  20. Lin Y-W, Lin H-Y, Tsou Y-L, Chitra E, Hsiao K-N, Shao H-Y, Liu C-C, Sia C, Chong P, Chow Y-H (2012) Human SCARB2-mediated entry and endocytosis of EV71. PLoS ONE 7:e30507 CrossRef
  21. Lonberg-Holm K, Gosser LB, Kauer J (1975) Early alteration of poliovirus in infected cells and its specific inhibition. J Gen Virol 27:329鈥?42 CrossRef
  22. Lum L, Wong K, Lam S, Chua K, Goh A (1998) Neurogenic pulmonary oedema and enterovirus 71 encephalomyelitis. Lancet 352:1391 CrossRef
  23. Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124:729鈥?40 CrossRef
  24. Mavridis L, Hudson BD, Ritchie DW (2007) Toward high throughput 3D virtual screening using spherical harmonic surface representations. J Chem Inf Model 47:1787鈥?796 CrossRef
  25. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40:658鈥?74 CrossRef
  26. Neculai D, Schwake M, Ravichandran M, Zunke F, Collins RF, Peters J, Neculai M, Plumb J, Loppnau P, Pizarro JC (2013) Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 504:172鈥?76 CrossRef
  27. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shimizu H (2009) Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15:794鈥?97 CrossRef
  28. Nishimura Y, Lee H, Hafenstein S, Kataoka C, Wakita T, Bergelson JM, Shimizu H (2013) Enterovirus 71 binding to PSGL-1 on leukocytes: VP1-145 acts as a molecular switch to control receptor interaction. PLoS Pathog 9:e1003511 CrossRef
  29. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data. Methods Enzymol 276:307鈥?26 CrossRef
  30. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG (2012) Crystal structure of human enterovirus 71. Science 336:1274 CrossRef
  31. Reczek D, Schwake M, Schr枚der J, Hughes H, Blanz J, Jin X, Brondyk W, Van Patten S, Edmunds T, Saftig P (2007) LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of 尾-glucocerebrosidase. Cell 131:770鈥?83 CrossRef
  32. Ren J, Wang X, Hu Z, Gao Q, Sun Y, Li X, Porta C, Walter TS, Gilbert RJ, Zhao Y (2013) Picornavirus uncoating intermediate captured in atomic detail. Nat Commun 4:1929
  33. Rossmann MG, He Y, Kuhn RJ (2002) Picornavirus鈥搑eceptor interactions. Trends Microbiol 10:324鈥?31 CrossRef
  34. Smith AE, Helenius A (2004) How viruses enter animal cells. Science 304:237鈥?42 CrossRef
  35. Smith TJ, Kremer MJ, Luo M, Vriend G, Arnold E, Kamer G, Rossmann MG, McKinlay MA, Diana GD, Otto MJ (1986) The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 233:1286鈥?293 CrossRef
  36. Sun Y, Wang X, Yuan S, Dang M, Li X, Zhang XC, Rao Z (2013) An open conformation determined by a structural switch for 2A protease from coxsackievirus A16. Protein Cell 4:782鈥?92 CrossRef
  37. Tan CW, Poh CL, Sam I-C, Chan YF (2013) Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol 87:611鈥?20 CrossRef
  38. Tuthill TJ, Groppelli E, Hogle JM, Rowlands DJ (2010) Picornaviruses. In: Cell entry by non-enveloped viruses. Springer, New York, pp 43鈥?9
  39. Velayati A, DePaolo J, Gupta N, Choi JH, Moaven N, Westbroek W, Goker-Alpan O, Goldin E, Stubblefield BK, Kolodny E, Tayebi N, Sidransky E (2011) A mutation in SCARB2 is a modifier in Gaucher disease. Hum Mutat 32:1232鈥?238 CrossRef
  40. Vlasak M, Goesler I, Blaas D (2005) Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J Virol 79:5963鈥?970 CrossRef
  41. Wang X, Peng W, Ren J, Hu Z, Xu J, Lou Z, Li X, Yin W, Shen X, Porta C (2012) A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat Struct Mol Biol 19:424鈥?29 CrossRef
  42. Wang Y, Qing J, Sun Y, Rao Z (2013) Suramin inhibits EV71 infection. Antiviral Res 103:1鈥? CrossRef
  43. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, Takemura T, Koike S (2009) Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15:798鈥?01 CrossRef
  44. Yamayoshi S, Iizuka S, Yamashita T, Minagawa H, Mizuta K, Okamoto M, Nishimura H, Sanjoh K, Katsushima N, Itagaki T (2012) Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J Virol 86:5686鈥?696 CrossRef
  45. Yamayoshi S, Ohka S, Fujii K, Koike S (2013) Functional comparison of SCARB2 and PSGL1 as receptors for enterovirus 71. J Virol 87:3335鈥?347 CrossRef
  46. Yang B, Chuang H, Yang KD (2009) Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol J 6:141 CrossRef
  47. Zachos C, Blanz J, Saftig P, Schwake M (2012) A critical histidine residue within LIMP-2 mediates pH sensitive binding to its ligand 尾-glucocerebrosidase. Traffic 13:1113鈥?123 CrossRef
  48. Zhang P, Mueller S, Morais MC, Bator CM, Bowman VD, Hafenstein S, Wimmer E, Rossmann MG (2008) Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proc Natl Acad Sci USA 105:18284鈥?8289 CrossRef
  
• 作者单位：Minghao Dang (1)
  Xiangxi Wang (1)
  Quan Wang (3)
  Yaxin Wang (1)
  Jianping Lin (3)
  Yuna Sun (1)
  Xuemei Li (1)
  Liguo Zhang (1)
  Zhiyong Lou (2)
  Junzhi Wang (4)
  Zihe Rao (1) (2) (3)
  
  1. National Laboratory of Macromolecules, Institute of Biophysics, Chinese Academy of Science, Beijing, 100101, China
  3. School of Life Sciences, School of Pharmacy, Nankai University, Tianjin, 300071, China
  2. Laboratory of Structural Biology, School of Medicine, Tsinghua University, Beijing, 100084, China
  4. National Institutes for Food and Drug Control, Beijing, 100050, China
  
• ISSN：1674-8018

文摘

Unlike the well-established picture for the entry of enveloped viruses, the mechanism of cellular entry of non-enveloped eukaryotic viruses remains largely mysterious. Picornaviruses are representative models for such viruses, and initiate this entry process by their functional receptors. Here we present the structural and functional studies of SCARB2, a functional receptor of the important human enterovirus 71 (EV71). SCARB2 is responsible for attachment as well as uncoating of EV71. Differences in the structures of SCARB2 under neutral and acidic conditions reveal that SCARB2 undergoes a pivotal pH-dependent conformational change which opens a lipid-transfer tunnel to mediate the expulsion of a hydrophobic pocket factor from the virion, a pre-requisite for uncoating. We have also identified the key residues essential for attachment to SCARB2, identifying the canyon region of EV71 as mediating the receptor interaction. Together these results provide a clear understanding of cellular attachment and initiation of uncoating for enteroviruses.